Although the focus of this article is nutritional rehabilitation, “rehabilitation” suggests that the insult has already occurred and that an intervention is needed to ameliorate the problem. This review stresses nutrition prophylaxis or prevention because these are the keys to a healthy childhood.
Research on children in the preschool age range is limited, therefore, this article identifies the most important contributors to morbidity in preschool children. The 10 leading risk factors globally in terms of burden of disease they cause are shown in Table 1(1). Together, these factors account for more than one third of all deaths worldwide. Of these 10 causes, 5 have direct relevance to preschool-age children, and 3 of the 5 are nutrition related. Clearly, nutrition has a huge bearing on the health of preschool-age children. The 3 nutrition-related causes include underweight, obesity and iron deficiency. This review focuses on these 3 conditions, on what the literature has to say about nutritional rehabilitation and prevention and what has been dubbed the “nutrition paradox” (2,3). This paradox is described as having underweight, obesity and micronutrient deficiencies in the same country, even in the same household at the same time.
All ages are at risk, but underweight is most prevalent among children under 5 years of age, and the World Health Organization (WHO) estimates that globally ≈27% of children in this age group are underweight. It is estimated that underweight was associated with 3.4 million deaths in 2000, including about 1.8 million in Africa and 1.2 million in countries in Asia. Underweight is considered to exist as a contributing factor in 60% of all child deaths in developing countries (1). Excluding North America and western Europe, there is a strong gradient of increasing child underweight with increasing absolute poverty (see Fig. 1). The strength of the association varies little across regions. People living on <$1/d generally are at 2- to 3-fold higher relative risk compared with people living on >$2/d. Clearly, poverty or the eradication of poverty will have a huge impact on underweight in children.
The etiology of underweight and growth deficits has been widely studied. Underweight and growth deficits are linked to impairment in terms of physical work capacity, cognitive skills and increased risk of morbidity and mortality. Thus, as reflected in the WHO documentation, these 2 factors are important. Underweight in preschool-age children is a combination of low birth weight, inadequate quantity and quality of complementary foods, limited breast-feeding and limited variety of appropriate postweaning foods. Combined with these nutritional causes of underweight are environmental conditions that predispose to poor child care practices and recurring infections. A lack of sanitary conditions, especially clean drinking water and refrigeration, exist as the cause of recurrent enteric infections, which lead to anorexia and chronic poor food intake.
Although it has been argued that there is a genetic component to the poor growth of preschool-age children in the developing world, several lines of evidence suggest that environment, including the social, political and economic environment, and not genetics explains growth faltering and underweight. Indeed, the consensus of research is that physical growth and development are sensitive indicators of the quality of the social, political and economic environment (4). For example, changes in birth weight and growth of children who emigrate to the developed world tend to support the role of environment. Ramakrishnan and Yip have documented that the mean birth weight of Chinese infants born in China are lower than Chinese infants born in the United States (5). Chinese infants born in industrialized countries do not show the typical growth faltering seen at 4 to 6 months of age. Wheeler and Swee (6) studied Chinese infants living in London in the 1980s. The families provided traditional Chinese foods as well as popular English foods to their children. These children grew at a similar rate to their UK counterparts for the first 2 to 3 years of life. Secular growth changes also reflect the role of environment in determining growth potential. Secular changes in growth in Chinese children in both China and Hong Kong between the 1960s and 1980s suggest that environmental constraints affected growth in the past. Growth and development surveys of children under 7 years of age in China reported a marked increase in both weight and length of infants from 1975 to 1985. This improved growth was possibly the result of the better economy and food availability. During the same time period, a similar change was observed in 2- to 18-year-old Hong Kong children and adolescents. It is interesting to note that as early as the mid-1980s there was a tendency for Hong Kong Chinese children to be overweight.
The second example is the migration of Mayan refugees from Guatemala to the United States (4). Guatemalan Mayans illustrate the “genetics versus environment” argument because at one point in history, they were considered a “pygmy” people of the Americas. They are, in fact, not pygmies. Comparing the height of Mayan children in their home villages versus those who moved to 2 cities in the United States, they are taller, heavier and carry more fat and muscle mass than Mayan children living in Guatemala. Within the same generation, Mayan children ages 4 to 14 years old growing up in the United States average 5.5 cm taller than their age-peers living in Guatemala. It is believed that the short stature of a population is a proxy for an ecology for human development that results in nutritional deficiency, excessive energy expenditure and poor health. Migration, in many cases, breaks the cycle of poverty into which Guatemalan Mayans are born. The political economy of Guatemala in the mid-1990s created an ecology for human development that deprived most Guatemalan Mayans of sufficient food, health care, drinking water, education and other basic needs. At the same time, the political economy of the United States offered economic, nutritional, educational and public health benefits unavailable to most Guatemalan Mayans.
The sample in Florida and California described by Bogin and Loucky (4) is, on average, taller than any sample of Guatemalan Mayans and taller than many samples of low-socioeconomic-status Ladinos of Guatemala. However, this American sample of the children of refugees is still significantly shorter in stature than the other ethnic groups in the towns in which they live. These results suggest that human phenotypes change at different rates for different traits. The present generation of Mayan refugee children is likely to be in the first stage of a process of increasing stature from generation to generation. Classic examples of this secular trend in growth of migrant children and more recent follow-up studies of these same populations show that over time the height of each generation of the children of migrants continues to increase until it converges on that of the host population. Perhaps the best example of this phenomenon comes from Mexican immigrants to the United States who have become taller on average, with each generation, since the 1930s. The most recent generation of US-born Mexican Americans under 12 y old has mean heights that are equal to the National Center for Health Statistics references (7).
Much of the existing research on the factors influencing plasticity in human phenotypes focuses on the physical environment, for instance, the hypoxia of high altitude, the cold and heat of extremes in latitudes or the nutritional stress experiences in traditional agricultural communities. Often, little can be done to alter the physical environment and variation in human physical and behavioural phenotypes is ascribed to inevitable accommodations to them. However, all people live within social, economic and political environments that also have powerful effects on human phenotypes. It is the author's hope that much can be done to change the social, economic and political environment to influence growth and undernutrition through peaceful change.
In his preamble to the 2002 WHO World Health Report, Dr Gro Harlem Brundtland stated, “Two of the most striking findings in this report are to be found almost side by side. One is that in poor countries today there are 170 million underweight children, over three million of whom will die this year as a result (1). The other is that there are more than one billion adults worldwide who are overweight and at least 300 million who are clinically obese. Among these, about half a million people in North America and Western Europe combined will have died this year from obesity-related diseases. Could the contrast between the haves and the have-nots ever be more starkly illustrated?” It has recently been suggested by Dr Benjamin Caballero that the combination of underweight in children and overweight in adults occurs at the same time in the same household in developing countries. He called this a nutritional paradox (2).
The nutritional paradox is most frequently found in developing countries undergoing economic transition. Nutritional transition may be defined as a country in the midst of changes in diet, changes in food availability and changes in lifestyle. These transitions typically occur in countries experiencing socioeconomic and demographic changes. Examples of these countries include Kyrgyzstan, Indonesia, Russia, Brazil and China. In such countries, as many as 60% of households with an underweight family member also have an overweight one, a situation that has been dubbed the “dual-burden household” (3). According to WHO statistics, among middle-income countries (ie, those with a per capita gross national product [GNP] of ≈$3000/y), overweight ranks fifth among the top 10 causes of disease burden, right below underweight (1). This is the same position held by overweight as a cause of disease burden in the developed world.
Traditionally, obesity has been linked with affluence and abundance, whereas undernutrition has been linked with poverty. As Caballero has suggested (2), it was anticipated that as developing countries improved their economic status and their GNP, undernutrition would improve and obesity would become worse, especially among members of the upper socioeconomic classes. The relationship between the economic status of a country and the prevalence of obesity is not straightforward, however.
HEALTHY RISK FACTOR TRANSITION
The nutritional transition encompasses changes in a range of risk factors and diseases. Traditionally, the dietary energy intake of the poorest people in a country may be limited by their inability to purchase enough food and the high energy demands of manual labour and daily survival activities. It is difficult for this group to achieve a net positive energy balance and therefore to gain weight. In more urbanized developing countries with a higher GNP, widespread access to television and mechanisation would favour sedentary activities and reduced daily energy expenditure. At the same time, as a country develops and more people buy processed food rather than growing and buying raw ingredients, an increasing proportion of energy tends to be drawn from sugars added to manufactured food and from relatively cheap oils. Alongside the change in diet, changes in food production and the mechanics of work and leisure result in a decrease in physical exercise. Thus, the consequent epidemic of diet-related noncommunicable diseases, including obesity, diabetes, hypertension and cardiovascular disease coexists with residual undernutrition, especially micronutrient undernutrition, and is projected to increase rapidly. For example, in India and China a shift in diet towards higher fat and lower carbohydrate is resulting in rapid increases in overweight among all adults in China and mainly among urban residents and high-income rural residents in India. Countries that have completed the transition to overnutrition are experiencing a continual increase in levels of obesity, as high-fat, high-energy and low-exercise lifestyles permeate their society. However, such a transition may not be inevitable, and a key challenge for policymakers is to generate a healthier transition.
It is somewhat self-evident that improvement in per capita GNP in countries in economic transition does not benefit all citizens equally. However, children under age 5 y are particularly at risk in this time of transition. For example, data from The World Bank show that the rates of poverty and underweight have actually increased among children under 5 y of age in urban areas of countries in socioeconomic transition. The reasons are not as esoteric as may be imagined. For example, families that move from rural to urban areas usually lose the ability to grow their own food, lose their contact with extended family and become dependent for their food on a cash market. It is also more likely that women who move to the city will join the labour force and therefore become less available to feed their children frequently or prepare food at home, relying more heavily on nonfamily-based child care and inexpensive commercially prepared foods for themselves and their families. Much of this store-bought food is high in fat and energy but low in micronutrients such as iron and zinc. For example, on a per-energy unit basis, a 5-y-old boy needs 5 times as much iron in his diet as an adult man. Cheap energy-dense, nutrient-poor foods may adversely affect the growth and micronutrient status of the child but at the same time may provide sufficient energy units for the adult to gain excessive weight.
The relationship between GNP per capita and dietary fat intake, expressed as a proportion of energy from fat, was studied for 88 countries and recently updated to include 121 countries (X. Guo et al., unpublished observation, 1999). Not surprisingly, there was a strong positive relationship between the 2, in other words, fat intake was higher in richer countries. There is 1 example, however, that goes against this trend: the Republic of Korea. Based on the regression equation between GNP per capita and dietary fat intake and using statistics from 1996, one could predict that the proportion of energy from fat in the Republic of Korea would be 35.5%. The actual percentage of energy from fat was 16.7%. This low level of fat intake may be part of the reason for the lower level of obesity in the Republic of Korea as compared with many other Asian countries. There are not many examples of societies successfully dealing with their own nutrition transition, but Korea is one example that is worth highlighting. The study, entitled Nutrition Transition in the Republic of Korea, describes a unique nutrition transition that has occurred in the Republic of Korea, a country that modernized earlier than most Asian countries. The analysis uses secondary data on economics, dietary intake, anthropometry and causes of death, including a series of comparable nationally representative dietary surveys (eg, the National Nutrition Survey).
The study addresses the question of why the fat intake in the Republic of Korea is low. The authors suggest 3 possible answers: (1) rice is still the staple food in Korea, so carbohydrate intake remains high; (2) cooking styles use small amounts of fat because traditional Korean cuisine adds small amounts of sesame oil to vegetables after they have been boiled or steamed, as opposed to Chinese cooking in which foods are stir fried in oil (with stir frying, there is a tendency to use more oil as the availability of oil increases); (3) there has been a strong, sustained national movement to retain the traditional Korean diet and cooking methods. Mass media campaigns promote local foods, emphasizing their higher quality and the need to support local farmers. A unique training programme is offered by the Rural Development Administration. Since the 1980s, the Rural Living Science Institute has trained thousands of extension workers to provide monthly demonstrations of cooking methods for traditional Korean foods such as rice, kimchi (a form of pickled and fermented Chinese cabbage) and fermented soybean food. These sessions are open to the public in most districts in the country, and the programme appears to reach a large audience. Although the combination of these 3 interventions may explain the low fat intake, with the lowering of trade barriers there is a trend to increasing obesity in young children, even in Korea.
A major impact of the nutrition transition, as previously mentioned, is the ingestion of relatively large amounts of energy-dense but nutrient-dilute foods. Because of the relatively high requirements for micronutrients by preschool children, they are at highest risk during the period of nutritional transition, but women of reproductive age and pregnant women are also at high risk for micronutrient deficiencies. For example, rates of iron deficiency and anaemia were higher in 2000 than they were in 1990. Thus, the control of micronutrient deficiencies is also high on the global priority list. We have done a reasonably good job in controlling iodine and vitamin A deficiencies with iodised salt and vitamin A capsules; however, the international nutrition community has not yet solved the problem of iron deficiency.
Recent WHO/UNICEF estimates suggest that the number of children with iron deficiency anaemia is >750 million (8). Iron deficiency is the most common preventable nutritional problem despite continued global goals for its control. Historically, the problem of iron deficiency anaemia in children largely disappeared in North America when foods fortified with iron and other micronutrients became available. In this group, the prevalence of iron deficiency anaemia has fallen from 21% in 1974 to 13% in 1994 (5). Although pockets of infants and children remain at risk, generally the eradication of iron deficiency in the West is recognized as a successful public health accomplishment. This solution has not worked in developing countries, where commercially purchased fortified foods are not available or are not used.
In the developing world, there are 3 major approaches available to address iron deficiency: dietary diversification to include foods rich in absorbable iron, fortification of staple food items including wheat and the provision of iron supplements. When dietary or fortification strategies are not logistically or economically feasible, supplementation of individuals and groups at risk is an alternative strategy. For the past 150 y or more, oral ferrous sulphate syrups have been the primary strategy to control iron deficiency anaemia in infants and young children (9). However, adherence to them is often limited due to a combination of their unpleasant metallic aftertaste, dark staining of the child's teeth and abdominal discomfort (10). Thus, despite the ongoing work of the UN Standing Subcommittee on Nutrition and others to solve the problem of poor adherence in infants and young children, all of the interventions to date have been universally unsuccessful (8–10). Our program in Toronto, the Sprinkles Global Health Initiative, has come up with what we believe to be 1 solution to the problem.
Our research group at the Hospital for Sick Children in Toronto conceived of the strategy of home fortification with Sprinkles, single-dose sachets containing micronutrients in a powder form, which are easily sprinkled onto any foods prepared in the household. We hypothesized that this would be a successful method to deliver iron and other micronutrients to children at risk (11). The idea of Sprinkles was formulated in 1996, when a group of consultants determined that the prevention of childhood iron deficiency anaemia was a UNICEF priority, yet the available interventions including syrup and drops were not effective (11).
In Sprinkles, the iron provided as ferrous fumarate is encapsulated within a thin lipid layer to prevent the iron from interacting with food. This means that there are minimal changes to the taste, colour or texture of the food upon adding Sprinkles. Other micronutrients including zinc, iodine, vitamins C, D and A, and folic acid may be added to Sprinkles sachets. Any homemade food can be fortified with the single-dose sachets, hence the term home fortification. Two formulations have been developed, a nutritional anaemia formulation (Table 1) and a complete micronutrient formulation (Table 2).
Over the past 5 y, we have completed 7 community-based trials in 4 different countries (12). The goal of these studies was to test the efficacy of Sprinkles in diverse settings. When we pooled data from 2 of our studies that compared Sprinkles to the reference standard, ferrous sulphate drops, we had a total of 518 anaemic infants (haemoglobin < 100 g/L) who were given 1 of 2 ferrous sulphate doses providing 15 or 40 mg of elemental iron as ferrous sulphate and 318 similar infants who received 1 of 4 doses of iron from Sprinkles providing 12.5, 20, 30 or 80 mg of elemental iron as microencapsulated ferrous fumarate. This gave us >97% power (α = 0.05) to detect whether the mean difference in end of study haemoglobuin concentrations between ferrous sulphate and Sprinkles regimens was within ± 5 g/L (a range of equivalence). Using a random effects model for study and dose that adjusted for baseline haemoglobin, we found no significant difference between Sprinkles and drops.
We further examined this through quantile-quantile plots of haemoglobin concentrations at the end of the studies for Sprinkles and ferrous sulphate drops. The overlaid plots of haemoglobin concentrations of the Sprinkles and drops groups demonstrate that these 2 distributions overlapped at all quantiles. These plots clearly indicate that the haemoglobin response to the 2 different forms of iron were equivalent. Thus, we have concluded that Sprinkles are as efficacious as the current reference standard for the treatment of anaemia. Overall, 55% to 90% of the anaemic infants who were provided with Sprinkles were cured.
Each stage in the evolution of the Sprinkles intervention has been evaluated in a controlled manner. We determined that the use of encapsulated iron did not appreciably change the taste or color of the food to which it was added; we showed that the haemoglobin response in anaemic infants was equivalent to the current standard of practice; and we documented the acceptability of Sprinkles among caregivers who used Sprinkles in their homes. Finally, through various partnerships, we have developed a successful model to scale up the intervention for countrywide use. A review of the progress and development of the Sprinkles initiative has recently been published (12).
In summary, the present review has identified the top 3 risk factors in terms of burden of disease, affecting preschool children. The impact of each factor on this age group has been assessed, and at least 2 examples of successful approaches to rehabilitation have been suggested.
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