TY - JOUR
AU - Koletzko, Berthold
AB - INTRODUCTION The complementary feeding period is the time when infants transition from an exclusively milk-based diet to an increasingly diversified diet with plant- and animal-based foods; the period ranges from approximately 6 to 24 months of life. It has been recognized as a window of opportunity for promoting health and for preventing acute and chronic disease. The complementary feeding period comprises approximately half of the 1,000-day window, a period considered to have a high degree of developmental plasticity. It has been estimated that globally, 6% of all child deaths could be avoided by optimal complementary feeding practices.1 This is because very few children achieve minimum adequate diets. Particularly concerning is the very low rate (28%) of children 6–23 months old around the world who achieve minimum dietary diversity.2 Both undernutrition and infectious diseases contribute to micronutrient malnutrition, and the incidence of infectious disease increases during the complementary feeding period. The World Health Organization issued global guidelines on complementary feeding that were first published in 2003 for breastfed children3 and 2005 for non-breastfed children.4 Global updates to these guidelines are planned5 because several emerging long-term effects related to complementary feeding, including the increasing trend of childhood overweight and obesity, have emerged in recent years.6,7 The incidence of certain noncommunicable, chronic diseases in childhood is also increasing. Although chronic diseases historically have been considered more common in high-income economies, it is becoming clear that low- and middle-income countries are also affected by increasing rates of other chronic diseases. Therefore, it is of global importance to understand the potential relationship between early nutrition and the development of chronic disease. This narrative review is based on a scientific presentation given at the conference “Complementary Feeding: A Piece of the Puzzle to Build Future Health,” held in November 2016 at the National Institute of Medical Science and Nutrition Salvador Zubirán in Mexico City, Mexico. The purpose of this review is to summarize the key points of this presentation and to discuss scientific evidence on the relationship between complementary feeding and long-term health outcomes. Scientific literature on specific chronic diseases like obesity, food allergies and asthma, diabetes mellitus (DM), and celiac disease are reviewed because these conditions have informative study data available and have either a high prevalence or are otherwise a large public health burden. METHODS In addition to the conference presentation, desk research was conducted to include a summary of evidence, primarily in the form of systematic reviews and meta-analyses, published since 2015. For this, a nonsystematic, nonexhaustive search was conducted from January to May 2019 for English-language literature available on PubMed. No systematic inclusion or exclusion criteria were applied for article selection. Overweight and obesity In high-income countries and increasingly also in medium-low and low-income countries faced by a rapidly rising double burden of malnutrition, the prevention of chronic diseases is key. Strategies are in place for the prevention of childhood overweight and obesity through the promotion of healthy diets in infancy and early childhood. Dietary data from infants and young children living in 18 countries in Asia and Africa show that in one-third of countries, > 20% of infants 6–8 months old consumed sugary snacks, whereas up to 75% of Asian children and 46% of African children consumed these foods in the second year of life.8 Despite these trends, studies from industrialized countries have not shown that complementary feeding practices have any major impact on obesity risk; however, they have shown that the age at introduction of complementary foods might effect on growth in infancy, especially in formula-fed children.9 Specifically, formula-fed children may be at a higher risk for childhood obesity when introduced to complementary foods before 4 months of age.10 In developed countries, the relationship between dietary interventions during the complementary feeding period have shown no clear effects on long-term health outcomes.11 The risk for overweight and obesity also has not been linked to specific types of foods or food groups.12 According to a systematic review of 49 articles that examined the types and amounts of complementary foods and their relationship to child growth, size, and body composition, there is insufficient evidence to draw conclusions on these outcomes.13 An article by Thompson14 in this journal comprehensively reviews evidence on the relationship between complementary feeding and overweight and obesity risk. Allergy, atopic dermatitis, and childhood asthma There is an increasing global burden of childhood asthma, rhinoconjunctivitis, and eczema.15–17 Atopic dermatitis is estimated to affect as many as 20% of children in some countries.18 Between 50% and 70% of children with an early onset of atopic dermatitis are sensitized to food allergens or other allergens like dust mites, plant pollens, and household pets.18 Food allergies in childhood have increased dramatically, with the prevalence of clinically proven food allergy in preschool children as high as 10% in high-income countries.19 Food allergy is not only a disease of high-income countries; it affects infants and children in many low- and middle-income countries, also, although quality data for many countries are lacking.19 A systematic review of 31 studies concluded there is moderate evidence that there is no relationship between the age at which complementary foods are introduced and the risk of developing food allergy, atopic dermatitis, or childhood asthma.20 In the same review, 47 studies investigating the types and amounts of complementary foods consumed concluded there is limited to strong evidence (depending on the complementary food studied) that introducing specific allergenic foods during the first year of life (after 4 months of age) does not increase the risk of food allergy and atopic dermatitis or eczema but may prevent food allergies to peanuts and eggs.20 Similarly, on the basis of a systematic review of randomized trials in 2016, Ierodiakonou et al concluded that earlier egg or peanut introduction (4–6 months of age) was associated with lower risk of development of egg or peanut allergy, whereas early fish introduction was associated with reduced allergic sensitization and rhinitis in observational studies.21 Celiac disease Celiac disease is a life-long autoimmune enteropathy triggered by dietary gluten from wheat-containing products in genetically susceptible individuals.22 The clinical presentation of celiac disease varies from asymptomatic patients to severe malnutrition.23 Globally, the prevalence of celiac disease is approximately 1.4%. Gluten intolerance is a concern in many parts of the world, with a prevalence of 0.4% in South America, 0.5% in North America and in Africa, 0.6% in Asia, and 0.8% in Europe and Oceania.22 The global prevalence is greater in children (0.9%) than in adults (0.5%;),22 and both the incidence and prevalence of celiac disease appear to be increasing globally.23 There does not seem to be evidence of an effect of the timing of introduction of gluten-containing complementary foods and the risk for celiac disease. A systematic review and meta-analysis of 21 studies concluded that neither breastfeeding duration nor the timing of introduction of gluten have an effect on the risk of developing celiac disease during childhood.24 On the basis of this evidence, the current complementary feeding recommendations in Europe are that gluten-containing complementary foods may be introduced between 4 and 12 months of age.25 Diabetes mellitus Type 1 DM is an autoimmune disease resulting from destruction of pancreatic β cells induced by autoantibodies. Between 1989 and 2013, the EURODIAB study including children from 26 centers in 22 European countries, reported a 3.4% annual increase in type 1 diabetes incidence among children younger than 14 years.26,27 In the birth to 4-years age group, rates of increase were similar in boys and girls (3.7% per year, respectively).27 The relationship between complementary feeding and risk for type 1 DM is under investigation. The BABYDIAB study conducted in Germany found that infants with high-risk type 1 DM genotypes who received gluten-containing foods before age 3 months had a higher risk for development of a certain diabetes-associated antibody.28 The Diabetes Autoimmunity Study in the Young in the United States examined infants with familial risk for type 1 DM (ie, first-degree relative with type 1 DM). Researchers found that infants exposed early (between birth and 3 months of age) or late (≥7 months of age) to cereals had an increased risk of development of islet autoimmunity.29 To date, evidence on the relationship between the timing of introduction to complementary foods and the risk for type 1 DM remains inconclusive.30 LONG-TERM EFFECTS OF MICRONUTRIENT DEFICIENCIES During periods of rapid development, like during infancy and early childhood, adequate micronutrient intakes ensure not only healthy development and function but also may prevent chronic disease states. Micronutrient malnutrition is a significant problem for infants and young children living in high- or low-income countries and often exists as multiple micronutrient deficiencies.31 Globally, infants and young children consume complementary foods low in iron, vitamin D, arachidonic acid (ARA) and docosahexaenoic acid (DHA)32 and iodine.33,34 Each of these micronutrients plays a unique role in the normal physiology and function of the human body. Iron Infants require iron from dietary sources for production and maintenance of hemoglobin for the transport of oxygen by red blood cells, rapid brain development, and proper development of several organ systems. Iron-deficiency anemia, therefore, causes microcytic anemia, impaired immune function, impaired endocrine function, and poor cognitive development.31,35 Several chronic diseases are associated with iron deficiency anemia, including chronic renal and cardiovascular diseases, cancers, and inflammatory bowel diseases.35 Iron-deficiency anemia is one of the most common micronutrient deficiencies in infants and young children globally. Infants accumulate hepatic iron stores in utero. Iron stores in infancy and early childhood are influenced by the timing of umbilical cord clamping at birth, especially in high-risk populations.36,37 Because of rapid growth, starting from the second half of the first year of life, infants rapidly deplete and exhaust iron stores that were accumulated during gestation. The amount of iron required from complementary foods varies between breastfed and formula-fed infants. This is because formula-fed infants generally consume iron-fortified infant formula and are at a lower risk of iron-deficiency anemia than are breastfed infants, because breastmilk is naturally low in iron. At approximately 6–12 months of age, infants require complementary foods that have a high iron density. Micronutrient needs are especially high relative to infant body weight and total caloric intakes between the sixth and eighth months of life.38 For example, an infant consuming 200 calories from complementary foods requires 4.5 mg of iron per 100 kcal, which is 9 times the iron required by an adult man per 100 kcal.38 The European Society for Pediatric Gastroenterology and Nutrition suggests the dietary iron requirement for infants aged 6–12 months to be 0.9–1.3 mg per kg of body weight per day.39 In a systematic review, Obbagy et al40 concluded there is moderate evidence suggesting that introducing complementary foods at 4 months instead of 6 months of age offers no advantages or disadvantages to iron status in healthy, full-term infants. There is strong evidence that complementary foods containing both heme and nonheme iron sources help maintain adequate iron status and prevent iron deficiency during the first year of life in infants at risk of insufficient iron stores; however, benefits for infants with sufficient iron stores are less clear.40 There is also insufficient evidence on the effects of complementary foods with less iron, such as fruits and vegetables, on infant iron status.40 Vitamin D Vitamin D status is important for infant skeletal health. Deficiency in vitamin D causes chronic diseases like rickets, as well as intellectual disabilities and impaired immune and endocrine function. A recent study from the United Kingdom reported an incidence of nutritional rickets of 0.48 (95% confidence interval [CI], 0.37–0.62) per 100 000 children younger than 16 years.41 There are limited population data on vitamin D status from low- and middle-income countries; however, available data suggest that vitamin D deficiency may be widespread globally.42 Two recent systematic reviews were conducted on timing of complementary feeding and the types and amounts of complementary foods and beverages on bone health.40,43 The authors concluded there is insufficient evidence to determine the relationship between the timing of introduction of complementary foods and infant vitamin D status.40 There is also currently insufficient evidence on the effects of the types and amounts of complementary foods and beverages on bone health.43 Essential fatty acids Essential fatty acids are important for development of the brain, nervous system, and eyes and play important roles in cell structures and homeostasis. Imbalances in dietary intakes of fatty acids are linked with chronic cardiometabolic diseases. Fatty acids are components of every cell membrane in the body. The types of fatty acids taken up through complementary foods influence body composition, function, and overall health. Polyunsaturated fatty acids are divided into 2 main categories, namely omega-6 and omega-3 fatty acids. Various long-chain polyunsaturated fatty acids within these 2 categories can be synthesized from the essential fatty acids, omega-6 linoleic acid and omega-3 alpha-linolenic acid. The most critical long-chain polyunsaturated fatty acids for proper brain, nervous system, and eye development and function are DHA and ARA, which are highly concentrated in the infant retina and brain and accumulate rapidly during growth spurts.44 DHA is essential for proper vision and is the main membrane constituent in the photoreceptor cells of the eye.44 Obaggy et al40 could not identify any studies in their review that assessed fatty acid status in relationship to the timing of complementary food introduction. Several randomized controlled trials45–51 have examined the effects of complementary foods with various fatty acid profiles on infant fatty acid status. Many of these trials have demonstrated that the fatty acid profiles in complementary foods like eggs influence both the fatty acid status46,48 and visual acuity45 of infants and young children. Iodine Iodine is important for development of the brain, nervous system, and thyroid. Iodine deficiency early in infancy and early childhood is linked to chronic diseases including hypothyroidism as well as permanent neuromotor impairment. During the complementary feeding period, low iodine intake through complementary foods may contribute to subclinical thyroid dysfunction.52,53 Globally, approximately 2 billion individuals have insufficient iodine intake, with approximately 50% of Europeans estimated to be mildly iodine deficient.54 A study assessing infant urinary iodine concentration in Swiss infants found that those who did not consume fortified infant formula or fortified complementary foods were at risk of inadequate iodine intake.55 Maternal iodine intake is particularly important during pregnancy for fetal brain development and is associated with language skills in infancy and early childhood.56 Infants are born with only small amounts of stored intrathyroidal iodine; therefore, they are dependent on iodine from human milk and complementary foods for normal physical and neurologic growth and development.57 Infants are at risk for iodine deficiencies due to their high iodine requirements per kilogram of body weight.58 Infants at risk for iron deficiency anemia are also at risk for iodine deficiency, because iron deficiency anemia impairs iodine metabolism and reduces thyroid hormone production.58 We found no comprehensive review on the effects of the timing or specific iodine-containing complementary foods on the iodine status of infants and young children. IMPLICATIONS FOR PUBLIC HEALTH NUTRITION POLICY AND PRACTICE Research on complementary feeding and chronic diseases is helpful for understanding the potential relationship between early nutrition and the development of chronic disease states. It is also important for informing public health nutrition policies that aim to promote healthy diets as a means of disease prevention. Previous public health nutrition policies have focused on infant survival and the prevention of acute and infectious diseases in childhood. Accordingly, complementary feeding guidance has included recommendations for the prevention of undernutrition and micronutrient deficiencies.3,4 Future policy recommendations should also encompass recommendations for the prevention of chronic diseases like childhood obesity and integrate messaging on the double burden of malnutrition. More empirical studies are needed to understand the complex relationships between the types and amounts of foods and the risk for noncommunicable diseases. Currently available evidence on some specific chronic diseases is not sufficient to make policy recommendations. Therefore, future policy recommendations should encompass policies for the prevention of these diseases as more research becomes available. Future nutrition programming should encompass messaging on the quality of complementary foods for chronic disease prevention. Given the importance of micronutrient-rich complementary foods for the prevention of chronic diseases, recommendations on the provision of complementary foods rich in key micronutrients, fortified foods, or micronutrient supplementation where diets are inadequate are still appropriate. Programmatic recommendations to achieve the relatively high estimated dietary requirements for iron are achievable through provision of red meat and liver or other organ meats.25 Dietary nonheme sources of iron include pulses like dried beans, peas, lentils, and chickpeas; nuts; green leafy vegetables; dried fruit; and iron-fortified staple foods like cereals.25 Other sources of iron include iron-supplemented infant formulas in non-breastfed infants and children, or iron supplementation. Heme iron is particularly beneficial because it is easily absorbed and it enhances absorption of nonheme iron. Iron absorption is enhanced by human milk and complementary foods that contain meat protein and vitamin C; iron absorption is also assisted by consumption of fermented vegetables.25 Importantly, iron absorption is inhibited by certain calcium-rich foods like cow’s milk. Observational studies have shown that the consumption of cow’s milk in late infancy increases the risk of iron deficiency at 12 months of age.59 For this reason, cow’s milk is discouraged as a beverage during the first year of life.25 Nutrition practice recommendations for the prevention of rickets include vitamin D supplementation in breastfed infants as well as the provision of complementary foods like fatty fish and egg yolks. Recommendations for foods rich in ARA include provision of meats, poultry, and eggs. Complementary foods rich in DHA include fish and seafood products.32 A review on dietary intakes of ARA and DHA by infants and young children living in low- and middle- income countries found that complementary foods based on local diets are predominantly plant based and, thus, inherently low in these types of fatty acids.32 In low-income countries, the longer duration of continued breastfeeding during the complementary feeding period is helpful in provision of these essential fatty acids through breastmilk but is nevertheless weakened by the exceptionally low provision of ARA and DHA from complementary foods.32 To achieve dietary intakes of DHA and ARA considered adequate by the European Food Safety Authority (ie, infants 0–6 months: 100 mg/d DHA, 140 mg/d ARA; and 6–12 months: 100 mg/d DHA),39 complementary foods containing DHA and ARA need to be offered in addition to human milk or infant formula. Infants living in either low- or high-income countries may be at risk of iodine deficiency because iodized salt is rarely consumed in infancy.55 This is because experts recommend no added salt (regardless of iodization) be given to infants during their first year and that cow’s milk (a dietary source of iodine) not be given to infants as a beverage during the first year of life.25,58 Therefore, fortified complementary foods may play an important role in ensuring adequate iodine intake during the complementary feeding period. Human milk is an important source of iodine for infants during early infancy and during the complementary feeding period.60 Maternal supplementation with high-dose or daily iodine is effective in increasing human-milk iodine, with some evidence of a dose-response relationship.57 Data suggest that human-milk iodine concentrations in the range of 150 μg/L during the first 6 months of lactation would achieve or exceed infant iodine requirement and prevent deficiency.57 Over first 6 months of life, breastfed infants living in regions of moderate to severe iodine deficiency whose mothers do not have adequate access to iodized salt can receive adequate iodine through human milk when their mothers receive a dose of iodine after delivery.61 For the prevention of childhood obesity and overweight, recommendations should include the elimination or reduction of discretionary food intakes, avoiding added sugar, salt, and beverages high in calories or sugar. CONCLUSION The incidence of various chronic diseases is increasing globally in both pediatric and adult populations. The global incidence of type 1 DM27 and of celiac disease23 is increasing; however, there is not a clear relationship between complementary feeding practices and timing of introduction to complementary foods and the risk for type 1 DM.30 Timing of introduction of complementary foods containing gluten does not seem to affect the risk for celiac disease.28,62 The incidence of noncommunicable, chronic disease in childhood, like overweight and obesity, is increasing globally.7 There is evidence of changing global food patterns and the consumption of discretionary foods by infants and children at very young ages in high- and low-income countries. It is recommended that only nutrient-dense complementary foods be provided to infants and young children, taking care to avoid added sugar and salt, and beverages high in calories and sugar, including fruit juice and sugar-sweetened beverages.25 The incidence of childhood food allergies is increasing.19 Limited to strong evidence suggests the introduction of specific allergenic foods during the first year of life may prevent food allergies to peanuts and eggs.20 There is moderate evidence that there is no relationship between the age at which complementary foods are introduced and the risk of development of food allergy, atopic dermatitis, or childhood asthma.20 Inadequate complementary feeding practices remain an important global problem and increase the risk for micronutrient deficiencies in infants and young children. Prevention of micronutrient deficiencies depends on timely introduction of complementary foods that are good sources of key micronutrients. All infants should receive iron-rich complementary foods regularly, including meat, fish, eggs, or iron-fortified complementary cereals.25 Vegan diets should only be used under appropriate medical or dietetic supervision to ensure that infants and young children receive a sufficient supply of micronutrients.25 Complementary foods containing both heme and nonheme iron sources help maintain adequate iron status and prevent deficiency during the first year of life in infants at risk of insufficient iron stores; however, benefits for infants with sufficient iron stores are less clear.40 The fatty acid profiles of certain complementary foods like eggs influence the fatty acid status of infants and young children.46,48 There is currently insufficient scientific evidence available to draw firm conclusions about the relationship between complementary foods and infant bone health.43 Coauthor email addresses: Melissa Theurich melissa@theurichconsulting.com Veit Grote: Veit.Grote@med.uni-muenchen.de Acknowledgements Author contributions. B.K. created the oral scientific presentation and interpreted relevant data. M.A. T. contributed to conception of the written manuscript and wrote the manuscript on the basis of written protocols from the oral presentation and slideshows. V.G. critically reviewed the manuscript. All authors read and approved the final manuscript. Funding. The Ludwig-Maximilians-Universität (LMU) München and its employee B.K. received financial support from the Commission of the European Communities (FP5-QLRT-2001–00389 CHOPIN; FP5-QLAM-2001–00582 PIANO; FP6-007036QLRT-2001–00389 EARNEST; FP7-289346-EarlyNutrition); the European Research Council (Grant ERC-2012 AdG—no.322605 META-GROWTH); the European Joint Programming Initiative NutriProgram ERA-HDHL; the European Erasmus+ programs Early Nutrition eAcademy Southeast Asia (573651-EPP-1–2016-1-EN-EPPKA2-CBHE-JP) and Capacity Building to Improve Early Nutrition and Health in South Africa (598488-EPP-1–2018-1-EN-EPPKA2-CBHE-JP); and the European Interreg Program Focus in CD (CE111). Additional funding was provided by the Federal Ministry of Education and Research (No. 01 GI 0825 and INST 409/224–1 FUGG), the German Research Foundation (KO912/10–1), the McHealth Innovation Initiative of the LMU, and the LMU Center for Advanced Studies. Declaration of interest. Ludwig-Maximilians-Universität and its employees V.G. and B.K. have collaborated with pharmaceutical food companies on scientific and educational projects, mostly as part of publicly funded research projects. None of these interactions has affected the content of this manuscript. M.A.T. declares no conflict of interest. References 1 Jones G , Steketee RW , Black RE , et al. How many child deaths can we prevent this year? Lancet . 2003 ; 362 : 65 – 71 . Google Scholar Crossref Search ADS PubMed WorldCat 2 White JM , Begin F , Kumapley R , et al. Complementary feeding practices: current global and regional estimates . Matern Child Nutr. 2017 ; 13 : E12505 . Google Scholar Crossref Search ADS WorldCat 3 Dewey K. Guiding Principles for Complementary Feeding of the Breastfed Child . Washington DC : Pan American Health Organization ; 2003 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC 4 World Health Organization. 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TI - Complementary feeding and long-term health implications
JO - Nutrition Reviews
DO - 10.1093/nutrit/nuaa059
DA - 2020-06-16
UR - https://www.deepdyve.com/lp/oxford-university-press/complementary-feeding-and-long-term-health-implications-iJeRpsKe1h
SP - 6
EP - 12
VL - 78
IS - Supplement_2
DP - DeepDyve
ER -