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Human Reproduction Vol.18, No.1 pp.

162166, 2003

DOI: 10.1093/humrep/deg030

A comparative study of the morphology of congenital


uterine anomalies in women with and without a history of
recurrent rst trimester miscarriage
R.Salim1, L.Regan2, B.Woelfer1, M.Backos2 and D.Jurkovic1,3
1

Early Pregnancy and Gynaecology Assessment Unit, King's College Hospital, Denmark Hill, London SE5 8RX and 2Recurrent
Miscarriage Clinic, St Mary's Hospital, Paddington, London W2 1NY, UK
3

To whom correspondence should be addressed. E-mail: davor.jurkovic@kcl.ac.uk

Key words: congenital uterine anomalies/recurrent miscarriage/three-dimensional ultrasound

Introduction
Congenital uterine anomalies have been implicated as a cause
of adverse pregnancy outcomes (Acien, 1993; Raga et al.,
1997). Women with a history of infertility or miscarriage are,
therefore, often offered surgery in an attempt to restore uterine
anatomy and improve the prognosis for future pregnancies
(Pellicer, 1997). The reported prevalence of congenital uterine
anomalies in women with recurrent pregnancy loss varies
between 6 and 38% (Makino et al., 1992a; Clifford et al., 1994;
Acien, 1996). This wide variation is likely to reect differences
in the diagnostic criteria and techniques used for diagnosis.
Although most authors subscribe to the American Fertility
Society Classication of Uterine anomalies (American Fertility
Society, 1988), the nal diagnosis is based on the subjective
impression of the clinician performing the test. So far, no
published study has investigated the reproducibility of different
tests used in routine clinical practice for the diagnosis of
uterine anomalies.
Most studies of uterine anomalies have been performed on
women with either a history of infertility or recurrent
pregnancy loss. However, little is known about the prevalence
and reproductive implications of uterine anomalies in the
162

general population. In the absence of such data, it is difcult to


be certain whether uterine anomalies are indeed a major cause
of recurrent pregnancy loss. We have recently reported on the
prevalence and morphological characteristics of uterine anomalies detected on screening low risk women using threedimensional ultrasound (Jurkovic et al., 1997; Woelfer et al.,
2001). In this study, we have used the same technique and
diagnostic criteria to investigate women with recurrent pregnancy loss. The aim of the study was to investigate the
prevalence and severity of uterine anomalies in women with
recurrent pregnancy loss and then to compare the results to the
ndings in low risk women.
Materials and methods
A total of 522 consecutive women with a history of recurrent
miscarriage was prospectively recruited from the Recurrent
Miscarriage Clinics at St Mary's and King's College Hospitals,
London, between August 1997 and January 2001. All women were
screened for the presence of antiphospholipid antibodies and both
partners had peripheral blood karyotyping. All women also underwent
a transvaginal ultrasound scan as a part of the investigations into the
causes of recurrent pregnancy loss. The inclusion criteria were a
European Society of Human Reproduction and Embryology

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BACKGROUND: The true impact of congenital uterine anomalies on reproductive outcomes is unknown. The aim
of this study was to examine differences in the morphology of uterine anomalies found in women with and without a
history of recurrent miscarriage. METHODS: A total of 509 women with a history of unexplained recurrent miscarriage and 1976 low risk women were examined for the presence of congenital uterine anomalies by three-dimensional ultrasound. The anomalies were classied according to the American Fertility Society classication. In
addition, the size of fundal distortion (F) and the length of the remaining uterine cavity (C) were measured to calculate a distortion ratio (F/F+C). The ndings were compared with the measurements obtained in low risk women
with an incidental nding of uterine anomaly. RESULTS: In all, 121 anomalies were detected in the recurrent miscarriage group and 105 in low risk women. There was no signicant difference in relative frequency of various
anomalies or depth of fundal distortion between the two groups. However, with both arcuate and subseptate uteri,
the length of remaining uterine cavity was signicantly shorter (P < 0.01) and the distortion ratio was signicantly
higher (P < 0.01) in the recurrent miscarriage group. CONCLUSION: The distortion of uterine anatomy is more
severe in congenital anomalies, which are found in women with a history of recurrent rst trimester miscarriage.

Uterine anomalies and recurrent miscarriage

Both operators were also tested for the intra-observer variability of


measurement. The mean differences for measurements of F were
0.157 mm (95% limits of agreement from 2.54 to 2.23 mm) and
0.277 mm (95% limits of agreement from 2.13 to 2.69 mm) for
operators R.S. and B.W. respectively. The mean differences for
measurement of C were 0.138 mm (95% limits of agreement from
2.87 to 3.02 mm) and 0.110 (95% limits of agreement from 1.91 to
2.13 mm) for operators R.S. and B.W. respectively.
A database le was set up using Microsoft Excel for Windows
(Redmond, WA, USA) to facilitate data entry and retrieval. Statistical
analysis was performed using SPSS for Windows (Version 6.0; SPSS,
Inc., Chicago, IL, USA). Student's t-test was used to compare the
mean ages of the women and septum length or depth of fundal
indentation, in arcuate uteri, and distortion ratio. Pearson's c2-test was
used to compare relative proportions of various types of uterine
anomalies between control and recurrent miscarriage groups. The
MannWhitney test for non-parametric data was used to compare the
differences in proportions of women who had been pregnant, rst
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history of three or more consecutive unexplained pregnancy losses


before 14 weeks gestation. The control group consisted of 2034 premenopausal women without a history of infertility of recurrent
miscarriage who were referred for an ultrasound scan for a variety of
indications unrelated to reproductive outcomes. Exclusion criteria in
both groups of women were an ongoing pregnancy, presence of
uterine broids distorting the uterine cavity, previous hysterectomy or
myomectomy and inadequate visualization of the uterine cavity. The
study was approved by the Research Ethics Committees of both
institutions, and informed consent was obtained for the trial from all
participants.
Two-dimensional ultrasound was used rst to screen for congenital
uterine anomalies. Uterine anomalies were suspected when there was
evidence of duplication of uterine cavity or when the interstitial
portion of either Fallopian tube could not be seen. All women with
suspected anomalies were then examined by three-dimensional
ultrasound (Combison 530 3-D Voluson, Kretztechnik, Zipf,
Austria). In order to obtain three-dimensional ultrasound images, the
uterus was visualized in the longitudinal plane. A three-dimensional
ultrasound volume was then generated by the automatic sweep of the
mechanical transducer. The acquired volumes were in the shape of a
truncated cone with the depth of 4.38.6 cm and a vertical angle a =
90. The volumes were immediately stored on removable hard disk
cartridges (Magneto-Optic 3.0, 640 MB; Olympus Optical Co.,
Hamburg, Germany). The analysis of uterine morphology was then
performed online using the technique of planar reformatted sections
with the interstitial portions of the Fallopian tubes as reference points
(Jurkovic and Aslam, 1998). In all cases, the ultrasound operator was
aware of the clinical diagnosis of the woman being examined.
Congenital uterine anomalies were classied in accordance with the
modied American Fertility Society Classication (Woelfer et al.,
2001). In addition, in each case of arcuate and subseptate uterus a
distance was measured between the midpoint of the line joining the
two internal tubal ostia and the distal tip of fundal indentation or
uterine septum. Further measurements were then taken from this point
to the level of the internal os, this measurement representing the length
of the unaffected uterine cavity. The degree of distortion of uterine
architecture was then quantied by the ratio F/F+C, where F was the
length of the uterine septum or depth of the fundal indentation and C
was the length of the remaining uterine cavity (Figure 1).
Reproducibility of three-dimensional ultrasound measurement of
fundal indentation/septum length (F) and the residual normal cavity
length (C) was assessed in a randomly selected sample of 21 women,
which included eight arcuate and 13 subseptate uteri. In order to
examine inter-observer reproducibility, two experienced operators
(R.S. and B.W.) performed two blinded measurements of each
parameter. The mean differences for the measurements of F and C
between R.S. and B.W. were 0.157 mm (95% limits of agreement
from 1.137 to 1.451 mm) and 0.514 mm (95% limits of agreement
from 0.596 to 1.624 mm) respectively.

Figure 1. A coronal view of a septate uterus demonstrating the


normal outer uterine contour. The length of the septum (F) is
measured between its distal tip and the midpoint of the line
adjoining tubal ostia. The length of the residual uterine cavity
(C) was measured between the distal tip of the septum and the
internal os.

Table I. Demographics of women with uterine anomalies included in the nal data analysis

Mean age (range)


Total no. of women who were pregnant in the past (%)
Total no. of pregnancies
No. of pregnancies per woman (mean and range)
First trimester miscarriage (%)
Second trimester miscarriage (%)
Pre-term labours (%)
Live births (%)

Low risk
(n = 105)

Recurrent miscarriage
(n = 121)

32.4 (1848)
56 (53.3)
126
1.26 (09)
37 (29.4)
9 (7.1)
14 (11.1)
68 (53.9)

34.9 (2145)
121 (100)
491
4.0 (311)
411 (83.7)
35 (7.0)
9 (1.8)
36 (7.3)

<0.001
<0.001

<0.001
<0.001
0.020
0.423
0.012

163

R.Salim et al.

trimester miscarriage, second trimester miscarriage, pre-term labours


and live births.

Table II. Relative proportions of congenital uterine anomalies in low risk


women and those with a history of recurrent miscarriage
Uterine anomaly

Recurrent miscarriage n (%)

Low risk n (%)

Arcuate uterus
Subseptate uterus
Bicornuate uterus
Unicornuate uterus
Total

86 (71.1)
27 (22.3)
6 (5.0)
2 (1.6)
121 (100)

72 (68.6)
28 (26.6)
4 (3.8)
1 (1.0)
105 (100)

Discussion
In this study, congenital uterine anomalies were found in
23.8% of women with recurrent miscarriage. The most
common anomaly, however, was the arcuate uterus, whilst
major anomalies were present in 6.9% of women. Previous
studies of women with a history of recurrent early pregnancy
loss have shown a variable prevalence of congenital uterine
anomalies. In one study (Clifford et al., 1994), major uterine

Table III. Comparison of uterine morphology in all women with congenital uterine anomalies
Arcuate

No. of women
Mean septum length/fundal
indentation (mm)
Mean cavity length (mm)
Mean degree of distortion, a/a+b

Subseptate

Recurrent
miscarriage

Low risk

Recurrent
miscarriage

Low risk

86
5.57 (2.72)

72
5.42 (1.77)

0.383

NS

27
21.78 (5.42)

28
18.73 (8.76)

NS

NS

24.08 (5.44)
0.18 (0.004)

29.60 (6.09)
0.16 (0.004)

6.069
2.955

< 0.001
0.004

14.24 (5.34)
0.60 (0.12)

24.84 (11.43)
0.40 (0.25)

4.380
3.848

< 0.001
< 0.001

Values in parentheses are SD.


NS = non-signicant.

Table IV. Comparison of uterine morphology in nulliparous women with congenital uterine anomalies
Arcuate

No. of women
Mean septum length/fundal indentation (mm)
Mean cavity length (mm)
Mean degree of distortion, F/F+C
Values in parentheses are SD.
NS = non-signicant.

164

Subseptate

Recurrent
miscarriage

Low risk

56
5.84 (2.84)
23.61 (5.3)
0.2 (0.01)

42
4.77 (1.58)
27.65 (5.69)
0.15 (0.004)

2.376
3.765
3.628

0.019
0.001
0.001

Recurrent
miscarriage

Low risk

21
21.33 (21.33)
15.04 (5.25)
0.59 (0.12)

17
17.0 (5.72)
23.53 (12.4)
0.40 (0.28)

2.021
2.847
2.734

NS
0.007
0.010

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Results
A total of 509 women with a history of recurrent miscarriage
was included in the nal data analysis. Thirteen women (2.6%)
were excluded: three were found to have submucous broids,
which were signicantly distorting the uterine cavity, and nine
women had an irregular uterine cavity following previous
uterine surgery. An additional patient with the diagnosis of an
arcuate uterus tested positive for antiphospholipid antibodies
and therefore she was also excluded from the nal data
analysis. Of the 509 women who were included in the nal
analysis, 388 (76.2%) had a normal uterus and uterine
anomalies were diagnosed in 121 (23.8%) (Table I). In the
control group, satisfactory three-dimensional ultrasound
images were obtained in 1976 women (97.1%) with 43
women being excluded due to the presence of submucous
broids, 11 due to the presence of an intrauterine contraceptive
device and four women were excluded due to an irregular

uterine cavity following myomectomy. A conclusive diagnosis


of congenital uterine anomaly was made in 105 (5.3%) women.
The most common anomalies in both groups were arcuate
and subseptate uterus, which accounted for >90% of cases
(Table II). There was no signicant difference in the relative
proportions of congenital uterine anomalies in the two groups
of women. Morphological characteristics of uterine anomalies
in women with recurrent miscarriage were compared with the
control group. Depth of fundal indentation, in arcuate uteri, and
septum length, in subseptate uteri, were not signicantly
different between the two groups of women. However, in both
arcuate and subseptate uteri, the length of the normal uterine
cavity was signicantly shorter and the degree of distortion of
the uterine cavity was signicantly higher in women with a
history of recurrent miscarriage (Table III). In order to
eliminate a potential effect of parity on uterine morphology,
comparisons were also performed in the cohort of nulliparous
women only. This revealed similar results except that the depth
of fundal indentation in arcuate uteri in the recurrent miscarriage group was signicantly greater compared with that in low
risk women (Table IV).

Uterine anomalies and recurrent miscarriage

Makino et al. (1992b) tried to quantify the degree of


distortion of the uterine cavity by calculating the ratio between
the fundal distortion and the length of the uterine cavity on
hysterosalpinography. They found no association between the
severity of uterine anomaly and the number of previous
miscarriages. In contrast, the results of this study showed that
the degree of distortion of the uterine cavity in subseptate
uterus was higher in women with recurrent miscarriage,
compared with low risk women. This was mainly due to the
reduced length of unaffected cavity, rather than the increased
septum length. Differences between our and Makino's study
could be a result of different measurement techniques and
different denition of recurrent miscarriage in their study,
which included women with only two consecutive rst
trimester losses. Nevertheless our results indicate that the
distortion of the uterine anatomy in subseptate uterus is greater
in women with recurrent pregnancy loss. This nding supports
the hypothesis of septal implantation as a potential cause of
miscarriage as the likelihood of septal implantation increases
with an increasing ratio of septal size to functional cavity.
The prevalence of arcuate uterus in women with recurrent
miscarriage was 17%, which is signicantly higher compared
with the prevalence of 3.2% in low risk women (Jurkovic et al.,
1997). In addition, similar to the subseptate uterus, the
distortion of uterine cavity was greater in women with
recurrent rst trimester loss. The diagnosis of arcuate uterus
is difcult using conventional methods such as hysteroscopy or
laparoscopy and the diagnostic criteria are far from clear
(Golan et al., 1992). As a result, little is known about its
prevalence and clinical signicance. However, all studies
report an increase in adverse reproductive outcomes, mostly
second trimester loss (Tulandi et al., 1980; Acien, 1993; Raga
et al., 1997; Woelfer et al., 2001). The pathophysiology of
miscarriage in women with arcuate uterus remains unknown.
The only therapeutic intervention that has been proposed to
decrease the risk of miscarriage is the insertion of cervical
suture (Golan et al., 1990). However, this intervention is
unlikely to be helpful in women with a history of rst trimester
pregnancy loss.
This study also demonstrates the benets of using threedimensional ultrasound for the diagnosis of uterine abnormalities. The accuracy of three-dimensional ultrasound compared
with the traditional methods for the assessment of uterine
morphology has been assessed and was found to be satisfactory
(Jurkovic et al., 1995; Raga et al., 1996). The main advantage
of this technique is the ability to describe uterine anomalies in
quantitative terms and store ultrasound volumes permanently
in a form which enables further re-examination and independent evaluation of the diagnosis (Jurkovic and Aslam, 1998).
This provides an opportunity to pool diagnostic information
from a large number of diagnostic centres and to describe
anomalies using uniform diagnostic criteria. Accumulation of
such a large number of data may help to provide us with better
answers in the future about the clinical signicance and
optimal management of many different types of uterine
anomalies.
165

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anomalies were found in nine out of 500 cases (1.8%). Another


large screening study of 1200 Japanese women found major
anomalies in 4.6% of women (Makino et al., 1992a), whilst in a
study of 55 women (Tulppala et al., 1993), major uterine
anomalies were found in four cases (7.2%). The prevalence of
major uterine anomalies in our study is broadly in agreement
with these previous studies, which used invasive diagnostic
techniques to detect uterine anomalies. The lower prevalence
reported by Clifford et al. (1994) may be explained by the low
sensitivity of two-dimensional transabdominal ultrasound for
the diagnosis of congenital uterine defects.
The potential signicance of uterine anomalies in the context
of recurrent pregnancy loss cannot be established without
comparisons with the low risk population. In a previous
screening study of 1022 low risk women, we found major
congenital uterine anomalies in 2.3% of cases (Jurkovic et al.,
1997), which is comparable with the prevalence of 1.7% in this
series. Similar results have been reported by others who have
used a combination of invasive tests to screen for uterine
anomalies in women undergoing tubal sterilization. One study
(Ashton et al., 1988) found major anomalies in 1.9% of cases
using hysterosalpingography and hysteroscopy, whilst Simon
et al. (1991) reported the prevalence of 3.2% using a
combination of laparoscopy and hysterosalpingography. A
recent study (Byrne et al., 2000), using transabdominal twodimensional ultrasound to screen for anomalies, found prevalence of only 0.4% in 2065 low risk women. Similar to the
study by Clifford et al. (1994), this low prevalence is likely to
be the reection of the poor sensitivity of transabdominal twodimensional ultrasound for the diagnosis of uterine anomalies.
The results of these studies show that the prevalence of
major congenital uterine anomalies is ~3-fold higher in women
with history of recurrent miscarriage compared with the low
risk population. This suggests that congenital uterine anomalies may indeed be responsible for pregnancy loss in a small
proportion of women with recurrent miscarriages.
A recent literature review showed that the most common
major uterine anomaly in women with recurrent pregnancy loss
is subseptate uterus (Homer et al., 2000). The results of our
study are similar, showing that the subseptate uterus was the
most common major uterine anomaly, accounting for 77% of
cases. The subseptate uterus was also the most common
anomaly in low risk women, accounting for 7090% of cases
(Simon et al., 1991; Jurkovic et al., 1997; Raga et al., 1997).
Subseptate uterus accounted for 84% of major anomalies found
in low risk women in the present study, which is again
consistent with the data from the literature.
The pathophysiology of early pregnancy loss in cases of
subseptate uterus is explained by the inability of the relatively
avascular septum to provide adequate blood supply to the
developing embryo (Burchell et al., 1978). This view is
supported by histological evaluation of the septum, which
showed signicantly reduced vascular supply in relation to the
rest of the uterus (Nakada et al., 1989; Dabirasha et al., 1995).
If this theory is correct, then the likelihood of miscarriage
caused by septal implantation should increase with the severity
of the disruption of uterine morphology.

R.Salim et al.

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166

Submitted on February 11, 2002; resubmitted on July 12, 2002; accepted on


September 17, 2002

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