CHAPTER
II
321
Background
to
the
Study
SCOPE OF THE PROBLEM OF MALNUTRI-TION IN PRESCHOOL CHILDREN
LMOST 60 years have elapsed since
Correa2 in Yucatai’i, Mexico, described
a pathological condition called culebrilla
which was present mainly in toddlers and
was associated with a deficient intake of
foodstuffs of animal origin. Since that time
reports from South America, India, Africa
south of the Sahara, the Balkan Peninsula,
China, Southeast Asia, the Philippines and
Central America had by 1952 shown the
widespread occurrence of the syndrome.3
The prevalence surveys of Brock and
Au-tret in Africa,4 Autret and Behar in Central
America,5 and Waterlow and Vergara in
Brazil,6 have made the size of the problem
apparent and have fully confirmed previous
impressions of high frequency which had
been based upon cases admitted to general
and to pediatric hospitals. As a
conse-quence, since 1955 protein-calorie
malnutri-tion has come to be recognized as a
condi-tion having worldwide importance for the
people’s health.
Although its incidence and causal
back-ground may vary, the syndrome is
associ-ated with the same basic characteristics of
clinical and biochemical pathology in all
countries, and has regional variations of
only secondary importance.7 The literature
has grown steadily and many reviews of
protein-calorie malnutrition have appeared
over the last two decades. Of particular
value for providing a detailed picture have
been those of Waterlow, West Indies 1948,8
Meneghello, Chile 1949, Brock and Autret,
Africa 1952, Oomen, Indonesia
1953,’#{176}Go-palan and Ramalingaswami, India 1955,h1
Gomez, et a!. Mexico, 1953,12 Trowell,
Dav-ies, and Dean 1954,13 Behar et a!. 1953,14
Ramos and Cravioto 1953,15 Waterlow,
Cravioto and Stephen 1960, and Viteri, et
a!. 1964.16
PREVALENCE AND INCIDENCE OF MALNUTRITION
There are no fully valid estimates for
ei-ther the incidence or prevalence of
protein-calorie malnutrition. Hospital statistics
upon which most estimations have
de-pended are for obvious reasons of selection
bias of little or no value for the assessment
of incidence. In some regions it has been
stated that 50% oF all children admitted to
the pediatric wards are suffering from
mal-nutrition of some degree. However,
hos-pita! figures can only suggest whether a
dis-ease is rare, common or very common,
since without knowing the size and
com-position of the population served by the
hospital and the degree to which the
facili-ty is utilized, it is impossible to relate such
figures to the population at risk. Few field
surveys have been done on a large enough
scale to provide data for reasonably valid
inferences. An exception is the survey
car-ried out by Rao, et a!. in India in 1959, in
which over 4,000 rural children less than 5
years old were examined in their homes.17
The prevalence of severe protein-calorie
malnutrition, (i.e., number of cases in
rela-tion to the population at risk found at the
given moment of time), accompanied by
clinical edema was just under 1%. Since the
children studied by Rao were examined
only once, his prevalence figures are limited
to a single point in time. However, one may
assume, in accordance with clinical
experi-ence, that a child with severe protein
mal-nutrition either recovers spontaneously,
dies, or is removed to a hospital for
treat-ment within a month’s time. Making this
assumption it is reasonable to estimate, if
one assumes no seasonal variation in
preva-lence, that between 5% and 10% of the
chil-dren of preschool age would develop
clini-cally recognizable degrees of protein
40
330 a
Q.
w 20 a
10
1
MAGDALENA MA, 1948-1962 USA 1955
r
AGE-SPF:clFIc MORTALITY RATES FOR PR ESCHOOL ChILDREN IN .& VILLAGE IN RURAL (.;1kTEMAI.
AND IN TIlE UNITED STATES 1 day 1-7days 7-28days 1-5mOS. 6-llmonths
AGE GROUPS
Fic. 1. Age-specific mortality rates for preschool children in rural Guatemala and the United States.
MORTALITY
When the age-specific mortality rates for
preschool children in the United States, are
compared with those available for areas in
which protein-calorie malnutrition is
preva-lent, e.g., rural zones of Guatemala, it is
readily apparent that starting with figures
of almost equal value for deaths occurring
during the first day of life, the rates for the
United States show a rapid decline over
time as contrasted with the Guatemalan
figures which remain constant or increase
as the age of the infants advances18 (See
Fig. 1). The degree to which age during the
first year is differentially related to
mortali-ty rates is strikingly notable when the cross
cultural comparison is expressed as a ratio
of the respective rates (Table I).
The risk of death in the United States
de-clines sharply after birth, as soon as
perina-tal causes cease to be significant
determin-ers of mortality. Clearly, after the first
month of life, and even more so after the
first year, the chances of death are rather
small for the preschool child. In contrast, in
rural Guatemala the survivors of the
pen-natal period continue to be at a high risk
of dying during the whole first year of life
and remain at only slightly lessened risk for
the next 2 or 3 years. This pattern is not
unique to one country, but characteristic of
preindustrial communities.
An investigation of the causes of death
after the perinatal period shows that
respi-ratory and gastrointestinal disorders,
to-gether with intestinal parasites are the most
frequently reported causes in official
ords. Very seldom are deaths registered as
due to malnutrition. However, good
evi-dence indicates that this is largely an
arti-fact of reporting style and of death
registra-tion practices. Behar, et al.,’ through a
de-tailed investigation of each death occurring
over a period of 2 years in four rural
vil-lages of Guatemala, having mortality rates
representitive for those of the country as a
whole, .Iound that out of 109 deaths
occur-ring in children less than 5 years of age,
38 were typical cases of severe
protein-calorie malnutrition accompanied by edema
(kwashiorkor), and two were of severe
mal-nutrition unaccompanied by edema. In
other words, approximately 37% of all
deaths in children under 5 were
unques-tionably associated with severe
malnutri-tion. If one adds to this figure all other
cases in which malnutrition was an
impor-tant contributory factor, although not the
immediate or most important cause of
death, the evidence suggests that
malnutri-tion has played an important role in no less
than 50% of the total number of deaths in
preschool children.
At present it is well-known that deaths
due to malnutrition are customarily listed
under other causes. In part, official statistics
fail to reveal protein-calorie malnutrition as
a main contributor to the high rates of
mor-tality in preschool children, because, in the
vast majority of regions where malnutrition
is prevalent, medical certification of death
is minimal or absent. The laymen charged
TABLE I
Age Group
Rate per 1000
-‘
United Magdalena
States
Ratio of
Guatemala to
United
States
Less than I
dayold
lto7days
7to28days 28 days to 1 yr
lto4yr
13.8 21.3
14.9 77.8
29.5
10.0
7.0
2.1
7.3
1.1
1.3
3.0
7.0
10.6
with the responsibility for maintaining the
civil registers only rarely can or do make a
diagnosis of malnutrition. Moreover, since
in the terminal stage of illness, a large
num-ber of malnourished children come to
no-tice and die of acute electrolyte
distur-bances due to diarrhea,2#{176} or are cases in
whom death is precipitated by respiratory
infections, even in places with medical
certification many deaths due, in principal
part, to severe malnutrition are officially
entered as infectious diarrhea and/or
bron-chopneumonia.
It is of course important to recognize that
children living in preindustrial regions tend
to suffer more enteric infections and other
communicable diseases because of
inade-quate sanitary conditions. However, it has
been shown that the severity of the
conse-quences of these disease processes is
significantly related to the almost universal
antecedent presence of various degrees of
malnutrition. Thus Gordon, et a!. have
re-ported that the incidence of cases of severe
diarrhea in a rural zone of Guatemala
dur-ing the period February 1961 to June 1962
was 22.9% in well nourished children and
40.0% in third degree malnourished subjects
in the same age group.21 Similarly, Vega,
et a!.22 studying a measles epidemic found that the frequency and severity of bactcnial
complications, in children below the age of
5, increased in direct proportion to the sever-ity of malnutrition. It appears, therefore, that
although separately or in combination,
in-fection and malnutrition, as important
causes of death have been decreasing in
highly industrialized countries, in the
prein-dustrial areas of the world they continue to
be responsible for the largest proportion of
the total number of deaths.23
MORBIDITY
It is important to appreciate that at
pres-ent more children survive severe
protein-calorie malnutrition than die of it. Better
knowledge of the biochemical
character-istics of malnourished children together
with better means for early diagnosis of
and rapid assessment of the effects of
treat-ment of electrolyte disturbances and
infec-lions have played a major role in enhancing
survival. The increase in number of
sur-vivors is reflected in the fact that whereas
in 1952 approximately 30% of children who
came to medical attention with third
de-gree malnutrition died, less than 5% of those
affected with equal severity died during the
years 1962 to 1964.24 Thus, at present, the
great majority of children with
protein-cal-orie malnutrition do not die, and yield a
pool of survivors who may be handicapped
in a variety of ways and for varying periods
of time. The handicap may range from
transient effects to permanent alterations in
function.
When malnourished children start to
re-cover they do so with great rapidity at first.
The rate of change in weight and size is
very often twice or thrice the normal for
the chronological age. However, if
observa-tions are continued for a longer period it
becomes apparent that the initial growth
recovery rate is not excessive but is very
close to that seen in younger children who
are of the same size as the malnourished
subject. Later on in recovery, the growth
rate shows the periodic accelerations and
decelerations characteristic of normal
growth, but with a time lag in comparison
to the child who has not suffered early
mal-nutrition. ThereCore, the weight gain
ap-pears to be size dependent and not age
based.25
Pediatricians and nutritionists have often
been misled by the high rates of growth at
the beginning of the recovery period. They
have speculated that if this rate would
con-tinue the child will catch up and will attain
the size of a normal child. Unfortunately,
the few studies available indicate that
growth in length ceases at the usual
chrono-logical age having as a net result an
under-sized adult. At adolescence children from
areas where infantile malnutrition is preva
lent are shorter in stature than children
from the same age and ethnic group who
have grown up in more developed areas in
which acute or chronic malnutrition is less
prevalent.2633
Dean’s studies on the body weight and
re-habilitated cases show that after the child
has recovered, his body length remains
re-duced and his skeletal development
retard-ed in comparison to that of normal
individ-uals of the same age and ethnic group.34
Similar findings have been reported by
Bar-rera-Moncada who has followed
Venezue-lan children recovered from malnutrition
for periods of up to 10 years.35 The effects
of malnutrition during growth on the
ulti-mate proportions of body segments is
illus-trated by the data of Leitch,36 whose
analy-sis of the Carnegie-United Kingdom
Di-etary and Clinical Survey showed that leg
length was sensitive to expenditures on
food. Ramos-Galv#{225}n, too, has reported
abnormal ratios of body proportions in
school children living under conditions
which are conducive to the development of
chronic malnutrition in early infancy.
The effects of malnutrition are not
re-stricted to diminished size or altered body
proportions. There are numerous examples
of physiological and biochemical alterations
in malnourished children indicating that
malnutrition not only can arrest certain
as-pects of biochemical maturation but also is
capable of producing retrogressions to
ear-lier age-specific patterns of functioning.
Thus, when water content and distribution
in malnourished children are recalculated
on the basis of the age indicated by their
actual weight or height, it is apparent that
both content and distribution are “normal”
for adequately nourished younger children
whose norms for height and weight are
equivalent in magnitude to those of the
older malnourished individual. Similar
findings are obtained when the data for fat
absorption, plasma lipid concentrations,
changes in proportions of alpha and betaS
lipoproteins, modifications of cholesterol
concentrations in blood, and urinary
excre-tion of creatinine are plotted against the
age for height and/or the age for
weight.38’39
Immunologically, too, it is of interest that
children, when challenged antigenically
during recovery from malnutrition, give
re-sponses similar in magnitude to those
ob-tamed in normal infants of a younger age.4#{176}
Kumate, et al.,41 in 118 malnourished
chil-dren found a diminution of approximately
20% in the levels of hemolytic complement,
with all four components determined, c-i,
c-2, c-3 and c-4 showing similar decreases.
The correlation between complement level
and the degree of malnutrition, estimated
as the percentage of difference between the
expected weight for age and actual body
weight was statistically significant. Similar
results were obtained by Ramunni and
Moretti,42 and by Vasile.43 Unpublished
observations of Kumate, at the Hospital
In-fantil of Mexico have shown that 7-S
gamma-2-globulin is reduced in severe
mal-nutrition with average values in the
mal-nourished children of about 400 mg/iOO
ml, as compared with 1,000 mg/100 ml in
well nourished controls.
Protein metabolism is modified by severe
malnutrition and free amino acid
concen-trations in the blood plasma of children
affected with either marasmus or
kwashior-kor generally show an abnormally high
ratio of phenylalanine to tyrosine. A
similar set of findings based on the analysis
of urine in malnourished children, reported
by Cheung, et suggests the possibility
that the deprivation has resulted in a defect
in the enzyme system that subserves the
metabolic conversion of phenylalanine to
ty-rosine. The extent to which alterations in
normal biochemical maturation can be
pro-duced by malnutrition in humans, is
per-haps best illustrated by Dean and
Whitehead,46 who have been able to
dem-onstrate in preschool malnourished children
the absence or the marked reduction in the
ability to metabolize normally the aromatic
amino acids histidine, tyrosine and
phenyl-alanine. The abnormalities noted
corre-sponded to metabolic phenomena normally
present only in the newborn infant.
NERVOUS SYSTEM AND MENTAL DEVELOPMENT
Although impressive advances have been
made in the knowledge of the clinical and
mal-SUPPLEMENT
nutrition during the past 15 years, it is only
recently that investigators have become
concerned with the possibility that
significant lags in nervous system
matura-tion and in mental development may occur
in children who have suffered from
protein-calorie malnutrition in early childhood.
Probably, among many reasons, the
slow-ness with which concern for this possibility
has developed derives at least in part from
the fact that assessment of any residual damage to tile central nervous system that
may be produced by protein-calorie
malnu-trition involves long-term observations, and
studies of children at a considerable
dis-tance in time from the period of acute
ill-ness. However, such studies, though
dif-ficult to design and carry out, are
impor-tant not only because of their significance
for tile development of millions of children
affected by malnutrition all over the world,
but also because of the light which they
may shed on the neurophysiology and
neu-ropsychology of child development. In view
of these considerations it is disappointing
that the only laboratory established for the specific purpose of carrying out systematic
research on the relation of nutrition to be-havior, higher nervous activity and mental
performance was the Laboratory for the
Study of Higher Nervous Activity founded
by Makarychev in i948 as a part of the
In-stitute of Nutrition associated with the
Rus-sian Academy of Medical Science.
Unfortu-nately, the laboratory and its program were
discontinued in 1960 when the director
died.47
From a recent review made by Brozek48
of the Russian studies it is clear that these investigators have followed Pavlov’s school
which inferred “cortical dynamics” from the
properties of conditioned reflexes. The findings from these investigations suggest
that when intake of a variety of essential
nutrients is inadequate, changes in
condi-tioned reflexes occur in advance of the
de-velopment of clinical symptoms of severe
malnutrition, and are reflected in
modifica-tions of acquisition rate, maintenance imd
extinction. From the point of view of
pediat-rics, perhaps the most directly relevant work
is that of Alekseeva and
Kaplanskaya-Raiskaya4#{176} who have reported that protein
deficiency readily results, especially in
young children, in marked disturbances of
cortical function. The capacity to elaborate
new conditioned reflexes is said to be the
first function affected. However, as the
mal-nourished state continues even previously
well established reflex responses may be
depressed or abolished. In the course of
di-etary rehabilitation tile recovery of normal
ability to elaborate conditioned reflexes
dis-turbed as a result of deficiency is reported
to be slow, and is interpreted as reflecting
the slow normalization of metabolic
pro-cesses basic to the function of the cerebral
cortex. Andriasov and Makarychev5#{176}
through animal experiments have reported
a confirmation of the observations made in
children, and have emphasized the
significant effects of the protein content of
the diet on the functional status of the
cere-bral cortex, with particular reference to the
processes of internal inhibition and the
in-tensity of positive reflex organization.
In regions in which protein-calorie
mal-nutrition in children is widespread,
investi-gators have not tended to approach the
issue neurophysiologically. Rather than
ex-plore the question of the impairment of
mechanisms of brain functioning which
may result from deficient nutritive intake,
for which experimental studies have
pro-vided suggestive evidence,51 they have
at-tempted to answer the practical question of
whether the more readily noted reductions
in somatic growth and biochemical lag are
associated with reduced intellectual
compe-tence. Further, they have wished to know
whether such mental lags, when they have
been found, represent permanent changes
in functional effectiveness or are merely
transient phenomena which disappear with
nutritional recovery.
From the very first descriptions of
pro-tein-calorie malnutrition in children it was
clear that psychological disturbance was a
prominent feature of the clinical signs of
from different countries all showed that
apathy probably constituted the single most
common behavioral finding. The severely
ill, malnourished patients seemed to have
lost all the normal curiosity and desire for
exploration that is natural in a young child.
This condition of unresponsiveness is so
marked that renewal of interest in the
envi-ronment has come to be considered one of
the most reliable signs of improvement:
“The child who smiles is well on the way to
recovery.”3’525
It would, of course, be ingenuous to view
the observed apathy as the simple and
di-rect result of malnutrition. If one uses
Wilson’s56 attempt to distinguish four
cat-egories of apathy (primarily physiological,
primarily psychological, apathy at the
com-munity level, and apathy as a characteristic
of a regional culture), the apathy of the
protein-calorie deficient child can most
profitably be viewed as a mixed type.
Nu-tritional deprivation per se can and does
contribute to apathy and unresponsiveness
as is the case in experimental animals fed
on low-protein high carbohydrate diets.57
However, when noted clinically such
be-havior is never separable from possible
se-quelae to emotional deprivation and loss
which may be produced by the separation
which accompanies hospitalization. It has
been repeatedly stated that in most
com-munities where malnutrition is highly
prevalent the mother-child relationship
prior to weaning is very close and
frequent-ly includes the mother taking the nursling
with her everywhere she goes. This fact,
when considered together with the
observa-tions made by Geber and Dean58 that
re-covery is more rapid among infants whose
mothers show the greatest interest and
so-licitude, has been interpreted as suggesting
that separation from the mother may make
an important contribution to the behavioral
disturbance. In any event, the behavior of
the malnourished infant strikingly
resem-bles that described by Bowlby’9 in the 15 to
20-month-old healthy child who has been
abruptly separated from his mother by
hos-pitalization.
In considering psychological features of
severe malnutrition it is important to note
that in a high proportion of cases the
disor-der is closely associated in time with
wean-ing. In preindustrial societies the frequent
absence of effective and continued
mother-ing as reflected in the absence of a stable
surrogate and repeated “randomized”
change in the persons responsible for the
care of the weaned child may also play a
part in the production of apathy in those
communities in which this is a common
practice. Such a complication is particularly
likely at the time the mother shows the
evi-dent signs of a next pregnancy.6#{176} However,
despite the influence on behavior of these
non-nutritional general factors, as
Mene-ghello9 has pointed out, the
psychologi-cal changes in malnutrition are not
sim-ply a response to hospitalization or to
gen-eral maternal deprivation, since they are
present even if the child remains at home
and is most affectionately cared for by a
devoted, if nutritionally misguided, mother.
However, independently of whether the
cause of apathy is simple or multiple, it is
clear that during the development of
chron-ic malnutrition from the mild-moderate to
the severe case, failure to respond
ap-propriately to significant stimuli is reflected
in a progressive withdrawal from the
envi-ronment, and by progressive behavioral
regression. At the very least such changes
produce a period of experiential reduction.
It is, therefore, possible that although the
physical signs of bodily wasting are
per-haps more dramatic, the behavioral changes
may have greater developmental
impor-tance in the long run because of their
po-tential for interferring at critical steps6’
with the course of cognitive growth.
ELECTROENCEPHALOGRAPHIC STUDIES
Clinical electroencephalography as a
method for the assessment of the adequacy
of central nervous system functioning in
se-verely malnourished children has been
em-ployed by Sarrouy,#{176}’ Engel,63 Valenzuela,
and Nelson and Dean.64 On admission the
abnor-malities in tile form, frequency and
ampli-tude of electrical activity. Valenzuela, using
sedation by chloral hydrate, found the
rapid rhythm (waves with voltage of
100-150, and frequency of 18-26 per
sec-ond) characteristic of records obtained
from healthy children under the same
con-ditions to be absent in all his malnourished cases. On successful recovery from malnu-trition the EEG showed normalization, i.e.,
a tendency more closely to conform to that
of healthy children of the same
chronologi-cal age. The rate of recovery was rapid and,
in Valenzuela’s series, all abnormal features
of the EEG took no more than 40 days to
disappear.
Nelson and Dean64 found focal
distur-bances in the temporal areas of the brain in
approximately 11% of their malnourished
patients and have interpreted these as
in-dicative of special local sensitivity to a gen-eralized stage of intracellular overhydration
that is probably a very common feature of
severe chronic protein-calorie
malnutri-tion.65 The locus of disturbance in the
tem-poral lobe is as yet unexplained, but may
be a reflection of the lobe’s tendency to
react more readily to abnormal conditions
than is the case for other brain regions.
PSYCHOLOGICAL TEST STUDIES
MILD TO MODERATE DECREES OF
MAL-NUTRITION: In a preliminary study
Kugel-mass, Poull and Samuel66 analyzed the
effects of nutritional improvement on
men-tal performance in children who were
matched for chronologic age and
intelli-gence quotient (I.Q.) but who differed in
nutritional status. Two matched groups
each containing 50 children ranging in age
from 2 to 9 years were established. One was
identified as intellectually normal and well
nourished, and the other as intellectually
normal but malnourished. After a period
varying from 1 year to 33 years, during
which nutritional status was improved in
the malnourished group, psychological
testing was repeated. It was found that
whereas the average I.Q. of the initially
well nourished group was markedly stable,
that of the initially malnourished group
rose an average of 18 points following
im-provement in nutritional status.
Stoch and Smythe67 in South Africa,
using a semilongitudinal method, have
fol-lowed two groups each containing 21
Negro children. Eighteen of the children in
each group were between the ages of 10
months and 2 years and the remaining ones
between 2 and 3 years. At the beginning of
the study none of the children showed
evi-dence of organic disease apart from
gas-troenteritis that responded rapidly to
treat-ment. The essential difference between the
two groups was in their state of nutrition,
as judged by height, weight and head
mea-surements. The group considered better
nourished included children attending an
all-day nursery while both parents were in
full employment. At the nursery the
chil-dren received adequate meals and vitamin
supplements. The undernourished children
were seen for the first time at the age of
about one year. They were subsequently
examined at intervals of 6 to 12 months.
Al-though the families of the better nourished
group tended to be larger and with larger
incomes, less unemployment and a slightly
higher educational attainment, both groups
were considered to belong to the lowest
economic stratum of unskilled laborers with
minimal incomes. The intelligence
quo-tients of the parents of both groups were
very low with mean raw scores on the
Raven Matrices Test not significantly
dif-ferent.
The children under 2 years of age were
tested by using the Gesell Infant Scales of
Mental Development. From 2 to 6 years the
intelligence quotients were estimated by
means of the Merrill-Palmer Test adapted
for African children. Children over 6 years
of age were examined with the Individual
Scale of the National Bureau of
Education-al Research in South Africa, a test based on
the 1916 Stanford Revision of the
Binet-Simon Scale. Anthropometric
measure-ments were also repeated every time the
children were examined.
con-currently with lower values for height,
weight, and head circumference, the mean
intelligence quotient of the undernourished
group was well below the mean of the
bet-ter nourished group. The disparity between
the means remained relatively constant
throughout the observation period. A
difference of 22.62 points found at the time
of final testing was statistically significant at the 1% level. Interpretation of the finding
is made difficult by differences in nursery
school experience in the two groups.
Cross sectional studies of behavioral
de-velopment conducted in Uganda,68’69
Mex-ico7#{176}and Guatemala,71 using either the
Gesell technique or the Andre-Thomas
method for neuromotor assessment,72 have
shown that newborn infants in the
prein-dustrial regions of these countries have
scores in psychomotor and adaptive
de-velopment which are generally higher than,
and never below, those obtained in North
American or European children. The Gesell
tests, usually considered suitable only for
children over 4 weeks of age, can be used
with younger African, Mexican and
Gua-temalan children because their motor
de-velopment at 2 or 3 weeks of age is similar
to that of Western European infants 2 or 3
times as old. Interestingly, Nelson and
Dean64 have reported that
electroencephal-ograms of African newborn infants are also
suggestive of a greater degree of maturity
than usually found in the European
new-born child. Soon after birth, however,
chil-dren from these preindustrial areas begin to
show deceleration and by the ages of 18 to
24 months, their performance is often
below that shown by their European
con-temporaries.
If one applies Dean’s technique of
ex-pressing the Gesell Development Quotients
(Y) for a given age (x) on the basis of a
scale where 100 represents the performance
of the median “normal” North American or
European child of the same age as the child
being tested, the relationship between
quo-tients and chronological age can be
de-scribed by a curve of the type Y = ax for
the total span of 0 to 42 months. A
satisfac-tory approximation to this curve can be
ob-tained by fitting a series of straight lines
over subsets of small age intervals. When
this is done it is found that even children
who later develop kwashiorkor usually
de-velop well during the first months of life.
Later, when suitable supplements are not
provided at a time when the mother’s milk
no longer supplies the infant’s nutritional
requirements, weight and height
incre-ments begin to diminish. When the child is
completely weaned (which for most areas
of Latin America is usually between the
twelfth to twenty-fourth month) height
re-mains practically stationary and weight
may even show a slight decrease.
In six different communities, two of
typi-cal mestizos; one of Zapotec Indians, one of
Nahoa Indians in Mexico, as well as in two
communities of Cakchiquel Indians in
Gua-temala, high correlations between deficits
in height and weight and depression in
motor and adaptive developmental scores
were found. No systematic association
could be demonstrated between these
scores and ordinal position of the child,
cash income, crop income, parental
educa-tion, parental hygiene, and type of
hous-ing.7376
Ramos-Galv#{225}n has in the course of a
se-ries of cross-sectional and longitudinal
studies constructed the provisional tables of
weight and height for age of normal
Mexi-can children. When the actual weights
and heights of rural Mexican children
affected with mild-moderate protein-calorie
malnutrition were expressed as a
percent-age of the provisional standard related to
the children’s performance scores on the
Terman-Merrill test adapted to local
condi-tions, a positive correlation between height
and intellectual performance was found.
Further, it was found that mental age was
better associated with height age than with
chronological age in the malnourished
chil-dren. This finding strongly suggests a
con-current deceleration of somatic and mental
growth.78
SEvERE PROTEIN-CALORIE MALNUTRITION:
psy-chological test behavior of severely
mal-nourished children by means of the
Gesell technique. Performance in all the
fields of behavior tested gave lower
devel-opmental scores than the standard
calcu-lated for children of similar age and ethnic
group. In general, motor development
showed the least, and language
develop-ment the greatest retardation. It is possible
that the retardation effect was cumulative
since, as a rule, the older the child when
studied the more marked were the deficits.
Similar findings have been described for
Africa’s and for Mexico.79
Studies on the somatic growth of infants
living in Latin American communities with
a high prevalence of malnutrition and
in-fectious diseases have indicated that the
weight curves during the first 5 years of life
can be described in three well defined
phases.27 The first encompasses the period
of the first 4 to 6 months following birth. It
is characterized by weight gains similar to
those shown by normal full-term infants
born in highly industrialized countries. This
phenomenon is most apparent when gains
are not expressed as absolute values but as
percentages of birth weight. The second
phase extends from the sixth to
approxi-mately the thirtieth month. During this
pe-riod weight gains become progressively
smaller reaching their minimum between
the eighteenth and twenty-fourth month,
after which they show a tendency to rise
slowly but steadily. Finally, in the third
phase there is a return to incremental
val-ues normal for the chronological age.
Cra-vioto and Robles,8#{176} on the basis of animal
evidence have argued that the effects of
malnutrition on mental development, as
well as on ultimate size, in the mature
indi-vidual would vary as a function of the
peri-od of life at which the malnutrition was
experienced. They have predicted that
psychological deficit in severe malnutrition
would be most profound if the stress took
place during the first of the three different
age periods, i.e., in infants below 6 months
of age. From all the children admitted to
the Nutrition Ward of the Hospital Infantil
de Mexico, those classified as suffering
from third degree protein-calorie
malnutri-tion, as defined by the criteria of G#{243}mez,et al.20 and Bengoa8’ who include in the third
degree group all malnourished children
with pitting edema regardless of weight,
were selected for study. Immediately after
treatment of any infectious disease and
cor-rection of electrolyte disturbance, the
be-havior of the children was assessed by
means of the Gesell method. Tests were
re-peated at regular intervals of 2 weeks,
dur-ing the entire period that the children were
hospitalized. In all, serial information was
obtained on 20 children: 6 infants below 6
months of age, 9 between 15 and 29
months, and 5 between the ages of 37 and
42 months.
The results of the first test session
confirmed previous reports, since all
chil-dren were noted to have below age-norm
scores in all fields of behavior. As recovery
from malnutrition occurred, developmental
quotients increased in most of the patients
and the gap between normal age
expecta-tion and the actual performance of the
child progressively diminished for all
ex-cept those in the group whose age on
ad-mission was less than 6 months. These
younger malnourished infants showed no
tendency to “catch up” and increased in
de-velopmental age only by a figure equal to
the number of months they remained in the
hospital. In older children not all spheres of
behavior exhibited the same speed of
recov-ery. Language, which in general was the
function most affected, showed the slowest
rate of return toward normal age
expectan-cy. When the serial data for each child
were plotted against days of hospitalization it could be seen that the rate of behavioral
recovery from the initial deficit varied in
direct relation to chronological age at
ad-mission. The older the group the greater
the value of the slope. The slopes were
sufficiently steep, and progress in the first
two weeks of treatment was so rapid, that it
appeared unlikely that the differences
be-tween initial test performance and level of
be due solely to the extra care and
atten-tion that the children had received in the
hospital.
NON-NUTRITIONAL INFLUENCES
Associ-ATED WITH POOR PSYCHOLOGICAL TEST
Pis-FORMANCE IN MALNOURISHED CHILDREN:
Among the general factors which
con-tribute to the intellectual development of
the child, the educational level of the
par-ents, especially of the mother, and the
ma-ternal attitude to intellectual development
are frequently considered to be highly
influential. Knobloch and Pasamanick82
have $hown systematic variation of
devel-opmental quotients in accordance with the
level of maternal education and have
indi-cated that this relation is progressively
more manifest as the child grows older.
Similar findings of a direct association
be-tween the child’s LQ. and the parental I.Q.
have also been reported by Kagan and
Moss.83
‘
‘1,The influence of those non-nutritional
factors has ‘not been sufficiently taken into
account in studies
of
mental developmentof malnourished children. This is especially
regrettable since it is known that the great
majority of these children have parents who
are either illiterate or have a very low
scho-lastic achievement. In a study designed to
characterize the environment in which
these severely malnourished children live,
Martinez, Ramos-Galv#{225}n and De La
Fuente84 found a great number of mothers
who themselves had low intelligence
quo-tients. Furthermore, it is a recognized fact
that children suffering from protein-ealorie
malnutrition generally come from hoi#{241}es
where economic pressure hinders the
par-ents from providing adequate and varied
intellectual stimulation for development.
Stock and Smythe,67 too, in their
semi-lon-gitudinal study of mental development in
Cape Town, have reported that the parents
of both well nourished and undernourished
children scored at very low levels on the
Raven test of intelligence.
If one turns to a consideration of the
chil-dren themselves, it is apparent that the
di-agnosis of
mental
subnormality can seldombe established, even in severely defective
cases, before 16 weeks of age because the
assessment measures of intelligence bear
little or no correlation with those made at
subsequent ages.8’ After the first 16 weeks
the prediction of intellectual potential
be-comes somewhat more reliable, especially
in those groups of individuals for whom a
rich cultural environment is not expected.
Thus, Knobloch and Pas,amanickS2 in
sum-marizing the influence of certain variables
on the prediction of later intelligence, have
come to the conclusion that it is necessary
to abandon the concept that the level of
motor development in infancy is an index
which will predict the future intellect of the
child. Clearly, accelerated motor behavior
does not necessarily represent a superior
intellectual potential, and even children
with serious mental defects may exhibit a
normal motor development. Therefore,
without denying that it is important to
know the status of the motor development
in order to have a complete picture of
be-havior, this information is not by itself
sufficient to provide an estimate of the
hi-ture intellectual level. If intelligence is
defined as the ability to cope and adapt to
new circumstances of life, and is reflected
in the increasing complexity of the channels
through which the child acts on objects, it is
probable that, as Knobloch and Pasamanick
have suggested, the adaptive sphere is the
area of behavior that can best serve as an
analogue for later intelligence. Since the
Gesell 1ieasures of adaptive functioning are
concertred with the organization of stimuli,
the perception of interrelationships and the
separation of the whole into its component
parts with subsequent resynthesis in a
man-ner adequate to solve a new problem, they
may provide valuable clues to the future
course of intellectual development.
The persistence of low scores in adaptive
behavior during rehabilitation in infants
who have suffered protein-calorie
malnutri-tion before the age of 6 month suggests
more than a transient loss in intellectual
ca-pacity. It is possibly indicative of
years. In older groups of infants it is
possi-ble that the disordering of adaptive
capaci-ty is a transient phenomenon and that the
initial deficit will tend to be overcome if
other relevant factors do not interfere.
These inferences find some support in the
findings of Barrera-Moncada.” Although
this study is by no means definitive, its
findings are in accord with the picture that
is emerging from animal investigations of
age-specific malnutritional effects in experi-mentally induced malnutrition.
ANIMAL STUDIES: Studies with rats as
subjects have shown that by artificially
re-ducing the size of the litter, with
conse-quent availability of more milk for each
in-dividual, more rapid growth is achieved
be-fore weaning. Rats from such reduced
lit-ters continue after weaning to be larger
than rats from large litters.86 Since all the
rats, independently of the size of the litter,
stop growing at about the same
chronologi-cal age, a permanent size differential tends
to result among the adults in accordance
with initial litter size. When limitation of
food intake is introduced after weaning, the
effects on size are at first dramatic but
be-come less apparent and even disappear
once the animals are permitted a normal
adlibitum diet. Severe food restriction in
adult life of course can result in weight
loss, but even when it persists for
pro-longed periods of time the difference
be-tween theoretical and actual weight is
rap-idly overcome once the rats are again
placed on a good diet.87
By reducing the dietary intake of Rhode
Island cockerels, body weight can be kept
below 180 gm for 6 months, at which age
unrestricted broodmates are fully grown
and weigh about 4 kg. On dietary
rehabili-tation the experimental birds for a time
gain weight faster than did the normal
con-trols, but eventually slow down and rarely
attain full size. It has been suggested that
the failure of the bones to reach their
opti-mal length is due to disturbance in the
growth cartilage during undernutrition in
early life.88
Maintenance of pigs on a reduced intake
beginning when they are about 2 weeks old
keeps their weight below 10 kg until they
are one year of age. By this time their
lit-termates, raised on a diet of the same
quali-ty, but consumed adlibitum, have weights
of between 150 and 200 kg. Although
un-dernutrition of this degree of severity does
not prevent some growth from going
for-ward, it distorts the normal symmetry of
size and body proportions and modifies the
usual relation between biochemical
matura-tion and chronological age. For example,
the muscles of the deprived pigs are in a
stage of development wherein the gross
chemical composition more closely
resem-bles that of a fetus than it does that of a
normal one year old animal. Even when the
undernourished pigs are rehabilitated their
body composition continues to be abnormal
for a long period of time, and some
struc-tures such as the teeth are permanently
affected. In spite of having had one year of
severe malnutrition, resulting in size that is
below normal, bones that are smaller in
length, and weight which is below that of
their litter mates, the deprived sows seem
to have fine litters and to produce an
abun-dance of milk.89 It is of interest to note that
malnutrition, even if severe enough to hold
the body weight of an animal to an
ex-tremely low figure, does not prevent some
of the developmental processes from going
forward at least to some extent. However,
at the same time, some of the usual changes
associated with maturation are not only
ar-rested, but are even modified in such a way
that at the end of the period of food
depri-vation the chemical structure of certain
or-gans may resemble that of a much younger
individual.90
The speed of enzyme maturation also
ap-pears to be closely related to the rate of
physical development. Ross#{176}’found that
normally the relation between enzyme
ac-tivity, chronological age and dietary intake
is so well defined, that it is possible to
pre-dict levels of activity of various hepatic
en-zymes (alkaline phosphatase, histidase,
D-amino-oxidase) if the strain of rat is
animal are known. By altering the amount
and proportions of dietary constituents, it
was found that activity of individual
en-zymes could be changed from values found
at one age to those characteristic of
an-other, much younger age. Similarly,
Esco-bedo and Cravioto92 have delayed the
ap-pearance of phenylalanine-hydroxilase
ac-tivity in the liver of rats by maintaining
them under conditions of severe food
re-striction.
The biochemical maturation of the
regu-latory mechanisms for carbohydrate
metab-olism, too, is arrested in piglets suffering
from an induced kwashiorkor-like
condi-tion. Protein deficiency causes the affected
animals to exhibit biochemical behavior
characteristic of much younger but well
nourished individuals.
Glucose-6-phospha-tase activity in the liver of normal
piglets has been demonstrated after the
eleventh day of life.’#{176}However, if the
animals are fed on a vegetable mixture
hav-ing a 5% protein concentration during the
first 11 days such enzymatic activity cannot
be demonstrated. In contrast, if 5% casein is
added to the vegetable mixture
glucose-6-phosphatase activity does develop at the
normal rate.
Intravenous injections of insulin at a dose
of 0.1 unit per kg of body weight produces
prolonged hypoglycemia in normal young
pigs. The rate of glucose utilization also is
low at this age. As the animals grow older
they become less sensitive to insulin and
increase their rate of glucose utilization.
These normal age related changes are
significantly delayed when the pigs are
raised on a diet grossly deficient in
protein.9’
The central nervous system is not
im-mune to the influences which modify
struc-ture and chemical organization in other
or-gans and also appears to be significantly
affected by undernutrition. Under
condi-tions of severe food restriction, although
the brain continues to grow in size, to
in-crease in absolute weight, and to show
rela-tively normal increments in nitrogen and
phosphorus content, the concentrations of
sodium, potassium and chloride, do not
change appreciably, and correspond in
their levels to those found in normal
ani-mals of a much younger
age.9#{176}Further-more, findings in experimental animals
sug-gest that, in addition to the noted
electro-lyte alterations, severe malnutrition is
capa-ble of producing marked anatomical and
physiological changes in the central
ner-vous systems of a number of animal
spe-cies. Thus, Cowley and Griesel96 found that
in second-generation low protein rats there
is retardation of growth and a delay in the
emergence of certain early response
pat-terns. The eyes and the external ear flaps
open at a later age in the second filial
gen-eration of low protein rats, and the animals
respond to auditory stimuli at a later age
than do normally fed controls. These
findings have inclined Cowley and Griesel
to the view that concurrent with the
ana-tomical retardation, there is a retardation in
the functioning of the receptors. It is
possi-ble, too, that central changes have taken
place, since at maturity the deficient
ani-mals tested on the Hebb-Williams maze
scored a greater number of errors than a
control group. Lat and his co-workers97
have reported that rats from small litters, in
addition to being larger than rats coming
from large litters, demonstrate a greater
tendency to explore their surroundings,
suggesting either a greater degree of
matu-ration of the central nervous system or an
increased level of energy and activity
re-sulting in expanded opportunities to profit
from experience with the environment.
Flexner and his associates98’99 have
shown that the effectiveness of the
inhibi-tion of processes essential for the
incorpora-tion of valine into protein can be raised to a
95% level by combining subcutaneous with
intracerebral injections of puromycin. Mice
when treated in this way show degrees
of disorientation which are incompatible
with learning and memory. More recently,
Flexner’#{176}#{176}has also demonstrated that the
the degree and duration of the inhibition of
protein synthesis by the effect of the
anti-biotic.
Abnormalities in nervous system
func-tioning can derive from nutritional
depriva-tion of the pregnant mother as well as from
direct deprivation of the young. In this
con-nection Platt, et al.’7 have reported that
pups born from mothers raised on deficient
diets from 6 weeks of age, besides having a
high rate of neonatal deaths, have
sig-nificant morbidity in the survivors who
show retardation in motor development
and abnormal EEG recordings. Such
retar-dation and abnormality in EEG findings
have not been observed in pups born of
well nourished mothers.
OVERVIEW: A review of the available
lit-erature leads to at least the following
con-clusions:
a) Malnutrition is a significant factor
affecting the growth of children in all major
preindustrial areas. When a child has been
malnourished there is a persistent lag in
growth which at each age level is reflected
in short stature.
(b) Not only somatic growth, as reflected
in body length, weight and body
propor-tions, is affected by malnutrition. Its
occur-rence appears also to be associated with
changes in psychological functioning,
mani-fested in reduced intelligence test scores,
developmental lags, and defective learning.
(c) Animal experimentation provides
sup-port both for the stunting produced by
nu-tritional lacks in early life, and for the
effects of the deprivation on certain aspects
of behavior.
(d) Biochemical alterations induced by
dietary inadequacies or by the interference
with mechanisms for utilizing nutrients
ap-pear to result in arrest and regression of
biochemical maturation in selected tissues
and organs including the central nervous
system.
(e) The degree to which the individual’s
growth and development is affected by
malnutrition varies with the severity of
do-privation, the time of life at which this is
experienced, its chronicity, and with the
characteristics of the associated
complica-tions.
(f) Speed of recovery from malnutrition
depends not only on the introduction of
adequate amounts and kinds of foods but
also upon the environmental circumstances
in which the recovery is taking place.
(g) At the human level malnutrition is
most persistently present in children whose
familial environments are characterized by
cultural as well as economic inadequacies.
As a consequence, in attempting to assess
the effects of nutritional lacks on both
so-matic growth and behavioral development,
it is necessary either to control for or other-wise to assess the affects of these non-nutri-tional factors.
(h) The manner in which the nervous
sys-tem and its functioning are altered to result
in reduced levels of intellectual
compe-tence is only partially suggested by
psycho-logical test studies and by conditioned
reflex changes. It is necessary to examine
certain primary mechanisms underlying
cognitive growth if a fuller view of the
ways in which malnutrition affects intellect
is to be obtained. Further, such an analysis
is of potential significance for the
develop-ment of methods for the more effective
