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The consequences of hidden hunger for individuals and societies
Nevin S. Scrimshaw
Dr. Nevin Scrimshaw was the 1991 laureate of the World Food Prize, the foremost international award recognizing outstanding individual achievement in improving the quality, quantity, or availability of food in the world. Dr. Scrimshaw was the first nutritionist to receive this prize; all earlier recipients were recognized for efforts in production agriculture. He was honoured for accomplishments successfully linking food production and health, thereby alleviating hunger and malnutrition in developing countries. His achievements over five decades have substantially improved the lives of millions of people in dozens of countries around the world; more remarkable is that the nature of those achievements also enhance the future. His dedication to that ideal is evident in his leadership of this journal dedicated to disseminating information linking scientific, policy, and intervention activities related to food and nutrition. The Food and Nutrition Bulletin is pleased to publish the following paper based on his presentation at the time of the award ceremonies.
Cutberto Garza, Senior Associate Editor, Clinical and Human Nutrition
In 1991 the World Food Prize was given for the first time to someone whose life has been devoted to the processing, distribution, and consumption of food rather than to its primary production. Adequate food production for a growing world population depends on the continuing success of agricultural research and extension. But the conquest of hunger and malnutrition requires additional links in the food chain. These include post-harvest food conservation and storage, processing, and distribution, and' finally, consumption. Human need is not met and human demand is not effective unless people can consume an adequate diet.
Civil war and government oppression create refugee populations that furnish the news media with graphic pictures and heart-rending descriptions of dying children and wasted adults. While famines and the hunger of refugees periodically affect hundreds of thousands and even millions of people for limited periods of time, the silent emergency of hidden hunger chronically and often permanently damages hundreds of millions of individuals. I will try to convey the magnitude and consequences of the various kinds of hidden hunger that still devastate such a large proportion of the world's population and demonstrate that the conquest of hidden hunger is essential to the human future.
With modern communications, almost everyone in the western world is aware of the ravages of famine. The developed world tries to respond to each crisis, but only after great suffering has occurred, and it does little to prevent the next one. Because this kind of hunger is rooted in government cruelty, disinterest, corruption, and aggression, improved agricultural production can do very little for it. While drought may sometimes be an exacerbating factor, it is rarely famine's primary cause. As we have seen most recently in Ethiopia, Sudan, Somalia, and Iraq, it is government actions that result in desperate refugees. International assistance cannot eliminate hunger of this kind without changes in national government policy.
Wherever national disasters of flood or drought do occur, food can now be made available quickly to alleviate shortages if government policies facilitate the distribution of food that is available in other parts of the country or that can be rapidly supplied by international sea and air transport. Much more desirable than the alleviation of famine is its prevention. This is possible even where Hoods and droughts are common. The antifamine policies of India and China put an end to the frequent famines that ravaged these countries until as recently as the middle of this century. In 1971 nearly 15 million refugees fled to India to escape the civil war in East Pakistan. now Bangladesh. but, by using the food reserves it had built up and applying its famine-prevention experience, India successfully fed this huge population despite only limited international assistance. Yet famine was not prevented among recent and current refugee populations of Africa. because famine aid was obstructed rather than facilitated by the policies of the governments responsible.
Despite the public attention paid to famine and starvation, most of the hunger that is damaging the survival, development, and welfare of underprivileged populations is unrecognized. This is because, even when there are clinical symptoms, they are not associated with food intake. As shameful and tragic as is the occurrence of famine in today's world, its economic, social, and individual significance pales beside the tragedy of hidden hunger that afflicts a majority of the populations of most developing countries. It is this hidden hunger that is responsible for most of the excessive mortality and ill health afflicting developing-country populations, and for permanent impairment of physical capacity and cognitive performance. As already suggested, hunger. both overt and hidden, is largely the result of government policies . Overcoming hunger requires the implementation of policies that facilitate food production and increase social equity, improve nutrition and health, and reduce the burden of poverty. Foreign aid can do little to alleviate hidden hunger in a country without the active cooperation of its government.
The basic human rights are food, shelter, education, and opportunity for the future, and the most fundamental and urgent of these is food. International, bilateral, and voluntary agencies can and should be influential in promoting political changes that favour these basic human rights. However, ultimately the policies that governments adopt will determine the security with which their populations obtain these basic rights.
Chronic undernutrition in adults
I will first describe how the adaptive behaviour necessary to survive chronic dietary energy deficiency can have serious social and economic consequences. This statement requires explanation. The best available estimates of the dietary energy intakes of the populations in most developing countries indicate that they are significantly lower than the estimated requirements for their occupational patterns and lifestyles. The explanation is that. in order to survive, individuals must reduce their physical activity  Within limits this is a biologically successful adaptation, but its social and economic consequences can he severe.
In Central America, as in many other developing regions, workers are often paid by the task rather than by the hour because there is so much variation in the work that they accomplish in a given period of time. When all of their limited discretionary energy must be used for occupational work, there is nothing left over for household improvement, entrepreneurship, and the community activities upon which the development process depends. Such individuals are not lazy, as is so often thought, but are forced into inactivity in order to survive inadequate dietary energy intakes, a vicious circle in which they are trapped. They must adapt in this manner or die.
For example, Viteri and Torun [3,4] at the Institute of Nutrition for Central America and Panama (INCAP) observed that plantation workers walked home slowly from field work, remained sedentary for the rest of the day, and slept long hours. With supplementary feeding, their behaviour changed. They worked faster, walked home more rapidly' and had energy for home and village activities. In the Philippines, de Guzman et al.  found that, when poor families received supplementary food, more of their day was spent in moderate activities rather than sedentary ones. Moreover, for some activities, oxygen consumption per unit time increased, indicating that they were able to work harder per unit of time. In the Gambia it was found that energy-supplemented pregnant and lactating women participated more actively in village activities when given a food supplement . Road workers in Kenya experienced an increase of 12% in daily productivity with caloric supplementation . Physical performance has been linked directly to energy intake in many other studies (e.g. in Germany in World War II , Guatemala , Sudan  and Colombia ).
If the food energy available is less than can be compensated for by reduced physical activity, then lean body mass is lost as well. Loss of body cell mass lowers overall energy requirements and may permit a new metabolic equilibrium. There are many sophisticated ways of measuring lean body mass, but the simple relationship shown by weight in kilograms divided by the square of height in metres (body-mass index [BMI], or Quetelet's index) provides good results. ABMI below 18.5 can be taken as an indicator of one of three grades of chronic energy deficiency, without the need for activity analysis (table 1) [12, 13]. When various outcomes are measured by this criterion of undernutrition. the damaging consequences are evident .
TABLE 1. Grades chronic energy deficiency as indicated by body mass index (BMI)
Table 2 illustrates the association of higher mortality in Indian men with chronic undernutrition (data from Satyanarayana. 1991, personal communication). Table 3 shows the adverse impact of low BMI in Indian mothers on the birth weights of their offspring . Figure 1 (see FIG. 1 Relationship between body-mass index (BMI) and time lost from work because of illness by fathers in Bangladesh (data from ref. 13)) indicates the relationship found in Bangladesh between the father's BMI and the percentage of time not working because of illness . The fat-free mass of Guatemalan wage labourers has been shown to be correlated linearly with the amount of coffee beans picked per day. the amount of sugar cane cut or loaded, and the time taken to weed a given surface area . A loss in BMI has been observed seasonally in the Gambia , in Senegal , in Niger , and for women field workers in Ethiopia [20, 21].
TABLE 2. BMI and mortality in rural Indian men (deaths per 1,000 per year)
TABLE 3. Maternal BMI and birth weight in India
|Maternal status (CED, BMI)||% of mothers||Mean birth weight|
a. Grade of chronic energy deficiency (see table 1).
The classic experiments of Keys et al. during World War II  showed that, as the loss of lean body mass becomes progressively more severe and sustained in response to a deficient diet, it is associated with tiredness, muscle soreness, irritability loss of ambition and concentration. and moodiness and depression.
Protein-calorie malnutrition in children
Children are very susceptible to the effects of chronic energy deficiency because their requirements per unit of body weight are higher. INCAP researchers  observed the results of experimentally reducing by 10% the dietary energy intake of preschool children in a convalescent home who had previously been growing well on an ad libitum diet with adequate protein. During the following month there was a decrease in their activity that compensated for their reduced energy intake, and they continued to grow as before. When energy intake was reduced another 10% while maintaining the same amount of dietary protein, a further reduction in activity was not sufficient and their growth was affected. These observations, carried out under controlled conditions, reveal the impact of chronic energy deficiency on millions of children.
The children studied were fortunate, because they were promptly restored to a good ad libitum diet and quickly made up their growth loss and resumed normal activity. Reduced activity of children might seem to be of little consequence as long as growth is not affected. But it is the young child's interaction with the environment, including family members, that provides the stimuli for normal cognitive development. The reduction of this interaction in undernourished children may explain the findings of Cravioto and DeLicardie many years ago in rural Mexico [24, 25] that children in the lowest quartile of weight for age performed less well than those in the highest quartile on tests of intersensory perception. No association was found between test performances and weight for age in well nourished children from urban middle- and upper-income families.
Most young children in the lower socio-economic groups of underdeveloped countries become stunted during the weaning period, and they are likely to remain stunted when they enter school and as adults. Stunted adults have reduced work capacity, as has been shown in many different countries, including Colombia , Brazil , Ethiopia , Guatemala [9, 16, 29], and India [30, 31].
The causes of the chronic growth retardation that results in chronic stunting of preschool children are more complex than energy deficiency alone . Protein and micronutrients, as well as energy deficiency, are often involved. In addition, a high frequency of diarrhoeal and respiratory infections can result in protein-energy deficiency even when the diet would otherwise be adequate. Moreover, the high frequency and severity of infectious diseases among malnourished children in developing countries is due in large part to reduced resistance to infection resulting from malnutrition .
As Cravioto and DeLicardie and others [24, 25, 34-37] have shown, the effects of protein-energy malnutrition in early childhood go far beyond physical stunting. During 1969-1977, an INCAP study in two Guatemalan villages provided Incaparina, a highly nutritious vegetable mixture, to pregnant mothers and to their children during and after weaning for their first three years after birth. Their performance was compared with the children of two comparable villages in which only a low-calorie flavoured beverage was given to mothers and children [38, 39]. Concurrently, a somewhat similar study was under way in a rural Mexican village led by Adolfo Chávez of the National Institute of Nutrition [40, 41]. In both studies the supplemented children grew better, had fewer infections, were more active physically, and performed better on behavioural tests than did the non-supplemented controls.
Twenty years after the original study was started, the same investigators in the Guatemala study were able to return and re-examine most of the children, now adolescents and young adults, who had participated in the earlier programmes. The results were striking . Despite there having been no further interventions, the children who had received Incaparina maintained their height advantage and performed in a superior manner on the Central America Intelligence Test and on appropriate achievement tests when the groups were adjusted for the number of school years. Because the Incaparina group also completed more years of school, the overall differences between the two in test performance were even more pronounced . The relationship in this population of stunting to schooling is shown in figure 2 (see FIG. 2. Deviations from sex-specific means for the number of years of school completed in relation to stunting among subjects in rural Guatemalan villages. In both sexes, more severe stunting is associated with less schooling (data from H. Delgado, personal communication, 1991)) and to performance on a test of literacy in figure 3 (see FIG. 3. Deviations from sex-specific means for performance on a locally appropriate literacy test in relation to stunting among subjects in rural Guatemalan villages. In both sexes, more severe stunting is associated with poorer test performances (data from H. Delgado, personal communication, 1991)).
Very similar results have been obtained in the Mexican community (A. Chŕvez, personal communication, 1991). Thus, malnutrition at an early age affects not only the physical performance of adults but also their intellectual and social performance, a finding of tremendous significance for the future of developing countries and also for underprivileged children in industrialized countries. When genetic growth potential is reduced by undernutrition and associated factors, "small is beautiful" is a pernicious falsehood [44, 45].
Prevalence of undernutrition in children and adults
What proportion of the world's populations lives all or part of life in a state of chronic energy deficiency? If estimated energy requirements are compared only with average dietary energy intake figures, the problem is significantly underestimated because the higher income groups consume and waste more calories than they need , while the poorer groups are left with even less than they need. Table 4 gives an FAO estimate of approximately 512 million persons undernourished in 1985 . However, the FAO used a more stringent criterion than many of us feel to be appropriate. The World Bank estimate of 730 million undernourished persons in 1980 was more realistic, and the numbers are even greater today .
TABLE 4. Estimates of global hunger (millions)
Data involve 87 developing countries.
a. Ref. 47.
b. Ref. 46.
Figure 4 (see FIG. 4. Energy requirements as multiples of the basal metabolic rate (BMR) for maintenance and activity in adult men and women ) shows that an energy intake of 1.4 x BMR (40% above the basal metabolic rate) allows only for sedentary survival and not for the activity necessary for acquiring food or even for the maintenance of cardiovascular fitness . Sukhatme, the former head of statistics in the FAO, and Margen advanced the hypothesis that individuals subject to chronic food shortages could adapt at no cost to lower energy and protein intakes . Under the influence of this hypothesis, the FAO even calculated and published a figure for persons consuming less 1.27 x BMR "in case it should be confirmed that individuals could adapt to this figure." Despite this triumph of politics over science, the available evidence strongly refutes this misguided concept [2, 14, 50].
It should be emphasized also that estimates of food availability, food intakes, and energy requirements are each notoriously unreliable. By contrast, height and weight are measured directly and can be expressed as weight or height for age, weight for height, or body mass index or can be used longitudinally to determine growth in children. It is for this reason that anthropometric indices are more reliable indicators of undernutrition than the comparison of dietary data with presumed requirements.
Whatever the criterion chosen to determine the prevalence of undernutrition, a large proportion of the populations of most developing countries is found to be affected. Moreover, the situation is worsening in many countries under the pressure of economic adjustments imposed on those with large foreign debts. Figure 5 (see FIG. 5. Decrease in average calorie intake per capita in Mexico, 1975-1989 (data from H. Delgado, personal communication, 1991, from Mexican government sources)) shows a reduction in the per capita dietary intake in Mexico from 1975 to 1989 that is paralleled by an increase in infant mortality (see FIG. 6. Increase in mortality associated with nutritional deficiencies in preschool children in Mexico, 1980-1988 (data from H. Delgado. personal communication, 1991, from Mexican government sources). Compare this with the concomitant decrease in available calories shown in figure 5.). Even in Venezuela, a country with a once robust economy, a 20% drop was observed in the caloric intake per capita from 1983 to 1989 in a poor district of Caracas. Similar decreases have occurred in a number of other countries in Latin America and Africa. For all countries with chronic dietary energy deficits, the capacity of their low-income populations to respond to programmes for community development and home improvement are frustrated. Their capacity for productive work requiring moderate to heavy activity is also significantly reduced.
The most convenient and reliable basis for judging the prevalence of protein-calorie malnutrition in young children is retardation in physical growth. By this criterion, data compiled by the UN Subcommittee on Nutrition and by the World Health Organization show that from one-third to two-thirds of developing-country children show some degree of growth retardation. The First Report on the World Nutrition Situation in 1987  used a criterion of two standard deviations below the NCHI/WHO mean for well nourished children. By this standard, the proportion of underweight children varied from 25% in Africa to 70% in south Asia. Although percentages are decreasing in most regions, the absolute number of children retarded in weight and height continues to increase  INCAP has found that 95% of rural Guatemalan women are stunted. Height for age at the age of seven, when most developing-country children enter school, is a generally available and useful indicator. It not only reflects growth retardation during the early preschool years but also confirms its persistence.
A UNICEF global, regional, and country assessment of child malnutrition reported:
About 36% of children under five in the developing world, excluding China, or about 150 million are malnourished. About 39% or 163 million are stunted and 8% or 35 million are wasted. More than one in six malnourished children are suffering from severe malnutrition in terms of their weight for age, i.e., about 23 million children are severely malnourished. 
Another measure of the prevalence of undernutrition is the frequency of BMI below 18.5. It should be clear that this criterion includes only those individuals who have had to adjust biologically, not the additional persons who have adapted by restricting their physical activity sufficiently to conserve lean body mass. Nevertheless, when the figures are applied to population data, the extent of undernutrition in developing countries as judged by this index is still dramatic. In Ethiopia 63% of the population falls into one of the grades of undernutrition by this criterion . Table 5 shows that 50% of men in ten states of India are undernourished (W. P. T. James, personal communication, 1991).
TABLE 5. Prevalence of chronic energy deficiency in men in India (percentages)late 1980s
|CED grade||10 states||Hyderabad village||IFPRI rural village|
The importance of dietary protein
It is frequently stated that, if individuals and populations obtain sufficient calories from their usual diets, protein adequacy is assured. This generally true statement often leads to a false conclusion. All societies that have survived have found a way to supplement the protein of a cereal or root staple with other foods that improve the quality and quantity of protein in their usual diet. However, when societies or individuals, for economic or other reasons, are not able to obtain the complementary protein sources on which their adequate diet depends, high morbidity and even extinction ensue. Wherever individuals cannot obtain their usual diets because of poverty, war, civil disturbance, or natural disaster, attention to dietary protein becomes crucial.
Some of the confusion arises from a suggested protein allowance for adults proposed by the 1973 FAO/ WHO Expert Group on Protein-Energy Requirements that was much lower than in the past, while energy recommendations remained essentially unchanged . This led to a re-evaluation of developing-country diets and the conclusion that they were limiting in energy and not protein. Extensive multicountry research. sponsored by the United Nations University [55, 56], has established that the 1973 estimate for adult protein needs was much too low and that it needed to be increased by approximately one-third. This correction was made in the 1985 FAO/WHO/UNU report .
In addition, the 1985 and all previous committees on protein-energy requirements accepted an amino acid pattern for adults that underestimated essential amino acid needs per gram of protein by one-half to two-thirds. A joint FAO/WHO Expert Consultation proposed, primarily on the basis of research by Young et al.  using stable-isatope-labelled amino acids, that the 1985 amino acid reference pattern of FAO/WHO/UNU for preschool children  should be applied to persons of all ages except infants . This increased the possibility of lysine being the limiting amino acid in populations consuming high cereal diets, which makes improving the protein quality of cereal grain nutrients even more worthwhile than previously believed. Thus, the development of quality protein maize"  is a significant achievement for human as well as for non-ruminant animal nutrition.
The usual diets of healthy adults in most developing countries are rarely deficient in protein relative to calories, but those of the poorest families, particularly pregnant and lactating women and young children recovering from infection, are likely to be deficient in protein. Diarrhoeal, respiratory, and other infections are exceedingly common among underprivileged children because their resistance to infection is weakened by poor nutrition and their exposure to infection is increased by an unhealthy and contaminated environment. This susceptibility can be reversed by supplementation, as illustrated by data from a longitudinal study in Tezonteopan, Mexico  (see FIG. 7. Days of sickness due to infections in children 0-36 months old receiving nutritional supplementation in a rural Mexican village compared with children who received no supplement. After the first three months, when all were protected by breast-feeding, the supplemented group had progressively fewer days of sickness. The same relations held true for respiratory and intestinal diseases analysed separately, and for mild, moderate, and severe infections ).
Conclusions about the relative adequacy of protein and calories in developing-country diets are further biased by the use of averages instead of distributions that reveal the number of families on a low protein intake. They also neglect to allow for the increased protein intake needed to recover from infections. It is true, therefore, that the average diets of healthy persons in most developing countries are rarely deficient in protein relative to calories, but those of the poorest families and of children recovering from infection may be inadequate in protein.
An episode of infection in any individual worsens nutrition status [33, 60, 61] (see table 6). Recovery is usually rapid if the infection is acute, the individual is well nourished, and the diet during convalescence is adequate for rapid recovery. However, children whose nutrition status is marginal will be progressively depleted by repeated infections unless their diet allows for catch-up growth. Under these circumstances, the concentration and quality of protein in the diet becomes critical. The need for protein during recovery from infection may be double that for maintenance of a healthy child . Diets that would be adequate in protein for healthy children are seriously deficient for children in these circumstances. The severe protein-deficiency disease kwashiorkor is usually precipitated by prior episodes of infection in young children consuming marginal diets .
TABLE 6. How infection worsens nutrition status
|Decreased appetite||Always present with infection|
|Cultural and therapeutic practices||Some foods are withheld from individuals with infections|
|Malabsorption||A consequence of infections involving the gastro-intestinal tract|
|Catabolic losses||Urinary and nutrient losses always occur with infections|
|Anabolic losses||Nutrients are used internally for
formation of immunoglabulins
and other proteins essential to resistance mechanisms
|Fever||Increases energy requirement|
While I have emphasized the significance of chronic dietary energy deficiency because it is an indicator of inadequate food intakes, it must always be remembered that its correction requires an appropriate balance of available protein relative to calories in the increased food intake. When animal protein is limited for any reason, cereal and root staples must be complemented with legumes and oil-seed meals, which are more concentrated sources of essential amino acids and nitrogen. The development of high-protein-quality maize  and other potential improvements in the quality of other cereal proteins are desirable contribution, because their use can reduce the damage done when poor families cannot afford enough of the more costly animal and legume protein sources to complete their diets.
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