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Public Health Classics

This section looks back to some ground-breaking contributions to public health, reproducing them in their original
form and adding a commentary on their significance from a modern-day perspective. To complement this months
theme of the Bulletin, Mercedes de Onis reviews the 1956 paper by F. Gomez et al. on mortality in second and third
degree malnutrition. The original paper is reproduced by permission of Oxford University Press.

Measuring nutritional status in relation


to mortality
Mercedes de Onis1
In 1956, Federico Gomez and colleagues described
the clinical picture preceding death and the apparent
cause of death in malnourished children admitted to
the Nutrition Department of the childrens hospital
in Mexico City (1). The main purpose of their article, a
classic in the history of nutritional sciences, was to
provide information on clinical profiles of child
malnutrition and their associated risk of mortality.
What made this paper a landmark contribution was
the use of a simple anthropometric measurement
weight to develop an indicator (weight-for-age)
and, on this basis, a classification of varying degrees
of malnutrition. To do this, Gomez and his
colleagues relied on the average theoretical weight
they had found among Mexican children (2). Patients
were classified into three groups according to severity
of malnutrition, namely, first degree (7690% of the
theoretical weight average for the childs age),
second degree (6175%), and third degree (60% and less).
Their article linked this classification system to the
precise health outcome mortality and assigned
to varying degrees of malnutrition not only a clinical
value but also a prognostic significance. The authors
documented that the type of prognosis depended
mainly on the severity of malnutrition, measured as
weight deficit. Subsequently, reference to first, second
and third degrees of malnutrition became common
jargon not only among nutritionists, but also among
others working in the field of child health. With time,
the so-called Gomez classification (using the
Harvard reference values (3) and different cut-off
points, i.e., 80%, 70% and 60% of median) was used
widely both to classify individual children for clinical
referral and to assess malnutrition in communities.
The paper by Gomez et al. raised two
interrelated issues that are discussed below. The
1
Medical Officer, Department of Nutrition for Health and
Development, World Health Organization, 1121 Geneva 27,
Switzerland (email: deonism@who.int).

Ref. No. 00-0826


Bulletin of the World Health Organization, 2000, 78 (10)

first, which describes how to measure malnutrition,


considers such methodological issues as selecting
anthropometric indicators, choosing reference data
and establishing cut-off points. The second issue
concerns the relationship between malnutrition, as
measured by child anthropometry, and mortality.

Measuring nutritional status


The classification developed by Gomez et al. was
based on three prior selections: an anthropometric
indicator, a reference population with which to
compare the index child or community, and cut-off
points to classify children according to variable
degrees of malnutrition. Classifications developed
after Gomez have all relied on these same three
elements.

Anthropometric indicator
Nutritional status can be assessed using clinical signs
of malnutrition, biochemical indicators and anthropometry. Inadequacies in nutritional intake eventually alter functional capacity and result in many
adverse health outcomes that are distinct expressions
of malnutritions different levels of severity. Initially,
children adapt to inadequate diets through reduced
physical activity and slowed rates of growth. At
moderate degrees of malnutrition activity and growth
rates are affected to a greater degree and, in addition,
signs of wasting and some biochemical abnormalities
(e.g. reduction in serum albumin) begin to show. At
advanced stages of severity, all linear growth ceases,
physical activity is severely curtailed, body wasting is
marked, and clinical signs (e.g. oedema, hair and skin
changes) are noticeable. Anthropometry thus has an
important advantage over other nutritional indicators: whereas biochemical and clinical indicators are
useful only at the extremes of malnutrition, body
measurements are sensitive over the full spectrum. In
addition, anthropometric measurements are non-

World Health Organization 2000

1271

Public Health Classics


invasive, inexpensive and relatively easy to obtain.
The main disadvantage of anthropometry is its lack of
specificity, as changes in body measurements are also
sensitive to several other factors, including intake of
essential nutrients, infection, altitude, stress and
genetic background.
A childs body responds to malnutrition in two
ways that can be measured by anthropometry: a
deceleration or cessation of growth, which over the
long term results in low height-for-age or stunting;
and body wasting, which is a short-term response to
inadequate intakes, and commonly assessed by
weight relative to height. Height-for-age and
weight-for-height thus discriminate between different biological processes, unlike weight-for-age,
which could be low because of stunting (short
stature) and/or wasting (recent weight loss). The
Gomez criteria relied exclusively on weight-for-age
and hence could not discriminate between shortterm and long-term forms of malnutrition. Thus,
patients classified on the basis of weight-for-age
criteria are a mixed group in terms of their clinical
nutritional status. In post-Gomez classifications,
weight-for-height has emerged as a very important
indicator (4, 5) and, in fact, several authors have
identified low weight-for-height as the indicator of
choice for screening severely malnourished children
who are at increased risk of dying (69).

Reference population
Anthropometric values are compared across individuals or populations in relation to a set of reference
values. The choice of reference population to assess
nutritional status has a significant impact on the
proportion of children identified as being malnourished and, in turn, important programmatic implications for what to do about it (10). Much has been
written about growth references, but there remain
unanswered questions about the many factors that
determine human growth and indeed what constitutes normal growth. Gomez et al. used theoretical
weights among Mexican children (2), and later
nutrition classification standards have followed this
tradition by choosing reference values of their own. A
detailed account of the different growth references
used prior to the current international reference is
provided elsewhere (11). The US National Center for
Health Statistics (NCHS)/WHO international reference, in use since the late 1970s, has been found to
have important technical and biological drawbacks.
Consequently, WHO is conducting a multicountry
study aimed at developing a new growth reference. A
major innovation of this new effort is the use of an
internationally constituted reference population as
opposed to the strictly national samples in existing
references (12). The extent to which the new curves
differ from the current ones in shape and the spread
of values around the mean will affect the relationship
established using the old reference values
between child anthropometry and functional outcomes such as mortality.

1272

Cut-off point
Once an anthropometric indicator and a reference
population have been selected, it is necessary to
determine the limits of normality. There are three
classification systems for comparing a child, or a
group of children, to the reference population: Zscores (standard deviation scores), percentiles and
percent-of-median. The Gomez classification uses
the percent-of-median, which is a convenient
measure if the reference population distribution has
not been normalized. The percent-of-median is
simpler to calculate than a Z-score or percentile. In
the growth reference populations used prior to the
NCHS/WHO reference, the curves were generally
not normalized. However, in order to formulate the
software version of the current reference, the original
height and weight distributions were slightly modified by a normalization procedure (13). Since the
calculation of the percent-of-median ignores the
distribution of the reference population around the
median, the interpretation of any given percent-ofmedian value varies across age and height groups. For
example, depending on a childs age, 80% of the
median weight-for-age can be above or below -2 Zscores, resulting in different classifications of health
risk. In addition, common cut-offs for percent-ofmedian are different for the three distinct anthropometric indicators (5).
Since the late 1970s WHO has recommended
using the Z-score system because of its several
advantages (4). For population-based applications,
the software version of the NCHS/WHO reference
greatly contributed to the wide acceptance of the Zscore concept because it simplified the handling of
anthropometric data obtained from surveys and
nutritional surveillance. For individual applications,
however, there has been reluctance to adopt it
because the Z-score of an individual child is more
difficult to calculate than the percent-of-median.
While field staff generally have no difficulty learning
how to perform the calculation, they frequently
experience difficulties with understanding the concept of the Z-score. It is nevertheless generally
recognized that Z-score is the most appropriate
descriptor of nutritional status for both individual
and population-based applications, and health and
nutrition centres are gradually switching to its use.
Teaching how to use Z-scores, however, remains a
challenge, and imaginative and simple ways need to
be developed to convey this concept to health
professionals.
The use of a statistically defined cut-off point
(e.g. -2 Z-score) is not unique to anthropometry;
indeed, it is widely applied in many clinical and
laboratory tests. Nevertheless, it is important to bear
in mind that using a cut-off-based criterion to define
what is abnormal is somewhat arbitrary. In reality,
there are not two distinct populations one wellnourished and the other malnourished but rather a
continuous gradation of nutritional status. That is,
the risk of undesirable health outcomes such as
mortality does not change dramatically by simply
Bulletin of the World Health Organization, 2000, 78 (10)

Measuring nutritional status


crossing the cut-off line: significant deterioration
within the normal range may in fact carry greater
risk. For many purposes, the best descriptor of a
populations nutritional status is the mean, which in
less developed environments is usually shifted to the
left. This population approach resolves the
problem of focusing solely on the severely malnourished subpopulation falling below a certain cutoff. In most instances, the mild and moderately
malnourished subpopulations will be of greater
importance from a public health perspective because
there are many more children here than in the
severely malnourished category.
Predicted risk, which drives most interventions,
focuses on individuals, where the farther away from the
centre of the distribution an individual is, the greater
the risk of outcomes such as mortality. However, it is
inadequate for nutritional interventions to be driven
solely by an individual approach, limiting nutritional
support to children who fall below the accepted cut-off
level. This approach tackles only the tip of the
malnutrition iceberg. Ideally, both the population and
individual approaches should be combined so that
children who remain severely malnourished despite
population-based interventions are identified and
given special therapeutic attention (9).
Present practice often recommends the use of
a universal cut-off point, e.g. -2 Z-score, which is very
useful for population-based monitoring. However,
for individual applications in screening high-risk
children, cut-off points should be locally identified by
taking into account: the population-specific prevalence and nature of malnutrition; the cut-off point
below which children are shown to respond to
specific interventions; and the availability of resources, which will ultimately determine the proportion of children that the intervention can reach.

Child anthropometry and mortality


The point made by Federico Gomez and colleagues (1)
that severe malnutrition has a significant effect on
mortality is biologically plausible and hardly ever
disputed. Several other studies have documented that
severely malnourished children are at a much greater
risk of dying than are healthy children (14). An equally
important question is, how strong is the association
between mild or moderate malnutrition and the risk of
child mortality? An accurate answer is important for
the success of child survival programmes as the
number of children with mild and moderate malnutrition is several times greater than the number who are
severely malnourished (15). If mild and moderate
malnutrition are strongly associated with increased
mortality, efforts to reduce child mortality should be
directed to improving the nutritional status of all
children, instead of focusing primarily, or exclusively,
on severely malnourished patients.

Bulletin of the World Health Organization, 2000, 78 (10)

Few large prospective studies of mortality


during childhood have examined this issue. The one
by Chen et al. (16), who studied a cohort of
Bangladeshi children (1526 months at enrolment)
for two years, has been highly influential. Their
observations, which had important programmatic
implications, showed a pronounced threshold effect:
mortality increased with worsening nutritional status
when malnutrition was severe, but mild or moderate
degrees of malnutrition had little predictive power.
More recently, Pelletier et al. (17, 18) reviewed
28 community-based prospective studies on the
relationship between anthropometric indicators of
malnutrition and child mortality. The authors reached
two important conclusions. First, the accumulated
results were consistent in showing that the risk of
mortality was inversely related to anthropometric
indicators of nutritional status and that there was an
elevated risk even at mild-to-moderate levels of
malnutrition. Moreover, when considering the relative proportions of severe versus mild-to-moderate
malnutrition in populations, the authors showed that
the majority of nutrition-related deaths were associated with mild-to-moderate, rather than severe,
malnutrition. In programmatic terms, this implies
that strategies focusing primarily or exclusively on
severely malnourished children will be inadequate to
improve child survival in any significant way. To
make a substantial impact on mortality, the burden of
mild and moderate malnutrition in a population must
also be reduced. The second important result from
the review by Pelletier et al. is the confirmation that
malnutrition has a potentiating (multiplicative) effect
on mortality. Malnutrition, rather than acting in a
simple additive fashion, was in fact observed to
multiply the number of deaths caused by infectious
disease.
The substantial contribution to child mortality
of all degrees of malnutrition is now widely
recognized. As a consequence, current international
efforts such as the Integrated Management of
Childhood Illness strategy, which focuses on the
most important causes of child death, include a
number of key nutritional interventions (19). It was
pioneers like Federico Gomez and his colleagues who
laid the groundwork for todays approach by
developing the concepts that the international
nutrition community now takes for granted and
continues to refine in an effort to understand better
the magnitude of malnutrition and its impact on
health. Those who believe that assessing nutritional
status is a fundamental tool for protecting child
health are indebted to this pioneering work. n

Acknowledgement
I would like to thank Dr Adelheid Onyango for
her useful comments on the first draft of this
commentary.

1273

Public Health Classics

References
1. Gomez F et al. Mortality in second and third degree malnutrition.
Journal of Tropical Pediatrics, 1956, 2: 7783.
2. Gomez F et al. Malnutrition in infancy and childhood with special
reference to kwashiorkor. In: Levine SZ, ed. Advances in pediatrics.
New York, Year Book Publishers, 1955, VII: 131169.
3. Stuart HC, Stevenson SS. Physical growth and development.
In: Nelson WE, ed. Textbook of Pediatrics. 5th ed. Philadelphia,
WB Saunders, 1950: 1473.
4. Waterlow JC et al. The presentation and use of height
and weight data for comparing nutritional status of groups
of children under the age of 10 years. Bulletin of the World
Health Organization, 1977, 55: 489498.
5. Physical status: the use and interpretation of anthropometry.
Report of a WHO Expert Committee. Geneva, World Health
Organization, 1995 (WHO Technical Report Series, No. 854).
6. Bern C et al. Assessment of potential indicators for
protein-energy malnutrition in the algorithm for integrated
management of childhood illness. Bulletin of the World
Health Organization, 1997, 75: 8796.
7. van den Broeck J, Meulemans W, Eeckels R. Nutritional
assessment: the problem of clinical-anthropometrical mismatch.
European Journal of Clinical Nutrition, 1994, 48: 6065.
8. Trowbridge FL. Clinical and biochemical characteristics
associated with anthropometric categories. American Journal
of Clinical Nutrition, 1979, 32: 758766.
9. Management of severe malnutrition: a manual for physicians and
other senior health workers. Geneva, World Health Organization,
1999.
10. WHO Working Group on Infant Growth. An evaluation
of infant growth: the use and interpretation of anthropometry
in infants. Bulletin of the World Health Organization, 1995,
73: 165174.

1274

11. de Onis M, Yip R. The WHO growth chart: historical


considerations and current scientific issues. In: Porrini M, Walter P,
eds. Nutrition in pregnancy and growth. Basel, Karger, 1996
(Bibliotheca Nutritio et Dieta, 53: 7489).
12. WHO Working Group on the Growth Reference Protocol
and WHO Task Force on Methods for the Natural
Regulation of Fertility. Growth patterns of breastfed infants
in seven countries. Acta Paediatrica, 2000, 89: 215222.
13. Dibley MJ et al. Development of normalized curves for
the international growth reference: historical and technical
considerations. American Journal of Clinical Nutrition, 1987,
46: 736748.
14. Schofield C, Ashworth A. Why have mortality rates for severe
malnutrition remained so high? Bulletin of the World Health
Organization, 1996, 74: 223229.
15. de Onis M, Blossner M. WHO Global Database on Child Growth
and Malnutrition. Geneva, World Health Organization, 1997.
16. Chen LC, Chowdhury AKMA, Huffman SL. Anthropometric
assessment of energy-protein malnutrition and subsequent risk
of mortality among preschool aged children. American Journal
of Clinical Nutrition, 1980, 33: 18361845.
17. Pelletier DL, Frongillo EA, Habicht JP. Epidemiologic evidence
for a potentiating effect of malnutrition on child mortality.
American Journal of Public Health, 1993, 83: 11301133.
18. Pelletier DL. The relationship between child anthropometry
and mortality in developing countries: implications for policy,
programs and future research. Journal of Nutrition, 1994,
124: 2047S2081S.
19. Tulloch J. Integrated approach to child health in developing
countries. Lancet, 1999, 354 (suppl. II): 1620.

Bulletin of the World Health Organization, 2000, 78 (10)

MORTALITY IN SECOND AND THIRD DEGREE MALNUTRITION*


by

FEDERICO GOMEZ, M.D., RAFAEL RAMOS GALVAN, M.D., SILVESTRE FRENK, M.D., JOAQIUN CRAVIOTO
Mu:Noz, M.D., RAQUEL Cl!AvEz, M.D. AND JumTH VAzQUEZ, M.D.
(Nutrition Department, Hospital Infantil de Mexico, Mexico City.)

Malnutrition has been defined as a pathological condition of varying degrees of


severity, and diverse clinical manifestations, resulting from the deficient assimilation of the
components of the nutrient complex (G6MEz, 1955). This disease affects the physicochemical pattern of the tissues, reduces the defensive capacity to environmental aggressions,
lowers both the efficiency and the ability for work, and shortens life (EscUDERO, 1935 ;
TROWELL, 1948 ; DAVIES, 1952 ; ZUBIRAN, 1953).
The disease attacks with greater intensity certain social groups, and has a considerable
clinical importance.during critical stages of development of the child, such as infancy and
the pre-school age, which are characterized by rapid growth and high nutritional needs.
The causes responsible for malnutrition may be classified as primary- insufficient
food supply, or under-nutrition ; and secondary or conditioned- poor absorption,
increased excretion, increased requirements (JoLLIFFE, 1950). Most of the patients that
come to our Department are children suffering from chronic underfeeding resulting from an
insufficient diet, both in quantity and quality, to which they have been submitted for at
least three-quarters of their lives.
When underfeeding is moderate, or has acted for only a short time, the " nutritional
reserves " of the organism are only partially depleted, and malnutrition exhibits a mild
clinical picture, where the body weight ranges between 76-90 per cent. of the theoretical
average for the child's age. This, we call first degree malnutrition. As the effect of underfeeding becomes more serious, the picture becomes more marked, resulting in second degree
malnutrition. At this stage, the weight is between 61-75 per cent. of the theoretical average
for the age. The clinical picture, the prognosis, and the treatment become much more
complicated, and frequently the patient requires hospital care.
In third degree malnutrition, when the nutritional reserves are practically exhausted,
the maximum weight is never more than 60 per cent. of the average for the age ; while,
in addition, there are serious somatic and functional, including psychological, changes.
Treatment is very complicated and expensive, and the patient must be hospitalized. At
this stage, the disease has a high mortality rate - figures given by several authors ranging
from 30 to 60 per cent. (LEVINDER, 1912 ; GILLMAN, 1951 ; DEAN, 1954).
This classification of the disease - according to its varying degrees of severity and its
various clinical manifestations- which has been adopted by us since 1946, has oftentimes been criticised. Recently the Guatemalan research workers have introduced the
so-called "concept of Incipient Infantile Pluricarential Syndrome (pre-Kwashiorkor)"
(SCRIMSHAw, 1955). In other words, they also accept degrees of severity, but use a different
terminology.
We have conducted a careful study of both the clinical picture preceding death and of
the apparent cause of death in a large group of children suffering from chronic malnutrition
due to underfeeding seen between 1949 and 1952, and useful information has thereby
been obtained which will assist in assessing the prognosis and the correct form of treatment
in this type of case in the future. In due course, we shall also report on a second group
studied from 1953 through 1955.
MATERIAL
Our study consisted of 733 children admitted to the Nutrition Department of the Hospital Infantil de
Meldco, from 1949 through 1952. These cases had the following characteristics :
(a) Previous diet. All the children. had been submitted to a severe and prolonged restriction of food
(Table 1). The sources of protein were corn, beans, and wheat in small amounts. This diet was deficient
in lysine, tryptophane, isoleucine, valine, threonine, methionine and cystine. The biological value of the
protein mixture, calculated according to MITCHELL and BLOcK's formula (1946), was only 69 per cent.
Besides, it was consumed only in small amounts, consisting of 50 per cent. of the essential caloric, and
20-60 per cent. of the normal protein, requirements. (b) Sex incidence. 48 per cent. were males and
52 per cent. females. (c) Average age. 31 17 months. (d) Weight. 52 lO per cent. of the normal
weight for the age (Table II). (e) Height. This was less affected than weight, with maximum variations
of 15 per cent. (f) Clinical oedema. Present in 71 per cent and absent in 29 per cent. (g) Skin lesions
The incidence of these is shown in Table III. (h) Stigmata of malnutrition. Other signs of malnutrition
are shown in Table IV.

* Studies on the Undernourished Child No. XIV.


The Journal of Tropical Pediatrics, September, 1956
Bulletin of the World Health Organization, 2000, 78 (10)

1275

METHODS

Mortality was studied taking into consideration the time that elapsed between admission and death of the patient. Through the information obtained from the clinical
history and the physical examination, attempts were made to determine the cause of death
TABLE I.

Composition of the diet previous to hospitalization

Calories
Protein
Fat
Carbohydrate
Calcium
Phosphorus
Iron
Vitamin A*
Thiamine*
Riboflavin*
Nicotine acid*
Ascorbic acid*

*
TABLE II.

(GoMEZ, 1952).

Daily intake

Percentage of normal

700- 800
10- 30 gm.
5 - 15 gm.
80- 140 gm.
100 - 400 mgm.
200 - 500 mgm.
4 - 8mg.
2000 I.U.
400 - 1200 gamma
500 - 1500 mgm.
1 - 2.5 mgm.
Less than 50 mgm.

40- 50
20-60
10- 33
60- 85
10-40
20-50
50-80

Sufficient
Low
Low
Low

Vitamins calculated in raw foods.

Distribution of body weights in terms of percentage of the theoretical weight for the age.
Weight
31
41
51
61
71
81
91

to
to
to
to
to
to
to

40%
50%
60%
70%
80%
90%
100

of the normal
,
"
, "
"
, "
"
, "
"
, "

No. of cases

Percentage

75
241
268
105
20
3
2

10.50
33.75
37.53
14.70
2.80
0.42
0.28

"
"
"
"
in each case. The significance of some positive or negative signs due to malnutrition or
to other causes was also determined.
The data obtained were submitted to routine statistical analysis (MAINLAND, 1952) ;
a variant of the usual formula to calculate " X 2 " was used to estimate the possible influence
of certain clinical situations on mortality.
,

TABLE III.

Type of skin lesion


Dry hyperchromic skin
Very dry hyperchromic with mosaic
appearance
Follicular hyperkeratosis
Hyperkeratosis palmaris et plantaris
Fissures
Seborrhoea
Pellagrous erythema
Acute pellagrous dermatitis
Dyskeratotic hyperchromic lesions
Desquamating lesions in large flaps
Desquamating lesions in small flaps
Postdesquamation hypochromia
Hyperchromia along capillary circulation
Crusty lesions suggesting post-purpuric
lesions
Purpuric lesions
Perifolliculosis
Coldness and cyanosis of hands and feet
Marblization
Telangiectasis
Gangrenous lesions and eschars
Hypertrichosis
"Wet cloth" sign
Abdominal superficial circulation

* "t"

Incidence of skin lesions.


Without
clinical
oedema
(Percentage)

With
clinical
oedema
(Percentage)

90

94

38
20
48
3
42

46
26
37
8
49
47
40
83
21
37
26
8

13

18
50
8
13

15
1.4
6
24
1.4
62
11
1.4
11
24
27
6

11
28
11
82
18
6
18
20

"t "*

4.94
2.94
3.00
2.48
3.81
3.26

3.07

11

shows the significant degree of difference between children with and without clinical oedema.
" t " values below 2 were not reported, as they are not significant.

The Journal of Tropical Pediatrics, September, 1956


1276

Bulletin of the World Health Organization, 2000, 78 (10)

TABLE

IV.

Certain clinical features and laboratory investigations.


Percentage positive

Diarrhoea
Dehydration
Parental infection
Yomiting
Fever
Hypothermia

70
56
51
39
32
31

Intestinal parasites
Stool cultures
Shigellae
Salmonellae
Other agents
Mantoux test
Serological test for syphilis

28
28
14.3
9.4
4.5
4
3

REsULTS

(1)

70

Mortality.

eo

There were 234 deaths in the 733


cases studied, which gives a mortality of
31 per cent. Fig. 1 shows the number of
deaths that occurred during the first 14
days.

Ill

FIG. 1.
Number of deaths observed
during the first two weeks after
admission in 733 cases of malnutrition
(Gomez, 1955).

so

~40
...
0

Ill:

During the first 48 hours, there


were 105 deaths (44 per cent.). There
was a definite difference between the
mortality rate on the first day (29 per
cent.), and on the second day (15 per
cent.). Eliminating the deaths which
occurred during the first 48 hours,
the mortality is reduced to 129 deaths
out of 629 cases (20 per cent.).
(2)

~ 30

z 20
10

e
a
10
DAVS ELAPSED

12

14

Probable causes of death.

Water and electroyte imbalance was evident in 48 children out of 69 who died within
the first 24 hours. Acute broncho-pneumonia, either alone or combined with water and
electrolyte imbalance, was responsible for death in another group of 35. On the second
day, the mortality rate dropped to 36- out of these, there were 21 with disturbance of
water and electrolyte metabolism and 18 with acute bronchopheumonia, or a combination
of both.
Between the third and the seventh days, there were 76 deaths, and again electrolyte
and fluid imbalance (50 cases) alone or combined with acute bronchopneumonia (35 cases),
was considered to be responsible (Table V).
TABLE

V. Distribution of mortality by weeks.

Weeks

1st.

2nd

3rd.

4th.

Late cases

Number of cases

181

29

10

With fluid and electrolyte


imbalance
With bronchopneumonia

119
88

20
14

5
5

3
6

0
3

47

52

20

9
27
26

1
5
3

2
0
3

2
2
0

3
3
4

Fluid and electrolyte imbalance alone


Combined with bronchopneumonia
Fluid and electrolyte imbalance with other causes
Bronchopneumonia with
other causes
Bronchopneumonia alone
Other causes

September, 1956, The Journal of Tropical Pediatrics


Bulletin of the World Health Organization, 2000, 78 (10)

1277

Effect on mortality of certain clinical features found on admission.


(a) Weight. The death rate in 120 cases of second degree malnutrition was 22.6
per cent.; while in 544 cases of third degree malnitrition, it reached 33.53 per cent. The
significant statistical difference is : t = 2.3 (Table VI).
(b) Clinical Oedema. The gross mortality in patients with clinical oedema was
29.67 per cent., and in those without this sign it was 35.98 per cent. -the difference was
not statistically significant. On further analysis of these cases by the elimination of deaths
that occurred within the first 48 hours, the mortality was found to be 20 per cent. and
22.6 per cent. respectively, with "t" = 0.74 (Table VI).
(c) Skin lesions of "pellagra." The statistical significance on mortality of cases
with lesions of " pellagra," may be seen also in Table VI.

(3)

TABLE VI.

Effect on mortality of certain signs of malnutrition found on admisiosn.

Clinical groups

No. of
cases

Total
mortality
Percentage
deaths

Second degree malnutrition

128

22.65

Third degree malnutrition

584

33.53

With clinical oedema

519

29.67

"t ''*

Early mortality
(1st--48 hrs.)
Percentage
deaths

Percentage
deaths

"*

5.47

"t "*

18.18
2.80

2.30

0.80

14.70

21.50
20.00

12.13
1.85

1.67
Without clinical oedema

214

35.98

17.29

With " Pellagra "

465

31.70

12.25

Without " Pellagra "

268

31.40

"t

Late mortality

0.74

22.60
18.60

1.62

0.09
16.05

0.93
21.80

A value of " t " above 2 shows significant differences.

According to these data, in our clinical material the groups with and without pellagra,
and with and without oedema, showed no difference in mortality ..
Effect on mortality of certain clinical features not due to malnutrition found on admission.
(a) Fluid and electrolyte imbalance. Table VII demonstrates the differences in
mortality between children suffering from an obviously upset water and electrolyte balance
on admission, and those who did not. The presence of this type of disturbance has an
obvious effect on the mortality rate.
(b) Diarrhoea. The possible influence of this symptom was also considered and it
was studied in children without fluid and electrolyte imbalance, but with diarrhoea on
admission. Table VII shows that the difference in mortality rate between children with
and without this symptom is significant, though less so than when comparing the presence
and absence of dehydration.
(c) Bronchopneumonia. The differences in mortality were analysed only in those
cases where the cause of death was an acute pulmonary process, present since the time of
admission, but without a clinically evident fluid and electrolyte imbalance (Table VII).
The difference between both groups is significant.

(4)

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TABLE VII. Effect on mortality of some clinical signs found on admission, not directly due to malnutrition.

Total mortality
Clinical groups

No. of
cases

With fluid and electrolyte


imbalance

Death
percentage

" t "*

Early mortality
(1st. --48 hrs.)
Death
percentage

" t ,,..

19.10

Late mortality
Death
percentage
31.53

411

44.00

Without fluid and electric imbalance

322

15.00

With diarrhoea (but without


fluid imbalance)
Without diarrhoea or fluid
imbalance

152

21.40

168

10.70

With bronchopneumonia, but


without fluid imbalance

39

53.84

288

11.08

Without bronchopneumonia
or fluid imbalance

* A value of " t "

7.98

12.00

7.10

" t "*

12.00

9.36

2.60

4.86

above 2 shows significant differences.

DISCUSSION

As pointed out by DEAN (1954) and emphasized by BROCK(l9~5), the accurate comparison of mortality rates in cases of infantile malnutrition is difficult. Nevertheless, the high
mortality found in our department agrees with that reported by GILLMAN and GILLMAN
(1951), TRowELL (1954) and many others. The first mentioned authors point out that
gross mortality varies from one year to another, fluctuating from 30 to 50 per cent.,
" without any objective index of the gravity of the acute episode." It is obvious that in
our series water and mineral imbalances, and acute pulmonary processes, have a definite
influence on gross mortality, and this influence extends throughout the first two weeks of
hospital stay.
Independently of the cause of death, differences in weight have a significant effect
on mortality. There is a marked difference in mortality during the first 48 hours between
children with second degree malnutrition, and those with third degree. With these findings,
the classification of malnutrition by degrees acquires, not only a clinical value, but a definite
prognostic significance as well.
It has also been ascertained that other pathological disturbances, often found in severe
malnutrition, such as oedema and "acute" skin lesions, have no influence on mortality.
In view of the tendency other authors still have to consider as different entities cases with
or without clinical oedema and " acute " skin lesions, the above findings show that there
is probably no sound clinical basis for such classification.
In contra-distinction to the above, it has been shown that the difference in mortality
in children with clinically evident water and mineral imbalance, and in those without it,
gives a very high" t" (7.98), "p" being> 0.001. Similarly-, when diarrhoea was present
on admission, it also influenced mortality, possibly through the production of water and
mineral imbalance, which becomes established much more easily in children with serious
malnutrition than in healthy ones. There is evidence that malnutrition per se may be
September, 1956, The Journal of Tropical Pediatrics

Bulletin of the World Health Organization, 2000, 78 (10)

1279

responsible for a negative potassium balance (HANSEN, 1954), and this could partly explain
why diarrhoeal processes, however moderate, can bring about a marked derangement in
water and mineral metabolism in these children, and why successful treatment of this
situation is so difficult. The possible influence of the severity of undernutrition upon this
situation is illustrated by the higher early mortality in third grade malnutrition.
The statistical analysis of the cases of acute bronchopneumonia without clinically
evident fluid and water imbalance is especially difficult. The diagnostic signs, as pointed
out by TROWELL et al (1954) may be misleading. Moreover, bronchopneumonia by itself
may be responsible. for the production of acid-base disturbances, which may not be clinically
apparent. On the other hand, a process of this type may be the sole cause of death by
interfering with respiratory functions.
Malnutrition in itself may be regarded as a predisposing factor, but not as the direct
cause of such a high mortality. An answer to this acute problem may perhaps be sought
in a better understanding of the patterns of water and electrolyte metabolism in malnutrition, which obviously are different from those described in well-nourished children.
SUMMARY

The mortality rate in 733 malnourished children hospitalized from 1949 to 1952 has
been subjected to analysis. The significant influence on mortality of the degree of malnutrition and the presence of water and mineral imbalance, diarrhoea and acute bronchopneumopathy has been demonstrated. The existence of evident oedema or of skin lesions
has no influence on mortality. The significance of these findings has been discussed.
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Dean, R. F. A., Schwartz, R. (1954). Courier, 4, 292. Protein Malnutrition in Infants.
Davies, J. N. P. (1952). Ann. Rev. Med. 3, 99. Nutrition and Nutritional diseases. Stanford, Annual
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Hansen, J. D. L., Brock, J. F. (1954). Lancet, 2, 477. Potassium deficiency in the pathogenesis of
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Zubiran, S. and Gomez-Mont, F. (1953). Vitamins and Hormones. -Vol. XI, p. 97. Endocrine
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