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3. The effect of malnutrition on human development

Introduction: Chronic malnutrition
A poor village: Its reality and problems
The longitudinal intervention study: Design and implementation
The first eight months of life
The "valley of death" between 8 and 20 months
The preschool survivor and the nutritional crisis at school entrance
The teenager who was malnourished as a child
Comments: Nutrition in the life cycle and social development
References
Notes

A 24-year Study of Well-Nourished and Malnourished Children Living in a Poor Mexican Village
Adolfo Chávez, Celia Martínez, and Beatriz Soberanes1

Introduction: Chronic malnutrition

It was recognized in the 1950s that the severe forms of protein-energy malnutrition, kwashiorkor and marasmus, were associated with marked cognitive effects (Scrimshaw et al., 1968) although the lasting effects on survivors were unknown. The predominant type of malnutrition in Latin America has changed dramatically during the second half of this century. On the one hand, the prevalence of acute and severe forms of malnutrition that bring death to children has steadily declined. On the other hand, chronic malnutrition, which causes physical and intellectual impairments in the affected populations, has increased substantially.

Marginal or chronic malnutrition is a consequence of early malnutrition that is more noticeable between 8 and 20 months of age. Many individuals who experience childhood malnutrition survive and reach adult age. However, these individuals are "vulnerable survivors" with very specific developmental deficiencies that are the result of chronic malnutrition experienced during early childhood.

This study reports on an 1 8-year follow-up that gives us the opportunity to describe the natural history of two exceedingly important problems in developing countries: poverty and malnutrition. These data contribute to our understanding of the consequences of early childhood poverty and malnutrition for the individual's performance at birth, during the school-age period, and during adolescence and young adulthood.

The worldwide problem of malnutrition is related to the consumption of deficient and monotonous diets that are based on roots and cereals. Cross-sectional studies conducted in developing countries have shown that few children have the symptoms and clinical signs of severe protein energy or micronutrient malnutrition. Furthermore, the majority of these children seemed to tolerate well their chronic exposure to suboptimal diets. However, pioneering studies in Mexico (Ramos-Galván, 1949; Cravioto et al., 1966; Cravioto and DeLicardie 1968) showed that subclinical malnutrition, manifested only by impaired growth, significantly impaired intersensory perception. Concurrently Mönckeberg (1967) showed a significant relationship between growth retardation and reduced cognitive performance in low socioeconomic groups in Chile.

In this period, Federico Gómez, the Director of the Hospital Infantil de Mexico proposed a classification of malnutrition based on weight-forage that has been widely adopted. First degree malnutrition was identified as 10 to 25% below normal weight-for-age, second degree as 25 to 40% below and third degree as greater than 40% below standards for well nourished children for whom the normal range was plus or minus 10%. First and second degree malnutrition correspond to what is now called marginal nutrition (Gómez, 1946; Canosa et al., 1968).

The longitudinal study described in this chapter was carried out to understand the consequences of moderate malnutrition. Emphasis was on determining the relationship between chronic malnutrition and the physical, mental, and behavioral development of the individuals. To understand this relationship, the research design must control for nonnutritional factors that also affect human developmental needs by including longitudinal observations of both malnourished and well-nourished children living under the same social and ecological conditions.

By 1967, the year in which this study was planned, it was recognized that subclinical malnutrition associated with growth retardation was associated with deficits in learning and behavior. However, there was no agreement as to the extent with which these associations were due to malnutrition or to concurrent genetic, cultural or other environmental factors. As a result of this debate, this study was designed as an intervention in which it was possible to control for nonnutritional factors.

We decided to follow a small number of subjects prospectively in great detail, for two reasons. The data collection, which included measurements of milk volumes. interviews. and direct observations of child behavior.required field workers to live with the families for at least three consecutive days every two. The ethics of observing a control group of subjects without nutritional supplementation during the study has been questioned. The researchers considered the study to be ethical because its results would help to motivate decision-makers to invest in and support efforts to improve the nutritional status of the poor in Mexico and throughout the world, an expectation amply realized. Moreover, the control group benefited from the same enhanced medical care and stimulation as the supplemented group. Without a control group no children would have received a supplement.

Several of the social goals of the project were achieved. In 1973, a few months after the first report of the project was presented, the Mexican government launched a major program called Orientación Familiar, which taught women how to improve their infant feeding practices. The program promoted partial breast-feeding at three months of age, which meant the inclusion of clean foods available at home in addition to breast milk (Muñoz de Chávez and Chávez, 1986). This program was delivered to more than two million households by a large number of rural women who were trained in the use of educational materials. This was the largest public health effort that resulted from the study in Tezonteopan, which together with other smaller studies, was instrumental in decreasing the severity of malnutrition in Mexico.

Most of the original observations in Tezonteopan were made by the resident researcher Celia Martínez between 1968 and 1973. She still lives in the village 24 years after the initiation of the study and has also conducted, at times with few resources and little support, follow-up studies during adolescence and young adulthood. It is to her that we owe the accumulation of knowledge from this extraordinarily detailed study that illustrates how the functioning of poor Mexican infants is damaged by malnutrition and how it can be improved with better primary health care and nutrition.

A poor village: Its reality and problems

Tezonteopan had 1,495 inhabitants when the study was initiated in 1968. The village was very isolated, even though it was only 9 km from a paved road to Mexico City, only 2.5 hours away.

Tezonteopan covers 200 ha of agricultural land and was founded in 1884 by 18 families that ran away from a neighboring hacienda. In 1938 the government provided the village with an additional 552 ha of agricultural land. Agriculture is the main source of income for the villagers, who grow corn, beans, and squash for subsistence and peanuts as a cash crop.

The vast majority of the families are poor and have access to only 2 or 3 ha of land. Income received from crops is just enough to pay for the loans that are provided in kind or as cash by the local shop owners. These loans are usually used to acquire consumption and production goods and to cover expenses related to social events and health care.

In 1968 most of the dwellings were built of reeds or adobe and had only one room. The quality of life, including the level of hygiene, was very poor and the village lacked basic infrastructure such as electricity and potable water. At the beginning of the study, the average family income was 1 US$ per day.

In the two years prior to the initiation of the study, overall mortality was 18.5/1,000, infant mortality was 126/1,000 births, and the preschool mortality was 16.9/1,000 inhabitants. The annual birth rate was 58.8/1,000, which in pert can tee explained by the predominantly young population living in the village. Despite the high mortality, the birth rate was still high and the population increased. The secular trends (19661990) of fertility and mortality are presented in Table 1.

The period of fertility was short because the onset of menarche usually was late, at about 15.5 years of age, and the women reached menopause at the relatively young age of 40.5 years (A Chávez and Martínez, 1973). The period of postpartum amenorrhea was very long and lasted for 13.5 months. Therefore the birth intervals were long, with a mean duration of 27 months. The fecundity rates were high because the women had nine children in their short reproductive lives, only five of whom survived until adolescence or early adulthood.

TABLE 1 Demographic Data on the Community (Mean of 5 Years Around the Annual Rate)

The diet in the village was deficient in nutrients because meat products were hardly ever consumed. Corn provided two-thirds of the daily energy intake, and the remaining calories were provided by beans, sugar (in coffee and tea), and sometimes pasta, bread, and wild vegetables. The infant feeding patterns were very consistent in the village. Infants were given only breast milk up to 8 to 10 months of age. At this age other foods-atole (corn gruel), soups, and tortillas-were gradually introduced into the diet.

Since the project was designed around a nutritional intervention, it was decided to minimize the inclusion of other types of interventions such as health care and community development. For this reason, only basic health care was provided, and community events were supported only when this was specifically requested by the villagers.

Important changes took place in the community during the study. This was undoubtedly the result of the presence of the research team and the interest of the Mexican government in the community development of rural areas. At the beginning, these changes were slow; electricity and potable water were not requested by the villagers until the third and fifth year of the study, respectively. After this period the villagers wanted to experience a faster rate of community development, and by 1980 several projects were planned. These included the introduction of irrigation pumps, more profitable crops such as tomatoes, machines for removing peanut husks, and trucks for transporting agricultural products. The research center fully supported and communicated all these requests to the authorities in charge of making these decisions.

The process of change in the village was interrupted in 1982 as a result of a national economic crisis. The sharp increment in outmigration by young villagers that took place around this time probably reflected the fear and anguish caused by this crisis. In 1982, the first peasants went to work in a neighboring community, and now, 10 years after the first migrations, there are 150 villagers working in the United States and Canada.

In spite of the several changes that have taken place since 1975 as a result of social and economic openness, many aspects of basic life in the village have not changed. For example, in the 1990s almost all families have television and video sets. However, the villagers still sleep on a mat on the floor, and the houses still have the same appearance and size, even though they now use more brick and concrete. Most of the houses still lack windows and are as contaminated as before. The food habits and environmental conditions of the people are still the same, even though they now have higher incomes and water taps inside the households.

Infant feeding habits have changed: infants are now given more foods in addition to breast milk and are introduced to these foods at earlier ages. The families are now more likely to give cows' milk as a complement to breast milk. These changes in infant feeding practices are due to the fact that the families have seen the superior development of the children who were supplemented in the study.

There have been important improvements in health in the village. It is paradoxical that small changes could bring about such large effects. The community is still trying to produce more agricultural products, in spite of the national economic crisis of the last 10 years. However, the villagers are also obtaining resources by more diversified strategies that include migration. These recent migration patterns have brought about the most important changes that have benefited the village. In spite of the scarcity of credit and the decline in the prices of agricultural products, the community is now less isolated and more likely to seek external resources. Chronic or moderate malnutrition still persists today at about the same level as before, but there has been a decline in the number of cases of severe malnutrition. Regretfully, these changes have not been enough to promote the healthy development of the survivors.

The longitudinal intervention study: Design and implementation

The study was planned as an intervention in which one group of mother-infant dyads received food supplementation while a second group remained untreated. Whereas the treated group would tell us if an adequate nutritional status could be attained even under adverse socioeconomic conditions, the untreated group would provide important information about the natural course and consequences of chronic malnutrition (Madrigal and Avila, 1990).

This project was conceived as a study of cases and not as an epidemiological survey. At that time there were data suggesting that the problem of marginal malnutrition was related to breast-feeding (Martinez and Chávez, 1967). For this reason it was decided to devote a substantial amount of effort to measuring the quantity of breast milk produced and ingested. A great deal of effort also went into making behavioral observations of the children. This component was included because the research team believed that suboptimal child behavior was one of the main consequences of malnutrition. Because behavioral studies can only be done by direct observation in the households, the sample size could not be large. Based on a statistical procedure for taking into account the possibility of dropouts from the study, it was estimated that 20 dyads would be enough to test the behavioral hypotheses.

The supplemented and unsupplemented groups did not enter the study at the same time, because the people in the villages could have questioned the provision of food to some but not to other children. For this reason, during the first year of the study, only the nonsupplemented women and their newborns were recruited into the study. During the second and third year of the study, all the women who became pregnant received food supplementation. At the time of birth of the children, dyads with similar physical and socioeconomic characteristics to the unsupplemented group were recruited for continued supplementation.

The United States National Institutes of Health (NIH) initially funded the study for four years and later extended this period to seven years. The Mexican Council for Science and Technology (CONACYT) funded the project for another seven years. The project has continued to be funded by smaller grants, one of which was provided by the United Nations University (UNU).

The study was initiated in February 1968, and the first three months were devoted to a general study of the community and to establishing a close relationship with the families. Following this period, all the pregnant women in the village were studied. By the end of the first year, in June 1969, a group of 41 mother-infant dyads had been recruited. Twenty of these 41 women were selected for the measurements of milk production and intake and behavioral observations. The selection was based on socioeconomic status and maternal health, age, and anthropometry. The growth of the children of the remaining 21 dyads was followed longitudinally into the adolescent period.

The women and their children born in 1968 and 1969 were not given supplemental food and did not receive any type of intervention except in emergency situations. These children grew up with the support of their families under the usual conditions of the village. They were breast-fed for a prolonged period of time, and weaning foods were usually introduced with hesitation and at a very late age in an insanitary environment that constantly led to constant infections.

These children were born with low birth weight. They grew well in the first three months but then their growth velocity declined and therefore they began to suffer malnutrition. Of the 20 children who were selected for the full study, two were treated and dropped from the study because they developed severe malnutrition, one with edema and the other with marasmus. One of them was replaced by another child. Another child died of an infection under very difficult circumstances and one child emigrated. Therefore this group had a final sample size for the full study of 17 children. The total number of newborns of that year was later further reduced from 41 to 36 due to two additional migrations. This group has been analyzed and included in several reports dealing with preschoolers and teenagers.

The following year a second group of pregnant women was recruited and supplemented twice per day with a nutritious drink immediately following the first report of amenorrhea. The drink was made by mixing milk with fruits and was designed to provide 400 kcal per day and appropriate amounts of iron, niacin, riboflavin, and vitamins A and C. The intake of the food supplement was monitored, and it was shown that it provided 325 kcal per day. Supplemented women had similar socioeconomic and physical characteristics as the women in the nonsupplemented group that was recruited the previous year.

Supplemented subjects were matched at birth with their counterparts in the unsupplemented group, according to the physical and social characteristics of the mother-infant dyed. In addition to the 20 supplemented women who were included in the full study, another 20 women were also given food supplements and studied in some aspects of their development. The fact that the experimental and the control groups entered the study at different times was necessary, not only for interactions with the community but for logistic reasons.

The children in the experimental group began to receive supplementary food as soon as they showed the first signs of growth faltering, at about 12 weeks of age. First, the children were offered a bottle with milk during the night. When the children started to request to be breast-fed more often, even though they were being offered the bottle with milk, they were also given fruits and vegetables. Afterwards the infants were fed ad libitum with milk and a variety of strained foods. The research team always advised the women to continue breast-feeding during this time.

When the children were four years old, they were supplemented twice per day with a sandwich and a glass of milk. When the children began attending school, they sometimes missed one of the daily episodes of supplementation because they preferred to remain playing at school during recess instead of going out to receive their supplement. However, the children always received the supplementation after school hours. The supplementation intervention ended when the children were 10 years of age

Throughout the study, special care was taken to ensure that the only between-group difference was the nutritional supplementation. Measures were taken to balance the amount of contact with research workers and any other procedure that could have been considered a nonnutritional intervention.

Throughout the 24 years of existence of the Centro Rural de Tezonteopan, a variety of nutrition and child development parameters have been studied. The unsupplemented children are, as this report is being written, 22 years old and therefore have become young adults. The children in the supplemented group are now between 17 and 20 years of age. The range of ages in the latter group is explained by the fact that the large amount of effort needed for planning and implementing the project caused a slowdown in the rate of recruitment of subjects during the last years of the intervention phase.

The different types of studies are presented in the Results. The special methodologies that were employed are presented and discussed below.

a. All the women were included in longitudinal follow-ups of anthropometry and in a special study on fertility and reproduction.

b. The studies on food intake during early infancy included measurements of milk volume using a 72-hour test-weighing procedure at 2, 8, 16, 24, 36, 56, and 78 weeks of age.

c. The behavioral follow-up looking at mother-child interactions was the most significant component of the study. These observations were made between breast-feeding episodes while the observer was seated in a corner of the house pretending to read a book. Every 40 seconds the investigator looked over the book to make a "visual photograph" of the mother-child interaction (e.g., holding, feeding, kissing, verbalizing, degree of physical activity, etc.). Seventeen parameters were captured and written down every time a "visual photograph" was created. This procedure was carried out for 1.5 hours during the morning after the child woke up and for another 1.5 hours in the afternoon. This methodology is derived from that used for ethological observations of primates and is the one that captured the most important differences between the supplemented and unsupplemented children.

d. A similar methodology was used during the school period. The researchers made a hole in the wall of the classroom so that they could make behavioral observations of the children (e.g., standing, sleeping, attention span) while attending class. Each observation period lasted 1.5 hours and yielded information that discriminated between supplemented and unsupplemented children. Several national and international knowledge and problem-solving tests were also administered during the school period.

e. The physical activity of the infants was evaluated by observing the number of contacts that the heel made with the bed. Afterwards physical activity was measured as the number of steps taken in a specified period of time (10 minutes per hour for 10 consecutive hours).

f. The longitudinal assessments involving neurological, psychological, and cognitive measurements were done following traditional methods (A Chávez and Martínez, 1982).

g. Morbidity was recorded daily and the study also included a microbiological assessment of fecal contamination of household objects and members.

The experimental design was selected to test the hypothesis that nutrition during early childhood is an environmental factor that has a strong negative impact on long-term human development and function. The design of the study also contributed to a better understanding of the development of children in a deprived environment. It was also possible to study the life cycle in the families, since it included the follow-up of subjects from the time that they were in their mother's womb until they became pregnant.

The final objective of the project was to identify the critical point at which interventions that will achieve an optimal development in socioeconomically disadvantaged populations are most cost-effective.

The first eight months of life

The first impact of the supplementation interventions was on the mothers themselves. By the eighth month of pregnancy, the supplemented women consumed 20% more food (2,410 cal and 70.7 g protein vs 2,055 cal and 53.3 g protein) and had a higher pregnancy weight gain (+3.4 kg) than unsupplemented women. Among supplemented women, menstruation returned by 7.5+2.6 months postpartum, 6.2 months earlier than among unsupplemented women. An important consequence of this delayed return of menstruation was that the birth interval decreased from an average of 27 months to 19 months (A Chávez and Martinez, 1973). This effect cannot be attributed to decreased rates of breast-feeding, because all the supplemented women were breast-feeding en average of 7.3 times per day by the time that menses returned.

In this community, infants can be considered as extrauterine fetuses who depend on their mothers for survival during their first months of life. Then infants are fed almost exclusively on breast milk. Solid foods usually begin to make a critical nutritional contribution when the infant is beyond six to eight months of age.

The placenta is a very efficient organ for the transfer of nutrients from the mother to the fetus even when she is poorly nourished. However, this study demonstrates that maternal supplementation under these circumstances can improve birth weight. The newborns of supplemented mothers weighed 2,970 g at birth and were 180 g heavier than their counterparts in the unsupplemented group (A Chávez and Martínez, 1979c). This 6.5% increase m birth weight as trivial it might seem, IS Important for several reasons. First, this was the beginning of the anthropometric differences that persisted throughout life. Second, 39% (14/39) of the newborns in the unsupplemented group, but only 7.5% (3/40) of those in the supplemented group, were low birth weight (< 2.5 kg) infants. Third, food supplementation was also associated with increased total length, leg length, thorax circumference, ratio of head to thorax circumference, and ratio of leg to total length (A Chávez, 1978).

An important question is whether the decline in breast milk production even in the supplemented mothers is due to maternal malnutrition or is a natural phenomenon in the human species. The latter is a possibility, because all mammals follow a parabolic pattern of milk production, with a short incremental period and a long and progressive decremental stage. There is no reason for the human species to follow a different pattern of lactation. To respond to this question, the women who were supplemented during pregnancy continued to be supplemented during lactation. The total milk volumes plotted in Figure 1 show remarkable between-group differences. As with other mammals, breast milk production among supplemented women followed a parabolic pattern, peaking at four months, followed by a gentle decline.

The literature indicates that in developing countries, children begin to slow their growth at about three months of age. Therefore, it is important to consider the role of breast-feeding in the future of the child. A key finding from this study is that intake or production of breast milk in the unsupplemented group increased during the first eight weeks of lactation and fell thereafter (Martinez and Chávez, 1971). In the supplemented group it increased at least to 16 weeks. Unfortunately, milk volume measurements were not taken within the 8- to 1 6-week interval. However, by 16 weeks the milk volume had already decreased.

At eight weeks, the infants of unsupplemented mothers were consuming 32 ml per nursing episode, and by 16 weeks this figure decreased to 41 ml per episode. In Figure 2 a comparison of the breast milk intake per kilogram of body weight between the village children and Japanese children fed breast milk ad libitum with bottles indicates that the decrease in milk volume observed in the village after eight weeks is abnormal. This decline in breast milk production occurred despite the fact that children were breast-feeding about 13 times every 24 hours. Therefore, it is important to underscore that the decline in breast milk production is due to maternal supply and not infant demand. This decrease in breast milk production has important nutritional and developmental consequences for the child.

Chemical analysis of the milk samples indicated that the breast milk of unsupplemented women was not diluted according to the progressive pattern typical of other mammals. Unsupplemented women continued producing concentrated milk after their infants were eight weeks of age. By contrast, the milk of supplemented women was diluted beyond the expected range. Figure 3 includes the consumption of breast milk solids and shows that both groups of women secreted the nutrients following a pyramid-type pattern, although the peak is sharper among supplemented women. The peak for supplemented women was followed by a more gradual decline in the concentration of nutrients in breast milk after the infants were 3 months of age.

The between-group difference in the nutrient content of breast milk was 16% less in the supplemented group during the first eight months of life of the child. Although this difference does not seem large, it is important to underscore that it was greatest between 8 and 24 weeks. During this short period of time, the unsupplemented children ceased to be able to obtain all the breast milk that they demanded. To a certain extent, this also happened with the supplemented children, although in this case this phenomenon was observed at an older age and with a more gradual onset.

The decline in breast milk consumption by the children of poorly nourished mothers that begins at two to three months of age is the first insult that leads to malnutrition during early childhood. This situation could be easily corrected by introducing complementary foods available in the household by three months of age as required to maintain weight gain.

Figure 4 shows the between-group differences in energy intake. The deficiency in energy intake in the unsupplemented group begins at 12 weeks and is not corrected later. By eight months of age, the between-group differences in nutritional status are not readily apparent to the observer, i.e., the unsupplemented children were not obviously malnourished. However, more detailed analysis of their nutritional status shows some impairments. Photographs confirmed that supplemented and unsupplemented mother-child pairs had different attitudes and different characteristics of the skin, adipose and muscular tissues (Chávez and Martínez, 1982).

By eight months, the unsupplemented children had already been exposed to two nutritional insults. The first occurred in utero due to a deficient transfer of nutrients across the placenta. The second occurred at about three months of age due to a decrease in maternal breast milk production. In view of these insults, why were there so few clinical manifestations? First, breast-feeding allows infants to recover partially from the in utero insult. During the first three months of life, the infant has access to an abundant supply of milk and grows at a very fast rate. Second, biological mechanisms protect the child against nutritional insults. This is illustrated by the fact that the child can maintain lean tissue at the expense of his fat reserves. Another coping mechanism is a reduction in physical activity. This hidden malnutrition is likely to have negative long-term consequences for the future development of the child, even though dramatic effects are not evident by eight months of age.

FIGURE 4 Mean calorie consumption per day by age during the first two years after birth by infants whose mothers received food supplementation during pregnancy and who were given complementary feeding when growth began to falter (upper diagram) compared with the caloric intake of infants whose mothers were unsupplemented and who received only the complementary food spontaneously provided by the family (lower diagram).

As shown in Figure 5, the between-group difference in weight is small at eight months. Furthermore, it is still not possible to detect significant differences in the infants' utilization of nutrients, physical activity, or behavior. However, some indicators show consistent differences. Perhaps the most pronounced differences can be seen in neurological development both at birth and during early infancy (Rodríguez et al., 1979). By eight months, the unsupplemented child had less reflex control and poorer psychomotor development (A Chávez et al., 1975). There were also some behavioral differences. Unsupplemented children cried more, played less, and had less than optimal family interaction (A Chávez and Martínez, 1975).

The fact that there were no obvious clinical manifestations of malnutrition up to eight months of age has led some people to recommend exclusive breast-feeding for a minimum of six months. However, this study does not support this argument, since the breast milk supply begins to decline by three months, and small developmental, biological, and behavioral deficits begin to appear. These deficits become larger as the child grows older in a socioeconomically deprived environment.

In short, on the one hand, children who reach eight months of age with acceptable growth, such as weighing more than 8 kg, will be more likely to crawl, to demand attention, and to have better immunological defenses. On the other hand, a child who reaches eight months under adverse conditions, grows less well, has a poor appetite and low levels of physical activity and social interaction and is likely to become more malnourished.

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