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Vegetarian Infants and Complementary Feeding
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Vegetarian Infants and Complementary Feeding Silvia Scaglioni1, Valentina De Cosmi1,2, Alessandra Mazzocchi1,2, Silvia Bettocchi1,3, Carlo Agostoni1,2 1 FOND AZI O NE 2 UNIVERS I TY
I RCCS CÀ GRANDA OS P E D A L E MA G G I O R E P O L I C L I N I C O , MI L A N , I TA LY; O F M I L AN, M I L AN, I TA LY; 3 U N I V E R S I T À C AT T O L I C A D E L S A C R O C U O R E , MI L A N , I TA LY
1. Introduction Complementary feeding is the period of time when infants are introduced to food different from milk in their diet, together with a gradual reduction of the intake of milk (either breast milk or formula), to finally and gradually acquire their family’s diet model (Alvisi et al., 2015). This definition is based on the one proposed by the European Food Safety Authority (EFSA, 2009) and by the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN) (ESPGHAN Committee on Nutrition, 2015). The World Health Organization (WHO) has described the complementary feeding period as ‘‘the period during which other foods or liquids are provided along with breast milk’’ and states that ‘‘any nutrient-containing foods or liquids other than breast milk given to young children during the period of complementary feeding are defined as complementary foods.’’ The ESPGHAN Committee on Nutrition, the American Academy of Pediatrics (AAP), and the WHO consider that exclusive or full breast-feeding for 6 months is a desirable goal (ESPGHAN Committee on Nutrition, 2015; Kleinman, 2000; WHO, 2003). The introduction of complementary foods should not be before 17 weeks but should not be delayed beyond 26 weeks. Around the sixth month of life, breast milk becomes insufficient to meet requirements for macronutrients and micronutrients, as the infant’s age and weight both increase. Infants gradually lose the extrusion reflex, and they develop the ability to swallow solids and start to show an interest in adult family foods. A balanced number of factors let them gain a good relationship with food and the achievement of nutritional requirements (Alvisi et al., 2015): • acquisition of fundamental milestones in neuromotor development • development of taste and personal inclinations • maturation of renal and gastrointestinal functionality • qualitative and quantitative implementation of nutritional intake • interaction of cultural and socioeconomic factors with local and family traditions Vegetarian and Plant-Based Diets in Health and Disease Prevention. http://dx.doi.org/10.1016/B978-0-12-803968-7.00029-0 Copyright © 2017 Elsevier Inc. All rights reserved.
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Enough attention should be paid to all these aspects: nutritional and developmental reasons drive this transition, which will influence later health. The AAP recommends that breast milk should be continued for at least 12 months along with appropriate supplementary foods (American Academy of Pediatrics, 2005). Important data point out that breast milk has a favoring role in psychological and nutritional aspects and in the development of tolerance; thus, it might reduce the onset of allergies (Grimshaw et al., 2013). Exclusive breastfeeding by well-nourished mothers for 6 months can meet a healthy infant’s requirements for water, energy, protein, calcium, and most vitamins and minerals (EFSA, 2013). The breast milk of ovolactovegetarian women is similar in composition to that of nonvegetarians, and it is nutritionally adequate too (Craig et al., 2009). For that reason, there are no evidences that timing of solid foods introduction in vegetarian weaning should differ from nonvegetarians. In the first year of life, if breast-feeding is not possible, the only alternative is infant formula, or soy formula for vegan infants. The introduction of cow milk should not be before the 12th month of life, due to its high protein content, low iron concentration, and the risk of iron deficiency (Domellöf et al., 2014). Fortified soy milk can be used as a primary beverage starting at age of 1 year or older, too (Mangels and Messina, 2001). Other preparations including soy milk, rice milk, and homemade formulas should not be used to replace breast milk or commercial infant formula, due to their poor nutritional quality. Different weaning practices have characterized this stage of life according to traditions, ethnical origins, and scientific beliefs. Actually, there are not rigid schemes on timing of food introduction, especially fruits and vegetables (Alvisi et al., 2015). In the latest suggestions issued by AAP, ESPGHAN, and European Academy of Allergy and Clinical Immunology (De Silva et al., 2014), it is recognized that there is no scientific evidence to justify the delayed introduction of solid foods (after 6 months of age), even those recognized as more allergenic, to prevent allergic diseases (Agostoni and Laicini, 2014). Vegetarian complementary feeding is widespread because vegetarian families are increasing and they want their children to share their nutritional habits starting from complementary feeding: vegetarians and vegans have been estimated to constitute 5% and 2%, respectively, of the US population, and in Italy, vegetarians are 7.1% of the total population (EURISPES survey; Appleby et al., 2016). Literature informs that well-planned vegetarian diets are appropriate for individuals during all stages of the life cycle, including pregnancy, lactation, infancy, childhood, and adolescence, and for athletes (Craig et al., 2009). A vegetarian diet is characterized by the choice of a wide variety of foods of vegetal origin and by the exclusion of animal foods (meat, fish, and their derivatives). The reader may read Chapter 1 of this book for a full characterization of the different diets. The two main categories of vegetarian complementary feeding that will be discussed in this chapter are ovolactovegetarian, which includes dairy and egg products, and vegan weaning, which is characterized by the absence of any type of animal foods. The period from birth to 1 year is a time of nutritional vulnerability when attention to proper nutrition is critical to support the extremely rapid growth, including brain growth. In this phase, particular attention should be paid because a regular growth and neurodevelopment are relevant goals. Ovolactovegetarian weaning can be adopted, but it must be correctly designed, to favor a healthy diet and to prevent nutritional deficiencies that are
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a real risk of vegetarian diet. Foods in the vegan diet repertoire cannot alone cover energy, macronutrients, and micronutrients requirements of the infant; consequently supplementations are needed (Amit, 2010; Chalouhi et al., 2008; Kaganov et al., 2015).
2. Vegetarian Complementary Solid Food, Macronutrients, and Micronutrients Requirements Differences between vegetarian solid foods and nonvegetarian ones are limited to replacement of meat with mashed or pureed tofu, legumes (pureed and strained if necessary), soy or dairy yogurt, cooked egg yolk, and cottage cheese. Later, around 7–10 months, foods such as cubed tofu, cheese or soy cheese, and small pieces of veggie burgers can be started. A balanced use of foods out of the following alimentary groups—fruits, vegetables, cereals, dried fruits, legumes, water, and oilseeds—permit one to conduct a good vegetarian complementary feeding (Craig et al., 2009). In the second half of the first year of life, breast milk alone is not enough to supply a sufficient amount of calories, proteins, zinc, iron, and fat-soluble vitamins (vitamins A, D, K) that are necessary to guarantee an adequate growth to the infant (ESPGHAN Committee on Nutrition, 2015; EFSA, 2009). Complementary feeding is an important phase in the growth of a child, and it can play a major role in a child’s future health and in its future feeding behavior. Early feeding contributes to prevent noncommunicable adult diseases (United Nations System Standard Committee on Nutrition, 2006). The recommended intakes suggested subsequently for infants in the second semester of life have been extracted from EFSA Scientific Opinions on Dietary Reference Values for energy, micronutrients, and macronutrients and from a position paper by the American Dietetic Association (ADA) about vegetarian diets (Craig et al., 2009).
2.1 Energy in Infants (7–12 Months) EFSA: The recommended intake of energy is 76–79 kcal/Kg/day (EFSA, 2013). The recommended energy intake should be correctly distributed among the various macronutrients, both in terms of quantity and quality (Alvisi et al., 2015). It is known that the energy content of human milk varies within a meal, with lactational stage, and between individuals. Assuming an average energy content of human milk of 0.67 kcal/g, mean energy requirements are met by exclusive breast-feeding during the first 6 months of life and possibly longer (Butte, 2007). Also, the protein content of human milk changes with lactational stage and is on average 13 g/L in the second week, 9 g/L in the second month, and 8 g/L in the fourth month until weaning. In mature milk, there is a low content of iron (0.2–0.4 mg/L) and zinc (about 0.5 mg/L at 6 months), and both decrease with the length of lactation (EFSA, 2013). The energy density of many vegetarian foods (cereals, fruits, vegetables) is low, due to low fat and high fiber content, and infants may have difficulty consuming
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the necessary volume of diet to achieve adequate energy intake (British Paediatric Association, 1988). Their stomach capacity is limited, and children from 1–3 years of age are able to take 200–300 mL at each meal. Fiber and complex carbohydrates have a higher water content, and this results in a lower energy density of the foods and favors early satiation (Jacobs and JT, 1988). Energy is needed to maintain physiological activities and deposition of tissues. Growing is a dynamic and energy-consuming process that should be adequately supported: it is about 5 kcal/g of new tissue (3.5 kcal energy “stored” and 1.5 kcal for cost of synthesis). In the first month of life, energy requirements for growth are 40%, and they decrease to about 3% at the age of 12 months, due to the decrease of growth rate (Butte, 2007). Growth during complementary feeding should continue to be monitored and plotted on standard centile charts as part of health surveillance by the pediatrician, and mothers should be advised appropriately if growth deviates from the expected. It is important that vegetarian parents know how to ensure an adequate intake of energy by their infants. Doctors, dieticians, and nurses should give them practical tips on how to increase energy density of foods (Mangels and Messina, 2001). The first practical trick is to feed their baby at least four times a day, including energy-dense complementary foods at each meal. Ripe bananas have 15%–20% carbohydrate, and avocados are rich in fat; thus both of them are good sources of energy. Cereals and pulses are usually more energy-dense than fruits. Adding fats such as extra virgin olive oil to cereal meals or peanut butter to bread improve the energy density of the meal itself. Parents should promote water consumption, avoiding allowing the infant to drink any kind of energy-providing liquids. Key point: Energy is needed to support growth. High-fiber and high-complexcarbohydrate diets lower the caloric density of the foods and favor an early satiety.
2.2 Protein in Infants (7–12 Months) EFSA: The recommended intake is about 10% of total calories (1.1 g/Kg/day, average recommended intake 11 g/day for 6 months of age) (EFSA, 2012). ADA: Precautional protein increase of 10%–15% of the recommended intake for age (Craig et al., 2009). Recommended protein intake has been reduced in the past few years, due to the alignment on human milk content (EFSA, 2014a,b), falling in line with the hypothesis that hyperproteic diets in early life may favor the onset of obesity (Alvisi et al., 2015). An excess of proteins would stimulate the secretion of insulin and IGF1, both responsible for adipogenesis and the differentiation of adipocytes. Data available in literature suggest that between 6 and 24 months of age, a protein intake of more than 15% of total energy can lead, in some subjects, to early adiposity rebound phenomena, thus favoring the development of future obesity (Agostoni et al., 2005; Rolland-Cachera et al., 2006). No association has been found between a high intake of fats with complementary feeding and obesity in the following ages; on the contrary, Rolland-Cachera et al. identified in a high-protein and low-fat dietary pattern a hyperproteic and hypolipidic pattern of infants living in developed countries as a possible contributing factor of early adiposity rebound and, later in life, of body fat and
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leptin resistance (Rolland-Cachera et al., 2013; Alvisi et al., 2015; Escribano et al., 2012). The diet of infants in the general population is characterized by high protein and low fat intakes (Michaelsen and Greer, 2014). Together with the attention to protein and fat intake, energy has to be taken into account, since it represents the main determinant of fat deposition. Nevertheless, the relation between protein intake during complementary feeding and later risk of noncommunicable diseases is still unclear. Not only the quantity, but also the quality of proteins seems to play a role in the association between early intakes and later fatness. The longitudinal DONALD study reported that the protein sources that may be mostly responsible for the association with adiposity at 7 years old are animal protein, and more specifically dairy products at 12 months (Günther et al., 2007). However, in vegetarian infants the risk is rather to fail reaching the recommended protein intake, and this risk can be reduced by continuing the intake of breast milk or formula. It has to be taken into account that many vegetable proteins are low in one or more essential amino acids, and the total indispensable amino acid content in vegetable foods is low when compared to animal protein sources (Craig et al., 2009). Because vegetable foods have not the same quantity and quality of proteins, vegetarians’ dietary choices are crucial to achieve the adequate protein intake. Plant proteins can meet protein requirements when a variety of plant foods are consumed and energy needs are met (Mangels and Messina, 2001). Eating a huge variety of plant foods over the course of a day can provide all essential amino acids and adequate nitrogen retention (American Academy of Pediatrics Committee on Nutrition, 1998). Encouraging infants to continue to take about 500 mL/day of breast milk or formula reduces the needs for other proteins sources. Mixing breast milk or formula intake, which provides proteins rich in indispensable amino acids, with vegetable protein foods enhances the amino acid composition of the meal and improves net protein utilization. Legumes and soy beans have a high proportion of proteins (over 20% and about 36%, respectively), but a low biological value. Based on the protein digestibilitycorrected amino acid score, which is the standard method for determining protein quality, a combination of legumes and wheat proteins enhances the nitrogen utilization efficiency (Craig et al., 2009), and the choice of shelled beans minimizes the phytic acid intake. In vegetarian infant diet, a precautionary increase of proteins is suggested, around 10%–15% of the recommended energy intake for age. Attention should be paid to not to exceed the 15% and to avoid the risk of protein excess (Joint WHO/FAO/UNU Expert Consultation, 2007). Key point: Proteins are crucial for growth. In not well-balanced vegetarian diets, there is a consistent risk to not reach protein requirements.
2.3 Lipids in Infants (7–12 Months) EFSA: Lipids: recommended intake is 40% of total calories (EFSA, 2010a,b). Lipids are the main energy source in the infant diet and are necessary for normal growth and physical activity. Lipids are also important structural components of neural and other body tissues (Uauy and Dangour, 2009; Butte et al., 2010). The selection of dietary fat and
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fatty acid sources during the first years of life is now considered to be of critical importance (Uauy and Dangour, 2009). Consumption of n-3 PUFAs eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) have demonstrated physiological benefits on blood pressure, heart rate, triglycerides, and likely inflammation, endothelial function, and cardiac diastolic function (Aranceta and Perez-Rodrigo, 2012). DHA plays a major role in development of the brain and retina during fetal development and the first 2 years of life (Uauy and Dangour, 2009). When DHA-rich products are excluded, the recommended intake of total lipids and of ω-3 series cannot be achieved, and there is the risk of low DHA blood level and relative deficiency (Rosell et al., 2005). The proposal that dietary DHA enhances neurocognitive functioning in term infants is controversial. Theoretical evidence, laboratory research, and human epidemiological studies have convincingly demonstrated that DHA deficiency can negatively impact neurocognitive development (Schwartz et al., 2009). DHA deficiency may be the cause of many disorders, such as depression, inability to concentrate, excessive mood swings, anxiety, cardiac disease, type 2 diabetes, and dry skin (De Mel and Suphioglu, 2014). Nutrient deficiency during development may have long-lasting consequences for the central nervous system that range from devastating malformations to subtle effects on neural functioning. DHA is enriched in brain and retina membranes, where it functions in early development events, such as neurogenesis, neurite outgrowth, synaptic plasticity, axonal elimination, and gene expression (Mulder et al., 2014). One of the main considerations when trying to meet current recommendations for n-3 fatty acids is that current intake of PUFAs consists primarily of n-6 fatty acids. The competition for desaturases and elongases in n-3 and n-6 PUFA metabolism results in inverse effects on tissue concentrations of these fatty acids. This is of even greater concern in vegetarians and vegans, who have relatively high intakes of linoleic acid (LA) combined with low intakes of EPA and DHA (Aranceta and Perez-Rodrigo, 2012). Vegetarians tend to consume a lot of n-6 but marginal amounts of n-3 fatty acids. To restore n6/n3 balance, regular consumption of micro-algae (rich in DHA) and of walnuts, canola oil, flaxseed oil, enriched dairy products, seeds, peanut butter, soy beans, and derivatives (rich in alfa-linolenic fatty acid, ALA) is recommended (Van Winckel et al., 2011). EFSA has not established recommended intakes for n3-PUFAs but for specific n-3 fatty acids, namely ALA, EPA, and DHA. EFSA proposed not to set specific values for the n-3/n-6 ratio and to set an average intake of 100 mg DHA for infants (>6 months) and young children. In older infants, DHA intakes at levels of 50–100 mg per day have been found effective for visual function in the complementary feeding period and are considered to be adequate for that period. EFSA has set the adequate intake value of 0.5% of total energy for ALA in all population groups (EFSA, 2010a,b). The FAO/WHO 2008 report defines 15% of total energy as upper AMRD (acceptable macronutrients distribution rate) for infants 6–12 months old (Aranceta and PerezRodrigo, 2012).
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An increased intake of ALA, the precursor of endogenous DHA synthesis, has been supposed to be an (alternative) strategy to support infant DHA status. Few studies have tested the effect of replacing LA-rich corn oil with ALA-rapeseed oil in complementary food. It still seems to be a promising strategy, but it remains to be confirmed how this approach affects the DHA status (Libuda et al., 2016). Key point. Lipids are the main energy source (40% of total energy) for the infant, and they are essential for growth and for neural tissue structure. Polyunsaturated and monounsaturated fats have to be preferred. A regular intake of DHA-rich foods is recommended for both vegetarians and vegans.
2.4 Carbohydrates in Infants (7–12 Months) Dietary carbohydrates are the major macronutrients for humans. Both adults and children in the Western countries obtain approximately half their daily caloric requirements from dietary carbohydrates. In other countries, carbohydrate has been the major source of energy, at least until the more recent introduction of “Western foods,” with higher proportions of fat and protein, to many developing countries. There are not current recommendations for infants; EFSA has proposed 45%–60% of total energy as the reference intake range for carbohydrates applicable to both adults and children older than 1 year of age (EFSA, 2010a,b). To decrease the risk of overweight, obesity, and tooth decay, a WHO guideline recommends adults and children reduce their daily intake of free sugars to less than 10% of their total energy intake. A further reduction to below 5% would provide additional health benefits (WHO, 2015). Based on the available evidence on bowel function, EFSA has considered dietary fiber intakes of 25 g/day to be adequate in adults and of 2 g/MJ to be adequate in children from the age of 1 year (EFSA, 2010a,b). It is advisable to prefer starchy alimentary sources, if possible with a low glycemic index, and above all, it is strongly recommended to limit the intake of simple sugars (such as fruit juices, sugar, and sweeteners in general). Carbohydrates in foods with a low glycemic index are more slowly digested and absorbed; consequently, diets with a low glycemic index are beneficial in controlling postprandial plasma glucose excursions. Diets with a low glycemic index and glycemic load, but not low in total carbohydrates, are associated with lower type 2 diabetes mellitus risk, cardiovascular disease risk, and levels of proinflammatory markers and fasting insulin (Blaak, 2016; Rouhani et al., 2016). Recent literature failed to confirm that introducing gluten between week 17 and 26, while the infant is still being breast-fed, would have a protective role on the onset of celiac disease, type 1 diabetes, and wheat allergy (Vriezinga et al., 2014; Beyerlein et al., 2014). Cereals are rich in starch, proteins, minerals, vitamins, and insoluble fibers. Amaranth, quinoa, buckwheat, soy, and lupine have all the indispensable amino acids in sufficient amounts. Other cereals are low in lysine but rich in methionine, whereas this is the opposite in legumes; therefore these protein sources are well known to complement each other. Adding legumes to cereals is possible to obtain adequate biological protein value.
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Choosing refined and lower fiber cereals allows a reduction of phytic acid content, which usually lowers the absorption of minerals (namely, iron, zinc, calcium, and magnesium). ESPGHAN Committee on Nutrition recommends that iron-rich complementary foods (iron-fortified cereals) should be given to all infants from 6 months of age (ESPGHAN Committee on Nutrition, 2015). Both vegetarian and nonvegetarian infants should be introduced to whole grains before the end of the second year of life. Key point. Carbohydrates in starchy alimentary sources are preferred. Reducing free sugars to less than 10% of their total energy intake is recommended.
2.5 Iron in Infants (7–12 Months) EFSA: Iron: a daily intake of 11 mg is recommended (EFSA, 2015a,b,c). ADA: 1.8 times that of nonvegetarians (Craig et al., 2009). Iron is critical for normal growth, hematopoiesis, and neurologic development during infancy. When complementary feeding is not introduced in exclusive breast-fed infants, they are at risk of developing an iron deficit in the second semester (Alvisi et al., 2015). Prevalence of iron deficiency anemia among vegetarians is similar to that of nonvegetarians, and it is approximately 2%–3% at 6–9 months and 3%–9% at 1–3 years of life (Domellöf et al., 2014). Complementary foods have the important role to provide more than 90% of the iron requirements in breast-fed infants (Domellöf et al., 2014). Between 6 and 24 months of age, the infant becomes dependent on additional dietary iron, and because of rapid growth, iron requirements per kilogram body weight are higher than during any other period of life. It has been shown that infants have the ability to upregulate iron absorption when iron requirements increase (Domellöf et al., 2002). This ability of each individual to be able to adapt iron absorption to iron status is likely to make infants more resistant to iron deficiency. The ESPGHAN Committee on Nutrition states that meat products and iron-fortified foods are the major dietary source of iron. Therefore an early introduction of iron-rich complementary foods is highly recommended for preventing iron deficiency anemia in infants (ESPGHAN Committee on Nutrition, 2015). Foods containing iron are meat and fish (bovine: 1.9 mg/100 g; cod 0.7 mg/100 g) and some vegetables (legumes, endive, green chicory, spinach). EFSA assumes a mean value of 10% of iron absorption in healthy and nonanemic infants; however, absorption depends on iron bioavailability of different foods and on the infant’s iron storage. Iron found in fish and meat (heme iron) is absorbed for about 25%, while the percentage of iron absorbed from vegetables (nonheme) varies from 2% to 13% (EFSA, 2015a,b,c). Because of lower bioavailability of iron from a vegetarian diet, the recommended iron intakes for vegetarians are 1.8 times that of nonvegetarians (Craig et al., 2009) (Trumbo et al., 2001). The iron in plant foods is nonheme iron, which is sensitive to both inhibitors and enhancers of iron absorption. Inhibitors of iron absorption include phytates, calcium, and the polyphenolics compounds in tea, coffee, herb teas, and cocoa. Fiber only
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slightly inhibits iron absorption (Coudray et al., 1997). Some food preparation techniques such as soaking and sprouting of beans, grains, and seeds, and the leavening of bread, can diminish phytate levels. Other fermentation processes, such as those used to make miso and tempeh, may also improve iron bioavailability. Vegetable foods with high iron content are dark green leafy vegetables, lentils, chickpeas, peas, and curry powder (it is still unclear how efficiently the iron in curry powder is absorbed). Vitamin C and other organic acids found in fruits and vegetables can substantially enhance iron absorption and reduce the inhibitory effects of phytate and thereby improve iron status (Hallberg and Hulthén, 2000). Key point. Iron bioavailability of plant foods is low. Some food preparation techniques diminish phytate levels. Vitamin C enhances iron absorption. Iron-fortified cereals are recommended to all vegetarian and nonvegetarian infants from the sixth month of life.
2.6 Zinc in Infants (7–12 Months) EFSA: Zinc: a daily intake of 2.9 mg is recommended (EFSA, 2015a,b). The bioavailability of zinc from vegetarian diets is lower than from nonvegetarian diets, mainly due to the higher phytic acid content of vegetarian diets (Hunt, 2003). Zinc sources include soy products, legumes, grains, cheese, and nuts. Food preparation techniques are the same used for increasing iron bioavailability, which can reduce binding of zinc by phytic acid and increase zinc bioavailability, too (Lönnerdal, 2000). Organic acids, such as citric acid, can also enhance zinc absorption to some extent (Lönnerdal, 2000). The reader may read the specific chapter about zinc intake and status in vegetarians to further develop the question. Zinc is important for growth and the maintenance and development of immune cells of both the innate and adaptive immune system (Maares and Haase, 2016). Breast milk provides sufficient zinc for the first 4–6 months of life but does not provide recommended amounts of zinc for infants aged 7–12 months, who need 2.9 mg/day. Thus, foods with zinc (fortified or natural) should be introduced at 7 months. Vegetarian infants who grow slowly should be assessed for zinc intake and status. Key point. Zinc bioavailability of plant foods is low. As for iron, food preparation techniques and organic acids can enhance zinc absorption.
2.7 Calcium in Infants (7–12 Months) EFSA: Average intake is estimated to be 280 mg/day. This is close to the value derived using the factorial approach, 241 mg/day (EFSA, 2015a,b). Calcium intakes of ovolactovegetarians are similar to those of nonvegetarians, whereas intakes of vegans tend to be lower and may fall below recommended intakes (Craig et al., 2009). Breast milk and infant formula both provide an adequate amount of calcium. The bioavailability of calcium from soy infant formula fortified with calcium carbonate is equivalent to infant formula (Messina et al., 2003). Ovolactovegetarian babies can get calcium from low-oxalate greens (broccoli, cabbage, collards, and kale)
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that are sources of highly bioavailable calcium, and from calcium-set tofu and sesame seeds, almonds, and dried beans that have a lower bioavailability (Weaver et al., 1999). Many vegans meet their calcium requirements by using calcium-fortified foods (e.g., calcium-fortified cereals) or dietary supplements (Weaver et al., 1999). Factors present in plant-based diets such as oxalic acid and phytic acid can potentially interfere with absorption and retention of calcium and thereby have a negative effect on bone mineral density. As mentioned before, some food preparation techniques can diminish phytate level. Approximately 30% of calcium is absorbed from dairy products and fortified food; almost twice as much is absorbed from some vegetables such as broccoli and kale (Mangels, 2014). Another important source of calcium is mineral water that contributes to reach the requirements. The daily recommended intake of liquids is 100 mL/Kg (Alvisi et al., 2015). It is advisable to consume water and to avoid energy-providing liquids, which present a high content of free sugars. Key point. Dairy products and calcium-rich vegetables and fruits are recommended. Water is a fundamental calcium source.
2.8 Sodium in Infants (7–12 Months) EFSA: Data are not sufficient to establish an upper level from dietary sources; a reduction in the sodium consumed in the diet is recommended for the whole population (EFSA, 2005). Nonspecific recommendations are needed for vegetarian complementary feeding. For the general infant population, it is advisable not to add salt to food until 1 year of age, as the sodium content of some foods is enough to cover the daily requirement (EFSA, 2005). Key point. It is advisable not to add salt to food until 1 year of age.
2.9 Vitamin B12 in Infants (7–12 Months) EFSA: Average intake is 1.5 μg/day in infants aged 7–11 months (EFSA, 2015a,b). Plant foods do not contain a significant amount of active vitamin B12, thus the status of vegetarians is less than adequate (Herrmann et al., 2001). Vitamin B12 must be obtained from regular use of vitamin B12-fortified foods; otherwise a daily supplement is needed (Craig et al., 2009). Ovolactovegetarian infants usually have sufficient levels of vitamin B12 from a regular consumption of dairy foods, eggs, and vitamin B12-fortified foods (fortified soy formula and some cereals). Vegans are thus at great risk of B12 deficiency, and the infant born to a vegan mother may be already deficient in B12 and may present neural defects at birth (Peker et al., 2015). Breast-fed infants of nonsupplemented vegan mothers need to take vitamin B12 supplementation. Infants should be given supplements as prescribed by the health care provider (Craig et al., 2009). Key point. Plant foods are not a source of vitamin B12. B12-fortified foods (for example, cereals) have to be preferred. Supplements are needed both for vegan infants and vegan breast-feeding mothers.
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3. Conclusion Plant-based milk substitutes (such as soy, rice, or almond milk), homemade formulas, cow’s milk, and goat’s milk should not be used to replace breast milk or infant formula during the first year of life. These foods do not have the right amounts and quality of protein, fat, and carbohydrate. They do not have enough of many vitamins and minerals that the infant requires. A well-planned ovolactovegetarian diet can be completely adequate during infancy, and complementary feeding should follow the same timing and principles as for nonvegetarian infants. As concerning growth and development, some descriptive cohort studies have demonstrated an identical growth and weight evolution in ovolactovegetarian children and adolescents compared to their omnivorous peers, whereas vegan children tend to be leaner and smaller (Van Winckel et al., 2011). On the contrary, careful dietary planning is needed for infants who are weaned onto vegan diet, who have to be supplemented with vitamin B12, with special attention to adequate intakes of calcium and zinc and energy-dense foods containing enough high-quality protein. Vegetarian diets can be as diverse as omnivorous ones, but it is important to remember that the more restricted the diet and the younger the child, the greater the risk for deficiencies (Yen et al., 2008) and the risk of later feeding behavior difficulties. Parents and caregivers should be knowledgeable to provide an adequate vegetarian nutrition. The best advice for parents who want their children to follow a vegetarian regimen is to ask informed pediatricians or dieticians, to find out how to create an optimal dietary menu for their infants. As in the infant general population, monitoring weight changes, growth, and psychomotor evolution is indicated and part of the nutritional evaluation of vegetarian infants, too. The period of life between birth and 2 years is important for the development of eating habits and to shape infants’ preferences. The most important phase may be the beginning of complementary feeding, when infants discover the sensory (texture, taste, and flavor) aspect of the foods that will be part of their adult diet. In this period, eating preferences emerge, and they depend on the foods offered and on the context of feeding (Nicklaus, 2015). Offering food variety is the best rule to ensure the achievement of both nutritional requirements and the goal of teaching infants the different tastings of foods. If early experience includes exposure to a variety of foods and flavors, then a wider range of foods and flavors will be accepted. Caregivers have the responsibility for making the decisions about their infant’s feeding, and they may serve as a model for an infant’s eating, because much of the early learning about food occurs in the family (Birch and Doub, 2014). Doctors, nurses, and dieticians can play a key role in helping parents provide varied vegetarian diets for their infants that contain adequate amounts of nutrients and energy and to identify the characteristics of the eating experience that will contribute to drive an infant’s eating behavior. Further studies are needed to assess the bioavailability of micronutrients in vegetarian infants and relative supplementations and to tailor specific recommendations.
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4. Nutritional Advices in Vegetarian Infants (0–12 Months) • E xclusive breast-feeding for 6 months is a desirable goal. • The introduction of complementary foods should not be before 17 weeks or delayed beyond 26 weeks. • Vegetarian complementary feeding should be carefully planned by a pediatrician or dietician. Infant growth, neurological development, and nutritional habits should be all monitored. • Continued breast-feeding or at least 500 mL of infant formula during complementary feeding ensures reaching calcium requirements. • Rice, almond, and soy “milk” are not suitable milk substitutes, even if supplemented with calcium. Infant formula or soy formula are indicated. • The introduction of cow or soy milk should not be before 12 months of life. • Timing of solid foods introduction is the same as in nonvegetarians. • Particular attention should be given to reach adequate energy, protein, and lipids requirements. • Iron-rich complementary foods should be given to avoid iron deficiency. • Vitamin B12 supplements are recommended to ovolactovegetarians, and especially vegans, to ensure adequate vitamin B12 intake to prevent deficiency. • Caregivers should offer their infants a variety of foods to teach them different flavors.
References Agostoni, C., Laicini, E., 2014. Early exposure to allergens: a new window of opportunity for noncommunicable disease prevention in complementary feeding? Int. J. Food Sci. Nutr. 65 (1), 1–2. Agostoni, C., et al., 2005. How much protein is safe? Int. J. Obes. 29 (Suppl. 2), S8–S13. Alvisi, P., et al., 2015. Recommendations on complementary feeding for healthy, full-term infants. Ital. J. Pediatr. 41, 36. American Academy of Pediatrics Committee on Nutrition, 1998. Soy protein-based formulas: recommendations for use in infant feeding. Pediatrics 101 (1 Pt 1), 148–153. American Academy of Pediatrics, 2005. Breastfeeding and the use of human milk. Pediatrics 115 (2), 496–506. Amit, M., May 2010. Vegetarian diets in children and adolescents. Paediatr. Child Health 15 (5), 303–314. Appleby, P.N., Crowe, F.L., Bradbury, K.E., et al., January 2016. Mortality in vegetarians and comparable nonvegetarians in the United Kingdom. Am. J. Clin. Nutr. 103 (1), 218–230. Aranceta, J., Perez-Rodrigo, C., 2012. Recommended dietary reference intakes, nutritional goals and dietary guidelines for fat and fatty acids: a systematic review. Br. J. Nutr. 107, S8–S22. Association, N.S.C.O.T.B.P., 1988. Vegetarian weaning. Arch. Dis. Child. 63, 1286–1292 1–7. Beyerlein, A., et al., 2014. Timing of gluten introduction and islet autoimmunity in young children: updated results from the BABYDIET study. Diabetes Care 37 (9), e194–e195. Birch, L.L., Doub, A.E., 2014. Learning to eat: birth to age 2 y. Am. J. Clin. Nutr. 99 (3), 723S–728S. Blaak, E.E., 2016. Carbohydrate quantity and quality and cardio-metabolic risk. Curr. Opin. Clin. Nutr. Metab. Care 19 (4), 289–293.
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Butte, N.F., 2007. Energy requirements of infants. Public Health Nutr. 8 (7a). Butte, N.F., et al., 2010. Nutrient intakes of US infants, toddlers, and preschoolers meet or exceed dietary reference intakes. J. Am. Diet. Assoc. 110 (Suppl. 12), S27–S37. Chalouhi, C., Faesch, S., Anthoine-Milhomme, M.C., et al., August 2008. Neurological consequences of vitamin B12 deficiency and its treatment. Pediatr. Emerg. Care 24 (8), 538–541. Coudray, C., et al., 1997. Effect of soluble or partly soluble dietary fibres supplementation on absorption and balance of calcium, magnesium, iron and zinc in healthy young men. Eur. J. Clin. Nutr. 51 (6), 375–380. Craig, W.J., Mangels, A.R., American Dietetic Association, 2009. Position of the American Dietetic Association: vegetarian diets. J. Am. Diet. Assoc. 109 (7), 1266–1282. De Mel, D., Suphioglu, C., August 15, 2014. Fishy business: effect of omega-3 fatty acids on zinc transporters and free zinc availability in human neuronal cells. Nutrients 6 (8), 3245–3258. De Silva, D., et al., 2014. Primary prevention of food allergy in children and adults: systematic review. Allergy 69 (5), 581–589. Domellöf, M., et al., 2002. Iron absorption in breast-fed infants: effects of age, iron status, iron supplements, and complementary foods. Am. J. Clin. Nutr. 76 (1), 198–204. Domellöf, M., et al., 2014. Iron requirements of infants and toddlers. J. Pediatr. Gastroenterol. Nutr. 58 (1), 119–129. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2005. Opinion of the scientific panel on dietetic products, nutrition and allergies on a request from the commission related to the tolerable upper intake level of sodium. EFSA J. 209, 1–26. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2009. Scientific opinion on the appropriate age for introduction of complementary feeding of infants. EFSA J. 7 (12), 1423. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2010a. Scientific opinion on dietary reference values for carbohydrates and dietary fibre. EFSA J. 8 (3), 1462. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2010b. Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J. 8 (3), 1461. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2012. Scientific opinion on dietary reference values for protein. EFSA J. 10 (2), 2557, 66 pp. http://dx.doi.org/10.2903/j.efsa.2012.255. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2013. Scientific opinion on dietary reference values for energy. EFSA J. 11 (1), 3005. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2014a. Scientific opinion on dietary reference values for zinc. EFSA J. 12 (10), 3844. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA), 2014b. Scientific opinion on the essential composition of infant and follow-on formulae. EFSA J. 12 (7), 3760 106. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2015a. Scientific opinion on dietary reference values for calcium. EFSA J. 13 (5), 4101 82. EFSA Panel on Dietetic Products, Nutrition and Allergies (NDA), 2015b. Scientific opinion on dietary reference values for cobalamin (vitamin B12). EFSA J. 13 (7), 4150. EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA), 2015c. Scientific opinion on dietary reference values for iron. EFSA J. 13 (10), 4254, 115 pp. http://dx.doi.org/10.2903/j.efsa.2015.4254. Escribano, J., et al., 2012. Effect of protein intake and weight gain velocity on body fat mass at 6 months of age: the EU Childhood Obesity Programme. Int. J. Obes. (2005) 36 (4), 548–553. ESPGHAN Committee on Nutrition, 2015. Complementary Feeding: A Commentary by the ESPGHAN Committee on Nutrition, pp. 1–12.
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Grimshaw, K.E.C., et al., 2013. Introduction of complementary foods and the relationship to food allergy. Pediatrics 132 (6), e1529–e1538. Guideline: Sugars Intake for Adults and Children, 2015. World Health Organization, Geneva. Günther, A.L.B., et al., 2007. Early protein intake and later obesity risk: which protein sources at which time points throughout infancy and childhood are important for body mass index and body fat percentage at 7 y of age? Am. J. Clin. Nutr. 86 (6), 1765–1772. Hallberg, L., Hulthén, L., 2000. Prediction of dietary iron absorption: an algorithm for calculating absorption and bioavailability of dietary iron. Am. J. Clin. Nutr. 71 (5), 1147–1160. Herrmann, W., et al., 2001. Total homocysteine, vitamin B12, and total antioxidant status in vegetarians. Clin. Chem. 47 (6), 1094–1101 pp. 1–8. Hunt, J.R., 2003. Bioavailability of iron, zinc, and other trace minerals from vegetarian diets. Am. J. Clin. Nutr. 78 (Suppl. 3), 633S–639S. Jacobs, C., JT, D., 1988. Vegetraina infants: appropriate and inappropriate diets. Am. J. Clin. Nutr. 1–8. Joint WHO/FAO/UNU Expert Consultation, 2007. Protein and Amino Acid Requirements in Human Nutrition. World Health Organization technical report series, (935), pp. 1–265. Kaganov, B., Caroli, M., Mazur, A., et al., May 13, 2015. Suboptimal micronutrient intake among children in Europe. Nutrients 7 (5), 3524–3535. Kleinman, R.E., 2000. American Academy of Pediatrics recommendations for complementary feeding. Pediatrics 106 (5), 1274. Libuda, L., Mesch, C., Stimming, M., Demmelmair, H., Koletzko, B., Warschburger, P., et al., 2016. Fatty acid supply with complementary foods and LC-PUFA status in healthy infants: results of a randomised controlled trial. Eur. J. Nutr. 55 (4), 1633–1644. Lönnerdal, B., 2000. Dietary factors influencing zinc absorption. J. Nutr. 130 (5S Suppl.), 1378S–1383S. Mangels, A.R., Messina, V., 2001. Considerations in planning vegan diets: infants. J. Am. Diet. Assoc. 101 (6), 670–677. Maares, M., Haase, H., 2016. Zinc and immunity: an essential interrelation. Arch. Biochem. Biophys. 611 (Epub ahead of print). Mangels, A.R., July 2014. Bone nutrients for vegetarians. Am. J. Clin. Nutr. 100 (Suppl. 1), 469S–475S. Messina, V., Melina, V., Mangels, A.R., 2003. A new food guide for North American vegetarians. J. Am. Diet. Assoc. 103 (6), 771–775. Michaelsen, K.F., Greer, F.R., 2014. Protein needs early in life and long-term health. Am. J. Clin. Nutr. 99 (3), 718S–722S. Mulder, K.A., King, D.J., Innis, S.M., 2014. Omega-3 fatty acid deficiency in infants before birth identified using a randomized trial of maternal DHA supplementation in pregnancy. PLoS One 9 (1), e83764. Nicklaus, S., 2015. The role of food experiences during early childhood in food pleasure learning. Appetite 104, 3–9. Peker, E., Demir, N., Tuncer, O., et al., November 2015. The levels of vitamin B12, folate and homocysteine in mothers and their babies with neural tube defects. J. Matern. Fetal Neonatal Med. 23, 1–5 (Epub ahead of print). Rolland-Cachera, M.F., et al., 2006. Early adiposity rebound: causes and consequences for obesity in children and adults. Int. J. Obes. 30, S11–S17. Rolland-Cachera, M.F., et al., 2013. Association of nutrition in early life with body fat and serum leptin at adult age. Int. J. Obes. (Lond.) 37, 1116–1122. Rosell, M.S., et al., 2005. Long-chain n-3 polyunsaturated fatty acids in plasma in British meat-eating, vegetarian, and vegan men. Am. J. Clin. Nutr. 82 (2), 327–334.
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Rouhani, M.H., Kelishadi, R., Hashemipour, M., et al., April 2016. The impact of a low glycemic index diet on inflammatory markers and serum adiponectin concentration in adolescent overweight and obese girls: a randomized clinical trial. Horm. Metab. Res. 48 (4), 251–256. Schwartz, J., Dube, K., Sichert-Hellert, W., et al., 2009. Modification of dietary polyunsaturated fatty acids via complementary food enhances n-3 long-chain polyunsaturated fatty acid synthesis in healthy infants: a double blinded randomized controlled trial. Arch. Dis. Child. 94 (11), 876–882. Trumbo, P., Yates, A.A., Schlicker, S., Poos, M., March 2001. Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J. Am. Diet. Assoc. 101 (3), 294–301. Uauy, R., Dangour, A.D., 2009. Fat and fatty acid requirements and recommendations for infants of 0–2 years and children of 2-18 years. Ann. Nutr. Metab. 55 (1–3), 76–96. United Nations System Standard Committee on Nutrition, 2006. Report of the Standing Committee on Nutrition at its Thirty-Third Session. 1–27. Van Winckel, M., et al., 2011. Clinical practice: vegetarian infant and child nutrition. Eur. J. Pediatr. 170 (12), 1489–1494. Vriezinga, S.L., et al., 2014. Randomized feeding intervention in infants at high risk for celiac disease. N. Engl. J. Med. 371 (14), 1304–1315. Weaver, C.M., Proulx, W.R., Heaney, R., 1999. Choices for achieving adequate dietary calcium with a vegetarian diet. Am. J. Clin. Nutr. 70 (Suppl. 3), 543S–548S. WHO, 2003. Guiding Principles for Complementary Feeding of the Breastfed Child. 1–40. Yen, C.E., et al., 2008. Dietary intake and nutritional status of vegetarian and omnivorous preschool children and their parents in Taiwan. Nutr. Res. 28 (7), 430–436.
Vegetarian Infants and Complementary Feeding Silvia Scaglioni1, Valentina De Cosmi1,2, Alessandra Mazzocchi1,2, Silvia Bettocchi1,3, Carlo Agostoni1,2 1 FOND AZI O NE 2 UNIVERS I TY
I RCCS CÀ GRANDA OS P E D A L E MA G G I O R E P O L I C L I N I C O , MI L A N , I TA LY; O F M I L AN, M I L AN, I TA LY; 3 U N I V E R S I T À C AT T O L I C A D E L S A C R O C U O R E , MI L A N , I TA LY
1. Introduction Complementary feeding is the period of time when infants are introduced to food different from milk in their diet, together with a gradual reduction of the intake of milk (either breast milk or formula), to finally and gradually acquire their family’s diet model (Alvisi et al., 2015). This definition is based on the one proposed by the European Food Safety Authority (EFSA, 2009) and by the European Society for Pediatric Gastroenterology, Hepatology, and Nutrition (ESPGHAN) (ESPGHAN Committee on Nutrition, 2015). The World Health Organization (WHO) has described the complementary feeding period as ‘‘the period during which other foods or liquids are provided along with breast milk’’ and states that ‘‘any nutrient-containing foods or liquids other than breast milk given to young children during the period of complementary feeding are defined as complementary foods.’’ The ESPGHAN Committee on Nutrition, the American Academy of Pediatrics (AAP), and the WHO consider that exclusive or full breast-feeding for 6 months is a desirable goal (ESPGHAN Committee on Nutrition, 2015; Kleinman, 2000; WHO, 2003). The introduction of complementary foods should not be before 17 weeks but should not be delayed beyond 26 weeks. Around the sixth month of life, breast milk becomes insufficient to meet requirements for macronutrients and micronutrients, as the infant’s age and weight both increase. Infants gradually lose the extrusion reflex, and they develop the ability to swallow solids and start to show an interest in adult family foods. A balanced number of factors let them gain a good relationship with food and the achievement of nutritional requirements (Alvisi et al., 2015): • acquisition of fundamental milestones in neuromotor development • development of taste and personal inclinations • maturation of renal and gastrointestinal functionality • qualitative and quantitative implementation of nutritional intake • interaction of cultural and socioeconomic factors with local and family traditions Vegetarian and Plant-Based Diets in Health and Disease Prevention. http://dx.doi.org/10.1016/B978-0-12-803968-7.00029-0 Copyright © 2017 Elsevier Inc. All rights reserved.
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Enough attention should be paid to all these aspects: nutritional and developmental reasons drive this transition, which will influence later health. The AAP recommends that breast milk should be continued for at least 12 months along with appropriate supplementary foods (American Academy of Pediatrics, 2005). Important data point out that breast milk has a favoring role in psychological and nutritional aspects and in the development of tolerance; thus, it might reduce the onset of allergies (Grimshaw et al., 2013). Exclusive breastfeeding by well-nourished mothers for 6 months can meet a healthy infant’s requirements for water, energy, protein, calcium, and most vitamins and minerals (EFSA, 2013). The breast milk of ovolactovegetarian women is similar in composition to that of nonvegetarians, and it is nutritionally adequate too (Craig et al., 2009). For that reason, there are no evidences that timing of solid foods introduction in vegetarian weaning should differ from nonvegetarians. In the first year of life, if breast-feeding is not possible, the only alternative is infant formula, or soy formula for vegan infants. The introduction of cow milk should not be before the 12th month of life, due to its high protein content, low iron concentration, and the risk of iron deficiency (Domellöf et al., 2014). Fortified soy milk can be used as a primary beverage starting at age of 1 year or older, too (Mangels and Messina, 2001). Other preparations including soy milk, rice milk, and homemade formulas should not be used to replace breast milk or commercial infant formula, due to their poor nutritional quality. Different weaning practices have characterized this stage of life according to traditions, ethnical origins, and scientific beliefs. Actually, there are not rigid schemes on timing of food introduction, especially fruits and vegetables (Alvisi et al., 2015). In the latest suggestions issued by AAP, ESPGHAN, and European Academy of Allergy and Clinical Immunology (De Silva et al., 2014), it is recognized that there is no scientific evidence to justify the delayed introduction of solid foods (after 6 months of age), even those recognized as more allergenic, to prevent allergic diseases (Agostoni and Laicini, 2014). Vegetarian complementary feeding is widespread because vegetarian families are increasing and they want their children to share their nutritional habits starting from complementary feeding: vegetarians and vegans have been estimated to constitute 5% and 2%, respectively, of the US population, and in Italy, vegetarians are 7.1% of the total population (EURISPES survey; Appleby et al., 2016). Literature informs that well-planned vegetarian diets are appropriate for individuals during all stages of the life cycle, including pregnancy, lactation, infancy, childhood, and adolescence, and for athletes (Craig et al., 2009). A vegetarian diet is characterized by the choice of a wide variety of foods of vegetal origin and by the exclusion of animal foods (meat, fish, and their derivatives). The reader may read Chapter 1 of this book for a full characterization of the different diets. The two main categories of vegetarian complementary feeding that will be discussed in this chapter are ovolactovegetarian, which includes dairy and egg products, and vegan weaning, which is characterized by the absence of any type of animal foods. The period from birth to 1 year is a time of nutritional vulnerability when attention to proper nutrition is critical to support the extremely rapid growth, including brain growth. In this phase, particular attention should be paid because a regular growth and neurodevelopment are relevant goals. Ovolactovegetarian weaning can be adopted, but it must be correctly designed, to favor a healthy diet and to prevent nutritional deficiencies that are
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a real risk of vegetarian diet. Foods in the vegan diet repertoire cannot alone cover energy, macronutrients, and micronutrients requirements of the infant; consequently supplementations are needed (Amit, 2010; Chalouhi et al., 2008; Kaganov et al., 2015).
2. Vegetarian Complementary Solid Food, Macronutrients, and Micronutrients Requirements Differences between vegetarian solid foods and nonvegetarian ones are limited to replacement of meat with mashed or pureed tofu, legumes (pureed and strained if necessary), soy or dairy yogurt, cooked egg yolk, and cottage cheese. Later, around 7–10 months, foods such as cubed tofu, cheese or soy cheese, and small pieces of veggie burgers can be started. A balanced use of foods out of the following alimentary groups—fruits, vegetables, cereals, dried fruits, legumes, water, and oilseeds—permit one to conduct a good vegetarian complementary feeding (Craig et al., 2009). In the second half of the first year of life, breast milk alone is not enough to supply a sufficient amount of calories, proteins, zinc, iron, and fat-soluble vitamins (vitamins A, D, K) that are necessary to guarantee an adequate growth to the infant (ESPGHAN Committee on Nutrition, 2015; EFSA, 2009). Complementary feeding is an important phase in the growth of a child, and it can play a major role in a child’s future health and in its future feeding behavior. Early feeding contributes to prevent noncommunicable adult diseases (United Nations System Standard Committee on Nutrition, 2006). The recommended intakes suggested subsequently for infants in the second semester of life have been extracted from EFSA Scientific Opinions on Dietary Reference Values for energy, micronutrients, and macronutrients and from a position paper by the American Dietetic Association (ADA) about vegetarian diets (Craig et al., 2009).
2.1 Energy in Infants (7–12 Months) EFSA: The recommended intake of energy is 76–79 kcal/Kg/day (EFSA, 2013). The recommended energy intake should be correctly distributed among the various macronutrients, both in terms of quantity and quality (Alvisi et al., 2015). It is known that the energy content of human milk varies within a meal, with lactational stage, and between individuals. Assuming an average energy content of human milk of 0.67 kcal/g, mean energy requirements are met by exclusive breast-feeding during the first 6 months of life and possibly longer (Butte, 2007). Also, the protein content of human milk changes with lactational stage and is on average 13 g/L in the second week, 9 g/L in the second month, and 8 g/L in the fourth month until weaning. In mature milk, there is a low content of iron (0.2–0.4 mg/L) and zinc (about 0.5 mg/L at 6 months), and both decrease with the length of lactation (EFSA, 2013). The energy density of many vegetarian foods (cereals, fruits, vegetables) is low, due to low fat and high fiber content, and infants may have difficulty consuming
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the necessary volume of diet to achieve adequate energy intake (British Paediatric Association, 1988). Their stomach capacity is limited, and children from 1–3 years of age are able to take 200–300 mL at each meal. Fiber and complex carbohydrates have a higher water content, and this results in a lower energy density of the foods and favors early satiation (Jacobs and JT, 1988). Energy is needed to maintain physiological activities and deposition of tissues. Growing is a dynamic and energy-consuming process that should be adequately supported: it is about 5 kcal/g of new tissue (3.5 kcal energy “stored” and 1.5 kcal for cost of synthesis). In the first month of life, energy requirements for growth are 40%, and they decrease to about 3% at the age of 12 months, due to the decrease of growth rate (Butte, 2007). Growth during complementary feeding should continue to be monitored and plotted on standard centile charts as part of health surveillance by the pediatrician, and mothers should be advised appropriately if growth deviates from the expected. It is important that vegetarian parents know how to ensure an adequate intake of energy by their infants. Doctors, dieticians, and nurses should give them practical tips on how to increase energy density of foods (Mangels and Messina, 2001). The first practical trick is to feed their baby at least four times a day, including energy-dense complementary foods at each meal. Ripe bananas have 15%–20% carbohydrate, and avocados are rich in fat; thus both of them are good sources of energy. Cereals and pulses are usually more energy-dense than fruits. Adding fats such as extra virgin olive oil to cereal meals or peanut butter to bread improve the energy density of the meal itself. Parents should promote water consumption, avoiding allowing the infant to drink any kind of energy-providing liquids. Key point: Energy is needed to support growth. High-fiber and high-complexcarbohydrate diets lower the caloric density of the foods and favor an early satiety.
2.2 Protein in Infants (7–12 Months) EFSA: The recommended intake is about 10% of total calories (1.1 g/Kg/day, average recommended intake 11 g/day for 6 months of age) (EFSA, 2012). ADA: Precautional protein increase of 10%–15% of the recommended intake for age (Craig et al., 2009). Recommended protein intake has been reduced in the past few years, due to the alignment on human milk content (EFSA, 2014a,b), falling in line with the hypothesis that hyperproteic diets in early life may favor the onset of obesity (Alvisi et al., 2015). An excess of proteins would stimulate the secretion of insulin and IGF1, both responsible for adipogenesis and the differentiation of adipocytes. Data available in literature suggest that between 6 and 24 months of age, a protein intake of more than 15% of total energy can lead, in some subjects, to early adiposity rebound phenomena, thus favoring the development of future obesity (Agostoni et al., 2005; Rolland-Cachera et al., 2006). No association has been found between a high intake of fats with complementary feeding and obesity in the following ages; on the contrary, Rolland-Cachera et al. identified in a high-protein and low-fat dietary pattern a hyperproteic and hypolipidic pattern of infants living in developed countries as a possible contributing factor of early adiposity rebound and, later in life, of body fat and
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leptin resistance (Rolland-Cachera et al., 2013; Alvisi et al., 2015; Escribano et al., 2012). The diet of infants in the general population is characterized by high protein and low fat intakes (Michaelsen and Greer, 2014). Together with the attention to protein and fat intake, energy has to be taken into account, since it represents the main determinant of fat deposition. Nevertheless, the relation between protein intake during complementary feeding and later risk of noncommunicable diseases is still unclear. Not only the quantity, but also the quality of proteins seems to play a role in the association between early intakes and later fatness. The longitudinal DONALD study reported that the protein sources that may be mostly responsible for the association with adiposity at 7 years old are animal protein, and more specifically dairy products at 12 months (Günther et al., 2007). However, in vegetarian infants the risk is rather to fail reaching the recommended protein intake, and this risk can be reduced by continuing the intake of breast milk or formula. It has to be taken into account that many vegetable proteins are low in one or more essential amino acids, and the total indispensable amino acid content in vegetable foods is low when compared to animal protein sources (Craig et al., 2009). Because vegetable foods have not the same quantity and quality of proteins, vegetarians’ dietary choices are crucial to achieve the adequate protein intake. Plant proteins can meet protein requirements when a variety of plant foods are consumed and energy needs are met (Mangels and Messina, 2001). Eating a huge variety of plant foods over the course of a day can provide all essential amino acids and adequate nitrogen retention (American Academy of Pediatrics Committee on Nutrition, 1998). Encouraging infants to continue to take about 500 mL/day of breast milk or formula reduces the needs for other proteins sources. Mixing breast milk or formula intake, which provides proteins rich in indispensable amino acids, with vegetable protein foods enhances the amino acid composition of the meal and improves net protein utilization. Legumes and soy beans have a high proportion of proteins (over 20% and about 36%, respectively), but a low biological value. Based on the protein digestibilitycorrected amino acid score, which is the standard method for determining protein quality, a combination of legumes and wheat proteins enhances the nitrogen utilization efficiency (Craig et al., 2009), and the choice of shelled beans minimizes the phytic acid intake. In vegetarian infant diet, a precautionary increase of proteins is suggested, around 10%–15% of the recommended energy intake for age. Attention should be paid to not to exceed the 15% and to avoid the risk of protein excess (Joint WHO/FAO/UNU Expert Consultation, 2007). Key point: Proteins are crucial for growth. In not well-balanced vegetarian diets, there is a consistent risk to not reach protein requirements.
2.3 Lipids in Infants (7–12 Months) EFSA: Lipids: recommended intake is 40% of total calories (EFSA, 2010a,b). Lipids are the main energy source in the infant diet and are necessary for normal growth and physical activity. Lipids are also important structural components of neural and other body tissues (Uauy and Dangour, 2009; Butte et al., 2010). The selection of dietary fat and
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fatty acid sources during the first years of life is now considered to be of critical importance (Uauy and Dangour, 2009). Consumption of n-3 PUFAs eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) have demonstrated physiological benefits on blood pressure, heart rate, triglycerides, and likely inflammation, endothelial function, and cardiac diastolic function (Aranceta and Perez-Rodrigo, 2012). DHA plays a major role in development of the brain and retina during fetal development and the first 2 years of life (Uauy and Dangour, 2009). When DHA-rich products are excluded, the recommended intake of total lipids and of ω-3 series cannot be achieved, and there is the risk of low DHA blood level and relative deficiency (Rosell et al., 2005). The proposal that dietary DHA enhances neurocognitive functioning in term infants is controversial. Theoretical evidence, laboratory research, and human epidemiological studies have convincingly demonstrated that DHA deficiency can negatively impact neurocognitive development (Schwartz et al., 2009). DHA deficiency may be the cause of many disorders, such as depression, inability to concentrate, excessive mood swings, anxiety, cardiac disease, type 2 diabetes, and dry skin (De Mel and Suphioglu, 2014). Nutrient deficiency during development may have long-lasting consequences for the central nervous system that range from devastating malformations to subtle effects on neural functioning. DHA is enriched in brain and retina membranes, where it functions in early development events, such as neurogenesis, neurite outgrowth, synaptic plasticity, axonal elimination, and gene expression (Mulder et al., 2014). One of the main considerations when trying to meet current recommendations for n-3 fatty acids is that current intake of PUFAs consists primarily of n-6 fatty acids. The competition for desaturases and elongases in n-3 and n-6 PUFA metabolism results in inverse effects on tissue concentrations of these fatty acids. This is of even greater concern in vegetarians and vegans, who have relatively high intakes of linoleic acid (LA) combined with low intakes of EPA and DHA (Aranceta and Perez-Rodrigo, 2012). Vegetarians tend to consume a lot of n-6 but marginal amounts of n-3 fatty acids. To restore n6/n3 balance, regular consumption of micro-algae (rich in DHA) and of walnuts, canola oil, flaxseed oil, enriched dairy products, seeds, peanut butter, soy beans, and derivatives (rich in alfa-linolenic fatty acid, ALA) is recommended (Van Winckel et al., 2011). EFSA has not established recommended intakes for n3-PUFAs but for specific n-3 fatty acids, namely ALA, EPA, and DHA. EFSA proposed not to set specific values for the n-3/n-6 ratio and to set an average intake of 100 mg DHA for infants (>6 months) and young children. In older infants, DHA intakes at levels of 50–100 mg per day have been found effective for visual function in the complementary feeding period and are considered to be adequate for that period. EFSA has set the adequate intake value of 0.5% of total energy for ALA in all population groups (EFSA, 2010a,b). The FAO/WHO 2008 report defines 15% of total energy as upper AMRD (acceptable macronutrients distribution rate) for infants 6–12 months old (Aranceta and PerezRodrigo, 2012).
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An increased intake of ALA, the precursor of endogenous DHA synthesis, has been supposed to be an (alternative) strategy to support infant DHA status. Few studies have tested the effect of replacing LA-rich corn oil with ALA-rapeseed oil in complementary food. It still seems to be a promising strategy, but it remains to be confirmed how this approach affects the DHA status (Libuda et al., 2016). Key point. Lipids are the main energy source (40% of total energy) for the infant, and they are essential for growth and for neural tissue structure. Polyunsaturated and monounsaturated fats have to be preferred. A regular intake of DHA-rich foods is recommended for both vegetarians and vegans.
2.4 Carbohydrates in Infants (7–12 Months) Dietary carbohydrates are the major macronutrients for humans. Both adults and children in the Western countries obtain approximately half their daily caloric requirements from dietary carbohydrates. In other countries, carbohydrate has been the major source of energy, at least until the more recent introduction of “Western foods,” with higher proportions of fat and protein, to many developing countries. There are not current recommendations for infants; EFSA has proposed 45%–60% of total energy as the reference intake range for carbohydrates applicable to both adults and children older than 1 year of age (EFSA, 2010a,b). To decrease the risk of overweight, obesity, and tooth decay, a WHO guideline recommends adults and children reduce their daily intake of free sugars to less than 10% of their total energy intake. A further reduction to below 5% would provide additional health benefits (WHO, 2015). Based on the available evidence on bowel function, EFSA has considered dietary fiber intakes of 25 g/day to be adequate in adults and of 2 g/MJ to be adequate in children from the age of 1 year (EFSA, 2010a,b). It is advisable to prefer starchy alimentary sources, if possible with a low glycemic index, and above all, it is strongly recommended to limit the intake of simple sugars (such as fruit juices, sugar, and sweeteners in general). Carbohydrates in foods with a low glycemic index are more slowly digested and absorbed; consequently, diets with a low glycemic index are beneficial in controlling postprandial plasma glucose excursions. Diets with a low glycemic index and glycemic load, but not low in total carbohydrates, are associated with lower type 2 diabetes mellitus risk, cardiovascular disease risk, and levels of proinflammatory markers and fasting insulin (Blaak, 2016; Rouhani et al., 2016). Recent literature failed to confirm that introducing gluten between week 17 and 26, while the infant is still being breast-fed, would have a protective role on the onset of celiac disease, type 1 diabetes, and wheat allergy (Vriezinga et al., 2014; Beyerlein et al., 2014). Cereals are rich in starch, proteins, minerals, vitamins, and insoluble fibers. Amaranth, quinoa, buckwheat, soy, and lupine have all the indispensable amino acids in sufficient amounts. Other cereals are low in lysine but rich in methionine, whereas this is the opposite in legumes; therefore these protein sources are well known to complement each other. Adding legumes to cereals is possible to obtain adequate biological protein value.
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Choosing refined and lower fiber cereals allows a reduction of phytic acid content, which usually lowers the absorption of minerals (namely, iron, zinc, calcium, and magnesium). ESPGHAN Committee on Nutrition recommends that iron-rich complementary foods (iron-fortified cereals) should be given to all infants from 6 months of age (ESPGHAN Committee on Nutrition, 2015). Both vegetarian and nonvegetarian infants should be introduced to whole grains before the end of the second year of life. Key point. Carbohydrates in starchy alimentary sources are preferred. Reducing free sugars to less than 10% of their total energy intake is recommended.
2.5 Iron in Infants (7–12 Months) EFSA: Iron: a daily intake of 11 mg is recommended (EFSA, 2015a,b,c). ADA: 1.8 times that of nonvegetarians (Craig et al., 2009). Iron is critical for normal growth, hematopoiesis, and neurologic development during infancy. When complementary feeding is not introduced in exclusive breast-fed infants, they are at risk of developing an iron deficit in the second semester (Alvisi et al., 2015). Prevalence of iron deficiency anemia among vegetarians is similar to that of nonvegetarians, and it is approximately 2%–3% at 6–9 months and 3%–9% at 1–3 years of life (Domellöf et al., 2014). Complementary foods have the important role to provide more than 90% of the iron requirements in breast-fed infants (Domellöf et al., 2014). Between 6 and 24 months of age, the infant becomes dependent on additional dietary iron, and because of rapid growth, iron requirements per kilogram body weight are higher than during any other period of life. It has been shown that infants have the ability to upregulate iron absorption when iron requirements increase (Domellöf et al., 2002). This ability of each individual to be able to adapt iron absorption to iron status is likely to make infants more resistant to iron deficiency. The ESPGHAN Committee on Nutrition states that meat products and iron-fortified foods are the major dietary source of iron. Therefore an early introduction of iron-rich complementary foods is highly recommended for preventing iron deficiency anemia in infants (ESPGHAN Committee on Nutrition, 2015). Foods containing iron are meat and fish (bovine: 1.9 mg/100 g; cod 0.7 mg/100 g) and some vegetables (legumes, endive, green chicory, spinach). EFSA assumes a mean value of 10% of iron absorption in healthy and nonanemic infants; however, absorption depends on iron bioavailability of different foods and on the infant’s iron storage. Iron found in fish and meat (heme iron) is absorbed for about 25%, while the percentage of iron absorbed from vegetables (nonheme) varies from 2% to 13% (EFSA, 2015a,b,c). Because of lower bioavailability of iron from a vegetarian diet, the recommended iron intakes for vegetarians are 1.8 times that of nonvegetarians (Craig et al., 2009) (Trumbo et al., 2001). The iron in plant foods is nonheme iron, which is sensitive to both inhibitors and enhancers of iron absorption. Inhibitors of iron absorption include phytates, calcium, and the polyphenolics compounds in tea, coffee, herb teas, and cocoa. Fiber only
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slightly inhibits iron absorption (Coudray et al., 1997). Some food preparation techniques such as soaking and sprouting of beans, grains, and seeds, and the leavening of bread, can diminish phytate levels. Other fermentation processes, such as those used to make miso and tempeh, may also improve iron bioavailability. Vegetable foods with high iron content are dark green leafy vegetables, lentils, chickpeas, peas, and curry powder (it is still unclear how efficiently the iron in curry powder is absorbed). Vitamin C and other organic acids found in fruits and vegetables can substantially enhance iron absorption and reduce the inhibitory effects of phytate and thereby improve iron status (Hallberg and Hulthén, 2000). Key point. Iron bioavailability of plant foods is low. Some food preparation techniques diminish phytate levels. Vitamin C enhances iron absorption. Iron-fortified cereals are recommended to all vegetarian and nonvegetarian infants from the sixth month of life.
2.6 Zinc in Infants (7–12 Months) EFSA: Zinc: a daily intake of 2.9 mg is recommended (EFSA, 2015a,b). The bioavailability of zinc from vegetarian diets is lower than from nonvegetarian diets, mainly due to the higher phytic acid content of vegetarian diets (Hunt, 2003). Zinc sources include soy products, legumes, grains, cheese, and nuts. Food preparation techniques are the same used for increasing iron bioavailability, which can reduce binding of zinc by phytic acid and increase zinc bioavailability, too (Lönnerdal, 2000). Organic acids, such as citric acid, can also enhance zinc absorption to some extent (Lönnerdal, 2000). The reader may read the specific chapter about zinc intake and status in vegetarians to further develop the question. Zinc is important for growth and the maintenance and development of immune cells of both the innate and adaptive immune system (Maares and Haase, 2016). Breast milk provides sufficient zinc for the first 4–6 months of life but does not provide recommended amounts of zinc for infants aged 7–12 months, who need 2.9 mg/day. Thus, foods with zinc (fortified or natural) should be introduced at 7 months. Vegetarian infants who grow slowly should be assessed for zinc intake and status. Key point. Zinc bioavailability of plant foods is low. As for iron, food preparation techniques and organic acids can enhance zinc absorption.
2.7 Calcium in Infants (7–12 Months) EFSA: Average intake is estimated to be 280 mg/day. This is close to the value derived using the factorial approach, 241 mg/day (EFSA, 2015a,b). Calcium intakes of ovolactovegetarians are similar to those of nonvegetarians, whereas intakes of vegans tend to be lower and may fall below recommended intakes (Craig et al., 2009). Breast milk and infant formula both provide an adequate amount of calcium. The bioavailability of calcium from soy infant formula fortified with calcium carbonate is equivalent to infant formula (Messina et al., 2003). Ovolactovegetarian babies can get calcium from low-oxalate greens (broccoli, cabbage, collards, and kale)
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that are sources of highly bioavailable calcium, and from calcium-set tofu and sesame seeds, almonds, and dried beans that have a lower bioavailability (Weaver et al., 1999). Many vegans meet their calcium requirements by using calcium-fortified foods (e.g., calcium-fortified cereals) or dietary supplements (Weaver et al., 1999). Factors present in plant-based diets such as oxalic acid and phytic acid can potentially interfere with absorption and retention of calcium and thereby have a negative effect on bone mineral density. As mentioned before, some food preparation techniques can diminish phytate level. Approximately 30% of calcium is absorbed from dairy products and fortified food; almost twice as much is absorbed from some vegetables such as broccoli and kale (Mangels, 2014). Another important source of calcium is mineral water that contributes to reach the requirements. The daily recommended intake of liquids is 100 mL/Kg (Alvisi et al., 2015). It is advisable to consume water and to avoid energy-providing liquids, which present a high content of free sugars. Key point. Dairy products and calcium-rich vegetables and fruits are recommended. Water is a fundamental calcium source.
2.8 Sodium in Infants (7–12 Months) EFSA: Data are not sufficient to establish an upper level from dietary sources; a reduction in the sodium consumed in the diet is recommended for the whole population (EFSA, 2005). Nonspecific recommendations are needed for vegetarian complementary feeding. For the general infant population, it is advisable not to add salt to food until 1 year of age, as the sodium content of some foods is enough to cover the daily requirement (EFSA, 2005). Key point. It is advisable not to add salt to food until 1 year of age.
2.9 Vitamin B12 in Infants (7–12 Months) EFSA: Average intake is 1.5 μg/day in infants aged 7–11 months (EFSA, 2015a,b). Plant foods do not contain a significant amount of active vitamin B12, thus the status of vegetarians is less than adequate (Herrmann et al., 2001). Vitamin B12 must be obtained from regular use of vitamin B12-fortified foods; otherwise a daily supplement is needed (Craig et al., 2009). Ovolactovegetarian infants usually have sufficient levels of vitamin B12 from a regular consumption of dairy foods, eggs, and vitamin B12-fortified foods (fortified soy formula and some cereals). Vegans are thus at great risk of B12 deficiency, and the infant born to a vegan mother may be already deficient in B12 and may present neural defects at birth (Peker et al., 2015). Breast-fed infants of nonsupplemented vegan mothers need to take vitamin B12 supplementation. Infants should be given supplements as prescribed by the health care provider (Craig et al., 2009). Key point. Plant foods are not a source of vitamin B12. B12-fortified foods (for example, cereals) have to be preferred. Supplements are needed both for vegan infants and vegan breast-feeding mothers.
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3. Conclusion Plant-based milk substitutes (such as soy, rice, or almond milk), homemade formulas, cow’s milk, and goat’s milk should not be used to replace breast milk or infant formula during the first year of life. These foods do not have the right amounts and quality of protein, fat, and carbohydrate. They do not have enough of many vitamins and minerals that the infant requires. A well-planned ovolactovegetarian diet can be completely adequate during infancy, and complementary feeding should follow the same timing and principles as for nonvegetarian infants. As concerning growth and development, some descriptive cohort studies have demonstrated an identical growth and weight evolution in ovolactovegetarian children and adolescents compared to their omnivorous peers, whereas vegan children tend to be leaner and smaller (Van Winckel et al., 2011). On the contrary, careful dietary planning is needed for infants who are weaned onto vegan diet, who have to be supplemented with vitamin B12, with special attention to adequate intakes of calcium and zinc and energy-dense foods containing enough high-quality protein. Vegetarian diets can be as diverse as omnivorous ones, but it is important to remember that the more restricted the diet and the younger the child, the greater the risk for deficiencies (Yen et al., 2008) and the risk of later feeding behavior difficulties. Parents and caregivers should be knowledgeable to provide an adequate vegetarian nutrition. The best advice for parents who want their children to follow a vegetarian regimen is to ask informed pediatricians or dieticians, to find out how to create an optimal dietary menu for their infants. As in the infant general population, monitoring weight changes, growth, and psychomotor evolution is indicated and part of the nutritional evaluation of vegetarian infants, too. The period of life between birth and 2 years is important for the development of eating habits and to shape infants’ preferences. The most important phase may be the beginning of complementary feeding, when infants discover the sensory (texture, taste, and flavor) aspect of the foods that will be part of their adult diet. In this period, eating preferences emerge, and they depend on the foods offered and on the context of feeding (Nicklaus, 2015). Offering food variety is the best rule to ensure the achievement of both nutritional requirements and the goal of teaching infants the different tastings of foods. If early experience includes exposure to a variety of foods and flavors, then a wider range of foods and flavors will be accepted. Caregivers have the responsibility for making the decisions about their infant’s feeding, and they may serve as a model for an infant’s eating, because much of the early learning about food occurs in the family (Birch and Doub, 2014). Doctors, nurses, and dieticians can play a key role in helping parents provide varied vegetarian diets for their infants that contain adequate amounts of nutrients and energy and to identify the characteristics of the eating experience that will contribute to drive an infant’s eating behavior. Further studies are needed to assess the bioavailability of micronutrients in vegetarian infants and relative supplementations and to tailor specific recommendations.
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4. Nutritional Advices in Vegetarian Infants (0–12 Months) • E xclusive breast-feeding for 6 months is a desirable goal. • The introduction of complementary foods should not be before 17 weeks or delayed beyond 26 weeks. • Vegetarian complementary feeding should be carefully planned by a pediatrician or dietician. Infant growth, neurological development, and nutritional habits should be all monitored. • Continued breast-feeding or at least 500 mL of infant formula during complementary feeding ensures reaching calcium requirements. • Rice, almond, and soy “milk” are not suitable milk substitutes, even if supplemented with calcium. Infant formula or soy formula are indicated. • The introduction of cow or soy milk should not be before 12 months of life. • Timing of solid foods introduction is the same as in nonvegetarians. • Particular attention should be given to reach adequate energy, protein, and lipids requirements. • Iron-rich complementary foods should be given to avoid iron deficiency. • Vitamin B12 supplements are recommended to ovolactovegetarians, and especially vegans, to ensure adequate vitamin B12 intake to prevent deficiency. • Caregivers should offer their infants a variety of foods to teach them different flavors.
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Rouhani, M.H., Kelishadi, R., Hashemipour, M., et al., April 2016. The impact of a low glycemic index diet on inflammatory markers and serum adiponectin concentration in adolescent overweight and obese girls: a randomized clinical trial. Horm. Metab. Res. 48 (4), 251–256. Schwartz, J., Dube, K., Sichert-Hellert, W., et al., 2009. Modification of dietary polyunsaturated fatty acids via complementary food enhances n-3 long-chain polyunsaturated fatty acid synthesis in healthy infants: a double blinded randomized controlled trial. Arch. Dis. Child. 94 (11), 876–882. Trumbo, P., Yates, A.A., Schlicker, S., Poos, M., March 2001. Dietary reference intakes: vitamin A, vitamin K, arsenic, boron, chromium, copper, iodine, iron, manganese, molybdenum, nickel, silicon, vanadium, and zinc. J. Am. Diet. Assoc. 101 (3), 294–301. Uauy, R., Dangour, A.D., 2009. Fat and fatty acid requirements and recommendations for infants of 0–2 years and children of 2-18 years. Ann. Nutr. Metab. 55 (1–3), 76–96. United Nations System Standard Committee on Nutrition, 2006. Report of the Standing Committee on Nutrition at its Thirty-Third Session. 1–27. Van Winckel, M., et al., 2011. Clinical practice: vegetarian infant and child nutrition. Eur. J. Pediatr. 170 (12), 1489–1494. Vriezinga, S.L., et al., 2014. Randomized feeding intervention in infants at high risk for celiac disease. N. Engl. J. Med. 371 (14), 1304–1315. Weaver, C.M., Proulx, W.R., Heaney, R., 1999. Choices for achieving adequate dietary calcium with a vegetarian diet. Am. J. Clin. Nutr. 70 (Suppl. 3), 543S–548S. WHO, 2003. Guiding Principles for Complementary Feeding of the Breastfed Child. 1–40. Yen, C.E., et al., 2008. Dietary intake and nutritional status of vegetarian and omnivorous preschool children and their parents in Taiwan. Nutr. Res. 28 (7), 430–436.