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Even though breast-fed, socioeconomically disadvantaged children living in developing countries go through a period of particularly high health risks between 8 and 20 months of age. The most vulnerable children die during this period that can be characterized as the "valley of death. " The vast majority of those individuals who survive this period are the "vulnerable survivors."
The child needs to have adequate reserves to survive the passage through this period. The valley of death represents both a biological and a cultural reality. It is a biological phenomenon because it is linked with nutrition and infections. It is also related to culture because it is in part determined by child-rearing practices. Both adverse cultural and biological factors are present simultaneously during weaning and illness. In the valley of death, there are three situations in which feeding practices and health interact with each other.
The first is related to the finding that by eight months, the mothers, both supplemented and unsupplemented, cannot produce enough milk to meet the nutritional demand of their infants. At around this age, the volume of milk produced plateaus at about 450 ml per day. It is likely that this is a common situation among poor people, since similar findings were obtained in an urban area (Pérez-Hidalgo, 1970). This amount of breast milk is valuable for the nutrition of the infant. Therefore, prolonged breastfeeding is recommended for those women who do not have enough resources to obtain and safely handle cow's milk or a combination of foods. Although breast milk should be a major component of the infant's diet during the valley of death, it is also important to feed clean digestible foods as soon as possible.
The second feeding problem that occurs during this period is the tendency of children of this age to develop anorexia when the organism is exposed to an insult, particularly an infection. The anorexia during the passage through the valley of death contrasts with the good appetite of children younger than eight months who demand to be breast-fed even during episodes of severe diarrhea. This is desirable, because the infant replenishes nutrients that are being lost because of diarrhea. Some of this anorexia could be due to malnutrition, or perhaps it is normal at this age since the same phenomenon is observed among well-nourished children.
The third issue that needs to be considered is that during this period many children are weaned from the breast. Earlier it was believed that this was the cause of malnutrition, because the children were abruptly weaned without being offered foods of adequate protein quality and content. There is no doubt that weaning from the breast is an important event; however, it is often done at an age when the child is already malnourished. In fact, it is possible that women decide to stop breast-feeding because they notice an insufficient milk supply long before weaning. In the case of Tezonteopan, weaning from the breast during this period was not an issue, since only three of the unsupplemented women stopped breast-feeding before 20 months, and this did not pose a health risk to their children at this time.
A second period of decline in breast milk production was observed when the children were about 13 months of age. This is often associated with a new pregnancy. According to common wisdom, when a mother becomes pregnant during the period encompassing the valley of death, the child becomes jealous and changes his personality. What happens in reality is that the malnourished child becomes sad and irritated, and cries frequently. These signs could be interpreted as indicators of an increase in the severity of malnutrition related to the low milk supply produced by the mother.
The other biological phenomenon characteristic of the valley of death is related to infections, since this is the period when the child loses the passive immunity received from his mother and has acquired only limited active immunity. It is also the time when the child moves around in unsanitary areas and foods contaminated with pathogens are introduced. While not all immunity is lost by eight months, the epidemiological observations, however, show clearly that the supplemented and unsupplemented children had different patterns of frequency, duration, and severity of infectious diseases (Figure 6).
The role played by culture is similar to what has been reported for other socioeconomically disadvantaged groups. For this reason, it is possible to talk about a culture of poverty during the valley of death. In Tezonteopan weaning foods are introduced very late and in small quantities at about eight months of age. These foods are often withdrawn from the infant's diet with illness, particularly fevers and diarrhea, without taking into account the nutritional needs of the child. Another example is the practice of giving the child a corn tortilla to lick. Every time the tortilla falls down, the caretaker picks it up and gives it back to the child, even though it has dirt on it. The child is not able to ingest the tortilla and for this reason it obtains a minimum nutritional benefit from it. The same could be said of other foods that were given to the unsupplemented group, such as atoles and soups. Very frequently these foods contain fewer nutrients and are contaminated.
The differences in energy consumption after eight months between the supplemented and unsupplemented groups can be seen in Figure 4. In the supplemented group, the energy intake increases gradually, following the children's requirements. In the unsupplemented group, on the other hand, energy intake declines and reaches a nadir at about 10 to 11 months of age, unfortunately. At this point, the intake of non-breast-milk foods is still very small. Given the low nutrient intakes observed among the unsupplemented group in the valley of death, it is surprising that children survive and even show a small advance in their development. At two months of age, when the child weighs about 4 kg, he obtains almost 500 kcal from breast milk. Afterwards the energy intake declines from breast milk.
The growth curve shown in Figure 7 corresponds to the increments in body surface (Wetzel plot) and shows that by the third month, the growth of the unsupplemented child begins to falter in relation to that of the supplemented child. This difference becomes more pronounced between four and eight months of age. The figure represents the averages of 17 cases that were followed closely. However, if individual cases were plotted, a zigzag pattern with arrested, accelerated, or decelerated periods of growth would appear. This is due to episodes of illness that have negative growth effects through direct biological mechanisms (i.e., altered metabolism, anorexia, reduced absorption) and exogenous cultural mechanisms (i.e., withdrawal of solid food).
The growth patterns of supplemented and unsupplemented children differ not so much in the number and severity of infections as in the speed of recuperation from infections. Supplemented children had frequent episodes of infections during this period, and their growth and appetite were also affected. However, they recovered sooner from illness and ate very well while recovering from infections. Their anthropometry was better than that of the unsupplemented children. Between 6 and 18 months, the supplemented children grew less than normal, but they returned rapidly to their expected growth pattern between 18 and 24 months. The unsupplemented children recover very slowly, and before they can catch up fully, another episode of infection commonly occurs.
With the findings from this study, it is possible to clarify the relative importance of malnutrition and infection as determinants of child health in developing countries. Several researchers insist that infectious diseases are the main determinants, but this study shows that supplemented children are able to recover from infections sooner. This observation allows us to ascertain that nutrition is a more important determinant of child health than disease, because a well-nourished child is able to recuperate and return to his normal growth pattern in spite of suffering frequent episodes of infectious diseases.
It is not clear how the unsupplemented children can survive the valley of death while consuming less than 500 kcal/day and facing so many illnesses. However, the two principal factors are their reduced body size and less physical activity (A Chávez et al., 1972). Figure 8 shows clear between-group differences in physical activity.
There was no apparent between-group difference in physical activity at eight months of age. It is possible that the method of measurement of physical activity (i.e., the number of times that the feet touched the side of the crib) was not sensitive enough to pick up differences, because it is common to wrap the infants with blankets in the study village. After 10 months of age, however, the differences were remarkable, showing that as they grew older, the supplemented children increased their physical activity whereas the unsupplemented children did not.
As in other underdeveloped communities, almost all the children developed clinical signs of malnutrition at some point during the study. However, their symptoms were transient and improved even without medical care. Cross-sectional studies conducted in underdeveloped villages have reported similar nutritional findings to those encountered in Tezonteopan. Only 26.3% of the children under five years of age can be classified as having type II or type III malnutrition (i.e., moderate to severe malnutrition). This would suggest that the nutritional status of the population is heterogeneous. This is misleading, however, because the studies have examined children of different ages and at different stages of nutritional stress.
A frequency distribution of the nutritional status of the 41 unsupplemented children indicated that 14.6% were severely malnourished (i.e., type III malnutrition) when they were experiencing their worst nutritional status, 78.1% had type II malnutrition at worst, and only 7.3% had no worse than type I malnutrition at some point during the study. This is the real distribution of malnutrition in the community and is different from the prevalence estimates. With a cross-sectional study, it would have not been possible to detect these high levels of severe malnutrition, because all the children do not become malnourished at the same point in time and several of them could have already been dead when the study was conducted. Therefore severely malnourished children in the sample did not die in the Tezonteopan study, because they received medical care as soon as they began to become severely malnourished if they were not recovering spontaneously.
The previous data show that underdeveloped regions can have only a moderate prevalence but a high incidence of moderate to severe malnutrition. Therefore malnutrition can be the underlying cause of mortality during the critical period of human development studied in Tezonteopan. Furthermore, prenatal malnutrition associated with low birth weight, immaturity at birth, and low breast milk output after two to three months increases the relevance of nutrition for public health.
There is no doubt that malnutrition between 8 and 20 months adversely affects neurological function and other phenomena that have social repercussions. The low energy intake in the unsupplemented children and their reduced levels of physical activity are directly related to behavioral outcomes such as longer sleep periods and desire to remain in the crib for longer periods of time. It is also possible that malnourished children are carried for longer periods of time on their mothers' backs because they do not move and remain quiet. It is also possible that the low levels of physical activity have an indirect relationship with the suboptimal level of stimulation and interaction between the fathers and siblings and the malnourished child (A Chávez et al., 1975; A Chávez and Martínez, 1975).
In sharp contrast with the unsupplemented group, the supplemented children were more active, slept less, and did not want to remain in the crib or to be carried by their mothers for a long period of time. Fathers were often involved with the care of the supplemented children and smiled at and played with their offspring. The siblings also had to participate sooner and more intensely in the care of the child. All these events brought relatively more stimulation and interaction to the supplemented children.
Although the differences in physical activity explain part of the differences in behavior, stimulation, and degree of interaction, there might be other factors that also contribute to explaining these outcomes.
It is possible that malnutrition by itself is related directly to several personality traits. The unsupplemented children were withdrawn and insecure, and they cried frequently. The crying can be attributed to hunger and to the request to be breast-fed. However, the facts that even after eight months of age these children still cried frequently and with anguish during periods of anorexia and had low levels of physical activity (Figure 9) indicate different personality traits of supplemented and unsupplemented children.
Between 8 and 20 months, the unsupplemented children did not smile at their fathers, played less by themselves or with other individuals, and felt secure only if they were close to their mothers. The need to be in direct physical contact was so strong that several of them held to their mothers with great force for prolonged periods of time (Figure 10). Several of the unsupplemented children were afraid of their fathers and siblings and did not like to be cleaned. They hardly ever vocalized and only communicated by crying (Figure 11).
In general, the results show that the malnourished child is very insecure, and this leads to a passive and dependent personality. These characteristics of infant behavior become even worse as a result of several cultural practices that are frequently found in underdeveloped communities. In general, the mothers do not take the initiative to stimulate their offspring. As a result, there is a poor maternal-child interaction, which is limited to breast-feeding when the child cries or simply swinging the child in the crib or carrying him on her back.
In the case of the supplemented group, it is clear that the children stimulated responses from other people, demonstrating that supplementary feeding can break the passivity and apathy in the family. The children initiated interactions not only with their mothers but also with their fathers, siblings, neighbors, and animals. The behavior of the supplemented children changed traditional cultural patterns, since the fathers became involved with the care of young children. This was possible because the supplemented children were too active and difficult to be taken care of by their mothers alone, and also had happy personalities that attracted the fathers.
The different behavioral characteristics of supplemented and unsupplemented children influenced their mental development scores. It is curious, however, that between-group differences in intellectual performance were present as early as two months of age.
The psychomotor development of the unsupplemented group was higher from birth up to four to six weeks of age, when the lines crossed. The results for adaptive behavior are shown in Figure 12. The results for the first two months of life are not shown, because the scores of both groups, and in particular of the unsupplemented group, were very high. The finding that children born in underdeveloped communities are "smarter" at birth has also been reported in Africa and Guatemala. However, it is an artifact, because the scores are reported as percentage of days ahead in development with respect to the birth date. Therefore, for example, a three-day-old child who has a psychomotor age of 15 days has an advantage of 520%. This child seems to have very precocious development, when in fact he is only 12 days ahead, which might be trivial for his future development.
Changes in adaptive behavior of children in the maternal supplementation group (-) compared with children of unsupplemented mothers (- - -).
It is also possible that being far ahead in psychomotor development might be a sign of delayed and not of improved development. It is possible that it represents a delay in cortical function which allows for the presence of hypothalamic reflexes, as has been observed in other mammals that stand, walk, and even run during the first hours of life. When the cortex matures, these reflexes disappear and the movements become voluntary.
A remarkable finding is that, beginning at three to four months of life, the developmental lines of the two groups cross, and the supplemented children score 10 to 20 points above their unsupplemented counterparts. As will be shown, in spite of the fact that the differences in mental development vary as a function of age and the specific test that is applied, these differences are present even at adult age.
There is concern about the meaning of results from Western-type mental development tests applied to rural children in developing countries. However, the between-group comparison in this study is a valid one, because both groups were equally rural and similar in their socioeconomic conditions.
The only potential confounder of the mental development results is the between-group personality differences. However, the fact that there were developmental differences very early in life, when there were still no differences in personality, demonstrates that the tests captured differences not only in personality but also in mental capacity. In domains such as language and social development, the between-group differential patterns presented oscillations. However, in tests of adaptive behavior and motor development, the unsupplemented children were constantly below their supplemented counterparts and at points almost reached the lower limits of normality.
The time trends in the figures suggest that the between-group developmental differences could have originated in utero. This is likely if the "early advantage" of the unsupplemented children in reality represents a developmental delay, because it would mean that the two groups were different from birth until adulthood. This could be the result of delayed neurological maturation in utero caused by poor maternal nutrition during a time when the brain is highly vulnerable.
However, another potential explanation for the poor development of the unsupplemented children is the lack of stimulation received from their environment, which is caused by their own withdrawn personality and low levels of physical activity.
Of the three factors that have been postulated, the authors think, based on their intensive contact with the maternal-infant dyads, that the low energy intake and physical activity of the children are the leading causes of poor mental and behavioral performance. If the brain is considered as a computer that cannot program itself but that is structured according to the needs of the user, it is possible to argue that the lack of stimulation received by the vulnerable survivor is what causes the important limitations on the development of the intellect.
The onset of low energy consumption, low physical activity, poor stimulation, and poor brain development takes place when the production of breast milk falls at around three months of age. The delay in the development of the brain increases until the age of 20 months and then stabilizes.
The interpretation of the results by the authors is reinforced by the fact that malnutrition after eight months of age has a clear negative impact on the development of language, which is essential for an adequate performance in the tests of mental development.
The developmental delays of the unsupplemented children stabilize at the end of the valley of death at 20 months of age. Afterwards their developmental curves run parallel to and always below those of the supplemented and reference children. As a result, the unsupplemented child leaves the valley of death as a vulnerable survivor.
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