Behavior nutritional

Ernesto Polllu,4

of infant in 12,3 causation marasmus

Ph.D.

of

Most investigators recognize causality in severe protein-calorie malnutrition, especially in nutritional marasmus, as being complex and multifactorial (1-3). Hegsted (4) points out that investigators accept different factors as significant and accord them different emphasis. Factors include inadequate quantity and quality of food, poverty, an unsatisfactory physical and psychosocial environment, and parents who are ignorant of appropriate child care. The major cause of protein-calorie malnutrition is generally placed in factors of the as a

data relevant to the issues raised above and to propose the hypothesis that behavior of the infant influences occurrence of nutritional
marasmus. Multiparity

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Reports from family characteristics protein-calorie

many children
study

developing countries on of children with severe malnutrition often show

infants to be late-born

malnourished of

Peru
later

grandmultiparous of 22 cases of typical gives evidence that 41%

born, and all of these were

women. marasmus were sixth

the last born

A in or

physical,
environment.

biological,
Except

and
for

sociopsychological
noting anorexia

contributory
is not affected taken by is usually that

factor,
into of the

the

behavior
The infant of

of the
impression

host
left

account. a helpless vicissitudes

adversely a life modor predict is seen as in

poverty.
causality els child

Such
resembles

a
used Most

unilateral
to often explain the by for

explanation

of

sociopsychological child

of kwashiorkor, 88% were third or later born (7) (Table 1). In Colombia, 49% of 145 children with protein-calorie malnutrition were sixth or later born. By contrast, Table 2 shows that only 37% of 386 children who were fifth or earlier born had a similar condition (P < 0.05) (8).
Closely spaced pregnancies

of a family.

Of 55 cases

commonly behavior.

unidirectionally ences without that parental

affected accounting socializing

parental influthe possibility could be

Other
ciation closely Jordan,

reports
between spaced 78%

demonstrate
preschool pregnancies of

a close
malnutrition the mother. of malnourished

assoand In

behavior

partly dependent upon peramental characteristics

Disregard a host is for surprising nutritionally early, grandmultiparous

constitutional or temof the child (5, 6). the behavior of the child as
because marasmic of

of the

mothers

children
pregnancies

weaned
(9).

their
A

babies
significant

because
positive

of new
cor-

reports

that weaned
of of

published children the

off-

relation between dren in the family

was also found

are
spring history

are

commonly
women

with and that

inter-

are likely These

sucking relationships

closely spaced pregnancies, to have low birthweights. characteristics should suggest

level with the of arousal, are and mother adversely

Of

79

children

numbers of preschool chiland preschool malnutrition in the Colombian study cited. with four or more preschool of Nutrition and Food

the Department
Science, Massachusetts

behavior,

affected in the infant ment of malnutrition. tions probably hinder fore

264

prior to the developIn turn, such condifood intake and therestatus. is to present
Journal

affect nutritional The purpose now

available
of Clinical

Institute of Technology, Cambridge, Massachusetts 02139. This publication is contribution No. 2000 from the Department of Nutrition and Food Science. by Public Health Service Contract No. NIH 7 1-2417 with the National Institutes of Child Health and Human Development, Bethesda, Maryland 20014. 4Associate Professor of Growth and Development, Department of Nutrition and Food Science. Nutrition 26: MARCH 1973, pp. 264-270. Printed in U.S.A.

The American

CAUSATION

OF

NUTRITIONAL

MARASMUS

265

siblings, 47.9% were malnourished, whereas 352 with three or less preschool siblings had a frequency of only 29% (8) (Table 2). In a study of undernutrition and mental development in Colorado (10), similar patterns occurred; e.g., 19 children admitted to the Denver General Hospital with generalized undernutrition were compared for selected social factors with matched controls of similar economic level. One differentiating social factor was the stress of one or two siblings less than 2 years old. These findings were corroborated in a study on the effect of socioeconomic and cultural influences on child growth in the village of Lawrence Tavem in Jamaica (1 1).

TABLE
Family

1
size and birth order of patients

kwashiorkor

and nutritional

marasmus
Type

with in Perua

of malnutrition

Characteristics Kwashiorkor Marasmus (typical)

No. of cases Children in family Average number Age range

51 3.9 2-10 1 5 15 6 3 4 28
b

22 5.0 2-12

Patients

order

of birthb
(3) (15) (44) (18) (9) (12) (82) 1 (5) 6 (27) 6 (27)

First born Second Third Fourth Fifth Sixth or later Last born
a

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9 (41) 22 (100)

Low

birthweight From
not

(7).

Two

atypical

cases

oimarasmus in parentheses

There are fewer than a handful of studies on birthweights of severely malnourished children. That lack is wholly understandable, given the generally low education of mothers,
the unreliability of retrospective data, and

are are

included percentages.

(see text).

Numbers

the

the inadequacy of clinical records in hospitals servicing rural or low income areas (12). Moreover, prospective studies in which the case histories of low birthweight children are followed until they become severely malnourished are rare because of obvious moral implications. Some published data suggest that children who become severely malnourished often had low weights at birth. For example, in the Colorado study (10), 10 of the 19 cases with generalized undernutrition had birthweights of 2,500 g or less. A sample
of malnourished weights above

TABLE 2 Association of protein-calorie preschool children with birth preschool children in family

malnutrition in rank and number in Colombiaa

of

I
Demographic factor Population in category

PCM P Number Percent

reported by Monckeberg (13). His sample of 14 hospitalized malnourished children had a range in birthweight from 2.9 to 3.8 kg (in = 3.4). Despite reports to the contrary, it is indeed
probable that the incidence of prematurity

children 2,500 g

all is

with

birth-

Birth rank 5th or lower 6th or higher No. of preschool children in family 3 or less 4 or more
a

773 295

286 145

37.0 49.2

<0.05 7.52

903 165 (8).

352

39.0

79

47.9

<0.05 4.23

Adapted of

from

regardless maturity
rates being

economic positively
among

level,

rates with

of parity,

prethe

correlate
greatest

grandmultiparous

women
spaced

or low birthweight among nutritionally marasmic children is greater than that for the general population. This inference is supported by information of adverse effects of high parity and short spacing between pregnancies. A considerable amount of research data shows an increased reproductive risk, most marked in low income groups (14), as a function of parity. Birch and Gussow (14) show from a review of relevant studies that,

closely that children born within 1 year of a previous full-term pregnancy have lower birthweights than those born after 2 to 5 years (16). Rosa and Turshen (16) quote an unpublished study in Uganda in which infants with birthweights under 2,500 g were born an average of 18 months after the mothers last pregnancy. By contrast, for infants weighing more than 2,500 g, the average interval was 30 months.
(15).
pregnancies, there is evidence

In

connection

with

266

owrr
nutrition is greater in developing countries or

Accordingly, there is justification for inferring that a considerable proportion of severely malnourished children are premature or have lower birthweights than the

in low income

areas

where

birthweights

aver-

population
TABLE
Mean status

average.
3

The

incidence

of mal-

age less than in developed countries or in high income areas (17, 1 8) (Tables 3, 4). Low birthweight in developing countries and

in low income
retarded
to socioeconomic and Indonesia)
Mean birthweights,

areas

intrauterine

apparently results growth stemming

from from

birthweights according (India, Congo, Ghana,

Place

Population

Subjects

status

Madras South
Bombay

Indian

Well-to-do Mostly poor

Wealthy Poor Upper class Upper middle class Lower middle class Lower class Paying pa-

2,985 2,736
3,182 2,810 3,247 2,945 2,796 2,578 2,851 2,656

in fetal nutrition (16, 19). If average birthweights of severely malnourished children fall on the negative side of distributions of population birthweights, they are likely to be significantly below the WHO cutoff point (2,500 g) for prematurity. disturbances

India

Indian Indian

Early

weaning

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A few reports
nutritional

also

show
for

early

weaning
com-

in to
that

marasmus:

example,

paring
kwashiorkor
Marasmus

his

experience
in Jordan,

with
McLaren

marasmus
says

has

more

complex

basic

Calcutta

Indian

Congo

Bantu

tients Poor class Very wellnourished

Well-nourished Badly nourished

etiology with a monotonously tern of early weaning (9). study of 22 cases of typical

constant patIn the Peruvian marasmus, an

3,026
2,965 2,850 2,635 3,188

average duration of only 2.0 months of exclusive breast feeding was recorded; in kwashiorkor it was 7.8 months. Malnutrition appears to develop slowly as breast feeding ends, and the diet thereafter
ments

Ghana

(Ac-

Pygmies African

Prosperous

fails
of

cra) General
lation

popu-

2,879
3,022

detailed dynamics Behavioral

to meet the nutritional the infant. There is interdisciplinary surveys of early weaning (20). effects

requireneed for into the

Indonesia (Jogjakarta) Adapted

TABLE 4

Javanese from (18).

Well-to-do Poor

2,816

From a review parity and closely drop and Bell (21)

in Africa and
dependent,

of a series of studies on spaced pregnancies, Walconcluded that ineffectual,

Mean birthweight of newborns tra1is-Saharan territories

Place

Mean

birthweig

bts,

kg

was associated siblings. They esis that infants

immature with
then

behavior in many closely

developed the

children spaced
hypoth-

Congo
Nigeria

(Mayumbe) (Ibadan) (Lagos)

Nigeria

Nyasaland, rural South Africa (Durban) Southern Rhodesia (Salisbury) Uganda (Kampala)
a

6 lb, 7 oz 6 lb, 5 oz 6 lb, 6 oz 6 lb, 13 oz 6 lb, 10 oz 6 lb, 9.5 oz 6.77 lb 6.3 lb

(2.92)

(2.86) (2.89)
(3.90) (3.01) (2.99)

(3.07) (2.86)
(2.95)

6 ib, 8 oz
b

Adapted

from

(19).

Now

known

as

Malawi.

born to mothers who had experienced a large number of closely spaced pregnancies would be lethargic. Specifically, they were interested in whether newborns from large, densely concentrated families were inefficient in obtalning nourishment as measured by suck rate and number of sucks, would cry little, and with low intensity even when uncomfortable and hungry, and would be slow to respond to a stimulus such as the removal of a nipple on which they were sucking.

CAUSATION

OF

NUTRITIONAL

MARASMUS

267

Waidrop score as
2)

(FSD). average span in months between births, and 3) months to the next older sibling. They observed the behavior of 74 infants born to multiparous women, and only children with weights over 2,500 g were included in the
sample.

and Bell developed a composite family size and density index It included: 1) number of children, a

eating
neonatal

behavior group

of neonates (24). The of main concern to the

authors
with

in this
above average

latter of

investigation
birthweights.

was

that

The

existence

a positive

correlation

The sucking

FSD index behavior

correlated and total

negatively crying but

with posi-

tively with a composite total crying,

size and predictor

lethargy. Lethargy score that included and initial reaction

was based on sucking rate, time. Family

density of food
positive later,

index intake.

proved a Furthermore,

reliable sigwhen tested

nificant
2.5

years

correlation developed FSD scores were

against a nursery school rating of contact with a female teacher (r = + 0.36; P <
0.01); the correlation exhibited score, with ability by contrast, the number to defend (r = -0.35; had a negative of times a child himself against P < 0.01).

peer aggression In a recent study Thoman, Liederman (22) could establish

ship between parity and

Barnett

and

amount

no relationof formula

consumed

by infants

regardless

of whether

the infant was fed by a nurse or mother, although such variables as age did evidence an effect. Note, however, that Thoman et al. used only parity as a variable, whereas Waldrop and Bell (21) employed a composite score including months of age difference between the children studied and the next older sibling and average span between births of all the children of a family as well as parity. Moreover, Waldrop and Bell assessed the effects of different numbers of pregnancies, whereas Thoman et al. assessed multiparity as a global category in which most mothers were of second and third parity. Two recently published studies yielded positive associations between birthweight and food intake. In a sample of 210 babies, the heavier babies had a larger mean daily intake in calories and ounces than lighter infants, a relationship apparently mediated by differences in sucking behavior (23). A similar pattern was established in a study on the

between the effectiveness of the suck and weight at birth among 40 infants with birthweights ranging from 1,700 to 2,500 g endorses the clinically well-known fact that the suck-swallow pattern of premature infants is less adequate than for infants of normal weight. An extreme illustration of this inadequacy is reported for seven infants of 1,800 to 1,890 g (32 to 34 weeks gestation); when offered the nipple for the first 3 to 5 days, they mouthed it with only slight sucking attempts. The first true sucking appeared 3 to 10 days after initiation of feeding (10 to 26 days of age) (25). In another study on the sucking capability of 49 premature infants, birthweight and rate of water intake during the first 3 days of life were found to be positively and significantly correlated. Birthweights ranged from 1,350 to 2,450 g; 32 infants weighed 2,000 g or more. A similar relationship existed between water intake during the first 3 days and formula ingested from the 4th to the 6th day of life. The 49 premature infants, with a mean birthweight of 2,109 g, had a mean sucking rate of 0.2 to 0.3 cm3/sec within the first 3 days of formula feeding. By contrast, the mean sucking rate of 32 full-term controls, with a mean birthweight of 3,231 g,
was

Downloaded from ajcn.nutrition.org by guest on November 22, 2013

0.6

cm3/sec.

No

association

existed

be-

tween

birthweight

and

sucking

efficiency

among the full-term controls (26). Nutritionally marasmic children born of grandmultiparous women with closely spaced
pregnancies and with low birthweights would presumably be doubly handicapped. They are probably unable to ingest maternal milk in amounts sufficient for usual development during at least the 1st month of life due to lethargy or immature sucking. A study on weight gain of infants during the 1st month of life was a function of average quantity of formula ingested per day (27). Bell has brought out that parent and child together constitute a social system wherein the response of each is a stimulus to the other. He postulates that parents have a

268

PoLzm

repertoire of actions aimed at accomplishing different socializing objectives in the child, and that one of the activating elements in the repertoire is stimulation from the object of acculturation. Such usual characteristics of infants and children as helplessness evoke responses. Bell differentiates two types of

3 weeks and again at 3 months quency of the mothers contact fant. A causal sequence in relationships apparently exists instigates maternal intervention

the frewith the inmother-child when the cry (30). An-

with

parental control repertoire. One, an upper limit control behavior, induces and redirects behavior of the child which exceeds parental standards of intensity, frequency, and competence for the childs age; the other, lower
child bestandards. Parent control behavior is, in a sense, homeostatic relative to child behavior. To illustrate, Bell (5, 6) states that the average limit havior control that behavior, is below stimulates parental

other study on mother-neonate interaction gave evidence that a mothers engagement in feeding her young depended upon the level of infant activity. The mother would not rouse an infant for feeding if the child was
asleep relation Finally, a highly significant corbeen reported between infants during breast feeding and the number (31). has

intake of weeks

the mothers

breast

fed their

children
Downloaded from ajcn.nutrition.org by guest on November 22, 2013
may In a

parent

would

show

an increase

in upper

limit

(32). In severe infant malnutrition, extend past an effect on child study of 40 mother-neonate

parity behavior.

control behavior in response to excessive crying by an infant, or in response to impulsive, hyperactive, or overly competent or assertive behavior by the young child. In keeping with the above, it can be assumed that lethargic, listless behavior in an infant could evoke lower limit control
behavior in the parents to enhance the re-

pairs including primiparous women talked more to their infants and provided more general stimulation. Primiparous mothers who talked frequently to their young also fed them for longer periods of time (33). The investigations just cited suggest that 20 multiparous women,
attention to the child varies with parity. That being true, late-born children conceivably receive less attention than needed, the problem being accentuated if late-born children are lethargic and possess a limited behavioral repertoire that fails to attract maternal attention. Both conditions could then interfere with meeting nutritional needs,

sponsivity of the child, thus facilitating the developmental process. Different types of parental response might, by contrast, reinforce lethargic behavior, thereby hindering

socialization and, possibly, physical growth. Early weaning of marasmic children might well be a maternal response to ineffectual sucking and lethargy of the infant. Also,
declining breast milk output from decreased

through earlier
nutritional Implications

limiting weaning,
marasmus.

frequency of and possibly

feeding resulting

and in

pituitary

prolactin

might

be

due

to

inadeExcept for attention to greater morbidity and anorexia, the role of the host has had far less consideration than environment in analysis of causality of severe malnutrition. Evidence has been introduced that selective be-

quate nipple stimulation. Early weaning fails to enhance responsivity of the child and creates instead an organic imbalance if the substitute diet lacks nutritional requirements

in protein and calories. Studies on infant state and havior support an assumption
can regulate maternal response

sucking bethat infants

as well as

havior sucking and an

of the malnourished child, such as and lethargy, conceivably contribute

deficiency. Lethargic behavior

timing of weaning. State, a popular term in infant behavioral research, defines activity level and degree of alertness in the infant (28, 29). In a study on influence of infants sex, age, and state upon mother-infant interaction, the frequency of cries in female infants correlated positively during the
first

to nutritional

immature

sucking

response

hinder

milk intake and secretion; similarly, both factors might adversely affect the ability of the child to stimulate the attention of a

mother children.

heavly

burdened

by

care

of

other

CAUSATION

OF

NUTRITIONAL

MARASMUS

269

Ineffective sucking and lethargic behavior are probably hardly necessary nor sufficient conditions to produce malnutrition; both characteristics, however, place the child at the risk of malnutrition. Physical and sociopsychological environmental conditions will probably dictate a developmental course to

a considerable infants with

degree. By inference, active effective sucking are to an ex-

tent protected even in a severely adverse environment. The proposed hypothesis that behavior of the infant influences the frequency of severe malnutrition requires testing. If valid, the implications are important, substantiating the need for education in child care within

health

and

nutrition

programs

in low income

malnutrition in Candelaria, Colombia. I. Preyalence: social and demographic causal factors. J. Trop. Pediat. 15: 76, 1969. 9. MCLAREN, D. S. A fresh look at proteincalorie malnutrition. Lancet 2: 485, 1966. 10. CHASE, H. P., AND H. P. MARTIN. Undernutrition and child development. New Engl. J. Med. 282: 933, 1970. 1 1. DESAI, P., K. L. STANDARD AND W. E. MIALL. Socioeconomic cultural influences on child growth in rural Jamaica. I. Biosocial Sci. 2: 133, 1970. 12. PoLLIrr, E., AND H. RICCIuTI. Biological and social correlates of stature among children in the slums of Lima, Peru. Am. I. Orthopsychiat. 39: 735, 1969. 13. M#{212}NCKEBERG, F. Effect of early marasmic malnutrition on subsequent physical and psychological development. In: Malnutrition, Learning, and Behavior, edited by N. S. Scrimshaw and J. E. Gordon. Cambridge: MIT

Downloaded from ajcn.nutrition.org by guest on November 22, 2013

areas or developing countries. Specifically, public health education in feeding practices requires incorporation of measures to compensate for ineffective sucking, as well as the means to stimulate the sucking response of the lethargic child. Furthermore, another reason to integrate family planning within health programs is that the large family

Press,
14.
BIRCH,

1968, p. 271.

15.

H. G., AND J. D. Gussow. Disadvantaged Children. Health, Nutrition, and School Failure. New York: Harcourt, Brace and Jovanovich, 1970, p. 81. DONNELLY, J. F., C. E. FLOWERS, R. N. CREADISK, H. B. WELLS, B. 0. GUENBERG AND

K. B.

SURLES.

Maternal,

fetal,

and environmen-

affects the nurture very naturefi

The
John

of the child

as well

as his

critical
E. Gordon

comments
are gratefully

and

suggestions
acknowledged.

of Dr.

References 1. LE RICHE, W. H., AND J. MILNER. as Medical Ecology. Baltimore: Wilkins, 1971, p. 373. 2. R1os-GALvAr4, R., C. MARISIAE, AND B. PEREz-ORT!Z. Desnutricion Epidemiology Williams

&

A. 1969.

VINIEGRA

en el Ni#{241}o.

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tal factors in prematurity. Am. I. Obstet. Gynecol. 88: 918, 1964. 16. ROSA, F., AND M. TURSHEN. Fetal nutrition. World Health Organ. Bull. 43: 785, 1970. 17. Report of a WHO Expert Committee on Nutrition in Pregnancy and Lactation. World Health, Organ. Tech. Rept. Ser. No. 302, 1965. 18. JELUFFE, D. B. Infant nutrition in the subtropics and tropics. World Health Organ. Monograph Ser. No. 29, p. 85, 1968. 19. LECHTIG, A. Environmental factors affecting birth weight in rural populations in Guatemala. Presented at the IX Intern. Congr. Nuir., Mexico City, September 5, 1972. 20. JELLIFFE, D. B., AND E. F. P. JELLIFFE. Lactation, conception, and the nutrition of the nursing mother and child. I. Pediat. 81: 829, 1972. 21. WALDROP, M. F., AND R. Q. BELL. Effects of family size and density on newborn characteristics. Am. I. Orthopsychiat. 36: 544, 1966. 22. THOMAN, E. B., C. R. BARNETU AND P. H. LIEDERMAN. Feeding behavior of newborn infants as a function of parity of the mother. Child Develop. 42: 1471, 1971. 23. DUBIGNON, J., D. CAMPBELL, M. CURTIS AND

M. W. oratory

PARTIGNON.

measures

The relation between of sucking, food intake,

laband

24.

perinatal factors during the newborn period. Child Develop. 40: 1107, 1969. NESBITT, R. E., AND S. B. GURWITZ. Weight, sex and the eating behavior of newborn humans. I. Comp. Physiol. Psychol. 73: 245,

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Moss,

H.

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M. Behavioral Analysis: Analysis of Observations as Applied to Mother-. Relationships. Springfield, illinois: Thomas, 1958. HILLENBRAD, E. D. The Relationship of Psychological, Medical and Feeding Variables to Breast Feeding. Unpublished Masters Thesis. George Washington University, Washington, D.C., 1965. THOMAN, E. B., P. H. LIEDERMAN AND J. P. Clinical Newborn
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