|Food preference; Children; Maternal diet; Prenatal period; Flavor; Exposure
|Food preference in children is molded by the interplay of genetic and environmental factors , and is the most consistent feature predicting their food selection [2-4]. Food preference can be innate or learned. For instance, the usual preference by children for high-fat and sweet foods reported in many countries and the near universal dislike for vegetables [5-7], suggests the existence of innate predispositions towards tastes . This is corroborated by the fact that a preference for sweet taste and an aversion to sour or bitter taste is universally present in newborns as measured by the observation of facial grimaces [8,9]. In the past, the innate tendency to reject sour and bitter foods may have served to protect individuals from toxins; a tendency that now contributes to the widespread aversion for vegetables in childhood . On the other hand, children’s food preferences can be learned through repeated exposures to foods [10-12]. Neophobia in children (tendency to reject new or unfamiliar foods) was reported to be modified through such repeated exposures, as a minimum of 8-10 exposures to new foods increased preference for these foods [10-13].
|The first few years of life are acknowledged as an extremely important period for the development of food acceptance patterns [14,15]. Prenatal and postnatal exposures to flavors through amniotic fluid and breast milk have been suggested as a possible influence on food acceptance [16,17], as the like for flavor is the major determinant of food preference, and thus food consumption in children [18,19]. Flavor transmission through the amniotic fluid during the fetal intrauterine life is therefore a strong evidence for the influence of prenatal maternal diet on the child’s food preference early in life.
|The present review seeks to appraise the current evidence in medical literature linking prenatal experience with flavors emanating from maternal diets to later food preference and food-acceptance patterns in children, especially toddlers. It is hoped that the review may expose the need for further research focused on increasing children’s healthy feeding patterns.
|Literature Search Strategy
|Google, PubMed and Medline databases were searched for articles on children’s eating behavior, picky eating behaviors of preschool children, as well as acquisition of flavor and food preference in children. Relevant search terms included picky eating, food preference, maternal diet, prenatal period, and amniotic flavor exposure. Articles and crossreferences were included in the review if they contained information on picky eating behaviors in preschool children, determinants of children’s eating behavior and prenatal flavor transmission.
|What is ‘Food Preference’ in Children?
|Food likes and dislikes play an important role in food choices, particularly in children . Food preference simply means that “children eat what they like” . Strong food preferences are a distinctive component of picky eating behaviors which also include rejection of certain types of food, acceptance of only certain foods, food neophobia and limited intake of some food groups [21,22]. About 25% to 35% of toddlers and preschool children are reported by their parents as picky eaters . In a US nationally representative study in 2002, the prevalence of picky eating among 19 to 24 month-old children was 50% .
|The genetic determinants of food preferences in children are well documented, as there is evidence for a strong genetic influence on appetite traits in children [25-28]. Specifically, twin studies have reported a co-efficient of heritability for food types, with indications of genetic influence on food preferences being strong for protein foods (co-efficient of heritability: 0.78) and moderate for fruit (co-efficient of heritability: 0.51), vegetables (co-efficient of heritability: 0.37) and dessert foods (co-efficient of heritability: 0.20) . Furthermore, food preferences are the outcome of an interaction between genetic and environmental factors which result in veritable individual differences in the extent to which children generally display fussiness about food as well as in their likes and dislikes for specific foods . Extensive research has been conducted to establish the existence of a strong nexus between fetal exposures in the intra-uterine life and the child’s feeding patterns in the extra-uterine life. It underscores the role of the interaction between the child and his environment in shaping food preferences.
|Interaction with the Intra-Uterine Environment
|The development of the child’s preferences for foods and drinks is mediated by a variety of exposure-related mechanisms such as flavor transmission through the amniotic fluid and breastfeeding . Flavor is the most prominent feature of foods and beverages for humans, and its perception is the outcome of the interaction and integration of two types of chemical information namely gustatory stimuli (tastes) and olfactory stimuli (odorants) [31,32]. Some researchers have constantly demonstrated that the gustatory and olfactory functions are already present in newborns [33,34], but continue to develop in the postnatal period . Indeed, as early as the 15th week of pregnancy intact taste buds have developed and contact with amniotic fluid ensures at least some experience of volatile compounds originating from maternal diet . Obviously, flavor transmission through the amniotic fluid during the prenatal period is the first type of exposure in utero which influences later flavor preferences. Throughout gestation, changes in the mother’s diet are actually reflected in the chemical composition of amniotic fluid . Chemical compounds present in the diet come in contact with fetal chemical receptors as amniotic fluid circulates through the oral-nasal passages. However, it is not clear at what point flavor is experienced but there is evidence that premature infants do respond to taste . Apart from taste, olfactory preferences may be learned in the intrauterine life. Several evidence-based studies have confirmed this observation [33,39-43]. For instance, Faas et al.  reported significantly higher rates of motor responsiveness to ethanol odor in 1 to 2 day-old newborns with maternal history of frequent alcohol consumption during pregnancy compared to their counterparts whose mothers did not indulge in such consumption while pregnant. Second, Varendi et al.  have demonstrated that newborns cried significantly less when exposed to the odor of their mother’s amniotic fluid in comparison to newborns exposed to their mothers’ breasts or those with no odor exposure. Similarly, other workers [40,41] reported preferential response of newborn infants to the odor of their own amniotic fluid within the first 2-4 postnatal days rather than the odor of formula milk, odorless distilled water, or unfamiliar amniotic fluid. Similarly, the findings of Schaal and colleagues , as well as Mizumo and Ueda  support the prenatal acquisition of olfactory preferences.
|The Link with Later Food Preference and Acceptance
|Several investigators [44-47] have demonstrated a relationship between these fetal interactions with the intrauterine environment and the establishment of flavor and food preferences, as well as foodacceptance patterns which are sustained even after weaning till later childhood. For instance, Mennella et al.  reported less negative facial expressions among infants fed on a carrot-flavored cereal whose mothers repeatedly drank carrot juice during pregnancy than among those who had no such exposure to carrot juice in utero. In another interview-based study, the weaning diets accepted by a group of Mexican infants correlated with the types of foods eaten by their mothers during the antenatal period . Furthermore, Crystal and Bernstein  documented a greater preference for snack foods with the highest level of salt among young adults whose mothers had a history of emesis gravidarum in comparison to those whose mothers had no such history. The same authors were able to replicate these findings in a subsequent study conducted among 4 month-old infants with maternal history of vomiting in pregnancy. These infants showed less negative facial expressions on exposure to a liquid solution with high levels of salt compared to infants whose mothers reported no emesis gravidarum .
|Interaction with the Extra-Uterine Environment
|After birth, postnatal exposures to flavors and foods continue to stimulate acceptance of and preference for those prenatal chemical stimuli . Flavors from maternal diet transmitted to the breast milk may be ‘sensed’ by breastfeeding infants; thus providing “chemical continuity” from the intra-uterine environment . Such early exposure may lead to the development of preferential responsiveness to food-related tastes and odors which remain noticeable throughout weaning . Several reports by Mennella , and Mennella and Beauchamp [50-53] have confirmed that this responsiveness to maternal breast milk varies as a function of the presence or absence of specific flavors linked to the maternal diet, such as vanilla, garlic and alcohol. These researchers have also demonstrated specific flavor preferences arising from exposure to formula-milk-based feeding . For instance, after a brief exposure to vanilla-flavored formula, three- month old infants sucked significantly more when fed the vanilla-flavored formula rather than a control formula. In addition, during a second and longer feeding session, they fed longer when the formula was vanilla-flavored . Indeed, it has been shown that foods offered during the first two years of life predict food preferences later in childhood and adolescence [54,55].
|The Link with Food Acceptance at Weaning
|Again, studies have established a clear relationship between food acceptance at weaning and flavor transmission through breastfeeding [44,56], as well as through formula- milk feeding during infancy [34,57,58]. First, Mennella and Beauchamp  observed that infants who were fed with cereal prepared with maternal milk rather than water exhibited higher rates of consumption of a carrot-flavored cereal at weaning. This pattern of food acceptance was attributed by the investigators to previous exposure to the carrot flavor (through the mother’s diet) during the lactation period. A subsequent study  also showed that infants whose mothers drank carrot juice during the first two months of lactation preferred cereal prepared with carrot juice rather than plain cereal at the time of weaning, and consumed more of the flavored cereal than did infants with no prior carrot exposure . Moreove, the effects of gustatory imprinting following introduction to artificial milk have also been noted at weaning . In one study, the authors demonstrated that infants fed on bitter, sour and savory hydrolyzed formulas during the first three months of life ate more cereals with similar tastes and odors than did infants fed on bovine milk-based formulas or breast milk when they were tested after weaning. Likewise, other workers  corroborated this observation when they found that infants who were fed a specific hydrolyzed formula (Nutramigen) for a 7-month period more readily accepted Alimentum (another hydrolyzed formula similar to Nutramigen) than did control infants who were exposed to milk-based formula (Enfamil) for the same period .
|It is therefore safe to conclude that the child’s gustatory and olfactory exposures to flavors during the three successive stages of early development result in modifications in the expression of flavor, food and drink preferences in later stages of life. The three developmental stages are the prenatal period (fetal experience), the postnatal milkbased feeding period and early childhood (at weaning) . Both the intra-uterine (prenatal period) and extra-uterine (postnatal period) environments are therefore critical in shaping the child’s feeding behavior. These early experiences with flavors and foods trigger a gustatory imprinting which is manifested in preferences for those same stimuli in later stages of life. The assumption that the toddler’s food preferences are influenced by the mother’s prenatal dietary experience is thus evidence-based. Nevertheless, future research is needed to elucidate some grey areas. For instance, the specific age or ages during which the gustatory imprinting may occur remain largely unknown and require further investigation. Since prenatal and postnatal exposure to different flavors determine the extent to which innate dispositions to tastes are expressed, it is possible to formulate effective strategies aimed at increasing children’s healthy feeding patterns.
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