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Int J ColorectDis (1988) 3:67-89

Coloi eclal
Disease
9 Springer-Verlag1988

Symposium
Proctography
Participants: D.C.C. Bartolo, Bristol; C. I. Bartram, London; O. Ekberg, Lund; F.-T. Fork, Malmo;
I. Kodner, St. Louis; J. H. C. Kuijpers, Nijmegen; P. H. G. Mahieu, Brussels; P.J. Shorvon, London;
G.W. Stevenson, Hamilton; N. Womack, London
Moderator: I. G. Finlay, Glasgow

Introduction
Moderator Mr. Finlay: Over the past decade
there has been increasing interest in the pathophysiology of the anorectum, particularly in disorders of function such as incontinence, prolapse,
obstructed defaecation and solitary rectal ulcer
syndrome. Manometry and electromyography of
the anal canal and pelvic floor have been used
predominantly by enthusiasts for research purposes. Subsequently techniques to visualise the
anorectum have been introduced and the term
proctography has been used to describe the
dynamic radiography study of this area. The technique has evolved in different ways in each centre
and the purpose of this symposium is to bring
together that experience so that we might determine whether patterns of technique, patient selection and clinical application are emerging. A
series of questions relating to these aspects has
been put to a group of experts all active in the
field to determine the present state of knowledge
and reproducibility of the technique.
Technique: What is your technique? Please define
and comment on any variations such video,
integrated or spot film proctography.
Mr. Bartolo: We have employed three differing
techniques according to the type of information
required.
a) Evacuation proctography. No bowel preparation is used since it is deemed more physiological
to observe anorectal morphology without prior
preparation. Fifty millilitres of dilute barium
sulphate is introduced into the rectum to coat the
rectal wall. A semi-solid paste is made up with

barium and dehydrated potato. This is injected


into the rectum. The subject is then seated on a
specially designed perspex water-filled commode.
This is important to obtain good quality radiographs as conventional commodes result in suboptimal radiographs when using an automatic
exposure system (lontomat). X-ray films are taken
by ampliphotography using a 100mm camera
(Sircam 106, Siemens) 0.6 m m focus and a voltage
of 125 KV from a 1000 mA generator to give a
short exposure at a rate of 1 frame/sec. Each
frame is numbered automatically enabling the
sequence to be analysed in detail. We use video
for dynamic investigations where proctography is
combined with manometry, to measure anal and
rectal pressures, and electromyography of the
external anal sphincter and puborectalic muscles.
b) Standard proctography. Prior to the evacuation proctogram, the anorectal angle and its
relationship to the pubococcygeal line are measured from static radiographs taken at rest, during
a maximal sphincter contraction and whilst the
subject strains.
c) Video proctography. In selected patients simultaneous anorectal manometry and electromyography are performed. The measurements which
are fed into a computer are superimposed on the
television monitor such that at any one time
during defaecography we have a dynamic assessment of anal and rectal pressures together with
external sphincter and puborectalis electromyographic measurements.
Dr. Bartram: Perhaps one should start by agreeing on terminology. We use the term "evacuation
proctography" to describe this examination [1],
which is really imaging voluntary rectal expul-

68
Sion, and not true defaecation. Video is used as it
is convenient and cheap, does not involve higher
radiation as does cine, and allows video mixing of
other electrical inputs for integrated examinations. Spot films are taken simply to provide a
better record of some interesting feature, as slide
reproduction from video is poor.
Dr. Fork and Dr. Ekberg: Patients are pretreated
with Pico-Salax | In order to delineate small
bowel loops in the pelvis, 150ml of barium
contrast m e d i u m is given orally, one hour before
defaecography. Filling of the loops down to the
terminal ileum is checked fluoroscopically.
Ordinary physiological conditions during
defaecography are simulated by injecting 300 ml
of a thick barium paste (Mixobar oesophagus |
Astra) into the rectum with a caulking gun. This is
done with the patient in the left lateral position.
By placing a tampon soaked in iodine contrast
m e d i u m in the vagina the precise location of the
posterior fornix is readily identified radiographically in female patients.
The patient is then seated on a radiolucent
toilet placed in a remote control stand. Wedges
are used. Single films are obtained together with
videotape recordings. The images are centred over
the rectum and pelvis during resting, straining
and squeezing using lateral views. Thereafter a
further volume of thick barium paste is injected
and completing video and single films are obtained with the patient in the posteroanterior
projection.
Dr. Kodner: Our technique involves mixing
methyl cellulose with barium sulphate to thicken
it to a consistency approximating stool. Approximately 200 cc of thickened barium is instilled into
the rectum under fluoroscopic control to fill the
rectosigmoid. The patient is then seated on a
water-filled ring placed on a bed pan situated on
top of a wooden box and defaecation is then
observed by fluoroscopy from a lateral position.
The examination is recorded on videotape and
selected spot films are obtained by the radiologist.
The position of the rectosigmoid in relation to the
sacral promontory must be documented. The
rectum is observed for movement during defaecation. It is important to examine the rectum from
the sacral promontory to the level of the coccyx.
It is difficult to see the air-tissue interface at the
anus because of the extremes of contrast, and in
some cases actual prolapse of the rectum has been
missed. One should also look for motion of the

perineum. It has been our practice to place a


small metal clip held or taped to the perianal
skin, although a thick contrast paste would probably be better. We have found it useful in certain
circumstances to place contrast in the urinary
bladder and the vagina to evaluate adjacent structures in relation to the motion of the rectum.
The total fluoroscopy time required for this
examination is 1 min, 40 s. The dosage of irradiation received by a patient during this study
as calculated by the physicists at the Mallincrokdt
Institute of Radiology is 270 millirads. This compares with 750 millirads for a routine barium
enema examination.
Dr. Kuijpers: The investigation is done with the
patient in the right lateral position. The rectum is
filled with barium paste to the promontory. We
used to mark the anal canal with barium paste to
be able to measure the anorectal angle and to
determine the position of the anal canal during
straining [2], but these factors have become less
important and this is not done any more.
The investigations are recorded on video.
Recordings are made at rest and during squeezing
and straining.
Straining is done both with the rectum filled,
to study the excretory ability, and after emptying,
to detect the presence of rectal intussusception.
When the patient's history suggests intussusception and this is not demonstrated during "right
lateral" defaecography, the study is repeated in
the squatting position. However this procedure
has not led to the detection of more intussusceptions.
Dr. Mahieu: Since 1978 we have proposed a
method which is simple, quick, physiologically
reliable [3] and widely followed by radiologists
interested in coloproctology.
No bowel preparation is required and a water
enema is contraindicated. The contrast m e d i u m
used must be semi-solid like faeces. No adequate
paste is available on the market but a paste that is
reasonably satisfactory is prepared by diluting
150ml of a 100% weight per volume barium
suspension with 400 ml of water. This is heated
and gradually mixed with 100 g of potato starch,
beaten with a whisk, until a smooth paste is
obtained [4, 5]. A pistol injector [6] is needed to
inject this thick paste into the rectum. As the
injector is being withdrawn injection is continued
to outline the anal canal [3]. For improved
coating of the rectal mucosa, 50 ml of a con-

69
centrated suspension of barium can be injected
before the paste [5]. In females a barium-soaked
gauze can be placed in the vagina.
We have designed a special commode [3, 5, 7]
acting as a filter. This commode consists of several
rubber air rings filled with water, secured on top
of each other and lined by a disposable plastic
bag.
Profile views are taken by videotape or
preferably by ampliphotography using a 100 m m
camera, 0.6 m m focus, and a voltage of 117 kV at
a rate of 1 or 2 frames per second. Standard films
(24
cm) are taken at rest, during squeezing
and straining.
Professor Stevenson and Dr. Shorvon: A wooden
commode has been constructed furnished with a
solid pine seat (plywood produces artefactual
lines), and mounted on wheels. Metal hooks are
attached to the sides of the upright fluoroscopy
table so that the c o m m o d e can be moved with
remote table movement for easier centring. A
plastic rod with radio-opaque centimetre markings is mounted in the mid line below the seat for
accurate measurements in this plane. Two copper
plates (4 m m thick), one being shaped to the
curve of the buttocks and the other square,
provide radiological infiltration, to avoid 'flare'.
No bowel preparation is given, and a contrastsoaked tampon is inserted into the vagina in
female patients. Barium paste as described by
Mahieu et al. [5] is introduced with an orthopaedic cement gun and disposable plastic syringe.
A mixture of barium and petroleum gel is
smeared on the skin at and posterior to the external anal orifice to mark the skin. The examination is recorded on video, and four or five
105 m m films are taken with the patient at rest,
during squeezing or lifting and straining during
and at the end of defaecation.
Certain modifications of the technique are frequently used. In patients who have difficulty in
evacuation liquid barium is often used alone and
a second examination with paste is performed
only if the liquid has been successfully expelled.
In patients with suspected enterocele or sigmoidocele the small bowel and sigmoid colon are
first opacified with barium. Anteroposterior and
oblique views are taken in patients with unusual
radiographic findings, and the c o m m o d e is on
wheels to facilitate this.

Mr. Womack: In our unit we have developed


contrast proctography integrated simultaneously

with anal canal and rectal pressure measurements


and E M G recordings of the pelvic floor skeletal
musculature [8]. A semi-solid contrast m e d i u m
simulates soft stool to be voided and delineates
the anorectum which is visualized by image
intensification radiology. External sphincter E M G
is recorded using fine wire electrodes inserted into
the puborectalis and superficial components of
the external anal sphincter. An intrarectal pressure sensitive radiotelemetry capsule monitors
intrarectal pressure. A micro-computer produces
a visual display of the E M G and pressure data,
and these are mixed with the output of the image
intensifier to produce a composite image which is
stored using a video cassette recorder.
Moderator Mr. Finlay: The responses to this

question included details on the following aspects.


a) Preparation of patient: All contributors with
the exception of Dr. Fork and Dr. Ekberg use no
specific preparation. The Swedish group, however,
gave Picolax and also 150 mls of barium contrast
orally one hour prior to the examination in an
attempt to delineate small bowel loops. Filling of
the terminal ileum was then checked fluoroscopically.
b) Position of patient: Dr. Kuijpers was the only
contributor to use the right lateral position in
preference to the sitting position employed by all
the other groups. He indicated that in his experience using routinely both positions he was
unable to find more pathology in the sitting
position. He did however indicate that if he obtained a negative result in the lateral position, but
the patient had a good history, then he would
place them in the squatting position.
The remaining contributors had all developed
their own "seats" specifically for the examination.
Dr. Kodner uses a water-filled ring placed on a
bedpan which in turn is placed on top of a
wooden box. Dr. Bartram uses a seat which
clamps to a standard X-ray table in the upright
position. The Swedish group use a wooden chair.
Dr. Bartolo uses a specifically designed perspex
water-filled commode, commenting that conventional commodes give rise to "flaring" with poor
pictures. All authors in fact commented on the
difficulty in reducing "flare" on the images.
Dr. Mahieu has designed a special c o m m o d e
consisting of several rubber air rings filled with
water, secured on the top of each other and lined
by disposable plastic bags. Professor Stevenson
and Dr. Shorvon constructed a solid pine seat,

70
having found that plywood produced artefactual
lines. A plastic rod with radio-opaque centimetre
markings is m o u n t e d in the midline below the
seat for accurate midline measurements. Copper
plates shaped to the curvature of the buttocks
were used to avoid flare.
c) Contrast material: Dr. Mahieu advocates that
the m e d i u m must be semi-solid in an attempt to
simulate faeces. He uses 150 mls of 100% weight
per volume barium suspension with 400 mls of
water. This is beaten and gradually mixed with
100 grams of potato starch and beaten with a
whisk until a smooth paste is obtained. A pistol
injector is then required to place this thick paste
into the rectum. While the injector is being
withdrawn, injection is continued to outline the
anal canal. For improved coating of the rectal
mucosa, 50 mls of a concentrated suspension of
barium can be injected before the paste. Professor
Stevenson and Dr. Shorvon use the same technique but employ an orthopaedic cement gun to
introduce paste into the rectum. Dr. Bartolo and
Dr. Womack both use a semi-solid paste by
mixing barium with dehydrated potato. The
Swedish group use 300 mls of thick barium paste
(Mixobar oesophagus astra) placed into the rectum using a caulking gun. Dr. Bartram and Dr.
Kuijpers both use a liquid barium solution, while
Dr. Kodner uses 200 cc of thickened barium.
d) X-ray technique: All contributors used video
to make this a dynamic investigation including
selected spot films. Dr. Mahieu takes profile views
by ampliphotography using a 1 0 0 m m camera
0.6 m m focus and a voltage of 117 kV at a rate of
1 or 2 frames per second. Standard films (24x
30 cm) are taken at rest, during squeezing and
straining. Dr. Bartolo also uses ampliphotography
with a voltage of 125 kV from a 100 m A generator
to give a short exposure at a rate of 1 frame per
second. Each frame is numbered automatically
enabling the sequence to be analysed in detail. He
distinguishes evacuation, standard and video
proctography. Standard proctography provides a
static picture of the anorectal angle and its relationship to the pubococcygeal line taken at rest,
during a maximal sphincter contraction and
whilst the subject strains. Dr. Kodner noted that
his examination required 1 min 40 s of exposure
time with an irradiation dose calculated to be 270
millirads. This compares with 750 millirads for a
routine barium enema.
Although the technique used by the other
contributors was less extensively described, Dr.
Fork and Dr. Ekberg commented that they would

use the antero-posterior view on occasions to gain


further information. Dr. Womack and Dr. Bartolo
both use an integrated system of electromyography, pressure study and proctography in selected
patients. Dr. Mahieu, Professor Stevenson and Dr.
Shorvon, Dr. Kodner and the Swedish group all
use barium-soaked tampons in the vagina. Dr.
Kodner noted that he might also fill the bladder
with contrast.
Comment: It is immediately apparent that there is
considerable variation in technique. The majority
of participants have employed the sitting position
using a semi-solid paste on the basis that this is
more physiological. Although there is some
evidence that anomalies are more pronounced in
the sitting position, it has not been suggested that
this leads to a higher overall diagnostic rate. It is
of interest that Dr. Kuijpers is of the opinion that
sufficient information may be obtained with the
patient in the lateral position. There is no doubt
that the lateral position would be easily acceptable by radiology departments generally. Further
comparative studies to clarify this are required. A
similar argument may also apply to the use of
semi-solid paste as the contrast material. It may
be that sufficient information could be obtained
using liquid contrast only. Again, this would
simplify the procedure for routine use.
There is no doubt that this is an embarrassing
investigation for patients and given that is
involves voluntary evacuation, there is difficulty
in determining when patients are producing a
maximal effort. This difficulty will be discussed
again with reference to puborectalis paradox.
It seems to be agreed that video screening
with selected spot films is the best technique for
routine use. Although proctography integrated
with electromyography and manometry is
probably the optimal investigation, it is likely that
this will remain a research tool for the foreseeable
future owing to its complexity.

How long have you done proctography for


and what is your experience?
Mr. Bartolo: We have used standard proctograms
for measuring the anorectal angle and extent of
perineal descent since 1980 [9]. Since 1983 we
have also used evacuation proctography using a
technique similar to that described by Mahieu [5,
10]. Since 1980 in excess of 1000 patients have
been investigated. The majority were women with
obstructed defaecation, constipation, or anorectal

71

incontinence. The abnormalities in the last 252


proctograms are shown in Table 1.
Dr. Bartram: Over a 3-year period we have
performed about 700 proctograms. All have been
adults with a preponderance of females, reflecting
the clinical interest in constipation at St. Mark's.
The age range is 20-75 years. The largest group
includes those complaining of difficulty in defaecation. Anterior mucosal prolapse, suspected
internal intussusception or rectal prolapse form
the second largest group, with smaller numbers of
the solitary rectal ulcer syndrome, incontinence,
anal pain, and a relatively small n u m b e r of patients postoperatively with rectopexy for the
solitary rectal ulcer syndrome, sphincter division,
various operations for congenital abnormalities
and a few patients with ileo-anal reservoir construction.
Dr. Fork and Dr. Ekberg: All patients were investigated for symptoms including perianal pain,
constipation, obstructed defaecation or incomplete evacuation. The physical examination of the
anorectum of these patients was within normal
limits in all cases.
Proctographies have been performed at our
institution since 1978. A total of 180 women and
45 men has been examined. The average age of
the patients was 56 years, range 18-85 years.
Dr. Kodner: We have performed defaecography in
165 patients over the last 7 years. Ninety per cent
of these have been in females. The distribution of
disease discovered is seen in Table 2.
It should be stressed that the incidence of nonrelaxing puborectalis is very low because it is only
within the last year that we have been specifically
looking for this abnormality.
Dr. Kuijpers: We have performed defaecography
since 1983. It has enabled us to study the function
of the pelvic floor muscle and rectal configuration
both at rest and during squeezing and straining.
About 600 investigations have been carried
out. They were done to investigate patients with
defaecation disorders including constipation and
incomplete evacuation, to study the pathophysiology of existing abnormalities such as the solitary
rectal ulcer syndrome and faecal incontinence,
and to assess the results of surgery, for example,
rectopexy, ileoanal anastomosis, sphincter repair
and postanal repair. The number of proctographies
done has declined in recent months since we have

Table 1. Radiological findings in 252 consecutive proctograms


Normal
Rectocele
Intussusception
recto-rectal
recto-anal
complete rectal
prolapse

41
28
36
23
29

Puborectalis accentuation 49
Anterior rectal wall
24
prolapse
Perineal descent only
13
Solitary ulcer only
5
Megarectum
4

Table 2. Results of defaecography in 165 patients


Internal rectal intussusception
Rectal prolapse
Nonrelaxing puborectalis
Rectocele
Descending perineum
No abnormality

47%
19%
9%
6%
4%
15%

found that functional disorders can more easily be


demonstrated by other types of investigation.
Dr. Mahieu: We have performed defaecography
for 10 years. Since 1978 we have examined 1000
patients. Of the last 300, 219 (73%) were female
and 81 (27%) male. The m e a n age was 46 (range
9-81) years in men and 50 (range 17-85) years in
women.
The most c o m m o n indications for defaecography [10] are difficulties in emptying the rectum
(dyschesia or terminal constipation), frequent
small non-diarrhoeal stools, mucus or blood discharge with no associated polyp or cancer,
tenesmus, perineal or low abdominal pain often
in one of the iliac fossae, feeling of an obstacle
preventing emptying of the rectum (anal blockage) or incomplete evacuation, digital intra-anal
intromission, manual support of the pelvic floor
facilitating defaecation by pressing on the perineum or by inserting a finger into the vagina and
pressing posteriorly to reduce a rectocele, and
faecal incontinence.
Professor Stevenson and Dr. Shorvon: We started
proctography in 1984 and have now examined
over 700 patients. The ages range from 15 to 84
years and the vast majority are female. Initially
most patients referred had disorders of constipation or obstructed defaecation, reflecting the
interest of the physician who encouraged us to
start the service, but more recently incontinence
has become the commonest indication. Rectal
pain, suspected enterocele and rectocele are less

72
Table 3. Resultsofdefaecography(117 patients)
No. of FeMales Age (years)
patients males
mean and
range
Rectal prolapse
Constipation
Faecal incontinence
Solitaryulcer
syndrome

9
59
31
18

6
51
25
12

3
8
6
6

49 (19-68)
45 (19-77)
58 (44-81)
30 (19-64)

frequent reasons for referral, and a study of


patients with irritable bowel syndrome is underway.
Mr. Womack: Our experience of proctography
extends over 4 years, during which approximately
140 investigations have been performed. Criteria
for a normal examination were established from
studies performed on 23 volunteers (18 females
and 5 males; median age 45 years, range 35-68
years) free of anorectal symptoms. Clinical conditions investigated are shown in Table 3. They
include rectal prolapse, functional problems including severe constipation [8], faecal incontinence and the solitary rectal ulcer syndrome [11,
12]. Constipated patients with both normal and
slow colonic transit have been investigated and
incontinent patients with and without rectal
prolapse have been studied.
Moderator Mr. Finlay: It is clear from the answers to this question that there is considerable
accumulated experience among our participants
which makes their individual comments all the
more valuable. The patient population studied by
the technique was as expected, the largest group
being those patients with obstructed defaecation.

What is your experience in control patients?


Mr. Bartolo: We have a relatively small experience of only 20 control patients. It is difficult on
ethical grounds to X-ray the pelvis of normal
subjects particularly women of childbearing age.
We are currently expanding our control series.
Dr. Bartram: Some series have extrapolated
"controls" by selecting those with normal radiological examinations. This will obviously give a
precise though preconceived definition of "nor-

mal", which may well be fallacious as the variability within an asymptomatic population will
not be established. We have recently reviewed 20
patients who were carefully screened to exclude
any defaecatory abnormality [13]. Ten male and
ten female patients were questioned to exclude a
history of frequency, excessive straining, incontinence with a normally formed stool and examined proctoscopically to exclude significant
haemorrhoids. Their mean age was 58 years
(range 38-70 years).
Dr. Fork and Dr. Ekberg: Control patients. We
have not been able to examine asymptomatic
volunteers.
Dr. Kodner: We have studied very few control
patients and would rely on the sophisticated study
done by Professor Stevenson at McMaster University to define the spectrum of normal findings.
We do recognise that there are levels of internal
intussusception seen even in completely asymptomatic patients. The most important issue is,
therefore, to define the indication for surgical
correction of the anatomical abnormalities seen
on defaecography.
Dr. Kuijpers: We have used control studies after
sphincter repair as normals. In these patients the
anal sphincters only were damaged, and repair
resulted in complete restoration of faecal continence. Needless to say, they were all young
women. However, in later studies we detected that
sphincter rupture was accompanied by denervation in at least 20-30%. So the need for normal
studies is growing more and more.
Dr. Mahien: Between 1978 and 1982 we studied a
series [5] of 56 patients whose defaecograms were
considered normal: 8 were made in asymptomatic
patients, 27 in patients with a functional colopathy, and 21 in patients with first-degree
haemorrhoids. Proctoscopy revealed no other
abnormalities. The 56 patients included 22 men
and 34 women with a mean age of 47.5 years
(range 17-80 years).
Professor Stevenson and Dr. Shorvon: Because a
number of abnormal findings were being seen
unexpectedly we studied 47 normal adult individuals (25 men and 23 women). Nearly half
(44% men, 45% women) had an intussusception

73
and 77% of the women had an anterior rectocele
which was moderate to large in 9 of the 23 patients. Mean pelvic descent in women was 2.0 cm
and 1.9 cm in men. Respectively, 23% and 20%
had a descent of more than 3 cm. Four patients
had an open anal canal at rest without incontinence (see below for further details) [14].
Mr. Womack: Integrated pressure - EMG
Proctography has been performed in 23 control
subjects (18 females and 5 males, median age 45
years, range 35-68 years). These subjects were
volunteers who had been admitted to hospital for
surgical procedures. They were all free from
anorectal symptoms at the time of the investigation and had no significant history of previous
anorectal symptoms or surgery. Nine female
subjects had been admitted for hysterectomy (6
for menorrhagia, 3 for localised neoplasia, none
for uterine prolapse). Others required treatment
for varicose veins (2), duodenal ulcer (2), gallstones (2), breast lumps (2), and non-specific
upper abdominal pain (1). The males required
admisstion for treatment of inguinal hernia (2),
hiatus hernia (1), duodenal ulcer (1) and renal
colic (1).
Moderator Mr. Finlay: Primarily for ethical
reasons, there is a paucity of information in
control patients. For example, Dr. Mahieu has
studied only 8 truly asymptomatic patients
despite performing over 1000 examinations. It is
for this reason that the study by Professor Stevenson is extremely important. It will now be necessary to reconsider our criteria of a normal
proctogram. In particular, he has demonstrated
that a degree of perineal descent, rectocele and
even intussusception may occur in asymptomatic
subjects. Thus there is clearly a danger that a
proctogram in isolation may be over-interpreted.
It may be that as further information is gained
from integrated studies, using EMG and pressure
monitoring, the important factors which distinguish
symptomatic from non-symptomatic patients may
be identified.

Can you define in precise terms the findings


in a normal study?

Mr. Bartolo: The normal appearances in our


experience of evacuation proctography consist of
the following:

a) Descent of the anorectal angle; less than 3 cm


below the resting position.
c) Increased anorectal angulation.
c) Loss of the puborectalis impression.
d) Shortening of the anal canal.
e) Funnelling of the anorectum.
f) Rectal emptying.
g) At completion of rectal emptying a small
amount of infolding of the anterior and
posterior rectal walls is normal. This may look
similar to a small intussusception.
Dr. Bartram: The findings in our 20 control subjects were as follows. At rest the anorectal junction lay at a median of 1.4 cm above the plane of
the ischial tuberosities, descending 3 cm on evacuation - to the point where the anal canal just
started to open. The anorectal angle at rest was
94_+ 19 ~ and 113_+ 16 ~ during evacuation, when
measuring along the posterior wall of the rectum
which is more accurate than using the central axis
of the rectal lumen. The median width of the fully
opened anal canal was 1.45 cm (range 0.8-2 cm).
The time taken for the anal canal to open fully
was a median of 4.5 seconds, with rectal evacuation taking 11 seconds. A clearly defined "zone of
evacuation" was demonstrated with only the
distal half of the rectum, usually below the transverse fold, emptying. Anterior rectocele formation
was present in 10 patients including 8 females and
a posterior rectocele was seen in 5 including 2
females. Towards the end of evacuation small
anterior wall folds were noted in 3 patients and
posterior folds in 17. The anterior wall of the
distal rectum collapsed down onto the anal canal
in seven at the end of evacuation. Thus, this
asymptomatic population exhibited a considerable variation in configuration of the rectum
during evacuation.

Dr. Fork and Dr. Ekberg: During resting conditions the anorectal angle in normal patients
measures 70~
~ mean 114 ~ During defaecation, this increases to 110~
~ mean 135 ~
Normally the anal canal opens symmetrically and
attains the form of a cone, being wider cranially.
This is seen in both lateral and anteroposterior
projections. The initial event is a widening in the
anterior aspect of the upper third of the anal
canal. The contrast medium in the rectum is then
emptied by contraction of the rectum. This is
usually seen as a simultaneous contraction of the
entire rectum, and only occasionally as a peristal-

74

MeanValueatRest
30"

~ 20. ~
._~

92 ~

MeanValueDuringStraining
137 o

~ AtRest
Strainin~~
-~-

"a
~ lO,

65- 75- 85- 95- 105- 115- 125- 135- 145- 155ValueoftheAnomctalAngleInD~n~s
Fig. 1. Anorectal angle in 56 normal patients at rest and during straining. After Mahieu et al. [5]
tic wave. The evacuation of the rectal content in
these cases is complete. There is often a folding
tendency of the lower rectal mucosa, seen as a
mucosal impression, about 5 mm thick, on the
barium column. The indentation moves a few
centimetres in a distal direction. During defaecation there is a concomitant descent of the pelvic
floor by 2 to 8 cm (mean 4 cm) as seen on the
lateral rectal films.
Dr. Kodner: We have defined our criteria for a
normal defaecogram or proctogram as follows:
(a) an increase in the anorectal angle on straining;
(b) relaxation of the puborectalis muscle on
straining; (c) wide opening of the anal canal; (d)
total evacuation of rectal contents; (e) normal
resistance of the pelvic floor; (f) maintenance of
the rectal fixation at the sacral promontory during
straining; (g) absence of internal intussusception.
Dr. Kuijpers: Although we have not done a study
in normal subjects, we have our definitions of a
normal defaecography. The anorectal angle at rest
is about 85-90 ~. In older people, especially
women, it may be increased to 95-100 ~ It decreases to 75-80 ~ during squeezing and increases
to about 135 ~ during straining.
Barium is excreted without difficulty in 5 to
10 s. The posterior rectal wall remains fixed to the
anterior sacral surface over its full length. The
anorectal junction descends about 3 cm. Rectal
configurations generally remain straight, but
small rectal wall invaginations may occur at different levels. Asymptomatic rectoceles are common in older women.
Dr. Mahieu: We prefer the term of "defaecography" instead of "proctography" because defaecography more clearly implies that a physiological function (defaecation) is examined under

dynamic conditions analogous to the investigation


of deglutition or micturition. Proctography would
be a suitable term for a static and morphologic
study of the anorectal system. Defaecography describes better the aim of the examination, namely,
the study of the mechanism of rectal evacuation
and of its disorders.
A normal defaecogram consists of five fundamental conditions [5] - the first two are due to
relaxation of the puborectal muscle:
a) Increase of the anorectal angle. In our series of
56 normal patients the anorectal angle measured
a mean value of 92 ~ at rest and 137 ~ during
straining. Figure 1 illustrates the distribution of
the anorectal angle values in both conditions.
b) Obliteration of the impression of the puborectalis sling on the posterior wall of the distal rectum.
c) Wide aperture of the anal canal.
d) Evacuation of the rectal contents, totally (55%)
or slightly incompletely (45%).
e) Good resistance of the pelvic floor, the mean
normal descent of which is not more than 3.5 cm
[151.
Professor Stevenson and Dr. Shorvon: In our
control patients the mean anorectal angle was 96 ~
in males and 95 ~ in females but there was a wide
variation of 61 ~ and 64 ~ respectively. An astonishing variation in all other measurements was
found. For example the mean length of the anal
canal was 22 mm in males and 16 mm in females
but in five females this was less than 10 mm and
in one it was only 6 mm. One male and three
females had an open canal at rest, although all
but one closed on squeezing. All four were apparently incontinent on coughing and straining and
all had an anorectal angle in the upper end of the
range. In all male subjects the anorectal junction
was at or above the level of the ischial tuberosities, while in 23% of the females the anorectal
junction lay below the tuberosities. The mean lift
of the anus on squeezing was 1 cm in both sexes.
While pelvic descent averaged 2 cm, the range
was considerable being up to 39 mm in males and
54 mm in females. This range of movement was
greater than occurs when patients are examined
in the left lateral position.
Intussusception was graded (see Fig. 2) and
we were surprised by the amount of intussusception found during normal straining. Nine of
the 46 normal individuals had a grade 5 or 6
intussusception. This caused us to revise our ideas
on the pathological significance of moderate intra-

75
contracts. Although to my knowledge this has not
been conclusively demonstrated, I would agree
that in a normal study there is the appearance of
a contraction wave.
All participants agree that the measurement of
the anorectal angle is inexact because the configuration of the lower rectal wall is variable.
Anorectal angle therefore, at best, must be an
approximate measurement.
Enumerate the radiological abnormalities
observed on proctography
Fig. 2. Grading of mucosal prolapse and intussusception.
Grades 1 and 2 involve folds of mucosa of 3 mm or less in
thickness. For grades 3 and above the folds are of greater than
3 mm. In grade 5 the circumferential fold impinges on the internal and orifice, in grade 6 extends into the anal canal and in
grade 7 prolapses externally

rectal or even rectoanal intussusception. It is not


possible to differentiate mucosal prolapse from
full thickness intussusception since only the
mucosa is coated, but we believe any fold of more
than 3 m m in thickness is likely to be more than
the mucosa alone.
Mr. Womack: Voiding is initiated by voluntary
straining that increases intrarectal pressure to
60cm of water (range 50-140cm). External
sphincter EMG activity is inhibited though transient recruitment occurs at the onset of straining
in some cases. The pelvic floor descends as the
rectal contents distend the upper anal canal. The
anorectal angle widens from 93 ~ (range 86-108 ~
at rest to 132 ~ (range 120-145 ~) during voiding
when the anal canal anteroposterior diameter
becomes 2.3 cm (range 1.2-3.0 cm). The rectum
empties completely without prolapse of its wall
into the anal canal. Following voiding the resting
anatomy is restored by a contraction of the pelvic
floor and external sphincter :musculature.
Moderator Mr. Finlay: It is of interest that
although only Professor Stevenson and Mr.
Womack have a good study of normal patients, all
the participants claim to have a very clear knowledge of what is required in a normal study. These
were best summarised by Dr. Bartolo and Mr.
Womack. Indeed, there was a broad measure of
agreement regarding this question. I was particularly interested to note that Dr. Fork and Dr.
Ekberg were of the opinion that the rectum

Mr. Bartolo: Abnormal radiological signs include:


a) Persistent puborectalis impression. This is
usually associated with failure to evacuate contrast. The anorectal angle remains acute.
b) Rectocele. The anterior rectal wall herniates
forward into the vagina and contrast is displaced
anteriorly.
c) Rectal intussusception. Minor folds in the
rectal wall do not constitute intussusception. To
fulfill the criteria for diagnosis, there must be an
obvious intussusceptum contained within an
intussuscipiens. It should be emphasised that a
small amount of internal prolapse at completion
of defaecation is normal. Rectal intussusception
may be (a) rectorectal with infolding of the full
thickness of the rectal wall such that the upper
rectum descends into the flattened distal rectum.
This is associated with separation of the rectum
from the sacral promontory; (b) rectoanal, here
the upper rectum enters the dilated anal canal; (c)
complete rectal prolapse, the intussusception
emerges through the anal canal and is seen
protruding below the external anal verge.
d) Anterior rectal wall prolapse. Prolapse of the
anterior rectal wall with intussusception.
Dr. Bartram: These can be divided into structural
abnormalities seen in the configuration of the
rectal wall during evacuation and "sphincteric
dysfunction" or pelvic floor spasm. Concentrating
on the sphincteric aspect first, the anal canal
should be closed at rest, becoming rapidly effaced
during evacuation so that the anorectum is a
broad open-ended tube which empties rapidly
(less than 30 s). It is abnormal for the anal canal
to be open at rest, and leakage of contrast (120 ml
injected) suggests weakness of the sphincter. Conversely, failure of the sphincter to open properly
correlates with paradoxical contraction of the
puborectalis on integrated proctography. A per-

76
sistent posterior indentation during evacuation
suggests puborectalis contraction, but this is infrequent and usually the anal canal shows a Vshaped configuration. This is associated with slow
evacuation, of more than 30 s, which is often incomplete.
Anterior rectocele formation may be regarded
as a normal variant in females. When present, the
rectocele collapses down onto the anal canal at
the end of evacuation. This can be difficult to
distinguish from intra-anal intussusception. However, the dividing line is any movement into the
anal canal. Any fold that prolapses into the anal
canal is abnormal and implies intussusception.
Dr. Fork and Dr. Ekberg: There appear to be us
to be least eight features which indicate abnormality.

Fig. 3. Internal intussusception also showing increased postrectal space

a) Prolapse of the anal mucosa:


During resting conditions the anorectal radiographic morphology is normal. During straining
the mucosa in the opened-up anal canal folds,
bulges and broadens. In typical cases this is seen
from a level 3-6 cm above the external anus. The
folds descend up to 4 cm through the external
orifice. The thickness of the prolapsed mucosa
does not exceed 1 cm.

the rectum after straining. It is probably due to


absent or impaired contraction of the rectum
lumen.

b) Internal proccidentia:
This is a condition in which a circular indentation
in the barium column is seen 6-1 l cm above the
internal anus. The indentation progresses and
deepens to form a ring pocket. This may reach up
to, into or through the anal canal. In the latter
case it is referred to as a rectal prolapse. The
thickness of the intussusception varies between 2
and 4 cm in anteroposterior diameter and is
usually deeper anteriorly than posteriorly.

g) Faecal incontinence:
Patients with uncontrolled loss of faecal material
under resting conditions are suffering from faecal
incontinence. Radiographically the anorectal
angle at rest can be seen to be increased. This
condition is evident on lateral radiograms.

c) Enterocele:
This is a condition observed in patients in whom
a deep rectogenital fossa is seen on lateral films. It
is diagnosed as an increased distance between the
vagina and the rectum. This space may or may
not contain small bowel loops, i.e. forming an
enterocele.
d) Rectocele:
This condition is seen as a forward bulging involving the anterior aspect of the rectum. A
rectocele may sometimes have a considerable
depth.
e) Retention of barium:
This is a fairly uncommon finding in patients in
whom there is residual contrast medium within

t) Abnormal descent of the pelvic floor on


straining:
This is seen as either an increased or decreased
descent.

h) Defective opening of the anorectal angle:


This condition is seen in cases with a persistent
indentation of the puborectal muscle in the dorsal
aspect of the lower rectum seen in true lateral
projection.
Dr. Kodner: We have found five categories of
disease abnormality, each with its own findings
on defaecography (see Table 2). Internal intussusception (Fig. 3) presents on defaecography with a
typical funnel-like configuration of the intussusception, markedly abnormal mobility of the rectum from the sacral promontory and almost
always a redundant sigmoid colon. Complete
rectal prolapse, of course, shows all the findings of
intussusception with complete extrusion of the
rectum through the anal orifice. The syndrome of
non-relaxing puborectalis muscle (Fig. 4) should

77
obvious forceful straining by the patient during
the defaecography. The patient with the descending perineum syndrome can be shown on
defaecography to have exaggerated motion of the
perineum. Measurements on plain films and with
perineometer have proved to be more accurate.
Patients with rectocele have been observed many
times on defaecography to also have internal
intussusception of the rectum. The internal intussusception is probably a significant component of
the condition referred to as rectocele. We have
found that patients treated surgically for intussusception of the rectum who have had refractory
rectoceles have in fact not needed additional
surgery to correct the rectocele.
I

Fig. 4. Non-relaxingpuborectalisduring attempted evacuation

Fig. 5. Perinealbulging or herniation. The centre of the levator


muscledescendsdistallyto the line drawn betweenthe anorectal angle and the tip of the coccyx. The impression of the
puborectalis sling ean be seen. The anal canal remains closed,
barium is not excreted

possibly be better called pelvic floor outlet obstruction since we are not sure of the primary
defect. A very prominent posterior intendentation
and anterior distortion of the low rectum is seen
even during straining to defaecate. The normal
straightening seen from relaxation of the pelvic
floor and sphincter mechanism does not occur.
The rectal ampulla does not empty in spite of

Dr. Kuijpers: Radiological signs of functional


rectal disorders consist of abnormal changes of
rectal configuration during straining.
The anterior rectal wall may bulge just above
the anal canal and form a rectocele. Its expansion
into the rectovaginal septum can be demonstrated
by simultaneously marking the vagina. Also, the
centre of the levator muscle may descend distally
to the line drawn between the anorectal angle and
the tip of the coccyx. This perineal bulging may
occur when straining is done on a contracting,
normal puborectalis sling and a denervated levator muscle giving way. We consider it a complication of the spastic pelvic floor syndrome (Fig. 5)
[16]. The levator has been denervated due to
persistent defaecation straining against a contracting pelvic floor.
When both the puborectalis and levator
muscles are denervated and only the external
sphincter functions normally, the anorectal junction descends much deeper and a hockeystick-like
configuration may be seen (Fig. 6). Small herniations due to local defects in the pelvic floor may
also be seen [16].
Invaginations may occur at any point along
the anterior and posterior rectal walls, but are
most frequent in the lower rectum. They can be
demonstrated by filling the small intestine with
barium or by performing peritoneography which
will locate the lowest part of the Pouch of Douglas. Rectal invagination at this point must mean
peritoneal herniation. Both anterior and posterior
wall invagination at the same level represent
circular invagination, i.e. rectal intussusception.
In the lower rectum the typical funnel-like configuration as seen in complete rectal prolapse may
occur (Fig. 6).

78
[1

Fig. 6. Rectal intussusception. The typical funnel-like configuration of internal intussusception, created by prolapse of both
the anterior and posterior rectal wall. Protrusion through the
anal canal as in complete rectal prolapse does not occur (reprinted with permission of Digestive Disease)

Proctography also enables us to study the


movements of the pelvic floor. An increased angle
at rest suggests denervation. When during squeezing the angle does not decrease, either there is no
muscular function or the patient does not know
how to squeeze. Conversely, when during straining
the angle does not increase, abnormal contraction
of the pelvic floor would seem to be present [17].
However, denervation of part of the pelvic floor
muscle in a patient with a contracting pelvic floor
during straining may simulate an increase of the
anorectal angle (hockeystick-like configuration)
[16], and thus suggest that pelvic floor relaxation
is taking place.
Dr. Mahieu: Three measurements are to be con-

sidered in defaecography: the position of the


pelvic floor, the size of the anorectal angle and
the diameter (and length) of the anal canal.

Fig. 7. Methods of measurement of the anorectal angle. On the


same image, the value of the anorectal angle is different if the
rectal axis is drawn as the line AC or AD. In the method proposed by Mahieu et al. [3], AC is parallel to the line a and varies with the degree of impression of the puborectal muscle on
the posterior rectal wall. The value of the anorectal angle, thus
measured, is representative of the state of contraction or relaxation of the puborectal muscle. The anorectal angle whose rectal axis is AD, as proposed in the usual method does not adequately reflect the muscular activity in the different situations
(at rest, during squeezing or straining)

The position of the pelvic floor can be defined


in relation to a bony landmark, for instance, the
pubococcygeal line (a line drawn from the upper
edge of the pubic symphysis to the distal edge of
the coccyx). The distance between this line and
the anorectal junction expresses the position of
the pelvic floor in centimetres. This value remains
normally under 8.5 cm [15]. Changes in position
can be measured in centimetres during squeezing
and straining.
The value of the anorectal angle is only interesting if it is representative of the activity of the
puborectal muscle, so that we take the proximal
axis of the anorectal angle as the line drawn
parallel to the posterior edge of the rectal ampulla
at the impression of the puborectal sling [5]
(Fig. 7).
Six main radiological abnormalities can be
observed:
1. Mucosal or full-thickness rectal intussusception
or prolapse. Different stages can be observed in
rectal intussusception. Mucosal prolapse concerns
only the mucosal layer and produces only very

79
thin folds seen on the films. Full-thickness intussusception can be intrarectal, intra-anal or
external (rectal prolapse).
2. Outpocketing of the rectal wall which protrudes
anteriorly or posteriorly during evacuation.
3. Intermittent or permanent paradoxal imprint of
the puborectalis sling during evacuation, consecutive to a lack of coordination in the pelvic
floor muscle activity.
4. Pelvic floor descent at rest or during straining
(the anorectal junction should not drop more
than 3.5 cm in a normal subject during defaecation [13, 15, 18].
5. Widening of the anorectal angle at rest or
during straining.
6. Permanent opening of the anal canal and
eventual unvoluntary loss of contrast m e d i u m
injected in the rectal lumen.
Professor Stevenson and Dr. Shorvon: The radiological abnormalities that can occur on proctography are observed during various phases of
the examination. Thus they include features at
rest and during different manoeuvres.

a) At rest: Abnormal anorectal junction position, abnormal anorectal angle, reduced canal
length or open canal, incontinence. Flat rectal
floor, small or large volume rectum.
b) Squeezing: Failure to elevate the pelvic floor,
failure of canal to close, failure of increase in
puborectalis impression, separate indentation of
puborectalis and posterior parts of levators.
Unusually prominent puborectalis. Failure of
abnormal anorectal angle or sphincter appearances to return to normal.
c) Straining: Failure to descend or abnormal
descent, failure of puborectalis to relax (real or
inhibition?), incontinence, prolapse or rectocele or
enterocele. Postero-lateral pouches (these are seen
as mid-rectal posterior bulges and represent
lateral herniations of the rectal mucosa through
the levators in patients who habitually strain).
d) Evacuation: Failure to relax the puborectalis or
paradoxical tightening of puborectalis. Delay in
opening or incomplete opening of sphincter.
Intussusception with or without obstruction to
defaecation, and with or without rectocele formation. Enterocele or sigmoidocele formation is
shown by separation of rectum and vaginal
tampon. If opacified prior to the procedure, sigmoid colon or small bowel can be seen prolapsing
into the gap.

e) Post-evacuation: Assessment of degree of


emptying. If no emptying, a bisacodyl suppository
can be given to assess its effect.
Mr. Womaek: The most striking abnormalities
seen on proctography are rectal intussusception,
rectocele formation and localised irregularities of
the rectal mucosa. Rectal intussusception varies in
degree forming a spectrum of conditions. In its
most limited form the anterior rectal wall invagihates into the rectum or anal canal as an anterior
rectal wall prolapse. Next in degree is an intrarectal intussusception where a circumferential invagination of the rectal wall forms the head on an
intussusception that travels within the rectum
towards the anus. When the head of the intussusception enters the anal canal an intra-anal intussusception is present. If it passes through the anal
canal it becomes an extra-anal intussusception.
Eversion of the mucosa of the anal canal may
accompany this, resulting in a full thickness rectal
prolapse. A rectocele results from inadequate
support of the anterior rectal wall above the anal
canal. On straining the rectum balloons forward
into the upper vagina. Mucosal irregularities
occur in neoplasia and the solitary rectal ulcer
syndrome. They may be due to polypoid elevations or mucosal ulceration.
Other abnormalities revealed by proctography
are less visually striking. They are nonetheless
associated with major disturbances of anorectal
function. They include failure of the anorectal
angle to widen with straining and excessive distension of the anal canal during voiding.
Moderator Mr. Finlay: All the participants agree
that intussusception and prolapse are the most
apparent abnormalities on proctography. The
majority also include large rectocele as an abnormality, although they recognise that small rectoceles are probably normal. It has been noted
that those patients with rectocele also frequently
have a bulging posterior pelvic floor. Dr. Kuijpers
is very firmly of the opinion that this is an event
secondary to the failure ofpuborectalis relaxation.
Paradoxical contraction of the puborectal
muscle on straining and descent of the pelvic
floor have also been included. This however may
be related to patient compliance and it is important to ensure that maximal straining is achieved.
In addition, normal patients may contract the
puborectalis because of embarrassment in an
attempt to avoid uncontrolled expulsion of intrarectal content. It is clear that the pathophysiology
of outlet obstruction has yet to be explained.

80
What correlations do radiological abnormalities
have with the various disease entities studied?
Mr. Bartolo: Persistent puborectalis impression is
the commonest finding in slow transit constipation. This is usually accompanied by failure of
evacuation so should not be over-interpreted
since it may reflect lack of rectal awareness. A
normal defaecatory response will accordingly not
ensue. Rectal intussusception is the commonest
abnormality associated with perineal descent of
more than 3 cm on straining. In our experience
the remaining patients with descent have either
a rectocele or prolapse of the anterior rectal wall.
Failure to open up the anorectal angle is rarely
seen in this group but dynamic studies with
simultaneous electromyography may show paradoxical contraction of the sphincter muscles
despite apparent relaxation on radiological screening. Such findings may have important bearing on
the pathogenesis of pelvic floor descent and
obstructed defaecation.
Rectoceles are c o m m o n findings in women
with obstructive symptoms, yet in some patients
in whom they are associated with intussusception,
rectoceles have been repaired by combined anterior and posterior rectopexy [19] with little improvement in obstructive symptoms. This suggests
that they are more likely to be manifestations of a
weakened pelvic floor than the primary cause of
obstructive symptoms. Proctography usually
reveals abnormalities which correlate with the
presenting symptoms, but unfortunately all too
frequently the demonstration of a specific abnormality does not readily translate into a particular
therapy in which correction of the pathology
yields a satisfactory clinical result.
Dr. Bartram: We have used evacuation proctography in the investigation of constipation to determine which patients have a defaecatory disorder.
In 13 women with severe constipation [20] there
was gross delay in evacuation, with six being
unable to expel any barium. These patients
represent the most severe end of the spectrum of
the spastic pelvic floor. In a larger study of 58
consecutive patients with idiopathic constipation
[21] a more representative range of patients was
investigated. The only significant differences from
normal were the time taken for evacuation and
the amount of barium remaining in the distal
rectum. Fifteen of the 20 controls evacuated
within 20 s, whereas 45 of the 58 patients took

Fig. 8. Proctogram in a female patient with refractory idiopathic constipation. Note the pelvic floor descent from continued straining, poor opening of the anal canal associated
with delayed and incomplete evacuation - typical findings of
sphincter dysfunction

longer. Nineteen of the 20 controls evacuated


more than 60% of the area of the distal 4 cm of
rectum, compared with only 25 of the 58 patients
in the study group (Fig. 8).
In the solitary rectal ulcer syndrome there
may be a combination of intussusception and
sphincter dysfunction. Proctography can demonstrate both components, although if the patient is
unable to evacuate internal intussusception may
not be seen, although large fixed folds are often
apparent at the site of the ulcer.
Dr. Fork and Dr. Ekberg: Our observations suggest the following associations between diseases
and radiological abnormalities.
Internal proccidentia: The formation of a ring
pocket corresponds to a mucosal invagination.
Enterocele is due to a deep Pouch of Douglas
while rectocele is due to laxity of the rectovaginal
septum. Retention of barium is due to defective
contraction of the rectal wall. This in turn may be
due to defective nerve supply or defective musculature as in diabetes mellitus, alcoholism etc.
Defective opening of the anorectal angle is due to
defective relaxation of the puborectal sling. Increased descent of the pelvic floor may indicate
laxity of the levator ani muscle.
Separation of the rectum and sacrum indicates
the presence of a mesorectum. This is one of the
prerequisites for the development of an intussusception.

81
Table 4. Indications for defaecography
Longstandingconstipation with forceable straining
Sensation of incomplete rectal evacuation
The need for digital manoeuvres in order to evacuate the
rectum
Significantsensation of pelvic pressure and pain
Variable degrees of incontinence in conjunction with a background history of constipation

barium solution used also plays a role. Watery


solutions will easily mimic water enemas.
Likewise, E M G is a necessary diagnostic supplement when barium excretion is difficult or
prolonged, despite a seemingly increasing angle.

Dr. Mahieu: a) Mucosal and full-thickness intus-

Dr. Kodner: Our indications for defaecography


include symptoms which are attributed to pelvic
floor abnormalities or suspected abnormalities of
colonic transit. These are listed in Table 4.
With increasing experience in defaecography
and in the clinical evaluation of patients with
these problems, we have increased the correlation
between symptoms and abnormal X-ray findings.
In the past year, 95% of patients evaluated with
defaecography have had X-ray findings which
explain their presenting symptoms. It is difficult
to distinguish pelvic floor outlet obstruction from
internal intussusception without defaecography.
There is also some question as to whether one can
exist without the other.

Dr. Kuijpers: A rectocele is c o m m o n in older


women and does not routinely need treatment.
The clinical equivalent of the various radiological
abnormalities manifesting as perineal herniation
is the descending perineum syndrome.
Rectal intussusception should be treated by
rectopexy. However, about 20% of patients treated
surgically have persistent complaints despite an
adequately fixed rectum as demonstrated by control defaecography.
We have done a study in patients with faecal
incontinence which showed that the anorectal
angle at rest was increased in only 80% of patients
with pelvic floor denervation. On the other hand,
an anorectal angle of 90 ~ did not necessarily
represent normal pelvic floor function. Our conclusion was that it is a rather inaccurate technique
to diagnose pelvic floor denervation. Moreover,
single fibre E M G is a much better test to diagnose
and quantify denervation.
Pelvic floor contraction during straining is
frequently observed. Some patients are completely
unable to open their anal canal and excrete barium
and others will lose a little only after several
attempts. Uneasiness and embarrassment should
be excluded as causes of pelvic floor contraction,
which can be done by E M G and segmental
colonic transit time. No doubt the viscosity of the

susception or prolapse. The clinical significance of


mucosal folds seen at the end of defaecation in
the rectal lumen is uncertain and the differential
diagnosis between normal folds and mucosal
prolapse is difficult [13, 15]. Redundant folds
protruding in the anal canal could be considered
as certain mucosal prolapse. Diagnosis of intrarectal, intra-anal intussusception and external
prolapse is more evident.
b) Rectocele. An asymptomatic small outpocketing
of the anterior wall of the rectum has been
observed, even in men, and can be considered as
a normal variant [5] confirmed by Bartram [13].
Symptomatic rectoceles present a larger size,
retain some residual paste at the end of defaecation, and need digital pressure on the posterior
wall of the vagina to be emptied.
c) Dyskinetic puborectal muscle. This is usually
hypertonic and is associated with difficult evacuation, anal blockage, multiple attempts to evacuate,
largely incomplete evacuation and sometimes
digital intromission. The hypertony can be intermittent or transitory and followed by total evacuation.
d) Descending perineum syndrome. The patient
complains of a sensation of obstruction, mucous
and bloody discharge, vague dull aching pain in
the perineum and eventually incontinence. Pelvic
floor descent can be present at rest (more than
8.5 cm) or during straining (more than 3.5 cm)
and the perineum bulges posteriorly between the
coccyx and the anus. The association with intussusception or mucosal prolapse is not a constant
finding. Obliteration of the imprint of the
puborectal muscle is frequent at rest.
e) Incontinence. This is expressed not only by an
increase of the anorectal angle at rest, but also by
an enlarged opacified anal canal due to anal
sphincter hypotony.
f) Solitary ulcer syndrome of the rectum. The
commonest abnormality in a personal series of 43
patients [22] was the presence of an intussusception, seen in 34 patients (79%). Of these, 19 (44%)
had an external rectal prolapse and 15 (35%) an

82
intra-anal or intra-rectal intussusception. Dyskinetic contraction of the puborectal muscle was
recognised in only four cases (9%) and was associated with intra-anal rectal intussusception in
only one case. Self-digitation was admitted by one
third of the patients.
Professor Stevenson and Dr. Shorvon: The symp-

tomatology of defaecation disorders is complex


and involves both rectal and colonic function as
well as the patient's psyche. This last factor may
confuse any radiological correlations that might
exist. It is therefore important to review the films
and videos with clinicians.
Constipation: In patients who complain of difficulty in initiating defaecation, a variety of appearances may be seen including those occurring
in normal individuals. Some patients have a
prominent puborectalis which tightens further on
attempted defaecation. Others have a flat rectal
floor with a long anal canal which fails to open,
and this appearance has been seen in patients
with spinal multiple sclerosis and previous spinal
cord tumours. Patients with a long history of
straining may show a postero-lateral rectal bulge
and may progress to incontinence.
Interrupted Defaecation: These patients may have
an intussusception which obstructs the upper anal
canal and sometimes traps barium in a rectocele.
An enterocele may similarly obstruct defaecation
and is usually associated with an intussusception.
Incontinence: A wide variety of appearances is
seen. Some patients have a patulous sphincter

and absent puborectalis, and no other obvious


abnormality. Preservation of either sphincter or
puborectalis with loss of the other one is seldom
accompanied by radiological demonstration of
incontinence. Some patients in addition have a
very low pelvic floor, or extreme mobility of the
pelvic floor in addition to the sphincter and
puborectalis abnormalities. Some have a posterior
rectal bulge, an enterocele or intussusception and
a history of straining for years. It seems likely in
these cases that an inability to initiate defaecation
has led, through straining, to weakness of the
pelvic floor musculature and incontinence,
whether by neurogenic means or by simple direct
stretching.
Solitary rectal ulcer syndrome: Grade 4 or more
intussusception with failure of puborectalis/
sphincter relaxation [ 12].
Mr. Womaek: Table5 shows the radiological
abnormalities revealed by proctography in control
subjects and three clinical conditions studied.
Rectoceles occurred with a similar incidence in
the control subjects and the three patient groups.
There were significantly higher incidences of rectal intussusception in the constipated patients
(p < 0.01), incontinent patients (p < 0.001) and the
solitary rectal ulcer patients (p <0.001) than in
the control subjects. The incontinent patients
(p < 0.02) and the solitary ulcer patients (p < 0.001)
had significantly higher incidences of rectal intussusception than the constipated patients. In addition the intussusceptions were of a more advanced degree in the incontinent patients (p < 0.01)

Table 5. The incidences of radiological abnormalities in control, constipated, incontinent, and solitary rectal ulcer syndrome
(SRUS) subjects

Rectocele

Controls
n=23

Constipation
n=59

Incontinence
n=31

SRUS
n=18

13%

22%

13%

6%

Ant rect wall prolapse


Recto-rectal intussusception
Intra-anal intussusception
Extra- anal in tussusceptio n

0%
4%
0%
0%

6%
17%
14%
6%

0%
3%
37%
16%

11%
0%
45%
28 %

Total intussusception

4%

43%

56%

84%

2.5
( 1.5-3.0)

3.0
( 1.7-5.3)

4.2
(1.5-5.4)

A-P diameter of anal canal cm


Anorectal angle
Resting
Voiding

2.3
( 1.0-3.3)
93
(86-108)
132
(120-145)

96
(86-132)
124
(106-160)

121
(90-152)
145
(116-166)

96
(88-122)
134
(92-160)

83
and the solitary ulcer patients (p < 0.05) than the
constipated patients. There was a correlation between the presence of an intussusception and the
anteroposterior diameter of the anal canal during
voiding, with the patients with more advanced
degrees of intussusception having greater anteroposterior diameters. This resulted in the anal canal
diameters being significantly greater in the incontinent patients (p <0.001) and the solitary ulcer
patients (p <0.001) than in the control subjects.
The anorectal angles at rest and during voiding
were similar in the control, constipated and solitary ulcer subjects, but both the rest (p<0.001)
and during voiding (p <0.001) angles were significantly wider in the incontinent patients than
in the control subjects.
Moderator Mr. Finlay: All contributors have
emphasised the ability of the technique to identify
prolapse and intussusception. This would appear
to be the only clinical entity which can be
identified with certainty. Although perineal
descent, rectocele, posterior pelvic floor hernia
and puborectalis paradox have been observed by
all the participants, the clinical significance of
these findings has yet to be determined with
certainty.
It is clear that the aetiology and nature of
"puborectalis paradox" has yet to be elucidated.
Indeed, there is still no uniformity of nomenclature for this clinical entity. It has been called
outward obstruction constipation, obstructed defaecation or spastic pelvic floor syndrome. Dr.
Kuijpers has indicated that he would now favour
electromyography for the diagnosis of this clinical
entity rather than the use of videoproctography.
Further study using integrated manometry, EMG
and videoproctography may help to shed light on
the pathophysiology of this condition.
Several contributors indicated that these
features rarely occur in an individual patient in
isolation. Indeed, there is considerable overlap,
such that they may all be components of a single
clinical entity. In this respect, one might speculate
that idiopathic faecal incontinence is the end
stage of that disease process.

Can proctography influence treatment?


Mr. Bartolo: We routinely use proctography to
investigate patients with incontinence, obstructed
defaecation and constipation. Incontinent patients
can usually be subdivided into those with sphinc-

Table 6. Evacuation proctography: Anorectal physiology in 17


patients with solitary rectal ulcer syndrome
Postoperatively 12 improved - Group A
5 unchanged - Group B
Proctography

Complete evacuation < 30 s


Perineal descent
Internal intussusc.

9
4/9
6

5/5 a
5

AR physiology
basal squeeze
Anal eanalp
Pudendal n 1at.

96 + 14

77 + 18

65 +_ 16
2.26+0.15

70_+ 10 mm Hg
2.83 +0.034

" Significancep < 0.05

ter divisions, prolapse or neurogenic incontinence


or combinations of each of the three. Where rectal
prolapse, either complete or occult (internal), is
demonstrated on proctography the procedure of
first choice is an abdominal rectopexy. The remainder with normal proctograms have electromyography to determine whether to perform an
anterior or posterior sphincter repair. The majority of patients with slow transit constipation
exhibit a complete failure to relax the puborectalis accompanied by an inability to evacuate any
contrast. Since we do not recommend puborectalis division, this finding does not help management. Rectal intussusception is frequently observed in patients with obstructed defaecation.
Unfortunately in our hands the results of abdominal rectopexy to relieve obstructive symptoms as
indicated above are very poor. Because of this we
try to relieve associated constipation with laxatives, enemas and suppositories. Many patients
have severe symptoms which justify a surgical
approach. If a rectal intussusception has been
demonstrated we now combine a rectopexy with a
partial colectomy. If transit studies reveal slow
transit constipation we do a subtotal colectomy
with the rectopexy.
Dr. Bartram: In the solitary ulcer syndrome some
patients are not improved by anterioposterior
rectopexy. In a preoperative study of 17 patients
[23], those with evidence of sphincter dysfunction
who had slow and incomplete evacuation were
not symptomatically improved compared with
those in whom evacuation was normal (see Table 6).
Patients with severe refractory constipation
pose a considerable problem in management.

84
Surgery may be contemplated, and it is then vital
to know if there is a gross defaecatory disorder
present. If so, then simply resecting part of the
colon will not help for the same reasons that
laxatives or bulk forming agents will not [20].
Unfortunately the results of puborectalis division
have not been encouraging, so that as yet no
sphincteric surgery has been developed with
which to correlate proctographic findings.
Proctography therefore has a role in patients
with solitary ulcer syndrome and severe constipation, to identify those with difficulty in evacuation
in whom surgery might not be beneficial. It is of
limited value in patients with incontinence. Pelvic
floor descent at rest, a widely open anal canal
with a vertical rectum are typical appearances of
incontinence due to neuromuscular damage. The
anatomical configuration pre- and post-surgery
has been used to define the changes after a
postanal repair.
I have performed a few examinations on
patients who have had surgery during infancy for
congenital anomalies. These have not proved
valuable in assessing residual sphincteric function,
and other imaging techniques such as computerized tomography would be recommended
[24].

raphy. We feel that because of the significant


overlap of symptoms for many conditions of the
pelvic floor the more documentation we can
obtain for specificity of disease the better. There is
a small subset of patients who have a very distal
intussusception without marked mobility from the
sacral promontory, and we are concerned that our
usual fixation procedure will not be adequate for
these patients.
Perhaps more important is the misdiagnosis of
patients with haemorrhoids and symptoms of
difficulty having bowel movements. We suspect
that the recently reported disastrous results of
elastic ligation of haemorrhoids have occurred in
patients having either internal intussusception of
the rectum or pelvic floor outlet obstruction. We
stress that a patient who is found to have haemorrhoids, but who has symptoms of pelvic floor
abnormality should be evaluated at least with
proctography. The diagnosis of outlet obstruction
is confirmed by the inability to defaecate a
balloon in the setting of a normal sphincter
mechanism. We feel it is a mistake to treat
haemorrhoids surgically in these patients. This
combination of problems we have seen in males,
as well as females.

Dr. Fork and Dr. Ekberg: In patients with an


internal intussusception of the rectum a Ripstein
rectopexy is often helpful. Patients without such
an intussusception do not benefit from rectopexy.
The internal intussusception cannot be revealed
by diagnostic modalities other than defaecography.
No treatment of choice is available for the other
diseases discussed in this symposium.

Dr. Kuijpers: Defaecography has helped us to


understand that functional disorders of defaecation
occur during straining and therefore cannot be
detected by static tests that show anatomical
abnormalities only. It has been of great value in
diagnosis and assessing different types of treatment. However, after obtaining a better understanding of these disorders we realised that other
types of test would provide a more objective
assessment and would be easier to perform. Thus,
we now put a higher value on electromyography
in diagnosing the spastic pelvic floor syndrome. It
is a direct and simple test to demonstrate pelvic
floor activity during the different actions. It is also
much less confusing than measuring the anorectal
angle, which may be difficult and unreliable due
to the curved rectal configurations.
We have also started to perform digital rectal
investigation while the patient is straining, sometimes even in the squatting position. Rectoceles
and perineal herniations can thus easily be palpated. However, diagnosis of intussusception by
palpation is difficult as this requires considerable
experience and may be missed easily. We therefore consider defaecography an indispensable
supplement when palpation is negative.

Dr. Kodner: The results of proctography influence


treatment in patients who have symptoms consistent with internal intussusception of the rectum
or pelvic floor outlet obstruction. We offer fixation of the rectum to the sacral promontory to
patients with very symptomatic internal intussusception, proven by psychological evaluation not
to have a primary psychiatric disorder, and not
having severe irritable bowel syndrome. This is
our standard operation for both internal intussusception and prolapse. The patient with pelvic
floor outlet obstruction, on the other hand, will
have similar symptoms and will certainly not
benefit from this surgical procedure. We would
not consider surgical correction of internal intussusception without documentation by proctog-

85
Dr. Mahieu: The results of defaecography determine the choice between medical or surgical
treatment.
a) Mucosal prolapse is usually treated with satisfactory results by elastic ligature. External prolapse and intra-anal intussusception are not
always detected by clinical a n d / o r endoscopic
examination; defaecography is much more sensitive [10]. These conditions, when radiologically
proven, can be treated surgically (Orr-Loygue
rectopexy).
It is difficult to make the diagnosis of intrarectal full-thickness intussusception without
defaecography. Once made we prefer medical
treatment (diet, prevention of excessive straining).
b) Dyskinetic puborectalis sling. Medical treatment (kinesitherapy) is preferred.
b) Descending perineum syndrome. We have no
great experience of postanal repair and have
used biofeedback and kinesitherapy.
d) Incontinence. We would perform a postanal
repair for idiopathic incontinence and direct
sphincter repair in post-traumatic incontinence.
e) Solitary ulcer syndrome of the rectum. We
have operated by rectopexy only on those patients
presenting with external prolapse and intra-anal
rectal intussusception. The operation is usually
followed by rapid healing of the ulcer after 2 to 3
months. Intrarectal intussusception is not yet
proven to be an indication for surgery.
Professor Stevenson and Dr. Shorvon: We have
learned a great deal about the normal and abnormal appearances of defaecation, but the application of this knowledge to treatment is in its
infancy. The finding of impaired relaxation of
puborectalis is being experimentally treated with
biofeedback methods of retraining but we do not
yet have reportable results. When sphincter and
puborectalis tone are impaired but not absent in
patients with incontinence, biofeedback techniques
are also tried. Large rectoceles are usually obvious clinically and small ones are normal. Enteroceles have been found that were clinically
unsuspected as a cause of obstructed defaecation.
One result of our normal study is that intrarectal
intussusception is a normal event (at least seen on
defaecography) and should not be considered as a
reason for surgical treatment unless at least of
grade 5 or more.

Mr. Womack: Non-integrated proctography is a


simple, easily performed diagnostic procedure

that should be widely available to surgeons dealing with anorectal conditions. It can demonstrate
lesions which, although clinically occult, are the
cause of m u c h discomfort to the patient. Its main
influence on treatment must, therefore, be to
improve diagnosis and aid selection of the correct
treatment for the patient. A further role is the
reinvestigation of patients after treatment. This
provides the opportunity to determine if the treatment has achieved its intended object and allows
appropriate refinement of the treatment regime if
this is found to be necessary.
Integrated pressure - E M G proctography is a
more complex and time-con~suming procedure
that is best suited to centres with a specialist
interest. It provides more detailed information
about the pathophysiology of disease entities,
leading to a greater knowledge of a condition and
its aetiology. It is, therefore, more than a simple
diagnostic procedure. In addition to the contributions to patients' management referred to
above it is thought that a better understanding of
the causes of, and interrelationships between, the
conditions studied may allow earlier diagnosis
and treatment at a stage in the aetiology before
irreversible changes in the pelvic floor and anal
sphincter musculature have become severe.

Moderator Mr. Finlay: It is of interest that all the


contributors would proceed to rectopexy when
they found unequivocal evidence of intussusception and rectal prolapse. It is clear, however, that
rectopexy is not invariably successful in improving these patients. As referred to by Dr. Bartram
the operation will fail if the prolapse is associated
with delayed evacuation. Videoproctography,
however, did have a role in predicting those patients for w h o m the operation might be successful.
It is clear that the role of surgery for the other
clinical entities has not been determined. Several
centres have now followed Dr. Kuijpers in the use
of biofeedback and we await with interest further
experience.
Dr. Kodner made an extremely important
point in counselling against haemorrhoidectomy
for those patients with perineal descent. Certainly,
these patients have eversion of the anorectal junction which can readily be interpreted by the
unwary as prolapsing haemorrhoids. Not only
will haemorrhoidectomy fail to improve their
symptoms but it may make a proportion of these
patients incontinent.

86
How useful has proctography been in the study
of the pathophysiology of particular conditions?
Mr. Bartolo: Proctography has been particularly
useful in elucidating the pathophysiology in patients with incontinence. Perineal descent and the
anorectal angle can be measured together with
detecting occult or overt rectal prolapse. As far as
the constipation and obstructed defaecation syndromes are concerned, we do not understand the
pathophysiology. Moreover, we do not know
whether the observed abnormalities on proctography are cause or effect. To elucidate these
disorders it is important to document abnormalities of structure and correlate them with function.
This allows an objective assessment before and
after surgical procedures. The 18 patients described above with obstructed defaecation and
rectal intussusception all had their anatomic
abnormalities corrected by abdominal rectopexy,
yet only four achieved a successful result. Clearly
the intussusception is unlikely to have been the
cause of the obstructive symptoms. We do not
know how commonly rectal intussusception
progresses to complete rectal prolapse. Longitudinal proctographic studies should indicate how
frequently this occurs.
When the puborectalis fails to relax and the
rectal contents are retained, one cannot necessarily infer an inappropriate reflex response, since
the patient may lack rectal awareness. Moreover
there may be no desire to defaecate, or embarrassment may prevent evacuation. Alternatively
the volume of contrast may be too small or fail to
stimulate rectal contraction. To try and elucidate
these factors we try to fill the rectum until
sensation is perceived. Where interpretation is
difficult, we use simultaneous electromyography
and manometry to improve the assessment of the
aetiology of outlet obstruction.
Although proctography has helped our understanding there remain great gaps in our comprehension of the pathophysiology of pelvic floor
disorders. In isolation, proctography makes a
small contribution, but together with other physiological tests we can establish global assessment
of the patient's defaecatory function. Careful
audit of such evaluations in relation to the
outcome of treatment regimens may in the long
term improve our knowledge of the pathophysiology.
Dr. Bartram: Evacuation proctography gives a
unique view of the configuration of the rectum

during evacuation that has allowed the diagnosis


of internal intussusception and particularly intraanal intussusception to be made. The relationship
between internal intussusception and prolapse has
already been established.
Constipation has proved an interesting field
for investigation. Proctography quantifies the rate
and completeness of evacuation to determine
those patients with a defaecatory disability. The
same applies to the solitary rectal ulcer syndrome.
Proctography has therefore provided both
structural and dynamic information as to the
pathophysiology of various conditions. This can
be quantified and may provide a simple noninvasive method, giving as much relevant information as other more invasive and time-consuming tests. Unique information is obtained
regarding structural lesions. In other respects it is
a research tool, to be compared with other tests,
and its role reassessed as the treatment and
understanding of pelvic floor disorders advances.

Dr. Fork and Dr. Ekberg: Even if no transition


between an internal intussusception and a flank
rectal prolapse has been observed, it can be
assumed that the similar radiologic appearance of
an intussusception and a small prolapse indicates
a close relation. Similarly, it is easy to imagine a
solitary rectal ulcer developing at the advancing
front of an intussusception which, on prolonged
straining, is lodged in the anal canal. Our patients
who complained of not being able to empty the
rectum are, almost without exception, in fact able
to evacuate the barium contrast paste given. However, this discrepancy can be explained in patients
with a persistent internal intussusception which,
most probably, will simulate an incomplete
emptying of the rectum and thus give the patient
the feeling of an obstacle.
Dr. Kodner: Proctography is a very important
component of the complete evaluation of pelvic
floor abnormalities. It should be used in conjunction with manometry, electromyography and
colonic transit studies to evaluate fully the
defaecatory mechanism. The spectrum of disease
is not yet clarified. I feel that patients being
considered for surgical correction should be investigated first in an institution which has the
ability to evaluate all aspects of the problem. We
will no longer operate for internal intussusception
unless the patient first completes a psychological
assessment. The problem of pelvic floor outlet

87
obstruction is treated with techniques of biofeedback described by Han Kuijpers.
If a patient is incontil~ent with internal intussusception or prolapse of the rectum the sphincter
and pudendal nerves are evaluated with manometry and electromyography. If the pudendal
nerves are intact continence will be restored after
fixation of the rectum. This has been documented
by manometric studies and proctography in
some cases to demonstrate continued fixation of
the rectum.

rectum. In the measurement of perineal descent


we now have precise data. The normal distance
between the pubococcygeal line and the anorectal
junction is less than 8.5 cm (pelvic floor position
at rest) [15], and the normal distance of descent of
the anorectal junction on straining (pelvic floor
descent at strain) is less than 3.5 cm [13, 15]. In
the case of the solitary ulcer syndrome, defaecography has revealed the aetiological role of the
functional abnormalities of rectal intussusception
and prolapse [22].

Dr. Kuijpers: Defaecography has greatly increased


our knowledge of the understanding of constipation and the solitary rectal ulcer syndrome. We
have demonstrated by using segmental colonic
transit studies that paradoxical contraction of the
pelvic floor muscle during straining causes functional outlet obstruction, i.e. the spastic pelvic
floor syndrome [16].
In another study in which we have performed
defaecography and segmental colonic transit
studies in 130 patients complaining of constipation, outlet obstruction due to abnormal pelvic
floor function was found in over 75% of patients.
We have treated 20 patients with defaecographic
outlet obstruction combined with various types of
delayed segmental transit by biofeedback, aimed
at re-learning to relax the pelvic floor during
straining [25]. Ninety per cent completely succeeded in regaining normal defaecation, which
confirms our conclusion that paradoxical pelvic
contraction may cause constipation.
Defaecographic studies in 39 patients with the
solitary ulcer syndrome revealed that over 95% of
patients had a functional disorder of defaecation
that caused an urge to strain. They had either
rectal intussusception or the spastic pelvic floor
syndrome [26]. Treatment of the disorder that was
present resulted in healing of the ulcer. We therefore concluded that the solitary ulcer syndrome
involves ulceration due to a mechanical factor
caused by straining as a result of some disorder of
defaecation of unknown cause.

Professor Stevenson and Dr. Shorvon: Clearly the


solitary rectal ulcer syndrome only develops in a
very few cases of intrarectal intussusception since
the latter is so common.
In patients with constipation, a combination of
proctography and transit studies with plastic
shapes should facilitate separation of impaired
defaecation from impaired colonic transit.
In obstructed defaecation, proctography can
distinguish a non-relaxing or paradoxically contracting puborectalis from the inability to relax
the sphincter as causes of outlet obstruction. It
can also distinguish enterocele from intussusception as the cause of mid-defaecation obstruction.
Incontinence appears from proctography to be
a major problem only when both puborectalis
and sphincter are damaged. This may occur following trauma, infection, radiotherapy or malignant disease. It also seems to occur as the end
result of straining when the basic problem is a
difficulty in initiating defaecation. Some normal
women have such a short anal canal as probably
to be at high risk of incontinence from minor
damage and it may be this group which is at most
risk from childbirth trauma. Proctography, taken
with the clinical history can often distinguish
these possibilities.
Proctography alone provides only a visual
record of events taking place during defaecation,
and it seems likely that further understanding of
the pathophysiology will require manometric,
electromyographic and proctographic data in
some of these patients. Proctography is potentially
more available than these other techniques as
every hospital will have a fluoroscopic suite.
Studies to relate the proctographic findings with
other physiological data are underway and necessary. Studies relating the pre- and post-operative
defaecography with clinical results are needed.

Dr. Mahieu: Defaecography has helped to classify


defaecation disorders in several clearly defined
functional categories including intussusception
and prolapse, rectocele, dyskinetic pelvic floor,
pelvic floor descent and faecal incontinence.
Two syndromes have been studied in more
detail, namely, the descending perineum syndrome and the syndrome of solitary ulcer of the

Mr. Womack: Integrated Pressure - EMG


proctography has proved extremely useful in the

88
Table 7. The increase in intrarectal pressure and change in anorectal angle associated with voiding and attempted voiding in constipated patients and control subjects
Increase in intrarectal
pressure on attempted
voiding (cm water)
Controls
Constipation
Voided
Failed to void

(n = 11)
(n = 16)
(n = 7)
(n = 9)

60 (50-140)
114 (30-225)"
120 (80-215)
100 (30-225)

Anorectal angle at rest and during


attempted voiding (degrees)
At rest

Strain

93 (86-108)
95 (86-120)
102 (92-120)
93 (86-110)

132 (120-145)
112 (92-120)
118 (108-138)
110 (92-114) b

Values are medians and range. "Significantlydifferent to controls,p < 0.01. b Significantlydifferent to "voided", p < 0.01

Table 8. The increase in intrarectal pressure with voiding in


solitary rectal ulcer syndrome (SRUS) patients and control
subjects

Increase in intra-rectal
pressure during voiding
(cm water)
Controls
SRUS
SRUS with mucosal
ulceration
SRUS without mucosal
ulceration

(n = 9)
(n = 18)

60 (50-140)
95 (60-210) a

(n= 11)

100(71-210) a

(n = 7)

65 (60-95) b

Values are median and range. " Significantly different from


controls, p < 0.02. b Significantly different from SRUS with ulceration,p < 0.01

study of the pathophysiology of several conditions.


a) Severe chronic constipation: A study of 16
patients with profound difficulty passing formed
stool [8] has demonstrated an abnormal increase in
external anal sphincter activity during voiding.
The patients consequently required higher intrarectal pressures to void than control subjects (Table 7). Inability to void was associated with failure
to widen the anorectal angle on straining.
b) Solitary rectal ulcer syndrome: A study of 18
patients with the solitary ulcer syndrome [11]
revealed a high incidence o f rectal intussusception
in this condition. Overactivity of the anal sphincter
during voiding contributed to a significantly
higher voiding pressure in patients with mucosal
ulceration than in patients with histological
changes of solitary ulcer syndrome but no mucosal ulceration and in control subjects (Table 8).
This led to the hypothesis that solitary rectal
ulceration results from a combination of a high
voiding pressure and rectal prolapse.

c) Idiopathic faecal incontinence: Rectal intussusception, two thirds of which were clinically occult,
was demonstrated in 59% of patients with idiopathic faecal incontinence. The intussusception
distended the anal canal and the resulting anteroposterior diameter correlated inversely ( R s =
-0.54, p < 0 . 0 0 1 ) with the basal anal canal pressure. This suggests anal canal distension m a y be
the cause of the internal sphincter damage that
has been previously demonstrated in this condition [27].
Moderator Mr. Finlay: It is apparent that we still
do not understand the pathophysiology of any o f
these conditions. M a n y of the contributors have
indicated that they believe these components to
be secondary features, often an as yet unidentified
primary event. In this respect it is of interest to
note from a recent report that 72% of patients
with obstructed defaecation attributed their symptoms to childbirth. A further 20% implicated a
hysterectomy in the onset o f symptoms [28]. It is
of particular interest that each clinical feature
appears to overlap, suggesting an interrelationship perhaps between all o f these events. As one
might expect proctography appears to have raised
more questions than it has provided answers. A
foundation however has been laid upon which we
might build in terms of defining the pathophysiology of these pelvic floor disorders, followed by the
assessment of various modes of treatment.

References

1. Bartram CI, Turnbull GK, Lennard-Jones JE (in press)


Evacuation proctography: an investigation of rectal expulsion in 20 subjects with defecatory disturbance. Gastrointestinal Radiol
2. Kuijpers JHC, Strijk SP (1984) Diagnosis of disturbances
of continence and defecation. Dis Colon Rectum 27:
658-662

89
3. Mahieu P, Pringot J, Vanheuverzwyn R, Goncette L (1981)
Les prolapsus du rectum. Apport du lavement baryt6 et de
la d&rcographie. Acta Gastroenterol Belg 44:502-512
4. Mahieu P (1983) La drfrcographie. Description d'une
technique simiplifire et apport diagnostique. Ann
Gastroentrrol Hrpatol 19:345-350
5. Mahieu P, Pringot J, Bodart P (1984) Defecography: I.
Description of a new procedure and results in normal
patients. Gastrointest Radiol 9:247-251
6. Bartram C, Mahieu P (1985) Radiology of the pelvic floor.
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pelvic floor. Butterworths, London, pp 151-186
7. Mahieu P (in press) La drfrcographie. Technique
d'imagerie de la drfrcation et de ses drsordres fonctionnels. Encycl Mrd-Chir (Paris)
8. Womack NR, Williams NS, Holmfield JHM, Morrison
JFB, Simpkins KC (1985) New method for the dynamic
assessment of anorectal function in constipation. Br J Surg
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11. Womack NR, Williams NS, Holmfield JHM, Morrison
JFB (1987) Pressure and prolapse - the cause of solitary
rectal ulceration. Gut 28:1228-1233
12. Womack NR, Williams NS, Holmfield JHM, Morrison
JFB (1987) Anorectal function in the solitary rectal ulcer
syndrome. Dis Colon Rectum 30:319-323
13. Bartram CI, Turnbull GK, Lennard-Jones JE (1987)
Evacuation proctography: an investigation of rectal expulsion in 20 subjects without defecatory disturbance.
Gastrointestinal Radiol 13:72- 80
14. Shorvon PJ, McHugh S, Somers S, Stevenson GW (1987)
Defaecography findings in young healthy volunteers. Gut
28:A1361-1362
15. Mahieu P (in press) Defecography: a radiological method
for evaluation of anorectal disorders. In: Margulis AR,
Burhenne HJ (eds) Alimentary tract roentgenology. CV
Mosby, St. Louis
16. Kuijpers JHC, Bleijenberg G, de Morree H (1986) The
spastic pelvic floor syndrome. Large bowel outlet obstruction caused by pelvic floor dysfunction: a radiological
study. Int J Colorect Dis 1:44-48
17. Kuijpers JHC, Bleijenberg G (1985) The spastic pelvic
floor syndrome. A cause of constipation. Dis Colon
Rectum 28:669- 672
18. Mahieu P, Bartram CI (1985) Apport de la radiographie
l'rtude des troubles de la drfrcation. Acta Gastroenterol
Belg 48:11-20
19. Nicholls RJ, Simson JNL (1986) Anteroposterior
rectopexy in the treatment of solitary rectal ulcer syndrome without overt rectal prolapse. Br J Surg 73:
222-226
20. Turnbull GK, Lennard-Jones JE, Bartram CI (1986)
Failure of rectal expulsion as a cause of constipation: why
fibre and laxatives sometimes fail. Lancet ii:767-769
21. Turnbull GK, Bartram CI, Lennard-Jones JE (in press)
Radiological studies of rectal evacuation in adults with
idiopathic constipation. Dis Colon Rectum

22. Mahieu P (1986) Barium enema and defaecography in the


diagnosis and evaluation of the solitary rectal ulcer syndrome. Int J Colorect Dis 1:85-90
23. Finlay IG, Bartram CI, Nicholls RJ (1987) Can videoproctography and anorectal physiology predict outcome
after rectopexy for Solitary Rectal Ulcer Syndrome
(SRUS)? Gut 28:A1361
24. Kohda E, Fujioka M, Ikawa H, Yokoyama J (1985) Congenital anorectal anomaly: CT evaluation. Radiology 157:
349-352
25. Bleijenberg G, Kuijpers JHC (1987) Biofeedback treatment for constipation: First results. Dis Colon Rectum
30:108-111
26. Kuijpers JI-IC, Schreve R, ten Cate Hoedemakers G (1986)
Diagnosis of disorders of continence causing the solitary
rectal ulcer syndrome. Dis Colon Rectum 29:126-129
27. Womack NR, Morrison JFB, Williams NS (1986) The role
of pelvic floor denervation in the aetiology of idiopathic
faecal incontinence. Br J Surg 73:404-407
28. Brown DC, Rodder J, Poon F, Finaly IG (in press)
Outward obstruction constipation or failure of the posterior pelvic floor? Gut

Addresses of participants
Mr. D. C. C. Bartolo, MS, FRCS, Department of Surgery
Bristol Royal Infirmary, Bristol BS 2 8HW, UK
Dr. C. I. Bartram, Department of Radiology, St. Mark's
Hospital, City Road, London EC1V 2PS, UK
Dr. O. Ekberg (jointly with Dr. Fork), Department of
Diagnostic Radiology, University of Lund, Malmo General
Hospital, S-214 01 Malmo, Sweden
Dr. F.-T. Fork, Department of Diagnostic Radiology, University of Lund, Malmo General Hospital, S-214 01 Malmo,
Sweden
Dr. I. Kodner, The Jewish Hospital of St. Louis, 216 South
Kingshighway Boulevard, P.O. Box 14109, St. Louis, Mo,
63178, USA
Dr. J. H. C. Kuijpers, Katholieke Universiteit Nijmegen, Sint
Radboudziekenhuis, Algemene Chirurgie, Geert Grooteplein zuid 14, NL-6500 HB Nijmegen, The Netherlands
Dr. P. H. G. Mahieu, Service de Radiologie, Institut Chirurgical de Bruxelles, Universite Catholique de Louvain, Square
Marie-Louise 59, B-1040 Bruxelles, Belgium
Dr. P. J. Shorvon (jointly with Professor Stevenson), Department of Radiology, Central Middlesex Hospital, Acton
Lane, Park Royal, London NW10 7NS, UK
Professor G. W. Stevenson, Chairman, Department of Radiology, McMaster University, 1200 Main Street West,
Hamilton, Ontario L8N 3Z5, Canada
Mr. N. Womack, The London Hospital Medical College,
Surgical Unit, The London Hospital, Whitechapel, London
E1 1BB, UK

Address of moderator
Mr. I. G. Finlay, Consultant Surgeon Glasgow Royal Infirmary, Glasgow G4 0SF, Scotland, UK

Col6['eclal
Disease

Int J Colorect Dis (1988) 3:90-95

9 Springer-Verlag 1988

Original articles
Sympathetic nervous influence on the internal anal sphincter
and rectum in man
A. Carlstedt ~, S. Nordgren ~, S. Fasth ~, L. Appelgren 2 and L. Hult~n
1Department of Surgery and 2 Department of Anaesthesiology, University of G6teborg, G6teborg, Sweden

Abstract. The effect of sympathetic nerve block


and efferent stimulation of the sympathetic nerves
on anorectal motility was studied in 21 patients
undergoing operation for rectal carcinoma. Anal
pressure and rectal volume were simultaneously
recorded before and after epidural anaesthesia
and during nerve stimulation. Efferent electrical
stimulation of the presacral hypogastric nerves
(HGN) elicited a contraction of the internal anal
sphincter (IAS) in 13 out of 15 patients. The
contraction was preceded by a relaxation in seven
patients. In the rectum stimulation of the HGN
caused variable responses. A weak contraction
was the most frequent response. Efferent stimulation of the periarterial lumbar colonic nerves
(LCN) elicited a clear-cut contraction of the IAS,
while rectal motor responses were only occasionally observed. Epidural anaesthesia encompassing the thoraco-lumbar region (EDA), when
used to block the sympathetic discharge to the
IAS and the rectum, caused a reduction of anal
pressure (28_+ 11%) and an increased rectal tone.
The results imply that the human IAS receives a
sympathetic excitatory innervation via both the
HGN and the LCN. Furthermore, it appears that
the HGN convey inhibitory fibres to the IAS. The
rectal responses to EDA and sympathetic nerve
stimulation also indicate the presence of both
excitatory and inhibitory neurones in the sympathetic nerve supply to the rectum in man.
The extrinsic sympathetic nervous control of the
rectum and the internal anal sphincter (IAS) has
been extensively studied in the experimental
animal. There is strong evidence for an excitatory
influence exerted by fibres in the sympathetic
hypogastric or presacral nerves (HGN) [1-4] although inhibitory responses have been reported

[1]. High spinal anaesthesia in man, which blocks


the sympathetic outflow to the paravertebral
ganglia, causes a reduction of anal pressure [5].
The effect of efferent sympathetic nerve stimulation on anal pressure in man is still controversial.
Rankin and Learmonth in 1930 [6] reported a
strong anal contraction on stimulation of the
HGN in one patient, whereas Shephard and
Wright [7] and Lubowski et al. [8] both demonstrated anal relaxation in response to HGN
stimulation. The periarterial nerve fibres, accompanying the inferior mesenteric artery, form
the lumbar colonic nerves (LCN) and convey
excitatory fibres to the IAS in the experimental
animal [1, 4, 9, 10]. Whether, and if so to what
extent, the human IAS is also controlled by the
LCN is unknown.
Stimulation of the HGN and the LCN elicits
both excitatory and inhibitory rectal motility
effects in various experimental animals [4, 11, 12].
Although there is pharmacological evidence for
the existence of excitatory alpha- and inhibitory
beta-adrenergic receptors in the distal colon and
rectum in man [13, 14], little is known about the
extrinsic sympathetic nervous control of the
human rectum.
The purpose of the present investigation was
to study the functional organization of the
sympathetic nervous control of the IAS and the
rectum in man by studying the effects of blockade
of the thoraco-lumbar sympathetic outflow and
the effects of graded efferent electrical stimulation
of both the HGN and the LCN.
Patients and methods
Patients
Twenty-one patients undergoing operation for cancer of the
proximal two thirds of the rectum were studied. Mean age at

91

operation was 67 years (range 49-82 years). Informed consent


was obtained from all patients. The study was approved by the
Ethical Committee, University of Gtteborg.

i::

Lt

HGN

Anaesthesia and operative procedures


Preoperative bowel preparation was performed by whole gut
irrigation and multiple enemas. Pethidine (25 mg i.m.) was
given as premedication, whereas atropine was withheld as
premedication and during anaesthesia. General anaesthesia
was induced with thiopental (4 mg x kg -1). Complete muscle
relaxation was achieved by the use of succinyl choline (8 m g
rain -1 i.v.). Anaesthesia was maintained with nitrous oxide
and oxygen (70/30) and repeated doses of 0.1 mg fentanyl i.v.
In eight patients an epidural catheter was inserted preoperatively for subsequent administration of epidural anaesthesia
(2% mepivacaine, 10 ml) of the thoraco-lumbar region aimed at
a level of Th 8-L 4. No anaesthetic agent was given in the
catheter prior to operation. The level of the anaesthesia was
assessed by testing ventral dermatomes for sensitivity of pain
and touch postoperatively.
All operations were performed with the patients in the
Trendelenburg lithotomy position. The abdomen was opened
through a midline incision. The HGN (the presacral nerves)
were identified and dissected free for subsequent stimulation
at the sacral promontory. The LCN (the periarterial nerve
fibres along the inferior mesenteric artery) were dissected
free at the intended level of vascular ligature and divided
(Fig. 1).

Motility recordings
Rectal motility was studied by means of a volume recording
device. A polyethylene bag, 12 cm long, and wide enough to
prevent complete expansion at maximal rectal relaxation, was
mounted on an 18 Ch polyethylene tube introduced via the
anus and placed in the lower part of the rectum. The polyethylene tube was connected to an air-reservoir. The pressure
in the rectal balloon was kept at 20 cm water by means of a
water-reservoir draining into the air-reservoir. The water-

~/~.. ~

Fig. 1. Schematic illustration showing the sympathetic innervation of the rectum and the internal anal sphincter. Abbreviations: HGN, hypogastric (presacral) nerves; LCN, lumbar colonic nerves

reservoir was Suspended on a weight recorder (Grass Force


Displacement Transducer FT 10 C) operating a Grass polygraph model 7 D. Displacement of air into the rectal balloon
was recorded as weight change of the water-reservoir.
Anal pressure was measured using a 32 mm long waterfilled cuff (Malincrodt Endo-Tracheal Tube no 7) positioned in
the anus with its distal end at the anal verge. The tubing from
the cuff was connected to a pressure transducer (P 23 AD)
operating the polygraph. For details see Fasth et al. [15].

75
Anal pressure

50

(mmHg)
25
0
Rectal volume

50

(ml)

100
150
i|

EDA

Fig. 2. The effect of epidural anaesthesia (EDA) on anal pressure and


rectal volume. Note that EDA
caused a fall in anal pressure and increased rectal tone

(Mepivacaine,2%, lOml)

Time (min),
0

10

15

20

92
Anal pressure
mmHg
80

ml
200

60

150

40

100

20

50

Rectal volume

Nerve stimulations
Stimulation of the HGN was accomphshed by use of a hookelectrode on intact nerves or Unilaterally after nerve division.
The distal cut ends of the LCN were put on silver ring
electrodes for subsequent electrical stimulation.
Unidirectional square wave pulses were delivered from a
Grass stimulator, model S 5 E. Stimulation frequency was 5 or
10 Hz corresponding to the upper range of the physiological
discharge rates in postganglionic nerves. Voltage was kept at
8-20 V. The stimulation threshold of these nerve fibres was
determined by varying the pulse duration between 0.5 and
l0 ms.

Results

EDA

EDA

Fig. 3. Anal pressure and rectal volume before and 15 min after EDA in eight patients

Anal pressure
ImmHg)

100]

"]

"~-~'-

- -

50

Resting conditions
Anal pressure (n = 15) as r e c o r d e d u n d e r general
anaesthesia a n d m u s c l e relaxation was 5 2 +
13 m m H g ( m e a n + SD). The IAS exhibited spontaneous r h y t h m i c contractions at a f r e q u e n c y o f
8 - 1 0 / m i n , s u p e r i m p o s e d on ultra slow waves
( 0 . 5 - 1 / m i n ) . Rectal v o l u m e varied c o n s i d e r a b l y
b e t w e e n the patients. M e a n v o l u m e was 8 7 +
23 m l ( m e a n + SD). S p o n t a n e o u s motility in the
r e c t u m was generally absent.

Rectal
at 20(ml)cmVOlUmeH20 500 t

The effect of epidural anaesthesia (EDA )


100
0.5ms

HGN stim. (5Hz,8V)


Time (min)

5ms

a i

-J--,

Fig. 4. The effect of HGN stimulation on anal pressure and

rectal volume. Note absence of response on stimulation with a


short pulse duration. This type of response was observed in six
patients

Anal pressure

100]

Effects of nerve stimulation

(mmHg)
50
Rectal volume
(ml)

HGN. Efferent electrical stimulation o f the H G N

60 -]
80 1

100
(5ms, 10V)
~

HGN stim. (5Hz)


Time (min)

The effect o f E D A , which was studied in eight


patients, caused an a n a l pressure decrease in all
subjects. The effect was g r a d u a l in onset and
m a x i m a l within 1 5 - 2 0 m i n after the injection
(Fig. 2). The m e a n r e d u c t i o n o f anal pressure was
28% (range 11-40%), (Fig. 3).
There was in all patients a c o n c o m i t a n t
increase in rectal tone, as reflected b y a v o l u m e
decrease o f the rectal b a l l o o n (Figs. 2 a n d 3) and
at the s a m e time a phasic m o t o r activity ( 3 4 / m i n ) was observed.

( 10ms,20V)

J ,

~ ,

Fig. 5. The effect of HGN stimulation on anal pressure and


rectal volume. Note initial anal relaxation on high intensity
stimulation. This type of response was observed in seven patients. Also note rectal contraction in response to HGN stimulation

with a pulse d u r a t i o n exceeding 1 ms elicited an


anal contraction in 13 o f 15 patients. The contraction was i m m e d i a t e in onset a n d r e a c h e d a
m a x i m u m within 15 s (Fig. 4). In seven patients
the contraction was p r e c e d e d b y a relaxation
which varied c o n s i d e r a b l y as regards duration
a n d m a g n i t u d e . The initial relaxation a p p e a r e d to
be elicited at higher s t i m u l a t i o n intensity t h a n the
contraction (Figs. 5 a n d 6). A p u r e l y relaxatory
response was o b s e r v e d in one patient, whereas no
response was n o t e d in o n e case. H G N stimulation
evoked a rectal c o n t r a c t i o n in six patients (Fig. 5),
whereas a r e l a x a t o r y r e s p o n s e was o b s e r v e d in

93

Anal

pressure

(mmHg)

8ot

Discussion

6O

401

Rectal

volume

(ml)

50

-"N,,,j_..~---~

100
5Hz,O.5ms, IOV lOHz, lOms,20V
stim.

HGN

Time,(min)

Fig. 6. Effect o f H G N s t i m u l a t i o n in one p a t i e n t with a pred o m i n a n t anal relaxation o n h i g h intensity stimulation. In this
case H G N also elicited a w e a k rectal relaxation

three (Fig. 6). In the remaining six patients no


effects could be seen. The motor responses were
generally weak.
LCN. Efferent electrical stimulation of the LCN
with a pulse duration exceeding 1 ms caused an
anal contraction in seven out of ten patients
(Fig. 7), the contraction being less pronounced
compared to that elicited by stimulation of the
HGN using the same stimulation parameters. In
two patients the anal pressure increase persisted
after cessation of stimulation and returned to
prestimulatory level after 3 and 5 minutes. Biphasic or inhibitory responses of the IAS to LCN
stimulation were not recorded.
LCN stimulation elicited a weak rectal contraction in three experiments and no response in
seven cases.

Anal

The functional importance of autonomic n e r v e


fibres is signified by the effects obtained when
these nerves are blocked and when they are
electrically stimulated. The results of the present
study clearly demonstrate that anal pressure in
patients under general anaesthesia and muscle
relaxation is significantly reduced by epidural
anaesthesia. These findings which are in agreement with Frenckner and Ihre [5], who reported a
profound anal pressure reduction on high spinal
anaesthesia, imply that there is a tonic excitatory
discharge to the IAS in the thoraco-lumbar
sympathetic outflow in man. In vivo experiments
in human volunteers [16] and in vitro studies on
sphincteric muscle [17-19] demonstrating an excitatory effect by noradrenaline on the IAS indicate an excitatory influence on the IAS
mediated by alpha-adrenergic receptors.
Epidural anaesthesia increased rectal tone,
implying that there is also a tonic sympathetic
discharge to the h u m a n rectum. This is in contrast
to the findings of Frenckner and Ihre [5] who
could not observe any changes in rectal pressure
after high spinal anaesthesia. This discrepancy
may be explained by the different recording techniques or more selective blockade of the thoracolumbar segments by EDA compared to a high
spinal anaesthesia, which also blocks the parasympathetic sacral outflow. It is also in contrast to
animal studies, in which sectioning of the sympathetic innervation to the rectum caused a predominant rectal relaxation [4, 12].
In the majority of patients efferent stimulation
of the HGN elicited a contraction of the IAS
often preceded by a transient initial relaxation,

pressure

(mmHg)

so

25

Rectal

volume

(ml)

70t

120

170-t
LCN

stim.

Time

(rain)

5Hz,5ms,8V

IOHz, l O m s , 2 0 V

. . . .

Fig. 7. T h e effect o f L C N s t i m u lation on a n a l p r e s s u r e a n d rectal


volume

94
which is in accordance with previous animal
observations [1-4, 10, 11]. Reports on the effects
of HGN stimulation in man are sparse and
contradictory. While Rankin and Learmonth [6]
reported an anal contraction, studies by Shephard
and Wright [7] and more recently by Lubowski
et al. [8] showed that HGN stimulation invariably
caused a relaxation of the IAS. A possible explanation for the variation in results may be that
the stimulation parameters used both by Shepard
and Wright [7] and Lubowski etal. [8] were
subthreshold (pulse duration 0.5-1 ms). Moreover, due to the short-lasting stimulations used in
both investigations (3-30 s), the sphincter contraction often occurring after a preceding relaxation might have been overlooked.
As mentioned above it is likely that the anal
contraction on HGN-stimulation is mediated
through an alpha-adrenergic transmission. The
pathways and receptors involved in the intitial
relaxation on HGN stimulation in the present
experiments cannot be determined in an in vivo
study in man. Direct activation of inhibitory betaadrenergic receptors on the IAS may be one
explanation for this effect as suggested by Lubowski et al. [8]. This is supported by in vitro
experiments on h u m a n sphincteric muscle, which
have revealed the presence of beta-receptors on
the IAS [17-19]. Furthermore, there is pharmacological evidence, in vivo, of an inhibitory betaadrenergic influence on human IAS [16]. Secondly
antidromic activation of afferent fibres in the
HGN may cause a relaxation of the IAS via
activation of sacral spinal reflexes. Such reflexes
have been described by Langley and Andersson
[1]. A third possible mechanism may be a release
from adrenergic nerve terminals of a second
neurotransmitter with inhibitory action. It has
thus been suggested that ATP may be released
from sympathetic nerves, modulating the effect of
noradrenaline [20].
Unlike the colon, in which the sympathetic
innervation is mainly inhibitory [21], recent
studies [12] have revealed an excitatory alphaadrenergic innervation to the rectum in the cat. In
our experiments efferent stimulation of the HGN
elicited rectal contractions (sphincter-like effect)
in some experiments and relaxation (colon-like
effect) in others. The HGN thus seems to exert a
dual effect on the rectum, which has not been
previously shown in man.
Most previous investigations on the extrinsic
innervation of the IAS show that the motor
supply to the sphincter is provided by sympathetic fibres in the HGN, although reports from

animal experiments have revealed a sympathetic


outflow to the IAS in the LCN as well [1, 4, 9, 10].
In the present experiments, stimulation of the
LCN elicited a contraction of the 1AS, which has
not been previously demonstrated in man. Unlike
the IAS response to HGN stimulation, no inhibitory effects were noted on stimulation of the
LCN.
It is concluded from the present investigation
that the human IAS receives a tonic excitatory
input both from the HGN and the LCN, and that
inhibitory neurons may be mediated by the
HGN. The sympathetic nerves exerted a dual
effect on rectal motility. These findings may be of
importance for the understanding of the normal
mechanisms for preserving anal continence.

Acknowledgements. This investigation was

supported by grants
from the Swedish Medical Research Council (17 X-03117),
from the University of GOteborg, from Gtteborgs L~tkaresallskap and from Assar Gabrielsson's Fund.

References
1. Langley JN, Anderson HK (1895) On the innervation of
the pelvic and adjoining viscera. J Physiol 18:67-105
2. Garrett JR, Howard ER, Jones W (1974) The internal anal
sphincter in the cat: a study of nervous mechanisms
affecting tone and reflex activity. J Physio1243:153-166
3. Bouvier M, Gonella J (1981) Nervous control of the
internal anal sphincter of the cat. J Physiol 310:457-469
4. Carlstedt A, Fasth S, Hulttn L, Nordgren S (in press) The
sympathetic innervation of the internal anal sphincter and
rectum in the cat. Acta Chir Scand
5. Frenckner B, Ihre T (1976) Influence of autonomic nerves
on the internal anal sphincter in man. Gut 17:306-312
6. Rankin FW, Learmonth JR (1930) Section of the sympathetic nerves of the distal part of the colon and rectum
in the treatment of Hirschsprung's disease and certain
types of constipation. Ann Surg 92:710-720
7. Shepard J, Wright PG (1968) The response of the internal
anal sphincter in man to stimulation of the presacral
nerve. Am J Dig Dis 13:421-427
8. Lubowski DZ, Nicholls RJ, Swash M, Jordan MJ (1987)
Neural control of internal anal sphincter function. Br J
Surg 74:668-670
9. Learmonth JR, Markowitz J (1929) Studies on the function
of the lumbar sympathetic outflow. Am J Physiol 89:
686-691
10. Mizutani M, Nakayama S (1986) Role of lumbar colonic
nerves on internal anal sphincter motility in dogs. Ital J
Gastroenterol 18:134-139
11. Rayner V (1979) Characteristics of the internal anal
sphincter and the rectum of the vervet monkey. J Physiol
286:383-399
12. Hedlund H, Fasth S, Hulttn L (1984) Efferent sympathetic
nervous control of rectal motility in the cat. Acta Physiol
Scand 121:317-324
13. Lyren~is E, Abrahamson H, Dotewall G (1985) Effects of
beta-adrenoceptor stimulation on recto-sigmoid motility in
man. Dig Dis Sci 6:536-540

95
14. Gagnon DJ, Devroede G, Belisle S (1972) Excitatory
effects of adrenaline upon isolated preparations of human
colon. Gut 13:654-657
15. Fasth S, Hult6n L, Nordgren S, Akervall S, Oresland T (in
press) Manovolumetry - a new method for investigation of
anorectal function. Gut
16. Gutierrez JG, Shah AN (1975) Autonomic control of the
internal anal sphincter in man. In: Van Trappen G (ed)
Fifth International Symposium of Gastrointestinal
Motility. Typoff Press, pp 363-373
17. Parks AG, Fishlock DJ, Cameron JDH, May H (1969)
Preliminary investigation of the pharmacology of the
human internal anal sphincter. Gut 10:674-677
18. Friedmann CA (1968) The action of nicotine and catecholamines on the human internal anal sphincter. Am J Dig
Dis 13:428-431

19. Burleigh DE, D'Mello A, Parks AG (1979) Responses of


isolated human internal anal sphincter to drugs and
electrical field stimulation. Gastroenterology 77:484-490
20. Burnstock G (1976) Do some nerve cells release more than
one transmitter? Neuroscience 1:239-248
21. Hult6n L (1969) Extrinsic nervous control of colonic
motility and blood flow. Acta Physiol Scand [Suppl] 335:
1-116
Accepted: 22 December 1987
Dr. Anders Carlstedt
Department of Surgery
Sahlgrenska sjukhuset
S-413 45 G6teborg
Sweden

Coloi'ectal
Disease
9 Springer-Verlag 1988

Int J Colorect Dis (1988) 3: 96-101

The functional results after colectomy and ileorectal anastomosis


for severe constipation (Arbuthnot Lane's disease) as related
to rectal sensory function
S. Akervall, S. Fasth, S. Nordgren, T. Oresland and L. Hult6n
Department of Surgery, Sahlgren's Hospital, University of G6teborg, G/3teborg, Sweden

Abstract. Rectoanal
manovolumetry
during
graded isobaric rectal distension was carried out
in 12 w o m e n with severe constipation classified as
slow transit constipation (Arbuthnot Lane's disease).
The resting anal sphincter pressure, the rectoanal
inhibitory reflex and the rectal capacity were all
normal. While the distension volumes required to
elicit sensation of rectal filling a n d an urge to
defaecate were within normal limits in all patients
the distension pressures required to elicit such
sensations fell outside the 95% limits of variation
of control subjects in 4 patients. All patients were
subsequently subjected to colectomy and ileorectal anastomosis. Patients with normal rectal
sensory function had a satisfactory functional
result after colectomy, whereas the four patients
with blunted sensation did not improve. These
findings suggest that rectoanal m a n o v o l u m e t r y
with determination of the distension pressures
required to elicit rectal sensation is an important
preoperative measure to be used in patients with
severe constipation for selection of patients suitable for colectomy and ileorectal anastomosis.

dominal distension, nausea and abdominal pain


often aggravated by excessive doses of stimulant
laxatives a n d / o r enemas [8, 9, 10]. Although most
patients can be m a n a g e d by dietary manipulation
and judicious use of laxatives there is a group of
patients which is unresponsive to conservative
measures and to which the condition causes so
much distress that surgical treatment has to be
considered.
Different surgical procedures such as partial
colectomy and colectomy with caecorectostomy
have been e m p l o y e d but have often been unsuccessful [7, 11]. Colectomy with ileorectal
anastomosis appears to offer the best possibility of
benefit although the outcome in some cases even
after this procedure is not satisfactory and the
functional results unpredictable [4, 6, 7, 10]. The
aim of the present study was to investigate anorectal function in a series of patients suffering
from this condition in an attempt to determine
whether patients with a poor result after colectomy and ileorectal anastomosis might exhibit
specific abnormalities as c o m p a r e d to those with
a successful functional outcome.

A condition characterized by severe constipation


which is unrelated to outlet obstruction, Hirschsprung's disease or idiopathic megacolon, is sometimes caused by a motility disorder associated
with a distinctive abnormality of the myenteric
plexus of the colon to which chronic abuse of
stimulant laxatives m a y have contributed [1, 2].
The condition, almost exclusively seen in women,
is referred to as slow transit constipation [3],
functional constipation [4], colonic inertia [5],
idiopathic constipation [6] and Arbuthnot Lane's
disease [7]. The most striking symptom is the "no
urge" type of constipation combined with ab-

Patients and methods


The study comprises 12 consecutive female patients (mean age
39.0 years, range 26-62 years) treated between January 1980June 1986. The onset of constipation was in childhood or early
adolescence in all except three patients (Table 1). All patients
suffered from totally obstinate constipation. None of them
experienced a normal call to stool and abdominal distension,
nausea and abdominal pain were often troublesome symptoms. Seven patients had previously undergone resectional
surgery, four with colectomy and caecorectostomy and two of
these patients (cases 1 and 10) had also had an obliteration of
the rectovaginal pouch (Moschkowitz operation). Function
failed to improve in all these patients, however.
Metabolic and endocrine disorders known to cause constipation had been ruled out by careful investigation in a

97
rectoanal
reflex inhibition
50

Weight transducer
(Rectal

volume)

Pressure transducer

<

(Anal pressure)

E_

200

~ E

1OOi

rectal c o n t r a c t i o n

~n
i

Distension pressure
(5-80cm

H20)

i
4s

initial volume

~nal prooe

60s
final volume

Rectal distension

Fig. 1. A Schematic illustration of the method used for anorectal manovolumetry, and B a recording from a normal subject. The
pre-set distension pressure and the corresponding volume in the balloon recorded at 4 s (initial volume) were used to determine
sensory thresholds. For further details see Methods

gastroenterology unit. Perineal descent, rectocoele, anterior


wall prolapse, rectal intussusception and solitary ulcer were
excluded by inspection of the perineum during straining on a
commode and by anoscopy and sigmoidoscopy. When in
doubt an evacuation proctogram was performed. A barium
enema was performed to rule out megacolon and organic
causes of constipation. The recto-sphincteric inhibitory reflex
was present in all cases excluding Hirschsprung's disease.
Bowel transit studies, performed in 6 patients were above the
normal range as defined by Abrahamsson et al. [12] in all.

Rectoanal manovolumetry
Rectal volume, rectal sensation, anal pressure and rectoanal
reflex inhibition were studied by a technique allowing simultaneous recording of rectal volume and anal pressure in
response to graded isobaric rectal distension [13]. The rectoanal manovolumetry device illustrated in Fig. 1A, consists of
two main units: (1) an adjustable reservoir system reflecting
rectal volume which also effects rectal distension by means of
a high compliance balloon inflated with constant pre-set
pressures, (2) a unit for anal pressure recording. The investigation was performed as series of distensions with 5 cm water
increments from 5 cm water to 80 cm water and the sensory
thresholds for sensation of rectal filling and appreciation of
urge for defaecation were assessed, see Fig. 1. The threshold
distension pressure and rectal volume for eliciting rectoanal
reflex inhibition was also determined. A rectal contraction was
defined as the occurrence of a shortlasting decrease of rectal
volume following the initial rapid volume expansion at a
distension pressure of 25 cm water. Rectal capacity was defined as the volume in the balloon recorded at a pressure of
40 cm water exerted for 60 s. (Final volume at 40 cm water,
60 s = rectal capacity, Fig. 1 B).
Results of the studies were compared with 24 matched
control subjects, all women (mean age 39.8, range 25-63
years) with normal bowel function and without a history of
anorectal disease. The statistical significance of data compared
in this study was evaluated using the Wilcoxon rank test for
unpaired data and Fischer's exact test. Whenever data were
positively skewed log-transformation was performed to obtain
the 95% limits of variation. The study was approved by the
Ethical Committee of the University of G6teborg.

Operative procedures
Abdominal pain, bloating and nausea were dominating symptoms in two patients. To confirm that these symptoms also
were related to the colonic disorder a diverting loop ileostomy
was performed as a first stage operation. Both patients became
free of symptoms during a 4 and 12 months period, respectively, and a colectomy with ileorectal anastomosis was subsequently performed. Eight patients had a colectomy and ileorectal anastomosis performed as a one-stage procedure. In two
patients the operation was done in two stages, a diverting loop
ileostomy being closed 10 weeks later. The ileorectal anastomosis was in all cases constructed at the level of the promontory.

Postoperative complications
One patient had an anastomotic leakage with a pelvic abscess
which resolved on conservative treatment. Four patients were
laparotomized for small bowel obstruction caused by adhesions and an extensive small bowel resection had to be
performed in one of these patients.

Follow up
All patients have been followed up in the out-patient clinic on
a regular basis. Mean length of the follow-up was 3.4 years,
range 12 months to 6 years.

Results

Outcome of surgery
D e t a i l s o f t h e c l i n i c a l r e s u l t s a p p e a r i n T a b l e 1.
E i g h t o f t h e 12 p a t i e n t s s t a t e d t h a t t h e y h a d r e l i e f
from their symptoms
and from constipation
having daily evacuations without need of laxatives o r e n e m a . T h e s t o o l f r e q u e n c y , r a n g i n g f r o m

98
Table 1. Details of patients treated by colectomy and ileorectal anastomosis for severe constipation
Case

Age at
onset

Age at
operation

Previous problems
or operation

Preoperative
bowel habits

Postoperative
bowel habits

Length of
follow-up
years

Subsequent problems
or operations

30

53

Moschkowitz operation;
colectomy (CRA)

Enema

Unchanged

SBO laparatomy x 3
with division of
adhesions

Childhood

36

Sigmoid resection;
colectomy (CRA)

Enema

Unchanged

SBO laboratomy with


division of adhesions;
continent ileostomy

40

58

Enema

3/day; retarding drugs

SBO laparatomy with


division of adhesions

Childhood

26

Colectomy (CRA)

1-2/2 weeks
laxatives

1/day

Puberty

31

Ovarian cystectomy;
hysterectomy;
sigmoid resection

Enema

4-6/day

Puberty

50

Cholecystectomy;
colectomy (CRA)

1/week
laxatives

Unchanged

Continent ileostomy

25

29

Anorexia nervosa;
endogenous depression;
gastropexy (volvulus)

Enema

1/day for
6 months;
enema after
rectopexy

Abdominal rectopexy
for complete rectal
prolapse; SBO with
100 cm jejunal
resection

Puber~

26

Sigmoid resection;
Caecopexy

Enema

2-3/day

Intermittent anal
pain; anal stretch x 3

Childhood

39

1/2 weeks
laxatives

1/day

10

Puber~

27

Moschkowitz operation;
left-sided hemicolectomy

Enema

Unchanged

11

Childhood

31

I/2 weeks
laxatives

1-3/day

12

Childhood

62

Enema

3-4/day

Awaiting ileostomy

CRA, Caecorectal anastomosis; SBO, small bowel obstruction

Table 2. Results of anorectal manovolumetry in women with severe constipation and normal controls
Constipation (n = 12)
Resting anal sphincter pressure
(mm Hg)
Thresholds for rectoanal
reflex inhibition

Distension pressure (cm water)


Distending volume (ml)

Rectal capacity (ml)


First sensation of rectal
filling

Distension pressure (cm water)


Distending volume (ml)

First sensation of urge


to defaecate

Distension pressure (water)


Distending volume (ml)

Controls (n = 24)

62.1 --_ 3.9 (40-80)

55.6_+ 1.9 (42-75)

n.s.

15.0_+ 1.2 (10-20)


83.3_+ 14.8 (35-175)

12.9__+ 0.8 (10-20)


63.0_+ 4.1 (22-102)

n.s.
n.s.

233.8__+39.7 (175-310)

232.3__+ 9.4 (158-370)

n.s.

23.3__+ 4.3 (5-50)


96.6_+15.9(35-175)

12.7___ 0.9 (5-25)


63.1+ 7.5(12-135)

p < 0.05
n.s.

47.1+ 6.9(10-80)
170.0_+ 18.7 (90-275)

27.1__+ 1.9(15-60)
117.8_ 11.0 (24-292)

p < 0.01
n.s.

All results expressed as means + SEM (range). Statistical analysis by the Wilcoxon rank test for unpaired data

99

1 to 6/day at the latest follow up, remained


virtually unchanged throughout the follow up
except in one patient. This woman (case 7) who
had a normal preoperative evacuation proctogram had 1-2 motions/day for 6 months when
she developed a complete rectal prolapse. Abdominal rectopexy with an anterior Marlex mesh
restored the anatomical defect but function remained impaired and the patient became dependent on enema and laxatives for defecation. In
four patients (cases 1, 2, 6 and 10), all previously
operated with colonic resections and two of them
also with obliteration of the rectovaginal pouch,
constipation with abdominal distension, nausea
and abdominal pain persisted. Two of these four
patients have had a continent ileostomy subsequently with complete relief of symptoms and
another patient is awaiting such a conversion.

Rectoanal manovolumetry

300.

250.

200.

9
150 9

100 -

50.

,o

,'~

,o

;~

3o

3'5

,;o

5o

Distension pressure, cm H 2 0

Fig. 2. Clinical outcome of colectomy and ileorectal anastomosis as related to first sensation of rectal filling. The shaded
area shows the 95% interval of variation for normal women.
Note that the four patients who did not improve had a markedly blunted sensation

300,
m
250

As shown in Table 2 there were no statistically


significant differences between constipated patients and controls, neither in resting anal pressure nor as regards the lowest rectal distension
pressure and distending volume required to elicit
rectoanal reflex inhibition. All patients fell within
the range of the normal. Rectal capacity was
similar in patients and controls and none of the
patients fell outside the range of the controls.
All patients as well as the controls perceived a
sensation of filling of the rectum at lower distension pressure than that required to elicit a sensation of urge but the thresholds for the two
modalities of sensory function were significantly
higher in the patients. In contrast no significant
differences were found between the distension
volumes that elicited first sensation of filling and
an urge to defaecate, although there was a tendency to higher volumes in the constipated patients. A rectal contraction occurred in 17/24 of
the normal subjects, whereas only 3/12 of the
patients showed such a response (p < 0.05).

200

150

100

50

20

40

60

80

Distension pressure, c m H20

Fig. 3. Clinical outcome of colectomy and ileorectal anastomosis as related to threshold of urge to defaecate. Shaded area
95% interval of variation for control subjects.Note that the distension pressures are increased in patients who turned out to
be failures
tion of filling in the four patients who did not
improve after colectomy. Moreover, a considerably higher distension pressure was required to
elicit a sensation of urge to defaecate in these
patients than in the controls whereas patients with
satisfactory postoperative function fell within the
95 % limits of variation of the controls (Fig. 3).

Correlation between manovolumetric findings


and outcome of surgery
Discussion

As is shown in Fig. 2 the threshold pressure and


volume which elicited first sensation of rectal
filling were within the 95% limits of variation for
control subjects in those patients who had a
successful outcome. In contrast a markedly higher
distension pressure was required to elicit a sensa-

Severe idiopathic slow transit constipation is a


complex disorder almost entirely confined to
women. Evidence has been provided that patients
suffering from this disease have a disordered
motility in other parts of the gastrointestinal tract

100
and it has been suggested that the constipation is
a manifestation of a systemic disease [5]. Nevertheless, patients often suffer from constipation
and abdominal symptoms to such an extent that
surgical intervention is considered justified. The
present study shows evidence that the assessment
of rectal sensory function might be of predictive
value for the selection of patients who may
benefit from colectomy and ileorectal anastomosis
which appears to be the common operation
employed for the condition.
The resting anal pressure in the constipated
patients did not differ from controls. This is in
keeping with a recent report by Roe et al. [10] on
patients with slow transit constipation but contradictory to other studies on similar patients where
both raised pressures [5] and low pressures [14, 15]
have been reported. The reason for the conflicting
results is obscure especially so as the patients in
these series appear to be rather homogenous. In
accordance with other reports [10, 14] the
threshold volumes required to elicit recto-anal
reflex inhibition were within normal limits indicating that the intramural neurones involved in
this response [16] are intact in patients with slow
transit constipation. The reflex rectal contraction
following distension was observed less often in
constipated patients than in controls. A decreased
rectal motility on distension was also noted by
Read et al. [14] in a substantial number of constipated patients. These findings might suggest a
motility disorder in the rectum that contributes to
the constipation by preventing an efficient
squeezing of rectal contents towards the anal
canal.
It has been shown by Hurst [17] that balloondistension of the rectum causes a sensation that is
interpreted as a desire to pass wind or motion,
contrasting to the vague abdominal sensation of
discomfort or pain felt at distension of the colon.
In four of the patients the distension pressure
required to elicit rectal sensation was significantly
higher than in the controls both as regards the
sensation of filling and the urge to defaecate. In
contrast the threshold volumes associated with
perception of rectal sensation did not differ from
those recorded in the controls. This observation is
in keeping with other reports [10, 14] suggesting
that rectal sensation as assessed by the volume at
which rectal filling is first appreciated is not
significantly affected in patients with slow transit
colon. In contrast the report by Baldi et al. [18]
states that a larger volume than normal was
required to evoke initial awareness of rectal filling. Read et al. [14] presented evidence that in

contrast to the sensation of filling the sensation of


desire to defaecate was blunted in many of the
constipated patients and therefore these authors
suggested that the sensory pathway for the desire
to defaecate is distinctly different from other
rectal sensations. However, in the present study
patients with a blunted sensation of filling,
perhaps representing inability to appreciate gas,
also had a blunted sensation of urge to defaecate.
It has not been established precisely where the
nerve endings which transmit sensation from the
rectum are situated, i.e. whether they are located
in the muscularis [17] or in the rectal mucosa [19]
or both or whether part of the sensation may in
fact depend on extramural structures in the pelvis
[20]. The observation that patients in whom the
colon has been brought down into the pelvis to
restore continuity after sphincter saving resections
of the rectum often acquire a sort of rectal sensation lends support to the latter hypothesis [21].
Regardless of the localization of the receptors it
appears that a substantial proportion of patients
with severe constipation of colonic origin have
sensory abnormalities which can be demonstrated
by using graded isobaric rectal distension but
which can be overlooked if only the distending
volume is recorded.
There is no consensus regarding the option of
surgical treatment of severe constipation but in
patients with slow transit constipation most
authors advocate total colectomy and ileorectal
anastomosis, [4, 6, 7, 10]. However, it appears
from the few published series of cases and the
present study that the outcome is far from satisfactory in all patients. Thus Hughes et al. [4] who
treated 10 women with the "no urge" type of
constipation with colectomy and ileorectal anastomosis had to perform a permanent ileostomy
subsequently in two patients for "severe rectal
inertia".
The results of the present study indicate that
the functional outcome of total colectomy and
ileorectal anastomosis is markedly influenced by
the sensory function of the rectum. Thus patients
with a normal sensation of rectal filling and
normal urge to defaecate had a successful outcome, whereas four patients with a blunted sensation as assessed by graded isobaric rectal distension did not improve. Three of these failures had
previously had a colectomy and caecorectostomy
making it difficult to assess whether an ileorectal
anastomosis is a better option. However, one
woman with normal rectal sensation who did not
improve after colectomy and caecoproctostomy
had excellent function after conversion to an ileo-

101

rectal anastomosis, favouring this procedure as


the surgical option in patients with severe constipation and normal rectal sensory function.
Colectomy and ileorectal anastomosis is a
major surgical procedure associated with a high
postoperative morbidity [4, 7] and should therefore only be considered in greatly disabled patients where medical treatment has proved ineffective. Furthermore all patients should be
offered a careful investigation of rectal sensory
function, before the option of surgical treatment is
offered. Patients with normal rectal sensory function appear to have a good prospect of a satisfactory functional result after colectomy and ileorectal anastomosis whereas patients with blunted
sensation are probably better treated with an
ileostomy, preferably a continent one. Whether or
not a restorative proctocolectomy with construction of a pelvic pouch and ileoanal anastomosis
might be justified in these patients remains to be
shown.

8.
9.
10.
11.
12.

13.
14.
15.

Acknowledgement. The study was supported by grants from


the Medical Society of G6teborg, the University of GOteborg,
the Swedish Medical Research Council (MFR: 17X-03117)
and Assar Gabrielsson's Fund.

16.
17.

References
1. Smith B (1973) Pathological changes in the colon produced by anthraquinone purgatives. Dis Colon Rectum
16:455-458
2. Krishnamurthy S, Schuffier MD, Rohrmann CA, Popell
CE (1985) Severe idiopathic constipation is associated
with a distinctive abnormality of the colonic myenteric
plexus. Gastroenterology 88:26-34
3. Hinton JM, Lennard-Jones JE (1968) Constipation: definition and classification. Postgrad Med J 55:720-723
4. Hughes ESR, McDermott FT, Johnson WR, Polglase AL
(1981) Surgery for constipation. Aust NZ Surg 51 : 144-151
5. Watier A, Devroede G, Duvanceau A, Alderrahman M,
Dugnay C, Forand MC, T6treault L, Arhan P, Lamarche
J, Elhilali M (1983) Constipation with colonic inertia. A
manifestation of systemic disease? Dig Dis Sci 28:
1025-1033
6. Goligher JC (1984) Surgery of the anus, rectum and
colon, 5th edn. Balli6re - Tindall London, pp 335-345
7. Preston DM, Hawley PR, Lennard-Jones JE, Todd IP
(1984) Results of colectomy for severe idiopathic constipa-

18.

19.
20.
21.

tion in women (Arbuthnot Lane's disease). Br J Surg


71:547-552
Poisson J, Devroede G (1983) Severe chronic constipation
as a surgical problem. Surg Clin North Am 63:193-213
Preston DM, Lennard-Jones JE (1986) Severe chronic
constipation of young women: idiopathic slow transit
constipation. Gut 27:41-48
Roe AM, Bartolo DCC, Mortensen NJMcC (1986) ~
Diagnosis and surgical management of intractable constipation. Br J Surg 73:854-861
Fasth S, Hedlund H, Svaninger G, Oresland T, Hult6n L
(1983) Functional results after subtotal colectomy and
caecorectal anastomosis. Acta Chir Scand 149:623-627
Abrahamsson H, Antov S (1987) Gastrointestinal transit
time (GITI) in constipated patients evaluated by a single
abdominal radiogram. Scand J Gastroent 22 [Suppl 135]:
55
Akervall S, Fasth S, Hult6n L, Nordgren S, Oresland T
(in press) Rectoanal manovolumetry - a new method for
investigation of anorectal function. Gut
Read NW, Timms JM, Barfield LJ, Donnelly TC, Bannister JJ (1986) Impairment of defecation in young women
with severe constipation. Gastroenterology 90: 55- 60
Lanfranchi GA, Bazzocchi G, Campieri M, Brijnola C,
Fois F, Marzio L, Labo J (1984) Intestinal transit time is
related with different ano-rectal motility patterns in
chronic non-organic constipation. In: Ramon C (ed)
Gastrointestinal motility. MTP Press: Lancaster, pp
477-481
Penninckx FM, Mebis JH, Kerremans RP (1982) The
rectoanal reflex in cats analyzed in vitro. Scand J Gastroenterol 17 [Suppl 71]: 147-149
Hurst AF (1911) The sensibility of the alimentary canal.
Goalstonian Lectures. Frowde, London Oxford
Baldi F, Ferrarini F, Corinaldesi R, Balestra R, Cassan M,
Fenati GP, Barbara L (1982) Function of the internal anal
sphincter and rectal sensitivity in idiopathic constipation.
Digestion 24:14-22
Garry RC (1933) Responses to stimulation of the caudal
end of the large bowel in the cat. J Physiol 78:208
Lane RHS, Parks AG (1977) Function of the anal
sphincters following colo-anal anastomosis. Br J Surg 64:
596-599
Goligher JC, Hughes ESR (1951) Sensibility of the rectum
and colon, its role in the mechanism of anal incontinence.
Lancet 1:543-548

Accepted: 20 January 1988


S. Fasth, Associate Professor
Department of Surgery
Sahlgrenska sjukhuset
S-413 45 G6teborg
Sweden

Colol'eetal
Disease

Int J Colorect Dis (1988) 3: 102-108'

9 Springer-Verlag 1988

Changes in small intestinal epithelial expression of MHC Class II


antigen after terminal ileal resection for Crohn's disease
K. Geboes, P. Rutgeerts, F. Penninckx, V. Desmet, and G. Vantrappen
Department of Medical Research, Laboratory of Histochemistry and Cytochemistry, Department of Gastroenterological Surgery,
University Hospital St. Rafa~l, Leuven, Belgium

Abstract. Aphthous lesions in the neoterminal


ileum from patients operated for Crohn's disease
are an early sign of recurrence that can be
identified during ileocolonoscopy. The origin of
these lesions was studied in nine patients treated
by terminal ileal resection and right hemicolectomy for complicated Crohn's disease. During
surgery the neoterminal ileum was turned inside
out, the mucosa was carefully inspected and two
large mucosal biopsies were obtained. The same
procedure was carried out in seven patients
operated for other diseases. Four to six months
after surgery endoscopy of the neoterminal ileum
was carried out and multiple biopsies were obtained from the neoterminal ileum. Another follow-up colonoscopy with biopsies was carried out
one year after the operation. The operative specimens and the per- and postoperative biopsies
were submitted to routine microscopy and immuno- and enzyme-histochemistry. None of the
Crohn's patients had macroscopic lesions in the
neoterminal ileum at operation and only one had
microscopic signs of inflammation and a positive
section margin. Four-six months after operation all Crohn's patients had active aphthous
lesions in a 5-20 cm segment of the neoterminal
ileum at endoscopy. Biopsies taken at this time
showed microscopic features which were not observed in biopsies from control subjects: an increase of HLA-DR +, ATPase + dendritic cells in
the ileal mucosa and a defective expression of
MHC class II antigens by the small intestinal
epithelial cells. MHC class II expression by the
small intestinal epithelial cells returned towards
normal after one year. The lesions observed in the
early postoperative biopsies indicate that an early
local temporary dysfunction of the immunologic

system may be important in the pathogenesis of


anastomotic recurrence in Crohn's disease.

Recurrence after surgical treatment for Crohn's


disease is well recognised [1, 2]. It ranges from a
few per cent to 100% in various published reports
[2]. In an endoscopic and histological study carried out in 114 patients, treated by "curative"
resection, we found that endoscopic and microscopic signs of inflammation were present in the
neoterminal ileum in 72% of the patients examined within one year after operation [3]. These
findings were later confirmed [4]. It is not clear
whether these lesions result from an exacerbation
of a pre-existing inflammatory lesion, or from a
more generalized intestinal disease, or if they are
"de novo" lesions. Recrudescence cannot be excluded although various studies dealing with the
effect of resection margin histology on recurrence
rate suggest on balance minimal correlation [5,6, 7].
The present study was performed in order: (1)
to see if the lesions observed at endoscopy early
after operation could be explained by the presence of pre-existing inflammation within the
ileum or colon at the time of the operation; and
(2) to study immunologic phenomena as they
occur in the tissue in biopsies obtained at operation and postoperatively in the neoterminal
ileum.
For this purpose we examined the expression
of MHC class II antigens by intestinal epithelial
and lamina propria cells, as well as the composition of the dendritic and lymphocytic cell populations within the lamina propria in biopsies from
patients with Crohn's disease and in control
patients.

103

Methods

Results

Patients

Macroscopic observations

Nine patients (6 females, 3 males) with established Crohn's


disease (mean age 37 years - 29-45) underwent terminal ileal
resection and right hemicolectomy for ileal stenosis (n = 7) or
for ileal stenosis with internal fistulae (n = 2). During surgery
the neoterminal ileum was everted, the mucosa was carefully
examined and two large mucosal biopsies were taken 4 cm
proximal to the anastomosis. The same procedure was followed in seven patients operated for other conditions (ileal
adenocarcinoma (1), abdominal trauma (3), colonic carcinoma
(2) and ileal perforation due to a solitary ulcer (1)).

N o n e o f the patients with C r o h n ' s disease a n d


n o n e o f the control patients h a d m a c r o s c o p i c a l l y
identifiable lesions in the ileal s e g m e n t used as
n e o t e r m i n a l i l e u m d u r i n g the o p e r a t i o n .
At e n d o s c o p y 4 - 6 m o n t h s after the o p e r a t i o n ,
a p h t h o u s lesions w e r e f o u n d in a 5 - 2 0 c m long
s e g m e n t o f the n e o t e r m i n a l i l e u m in all patients
with C r o h n ' s disease a n d in n o n e o f the control
patients. The chronicity o f these lesions was conf i n n e d b y a second follow-up e n d o s c o p y , 10
m o n t h s postoperatively.

Four to six months after surgery, colonoscopy with ileoscopy was performed in all patients and controls. The neoterminal ileum was carefully examined over 30 cm and multiple biopsies were obtained 4 cm above the anastomosis, in
the area where the intraoperative biopsies had been taken.
The biopsies were obtained from normal-appearing mucosa as
well as from lesions. Ileocolonoscopy with biopsy was repeated
six months later. All patients gave informed consent for the
various procedures.

Pathological studies
The operative specimens and the per- and postoperative
biopsies were submitted to routine microscopy, enzyme histochemistry and immunohistochemistry. Routine microscopy
(H.E. staining) on Bouin fixed, paraffin embedded semiserial
sections was performed for diagnostic purposes and for the
assessment of the presence and the extent of microscopic
inflammation. Enzyme histochemistry involved the staining of
6 Nn cryostat sections of freshly frozen tissue specimens for
acid phosphatase (ACP) and adenosine triphosphatase (ATP)
according to a modified metal salt method [8, 9]. This
technique was used to distinguish further between various
types of dendritic cells involved in the inflammation. Immunohistochemistry was performed on serial frozen sections using
an indirect immunoperoxidase method. Six gm thick sections
of the freshly frozen biopsies were dried overnight at -20 ~
and fixed in acetone for 30 min at room temperature. Serial
sections were incubated for 30 rain with the following monoclonal antibodies:
OKT3 (CD code CD3) reactive with T ceils; OKT8 (CDs)
defining cortical thymocytes and probably cytotoxic/suppressor T cells; OKT4-Leu 3 a (CD,) defining helper/inducer Tcells; HLA-DR reacting with the common framework of
human MHC class II antigens; B1 (CD2o) reacting with all Bcells; and Leu7 for natural killer cells. The monoclonal
antibodies were obtained from Ortho Pharmaceutical Co.,
Raritan, NJ, USA (OKTJOKTs/OKT4),from Becton-Dickinson, San Francisco, Ca (Leu-7, Leu-3a and HLA-DR) and
from Coulter Immunology, Hialeah, F 1a (B0.
For the immunohistochemical
bound (S) immunoglobulins on
cytoplasmic (C) immunoglobulins
embedded sections, an unlabeled
(PAP) procedure was performed
clonal antibodies to human IgA,
Copenhagen, Denmark).

demonstration of surfacecryostat sections and of


on Bouin fixed paraffin
peroxidase-antiperoxidase
using monospecific, polyIgM, IgG (Dakopatts a/s

Microscopic observations
Routine microscopy. R o u t i n e m i c r o s c o p i c e x a m ination o f the o p e r a t i v e s p e c i m e n s c o n f i r m e d the
diagnosis o f C r o h n ' s disease in all nine cases
o p e r a t e d for this disease. Ileal a n d colonic resection m a r g i n s r e v e a l e d no signs o f m i c r o s c o p i c
i n f l a m m a t i o n in eight o f these nine cases. In one
patient, i n f l a m m a t o r y lesions were p r e s e n t at the
ileal resection m a r g i n .
The biopsies o b t a i n e d d u r i n g the o p e r a t i o n in
the ileal s e g m e n t left behind, were n o r m a l in
eight o f these nine patients. Microscopic signs o f
i n f l a m m a t i o n (i.e. a n increased cellular infiltrate
in the l a m i n a p r o p r i a c o m p o s e d o f p o l y m o r p h s
a n d l y m p h o c y t e s ) w e r e p r e s e n t in the biopsies o f
one patient. This was the s a m e p a t i e n t in w h o m
the ileal resection m a r g i n s h o w e d an i n f l a m m a t o r y reaction.
No i n f l a m m a t o r y lesions consistent with
C r o h n ' s disease were f o u n d in the o p e r a t i v e
specimens f r o m the control patients. All the intrao p e r a t i v e ileal biopsies f r o m these patients w e r e
normal.
All biopsies o b t a i n e d d u r i n g the follow-up
endoscopies in p a t i e n t s with C r o h n ' s disease
showed u n e q u i v o c a l m i c r o s c o p i c signs o f i n f l a m m a t i o n i.e. b l u n t i n g a n d irregularity o f the villi,
superficial m u c o s a l defects, a n d a focal i n f l a m m a tion o f the l a m i n a p r o p r i a (3). Similar lesions
were not o b s e r v e d in the biopsies f r o m the control
patients.

Immunohistochemistry
A positive staining for H L A - D R or M H C class II
antigens was o b s e r v e d o n small intestinal epi-

104

Fig. 1. Early postoperative biopsy from a patient with Crohn's disease. MHC class II antigens are not expressed by the epithelial
cells (e), and the cellular infiltrate in the lamina propria (Lp) is minimal ( x 200)
Fig. 2. Microphotograph of small intestinal biopsy showing epithelial cells and lamina propria cells. Magnification x 200. Stained
for MHC class II antigens. This is a biopsy from a patient with postoperative recurrence of Crohn's disease obtained during a second follow-up ileoscopy. MHC class II is expressed by the epithelial cells (arrows) as well as by the lamina propria cells. The central
lacteal is dilated. Its endothelial lining is negative for MHC class II (arrowhead)
Fig. 3. a Intraoperative biopsy from a patient with Crohn's disease stained for OKT4. The villus shows a normal configuration and
the number of lamina propria lymphocytes (L+ arrows) is normal (x200). b Intraoperative biopsy from a patient with Crohn's
disease stained for OKTs. Intraepithelial lymphocytes are clearly visible (arrows)

105
thelial cells, on capillary endothelial cells from the
lamina propria and the submucosa and on numerous round and irregularly shaped inflammatory
cells of the lamina propria in the intraoperative
biopsies from the patients with Crohn's disease.
Similar findings were obtained in the biopsies
from the control patients. The positively staining
irregular cells were mainly present in the villi in a
subepithelial position.
The endoscopic biopsies obtained from patients with Crohn's disease during follow-up colonoscopy 4 to 6 months after the operation
showed either no or only weak positive staining
for MHC class II antigens on the small intestinal
epithelial cells (Fig. 1). A clear and strong positive
epithelial staining pattern reappeared in the postoperative biopsies obtained one year after the
operation. The postoperative biopsies from the
control patients obtained at the same intervals
showed always a normal positive staining for
MHC class II on the epithelial cells. Endothelial
cells and lamina propria cells remained positive
for MHC class II in the postoperative biopsies
from the patients with Crohn's disease and from
the control patients (Fig. 2).
Intraepithelial lymphocytes were mainly
OKT8 +, HLA-DR negative cells in all biopsies.
Only rare OKT4 +, HLA-DR-intraepithelial lymphocytes were observed. No differences were seen
between the biopsies from patients with Crohn's
disease and from the controls.
Table 1. Lamina propria lymphocytes in Crohn's disease of
ileum
T,

m~

T,/T~

Intraoperative biopsies
19.8 4.3 16.7_+5.2 1.2_+0.4
Early postoperativebiopsies 21.5+4.6 18.7+5.0 1.1_+0.3
Late postoperativebiopsies 24.3___4.7 19.8+ 5.7 1.2_0.5
Lymphocytesare expressed as number of cells per 100 lamina
propria cells (+ SEM)

Lamina propria lymphocytes were BI+B lymphocytes as well as OKT~+T lymphocytes and
Leu-7 + natural killer cells in all biopsies.
Few B1 stained lymphocytes were present,
except in areas adjacent to or in lymphoid aggregates. No differences were observed between
the various groups of biopsies. Leu-7 + cells were
also rarely observed.
OKT4 +, Leu-3a + and OKT8 + lamina propria
lymphocytes were present in all intraoperative
and postoperative biopsies. The absolute number
of these cells expressed as number of cells per 100
lamina propria cells was increased in the early
and late postoperative biopsies from patients with
Crohn's disease when compared with the controls
(Fig. 3). But the OKT4/OKT8 ratio remained
unchanged (see Table 1).
An increase of immunoglobulin-containing
plasma cells was observed mainly in the postoperative biopsies from the patients with Crohn's
disease. The relative number of IgA, IgM and
IgG-containing cells expressed as a percentage
per 500 lamina propria cells remained unchanged
except for a relative increase of IgM-containing
cells. Surface immunoglobulin presenting cells
were rare except adjacent to or in lymphoid
follicles.

Enzyme histochemistry
HLA-DR positive irregular cells were observed
mainly in the lamina propria of the villi of the
ileal biopsies immediately underneath the epithelial basement membrane. Enzyme histochemistry
demonstrated that these cells formed a heterogeneous population composed of a mixture of
cells showing either strong membrane adenosine
triphosphatase (ATPase) activity but weak cytoplasmic acid phosphatase activity or strong ACP
activity but no detectable ATPase activity.

Table 2. Enzymehistochemistry
Results

Crohn's Disease

ATPase+cells
ACPase+cells

Controls

Intraoperative
biopsies

Postoperative
biopsies

Intraoperative Postoperative
biopsies
biopsies

25 4.2
15+_1.2

28 + 2.3
10_+2.3

12.5_+2.9
14 + 2.6

15 2.6
12 4.2

Positive lamina propria cells in the ileum expressedper 500 lamina propria cells (+ SEM). The biopsies of Crohn's patients contain
significantlymore HLA-DR+,ATPase+dendriticcells than the biopsies of normal controls(p < 0.001)

106

Fig. 4. Intraoperative biopsy from a patient with Crohn's disease stained for a acid phosphatase and b for ATPase showing the
presence &numerous ATPasepositive macrophageshigh in the lamina propria (arrows),and a positivebrush border staining

The positive cells were counted in the ileal


biopsies and expressed per 500 lamina propria
cells (see Table 2). From these countings it appears that ATPase + cells are more numerous in
biopsies of patients with Crohn's disease, whether
these biopsies are obtained during or after the
operation. The number of ACPase + cells is similar
in the biopsies from patients with Crohn's disease
and in the biopsies from the control patients
(Fig. 4).

Discussion

These findings suggest that the lesions observed


in the neoterminal ileum in patients with Crohn's
disease 4 to 6 months after surgery are not due to
the operation itself since they do not occur in
control patients. They could be the result of a
recrudescence of the disease, perhaps because of
stenosis, or the result of pre-existing lesions not
recognizable by routine, microscopy. The intraoperative and postoperative ileal biopsies from
patients with Crohn's disease show definite abnormalities, not present in the biopsies from the
control patients. The intraoperative ileal biopsies
from patients with Crohn's disease contain an
increased number of ATPase +, HLA-DR + irreg-

ular cells in a subepithelial position in the villi.


These cells are not easily identified on routine H.
and E. stained sections. Similar findings have
already been described in Crohn's disease of the
large intestine with immunohistochemistry [10]
and transmission electron microscopy [11].
The precise function of these irregular
ATPase +, HLA-DR + cells is not yet established.
They are probably involved in the inflammatory
process as antigen presenting cells and may play a
role in the interaction with and activation of T
lymphocytes [ 12].
Such a role has been demonstrated in inflammatory lesions such as Yersinia infections and
dermatoses [13, 14]. In Crohn's disease a predominance of T cells in areas of heavy lymphocytic infiltration [15] as well as a predominant
localization of the granulomas in the T cell area
in lymph nodes [16] have already been described.
All these observations point towards the involvement of T cells in the pathogenesis of Crohn's
disease, and the increase of the ATPase +, HLADR + cells might be the expression of an increased
antigen load. HLA-DR is normally expressed by
small intestinal epithelial cells. We found a positive epithelial staining pattern in the intraoperative biopsies from patients with Crohn's disease as
well as from controls. The positive staining for

107

HLA-DR is absent in the early postoperative


biopsies from patients with Crohn's disease but
reappears in the late postoperative biopsies. A
weakening or disappearance of HLA-DR expression by small intestinal epithelial cells has already
been reported in cow's milk protein intolerance
[17, 18] and in coeliac disease in children [18, 19,
20] and in Whipple's disease in adults [21]. Increased HLA-DR expression has been reported in
coeliac disease [17]. The significance of the HLADR expression by the small intestinal epithelial
cells is not clear [22, 23, 24, 25].
The temporary absence of expression of HLADR by intestinal epithelial cells from patients
with Crohn's disease, which we demonstrated,
may also be nonspecific. It can be the result of a
postoperative lack of cellular adaptation and immaturity, although we have not observed a similar
absence in the biopsies from our control patients.
But the temporary absence might also point
towards a temporary dysfunction of the intestinal
epithelial cells. This dysfunction could, if the
HLA-DR expression is immunologically important, predispose the gut wall to an increased
antigen load and hence to chronic inflammation.
A possible involvement of HLA-DR in Crohn's
disease has already been proposed theoretically
by Kirsner [26] and was also suggested because of
its strong expression by macrophages, capillary
endothelia and the intestinal epithelium in involved areas of the ileum and the colon [27]. Our
findings support this hypothesis. They indicate
that an early local immunological dysfunction
may be important in the pathogenesis of anastomotic recurrence in Crohn's disease. A strong
expression of HLA-DR by epithelial cells has
been found together with a decrease of OKT8 +
intraepithelial lymphocytes in diseased ileal mucosa [27]. We found no changes in the ratio of
helper (OKT4 +) cells to suppressor (OKT8 +) cells
in the lamina propria and no changes in the
number of intraepithelial lymphocytes. But the
number of cases we studied may be too small for
an evaluation of quantitative abnormalities of the
lymphocytes and is certainly not adequate for an
evaluation of their function.

11.

References

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i. Hellers G (1986) Prognostic factors to recurrence of


Crohn's disease. In: Rachmilewitz D (ed) Inflammatory
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2. Lindhagen T, Ekelund G, Leandoer L, Hildell J, LindstrOm C, Wenckert A (1983) Recurrence rate after surgical

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management of Crohn's disease. Influence of disease at
the margin of resection. Ann Surg 192:311-318
Heuman R, Boeryd B, Bolin T, Sj6dahl R (1983) The
influence of disease at the margin on the outcome of
Crohn's disease. Br J Surg 70:519-521
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and practice. Chicago University Press, Chicago, p 193
Barka T, Anderson PJ (1963) Histochemistry. Theory,
practice and bibliography. Evanston, London/Harper and
Row, New York
Selby WS, Poulter LW, Hobbs S, Jewell DP, Janossy G
(1983) Heterogeneity of HLA-DR positive histiocytes in
human intestinal lamina propria: a combined histochemical and immunohistological analysis. J Clin Pathol 36:
379-384
Thyberg J, Graf W, Klingenstrom P (1981) Intestinal fine
structure in Crohn's disease. Lysosomal inclusions in
epithelial cells and macrophages. Virchows Arch (Pathol
Anat) 39:141-152
Poulter LW, Janossy G (1985) The involvement of dendritic cells in chronic inflammatory disease. Scand J
Immunol 21: 401-407
Vuento R, Eskola J, Leino R, Viander M, Toivanen A
(1984) Role of Ia-positive cells in the lymphocyte responses to Yersinia. Scand J Immuno120:141-147
Wilders MM, Drexhage HA, Kokj6 M, Verspaget HW,
Meuwissen SGM (1984) Veiled cells in chronic idiopathic inflammatory bowel disease. Clin Exp Immunol 55:377-387
Meuwissen SGM, Feltkamp-Vroom TH, Brutal de la
Rivi6re A, Von dem Borne AEG Kr, Tytgat GNJ (1976)
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special reference to identification of lymphocyte-subpopulations. Gut 17: 770-780
Geboes K, Van den Oord J, De Wolf-Peeters C, Desmet V,
Rutgeerts P, Janssens J, Vantrappen G, Penninckx F,
Kerremans R (1986) The cellular composition of granulomas in mesenteric lymph nodes from patients with Crohn's
disease. Virchows Arch (Pathol Anat) 409:679-692
Arnaud-Battandier F, Cerf-Bensussan N, Amsellem R,
Schmitz J (1986) Increased HLA-DR expression by enterocytes in children with celiac disease. Gastroenterology
91:1206-1212
Geboes K, Tshibassu M, Eggermont E, Desmet V, Vantrappen G (1985) HLA-DR expression and lymphocytic
subsets in small bowel biopsies in coeliac disease and
cow's milk intolerance. Gastroenterology 88: 1391
Avigad S, Jonas A, Shiner M, Gazit E (1985) Ia-like
antigens in the small intestinal mucosa of normal and
celiac children. Isr J Med Sci 21:405-409
Sarles J, Gowel JP, Olive D, Maroux S, Mawer C, Giraud
F (1987) Subcellular localization of class I (A, B, C) and
class II (DR and DQ) MHC antigens in jejunal epithelium
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21. Geboes K, De Vos R, Rutgeerts P, Desmet V, Yantrappen
G (1987) Light microscopic and ultrastructural immunocytochemical study of Whipple's disease. Gastroenterology
92:1401
22. Scott H, Solheim BG, Brandtzaeg P, Thorsby E (1980)
HLA-DR like antigens in the epithelium of the human
small intestine. Scand J Immunol 12:77-82
23. Cerf-Bensussan N, Quaroni A, Kurnick JT, Bhan AK
(1984) Intraepithelial lymphocytes modulate la expression
by intestinal epithelial cells. J lmmunol 132:2244-2252
24. Unanue ER, Allen PM (1986) Comment on the finding of
Ia expression in nonlymphoid cells. Lab Invest 55: 123125
25. Brandtzaeg P, Baklien K (1977) Intestinal secretion of IgA
and IgM: a hypothetical model in immunology of the gut.
Ciba Foundation Symposium 46 (new series). Elsevier,
Excerpta Medica North-Holland, Amsterdam, Oxford,
New York, pp 77-108

26. Kirsner JB (1986) Observations on inflammatory bowel


disease - 1985: present status and future prospects. In:
Rachmilewitz D (ed) Inflammatory bowel diseases. Martinus Nijhoff Publishers, Dordrecht, Boston Lancaster,
pp 309-328
27. Hirata I, Berrebi G, Austin LL, Keren DF, Dobbins III
WO (1986) Immunohistological characterization of intraepithelial and lamina propria lymphocytes in control
ileum and colon and in inflammatory bowel disease. Dig
Dis Sci 31: 593-603
Accepted: 20 January 1988
Dr. K. Geboes
U.Z. St.-Rafa~l
Laboratorium voor Histo- en Cytochemie
Minderbroedersstraat 12
B-3000 Leuven
Belgium

Col6i'ec/al
Disease

Int J Colorect Dis (1988) 3:109-118

9 Springer-Verlag 1988

Anal epidermoid carcinoma: a population-based clinico-pathological


study of 164 patients
S. G o l d m a n 1, B. Glimelius 2, L. P ~ h l m a n 3, E. S t ~ h l e 3 and E. Wilander 4

1Department of Surgery, S6dersjukhuset, Stockholm and Departments of 2Ontology, 3Surgery and 4 Pathology,
University of Uppsala, Akademiska sjukhuset, Uppsala, Sweden

Abstract. The clinical and pathological features of


164 patients with anal epidermoid carcinoma
were investigated in a population-based study
between 1978 and 1984. Twenty-three tumours,
the majority of which were small and well differentiated squamous cell carcinomas, were situated in the perianal region. Twenty of these
patients are alive and disease-free. O f 141 tumours in the anal canal two-thirds were of the
cloacogenic type, i.e. displaying transitional cell
differentiation. The overall 5-year survival was
between 40 and 50% for both cloacogenic and
squamous cell carcinomas, respectively. However,
poorly differentiated squamous cell carcinomas
and cloacogenic carcinomas without any squamous cell differentiation (subtype A) h a d a more
aggressive course, especially in men, than the
other subgroups. Clinical stage also h a d an
impact on prognosis. Both stage, sex, degree of
differentiation and histologic subtypes revealed
independent prognostic information. Although
the primary aim of this study was not to evaluate
therapy, it was noted that patients primarily
treated with irradiation (with or without chemotherapy) had a more favourable course than
patients treated with surgery alone.

Epidermoid carcinoma of the anus is a rare


neoplasm. The natural history of the disease and
its proper treatment remain uncertain. Several
distinct t u m o u r types originating from the various
epithelial layers lining the anus have been described [1-3]. The relative frequency of these
histopathologically identified types has varied
considerably. It has also been debated whether
any form of subdivision, even descriptive, is of
clinical importance. Recent studies have, for example, suggested that the two major types, the

squamous cell carcinomas derived from the squamous epithelium and the so-called cloacogenic
carcinomas derived from a transitional epithelium
in the anal canal should be considered as a single
entity since they apparently behave in a similar
way clinically and their prognoses are identical
[4-9].
The purpose of the present study was to
compare the natural history of different histological types and gradings in relation to sex, age,
site, staging and survival in an unselected population-based series in order to assess the proportion
of the various subtypes and their clinical importance. A simplified pathological subclassification using clearly defined and easily identified
criteria was used.

Patients and m e t h o d s

Patients
In order to obtain an unselected and representative series,
data on all patients with diagnosed rectal and anal carcinomas
(International Classification of Diseases, ICD 8, No 154) who
were residents of the Swedish counties of Stockholm, Uppsala,
Kopparberg, V~istmanland and J~mtland (totally approximately 2.5 million inhabitants) between January 1978 and
December 1984 were gathered from: (1) the diagnostic files of
all surgical and oncological departments in the counties, and
(2) the Cancer Registries of the Uppsala and Stockholm health
care regions. In this way, 177 patients with a neoplasm in the
anus were identified. There were 166 patients with a tumour
of an epidermoid type, five were adenocarcinomas, four
malignant melanomas, one basal cell carcinoma and one
leiomyosarcoma. Of the 166 patients, two could not be
included in the study due to insufficient pathological material.

Histopathological evaluation
Microscopic material from all 164 patients was re-evaluated
by one experienced pathologist (EW) without knowledge of

110

111
the original classification, the clinical course or the location of
the tumour.
Formalin-fixed and paraffin-embedded blocks of all carcinomas were cut in 4 ~tm thin sections and stained with hematoxylin-eosin and/or van Gieson's stain and examined by light
microscopy. In most instances, multiple, well preserved
tumour areas were available. On the basis of their histological
pattern, the turnouts were classified into two types: squamous
(71 cases) or cloacogenic (basaloid, transitional cell, 93 cases)
carcinomas.
To secure a diagnosis of squamous carcinoma, the whole
tumour, including all individual tumour cells, had to display a
squamous differentiation. Most of these tumours, but not all,
contained areas with keratinization and pearl formation. All
squamous carcinomas were subgrouped as follows, [1] well
differentiated tumours in which all the turnout cells were
attached to each other and the borders between tumour tissue
and surrounding stroma were sharp and always evident, [2]
moderately differentiated tumours which displayed signs of
tumour cell dissociation and the borders between the tumour
aggregates and the stroma were less evident, and [3] poorly
differentiated tumours, which were identified by the ability of
the tumour cells to dissociate diffusely in the stroma tissue
(Figs. 1-3). Thus, the subgrouping of the squamous carcinomas was exclusively based on the degree of dissociation of the
turnout cells. Parameters such as atypia (cell polymorphism),
frequency of mitotic figures, presence of keratinization and
pearl formation and degree of lymphocytic infiltration in the
tumour stroma were not evaluated.
Tumours classified as cloacogenic carcinomas were
mainly built up of transitional epithelioid cells. They were
subgrouped as follows; grade I-tumours consisted of transitional epithelioid cells with an obvious and distinct cell
palisading in the periphery of the tumour aggregates. Grade
II-tumours were characterized by a partial, but not total, loss
of the peripheral cell palisading. Grade III-tumours were
identified by the total loss of peripheral cell palisading on the
tumour buds. Cloacogenic carcinomas disclosing no squamous
differentiation and thus composed entirely of transitional
epithelioid cells were classified as subtype A, and tumours with visible squamous differentiation, mostly with
signs of keratinization and pearl formation, were designed
subtype B (Figs. 4-6). The histopathological grading and subtyping of the cloacogenic carcinomas used in the present study
is regarded as a simplified modification of the Klotz et al.
histological classification of 1967 [2].

Tumour staging
Tumour size and localisation were prospectively evaluated for
all cases referred to Akademiska sjukhuset, Uppsala. The
same information was collected retrospectively from the diagnostic files of cases not referred to this hospital. The upper
limit of the anal canal was at the ano-rectal junction and the
border between the perianal region and the anal canal was at
the anal verge. The outer border of the perianal region was

6 cm from the anal verge. Tumours extending into both


regions were classified according to their predominant portion.
A few very large tumours in the retrospective part of the
material were considered as anal canal tumours, although a
"proper judgement of their origin" could not be made. This
classification was made prior to the results of the histopathological subclassification.
The tumour stage for both perianal and anal canal
tumours was based upon tumour size, where tumours less than
2 cm in diameter were designed T1, between 2-4 cm as T2
and above 4 cm as T3. Tumours invading other organs except
the rectum and skin were designated as T4, irrespective of
tumour size. This classification follows the classification proposed by Papillon [10] for tumours in the anal canal and the
UICC staging system [11] for perianal tumours. Lymph node
involvement and metastatic disease was as proposed by the
UICC.

Treatment
During the time period, the majority of the patients were
treated either at the Departments of Surgery and Oncology,
Akademiska sjukhuset, Uppsala, the Karolinska sjukhuset,
Stockholm or Srdersjukhuset, Stockholm, respectively. Except
in cases with a small, superficially located tumour, which was
excised locally, primary treatment was radiation, usually in
combination with chemotherapy (bleomycin [12], bleomycin
with vincristine or bleomycin with 5-fluoro-uracil with cyclophosphamide). In Stockholm during the first 3-4years,
surgery was then usually performed, whereas in Uppsala [12]
and in Stockholm during the last 1-2 years, surgery was only
performed in cases of insufficient response to radiation. Cases
not referred to these hospitals were treated in many different
ways. Some elderly patients as well as the single case identified at routine autopsy did not obtain any specific therapy.
Of the 23 patients with a perianal tumour, 12 (52%) were
treated with irradiation with or without chemotherapy alone,
one patient with irradiation with chemotherapy followed by a
rectal excision and nine patients with local excision. One 91
year old woman with inguinal node metastases was only
treated palliatively.
Of the 50 squamous cell carcinomas in the anal canal,
four (8%) patients were operated locally and six (12%) underwent a rectal excision. The majority (31 (62%) patients) were
treated with irradiation (with or without chemotherapy), and
19 of these did not have additional major surgery. Nine
patients were only treated palliatively or received no specific
therapy. Of 91 cloacogenic carcinomas, six (7%) were locally
operated, 16 (18%) patients underwent radical excision of the
rectum and 36 (39%) were irradiated, sometimes combined
with chemotherapy as their sole treatment. Twenty-three
(25%) patients received a combined therapy of irradiation with
or without chemotherapy followed by major surgery. Ten
(11%) patients received no therapy or only palliation because
of advanced age, disseminated disease and/or poor general
condition.

Figs. 1-3. Illustration of squamous cell carcinomas with various degrees of differentiation. 1 Well differentiated tumour with
regular sheets of tumour cells and sharp borders between tumour tissue and stroma component. 2 Moderately differentiated tumour
in which some single cells or small aggregates of turnout cells are diffusely spread in the stroma and 3 poorly differentiated tumour
with obvious signs of pronounced tumour cell disintegration. Hematoxylin-eosin stains x 160
Figs. 4-6. Picture of cloacogenic carcinomas with various morphology. 4 Grade I tumour built up of regular tumour aggregates
with distinct cell palisading. 5 Grade II tumour with partial but not total loss of the peripheral cell palisading and 6 Grade Ill
tumour with partly disintegrated tumour cells without identified cell palisading. Hematoxylin-eosin stains x 160

112
Statistical analysis

Sex and age distribution

The generation of the survival curves and the statistical


significance test (log rank test) were carried out according to
Peto et al. [13]. The multivariate analyses were performed
using the Cox proportional hazards model [14]. Unless otherwise indicated, the statistical significance level used for testing
the various hypotheses was p--0.05. Patients dying of intercurrent diseases are not included in the population at risk after
their death, provided they were in complete clinical remission;
if not, they were regarded as dying of anal carcinoma. All
patients were followed until January 1987, resulting in a
median follow-up of living patients of 65 months (range
25-107 months) with no difference between groups.

Perianal carcinomas were equally c o m m o n in


both sexes, whereas the female to male ratio was
about 3.5:1 among the anal canal carcinomas.
The female predominance was particularly pronounced in subtype IIB, where only two of 42
cases were male. In contrast, 17 of the 39 patients
in subtype IIA were male (Table 1). This difference is statistically significant (Z2=17.0, p <
0.001). The median age was between 67-69 years
(range 34 to 93 years) in all subtypes and both
sexes except in the perianal carcinomas, where
the median age was lower, 61 years (range 29 to
89 years).

Results

Tumour location and histological appearance

Clinical stage in relation to tumour location


and histology

Of the 164 anal carcinomas, 23 (14%) were


situated in the perianal region and the remainder
in the anal canal. Twenty-one of the 23 perianal
tumours were of the squamous cell type, the
majority of which (14/21, 67%) were well differentiated (Table 1). Two of the perianally
located tumours were histopathologically classified as cloacogenic carcinomas; both of these
cases displayed squamous cell differentiation
(subtype IIB).
In the anal canal, the cloacogenic type was
more c o m m o n (91 cases, 65%) than the squamous
cell type (50 cases, 35%). Of the squamous cell
carcinomas, most tumours were poorly differentiated (29/50, 58%; Table 1). The large majority
of the cloacogenic carcinomas were of grade II (81
cases) with only 5 cases belonging to each of
grade I and III, respectively. All grade I cases and
approximately half (42/81) of the grade II cases
had squamous cell differentiation (subtype B,
Table 1).

The majority (15/23, 65%) of the perianal tumours were small (T1). Only two (9%) of the
patients had inguinal lymph node metastases at
diagnosis and none had generalized disease (Table 2).
Most of the anal canal carcinomas were more
advanced tumours, i.e. primarily in stage T3 (67
cases, 48%) or T4 (22 cases, 16%) (Table2).
Cloacogenic carcinomas and squamous cell carcinomas had approximately the same distribution
in the different T-stages and there was an equal
distribution of male and female patients. The
T-stage could not be assessed in two cases.
Inguinal node metastases were rare in stages
T1-T2 (5 cases, 10%). Twenty percent (11/55) of the
T3 tumours had inguinal node metastases at diagnosis; this figure was 61% (11/18) in advanced
cases (T4). It should be noted that due to the
retrospective nature of part of this material the N
stage could not be properly assessed in 16 cases

Table 1. Tumour location and histology


Type

Perianal

Differentiation/subtype

Men

Women

All

Men

Women

All

All

Squamous cell
Well
Moderate
Poor

12
9
2
1

9
5
3
1

21
14
5
2

11
0
3
8

39
5
13
21

50
5
16
29

71
19
21
31

0
-

2
2
-

21

70

91

93

17
2

22
40

39
42

39
44

2
2
-

12

11

23

32

109

141

164

Cloacogenic
IB
II A
II B
IIIA
Total

Anal canal

Total

113
Table 2. Tumour stage
Perianal

T1NoMo

Anal canal"

Squamous

Cloacogenic

All

Squamous

Cloacogenic

All

14

15

10

14

T2

14

17

31

T3
T4

2
-

2
-

9
3

33
4

42
7

TaNxMo

T2

.
-

T~
T4

8
1

4
3

12
4

TaN+ Mo
T2

0
1

1
0

2
1

3
1

T3

T4

TaN0-+Ma

T2

T3
T4

2
1

2
4

4
5

50

89

139

21

23

T-stage could not be properly defined in two cases

(12%, NX, see Table 2). Distant metastases were


rare and only 10 (7%; 6 liver, 2 lungs, 1 skeleton,
1 para-aortic lymph nodes) of the 141 tumours in
the anal canal had such metastases at diagnosis.
Seven of these cases were of the cloacogenic type.
Prognosis, univariate analyses
Perianal tumours. Perianal tumours had a favourable outcome. Of the 23 patients, 20 are still alive,
with a five year probability of survival exceeding
85% (Fig. 7), whereas 3 patients have died from
disease. Two of the three dead patients, both men,
were initially in stage T1 and T2 without any
known metastases. These two patients were
primarily treated with local surgery. The third
diseased patient had lymphatic node metastases
at diagnosis and was only palliatively treated.

tiated tumour appeared less favourable than for


female patients but the n u m b e r of male patients
was small and the difference statistically insignificant (p > 0.1).
Among the cloacogenic carcinomas, 5/5 patients are alive in grade I (all subtype B), about
50% in grade II (39A, 42B) and only 1 of 5 in
grade III (all A). The 5 year survival for patients
with subtype IIA was significantly inferior (p <

10

I
@

O"

"~ 0s
9

,b

(8}

Anal canal tumours. The overall survival of anal


canal carcinomas was between 40 and 50% at five
years with no major difference (p > 0.1) between
cloacogenic carcinomas and squamous cell carcinomas (Fig. 7).
The prognosis for patients with a well and
moderately differentiated squamous carcinoma
was superior to that of patients with a poorly
differentiated squamous cell carcinoma (58%
versus 31% at 5 years, p < 0.05, Fig. 8). The prognosis for male patients with a poorly differen-

ca_

12

24
36
Time (months)

48

60

Fig. 7. Probability of survival in 164 patients with an invasive


epidermoid anal carcinoma, all stages; perianal tumours,
(n = 23, z~
z~), anal canal tumours, cloacogenic carcinoma
(n=91, 9
9
and squamous cell carcinoma (n=50,
9
9 respectively. The figures in parentheses indicate the
number of patients surviving 5 years

114
10

10

t
(5)

o 0.5

"~ 0.5
)3)
(3)

(71
h(4)

o-

12

24
36
Time (monthsl

48

Fig. 8. Probability of survival in 50 patients with a squamous


cell carcinoma of the anal canal, all stages, according to degree
of differentiation and sex. Well or moderately differentiated
(n--21, []
[]), poorly differentiated (n--29, 9
9
Among the poorly differentiated tumours, prognosis tended to
be more favourable for women, (n = 21, o
o) than for men
(n = 8, 9
O)

.>

12

24
36
Time (months)

(7)

&

(11)

'B 05

ii

48

j.

L
i

24
36
Time (monfhs]

6 119)
!8)
,i-

60

(11)

)11
m_

12

&

)41

ca_

60

10

{[

'~ 05

46

Fig. 1O. Probability of survival in 79 patients with cloacogenic


carcinoma grade II of the anal canal, all stages, according to
subtype and sex. Subtype IIA, female (n--22, []
n) and
male (n=17, 9
l ) and subtype IIB, female (n=40,
zx
A)

(31

10

60

12

,1,

24
J6
Time (months)

48

60

Fig. 9. Probability of survival in 91 patients with cloacogenic


carcinoma of the anal canal, all stages, according to grade and
subtype. Grade I, (all subtype B, n = 5, - - ) , grade II (n = 81,
A
z~), subtype IIA (n = 39, 9
e), subtype IIB (n =42,
9
9 and grade III (all subtype A, n = 5, 9
m)

Fig. 11. Probability of survival in 139 patients with an epidermoid carcinoma of the anal canal according to clinical stage.
T1-4 NOMO (n = 94, []
Ez), T1-2 NOMO (n = 45, A
z~),
T3-4 NOMO (n=49, 9
--), T1-4 NXMO (n= 16, 9
o),
T1-4 N + M O (n--19, 9
~), T1-4, N O - + , M1 (n=10,
9 . 9

0.01) to that of patients with subtype IIB (Fig. 9).


However, sex also had an impact on prognosis
with a better (p < 0.05) prognosis in female patients than in male patients. Considering female
patients only, there was still a difference
(p < 0.01) between subtypesIIA
and IIB
(Fig. 10). Male patients, all but two in subtypes
IIA, had a poor prognosis with only 11% surviving after 4 years.
Clinical stage also had an impact on prognosis. For patients without known lymphatic node
or distant metastases, the 5-year survival of small
tumours (stages T1-T2) was 75%, whereas it was

about 45% for those in stages T3-T4 irrespective


of histological type (p < 0.001; Fig. 11).
Patients with primary lymphatic node metastases but without known distant metastases had a
poor prognosis with a five year survival rate of
approximately 15% (Fig. 11). The prognosis for
the 16 patients where the lymphatic node status
could not be properly assessed (see above) was
also poor. These patients were, however, elderly,
had advanced T-stages (Table 2) and some were
either not treated or usually only treated palliatively. All patients but one with distant metastases
have died from their disease (Fig. 11).

115
10
(12)

Table 3. Stage, differentiation, sex and localization in primary


anal carcinoma - a multivariate analysis in non-disseminated
cases

ez
>

I 16

"G 05

Estimation variable

Univariate

Multivariate

Step

Entering

)~

)~2
p
(values in the
final model)

Stage
(T1-2 vs T3-4)

9.59

9.59

Differentiation
(well + moderate
versus poor)

7.75

9.78

(11
(21

a_

12

24

36

1.8

60

Time (months)

Fig. 12. Probability of survival in 89 patients with an epidermoid carcinoma of the anal canal without known metastases,
according to primary treatment. T1-2 NOMO, primary radiotherapy with or without chemotherapy (n = 29, o
9 or
surgery (n = 14, 9
9 and T3-4 NOMO radiotherapy with
or without chemotherapy (n= 38, []
[]) or surgery (n= 8,
9
m)

In all T-stages in patients without known


metastases, patients primarily treated with irradiation a n d / o r chemotherapy had a more favourable outcome than patients treated with primary
surgery alone (Fig. 12). This difference was particularly pronounced for small turnouts (T1-2,
p < 0.01). The prognosis was particularly poor for
patients treated with local surgery only, where
only one of nine patients, all in stages T1-2, was
alive at 3 years.

Sex

3.79

6.42

Localization

7.91

7.03

"

" p<0.01; bp < 0.05

Table 4. Additional prognostic information by sex and histological subtype within the cloacogenic carcinomas - a multivariate analysis in non-disseminated cases
Estimation variable

Univariate

Multivariate

Step

Entering

)d

)~2
p
(values in the
final model)

Stage T1
T2
T3
T4

Ref
0.63
1.86
3.58

7.59

Sex

8.90

4.34

9.40

4.12

Subtype

(A vs B)

Prognosis, multivariate analyses


Since a number of parameters was found to be
related to prognosis in the univariate analyses,
multivariate analyses were performed in order to
more readily assess the importance of each factor
in determining survival. These analyses were restricted to non-disseminated cases only (any T,
N0(X), M0), since dissemination had such a
severe impact on prognosis (Fig. 11). Neither was
treatment included due to an extreme heterogeneity, although it appeared to have an impact
on prognosis.
When clinical stage (T1-2 one group, T3-4(X)
the other group), sex, localization (per(anal versus
anal canal) and histologic picture (see below)
were evaluated in all patients, stage was found to
reveal most information (Table 3). Both sex and
localization had independent prognostic information irrespective of how the histologic picture was
grouped. The division of the carcinomas into
cloacogenic versus squamous cell types, respec-

~ p<0.01; by<0.05

tively, had, as already shown in the univariate


analyses, no relation to prognosis (not separately
illustrated), whereas if by histopathology they
were grouped into those with a well and moderately differentiated tumour versus those with a
poorly differentiated tumour, statistically significant independent prognostic information was
noticed. In these analyses, within the cloacogenic
carcinomas, grade I was considered as well,
grade II as moderately and grade IH as poorly
differentiated, respectively. In fact, the information provided by differentiation (grading) was
included in the model prior to sex and localization (Table 3).
In the group of squamous cell carcinomas
only, the degree of differentiation was the only
factor that gave additional information besides
stage (data not illustrated).

116
Table5. Additional prognostic information given by sex,
localization and histological type - a multivariate analysis in
non-disseminated primary anal carcinoma
Estimation variable

Univariate

Multivariate

Step

Entering

X2

Z2
p
(values in the
final model)

Differentiation
well + I
moderate + II
poor+III

Ref.
5.05
15.28

8.77
20.11

b
a

Stage T1
T2
T3
T4

Ref
0.41
2.30
4,20

7.97
4.40

b
c

Sex

9.78

9.91

minor areas with signs of mucous production, but


this finding did not alter the histological classification. The grading of the tumours was exclusively based on the degree of dissociation between
the individual cells in squamous cell carcinomas
and in cloacogenic carcinomas on the occurrence
of peripheral cell palisading.
A n a l canal tumours

Variables not entering: localization (perianal versus anal canal,


Z2= 1.21) and histological type (squamous cell carcinoma versus cloacogenic carcinoma, Z~-- 0.74)
a p < 0.001; b p < 0 . 0 1 ; Cp< 0.05

In cloacogenic carcinomas, both sex and the


absence or presence of squamous cell differentiation (A versus B) were strong predictors of prognosis in the univariate analyses (Figs. 9, 10).
Irrespective of whether stage, the strongest predictor, was included in the regression model or not,
both sex and histologic subtype had independent
prognostic information, although sex was slightly
favoured in the analysis (Table 4).
The perianal tumours appeared to have an
excellent prognosis compared to anal canal
tumours (Fig. 7). These tumours were, however,
considerably more often smaller and more highly
differentiated (Tables 1, 2). After inclusion of the
degree of differentiation and stage in the regression model, sex, but not localization (perianal
versus anal canal), revealed independent prognostic information (Table 5).

Discussion

The histopathological classification used in the


present study was applied in order to obtain an
easy and reproducible method of accurately
identifying various histological types of carcinomas of the anal region in routine diagnostic work.
All tumours considered as squamous cell carcinomas displayed a pure squamous cell differentiation while the cloacogenic carcinomas showed
transitional cell differentiation with or without an
additional squamous component. A few tumours
classified as cloacogenic carcinomas contained

The classification appears to provide considerable, and independent prognostic information.


Although there was no overall difference between
the cloacogenic carcinomas and the squamous cell
carcinomas, major differenes were found within
these two types depending upon the degree of
differentiation and, within the cloacogenic type,
also depending upon whether squamous cell differentiation was present (subtype B) or not (subtype A).
The importance of histopathological subclassification in anal epidermoid carcinoma has been
much discussed ever since Grinvalsky and Helwig
in 1956 [15] and Klotz etal. in 1967 [2] drew
attention to the carcinomas derived from the
transitional epithelium. Both these reports used
the term transitional cloacogenic carcinomas for
tumours thought to be derived from that epithelium which is believed to originate from the
remnants of the cloacal membrane at the dentate
line. Although a few authors have claimed that a
subdivision of carcinomas from the anal canal
provides meaningful prognostic information [2,
16-18], most recent reports have mainly claimed
that any subclassification, although of academic
importance, provides no value for the clinician
[4-9]. The reasons for these differences in opinion
probably refer to differences in patient selection,
different methods of treatment a n d / o r to differences in criteria for subclassification. Our
findings of prognostic difference depending upon
grade (degree of differentiation) is of such magnitude that it could not be overlooked as a guide for
future prognostic evaluation and thus also of
possible importance for treatment selection. This
information was present both within the whole
material and within the two major types, squamous cell carcinomas and cloacogenic carcinomas. The importance of a subdivision into types
of differentiation (squamous, cloacogenic or
mixed) is less clear, partly because of smaller
differences, but also partly because of an uneven
sex distribution. The multivariate analyses indicated, however, that both sex and type of

117
differentiation revealed independent prognostic
information.
Besides the importance of histopathologic subgroup and stage for prognosis, we also noted a
clear correlation between sex and prognosis with
a considerably less favourable course for men
than for female patients. Such a difference has
not been reported before. The reason for the
difference is not known. Neither is it known why
the distribution of sexes within certain histopathological subgroups was so uneven.
An unselected population-based material
provides the most accurate way of truly assessing
parameters such as age and sex distribution and
the proportion of different histopathological subgroups and their possible clinical importance.
Due to the retrospective nature of part of a
population-based study, other factors such as the
incidence of, for example, lymphatic node metastases and, particularly, the importance of treatment can be less accurately assessed. This heterogeneity in treatment should be remembered when
correlating the pathological picture with clinical
behaviour and prognosis.
The unselected nature of this material is reflected in a higher median age of tumours in the
anal canal (68 years) than in previous, usually
hospital-based, series (50-60 years, [4, 5, 18, 19]).
The median age corresponds well with the figures
(66 years) in the Cancer Incidence of Sweden
1970-1983. Furthermore, the n u m b e r of larger
(more advanced) tumours appears to be considerably higher in this series than in previously published series [7, 18, 20], although it should be
remembered that staging procedures have varied
considerably. In the present series, two of three
tumours in the anal canal were larger than 4 cm
in diameter, whereas in previous series only between 1/5 to 2/5 of the tumours were of a
comparable size.
In contrast, this series does not have a higher
incidence of inguinal metastases or distant metastases [9, 19]. Similar to previous series there was a
marked predominance for female patients (3.5 : 1).
This figure is somewhat higher than in most
previous series (2-3 : 1) [4, 21].
In spite of a higher median age and larger
tumours in this series, the overall prognosis was
not less favourable. The reported 5-year survival
rates are usually in the order of 45 to 55% [2, 5,
22], although a recent series by Merlini and
Eckert from Switzerland noted only 20% 5-year
survivors [23]. In that series composed of 106
patients, it was found that the tumours were more

advanced (comparable with ours?) than usually


reported. Previous series, in which 5-year survival
rates are known, are usually composed of patients
treated with surgery as their main treatment
modality, whereas in the present series more
patients were treated with radiotherapy than with
surgery. Thus, although strictly comparable
studies comparing the role of different strategies
are still lacking, it appears that a primarily nonsurgical approach will result in higher survival
rates. Even if treatment selection principles are
not known in detail, survival after primary radiotherapy was superior to primary surgery in all
subgroups of patients in this material. Besides
this, anal function is more often preserved.

Perianal tumours

The perianal tumours differed from the anal


canal tumours in several respects; the patients
were younger, there was no female predominance
and the tumours were smaller and more highly
differentiated. A smaller size may well be explained by more easy detection due to the superficial location, whereas the three other differences
indicate differences in aetiology or pathogenesis.
Two (8%) of the perianal tumours were of the
cloacogenic type, both with squamous cell differentiation. Similar figures have been reported
previously [17, 24]. St has been claimed that these
cancers may arise from anal ducts at the dentate
line caudally penetrating the sphincters and the
perianal fat [2]. It should be stressed that histopathological classification and an assessment of
whether the t u m o u r was perianal or not was
m a d e independently.
As a group, the prognosis for perianal tumours
was better than for anal canal tumours, as has
also been noted in virtually all previous series [4,
24, 25, 26]. However, whether this prognostic
superiority depends upon the location as such or
upon differences in tumour size and differentiation is not certain; the n u m b e r of patients in comparable stages/degrees of differentiation was too
small. When the prognostic information by stage
and differentiation was included in a Cox regression model, it was found that localization did not
reveal any additional prognostic information.
This could indicate that the excellent prognosis
for perianal tumours is rather due to their small
size and high differentiation than to their localization. However, these data must be interpreted
with caution, since the n u m b e r of patients was
limited and treatment heterogeneous.

118

References
1. Harrison EG, Bearhs OH, Hill JR (1966) Anal and perianal malignant neoplasms: pathology and treatment. Dis
Colon Rectum 9:255-267
2. Klotz RG, Pamukcoglu T, Souilliard DH (1967) Transitional cloacogenic carcinoma of the anal canal. Cancer 20:
1727-1745
3. Beahrs OH (1979) Management of cancer of the anus. Am
J Radiol 133:791-795
4. Beahrs OH, Wilson SM (1976) Carcinoma of the anus.
Ann Surg 184:422-428
5. Singh R, Nime F, Mittelman A (1981) Malignant epithelial tumours of the anal canal. Cancer 48:411- 415
6. Bohe M, Lindstr6m C, Ekelund G, Leandoer L (1982)
Carcinoma of the anal canal. Scand J Gastroenterol 17:
795- 800
7. Frost DB, Richards PC, Montague ED, Giacco GG,
Martin RG (1984) Epidermoid cancer of the anorectum.
Cancer 53:1285-1293
8. Dougherty BG, Evans HL (1985) Carcinoma of the anal
canal: a study of 79 cases. Am J Clin Pathol 83:159-164
9. Adam YG, Efron G (1987) Current concepts and controversies concerning the etiology, pathogenesis, diagnosis,
and treatment of malignant tumors of the anus. Surgery
101:253-266
10. Papillon J, Mayer M, Montbarbon JF, Gerard JP,
Chassard JL, Bailly C (1983) A new approach to the
management of epidermoid carcinoma of the anal canal.
Cancer 51:1830-1837
11. Spiessel B, Schiebe O, Wagner G (1982) UICC - TNM
Atlas. Springer, Berlin Heidelberg New York
12. Glimelius B, Phhlman L (1987) Radiation therapy of anal
epidermoid carcinoma. Int J Radiat Oncol Biol Phys 13:
305-312
13. Peto R, Pike MC, Armitage P, Breslow NE, Cox DR,
Howard SV, Mantel N, MacPherson K, Peto J, Smith PG
(1977) Design and analysis of randomized clinical trials
requiring prolonged observations of each patient. II Analysis and examples. Br J Cancer 35:1-39
14. Cox DR (1972) Regression models and life tables. J R Stat
Soc B 26:103-110

15. Grinvalsy HT, Helwig ET (1956) Carcinoma of the anorectal junction I. Histological considerations. Cancer 9:
480-488
16. Morson BC, Dawson JM (1979) Gastrointestinal pathology, 2nd edn. Blackwell Scientific Publications, Oxford,
pp 741-753
17. Serota A, Well M, Russell W, Wollman J, Wilson S (1981)
Anal cloacogenic carcinoma. Arch Surg 116:456-459
18. Boman BM, Moertel CG, O'Connell JH, Scott M, Weiland
LH, Beart RW, Gunderson LL, Spencer RJ (1984) Carcinoma of the anal canal: a clinical and pathologic study
of 188 cases. Cancer 54:114-125
19. Cummings BJ (1982) The place of radiation therapy in the
treatment of carcinoma of the anal canal. Cancer Treat
Rev 9:125-147
20. Nigro ND (1984) An evaluation of combined therapy for
squamous cell cancer of the anal canal. Dis Colon Rectum
27:763-766
21. Goldman S, Ihre Th, Seligsson U (1985) Squamouscell carcinoma of the anus. Dis Colon Rectum 28:143-146
22. Golden GT, Horsley JS (1976) Surgical management of
epidermoid carcinoma of the anus. Am J Surg 131:
275-280
23. Merlini M, Eckert Ph (1985) Malignant tumors of the
anus. A study of 106 cases. Am J Surg 150:370-372
24. Greenall MJ, Quan S, Stearns M, Urmacher C, DeCosse J
(1985) Epidermoid cancer of the anal margin. Am J Surg
149:95-100
25. Stearns MW, Quan SH (1970) Epidermoid carcinoma of
the anorectum. Surg Gynecol Obstet 131:953-957
26. Nielsen OV, Jensen SL (1982) Cancer ani i Danmark
1943-1973. I. Carcinoma planocellulare a n i - diagnose,
behandling og prognose. Ugeskr Laeger 144:851-856
Accepted: 20 January 1988
Dr. Sven Goldman
Department of Surgery
SOdersjukhuset
Box 38100
S- 100 64 Stockholm
Sweden

Col6ree/al
Disease

Int J Colorect Dis (1988) 3:119-123

9 Springer-Verlag 1988

The role of the liver in the protection by elemental diets


against experimental colon cancer
T. Barton and M. R. Lewin
Department of Surgery, Faculty of Clinical Sciences, University College London, London, UK

Summary. This study investigates the mechanism


whereby the elemental diet 'Vivonex' protects
against experimental colon cancer. A total of 240
Wistar rats were randomly allocated to three
dietary groups: (A) Vivonex HN, (B) Vivonex HN
with 0.05% added cholesterol and (C) control
standard powdered diet. All received a colon
cancer-producing regimen of dimethylhydrazine
(DMH) at a dose of 4 0 m g / k g BW, s.c., once
weekly for 5 weeks. Ten weeks following the first
DMH injection, then at 5 weekly intervals until
the 40th week, 10 randomly selected rats from
each dietary group were weighed, killed and
necropsied. Total liver weights were recorded
with samples kept for total lipid extraction and
cholesterol and phospholipid assay. Each colon
underwent macroscopic examination and all neoplasms were recorded.
Results showed that control rats had a constant total liver lipid content over the 40 weeks
and an increased incidence, number and development of colonic neoplasms with time. In contrast,
u
fed rats had significantly elevated total
liver lipids, cholesterol and phospholipids over
the 40 weeks compared to controls and a significantly reduced number and rate of development
of colonic neoplasms. Rats fed on Vivonex+
cholesterol had total liver lipids intermediate and
significantly different from both the Vivonex and
control groups and a similar result was seen in
tumour development with time.
This study shows that a u
diet results in
an increase in hepatic lipids, this effect being
partially reversed with dietary cholesterol. The
protecive effect of Vivonex feeding in the DMH
model of colon cancer may thus be mediated in
part by the liver.

Dietary factors have been implicated in the aetiology of colorectal cancer [1]. Prime candidates for
such a role are dietary fats [2] and fibre-depleted
diets [3]. Results from epidemiological studies
have so far been inconclusive with respect to
which exact dietary component is important in
this disease. Similarly, dietary studies in experimental models of colon cancer have also been
inconclusive although dietary factors have been
shown to modify the disease, with fats increasing
tumour yields and incidence [4] and fibre generally reducing these parameters [5]. Of particular
interest are the reports of elemental diets conferring protection against experimental colon
cancer by reducing incidence, numbers of colonic
tumours and improving survival [6-9]. The
mechanism of this protection can be variously
attributed to intestinal mucosal hypoplasia [10,
11], the cholesterol-free nature of such diets [7]
and the effects on gut flora and faecal sterols [12].
Further, u
has been reported to cause a
reduction in biliary secretions in man [13] and
this effect may be of relevance in the animal
model. The purpose of this study was to investigate whether dietary Vivonex exerts its protective
effect against experimental colon cancer by a
liver-mediated mechanism.
Materials and methods
A total of 240 female Wistar rats (weight range 80-100 g) were
randomly allocated to three dietary groups: (A) Vivonex I-IN
powder (Norwich Eaton plc, Woking, Surrey), (B) Vivonex
kiN with 0.05% added cholesterol and (C) standard laboratory
powdered diet (MRC Formula 41B, E Dixon & Co, Ware,
Herts) and served as controls. Diets, the main constituents of
which are detailed in Table 1, and water were provided ad
libitum. All animals then received a colon cancer-producing
regimen of dimethylhydrazine (DMH) at a dose of 40 mg/kg
BW, s.c., once weekly for five weeks. The animals were housed

120
Table 1. The main dietary constituents of three experimental
groups
Dietary
components
Energy KCals/kg
Carbohydrates %
Protein %
Fat %
Fibre %

Vivonex HN

3,750
79.1
2.5
0.33"
0

Vivonex HN
+ 0.05 %
Cholesterol

41B
Control
diet

3,750
79.1
2.5
0.33 a
0

3,580
49.7
12.7
3.12 b
4.8

110//
//

100/

>

_J
ol

90-

iI

80-

(D

0~

70-

~
o

" Highly purified safflower oil (80% triglyceride oflinoleic acid)


b White fish meal to give 0.7% saturated triglycerides, 1.24%
linoleic acid and 1.18% other unsaturated fatty acids

VChol

60-

50-

40-

~o

l'S

20
TIME

in a temperature controlled room, in sub-groups of five, in


suspended cages with wide open mesh wire floors designed to
prevent coprophagia. The rats were weighed weekly and
inspected daily for signs of colonic disease.
Ten weeks after the first DMH injection and at 5-weekly
intervals until the 40th week, random groups of 10 rats from
each of the three dietary groups were selected, weighed,
painlessly killed and necropsied. The whole liver was removed
carefully, weighed and samples retained for histology and lipid
estimation. Each colon underwent a full macroscopic examination and all neoplasms were recorded. The total lipid
content of each liver was measured following a Folch extraction procedure [14]. The extracts were enzymatically assayed
for cholesterol [15] and phospholipids [16]. Lipid results in
terms of mg/g of liver were expressed as medians and ranges
and statistically analysed by the Wilcoxon rank sum test for
unpaired data and by the Fisher Exact test where appropriate.

io v

2's
IN

3'o

3'5

4o

WEEKS

Fig. 1. The changes in median total liver lipids with time in the
three dietary groups

5"0-

/ /

4"5-

//o

._1

.J

4-0-

E
VChol

(Z 3-5I.iJ
LIJ 3 " 0 -

C>
"12"5-

Results
The results for changes in total liver lipids, cholesterol and phospholipids and the development of
total colonic neoplasms with time in the three
dietary groups are illustrated in Figs. 1, 2, 3 and 4
respectively.
In control animals the total liver lipids remained unchanged over the 40week period
(Fig. 1) and this was associated with an increase
in both the % incidence and median number
(Table 2) and the development of colonic neoplasms with time (Fig. 4). In contrast, in the
Vivonex-fed group there was an upward trend in
total liver lipids with time (Fig. 1). These lipids
were significantly higher (p values < 0.01) over
the whole study period than in the control group
and associated with significantly fewer (p values
< 0.05) and significantly slower (p < 0.001) development of colonic neoplasms with time (Fig. 4).
Total liver lipids in the Vivonex+cholesterol
group fell between the curves for the other two
groups (Fig. 1) being significantly higher over the

41B

2-0

1'o

,5

2'o
TIME

2'5
IN

3'o

40

WEEKS

Fig. 2. The changes in median liver cholesterol with time in


the three dietary groups

15-0 /

oV

//
1.5
o~

?
~Q.
--1
0
Q.
m
0"1-

//

12"5....

"-~

~- - ////

VChol

10.0-

7"5-

~~176

418

5.0

ib

1%

2'o ,%
TIME

s'o

s%

20

IN WEEKS

Fig. 3. The changes in median liver phospholipids with time in


the three dietary groups

121
Table 2. The changes in % incidence and median numbers of colonic neoplasms with time in the three dietary groups
Weeks

10
15
20
25
30
35
40

Vivonex + Cholesterol

Controls

Incidence
%

Median (range)
Neoplasms/group

Incidence
%

Median (range)
Neoplasms/group

Incidence
%

Median (range)
Neoplasms/group

0
20
20 c
30 d
70
100
80

0 (0-0)
0 (0-1)
0 (0-1)"
0 (0-3)~
1 (0-3)"
2 (1-4)"
1 (0-3)"

0
10
30"
50 b
50 b
80
100

0 (0-0)
0 (0-2)
0 (0-3) a
1 (0-5)"
1 (0-4)"
2 (0-5)"
2 (1-5)"

10
50
90
100
100
90
100

0 (0-1)
I (0-3)
2 (0-18)
4 (1-11)
4 (1-13)
7 (0-13)
12 (2-22)

" p < 0.01; bp < 0.02; cp < 0.005; dp < 0.002 compared to controls
Table 3. Changes in the incidence of small bowel neoplasms
with time in the three dietary groups
Weeks

% Incidence of small bowel neoplasms

10
15
20
25
30
35
40

Vivonex

Vivonex +
Cholesterol

Controls

0
0
0
20
20
10
20

0
0
40
0
0
20
10

0
10
10
10
50
30
40

13041 B
120-

60-

z
~- 50z

o
0

40-

VCho[
30-

..a,
20-

jJ

" \,

.J

10O.J
10

15

20
25
30
TIME IN WEEKS

35

40

Fig. 4. The increase in total numbers of colonic neoplasms


with time in the three dietary groups
whole study period than controls (p values
< 0.05), and significantly lower than the Vivonex
group, but only at weeks 20, 30 and 40 (p values
< 0.05). A similar pattern of differences was seen
for both liver cholesterol and phospholipid, where
control levels were significantly lower than both

the Vivonex and Vivonex+cholesterol groups


over the whole study period (p values < 0.02).
There were no differences however between the
Vivonex and Vivonex+cholesterol groups with
respect to liver cholesterol and phospholipid,
although there was a trend for the latter group to
lie intermediate between the control and Vivonex
groups (Figs. 2 and 3).
The equations for the regression lines ( y =
mx + c) for the development of colonic neoplasms
with time in the three dietary groups (Fig. 4) were
given by:
Vivonex Group:
y = 0.64x-7.75,
r = 0.87, p < 0.02
Vivonex + Cholesterol Group:
y=0.80x-9.71,
r=0.94, p < 0.01
Control Group:
y = 3.44x-37.32, r--0.92, p < 0.01
The development of colonic neoplasms with
time in the u
cholesterol fed Group was
significantly less than in the control group
(p < 0.001) but significantly greater than the
Vivonex-fed group (p < 0.05).
The observations in this study were not due to
caloric effects since the three diets were almost
isocaloric [7]. The growth curves over the first
twenty weeks of the study, (when the cancers were
not severe enough to affect body weight), were
identical between the three dietary groups.
Further, the reduction in large bowel neoplasia in
the two Vivonex-fed groups was part of an overall
reduction in intestinal carcinogenesis since there
were also decreases in the incidence of small
bowel neoplasms in these two groups (Table 3).
Discussion

Vivonex is a low fat, high carbohydrate, minimal


residue elemental diet which is almost totally

122

absorbed in the upper small intestine [17]. When


used in the experimental model of colon cancer it
has been shown to be protective [6, 7] as have
other elemental diets [8, 9]. This is confirmed by
the findings reported here where Vivonex feeding
resulted in a reduction in the incidence, numbers
and rate of development of colonic neoplasms
together with a significant increase in total liver
lipids, cholesterol and phospholipids. Vivonex
feeding further resulted in an overall decrease in
intestinal carcinogenesis with reductions in small
bowel lesions also being noted.
The protective effect of Vivonex has previously been attributed to its lack of cholesterol
content [7]. In the D M H rat colon cancer model
these workers found that Vivonex reduced the
latent period, incidence and metastases and improved survival from colon cancer. Addition of
dietary cholesterol reversed these parameters and
hence they ascribed a co-carcinogenic role to
dietary cholesterol. Castleden [6] similarly noted a
reduced incidence of colon cancer in Vivonex-fed
rats but his experiments were confounded by the
rats eating sawdust from their cages; thus he was
unable to discount the possible protective effects
of dietary fibre. Using the elemental diet 'Flexical', Fleiszer et al. reported a similar protective
effect with a reduced incidence of experimental
colon cancer in rats [8, 9]. These authors rationalised the protective effect as the result of
'reduced alimentary-tract secretions'. A more
recent study [18] looked at the effect of a liquid
elemental diet on colon carcinogenesis in rats.
They reported that such a diet resulted in an
increased incidence of colon cancer, though a
possible explanation of their findings could be the
high fat content of the diet used [19].
The mechanism whereby this diet protects
against colon cancer remains obscure. That such
diets cause intestinal disuse atrophy with mucosal
hypoplasia is well documented [10, 11] and may
be an important factor in the mechanism of
protection. However, evidence against this was
that the addition of a single dietary variable
(cholesterol) to Vivonex abolished the protective
effect [7]. Thus other mechanisms must be
evoked. In this study and as previously reported
[20, 21], Vivonex feeding in rats leads to a significant accumulation of lipids and cholesterol in the
liver. It is known that Vivonex feeding reduces
both pancreatic and biliary secretions [13, 17]
hence reducing cholesterol and bile salt secretion
into the gut, both implicated in the pathogenesis
of colorectal cancer [22, 23]. There is also the
possibility that the hepatic metabolism of D M H

[24] may have been altered by the diet and the


carcinogenic potential of D M H reduced. This is
unlikely since it has been shown that Vivonex
feeding, starting 14 weeks following the last D M H
injection, still exerted a protective effect [25].
Further possible mechanisms include the
effects of Vivonex on gut flora and reduction in
the faecal excretion of both neutral and acid
sterols [12]. However, such mechanisms are likely
t o be mediated by the liver in response to dietary
modifications. Thus the decrease in faecal bile
acids following Vivonex feeding was concluded to
be the result of a reduced turnover of a normal
sized bile acid pool reflecting the reduction of
necessary bile acid synthesis [20]. High carbohydrate diets increase insulin output which
markedly stimulates hepatic HMGCo-A reducase activity and promotes hepatic lipogenesis [26].
Further, ligation of the bile duct leads to increased hepatic cholesterol synthesis, this effect
being inhibited by prior cholesterol feeding [27].
Perhaps the biliary stasis resulting from Vivonex
feeding was analogous to this effect and the lack
of a profound response to cholesterol in our study
explained by the low physiological dose used,
0.05% compared to 2% used by others [27].
In conclusion, this study, which for the first
time has sequentially examined hepatic changes
which accompany DMH-induced experimental
colon cancer, has shown that Vivonex feeding
protects against colon cancer by reducing the
incidence, numbers and development of colonic
neoplasms with time. This was accompanied by
significantly increased total hepatic lipids,
cholesterol and phospholipids. Addition of dietary cholesterol partially reversed these effects.
We suggest that the primary mechanism of protection is mediated by the liver in response to the
diet, with biliary stasis resulting in reduced
luminal concentrations of cholesterol and bile
salts.

Acknowledgements. MRL gratefully acknowledges support of


the Cancer Research Campaign (Project Grant S-12018) and
the British Medical Association for the T. P. Gunton Award.
Norwich Eaton plc, Woking, Surrey generously supplied the
Vivonex used in this study.

References
1. Armstrong B, Doll R (1975) Environmental factors and
cancer incidence and mortality in different countries, with
special reference to dietary practices. Int J Cancer 15:
617-631
2. Wynder EL, Reddy BS (1983) Dietary fat and fibre and
colon cancer. Semin Oncol 10:264-272

123
3. Burkitt DP (1971) Epidemiology of cancer of the colon
and rectum. Cancer 28:3-13
4. Reddy BS, Maeura Y (1984) Tumour promotion in AOM
induced carcinogenesis in female F334 rats: influence of
amount and source of dietary fat. J Natl Cancer Inst 72:
745 -750
5. Freeman HJ, Spiller GA, Kim YS (1980) A double blind
study on the effects of differing purified cellulose and
pectin fibre diets on 1,2-dimethylhydrazine-induced rat
colonic neoplasia. Cancer Res 40:2661 - 2665
6. Castleden WM (1977) Prolonged survival and decrease in
intestinal tumours in dimethylhydrazine-treated rats fed a
chemically defined diet. Br J Cancer 35:491-495
7. Cruse JP, Lewin MR, Ferulano GP, Clark CG (1978) Cocarcinogenic effects of dietary cholesterol in experimental
colon cancer. Nature (London) 276:822-825
8. Fleiszer D, Murray D, MacFarlane J, Brown RA (1978)
Protective effect of dietary fibre against chemically induced bowel tumours in rats. Lancet ii:552-553
9. Fleiszer DM, Murray D, Richards GK, Brown RA (1980)
Effects of diet on chemically induced bowel cancer. Can J
Surg 23:67-73
10. Janne P, Carpentier Y, WiUems G (1977) Colonic mucosal
atrophy induced by a liquid elemental diet in rats. Am J
Dig Dis 22:808-812
11. Morin CL, Ling V, Bourassa D (1980) Small intestinal and
colonic changes induced by a chemically defined diet. Dig
Dis Sci 25:123-128
12. Crowther JS, Drasar BS, Goddard P, Hill MJ, Johnson K
(1973) The effect of a chemically defined diet on the faecal
flora and faecal steroid concentration. Gut 14:790-793
13. Nelson LM, Carmichael HA, Russell RI, Atherton AT
(1977) Use of an elemental diet (Vivonex) in the management of bile acid-induced diarrhoea. Gut 18:792- 794
14. Christie WW:(1973) The isolation of lipids from tissue. In:
Christie WW (1973) Lipid analysis. Pergamon Press, Oxford, p 30-41
15. Stabler F, Gruber W, Stinshoff K, Roschlau P (1977) Eine
praxisgerechte enzymatische Cholesterin-Bestimmung.
Med Lab 30:29-37
16. Takayama M, Itoh Smagasaki T, Tanimizu I (1977) A new
enzymatic method for determination of serum cholinecontaining phospholipids. Clin Chim Acta 79:93-98
17. Russell RI (1975) Elemental diets. Gut 16:68-79
18. Tatsuta M, Yamamura H, Ishi H, Ichii M, Noguchi H,
Baba M, Taniguchi H (1985) Effect of a chemically

19.
20.
21.

22.

23.
24.
25.

26.

27.

defined diet in liquid form on colon carcinogenesis in rats.


J Natl Cancer Inst 75:911-916
Lewin MR (1986) Effect of a chemically defined diet in
liquid form on colon carcinogenesis in rats. J Natl Cancer
Inst 77:590
Nelson LM, Williamson I, Russell RI (1981) Elemental
diet composition: effect on bile acid metabolism and
hepatic lipids. Gut 22:A429-A430
Park RHR, Duncan A, Mitchell G, East W, Russell RI
(1985) Comparison of modular elemental and polymeric
liquid diets on growth, nitrogen (N) balance, N wastage,
faecal residue and hepatic lipid in rats. Gut 26:1112
Reddy BS, Wynder EL (1977) Metabolic epidemiology of
colon cancer: faecal bile acids and neutral sterols in colon
cancer patients and patients with adenomatous polyps.
Cancer 39:2533-2539
Cruse JP, Lewin MR, Clark CG (1979) Dietary cholesterol
is co-carcinogenic for human colon cancer. Lancet i:
752-755
Fiala ES (1977) Investigation into the metabolism and
mode of action of the colon carcinogens DMH and AOM.
Cancer 40:2436- 2445
Cruse JP, Lewin MR, Clark CG (1982) Dietary cholesterol
deprivation improves survival and reduces incidence of
metastatic colon cancer in dimethylhydrazine-pretreated
rats. Gut 23:594-599
Lakshmanan MR, Nepokroeff CM, Ness GC, Dugan RE,
Porter JW (1973) Stimulation by insulin of rat liver /~hydroxy fl-methylglutaryl coenzyme A reductase and
cholesterol synthesising activities. Biochem Biophys Res
Comm 50:704- 710
Harry DS, Dini M, McIntyre N (1973) Effect of cholesterol feeding and biliary obstruction on hepatic cholesterol biosynthesis in the rat. Biochim Biophys Acta 296:
209-220

Accepted: 20 January 1988


Dr. M. R. Lewin
Department of Surgery
Faculty of Clinical Sciences
University College London
The Rayne Institute
5 University Street
London WC 1E 6JJ
UK

Col6i'eeial
Disease

Int J Colorect Dis (1988) 3:124-126

9 Springer-Verlag 1988

A randomised trial to compare the results of injection sclerotherapy


with a bulk laxative alone in the treatment of bleeding haemorrhoids
A. Senapati and R.J. Nicholls
St. Thomas' Hospital, London, UK

Abstract. In a p r o s p e c t i v e r a n d o m i s e d trial, 43
patients with b l e e d i n g h a e m o r r h o i d s were allocated to receive either a b u l k laxative with
injection o f p h e n o l (5%) in arachis oil (20 patients) ( G r o u p 1), or a b u l k laxative a l o n e (23
patients) ( G r o u p 2). T r e a t m e n t was given b y one
a u t h o r a n d patients were assessed " b l i n d " b y the
other at 6 weeks, 3 m o n t h s a n d finally at 6
months. At 6 weeks 12 (48%) in G r o u p 1 a n d 12
(57%) in G r o u p 2 were still bleeding (NS; 3(2=
0.54). At 3 m o n t h s 10 (40%) in g r o u p 1 a n d 6
(35%) in g r o u p 2 (NS; X2=0.10), a n d at 6 m o n t h s
10 (43%) in g r o u p 1 a n d 7 (47%) in g r o u p 2 were
still bleeding (NS; ;(2 =0.04). N o significant difference in b l e e d i n g at 6 m o n t h s after either
injection s c l e r o t h e r a p y with b u l k laxative or b u l k
laxatives alone was found.

Injection s c l e r o t h e r a p y [1] is a m o n g the m o s t


p o p u l a r m e t h o d o f treating h a e m o r r h o i d s and
control o f b l e e d i n g has b e e n r e p o r t e d in 50 to
90% o f cases [2-6]. H o w e v e r , other studies [7-11]
h a v e s h o w n that b l e e d i n g stops in 20 to 70% o f
patients followed w i t h o u t a n y t r e a t m e n t or given
b u l k laxatives alone. There h a v e b e e n no r e p o r t e d
trials c o m p a r i n g these treatments.

Patients and methods


Forty-three patients with bleeding haemorrhoids were admitted to the trial. All had been referred to the hospital by the
general practitioner to whom they had initially presented. The
purpose of the trial was explained to each patient and consent
obtained. Ethical permission was obtained from the hospital
ethical committee. Only patients who had bled from haemorrhoids within 2 weeks of being seen in the outpatient clinic
were admitted. Spontaneously reducing prolapse was not an
exclusion as long as bleeding was present. Patients were
excluded if they had been treated for haemorrhoids within the
previous 6 months or had coexistant colorectal disease.

The patients were seen by one of the authors (RJN) and a


full anorectal examination was carried out. Colorectal disease,
when suspected, was excluded by appropriate further investigations. On establishing the diagnosis of bleeding haemorrhoids, the patient was randomly allocated to one of two
treatment groups by balanced randomisation. Twenty patients
in Group 1 were prescribed a bulk laxative (sterculia 15 ml
nocte) and received a submucosal injection of 9 ml of 5%
phenol in arachis oil above each haemorrhoid. Twenty-three
patients in Group 2 were also prescribed the same bulk
laxative but not given an injection. All other laxatives and
topical medications were stopped and the patients were asked
to fill in a diary card to record further bleeding. The patients
were not aware of whether an injection had been given or not.
The follow-up assessments were performed by a second
clinician (AS) who did not know into which group the patient
had been randomised. Patients were examined at 6 weeks, 3
months and 6 months. Bleeding, pain, prolapse, discharge and
urinary symptoms were recorded at each visit. Asymptomatic
patients were given no further treatment. If bleeding continued, but was improved, the patient continued in the trial
and was referred back to the second author to receive the
same treatment according to the group to which they had
originally been allocated. If the bleeding was unchanged or
worse at 6 weeks or 3 months the patient received an injection,
whatever the original treatment group, and was followed for 6
months after that.
Statistical evaluation by Chi-square analysis was used
throughout.

Results
There were 28 m e n a g e d b e t w e e n 20 a n d 79 years
( m e a n 47.8 years) a n d 15 w o m e n aged b e t w e e n
24 a n d 65 years ( m e a n 42.2 years).
N o patient r e p o r t e d u n t o w a r d side effects
f r o m injections. Six patients could not tolerate
sterculia and were given i s p a g h u l a as an alternative b u l k laxative within 4 days o f stopping the
former. All the patients a d m i t t e d to taking the
b u l k laxative regularly.
O n e patient in G r o u p 2 was s u b s e q u e n t l y
f o u n d to h a v e a sigmoid a d e n o m a a n d a n o t h e r
patient in G r o u p 2 did not attend for follow-up at

125
Table 1. Changes in denominator in Groups 1 and 2
Randomisation

6 weeks

3 months

6 months

2 lost follow-up
Group 1

20

> 24

f
Group 2

23

25
4 bleeding
worse

~ 21

/ I ~ 23
1 bleeding
worse

> 17

1 lost follow-up
1 sigmoid adenoma

15

1 lost follow-up

] C - ~ o u p 1 E~dklaxative& injection
80

[]

Group 2 Bulk laxativealone

60,

% bleeding

,0.

~i

% not bleeding 60-

801(:0.

0/52

6/52

3/12

6/12

Fig. 1. The percentage distribution of patients bleeding before


treatment and at 6 weeks, at 3 months and at 6 months after
treatment

% bleeding ! t

[]

Grouo 1 Bulk laxative& injection

[]

Group 2 B~k laxativealone

% not bleeding
1

0/52

6/52

3/12

6/12

Fig. 2. The percentage distribution of patients bleeding during


the study, excluding five patients in Group 2 who were injected
and therefore broke the protocol

all, leaving 41 patients for assessment. Three


further patients did not attend at 6 months (two
from Group 1 and one from Group 2), leaving 38
patients at the end of the study. Results in the 41
patients followed for at least 3 months were
assessed at 6 weeks and 3 months were therefore
included in the analysis.
On breaking the code at 6 months it was
found that five patients in Group 2 in whom
bleeding was unchanged or worse had been injected during the study. Four had been injected at
6 weeks and one at 3 months. All five were
followed up for 6 months from the injection, and
were analysed as though originally randomised to

Group 1. The numbers of patients in Group 1


consequently rose at 3 months to 25 and those in
Group 2 fell to 17. The size of the denominator in
each group during the trial is given in Table 1.
The results are given in Fig. 1. At 6 weeks 12
(50%) of the 24 injected patients were still bleeding compared with 12 (57%) of the 21 noninjected patients. This difference was not statistically significant (X2=0.54). At 3 months 10
(40%) of the 25 in Group 1 were still bleeding
compared with six (35%) in the remaining 17
patients in Group 2 (NS, X2=0.10). At 6 months
10 (43%) of the remaining 23 patients in Group 1
were bleeding compared with 8 (53%) of the
remaining 15 patients in Group 2 (NS; X2= 0.04).
Of the five patients in Group 2 who had moved to
Group 1, four were still bleeding at 6 months.
Eighteen patients were still bleeding at the end of
the study. Twelve (67%) (8 of the 10 in Group 1
and 4 of the 8 in Group 2) were improved with
only occasional bleeding on the toilet paper. Of
the remaining four, two were treated by haemorrhoidectomy and two had rubber band ligation.
All four patients stopped bleeding.
Overall, 44% of the injected patients re-bled
after initial cessation of bleeding compared with
41% of those that were not injected (NS, Z 2=
0.02).
Thirteen (31%) of the 43 patients were constipated and reported passing hard stools. Of
these, 40% in Group 1 had not stopped bleeding
at 6 months compared with 38% in Group 2 (NS,
X2--0.01). They were not asked specifically whether their stool consistency had changed with the
bulk laxative.
Even when the five patients who had moved
from Group 1 to Group 2 were returned to Group
1 for analysis, there was no significant difference
in the results with 33% in Group 1 compared with
55% in Group 2 still bleeding at 6 months (X 2=
1.8). When the same five patients were excluded
from the analysis altogether 33% in Group 1
compared with 47% in Group 2 were still bleeding
at 6 months (NS; Z 2 = 0.37) (Fig. 2).
Discussion

Over the last 20 years there has been a trend


away from haemorrhoidectomy and many trials
comparing different non-surgical treatments have
been published [2-13]. They are, however, difficult to interpret since haemorrhoidal symptoms
are intermittent and bleeding, for example, has
been reported to stop spontaneously with no
treatment or bulk laxatives in up to 60% of

126

patients [7-10]. These remission rates are very


similar to results reported after active treatment
including injection sclerotherapy which has been
reported to achieve resolution of bleeding in
50-90% of cases [2-6]. The results depend, however, on the duration of follow-up with improvement rates at 3 to 6 months falling by
10-20% at one year [2, 11]. To date there has
been no trial designed to assess the effectiveness
of injected against a suitable control group. Most
trials furthermore have included patients with
both bleeding and prolapse [2, 4, 8, 11] or have
not specified the nature of the symptoms [4, 6].
Sometimes the criteria for improvement have
been defined only loosely [3, 4, 6, 11, 15] so that
any assessment of effectiveness is impossible to
interpret owing to lack of satisfactory end points.
The present trial aimed to overcome some of
these difficulties. First the design included a
control group with which the test group could be
compared such that any effect of injections should
have been apparent. It was considered unethical
not to offer the patients any treatment at all and
for this reason a bulk laxative was given to both
groups. Secondly a follow-up period of 6 months
was adopted. Thirdly fairly strict criteria for entry
were used with the sole emphasis on bleeding.
Furthermore the most recent episode of bleeding
had to be within 2 weeks of presentation and
recent previous treatment was judged to be a
reason for exclusion. As a result of this design the
number of patients entering the trial was small
when compared with others [5, 6, 10, 11]. However, the results were assessed "blind" and the
assessment of results was as detailed as is possible
in such an outpatient study. The overall follow-up
rate at 6 months of 38 out of 42 cases (90%) is
evidence of the thoroughness of follow-up with
failure to attend at 6 months being evenly balanced in the two treatment groups (two in
Group 1; two in Group 2).
The conclusion from this study is that injection scleratherapy with phenol (5%) in arachis oil
and a bulk laxative is no more likely than a bulk
laxative alone to reduce the incidence of bleeding
from haemorrhoids over a 6-month period.
The trend in favour of injection when the data
were analysed according to group allocation
(bleeding at 6 months: 33% of Group 1; 55% of
Group 2) and the small numbers of patients in
each group might raise the objection that a
significant difference would have occurred with
more patients entered. However it would have
required a patient entry of nearly 100 in each
group to demonstrate a statistically significant

difference at the 5% level. We felt that in clinical


practice injection sclerotherapy should be substantially more effective than we observed to
justify any claim of efficacy. For the overall
analysis of all patients who were injected compared with those treated only by bulk laxatives,
bleeding rates of 43% and 47% in Groups 1 and 2.
respectively, do not show any significant advantage for injection.

Acknowledgement. We

wish to thank Mr. B. T. Jackson for


kindly allowing us to include his patients in this study.

References
1. Anon (1975) Outpatient treatment of haemorrhoids. Br
IVied J 1:651
2. Graham-Stewart CW (1962) Injection treatment of haemorrhoids. Br Med J 1:213-6
3. Greca F, Hares MM, Nevah E, Alexander-Williams J,
Keighley MRB (1981) A randomised trial to compare
rubber band ligation with phenol injection for treatment
of haemorrhoids. Br J Surg 68:250-2
4. Sim AJW, Murie JA, Mackenzie I (1981) Comparison of
rubber band ligation and sclerosant injection for first and
second degree haemorrhoids. Acta Chir Scand 147:71720
5. Cheng FCY, Shum DWP, Ong GB (1981) The treatment
of second degree haemorrhoids by injection, rubber band
ligation, maximal anal dilatation, and haemorrhoidectomy:
a prospective clinical trial. Aust N Z J Surg 51:458-62
6. Leicester RJ, Nicholls RJ, Mann CV (1981) Infrared
coagulation: a new treatment for haemorrhoids. Dis Colon
Rectum 24:602-5
7. Gartell PC, Sheridan RJ, McGinn FP (1985) Out-patient
treatment of haemorrhoids: a randomised clinical trial to
compare rubber band ligation with phenol injection. Br J
Surg 72:478-479
8. Hunt PS, Korman MG (1981) Fybogel in haemorrhoid
treatment. Med J Aust 2:256-8
9. Moesgaard F, Nielsen ML, Hansen JB, Knudson JT
(1982) High fibre diet reduces bleeding and pain in
patients with haemorrhoids. Dis Col Rectum 25:454-6
10. Webster DJT, Gough DCS, Craven JL (1981) The use of
bulk evacuant in patients with haemorrhoids. Br J Surg
65:291-2
11. Broader JH, Gunn IF, Alexander-Williams J (1974) Evaluation of a bulk forming evacuant in the management of
haemorrhoids. Br J Surg 61:142-4
12. Keighley MRB, Buchmann P, Minervini S, Arabi Y,
Alexander-Williams J (1979) Prospective trials of minor
surgical procedures and high fibre diet for haemorrhoids.
Br Med J 2:967-9
13. O'Callaghan JD, Matheson TS, Hall R (1982) In-patient
treatment of prolapsing piles: cryosurgery versus MilliganMorgan haemorrhoidectomy. Br J Surg 69:157-9
Accepted: 23 February 1988
Mr. R. J. Nicholls
Consultant Surgeon
St. Thomas' Hospital
London SE1 7EH
UK

Col61"eclal
Disease

Int J Colorect Dis (1988) 3:127-131

9 Springer-Verlag 1988

How I do it

The prediction of local recurrence in rectal adenocarcinoma


by histopathological examination
P. Quirke and M. F. Dixon
Department of Pathology, University of Leeds, Leeds, UK

Abstract. Local recurrence of rectal adenocarcinoma is mainly due to failure to remove all the
tumour. A method is described for the routine
detection of involvement of the circumferential
(lateral) resection margin. Current definitions of
the length of the rectum are inadequate for the
assessment of the risk of local recurrence as the
rectum frequently extends higher than 15 cm. Use
of the term recto-sigmoid should be replaced
clinically by sigmoidoscopic measurement of the
height of a tumour and pathologically by its
anatomical relationship to the level of peritoneal
reflection, i.e. lower or upper segment of the
rectum or the sigmoid colon. Tumours above the
peritoneal reflection (upper segment) are at risk
of circumferential resection margin involvement
due to their retroperitoneal component. The
amount of tissue excised varies considerably from
surgeon to surgeon. Meticulous attention to the
clearance of the tumour at the circumferential
resection margin is essential if local recurrence
rates are to be reduced. A trial of postoperative
radiotherapy should be instigated based on the
pathologist's identification of patients at high risk
of local recurrence.

Recent pathological [1] and surgical studies [2]


strongly suggest that a major cause of local
recurrence of rectal adenocarcinoma after surgery
is failure of complete local clearance of turnout.
Such studies do not rule out other possible mechanisms such as the shedding of free luminal tumour
cells or the possible anastomotic promotion of a
new primary tumour, but in our opinion these fail
to account for the relatively rapid development in
most cases of pelvic recurrence in patients after

surgery of a tumour with a proven slow doubling


time. Furthermore such theories fail to explain
the major differences in the incidence of local
recurrence in rectal as opposed to colonic
tumours. In this paper we would like to describe
the current practice of histopathological examination of the resected specimen in our Department.
We presently use a modification of the original
research method previously described [1]. Preliminary results on patients followed for at least
one year suggest that the modified method is a
satisfactory substitute for total embedding of the
tumour which is not applicable in routine practice
(Quirke, Holdsworth and Dixon, unpublished
observations).
Anatomical considerations

The rectum can be anatomically defined in a


variety of ways but it is commonly held to extend
for a distance of 15 cm from the pectinate line. It
originates at the lower end of the sigmoid mesocolon, at the termination of the mesentery and is
partially invested by peritoneum in its upper two
thirds, the lower third being retroperitoneal. The
level of the peritoneal reflection has been stated
to lie at approximately 5.5 cm from the anal verge
in females and 7.5 cm in males [3].
The rectum should be divided into two compartments when considering the risk of mesorectal
spread of tumour (Fig. 1). These do not strictly
agree with the anatomical description of the
rectum stated above, with respect to its length and
the height of the peritoneal reflection. The lower
compartment is totally below the peritoneal reflection and is therefore encircled by a circumferential or lateral surgical plane of resection.
This segment has been noted to occupy a variable
distance above the pectinate line ranging from 4

128

proximity to the circumferential margin in this


area; but such spread may happen in either lower
or upper segment tumours.
Above the upper segment, the mesentery of
the colon commences and marks the start of the
sigmoid colon. The sigmoid colon is totally
covered by peritoneum and therefore not at risk
of retroperitoneal spread, although peritoneal
penetration may occur here as in other areas of
the colon. The term recto-sigmoid should be
abandoned as this region does not exist anatomically and its use may distract the surgeon and
pathologist from considering the likelihood of
circumferential resection margin involvement. It
should be replaced by a strict definition of the
upper segment of the rectum, though again this
can only be determined by direct inspection at
surgery or on pathological examination of the
excised specimen.

Method

Fig. 1. The anatomy of the rectum. Posterior aspect of the


rectum to show the lower segment below the peritoneal reflection and the retroperitoneal surface of the upper segment
above it (modified from Gray's AnatOmy edited by
Williams PL, Warwick R and reproduced by permission of
Churchill Livingstone)

to 18cm in resected specimens (Quirke, unpublished observations). The upper segment,


starting at the peritoneal reflection is covered by
peritoneum on at least part of its anterior surface
and with increasing height above the pectinate
line the peritoneal investment gradually increases
and the retroperitoneal surface is lost. The upper
limit of this segment may extend up to a height of
25 cm from the pectinate line (Quirke, unpublished observations). Tumours which lie posteriorly in the upper segment of the rectum are at
risk of local recurrence because of their retroperitoneal aspect. This area is also important as it
provides a site where spread of tumour through
the circumferential resection margin may occur
from metastases within the main lymphatic or
vascular chains. These structures lie in close

The resected specimen is received fresh, opened anteriorly and


pinned under gentle tension to a cork board for fixation in
formalin. After fixation the peritoneal reflection is identified
and the relative position of the turnout noted, i.e. below,
partially covered by peritoneum or totally covered by peritoneum. Areas covered by peritoneum are inspected for
serosal penetration and if apparent are sampled separately.
Tumours completely covered by peritoneum are handled in
the routine manner for colonic specimens whereas those with
a retroperitoneal component are subjected to close scrutiny
for circumferential margin involvement by tumour. The
site of the tumour is sliced as thinly as possible (Fig. 2),
including up to two cm above and below, and laid out on a
flat surface for macroscopic inspection (Fig. 3).
The extent of the tumour involvement of the perirectal
tissue is assessed with particular attention being paid to the
circumferential resection margin. The maximum extent of
tumour spread from the outer limit of the muscularis propria
is measured by ruler (Fig.4); this should be to the edge of
tumour's greatest distance of penetration from the muscular
wall, be it direct (Fig. 3), discontinuous (Fig. 5), vascular
(Fig. 6) or lymph node involvement (Fig. 7). Area(s) of involvement can usually be seen by naked eye and any suspicious area should be sampled for histology. One block may
be sufficient but up to six might need to he taken in cases with
extensive spread before it is possible to be certain that all the
margins are free of tumour. On average four blocks will suffice
for the majority of tumours. The circumferential resection
margin of the block should be marked with India ink to
demarcate it on histology and rule out false positive tumour
involvement of a tissue margin caused by poor embedding
practice.
The specimen is now turned over such that the mucosal
aspect faces downwards and the retroperitoneal/mesenteric
face is upwards. The C2 node, is identified and sampled and
the whole of the specimen, from the proximal margin, i.e. that
nearest the surgical ligature of the inferior mesenteric artery,
down to the previously excised tumour segment, is serially

129

Fig. 2. Serial slicing of the tumour from the


mucosal aspect. Slicing should be continued for
two cms above and below the tumour (not shown)
Fig. 3. Display of serial slices for macroscopic
examination. An arrow marks the slice showing
spread to the circumferential margin. Note also
the irregularity of the surgical resection margin

Fig. 4. Measurements made on tumour slice


showing maximal spread are: A, distance from
mnscularis propria to outermost limit of tumour;
B, distance from tumour edge to circumferential
margin, and/or C, distance from a satellite deposit
of tumour or involved lymph node to margin

sliced down to the external aspect of the muscularis propria.


Similarily the segment of the rectum below the tumour is also
serially sliced. Whilst incising the mesentery and mesorectum,
lymph nodes and tumour deposits should be identified and
sampled. Metastases and lymph nodes adjacent to the circumferential margin should be sampled en-bloc with the resection
margin which again should be identified by painting with
India ink.
Lymph nodes greater than one cm from the circumferential resection margin or present in the mesentery of the sigmold colon may be sampled in a routine fashion. If the tumour is close to the distal resection margin (i.e. < 2 cm away
or in a bulky or poorly differentiated tumour < 5 cm away)
then of course this margin should also be sampled.
Accurate measurement of the minimum distance between
tumour and the circumferential resection margin should be
performed by microscopy on the haematoxylin and eosin
stained slide using the Vernier scale on the microscope stage.
Shrinkage of tissue occurs during processing but this does not
materially affect the accuracy of this measurement. Assessment by microscopy is preferred as a florid peri-tumoral in-

flammatory reaction or fibrosis will lead to an overestimate of


macroscopic tumour spread. Macroscopic measurements are
accurate enough for the distance from the muscular wall to the
edge of the tumour as this measurement is only used when
comparing local recurrence rates between surgeons.

Past and current results


The original total embedding technique gave a
p o s i t i v e p r e d i c t i v e v a l u e for l o c a l r e c u r r e n c e o f
86% [1]. H o w w e l l t h e p r e s e n t m e t h o d c o m p a r e s
must await longer term follow-up but preliminary
r e s u l t s i n a p r o s p e c t i v e s e r i e s o f 50 p a t i e n t s w i t h
rectal carcinoma
dissected using the above
m e t h o d a r e p r o m i s i n g . F o u r o f six p a t i e n t s w i t h
c i r c u m f e r e n t i a l r e s e c t i o n m a r g i n i n v o l v e m e n t (ile.
t u m o u r w i t h i n less t h a n 1 m m o f t h e r e s e c t i o n

130

Fig. 5. Mounted tumour slice


showing an example of discontinuous spread (arrows)

Fig. 6. Mounted tumour slice


showing gross vascular invasion
extending out to the circumferential resection margin in a
tumour from the upper segment
(above the peritoneal reflection
but below the origin of the sigmoid
mesocolon)

Fig. 7. Tumour slice showing circumferential resection margin


involvement in the upper segment by a lymph node metastasis

131

margin) have developed local recurrence within


12 months, thus it is probably fair to suggest that
the above method is a suitable routine substitute
for total embedding of a tumour. The selective
sampling method can be performed in any
Pathology department and with practice it should
add less than 5 min to the dissection of a rectal
carcinoma specimen.

Surgical and therapeutic considerations


Since the initiation of this study it has become
apparent that a variable amount of tissue is
removed by different surgeons, especially around
the lowest 5 cms of the rectum. Whilst acknowledging that this is a difficult surgical area, every
effort must be made to excise a wide margin of
perirectal tissue. Surgical specimens are also
received showing remarkable irregularity of the
perirectal tissue which can compromise the
tumour margin (see Fig. 3). Measurement of the
distance from the muscularis propria to the edge
of the tumour is a useful independent parameter
in comparing local recurrence rates between
surgeons, since this will indicate whether a high
rate of circumferential resection margin involvement is related to a greater proportion of more
locally advanced carcinomas or is due to differences in surgical technique.

The ability to predict the likelihood of local


recurrence of rectal carcinoma now provides a
rational basis for a trial of post-operative radiotherapy in patients with a positive circumferential
resection margin. By selecting patients at particularly high risk such a trial would be statistically
powerful by removing those patients who are
cured by surgery and it would also avoid the
ethical question of delivering high dose radiotherapy to patients with no or very low risk of
local recurrence.

References
1. Quirke P, Durdey P, Dixon MF, Williams NS (1986) Local
recurrence of rectal adenocarcinoma due to inadequate
surgical resection. Histopathological study of lateral tumour
spread and surgical excision. Lancet 2:996-999
2. Heald RJ, Ryall RDH (1986) Recurrence and survival after
total mesorectal excision for rectal cancer. Lancet 1:
1479-1482
3. Williams PL, Warwick R (eds) (1980) Gray's anatomy, 36th
edn. Churchill Livingstone, London

Dr. Philip Quirke


Department of Pathology
University of Leeds
Leeds, LS2 9JT
UK

Col6i'ee/al
Disease

Int J Colorect Dis (1988) 3:132-134

9 Springer-Verlag 1988

Rare disorders

Sclerotherapy of rectal varices


J. Richon, R. Berclaz, P. A. Schneider and M.-C. Marti
Policlinique de Chirurgie et Clinique de Chirurgie Digestive, D6partement de Chirurgie, HSpital Cantonal Universitaire, Geneva,
Switzerland

Abstract. R e c t a l v a r i c e s r e p r e s e n t a r a r e c o n d i t i o n
e v e n in c a s e s o f p o r t a l h y p e r t e n s i o n . A c a s e o f
b l e e d i n g a n o - r e c t a l v a r i c e s p r e s e n t i n g as t h e first
m a n i f e s t a t i o n o f p o r t a l h y p e r t e n s i o n is r e p o r t e d .
T r e a t m e n t b y s c l e r o t h e r a p y w a s successful.

Case report
A 90-year-old woman with chronic cardiac failure was admitted as an emergency with massive rectal bleeding. Eight

Fig. 1. Rectal varices

months previously she had had an episode of minor rectal


bleeding.
Anorectal examination revealed two oedematous dilated
swellings at the anus measuring 3 cm diameter. There was
ulceration on the surface with subcutaneous varices extending
from the anus laterally towards the buttocks (Fig. 1). Sigmoidoscopy showed an oedematous mucosa with visible
dilated veins. The patient had ascites which was shown on
ultrasonography of the abdomen, It also revealed a cirrhotic
liver and splenomegaly. Superior mesenteric arteriography
was performed and this demonstrated during the venous
phase a normal superior mesenteric vein but the inferior
mesenteric vein was dilated to 11 mm diameter with retro-

Fig. 2. Arteriography (venous phase). MSV--superior mesenteric


vein; M I V - inferior mesenteric vein

133
Table 1. Rectal varices reported in the literature

Fig. 3. Arteriography (venous phase): rectal varices

grade flow (Fig. 2) filling massive rectal varices draining into


the caval system (Fig. 3). An attempt was made on two
occasions to treat the lesions by direct surgical ligation at the
site of ulceration without success. Given the age and poor
general condition of the patient major surgery was contraindicated leaving sclerotherapy as the only alternative treatment.
All varices were injected with ethoxysclerol.

Comment

Haemorrhoids and rectal varices are different


conditions [1, 2]. Haemorrhoids arise from the
anal vascular cushions [3] and contrary to previous opinion [4, 5] they are not related to portal
hypertension. Despite the anatomical communication between systemic and portal systems in the
anal canal the incidence of haemorrhoids in
portal hypertension is not greater than in the
normal population [1, 2, 6].
Bleeding from rectal varices can be continuous
or intermittent and is usually massive. It is m u c h
more severe in cirrhotic than in non-cirrhotic patients. The hydrodynamic role of portal hyperten-

Authors

Case
Bleed- Therapy
number ing

Faivre 1970 [14]

Yes

Iszak 1980 [11]


Johansen 1980112]
Huguier 1980 [10]
Mashiah 1981 [5]
McCormack 1984
[13]
Hamlyn 1974 [4]

1
1
1
2
4

No
Yes
Yes
Yes
Yes

1
2

No
Yes

Death (hemorrhagy)
Colonic resection
No treatment
No treatment
Ligation of varices
Mesenterico-caval shunt
Cryotherapy
Ligation of varices
No treatment

sion is probably made worse by any associated


coagulation abnormality [6]. Rectal varices are
rare [1] with only 15 cases previously reported in
the literature until 1985 (Table 1); they are
located in the submucosa of the distal rectum and
the anal canal, eventually extending to the
perineum, buttocks and the upper thigh [5].
Besides portal hypertension they may also occur
in the presence of caval obstruction due to
turnout or ligation [7, 8] and may even develop
after injection sclerotherapy of bleeding oesophageal varices [9]. They form a natural route of
decompression between superior, middle and
inferior haemorrhoidal veins. The rarity of this
condition in portal hypertension has been suggested to indicate an anatomical abnormality of
the inferior mesenteric vein [10, 11]. However,
arteriography of our patient showed massive dilatation of the inferior mesenteric vein without any
other vascular abnormality.
A portosystemic shunt is the only available
long term measure for reducing portal pressure
leading to decompression of the inferior mesenteric system and collapse of the varices [3, 12].
However, this procedure involves a considerable
operative risk and may not be justified as the
initial surgical treatment for bleeding occurring in
an accessible site [5, 10]. Ligation of the inferior
mesenteric vein increases the risk of developing
oesophageal varices and cannot be r e c o m m e n d e d
[4, 10]. Mashiah [5] has suggested cryotherapy as a
simple outpatient treatment which can be
repeated if needed and McCormack [13] and
Johansen [12] have advised transanal ligation of
the anorectal varices reporting haemostasis without recurrence for up to one year after treatment.
In one of these cases post-mortem examination

134

after death from an unrelated cause at 10 months


showed no rectal varices. Our experience with the
present patient has shown that injection sclerotherapy is a satisfactory alternative both to these
treatments and also to major surgery which is
often contraindicated on grounds of the poor
general condition of the patient.

References
1. Lebrec D, Benhamou JP (1985) Ectopic varices in portal
hypertension. Clin Gastroenterol 14:105-121
2. Nivatvongs S (1985) Suture of massive hemorrhoidal
bleeding in portal hypertension. Dis Col Rect 28:
878-879
3. Marti M-C (1982) La maladie hemorroidaire et son traitement. Rev Med Suisse Romande 102:359-368
4. Hamlyn AN, Morris JS, Lunzer MR, Puritz H (1974)
Portal hypertension with varices in unusual sites. Lancet
II:1531-1534
5. Mashiah A (1981) Massive bleeding from hemorrhoidal
varices in portal hypertension. JAMA 246:2323-2324
6. Jacobs DM, Bubrick MP, Onstad GR, Hitchcock CR
(1980) The relationship of hemorrhoids to portal hypertension. Dis Col Rect 23:567-569
7. Berson H, Woringer M (1961) Varices coliques chez une
malade ayant subi une ligature de la veine cave inferieure.
J Radio142:416

8. Bramwit D, Hummel W (1968) The superior and inferior


mesenteric veins as collateral channels in inferior vena
cava obstruction. Radiology 92:90- 91
9. Keane RM, Britton DC (1986) Massive bleeding from
rectal varices following repeated injection sclerotherapy of
oesophageal varices. Br J Surg 73:120
10. Huguier M, Belghiti J, Valette M, Leclere J (1980) Varices
rectales hemorragiques chez un cirrhotique. Gastroenterol
Clin Biol 4:211-214
11. Iszak EM, Finlay JM (1980) Colonic varices. Am J Gastroentero173:131-136
12. Johansen K, Bardin J, Orloff MJ (1980) Massive bleeding
from hemorrhoidal varices in portal hypertension. JAMA
244:2084-2085
13. McCormack TI', Bailey HR, Simms JM, Johnson AG
(1984) Rectal varices are not piles. Br J Surg 71: 163
14. Faivre J, Balabaud C, Beraud C (1970) Rectorragies
recidivantes per varices rectales. Arch Fr Mal App Dig
59:801-805
Accepted: 20 November 1987

Dr. M.-C. Marti


Policlinique de Chirurgie
H6pital Cantonal Universitaire
24, rue Micheli-du-Crest
CH-1211 Gen~ve
Switzerland

Col6i ec/al
Disease

Int J Colorect Dis (1988) 3:135-138

9 Springer-Verlag 1988

Current practice
Is the Kock pouch still a viable option?
A. M. Vernava, III. and S. M. Goldberg
Division of Colon and Rectal Surgery, University of Minnesota, Minneapolis, Minnesota, USA

The answer to the question, "Is the Kock pouch


still a viable option?" seems at first glance irrelevant. The advent of the ileo-anal reservoir
has captured the interest of physicians, surgeons and patients worldwide, and seems to
have relegated the continent ileostomy to a present role of historical interest only. Indeed, the
initial reports of high complication rates associated with the Kock pouch seemed destined to
discourage even the most adventuresome surgeon.
However, while surgeons such as ourselves have
been captivated by the restorative proctocolectomy, much progress has been made by Professor
Kock and his colleagues, and this has made such
a view shortsighted and misinformed. Any surgeon interested in providing a continent option
for the patient requiring proctocolectomy should be
aware of the current status of the continent
ileostomy, particularly of the significant decrease
in the late complication rates achievable using
contemporary surgical techniques (Table 1).

Development
The continent ileostomy was initially described by
Kock in 1969 to provide a continent alternative for
ileostomates and thereby obviate many of the
physical and psychosocial difficulties which accompany a conventional eversion ileostomy [1].
His initial considerations were revolutionary and
included an internal ileal reservoir for storage, a
nipple valve to maintain continence and the
elimination of a protruding stoma and external
appliances. To the extent that the operation provided continence, he and others were immensely
successful. Many authors, including Kock, report
almost universal improvement in the quality of

life of the patient following successful conversion


from a conventional to a continent ileostomy
[1-5]. Indeed, over 90% of patients who required
reoperation following continent ileostomy preferred surgical revision of the continent reservoir
than conversion to a conventional ileostomy [5].
The difficulty with early acceptance by surgeons of this procedure was its complexity and
the high complication rates requiring revisional
surgery. Even Kock initially reported a reoperation rate for complications as high as 54% [6].
Such complication rates did not decline rapidly;
there was a long learning curve and evolutionary
process associated with this procedure. Nevertheless, the operation survived because when it was
successful it provided excellent continence and
vastly improved the patients' lifestyle [1-5].
With the development of the continent ileostomy both early and late complications have
progressively declined. Initially reported as high
as 23%, the rates of early complications now
approximate to those of any other major intraabdominal bowel surgery, i.e. about 8% [3, 7, 8].
In addition the incidence of late complications
requiring revisional surgery has decreased from a
high of 54% to between 9.3% and 25% [6, 7, 9].
Operative mortality, originally reported as high as
4.3%, is now essentially zero [6, 7, 9, 10]. This
marked improvement in the overall operative
result has occurred through numerous modifications of surgical technique and postoperative care.

General complications

Nipple valve slippage


The initial reports on the continent ileostomy
have indicated nipple valve slippage, resulting in
faecal incontinence, to be the most common

136
Table 1. Current complicationsfollowingcontinent ileostomy

Pouch ileitis
Nipple valve slippage
Fistulae
Stomal stricture
Nipple prolapse
Stomal necrosis
Complicationsrequiring revisional
surgery

15-30%
3-25 %
0-10%
@ 10%
4-6%
?
12-25%

complication, occurring in 30-54% of patients


[6, 7]. Revisional surgery has been required in all
cases, and not infrequently even subsequent revisional surgery is necessary. This difficulty has
largely been obviated by the development of new
construction techniques including various combinations of mesenteric stripping, staple stabilisation of the nipple valve, scarification and fascial,
Marlex| or Mersilene slings [6, 7, 9, 10]. Perhaps
the most useful of these techniques is the application of four rows of staples placed longitudinally
along the nipple valve. Either a GIA, without a
knife, or a TA 55 may be used [6, 7, 10]. Kock
prefers the TA 55 because it produces less ischaemia [6]. Several authors advocate the use of a
sling placed at the base of the nipple valve to give
it support [7, 10]. Early reports on the use of
Marlex| and Mersilene were favourable. However, these implants since have been implicated in
the development of internal fistulae and their use
is discouraged [6, 7, 10]. Barnett has recently
described the use of intestine as a valve. He uses a
segment of intestine with its lumen in continuity
with the pouch which is then wrapped around the
base of the nipple creating a valve similar to the
Nissen fundoplication [9]. Such new techniques
have reduced the reported incidence of nipple
valve slippage to between 3% and 25% [6, 7, 10].
Fistula

Internal fistulisation usually occurs at the base of


the nipple valve and is problematic because it
renders the patient incontinent. Aetiologic factors
include local necrosis caused by silk sutures or
local ischaemia. Operative revision is required.
The current incidence of fistula formation is
between 0% and 10% [6-8, 10].
Stomal necrosis

According to Kock et al. [6] the improvement in


nipple valve stabilisation by stapling and mesen-

teric stripping has resulted in a small but unspecified n u m b e r of patients with ischaemic necrosis of the nipple valve. Further modification of
the technique by Kock [6] and Skinner [11],
including the use of the less traumatic TA55,
removal of the distal 10 staples prior to engagement of the stapler and less aggressive mesenteric
stripping has resulted in a reduction in the incidence of this difficult problem. The precise
impact of stomal necrosis on current stabilisation
techniques is difficult to assess since most current
authors do not report this complication.
Stomal stricture

Stricture of the ileostomy stoma is reported in up


to 10% of patients and is due to either retraction
of the terminal ileal segment or distal ischaemia
[10]. Revision of the stoma can usually be accomplished by a local procedure.
Pouch ileitis

Pouch ileitis is the most c o m m o n and troublesome


complication following continent ileostomy construction. It occurs in approximately 15%-30% of
patients and is manifested by abdominal cramps
and excessive ileostomy discharge leading to water and electrolyte disturbance and dehydration
[7, 10]. For unknown reasons polyposis coli patients are spared this complication; pouch ileitis
occurs exclusively in patients with colitis (ulcerative colitis and Crohn's disease) [7]. The diagnosis
is easily made by endoscopy or contrast roentgenography. The precise aetiology of pouch ileitis
is unknown although it is thought to be of
bacterial origin. The bacterial overgrowth theory
does not completely explain the condition of
pouch ileitis, as pouch ileitis is practically unknown when the operation is performed for familial polyposis coli [7]. Therapy consists of catheter reservoir drainage for up to several weeks
and antibiotics including sulfasalazine or metronidazole [6, 7, 10]. Only rarely does pouch ileitis
lead to surgical removal of the reservoir.
Operative considerations and postoperative care

It is not the purpose of this paper to describe current operative techniques for the construction of a
continent ileostomy; these are well documented
elsewhere [6, 8, 12]. However, the authors would
like to make several points which have been stressed

137

in the current literature. The oper~ttion is complex


and requires a significant learning period and
should therefore be performed by surgeons trained
in the procedure. For those without experience, an
institution adept at the procedure should be visited
.and the operation observed several times before
carrying it out. The novice is well-advised to
construct an ileostomy proximal to the reservoir.
This allows time for the pouch to heal and also
ameliorates the effect of any potential complications such as suture line dehiscence [7, 13]. Postoperative care is of paramount importance and
should include a period of no less than two weeks
of continuous pouch decompression with a tube
[6-8, 10]. The reader is encouraged to review the
referenced material for further detail.
Indications

The contemporary indications for continent ileostomy are essentially those for restorative proctocolectomy and include ulcerative colitis and polyposis coli (Table 2). An occasional patient with
another condition such as multiple colo-rectal
carcinoma may also benefit from the construction
of a Kock pouch. As alluded to earlier, the ileoanal reservoir has provided for many patients an
opportunity for restoration of the normal defaecation pathway and is now the preferred alternative
to conventional ileostomy [14, 15]. However, the
ileo-anal reservoir is not suitable for all patients
who require proctocolectomy. Impaired continence
and even patient preference are instances when
restorative proctocolectomy would be unsuitable.
In these patients the Kock pouch provides a
continent alternative to conventional ileostomy.
In addition the continent ileostomy provides an
acceptable therapeutic alternative to the resection
of 50 cm of small intestine in the patient with a
failed ileo-anal reservoir. The incidence of failure
of the ileo-anal reservoir, due to either pelvic
sepsis or a poor functional result, is between 5%
and 15% [14, 15]. An excellent description of the
technique used to convert an ileo-anal reservoir to
a continent ileostomy can be found in the article
by Hulten [16].
Contraindications

Crohn's disease is an absolute contraindication to


the construction of a Kock pouch (Table 3) owing
to the risk of recurrent disease and the consequent requirement to resect a large segment of
small intestine. Difficulties with histologic assess-

Table 2. Indications for continent ileostomy

Ulcerative colitis
Impaired continence
Patient preference

Polyposis coli
Impaired continence
Patient preference

Failed ileo-anal reservoir


Miscellaneous

Table 3. Contraindications to continent ileostomy

Crohn's disease (absolute)


Mesenteric desmoids
Obesity
Advanced age
Poor motivation

ment of the bowel at the time of operation account for the small number of patients with
Crohn's disease who undergo the continent ileostomy. Most authors would disagree with Bloom's
contention that patients having quiescent Crohn's
disease are suitable candidates for conversion to a
continent ileostomy [17]. Relative contraindications to the continent ileostomy include obesity
owing to mesenteric shortening, advanced age
and insufficient motivation.
Conclusion

Despite the success the Kock pouch has had in


providing continence for many patients requiring
ileostomy, the procedure has failed to gain widespread acceptance as a viable option for patients
requiring proctocolectomy. The reasons for this
include the complexity of the operation, the initial
reports of high complication rates associated with
the Kock pouch and the advent of the ileo-anal
reservoir. However, technical developments and
experience have led to a progressive decline in
both early and late complications. Early complications now approximate to those of any other
major intra-abdominal bowel operation. The incidence of late complications requiring revisional
surgery has decreased from 54% to 9.3%-25%.
Operative mortality, originally reported as high as
4.3%, is now almost zero. Although the ileo-anal
reservoir is the preferred alternative to conventional ileostomy, it is not suited to all patients. The
current status of the continent ileostomy and its
role in patients with inflammatory bowel disease
is reviewed. Any surgeon interested in providing a
continent option for the patient requiring proctocolectomy should be aware of the significant

138

improvement in the operative results of the continent ileostomy using contemporary surgical
techniques.
The answer to the question "Is the Kock
pouch still a viable option?" is therefore unequivocally yes. Recent advances in surgical technique and postoperative care'qaave decreased the
incidence of complications tO acceptable levels
when performed by experienced surgeons. Patients unsuited to restorative proctocolectomy and
those 5-15% of patients who have failed after
restorative proctocolectomy may desire a continent option. The Kock pouch still offers a
valuable alternative to conventional ileostomy in
these patients.

References
1. Kock NG (1969) Intra-abdominal "reservoir" in patients
with permanent ileostomy. Preliminary observations on a
procedure resulting in fecal continence in five ileostomy
patients. Arch Surg 99:223-231
2. Kock NG, Myrvold HE, Nilsson LD (1980) Progress
report on the continent ileostomy. World J Surg 4:143-8
3. Kock NG, Myrvold HE, Nilsson LO, Philipson BM (1981)
Continent ileostomy. An account of 314 patients. Acta
Chir Scand 147:67-72
4. Gerber A, Apt MK, Craig PI~ (1984) The improved
quality of life with the Kock continent ileostomy. J Clin
Gastroenterol 6:513-7
5. Mcleod RS, Fazio VW (1984) Quality of life with the
continent ileostomy. World J Surg 8:90-5
6. Kock NG, Brevinge H, Philipson BM, Ojerskog B (1986)
Continent ileostomy. The present technique and long term
results. Ann Chir Gynaecol 75:63-70

7. Hulten L, Svaninger G (1984) Facts about the continent


ileostomy. Dis Colon Rectum 27:553-7
8. Gerber A, Apt MK, Craig PH (1983) The Kock continent
ileostomy. Surg Gynecol Obstet 156:345-50
9. Barnett WO (1987) New approaches for continent ostomy
construction. J Miss State Med Assoc 28:1-3
10. Olsson SA, Fredlund P, Pettersson V, Petersson BG (1987)
Continent ileostomy. A follow up study of 60 patients.
Acta Chit Scand 153:119-22
11. Skinner DG, Lieskovsky G, Boyd SD (1984) Technique
for creation of a continent internal ileal reservoir (Kock
pouch) for urinary diversion. Urol Clin North Am 11:741
12. Nicholls RJ (1982) The continent ileostomy and restorative
proctocolectomy with ileal reservoir. Clin Gastroenterol
11:247-59
13. Hulten L, Fasth S (1981) Loop ileostomy for protection of
the newly constructed ileostomy reservoir. Br J Surg 68:
11-13
14. Rothenberger DA, Wong WD, Buls JG, Goldberg SM,
Christenson CE (1984) Restorative proctocolectomy with
ileal reservoir and ileonal anastomosis for ulcerative colitis
and familial polyposis. Dig Surg 1:19
15. Kelly KA (1985) Ileal pouch-anal anastomosis after proctocolectomy. Surg Rounds (January) p 48
16. Hulten L (1985) The continent ileostomy (Kock's pouch)
versus the restorative proctocolectomy (pelvic pouch).
World J Surg 9:952-9
17. Bloom RJ, Larsen CP, Watt R, Oberhelman HA (1986) A
reappraisal of the Kock continent ileostomy in patients
with Crohn's disease. Surg Gynecol Obstet 162:105-8

Dr. A. M. Vernava, III.


Division of Colon and Rectal Surgery
University of Minnesota
420 Delaware Street SE
UMHC Box 327
Minneapolis, MN 55455
USA

A nnouncement
Tripartite Meeting
The meeting will be held from 19 to 22 June 1989 at the Metropole Hotel, National Exhibition Centre, Birmingham, England.
For further information contact:
Great Britain: Ms. Judy Cook, Sections Office, Royal Society
of Medicine, 1 Wimpole Street, London W1M 8AE, UK.
Mr. R. H. Grace, FRCS, Consultant Surgeon, The Royal Hospital, Wolverhampton WV2 1BT, UK.

United States: Ms. Harriette Gibson, Executive Director,


American Society of Colon & Rectal Surgeons, 615 Griswold,
Suite :~ 1717, Detroit, Michigan 48226, USA.
Australia: Mr. J. Mackay, FRACS, Hon. Secretary, Section of

Colonic & Rectal Surgery, Royal Australasian College of Surgeons, College of Surgeons' Gardens, Spring Street, Melbourne
3000, Victoria, Australia.

138

improvement in the operative results of the continent ileostomy using contemporary surgical
techniques.
The answer to the question "Is the Kock
pouch still a viable option?" is therefore unequivocally yes. Recent advances in surgical technique and postoperative care'qaave decreased the
incidence of complications tO acceptable levels
when performed by experienced surgeons. Patients unsuited to restorative proctocolectomy and
those 5-15% of patients who have failed after
restorative proctocolectomy may desire a continent option. The Kock pouch still offers a
valuable alternative to conventional ileostomy in
these patients.

References
1. Kock NG (1969) Intra-abdominal "reservoir" in patients
with permanent ileostomy. Preliminary observations on a
procedure resulting in fecal continence in five ileostomy
patients. Arch Surg 99:223-231
2. Kock NG, Myrvold HE, Nilsson LD (1980) Progress
report on the continent ileostomy. World J Surg 4:143-8
3. Kock NG, Myrvold HE, Nilsson LO, Philipson BM (1981)
Continent ileostomy. An account of 314 patients. Acta
Chir Scand 147:67-72
4. Gerber A, Apt MK, Craig PI~ (1984) The improved
quality of life with the Kock continent ileostomy. J Clin
Gastroenterol 6:513-7
5. Mcleod RS, Fazio VW (1984) Quality of life with the
continent ileostomy. World J Surg 8:90-5
6. Kock NG, Brevinge H, Philipson BM, Ojerskog B (1986)
Continent ileostomy. The present technique and long term
results. Ann Chir Gynaecol 75:63-70

7. Hulten L, Svaninger G (1984) Facts about the continent


ileostomy. Dis Colon Rectum 27:553-7
8. Gerber A, Apt MK, Craig PH (1983) The Kock continent
ileostomy. Surg Gynecol Obstet 156:345-50
9. Barnett WO (1987) New approaches for continent ostomy
construction. J Miss State Med Assoc 28:1-3
10. Olsson SA, Fredlund P, Pettersson V, Petersson BG (1987)
Continent ileostomy. A follow up study of 60 patients.
Acta Chit Scand 153:119-22
11. Skinner DG, Lieskovsky G, Boyd SD (1984) Technique
for creation of a continent internal ileal reservoir (Kock
pouch) for urinary diversion. Urol Clin North Am 11:741
12. Nicholls RJ (1982) The continent ileostomy and restorative
proctocolectomy with ileal reservoir. Clin Gastroenterol
11:247-59
13. Hulten L, Fasth S (1981) Loop ileostomy for protection of
the newly constructed ileostomy reservoir. Br J Surg 68:
11-13
14. Rothenberger DA, Wong WD, Buls JG, Goldberg SM,
Christenson CE (1984) Restorative proctocolectomy with
ileal reservoir and ileonal anastomosis for ulcerative colitis
and familial polyposis. Dig Surg 1:19
15. Kelly KA (1985) Ileal pouch-anal anastomosis after proctocolectomy. Surg Rounds (January) p 48
16. Hulten L (1985) The continent ileostomy (Kock's pouch)
versus the restorative proctocolectomy (pelvic pouch).
World J Surg 9:952-9
17. Bloom RJ, Larsen CP, Watt R, Oberhelman HA (1986) A
reappraisal of the Kock continent ileostomy in patients
with Crohn's disease. Surg Gynecol Obstet 162:105-8

Dr. A. M. Vernava, III.


Division of Colon and Rectal Surgery
University of Minnesota
420 Delaware Street SE
UMHC Box 327
Minneapolis, MN 55455
USA

A nnouncement
Tripartite Meeting
The meeting will be held from 19 to 22 June 1989 at the Metropole Hotel, National Exhibition Centre, Birmingham, England.
For further information contact:
Great Britain: Ms. Judy Cook, Sections Office, Royal Society
of Medicine, 1 Wimpole Street, London W1M 8AE, UK.
Mr. R. H. Grace, FRCS, Consultant Surgeon, The Royal Hospital, Wolverhampton WV2 1BT, UK.

United States: Ms. Harriette Gibson, Executive Director,


American Society of Colon & Rectal Surgeons, 615 Griswold,
Suite :~ 1717, Detroit, Michigan 48226, USA.
Australia: Mr. J. Mackay, FRACS, Hon. Secretary, Section of

Colonic & Rectal Surgery, Royal Australasian College of Surgeons, College of Surgeons' Gardens, Spring Street, Melbourne
3000, Victoria, Australia.

Answers: (1) Failure to distend a narrowed segment in the very distal sigmoid colon, where the mucosal
folds are therefore more prominent - the so called "crumpled paper" or "tacked down" appearance.
Note the normal mucosa through this segment. (2) Pericolic disease which has adhered to the sigmoid
colon preventing complete distension. (3) (a) adjacent abscess (diverticular disease); (b) adjacent
inflammation (Crohn's disease); (c) adhesions (previous operation); (d) tumour (primary extracolonic invasion or mural metastatic deposits). (4) There are no sigmoid diverticula and hence a
diverticular abscess would be very atypical. Adhesions involving the colon would similarly be extremely
atypical. There is no "mass effect" indenting the colon to indicate an adjacent tumour. On the lateral
film anterior to the rectum is an atypical small bowel loop (outlined with air) and the combination of
the large bowel signs and this loop strongly suggests Crohn's disease. (5) Small bowel study.

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