Plant based drinks in the diets of infants and young children

ABSTRACT

Plant based drinks (PBD) do not have a role in providing nutrition to infants, other than the feeding of commercial soy and rice hydrolysate based infant formulas for medical, religious or ethical reasons. For toddlers and young children, cow’s milk (CM) has a traditional place in their modern Western diet as an important source of protein, calcium and other nutrients. While milk is not essential to provide a healthy diet for young children, considerable dietary adjustments need to be made to compensate for its absence. Most PBD are not equivalent to CM in terms of inherent nutrient content and bioavailability and are more expensive. There is notable heterogeneity in their nutritional composition. According to recent studies, children who do not drink CM grow slower than those who do. There is relatively little information about the role of specific PBD in children’s diets. Their impact needs to be assessed in the context of their percent of the diet, child age, health status, nutritional requirements and the composition of the rest of the diet. There are both questionable and valid reasons consumers and parents drink and provide PBD to young children, including misinformation, medical conditions, worries about toxins in CM and ethical/religious beliefs. Parents, and consumers in general, are increasingly acting on concerns about animal welfare related to modern farming practices and the adverse environmental impact of meat and dairy farming. Improvements in available alternative drinks and more informative labelling of such products are likely to be welcomed by the marketplace. The new technology of precision fermentation has the potential to lead to milk alternatives that address many of the concerns about both CM and PBD.

INTRODUCTION

There are important nutritional differences among plant based drinks (PBD) and between them and the cow’s milk (CM) they may replace in the diets of children. These differences have been competently documented by a number of authors, on whose work this manuscript relies.^1–5 The North American Society for Pediatric Gastroenterology, Hepatology and Nutrition has identified nutritional concerns about the inappropriate use of PBD for children.⁶ Workers in other fields have examined the environmental impact of growing plants versus dairy and meat farming and ethical frameworks that exclude animal products  from  human  diets.  This  review article seeks to place what we know about the nutrition of CM and alternative PBD in the context of the reasons parents give for choosing PBD for their children.

Role of CM in the diets of children

In societies that farm milk-producing animals, animal milk has long been part of the diet, including the diet of children. Global milk availability has increased since advances in milk processing in the 19th century led to shelf-stable packaged milk products. The expansion of refrigeration in the early 20th century made safe fresh liquid milk more generally available in higher income countries. While thoughtful parents can provide children with a complete and healthy diet in the absence of CM or other animal milk,⁷ it can be difficult to meet all of children’s needs with a vegan diet.⁸ This may be especially true when other foods in the diet come from a narrow range of foods due to availability, selective food purchasing or selective eating behaviour.

CM is commonly added to the toddler diet after the first birthday. It can replace breast milk or formula as the liquid source of nutrition in the diet. By 1 year of age,other foods generally provide about a third of the diet. At this point, kidney function has developed such that the high protein and mineral content of CM is no longer metabolically stressful. The caloric density of CM approximates that of human milk and infant formula, but protein makes up a higher percent of the calories (table 1). Over the course of the second year of life, the United States Department of Agriculture (USDA) recommends intake of 1-2/3-2 cups of CM per day (https://ask.usda.gov/s/article/ How-much-dairy-should-I-provide-for-my- child-under-the-age-of-two-How-much-milk- should-my-child-drin). For 1-to 3-year-olds, milk is expected to contribute about 25–35% of calories (based on recommendations in https://www.myplate.gov/myplate-plan). Between ages 2 and 8 the recommendation is for 2 to 2-1/2 cups per day (https://www.cdc.gov/nutrition/InfantandToddlerNutrition/foods-and-drinks/cows-milk-and-milk-alternatives.html; Table 3-1 from https://www.dietaryguidelines.gov/sites/default/files/2021–03/Dietary_Guidelines_for_Americans-2020– 2025.pdf). The American Academy of Pediatrics recommends that toddlers should receive whole milk, and young children skim or 1% milk, although the rationale for the recommendations for skim milk has been seriously challenged.^9 10 Infants in the second year of life are at risk of poor intakes of iron, zinc, vitamin D and essential fatty acids. Nutritionally, milk complements other foods in the diet at this age^.6 The match is imperfect.¹¹ Given the high density of many nutrients in CM, it remains an important part of most Northern Hemisphere early childhood diets, particularly for providing protein, minerals and selected vitamins, including vitamins A and D, when the milk is fortified.¹² In Europe, young child milks are used in some countries as an alternative to CM, with their nutritional composition thought better to complement the diet of toddlers and young children.¹¹ The European Society for Paediatric Gastroenterology Hepatology and Nutrition has not recommended a formulation any different from follow-on formulas. However, toddler milks are not regulated like infant formulas¹³ and may not always provide the nutrient levels recommended for this age group, and often contain added sugars.¹⁴ A few of these are plant based (table 2).

Studies have shown that linear growth tends to be faster in children who receive CM as part of their diet, as frequently documented in children with CM allergy.^15–19 Some of this effect may be related to specific nutrients rich in CM including calcium, vitamin D and riboflavin^.20 Faster growth is perceived as broadly beneficial.²¹ However, there are concerns about potential deleterious effects of accelerated growth in certain circumstances, as it may be associated with obesity and metabolic syndrome^.22

There are other health concerns with feeding milk to infants and children. These include iron deficiency related to the low iron content of milk and adverse gastro-intestinal effects of milk, including blood loss in infants and anaemia with protein losing enteropathy in children given large volumes. Much of the world outside of populations native to western, southern and northern Europe becomes lactose intolerant in childhood.²⁵ This leads to symptoms in some with milk ingestion. There are rare inborn errors of metabolism for amino acids and sugars for which CM intake is contraindicated. Infants with William’s syndrome should not receive vitamin D fortified milk.

Many chronic health conditions have not been shown to be associated with CM intake. Whole milk has not been associated with obesity or consistently with diabetes. Blood low density lipoprotein cholesterol is not more likely to be abnormal in children consuming milk. The adult disease most strongly associated with milk intake is prostate cancer, and this association includes milk intake during childhood. Others have recently described and summarised the relationship of these conditions to milk intake^.9,10,26,28 It is not the purpose of this article to discuss these in detail. Acne has also been linked to CM intake, but this condition usually does not manifest until later in childhood or adolescence.

Milk provides a micronutrient dense source of calories and protein. Ingestion of CM with its high levels of branched-chain amino acids, milk insulin-like growth factor-1 (IGF-1), lactose, and micro RNA stimulates insulin secretion and hepatic IGF-1 release. This activates tissue mechanistic target of rapamycin complex 1 (mTORC1) and its associated anabolic and other (potentially adverse) effects.²⁸ mTORC1 functions as a signalling mechanism related to control of tissue growth, metabolism, inflammation and autophagy. Chronic milk ingestion may alter metabolism in the direction of insulin resistance.²⁸ In early life, this mTORC1 stimulation is central to the growth and development process. Interestingly, these mTORC1 pathophysiologic mechanisms do not appear to be activated by dairy products subjected to fermentation, which substantially changes the nutrient characteristics of the milk.

CM can bring with it substances unrelated to its nutritional composition. These include antibiotics, hormones, pesticides and other toxins.²⁹ Recent US data in this regard are reassuring relative to the low frequency of antibiotic detection³⁰ (https://www.nmdrd.com/fy-21. pdf). Of note, US organic milk rarely showed any presence of antibiotics. In some other parts of the world, anti-biotic residues in CM appear to be more common and of medical and public health concern.^29,31,32 Exposure to these potential contaminants can be reduced by use of organic milk.

Much of the commercial non-organic milk produced in the USA comes from cows treated with bovine somatotropin (BST). Administered BST does not transfer to milk, is digested by stomach acid (https://www.fda.gov/animal-veterinary/product-safety-information/bovine-somatotropin-bst) and is not bioactive.³³ However, the milk from BST treated cows has higher levels of IGF- 1,³⁰ which can be bioactive, at least in the gastrointestinal tract.³⁴ Concerns specific to BST and its associated higher IGF-1 content can be addressed with the selection of milk from non-BST treated cows and organic milk.

Dairy cows are commonly pregnant while milked, and pregnancy related sex hormones transferred to milk appear to be bioactive.³⁵ Studies have shown associations of CM intake and some later adulthood sex-hormone sensitive malignancies, possibly related to milk hormones and/or the metabolic effects of CM ingestion.^{9, 28}

PBD

There is no regulatory standard of identity for the composition of PBD. PBD can be based on legumes (soybeans, peas), seeds (hemp, sunflower), nuts (almond, pecan, macadamia), grains (rice, oats) and pseudo-grains (quinoa, buckwheat). The beverage protein is provided by one or more of these plant sources, and they contribute other nutrients and properties to the milk. The extensive processing necessary to convert these foods to milks includes soaking, grinding, blanching, separation procedures, homogenisation, thermal processing and formulation during which nutrients and other ingredients—usually including sugar and salt²—are added to achieve appearance, taste and mouth feel more closely resembling CM.^{2, 36} The process varies with the starting plant source or plant protein source and the desired final product attributes. The bioavailability of nutrients in PBD is usually less than that for CM due to lower digestibility and factors such as phytates that interfere with nutrient absorption.³⁷ These anti-nutritional factors are variably affected by food processing. Food manufacturers may make more than a single milk product from a plant source, for example, almond milk with or without added sugar. Some PBD are formulated to come close to the composition and properties of CM, and others are made without additives or fortification. PBD may be available in shelf stable, refrigerated and powder formats and in bulk or single serve packaging. Some are certified organic or use organic ingredients.

The plant sources used for PBD are lower in multiple— and variable—essential amino acids, compared with animal protein sources, reflected in part by the lower Digestible Indispensable Amino Acid Score (DIAAS), and may contain anti-nutritional factors that can interfere with nutrient absorption. However, the foods from which PBD are derived play a nutritious and healthy role in the diet (table 3). The same is less often true for the derived PBDs. As an example, almonds are rich in protein, mono- and polyunsaturated fatty acids, minerals and some B vitamins and can be part of a healthy diet. A 1 oz (28 g) serving of almonds is about 28 almonds. In contrast, a cup of many of the commercial almond milks provides the protein equivalent of four almonds (figure 1). Sugar may be added for flavour and vegetable oils for energy and essential fatty acids. Fortification is often the source of many of the nutrients claimed on the nutrition label. Fortified nutrients, notably calcium, have uncertain physical stability and bioavailability in the final matrix. Fermentation of plant ingredients, and including more than one plant source, may improve taste and nutrient content and availability.

The production of PBD generally requires sophisticated food processing machinery and know-how, making plant milks more expensive than CM.³⁸ PBD may be categorised as ultra-processed drink products using the NOVA system of food classification.³⁹ NOVA was developed in support of the United Nations Sustainable Development Goals and provides one means for categorising foods relative to their contribution to diet quality, impact on malnutrition and the sustainability of food systems.⁴⁰ Ultra-processed foods are manufactured from substances derived from foods and other organic sources and are ready-to-consume. They often contain flavouring agents, stabilisers, colouring agents and food processing aids such as emulsifiers. Ultra-processed foods now make up a high percentage of the diet of high-income (developed) countries (estimated at 67% for US youth)⁴¹ and an increasing percentage of the diet of low- and middle-income (developing) countries.⁴² Epidemiologic studies link ultra-processed foods to poorer diet quality and the rising level of chronic non-communicable diseases including obesity, dyslipidaemia and metabolic syndrome.⁴² Avoidance of minimally processed CM in favour of PBD, that may be classified as ultraprocessed, may entail its own potential diet-related morbidity or add to any attributable to ultra- processed foods. Some countries are now implementing efforts to suppress the incursion of ultra-processed foods into their food supply.

Plant based infant formulas and PBD for infants

For infants, the universally preferred and recommended milk is own mother’s milk. Current recommendations are for feeding human milk for at least 6 months and up to 2 years or longer.⁴³ Adherence to these recommendations is variable from country to country and within countries related to breast milk supply, maternal preferences and socioeconomic variables, including employment outside of the home and formula marketing practices. Most US infants receive a milk other than breast milk before the end of the first year of life^.44 When available, the recommended breast milk substitute for infants is an iron-fortified CM based commercial infant formula. Through the first year of life, breast milk and/or infant formula remain the dominant and preferred source of nutrition. Unmodified CM is not recommended in the first year of life due to its much higher protein and mineral content, the relatively low absorption of butter fat, the low content of essential and long chain polyunsaturated acids, its low iron and zinc content, and its association with faecal blood loss.

Few plant based protein sources have been utilised to manufacture infant formulas. Soy protein has an extended history of safe use. More recently, rice protein hydrolysate formulas have become available in a few European countries. Plant based infant formulas are not the first choice for infants with CM allergy.^24 45 However, soy formula is effective for managing immunoglobulin E (IgE)-mediated CM allergy. Rice protein hydrolysate formulas can be used in all forms of CM allergy. Both are suitable alternatives when parents want a vegan formula for their infant. They can also be used in galactosaemia and alactasia, as they are lactose- and galactose-free. Some expert groups advise that soy formulas not be fed to infants less than 6 months of age.²⁴ Low level concern persists regarding possible adverse effects of the phytoestrogens in soy formula on female reproductive development.⁴⁶

Marketed soy protein based and rice hydrolysate based formulas are supplemented with their limiting amino acids to bring their protein quality closer to CM. Soy formula contains added methionine, and rice hydrolysate formula contains added lysine, threonine and tryptophan. Both support satisfactory weight and length gain when provided as the sole source of milk.^47 48 Soy protein meets the protein efficiency ratio quality factor for US infant formulas under the Infant Formula Act, and soy and rice hydrolysates are approved protein sources for infant formulas under European Union (EU) regulations. Multiple adverse events have been reported, including malnutrition and micronutrient deficiencies, in infants fed other PBD not meeting nutritional standards for infant formulas.⁴⁹ Other specific adverse metabolic events have been associated with specific PBD, for example, oxalate kidney stones and metabolic alkalosis with almond milk. Concern persists regarding the arsenic content of some rice milks. Given the strong global recommendations for breastfeeding in infancy, the general availability of commercial infant formulas in high- and middle-income countries, and the mismatch of infant nutritional needs with the nutritional profile of most PBD, other than commercial soy and rice hydrolysate infant formulas, PBM have no nutritional role to play in the infant diet.

PBD for toddlers and young children

PBD are not generally designed specifically for children. The few US products that are marketed for children range from nutritionally complete to lacking in multiple nutrients present in CM. PBD have to taste good or children will have to be very hungry to accept them. However, making beverages sweet or improving taste with salt are not advantageous to health. Making alternative drinks that are both healthy and attractive to children has long been a challenge in developing nutritious alternative drinks for this age group.

PBD do not generally match CM in nutrient content, quality and bioavailability, except for iron, which CM lacks. A consortium of expert groups in North America advised against the use of PBD to replace milk in the diet of toddlers and young children (https://healthyeatin gresearch.org/wp-content/uploads/2019/09/HER-Heal thyBeverageTechnicalReport.pdf). Including PBD as a snack food or occasional beverage has little impact on the total diet. With the exception of soy, and a combined plant based protein toddler drink, using them as a replacement for CM poses variable nutritional challenges relative to making up the nutrients that would have been contributed by milk. Simply increasing the intake of plant based foods, without making thoughtful compensatory dietary adjustments, has the potential to place persons at risk for low intakes of calcium, protein, vitamin A and vitamin D.⁵⁰ Low iodine content is also of concern in PBD, as CM is a major dietary source, but fluoride content tends to be higher in PBD.

Generally, studies of vegan children find a lower prevalence of obesity, but evidence of nutrient insufficiency and slower linear growth compared with other children.^{8, 51} Not much has been written specifically about the nutritional impact of PBD and their contribution to nutritional status and growth of children. Given the heterogeneity of PBD, each would have to be studied in its own right to generate actionable nutritional information. In the EU and Canada, PBD are labelled as beverages rather than as milk. In the USA, it appears that manufacturers can continue to use the term ‘milk’ to describe PBD, but the label may need to clarify aspects of their nutrient content relative to CM (https://www.federalregister.gov/documents/2023/02/23/2023–03513/labeling-of-plant- based-milk-alternatives-and-voluntary-nutrient-state- ments-draft-guidance-for). Tables 1 and 4 demonstrate the mismatch in the composition of CM and PBD. There is less complete information about the micronutrient content of PBD.^1,52 Energy and protein digestibility content and amino acid scores are variable and generally less than for CM.¹ Soy milks generally come closest. As of 2015, there were an estimated 150 PBD available in Europe.⁵³ Given PBD variability and the often limited nutritional information at the product-specific level, statements about the nutritional role of PBD as a group have the potential to be misleading.

Vegan consumerism and preferences for PBD