The Role of Fermented Milk in Complementary Feeding of Young Children: Lessons from Transition Countries

The role of fermented milk in complementary feeding of young children: lessons from transition countries

F Branca1* and L Rossi1

1Human Nutrition Unit, National Institute for Research on Food and Nutrition, Rome, Italy

Probiotic bacteria are used for production of fermented dairy products. The use of probiotic bacteria has the potential to replenish the natural intestinal flora of the body. These bacteria competitively inhibit the growth and colonization of pathogenic bacteria. Breastmilk is the best food for babies, also from a probiotic point of view. Human milk, in fact, contains many substances that stimulate the growth of bifidobacteria in vitro and in the small intestine of infants. Improvement of lactose digestion and avoidance of symptoms of intolerance in lactose malabsorbers are the most profoundly studied health-relevant effects of fermented milk. In fact fermented milks are nutritionally similar to unfermented milk, except that some of lactose is broken down to glucose and galactose. The role of fermented milk in complementary feeding and in particular for the prevention of anaemia is an innovative theme, recently focused. Iron deficiency in infants and young children is widespread and has serious consequences for child health. Prevention of iron deficiency should therefore be given high priority. The too-early introduction of unmodified cow’s milk and milk products is an important nutritional risk factors for the development of iron- deficiency anaemia. Fermented milks represent an excellent source of nutrients such as calcium, protein, phosphorus and riboflavin. During the fermentation of milk, lactic acid and other organic acids are produced and these increase the absorption of iron. If fermented milk is consumed at mealtimes, these acids are likely to have a positive effect on the absorption of iron from other foods. European Journal of Clinical Nutrition (2002) 56, Suppl 4, S16 – S20. doi:10.1038/sj.ejcn.1601676

Keywords: fermented milk; complementary feeding; stunting; anaemia; transition countries

Introduction content becomes inadequate and complementary foods Iron deficiency anaemia (IDA) is the most common nutri- have to play a major role. In most instances children’s tional disorder in the world. The World Health Organization diets contain little animal source foods, rich in haem iron, estimates that 43% of the world’s infants and children under little vitamin C and often contain inhibitors of iron absorp- the age of 4 y suffer from it (World Health Organization, tion such as tannins, present in tea. Such feeding practices 2000). Iron is present in a relatively low concentration in explain the peak prevalence of anaemia between about 9 and human milk but is highly bioavailable, so that exclusively 18 months of age. About half the infants in developing breastfed children have a low risk of IDA before 6 months of countries become anaemic by 12 months (Ross & Thomas, age. Young children are especially vulnerable to iron defi- 1996). The prevalence of anaemia declines substantially after ciency between 6 and 24 months. During this period of rapid about 2 y of age, because growth rates decrease and iron growth iron requirements increase and breastmilk iron requirements fall after the first year of life. However, in countries where intakes of animal products are low, and parasites common, the prevalence of IDA may remain high. Stunting is the second most common form of malnutrition in early life. The global prevalence of stunting in *Correspondence: F Branca, National Institute for Research on Food and children under 5 y is 33% in developing countries, but Nutrition, via Ardeatina 546, 00178 Rome, Italy. varies widely (ACC=SCN, 2000). East Africa has the highest E-mail: [email protected] prevalence (48%) and South Central Asia has the second Guarantor: F Branca. Contributors: FB wrote the manuscript and LR analysed field data and highest prevalence (44%). West Africa (35%), South East Asia collaborated in the revision of the paper. (33%), Central America (24%), North Africa (20%), the Fermented milk in complementary feeding F Branca and L Rossi S17 Caribbean (19%) and South America (13%) follow in order of to intestinal immaturity. On the other hand, late introduc- prevalence. The age of onset of linear growth-faltering has tion of complementary foods could lead to inadequate cover- been reported to start as early as immediately after birth age of energy and nutrient requirements, especially for iron (Backstrand & Allen, 1996) or as late as 6 months or more of and zinc, since breastmilk has insufficient density of such age (Dewey et al, 1992). Linear growth-faltering typically nutrients for older children. In fact micronutrient require- continues until children are about 18 – 24 months of age. ments in this period of rapid growth are crucial. Even in Usually, stunted children fail to catch up to the size of the children who are breastfed between 6 and 12 months, 90% of well-nourished children, although some reversal of stunting iron and 88% of zinc should be provided by complementary is possible if there are marked improvements in diet and foods. After 12 months iron requirements are lower and environment (Golden, 1994). Poor maternal nutritional continued breastfeeding can provide approximately 10% of status at conception and undernutrition in utero, inadequate the required iron and 20% of zinc, and still a substantial breastfeeding, delayed complementary feeding, inadequate quota should be provided additionally. quality or quantity of complementary feeding, impaired absorption of nutrients due to intestinal infections or parasites are all concurrent causes of infant malnutrition. Complementary feeding and malnutrition in Transition countries such as former Soviet Union countries transition countries and the Balkan states are characterized by low population A recent review of current recommendations for comple- density, high literacy rate, high employment rate but a low mentary feeding revealed some similarities, as well as many average monthly income. These areas suffered from the break- differences, among national and international organisations down of the central planning health system and the collapse (Dewey, 2001). Despite the recent WHO recommendation to of the socio-economic system, causing a marginal health and exclusively breastfeed until the age of 6 months, in many nutritional status particularly in high-risk groups. Since the industrialized countries a 4 – 6 month range is still used. In dissolution of the Soviet Union, there has been a dramatic some Western European countries, nutrition guidelines indi- decrease in life expectancy at birth and this decline is due in cate that if the child growth is normal it is not necessary to part to a rise in mortality among infants and young children offer any complementary foods before the age of about (Michaelsen et al, 2001). While protein-energy malnutrition 6 months (Michaelsen et al, 2001). In many countries of is a rare event, chronic malnutrition is widespread, spanning Eastern Europe, feeding guidelines have been influenced by from 5 – 7% observed in the Balkans, with a peak of 10% in the recommendations of the Former Soviet Union (URSS Kosovo, to 10 – 13% in the Caucasus and 30% in Central Asia. Ministry of Health, 1982). Poor complementary feeding In these countries, micronutrient deficiencies are the most practices help to explain the poor iron status and possibly important nutrition problems. In several countries anaemia is the high levels of stunting among infants and young chil- well above the 15% level, calling for immediate interventions: dren in the European Region, particularly in the countries of in the Balkans observed prevalence ranges between 19% of the former Soviet Union. Non-adapted formulas in the Soviet children in Kosovo and 41% in Serbian refugees; in the Union included diluted fresh or fermented cow’s milk with Caucasus between 16% in Armenia and 34% in Ingushetia; added sugar, vitamins and minerals from the age of 3 60% in Central Asia (Michaelsen et al, 2001). months. Cow’s milk diluted with cereal water was recommended from 2 – 3 months and additional fluids, primarily tea and water with sugar were also recommended as a Role of complementary foods in the coverage of complement to breastmilk. According to international micronutrient requirements recommendations, unmodified cow’s milk should not be Complementary feeding is defined as the provision of foods used as a drink, and milk products should not be given in or liquids along with continued breastfeeding. Complemen- large quantities before the age of 9 months. They can, tary food is the term used to describe any nutrient- however, be used in small quantities in the preparation of containing foods or liquids, other than breastmilk, that are complementary foods from the age of 6 months. Between given to young children during this period (Brown, 1997). 9 and 12 months of age, cow’s milk and other milk products Complementary food includes both the ‘transitional’ foods given as a drink can be gradually introduced into infant prepared especially for the infant and the food prepared for diets, preferably in addition to breastmilk, if breastmilk other members of the households that are given to the intake is not sufficient or if the family wants to change children. from infant formula. Tea is a popular drink throughout Complementary foods should be introduced at the appro- Eastern Europe but is not recommended for infants and priate time. Early introduction will lead to a reduction in young children. Tea polyphenols bind iron and other miner- micronutrient intake, because breastmilk would be displaced als, thereby reducing their bioavailability. Furthermore, by other energy sources that have lower density of essential sugar is often added, blunting the appetite and inhibiting nutrients. Furthermore, infants may be exposed to microbial the consumption of more nutrient-dense foods. pathogens present in foods and fluids and thus have an Data collected recently indicate poor complementary increased risk of diarrhoeal diseases and food allergies related feeding patterns in the Eastern European region. In Armenia

European Journal of Clinical Nutrition Fermented milk in complementary feeding F Branca and L Rossi S18 water and tea were introduced at 3 months of age, while fruit acterized by a less acidic but more alcoholic content respect juice and cow’s milk were introduced at 5 months. In to kefir. Another fermented milk used in the area is the Ingushetia, only 6% of the children were exclusively Armenian matzoon. breastfed with administration of liquids (water, tea and Fermented milks are nutritionally similar to unfermented fruit juices) other than breastmilk even from the first milk, except that some of the lactose is broken down to months of life. A similar situation was found in the Balkans. glucose and galactose. Galactose is rapidly absorbed by the Macedonia was the only place with a remarkable 37% exclu- intestinal systems and is rapidly metabolized to glucose. This sive breastfeeding rate, as a result of an intensive campaign makes fermented milk an important food in cases of lactose for breastfeeding promotion. Early introduction of liquids intolerance. In very young children, lactose intolerance is and complementary foods was, however, a common attitude often due to an impaired activity of intestinal lactase follow- in Macedonia and in Kosovo, in which the absence of ing intestinal pathologies (Scrimshaw & Murray, 1988). Chil- exclusive breastfeeding was detected in more than half dren with lactose intolerance could receive fermented milks of the children surveyed. In these areas, early introduction without showing the classical clinical signs of impaired of unmodified cow’s milk and tea administration in the first absorption, such as intestinal bloating and gas production. months of life is also common (Table 1). In addition to that, lactase activity of live microrganisms present in fermented milk also remain after ingestion in the gastrointestinal tract, improving lactose digestion (Sieber Possible role of fermented milk in good et al, 1997). The use of special milk formulation for lactose complementary feeding intolerant subjects could not be affordable in poor regions in Fermentation is an expedient to extend the shelf life of milk, which the use of fermented milk can be a valid alternative. thereby allowing storage and transport. In fact the genera- Fermented milks represent an excellent source of nutrition of lactic and short-chain fatty acids from lactose, and ents such as calcium, protein, phosphorus and riboflavin. the consequent fall in pH inhibits the growth of many Fermented milk products are indeed able to enhance the pathogenic microorganisms. This technology has been absorption of some minerals, such as calcium and non-haem widely practised in Eastern European countries and in iron, as a result of their lower pH. The increased calcium central Asia for a long time, reaching also some areas in absorption with fermented milk consumption is related to Africa. Fermented milks have different denominations both a direct effect of the acidification of intestinal lumen according to the region of production. The two most and in the reduction of the mineral complex formation with common fermented milk available in the Eastern Europe other dietary components (Fukushima et al, 1998). Lactoba- that contain probiotics are yoghurt and kefir. Yoghurt is cillus acidophilus is effective for increasing iron availability in produced when milk (usually cow’s milk) is fermented with animal experimental model (Oda et al, 1994). During the Lactobacillus bulgaricus and Streptococcus thermophilus under fermentation of milk, lactic acid and other organic acids are defined conditions of time and temperature. Kefir is fermen- produced and these increase the absorption of iron. If fer- ted milk with a characteristic fizzy, acidic taste, which mented milk is consumed at mealtimes, these acids are likely originated in the Caucasus and currently accounts for 70% to have a positive effect on the absorption of iron from other of the total amount of fermented milk consumed in the foods. The bioavailability of iron is more important than the countries of the former Soviet Union (Komai & Nanno, total amount of iron in the diet. In contrast to breastmilk, 1992). It is produced when kefir grains (small clusters of iron from unmodified cow’s milk is poorly absorbed, as a microorganisms held together in a polysaccharide matrix) or result of the high content of protein and the low content of mother cultures prepared from the grains are added to milk vitamin C compared with commercial infant formula. and cause its fermentation. Kefir differs from the other Furthermore, the early introduction of unmodified cow’s fermented milks because it contains up to 1% ethyl alcohol. milk can cause blood loss from the intestinal tract, thereby A beverage very close to kefiriskoumis, originating from Asia having a negative influence on iron status, especially during and very common in the central Europe market. Koumis is the first 6 months of life (Sullivan, 1993; Ziegler et al, 1990; obtained form young cow’s milk fermentation and is char- Robson & Leung, 1993) and also during the second half of infancy (Sullivan, 1993; Michaelsen et al, 1995; Zlotkin, 1993). Table 1 Percentage of infants under 6 months consuming tea and other liquids in Ingushetia, A number of health benefits have traditionally been Macedonia and Kosovo attributed to fermented milk products, and they have been used to prevent a wide range of diseases including athero- Ingushetia Macedonia Kosovo sclerosis, allergies, gastrointestinal disorders and cancer Black tea 27% 0.5% — (Macfarlane & Cummings, 1999). Although empirical find- Water 85% 52% 44% ings are yet to be supported by controlled studies, initial Fruit juices 19% 31% 22% results from investigations into the antibacterial, immuno- Herbal tea 12% 40% 66% All liquids 45% 24% 24% logical, antitumoural and hypocholesterolaemic effects of fermented milk consumption suggest potential benefits.

European Journal of Clinical Nutrition Fermented milk in complementary feeding F Branca and L Rossi S19 The most important and recognized effect of the microrganisms used in milk fermentation is their ability to stabilize the bacteriological flora of the gastrointestinal tract. The potential health effects are caused by either the large amount of live bacteria present in the product, or by short-chain fatty acids or other substances produced during fermentation. The faecal microbial flora of breast-fed infants consist largely of Bifidobacteria, whereas other microorganisms predominate in bottle-fed infants. Human milk contains many substances that stimulate the growth of Bifidobacteria in vitro and in the small intestine of infants. Bifidobacteria and Lactobacilli are normally components of the intestinal flora throughout the life cycle. The presence of Bifidobacteria in intestinal environment and the resultant decrease in faecal pH are associated with lower rates of morbidity and mortality in breastfed infants (Bezkorovainy, 2001). The presence of such bacterial strains in fermented milk represents a sort of continuity for the gut environment produced by breastfeeding. In young children there is increasing evidence that certain strains of Lactobacilli have a beneficial effect against the occurrence and duration of acute diarrhoea (Saavedra, 2000). A multicentre, rando- mized, double-blind trial conducted over 4 months on 928 children aged 6 – 24 months showed a significantly reduction of diarrhoea incidence after supplementation with Lactobacillus casei fermented milk (Pedone et al, 2000). During diarrhoea, deterioration of children nutritional status due to anorexia and malabsorption is observed. The beneficial effects of fermented milk administration during diarrhoea episodes is not limited to the local effects on intestinal epithelium. According to Kaila et al (1995), the protection against diarrhoea given by probiotics was also related to an improved antibody response with a higher production of immunoglobulins, IgM, IgA and IgG, after supplementation with Lactobacillus casei. Furthermore, fermented milk products are an example of a nutrient-dense Figure 1 Introduction of fermented milk and cow’s milk in infant under mixture that may be advisable to promote compensatory 2 y in Kosovo (solid box), Macedonia (dark grey box) and Ingushetia (light grey box). growth in those who lose weight during illness, giving an additional protection for the gastrointestinal tract (Sullivan, 1998). the age of 6 months, fermented milk can be important in In Armenia, in Macedonia, in Ingushetia and in Kosovo complementary feeding to provide good nutrient balance, to the same pattern of inclusion of yoghurt and other fermen- prevent iron deficiency in populations using cow’s milk and ted milks was observed. These foods were introduced in to reduce gastrointestinal infections. There is scope for infant diet at 5 – 6 months of life, ie earlier than recom- promotion of the use of fermented milk as a transitional mended. However, fermented milk was introduced usually food especially in less developed regions. In those areas the later than cow’s milk (Figure 1). wide availability of local products at relatively low cost and the acceptability of the products, traditionally used, are further motivations for recommend their use. Conclusion Exclusive breast feeding is recommended for infants in the first 6 months of life. Introduction of fermented milk in References infant complementary feeding should be improved while ACC=SCN (2000): Fourth Report on the World Nutrition Situation. breastfeeding has to be maintained (Michaelsen et al, 2001). Geneva: International Food Policy Research Institute. Fermented milks maintain most of the nutritional properties Backstrand J & Allen LH (1996): Early feeding and somatic development: the timing and etiology of undernutrition. In: Terms Con- of unmodified cow’s milk and the early introduction of sequences of Early Feeding,pp1– 17, ed. J Boulton. Philadelphia, PA: fermented milks should also be discouraged. However, after Lippincott-Raven.

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