Poor nutrition is a leading lifestyle factor related to the development of several noncommunicable diseases. One strategy for eliminating health disparities and promoting long-term health is to get children to eat and like healthful foods (eg, fruits and vegetables) from an early age (1–4). Health organizations worldwide recommend 5 to 13 servings of fruits and vegetables per day, depending on one's caloric requirement (5,6). Despite such recommendations, adults are not eating enough fruits and vegetables (6) and neither are children (7,8). The 2004 Feeding Infant and Toddlers Study, designed to update knowledge on the feeding patterns of American children, alarmingly revealed that toddlers ate more fruits than vegetables and 1 in 4 did not even consume 1 vegetable on a given day (7,8). Instead, they were more likely to be eating fatty foods and sweet-tasting snacks and beverages and less likely to be eating vegetables. None of the top 5 vegetables consumed by toddlers was a dark green vegetable, those that are usually most bitter.
The best predictor of how much fruits and vegetables children eat is whether they like the taste of these foods (9). We would argue that what is lacking is a critical understanding of the factors that determine food and flavor preferences. In what follows, we first provide a basic overview of taste and smell, the differences between them and how they interact and integrate to help produce a single overall percept that we call flavor. We then review findings gleaned from our program of research that aims to understand the origins of human taste, flavor and food preferences, and habits and provide a scientific basis for recommendations to enhance nutritional outcomes of infants and children. Finally, we briefly suggest practical implications flowing from the basic research reviewed.
FLAVOR PERCEPTION: TASTE, SMELL, AND CHEMICAL IRRITATION COMBINED
The most salient feature of the foods and beverages we consume is flavor. We define flavor as the perceptual combination of 3 anatomically distinct chemical senses: taste, smell, and chemosensory irritation. Taste stimuli, which must be dissolved in saliva, are detected by taste receptor cells located in taste tissue in the tongue, palate, and perhaps even in the gut (10). The smell component of flavor is composed of volatile compounds detected by receptors in the upper regions of the nose. There are thought to be hundreds or thousands of different odors and it is these in flavor that make it possible to discriminate, for example, strawberry from lime. The third chemical sense, chemosensory irritation, is detected by receptors in the skin throughout the head but particularly, as regards food, in the mouth and nose. Examples include the burn of hot peppers and the cooling effect of menthol. A brief review of the molecular mechanisms underlying these 3 chemical senses follows (10).
Taste receptors are composed of modified epithelial cells on papillae of the tongue and throughout the oral cavity. Peripheral innervation of these cells is via branches of 3 different cranial nerves: the facial (VII), glossopharyngeal (IX), and vagus (X). Taste is generally thought to be composed of 5 primary qualities: sweet, salty, bitter, sour, and umami or savory. Although there are regional differences in the oral cavity in the relative sensitivity to these different taste qualities, virtually all can be perceived in all areas of the tongue. Several other different qualities have also been proposed (eg, fatty, calcium taste) but these remain controversial.
There has been considerable progress in identifying the initial molecular events in taste reception. For salty and sour tastes, it is widely believed that ion channels serve as receptors. Here H+ (sour) and Na+ (salty) ions are thought to flow through the channels into the cell thereby activating specific taste cells. However, for both of these taste qualities, the molecular identity of the receptors and their exact mechanism are unknown. For sweet, umami (savory taste exemplified by the taste of the free amino acid glutamate—most commonly encountered as monosodium glutamate [MSG]) and bitter, G-protein coupled receptors (GPCRs) appear to play the most prominent roles. These GPCRs bind taste molecules thereby activating the taste cell. For sweet and umami, a family of 3 GPCRs named T1R1, T1R2, and T1R3 apparently act in pairs (T1R1 + T1R3 for umami and T1R2 + T1R3 for sweet) to detect molecules imparting these taste qualities. For both sweet and umami, additional receptors may exist.
A substantially larger family of GPCRs, the T2R receptors (n ∼ 26), constitutes the bitter receptors. Each of the T2R receptors likely recognizes one compound or a few structurally related compounds. Presumably there are many bitter receptors because there are so many structurally different compounds that are potentially harmful if consumed by an animal.
Many parts of the molecular machinery involved in taste reception, including the T1R and T2R families of receptors, are expressed in the gut (11,12). The functional significance of this is still not clear although it is suspected that this molecular machinery may be involved in (unconscious) nutrient recognition and food and nutrient utilization. Indeed, it may be profitable to envision the taste system as extending along the digestive tract and having multiple functions for food acceptance, recognition, and utilization.
Smell or olfaction occurs when chemicals stimulate olfactory receptors on a relatively small patch of tissue located high in the nasal cavity. The human olfactory epithelium lines the roof of the nasal cavity, part of the nasal septum and the superior turbinates and may extend to the middle turbinates. The organization of the olfactory system reflects the need to recognize a wide range of odors and to discriminate one odor from another. In fact, the olfactory receptors (7-transmembrane GPCRs) are encoded by the largest mammalian gene superfamily consisting of more than 1000 genes (13). For humans approximately two-thirds of these receptors are no longer functional, possibly a consequence of the reduced importance of olfactory function for humans as compared to rodents or dogs, for example. Nevertheless, it is clear that olfaction is important in flavor perception, and it has been argued that with a greater amount of the brain devoted to olfaction, humans may in many ways equal other animals in their olfactory abilities (14).
Olfactory receptors located on olfactory cilia are thought to bind odorants that have been dissolved in mucus in the olfactory region of the nose. Each receptor cell apparently expresses a single receptor and each receptor is able to recognize a small number of odorants. Thus, this system works in a combinatorial manner although the exact mechanism underlying the perception of a complex odor (eg, the odor of coffee, made up of perhaps hundreds of different odor compounds) remains a puzzle (15).
Sensations resulting from chemicals stimulating receptors and free nerve endings of the trigeminal and vagus nerves lead to oral perceptions such as pain, heat, coolness, tingling, tickle, and itch. Recent research has shown that a family of transient receptor potential (TRP) channels is involved in detecting many of these chemicals (16). These channels also respond to actual heat and coolness. Apparently, plants have evolved chemicals that affect these channels as a protective device. For example, chili peppers contain capsaicin that burns (ie, stimulates the same receptors as are stimulated by noxious heat) and, hence, are avoided by potential predators. Other irritants include menthol, which interacts with channels sensitive to cooling, mustard oil, black pepper, and even CO2 (carbonation).
Because there is virtually no research on the ontogeny of trigeminally mediated, oral, or nasal responses to irritating chemicals, we will not consider this sense in what follows. However, developmental studies of this sense are certainly indicated as “irritating” sensations are critical in food and flavor acceptability.
ONTOGENY OF FLAVOR LEARNING
The extent to which flavors are liked or disliked is determined by innate or inborn factors, by environmental (eg, nutritional) perturbations, by learning, and by the interactions among these. Liking for taste stimuli is generally strongly influenced by inborn (innate) factors (17). For example, sweet foods and beverages are highly preferred by plant-eating animals, presumably because sweetness reflects the presence of caloric sugars. This preference for sweets is innately determined. Innate preferences for sweet-tasting compounds changes developmentally (infants and children have higher preferences than adults) and they can be modified by experience (18). Bitter tasting substances are innately disliked presumably because most bitter compounds are toxic: plants evolved systems to protect themselves from being eaten and plant-eating organisms evolved sensory systems to avoid being poisoned (19). With experience people may come to like certain foods that are bitter, particularly some vegetables and foods and beverages containing pharmacologically active compounds such as caffeine or ethanol.
For many species, particularly those that are primarily herbivorous, a sensitivity to and preference for salty tasting substances (almost the only one being NaCl) also appears to have an innate component. Human infants as young as 4 months of age prefer moderate concentrations of salt water to plain water and by 2 years of age, their preferences for salty foods are even greater than they are for adults (18,20). The degree to which this innate tendency to appreciate the taste of salt is modified by subsequent experience is a research area ripe for further investigation, particularly because high salt intake has been implicated in the development and/or maintenance of elevated blood pressure.
Along with proposed innate factors, prenatal developmental events appear to influence infant and child preferences for salty tastes. For example, several studies suggest that severe maternal emesis can have an enduring influence on response of offspring to salty taste (21–23). Similarly, we have recently shown (24) that several behavioral measures related to salty taste preference were inversely related to birth weight over the first 4 years of life. Because it is generally accepted that excess salt intake can lead to or exacerbate hypertension, we speculate that one mechanism predisposing babies to high salt intake is the heightened preferences that are caused by in utero events common to lower birth weight.
In contrast to flavor compounds detected by the sense of taste, preferences for flavor compounds detected by the sense of smell are generally more highly influenced with learning early in life, even in utero, being particularly salient (17,25). The sensory environment in which the fetus lives, the amniotic sac, changes as a function of the food choices of the mother as dietary flavors are transmitted and flavor amniotic fluid (26). Experiences with such flavors lead to heightened preferences for these flavors shortly at birth (27,28) and at weaning (29). Specifically, prenatal experiences with food flavors, which are transmitted from the mother's diet to amniotic fluid, lead to greater acceptance and enjoyment of these foods during weaning. In an experimental study, infants whose mothers were randomly assigned to drink carrot juice during the last trimester of pregnancy enjoyed carrot-flavored cereals more than infants whose mothers did not drink carrot juice or eat carrots (29).
Postnatal Effects: Breastfeeding
Flavor learning continues after birth as a consequence of exposure to the first nutrients in human milk or its substitute, generally a commercial formula. As human milk is composed of flavors that directly reflect the foods, spices, and beverages ingested or inhaled (eg, tobacco) by the mother (30–33), breast-fed infants are exposed to flavor compounds that the mother has chosen. In common with other mammals (34–36) exposure to a flavor (eg, carrots, garlic, fruits) in mothers' milk, as is the case with amniotic fluid, influences infants' liking and acceptance of that flavor in a food base (29,37,38).
Because it is highly likely that amniotic fluid and breast milk will have commonalities in flavor profiles when the mother eats the same types of foods during pregnancy and lactation, breast milk may serve as a “bridge” between the experiences with flavors in utero to those in solid foods. Moreover, the sweetness and textural properties of human milk, such as viscosity and mouth coating, vary from mother to mother (39), thus suggesting that breastfeeding (unlike formula feeding; see below) provides the infant with the potential for a rich source of varying oral sensory experiences. The types and intensity of flavors experienced in breast milk may be unique for each infant and are the flavors that are associated with nutritious foods, or at the very least, foods their mother had access to and chose to consume.
In a recent study, we found that breast-fed infants were more accepting of peaches than formula-fed infants, as determined by intake, rate of consumption, and facial expressions. This enhanced acceptance of fruit could be due to more exposure to fruit flavors because their mothers ate more fruits during lactation (38). If mothers eat fruits and vegetables, breast-fed infants will learn about these dietary choices by experiencing the flavors in mothers' milk, thus highlighting the importance of a varied diet for both pregnant and lactating women (40). These varied sensory experiences with food flavors may help explain why breast-fed infants are less picky (41) and are more willing to try new foods (42), which, in turn, contributes to greater fruit and vegetable consumption in childhood (43–45).
Postnatal Effects: Formula Feeding
During the past decade, we have been studying the impact of formula feeding on flavor learning as it allows us to control sensory experiences much more precisely than we can for breastfeeding mothers. Formulas made from unaltered bovine milk differ enormously in flavor from those made with hydrolyzed casein (HC), which have been the focus of our recent research. These latter formulas are the feeding regimen of choice for formula-fed infants who cannot tolerate cow's milk protein and other intact proteins. They are also extremely unpleasant to those unfamiliar with them, having a bitter and sour taste, and a nauseating smell and aftertaste (46). We have shown that naive (to HC formulas) infants less than 3 to 4 months of age readily accept HC formulas and appear not to dislike them as determined both by their willingness to consume them and by the absence of characteristic facial responses of rejection when feeding (47,48). In marked contrast, naive infants more than 5–6 months of age vigorously reject them and demonstrate, through negative facial expression, a strong dislike (47,48). In a subsequent experimental study (49) we found that early (before 5–6 months of age) experience with HC formula eliminated subsequent rejection. Thus, there appears to be a sensitive period in the first several months of life during which even distasteful flavors (to those not familiar with them) can be rendered acceptable and perhaps even liked. Moreover, the learning appears to be quite selective. In one study we exploited the fact that although all brands of protein hydrolysate formula share common flavor attributes and are judged unpleasant by adults, they differ in their flavor profiles (46). We found that infants fed on one or another brand of hydrolysate formula significantly preferred that familiar formula to the alternative unfamiliar formula. In other words, the acceptance pattern that develops is specific to the flavor profile experienced.
In a more recent study (50) we found that experiences with flavors in formula impacted on preferences for the taste qualities in food, especially among infants tested before being introduced to table foods. Infants feeding protein hydrolysate formulas ate more of infant cereals that tasted savory, sour, and bitter and ate them at a faster rate than those fed milk-based formulas. That they liked the savory and bitter tastes was suggested by the fewer facial expressions of distaste displayed during feeding. When compared with milk-based formulas, and presumably breast milk (39,51), hydrolysate formulas have more pronounced savory, bitter, and sour tastes and stronger odors (46). Thus, infants who regularly feed formulas based on casein hydrolysate have more experiences with these taste and flavor qualities. The current results demonstrate that they also display their preferences for these flavors in a food matrix (eg, cereal) with which they are familiar.
The effects of these experiences with formula flavors appear to be long-lived. Four- to 5-year-old children who were fed hydrolysates during infancy exhibited more positive responses to foods and beverages containing the sensory attributes associated with them (eg, sour taste, aroma, chicken, and broccoli) several years after their last exposure to the formula when compared with same-aged children without such experience (52,53). Consistent with these findings are results of a study on children and adults with phenylketonuria (PKU). The dietary regimen to treat PKU consists of a hydrolysate formula that is specifically treated with charcoal to remove most of the phenylalanine. When given a choice, children and adolescents with PKU preferred their bad-tasting formula to that of the new formulation that was more palatable to naive children and adults (54). In other words, the characteristic flavor of the formula experienced in early life is “imprinted” and remains as a preference for a considerable time.
The sensory world of infants is ever changing and dynamic and most evident as they begin the transition from an all-milk diet to one containing solid foods. Early flavor experiences in amniotic fluid, milk, and solid foods affect infants' taste acceptance patterns and infants communicate their acceptance by both intake and facial displays (Fig. 1). Further examination of how genetic differences in the sensitivity to the basic taste substances (55) interact with early experiences in establishing food likes and dislikes is an important area for future research. An appreciation of the role of early experiences and complexity of early feeding, and a greater understanding of the different means by which infants communicate their liking of tastes and flavors, will aid development of evidence-based strategies to facilitate healthy eating by children.
Physicians and caregivers should encourage pregnant and nursing women to consume healthful diets with a variety of flavors because their infants develop long-lasting flavor preferences very early in life. Infants of women who do not breastfeed should be exposed to a variety of flavors, particularly those associated with fruits and vegetables, first while the mother is pregnant and then beginning at an early age. For infants feeding hydrolysate formulas, the impact of their early taste experiences with formula may be magnified when they are offered table foods that taste savory, sour, or bitter. Early feeding practices set the stage for future healthy eating which plays a role in protecting against many common diseases.
1. Lederman SA, Akabas SR, Moore BJ, et al
. Summary of the presentations at the Conference on Preventing Childhood Obesity, December 8 2003. Pediatrics 2004; 114:1146–1173.
2. Gidding SS, Dennison BA, Birch LL, et al
. Dietary recommendations for children and adolescents: a guide for practitioners: consensus statement from the American Heart Association. Circulation 2005; 112:2061–2075.
3. Krebs NF, Jacobson MS. Prevention of pediatric overweight and obesity. Pediatrics 2003; 112:424–430.
4. Bazzano LA, He J, Ogden LG, et al
. Fruit and vegetable intake and risk of cardiovascular disease in US adults: the first National Health and Nutrition Examination Survey Epidemiologic Follow-up Study. Am J Clin Nutr 2002; 76:93–99.
5. World Health Organization. Diet, nutrition and the prevention of chronic disease. Report of a joint WHO/FAO expert consultation. WHO Technical Report Series No. 916 ed. Geneva, Switzerland: World Health Organization; 2003.
6. US Department of Health and Human Services, US Department of Agriculture. Dietary Guidelines for Americans 2005. 6th ed. Washington, DC: US Government Printing Office; 2005.
7. Fox MK, Pac S, Devaney B, et al
. Feeding infants and toddler study: what foods are infants and toddlers eating. J Am Diet Assoc 2004; 104:S22–S30.
8. Mennella JA, Ziegler P, Briefel R, et al
. Feeding Infants and Toddlers Study: the types of foods fed to Hispanic infants and toddlers. J Am Diet Assoc 2006; 106(1 Suppl 1):S96–S106.
9. Resnicow K, Davis-Hearn M, Smith M, et al
. Social-cognitive predictors of fruit and vegetable intake in children. Health Psychol 1997; 16:272–276.
10. Bachmanov AA, Beauchamp GK. Taste receptor genes. Annu Rev Nutr 2007; 27:389–414.
11. Margolskee RF, Dyer J, Kokrashvili Z, et al
. T1R3 and gustducin in gut sense sugars to regulate expression of Na+-glucose cotransporter 1. Proc Natl Acad Sci U S A 2007; 104:15075–15080.
12. Sclafani A. Sweet taste signaling in the gut. Proc Natl Acad Sci U S A 2007; 104:14887–14888.
13. Buck L, Axel R. A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 1991; 65:175–187.
14. Shepherd GM. Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann N Y Acad Sci 2007; 1121:87–101.
15. Touhara K. Progress in research and clinical practice concerning olfactory sensation—importance of the olfactory mucus in the olfactory sense and signal transduction to the brain. Nippon Jibiinkoka Gakkai Kaiho 2008; 111:475–480.
16. Bautista DM, Jordt SE, Nikai T, et al
. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 2006; 124:1269–1282.
17. Bartoshuk LM, Beauchamp GK. Chemical senses. Annu Rev Psychol 1994; 45:419–449.
18. Cowart BJ, Beauchamp GK, Mennella JA. Development of taste and smell in the neonate. In: Polin RA, Fox WW, Abman SH (editors). Fetal, Neonatal Physiology
. Vol 2, 3rd ed. Philadelphia, PA: Saunders, 2004. pp. 1819–1827.
19. Glendinning JI. Is the bitter rejection response always adaptive? Physiol Behav 1994; 56:1217–1227.
20. Cowart BJ, Beauchamp GK. The importance of sensory context in young children's acceptance of salty tastes. Child Dev 1986; 57:1034–1039.
21. Crystal SR, Bernstein IL. Morning sickness: impact on offspring salt preference. Appetite 1995; 25:231–240.
22. Crystal SR, Bernstein IL. Infant salt preference and mother's morning sickness. Appetite 1998; 30:297–307.
23. Leshem M. The ontogeny of salt hunger in the rat. Neurosci Biobehav Rev 1999; 23:649–659.
24. Stein LJ, Cowart BJ, Beauchamp GK. Salty taste acceptance by infants and young children is related to birth weight: longitudinal analysis of infants within the normal birth weight range. Eur J Clin Nutr 2006; 60:272–279.
25. Mennella JA. The chemical senses and the development of flavor preferences in humans. In: Hartmann PE, Hale T, editors. Textbook on Human Lactation. Amarillo, TX: Hale Publishing; 2007. pp. 403–414.
26. Mennella JA, Johnson A, Beauchamp GK. Garlic ingestion by pregnant women alters the odor of amniotic fluid. Chem Senses 1995; 20:207–209.
27. Schaal B, Marlier L, Soussignan R. Human foetuses learn odours from their pregnant mother's diet. Chem Senses 2000; 25:729–737.
28. Hepper PG. Adaptive fetal learning: prenatal exposure to garlic affects postnatal preferences. Anim Behav 1988; 36:935–936.
29. Mennella JA, Jagnow CP, Beauchamp GK. Prenatal and postnatal flavor learning by human infants. Pediatrics 2001; 107:E88.
30. Mennella JA, Beauchamp GK. Maternal diet alters the sensory qualities of human milk and the nursling's behavior. Pediatrics 1991; 88:737–744.
31. Mennella JA, Beauchamp GK. Smoking and the flavor of breast milk. N Engl J Med 1998; 339:1559–1560.
32. Mennella JA, Beauchamp GK. The transfer of alcohol to human milk. Effects on flavor and the infant's behavior. N Engl J Med 1991; 325:981–985.
33. Mennella JA, Beauchamp GK. The human infants' responses to vanilla flavors in human milk and formula. Infant Behav Dev 1996; 19:13–19.
34. Bilko A, Altbacker V, Hudson R. Transmission of food preference in the rabbit: the means of information transfer. Physiol Behav 1994; 56:907–912.
35. Galef BG Jr, Sherry DF. Mother's milk: a medium for transmission of cues reflecting the flavor of mother's diet. J Comp Physiol Psychol 1973; 83:374–378.
36. Nolte DL, Provenza FD. Food preferences in lambs after exposure to flavors in milk. Appl Anim Behav Sci 1991; 32:381–389.
37. Mennella JA, Beauchamp GK. The effects of repeated exposure to garlic-flavored milk on the nursling's behavior. Pediatr Res 1993; 34:805–808.
38. Forestell CA, Mennella JA. Early determinants of fruit and vegetable acceptance. Pediatrics 2007; 120:1247–1254.
39. Barker E. Sensory Evaluation of Human Milk [dissertation]. Manitoba, Canada: University of Manitoba; 1980.
40. Forestell CA, Mennella JA. Food, folklore and flavor preference development. In: Lammi-Keefe C, Couch SC, Philipson E, eds. Handbook of Nutrition and Pregnancy
. Totowa, NJ: Humana Press; 2008, pp. 55–64.
41. Galloway AT, Lee Y, Birch LL. Predictors and consequences of food neophobia and pickiness in young girls. J Am Diet Assoc 2003; 103:692–698.
42. Sullivan SA, Birch LL. Infant dietary experience and acceptance of solid foods. Pediatrics 1994; 93:271–277.
43. Skinner JD, Carruth BR, Wendy B, et al
. Children's food preferences: a longitudinal analysis. J Am Diet Assoc 2002; 102:1638–1646.
44. Nicklaus S, Boggio V, Chabanet C, et al
. A prospective study of food variety seeking in childhood, adolescence and early adult life. Appetite 2005; 44:289–297.
45. Cooke LJ, Wardle J, Gibson EL, et al
. Demographic, familial and trait predictors of fruit and vegetable consumption by pre-school children. Public Health Nutr 2004; 7:295–302.
46. Mennella JA, Beauchamp GK. Understanding the origin of flavor preferences. Chem Senses 2005; 30(Suppl 1):i242–i243.
47. Mennella JA, Beauchamp GK. Developmental changes in the acceptance of protein hydrolysate formula. J Dev Behav Pediatr 1996; 17:386–391.
48. Mennella JA, Beauchamp GK. Development and bad taste. Pediatr Allergy Asthma Immunol 1998; 12:161–163.
49. Mennella JA, Griffin CE, Beauchamp GK. Flavor programming during infancy. Pediatrics 2004; 113:840–845.
50. Mennella JA, Forestell CA, Morgan L, et al. Early milk feeding influences taste acceptance and liking during infancy. Am J Clin Nutr
51. McDaniel MR. Off-flavors in human milk. In: The Analysis and Control of Less Desirable Flavors in Foods and Beverages
. New York: Academic Press; 1980. pp. 267–291.
52. Liem DG, Mennella JA. Sweet and sour preferences during childhood: role of early experiences. Dev Psychobiol 2002; 41:388–395.
53. Mennella JA, Beauchamp GK. Flavor experiences during formula feeding are related to preferences during childhood. Early Hum Dev 2002; 68:71–82.
54. Owada M, Aoki K, Kitagawa T. Taste preferences and feeding behaviour in children with phenylketonuria on a semisynthetic diet. Eur J Pediatr 2000; 159:846–850.
55. Mennella JA, Pepino MY, Reed DR. Genetic and environmental determinants of bitter perception and sweet preferences. Pediatrics 2005; 115:e216–e222.