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David L. Yeung
David Yeung is the Director of Corporate Nutrition at the H. J. Heinz Company.
Mention of the names of firms and commercial products does not imply endorsement by the United Nations University.
Iron deficiency, one of the most prevalent problems of micronutrient malnutrition, occurs in both developing and industrialized countries. The impact of iron deficiency and iron-deficiency anaemia on the individual can result in lifelong disadvantages. The causes of the problem are many, but the principal cause is lack of iron-rich food. The International Conference of Nutrition sponsored by the World Health Organization (WHO) in Rome in 1992 estimated that over 2,000 million people worldwide suffer from anaemia, most of which is related to iron deficiency. Infants and young children are decidedly vulnerable groups, for a number of reasons. Their food choices are limited. The amount of food they consume is relatively low, but the demand for nutrients is high. Experience from industrialized countries indicates that one of the best strategies to eliminate or markedly reduce micronutrient malnutrition globally is through food fortification, with the goal of increasing the level of consumption of added nutrients to improve the nutritional status of the target population.
The current recommendation for infant feeding to ensure good iron status is breastfeeding for at least four to six months. The range of iron bioavailability in breastmilk is 50% to 80%, probably because of the presence of lactoferrin, which enhances iron absorption. Thus, it is not surprising that the prevalence of iron-deficiency anaemia in early infancy is inversely correlated with the incidence of breastfeeding. If breastfeeding is not possible, iron-fortified formula should be substituted. By about four to six months, an exogenous source of iron is required. The limited food choices and the few iron-rich foods generally available make fortification of complementary food mandatory. Iron-fortified cereal has been demonstrated to be one of the most effective food vehicles in combating iron deficiency. It is usually the first solid introduced to infants to supplement breastmilk. Clinical research in China, Chile, and Canada has shown that the iron is bioavailable and the iron-fortified infant cereals are effective in the prevention and treatment of iron deficiency. In the United States the use of iron-fortified infant formula and cereal has significantly reduced iron deficiency among infants and pre-schoolers. Many other examples illustrate the importance of the food industry and food fortification in combating micronutrient malnutrition. The Global Plan of Action advocated collaboration among governments, non-governmental organizations, the private sector, local communities, etc. in the elimination of the problem. It is clear that without the food industry, iron-rich foods will not be available. Support and recognition of public health organizations must be given to the food industry to encourage the development of affordable and culturally appropriate iron-fortified foods.
Infancy is a time of rapid physical growth as well as physiological, immunological, and mental development. During the first year of life, nutritional requirements are at their highest in the entire life cycle. Deficiency in energy or any of the essential nutrients can have dire consequences, some of which are long-lasting. In the first four to six months of life, the infants nutritional requirements can be totally satisfied by breastmilk. Afterwards, complementary foods need to be introduced to augment energy and nutrient intake.
Complementary foods are, therefore, transitional foods consumed between the time when the diet is composed exclusively of mothers milk and the time when it is mostly made up of family foods. Complementary foods are consumed during the relatively short period from around 4 to 6 months to about 12 months of age. During the time they are consumed, complementary foods make up a large proportion of the babys diet and contribute a significant amount of the nutrients that are necessary for growth and development.
The foods, therefore, must contain sufficient amounts of the essential nutrients to complement milk. Infants who do not receive enough complementary foods may be stunted or malnourished or both.
Among infants and pre-schoolers, the more prevalent forms of nutrient deficiencies are those of iron, vitamin A, iodine, protein-energy, riboflavin, calcium, and vitamin D. According to international agencies, millions of children suffer from deficiencies of iron, iodine, and vitamin A . The incidence of these problems is markedly higher in developing countries; however, infants in industrialized countries are not spared. Iron deficiency has no borders, and in industrialized countries, approximately 15% of infants consume insufficient amounts of dietary iron .
Depending on the nutrient and the severity of deficiency, the consequences of malnutrition may include growth stunting, anorexia, susceptibility to infections, behavioural changes, and learning disabilities. The latter may have lifelong effects. For example, research has found that iodine deficiency  and iron-deficiency anaemia  during infancy can cause mental retardation or inferior psychomotor function in childhood, even after the deficiencies have been corrected. The causes of these problems are multifactorial and include poverty, ignorance, faulty feeding practices, infections and infestations, food scarcity, consumption of foods of low nutrient density, and low bioavailability of food nutrients. Here, the focus is primarily on the nutrient content and bioavailability of the nutrients in complementary foods.
Infants are particularly susceptible to nutrient deficiency, for a number of reasons. Their food choices are limited. The amount of food they consume is relatively low, but the demand for nutrients is high. By and large, the primary cause of undernutrition during infancy is a lack of suitable nutrient-dense complementary foods during the weaning period. The underlying reasons for this are many. Experience from industrialized countries shows that one of the best ways to ensure that infants consume all the essential nutrients in adequate amounts is to provide culturally acceptable foods that are affordable and fortified with the nutrients that are commonly missing in traditional diets. Indeed, one of the major strategies to eliminate or markedly reduce micronutrient malnutrition globally is through food fortification  (M. C. Cheney and N. S. Lee, personal communication, 1993). Fortification of complementary foods adheres to the following recognized principles: the food to be fortified is habitually accepted and consumed by the target population; the food is a suitable vehicle for the nutrient to be added; the nutrient is stable and bioavailable over the intended shelf life of the product; the amount of the nutrient added is biologically meaningful but not high enough to cause toxicity or adverse reactions; the organoleptic properties of the food are not altered in a negative way by the addition of the nutrient; and the food is affordable by the target population [5-7]. The goal of food fortification is to increase the level of consumption of added nutrients to improve the nutritional status of the target population, which, in this case, is the infant population.
In industrialized countries the fortification of complementary foods is strictly regulated in terms of which foods are to be fortified, which nutrients are to be used as fortificants, and the minimum levels of the nutrients that may be added to a particular food. For example, juices may be fortified with vitamin C, and infant cereals are usually fortified with iron, calcium, phosphorus, thiamine, riboflavin, and niacin. Enrichment with protein is mandated, particularly if the cereal is not intended to be reconstituted with milk or formula. In certain situations, infant cereals may also be permitted to have added iodine, zinc, vitamin A, vitamin D, and other micronutrients. Meats, fruits, and vegetables are usually not fortified, although in the United Kingdom meat products for infants do contain added iron. In effect, if conditions require it, any food can be fortified with any nutrient, provided the principles of fortification are abided by and government regulations permit it.
In most societies nutrient-fortified cereals are the first complementary foods to be introduced to infants, sometime between four and six months of age. They are followed by vegetables, fruits, fruit juices, and meat products. By following this progression, a balanced diet containing all the essential nutrients can be achieved when the infant reaches eight to nine months. This dietary regimen obviates the need for nutrient supplements.
Iron deficiency is one of the most prevalent forms of malnutrition in the world. According to the report on Preventing Specific Micronutrient Deficiencies  of the 1992 International Conference on Nutrition (ICN) sponsored by the World Health Organization (WHO) in Rome, approximately 2,000 million people worldwide suffer from anaemia, mostly due to iron deficiency. The incidence of iron deficiency without anaemia is far greater than that of iron-deficiency anaemia. Virtually all countries are afflicted with the problem. The highest incidences occur in developing countries. The most afflicted groups, in descending order, are pregnant women, pre-school-age children, infants, other women, the elderly, school-age children, and adult men. The major causes of the problem are inadequate amounts of iron in the diet, low bioavailability of dietary iron, parasitic infestation, and excessive blood loss. In developing countries and in disadvantaged areas where the environment is unsanitary, all the above causes of iron deficiency may be present, whereas in industrialized countries where good health care is available, the main cause is a lack of sufficient amounts of available iron in the diet. This may be due to lack of foods rich in iron or poor food choice.
Iron is involved with a number of enzymes that are required for oxygen metabolism; thus, iron deficiency has important health implications. Iron-deficiency anaemia reduces oxygen-carrying capacity and interferes with aerobic functions . For older children and adults, it is well established that the work capacity and productivity of anaemic persons are much below those of non-anaemic persons . Very severe anaemia is associated with increased mortality during childhood and pregnancy .
Recent research has shown that there is a relationship between iron nutritional status and cognitive development in young children . Infants with iron-deficiency anaemia are easily fatigued, are more irritable, and have shorter attention spans. They also do less well in tests of psychomotor development during later childhood than those who were not iron-deficient in infancy. This effect is apparent even after the iron-deficiency anaemia has been reversed. The magnitude of the psychomotor deficit in childhood associated with iron-deficiency anaemia during infancy is approximately one standard deviation. However, iron deficiency without anaemia is not associated with psychomotor deficits. Thus, iron-deficiency anaemia during infancy may have long-term and irreversible adverse effects on cognitive development.
Iron deficiency has also been shown to increase the risk of childhood lead poisoning. Reports published in the United States showed that the prevalence of lead poisoning was three to four times higher among young children with iron deficiency than among children without iron deficiency . There is evidence that the absorption of iron and other divalent metals such as lead and cadmium is more efficient in iron-deficient persons. Thus, preventing and controlling iron deficiency during infancy and early childhood has important public health implications as well as implications for national development.
The current recommendation to ensure good iron status is to breastfeed babies for at least four to six months, and longer if possible . If breastfeeding is not possible or is terminated, the baby should be fed an iron-fortified infant formula until 9 to 12 months of age. At around 4 to 6 months, iron-fortified infant cereals are suggested . This should be continued until the child reaches two years or more. Fruit juices should be given along with the infant cereal to enhance iron absorption. Cows milk should be avoided until the infant reaches 9 to 12 months of age because it has a low iron content, interferes with iron absorption, and can cause microhaemorrhages in the small intestine .
Breastfeeding protects the young infant from iron deficiency. The level of iron in breastmilk is relatively low, but its bioavailability is in the range of 50% to 80%, probably because of the presence of lactoferrin, which enhances iron absorption. Exclusively breastfed infants have been shown to receive sufficient iron to sustain normal status until at least four to six months of age . Thus, it is not surprising that the prevalence of iron-deficiency anaemia in early infancy is inversely correlated with the incidence of breastfeeding, i.e., the higher the incidence of breastfeeding, the lower is the incidence of iron deficiency.
Cereals are usually the first solid foods given to infants, because they are readily available and culturally acceptable staple foods. They are introduced to infants at around four to six months to supplement breastmilk . It has been demonstrated that the addition of nutrients to cereals and cereal products is one of the most effective ways of combating nutrient deficiencies. In many countries, commercially prepared infant cereals are fortified with iron, and their wide consumption has contributed to lower incidences of iron deficiency. A number of forms of iron are recommended for use . However, the final choice depends on the availability of food-grade iron, the reliability of the supply, and compatibility with the process. In the past sodium iron pyrophosphate was used, which has since been found to be of low or variable bioavailability [17, 18]. Since 1972 it has been replaced by electrolytically reduced iron of small particle size that was deemed to be bioavailable.
In 1987 the bioavailability of electrolytically reduced iron was questioned . Short-term feeding studies using natural isotopes did not resolve the question. Furthermore, studies of persons with good iron status tend to underestimate bioavailability. Subsequently, large-scale clinical studies were conducted in Chile  and Canada . In both studies, normal and regular consumption of infant cereals fortified with electrolytically reduced iron was found to be efficacious in preventing iron deficiency.
The study in Canada was conducted to determine whether electrolytically reduced iron added to infant cereals was actually available for utilization by infants between 6 and 12 months of age. A six-month, double-blind trial involved 110 healthy term infants. All the infants were well-nourished and had good iron status. One group received 25 g per day of infant cereals containing 30 mg of added iron per 100 g. The control group received the same amount of non-fortified cereals. Other iron supplements were not included. Blood was collected monthly by fingerprick from each infant for determination of serum ferritin and haemoglobin. If ferritin fell below 10 mg/L, a putative end point was declared. Anthropometric measurements were performed to monitor growth of the infants.
At the completion of the study, the parents were offered a one-month supply of an iron supplement providing 8 mg of iron as ferrous sulphate per day. The parents were also asked to allow an additional blood sample to be taken at the end of the one-month period. The purpose was to assess iron storage in the two groups of infants. The extended study included 91 of the 110 infants. The results showed that significantly fewer infants given iron-fortified cereal were at risk of reaching low haemoglobin values at the end of the six-month trial period than controls. Furthermore, the infants who received iron-fortified cereal had lower haemoglobin and serum ferritin responses to the ferrous sulphate supplement than controls. Thus, the infants who received iron-fortified cereal had better iron status and greater iron storage than those who did not. This study confirms the efficacy of iron-fortified infant cereals in reducing the risk of iron deficiency. Indirectly, the results show that the iron is bioavailable. Since the infants had good iron status at the start of the trial, the study tested the utilization of the fortification of the iron under the most challenging conditions. Two recent studies in Chile  and Canada (G H. Beaton et al., personal communication, 1995) confirm the results of earlier studies in Canada  and China  showing that infant cereals fortified with electrolytically reduced iron and ferric ammonium citrate, respectively, were efficacious in reducing iron deficiency.
There is also evidence that wide usage of cereals is effective in preventing iron deficiency in a population. For example, a study in Canada showed that close to 96% of infants aged 4 to 10 months were customarily given the cereals, and that the cereals were clearly the main source of iron in the infants diets . It was apparent that the recommended dietary allowance for iron could not be met without the presence of iron-fortified infant cereals in the diet.
Further proof that iron-fortified infant cereals are effective in reducing iron deficiency was provided in a report of the Women, Infants and Children (WIC) Programme [2,23]. Regular consumption of iron-fortified infant formula and cereals by infants from disadvantaged families resulted in improved haematological indices of iron nutriture. Families in the WIC Programme were routinely provided with coupons for redemption of iron-fortified formula and cereal and vitamin C-fortified juice. Dietary assessment showed that these food items were indeed given to infants. Thus, the decline in the prevalence of iron deficiency in North America is attributable, in part, to the addition of a bioavailable form of iron in infant cereals and the widespread use of the cereals.
Experience in North America showed that the effectiveness of iron fortification of infant formula and infant cereals in reducing the incidence of iron deficiency was due to a number of important factors. Past social marketing had instilled wide awareness of iron-fortified foods. The forms of iron added are efficacious and the products are culturally acceptable and affordable. The use of iron-fortified infant formula and cereals is advocated by health professionals in accordance with recommendations of authoritative organizations, such as paediatrics and dietetics associations.
In summary, micronutrient malnutrition among infants and pre-schoolers remains a concern in many parts of the world. The causes are multifactorial. Nevertheless, the problems can be successfully managed if there is multisectoral collaboration. Food fortification of complementary foods is one solution. For this to be effective, the nutrients to be used as fortificants and the vehicles to which the nutrients are to be added must be clearly identified. Furthermore, the compatibility of the fortification system needs to be established, as outlined by WHO. Of importance is the clinical evaluation of the efficacy or bioavailability of the nutrient in the food vehicle. Population studies of the effectiveness of the fortification programme also need to be conducted. One area that has not been elaborated upon is the importance of nutrition education and appropriate product promotion and labelling with proper instructions for safe use; these are required to generate awareness of micronutrient-deficiency problems and to encourage use of the products by the target populations. Although emphasis has been placed on iron fortification here, the same principles and procedures should be followed for the fortification of complementary foods with other nutrients. Multisectoral collaboration, as exemplified in certain industrialized countries, can eliminate or at least drastically reduce micronutrient malnutrition among infants and preschoolers in developing countries in the not-too-distant future.
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