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Sensory Aspects of Bitter and Sweet Tastes During Early Childhood

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Taste and Flavor are Not Synonymous

Flavor is an integrated perception that arises from stimulation of 3 distinct sensory systems, taste, touch, and smell, that are found in the mouth, throat, and nose.1,2 Because chemosensation is the primary means by which children assess food acceptability,3 the importance of flavor for ingestive behavior is discussed here. However, terminology in this area can be very confusing and potentially misleading, because the jargon used by researchers and specialists is poorly aligned with the everyday language used by practitioners and the public. Strictly speaking, taste (gustation) only includes a very limited set of perceptual qualities. These include sweet, sour, salty, savory/umami, and bitter; however, the classic 5 may not be sufficient to represent the entire set of taste qualities.4,5 Other nontaste sensations like the drying/astringency of red wine or tea, the carbonation of beer, or the burn of chilies, may also arise in the mouth and nose. Nonetheless, these are not considered “tastes” because they occur via the touch system. Accordingly, the term chemesthesis was coined a quarter century ago to describe chemically initiated touch sensations.6 Finally, smell can be thought of as 2 separate senses behaviorally, where orthonasal smelling via the nostrils is used to assess external environmental cues, and retronasal smelling via the pharynx is part of the eating experience.7 Specifically, when we eat, odorants that activate olfactory receptors located in the nose are localized to the mouth in terms of their perception (ie, olfactory capture). That is, when we chew and swallow a cinnamon roll, we experience the cinnamon as occurring in our mouth regardless of the fact that the chemosensory transduction event responsible for the perception of cinnamon is actually occurring high up in the nasal cavity. Despite these independent inputs, taste, touch, and smell are integrated by the brain to form the unitary perceptions we experience as food flavor.

1. Lawless HT. Flavor. In: Friedman MP, Carterette EC, eds. Cognitive Ecology. San Diego, CA: Academic Press, Inc; 1996:325–380.

2. Duffy VB, Hayes JE. Smell, taste, and oral somatosensation: age-related changes and nutritional implications. In: Chernoff R, ed. Geriatric Nutrition: The Health Professional’s Handbook. 4th ed. Burlington, MA: Jones & Bartlett Learning, LLC; 2014: 115–164.

3. Mennella JA, Pepino MY, Reed DR. Genetic and environmental determinants of bitter perception and sweet preferences. Pediatrics. 2005;115(2):e216–e222.

4. Delwiche J. Are there “basic” tastes? Trends Food Sci Tech. 1996;7(12):411–415.

5. Running CA, Craig BA, Mattes RD. Oleogustus: the unique taste of fat. Chem Senses. 2015;40(7):507–516.

6. McDonald ST, Bolliet DA, Hayes JE, eds. Chemesthesis: Chemical Touch in Food and Eating. West Sussex, UK: John Wiley & Sons, Ltd; 2016.

7. Gibson JJ. The Senses Considered as Perceptual Systems. Boston, MA: Houghton Mifflin; 1966.


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INTRODUCTION

To support appropriate early childhood feeding, American Academy of Pediatrics guidelines encourage the use of feeding strategies to ensure food acceptance and the development of healthy eating behaviors and patterns.1 Although it is widely appreciated that taste preferences influence food choices and ingestive behavior,2,3 many healthcare providers and clinicians lack training in flavor science and chemosensory perception, which may lead to mischaracterization, misdiagnosis, and poor treatment when faced with a patient who complains “food no longer tastes good.”4,5 Such a complaint may reflect a true disruption of taste or smell function, an affective shift where sensory function remains normal but the hedonic response to a food has changed, or a change in appetite. Failing to distinguish between these various changes may lead to ineffective treatment. Separately, much of the historic research on taste or flavor perception was performed in highly controlled model systems with minimal generalizability to real foods, making translation to clinical situations difficult.6 This article attempts to break down disciplinary silos by improving practitioner understanding of how chemosensory research potentially informs childhood feeding.

Evolutionarily, the first food consumed by newborns is human breast milk. If adults tasted breast milk, they would find it to be noticeably sweeter than cow’s milk. Human milk has substantially more lactose than cow’s milk,7 and it also contains the odorants furaneol and maltol,8 both of which have a sweet caramelized odor. Accordingly, the nursing newborn immediately learns to associate sweetness with energy and a mother’s nurturing touch. These learned associations only serve to reinforce an innate, hardwired preference for sweetness that exists even before birth.9 In fact, positive responses to sweet stimuli and negative responses to bitter stimuli are apparent within hours after birth and are conserved across species.10,11 Evidence regarding an innate preference for saltiness is more mixed. It is widely claimed that newborns are indifferent to salty solutions;12 however, other data suggest that preferences for salty stimuli can be seen within 2 to 4 days after birth.13 In newborns, taste preferences can be assessed quantitatively by measuring the duration, strength, or volume of the sucking response or qualitatively by coding of facial responses. In early childhood feeding, facial responses may actually be the most important, because they inform maternal responses, behaviors, and decisions.10,11 Moreover, positive maternal responses may further reinforce the rewarding properties of sweetness via associative learning.

Positive responses to sweet stimuli and negative responses to bitter stimuli are apparent within hours of birth and are conserved across species.

It is critical to recognize that taste qualities such as sweetness, bitterness, and saltiness do not act independently; rather, they interact with each other to alter the sensation that the individual perceives, and these perceptions independently contribute to affective responses to real foods. For example, in a study where participants tasted grapefruit juice in the laboratory, sweetness was positively associated with liking, whereas bitterness was negatively associated with liking. Together, ratings of these taste sensations were able to explain 36% of the variability in liking.14 In other foods such as dark chocolate, bitterness may be tolerable or even desirable. Bitterness, which is almost exclusively aversive in isolation, becomes a key feature of a fine Belgian chocolate when it is experienced along with sweetness, cocoa aroma, and a rich, creamy texture. In addition, the stimuli that give rise to various taste qualities in real foods are frequently multifunctional ingredients—that is, they do more than add a taste.

Finally, when considering what is known about taste, flavor, and ingestive behavior, sensory sensation and function must be distinguished from the affective responses that those sensations elicit, as well as the preferences and behaviors that may result from these affective responses. In children, these 2 aspects are often conflated because we can only infer differences in sensory function from affective responses. Clearly, children who are preverbal cannot describe what they are experiencing. Less obviously however, many of the methods that are routinely used to measure sensory function in adults in an unbiased manner cannot be used even with older children because of the cognitive demands that these tasks require. Additional discussion on the need to carefully distinguish between sensory function and affective response and the implications for clinicians and practitioners is available elsewhere.4,5 Because responses to certain taste qualities are innate whereas responses to most odorants are learned, this article focuses primarily on taste, specifically on sweetness and bitterness. It is important to keep in mind that children are not merely small adults when considering chemosensation. Their sensory systems and affective responses differ considerably from adults and mature after birth and throughout childhood.

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BITTER AND SWEET TASTE IN EARLY CHILDHOOD

Sweetness

Infants are born preferring sweetness and reflexively rejecting bitterness.10,11,15 This seems to be hardwired by evolution; that is, these responses are innate and not learned. Similar reactions are found across species (eg, humans, nonhuman primates, rabbits, and rats), and these reactions do not depend on higher brain regions, because they are found in anencephalic infants and experimentally decerebrated rats. In humans, evidence of a preference for sweetness has even been reported before birth; when the nonnutritive sweetener saccharin is injected into the amniotic fluid of the mother, the fetus swallows more rapidly.9 Likewise, newborns (term and preterm) who are given sucrose increase the frequency and strength of sucking, relative to water or an unflavored nipple.13,16 Positive hedonic responses to sweetness (irrespective of calories) are highly conserved across species, modulate food preferences, and influence food choice across the lifespan.17 Infants and children consistently prefer more concentrated sucrose than adults do,18 and this affective shift may result from energy needs related to growth.19,20 Infant preferences can be assessed by 2 complementary methods: observation and coding of facial responses and consumption of solutions, which vary in taste (ie, sweet and bitter).10,11 Intake and facial responses measures each show increased reactivity to a range of taste stimuli (relative to water) over the first year of life (ie, from 3 to 12 months), and the agreement between intake and facial responses also increases with age.15 Regarding sweetness specifically, at 3 and 6 months, moderately sweet lactose solutions are liked more and consumed more than water; at 12 months, these differences (although still above neutral on average) are no longer statistically significant, suggesting that preferences for sweetness may drop somewhat between 6 and 12 months.15 However, this last finding should be interpreted cautiously, because absence of evidence is not evidence of absence. If confirmed, this may potentially presage changes in preferences seen later in life. Between adolescence and early adulthood, a substantial shift in sweet preference occurs, with adults preferring lower sucrose concentrations.19,21 This shift is believed to be related to a decline in metabolic rate and thus a diminished need for energy associated with sweetness.22

Infants and children consistently prefer more concentrated sucrose than do adults.

However, exposure also plays a central role in the preferred level of sweetness. That is, the context of foods and whether they historically have been experienced as sweet also predicts children’s preferences.23,24 In 1 study, 4- and 5-year-old children were exposed to a novel food (tofu) 15 times over several weeks in 1 of 3 contexts: plain, sweetened, or with added salt. Notably, the children did not universally like the sweetened version; rather, they learned to prefer the version they had been exposed to relative to the other versions (ie, they liked what they came to know).23 Presumably, the children learned to interpret the familiar stimulus as “normal” after repeated exposure. Other data supports the importance of exposure on preference; although the relative preference of sucrose over water declines somewhat between birth and 6 months, this decline is substantially smaller in infants who were regularly fed with water sweetened with sucrose, honey, or corn syrup. Thus, the development of sweet taste preferences likely involves complex interactions between evolutionarily programmed drives, biological demands related to growth, and previous exposure in which the individual encounters various foods over time.25

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Bitterness

As mentioned above, bitterness is innately aversive, and this rejection is conserved across species.10,11 This is typically explained as a protective evolutionary mechanism to prevent the ingestion of toxic compounds in the environment. However, not all bitter substances (bitterants) are toxic.26 Thus, the view that “sweet equals go” whereas “bitter equals stop” is probably an oversimplification. Rather, it seems likely that bitterness may instead signal the need for a cautious approach and for learning with small, repeated tastes.25,27 That children require encouragement and repeated opportunities to learn to accept bitter tastes is wholly consistent with this notion. The primary source of bitterness in children’s diets in the United States today is probably green vegetables, especially brassica vegetables, followed by olives and grapefruit. However, it should also be noted that historically, coffee was regularly given to children as a beverage, and this tradition continues today in other cultures outside the United States.

The view that “sweet equals go” whereas “bitter equals stop” is probably an oversimplification.

With regard to infant and toddler feeding behavior specifically, there is limited evidence to suggest that bitterness perception changes over early childhood.15 There is some evidence that bitterness perception varies over the lifespan, and this variation over time may be partially under hormonal control and/or regulation because changes occur in both puberty and pregnancy.28,29 In pregnancy, bitterness intensity peaks in the first trimester, consistent with the “fetal protection” hypothesis. Later in life, bitter perception seems to decline with aging; however, these alterations seem to be compound-specific rather than across-the-board changes in function.30 As noted previously, it is important to distinguish between true changes in sensory function versus changes in affective responses to various sensations. Currently, we do not know how affective responses to bitterness change with age. However, anecdotal experience would suggest that shifts in liking are quite common in adults, given the wide popularity of kale and Guinness stout. Presumably, such shifts are because of conditioned learning. For example, among regular caffeine consumers, liking for a novel flavor increases when it is paired with caffeine but not when it is paired with a placebo.31

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GENETIC VARIATION IN BITTERNESS AND SWEETNESS

The existing literature on bitter taste perception is difficult to interpret and synthesize because the biological complexity of the bitter taste system has only been fully appreciated within the last decade. The human genome contains a large family of bitter receptor genes known as TAS2Rs. Current evidence suggests that this gene family contains 25 functional genes, along with an additional 11 nonfunctional pseudogenes.32,33 Moreover, a handful of the 25 functional genes, TAS2R4, TAS2R13, TAS2R16, TAS2R31, TAS2R38, and TAS2R41, carry polymorphisms capable of altering function.29,34–44 Some of these functional polymorphisms associate with ingestive behaviors,45,46 including vegetable liking and intake.47–52

Because multiple TAS2Rs contain polymorphisms that alter receptor function, we now understand that bitterness perception is not a monolithic trait that is globally high or low within an individual.46 For example, the high functioning allele for the TAS2R31 gene increases the perceived bitterness of grapefruit, saccharin, and acesulfame potassium (Ace-K),37,40,53 whereas the high functioning allele for the TAS2R38 gene increases the perceived bitterness of alcohol, vegetables, and the bitter drug 6-n-propylthiouracil (PROP).37,38,40,43,47 Because the likelihood of carrying the high functioning allele for one of these genes is independent from the likelihood of carrying the high functioning allele for the other gene, one’s sensory responses to saccharin or grapefruit may be completely unrelated to one’s responses to alcohol or brassica vegetables. Accordingly, existing literature, particularly the older literature that does not account for this variability, needs to be read very cautiously to avoid overgeneralizing across various bitter stimuli.

Because of multiple bitter receptor gene polymorphisms, bitterness perception varies extensively.

Returning to the issue of developmental trajectories, some evidence suggests that age and genetics may interact to influence taste phenotypes. In a large study investigating the bitter drug PROP in relation to TAS2R38 diplotype in children and adults, age influenced sensitivity to PROP but only among the heterozygotes. No such differences were seen for either group of homozygotes.29 In a separate study, the proportion of adolescents who perceived bitterness from PROP was intermediate between adults and children,29,54 again suggesting that bitter-taste phenotype may change with age. At present, it is unknown whether genetic variation may interact with age in early childhood to influence either taste phenotype or ingestive behavior.

For sweetness, there is limited evidence that genetic variation may potentially influence sweetness perception. In contrast to bitterness, the genetics of sweet taste transduction are relatively straightforward, with 2 or 3 genes identified as affecting sweet perception (TAS1R2, TAS1R3, and GNAT3 [gustducin]).55,56 Although sweetness is thought to be universally liked, recent work suggests that sensitivity related to sweetness perception may be somewhat heritable, with individual variation (~30%) in sweetness detection thresholds accounted for by alterations in the TAS1R3 and the GNAT3 genes.57

From data that predate the era of modern molecular genetics, there is ample evidence that the affective response to sweetness differs across individuals.6,58,59 Surprisingly, however, there is very limited evidence on how these hedonic response patterns may influence food choice and ingestive behavior. Nevertheless, what evidence we do have suggests that there is a relationship. In children, the concentration of sucrose that is preferred in a forced choice task associates with the sugar content of favorite cereals and favorite beverages.54 In adults, different response patterns for sucrose seem to generalize to liking for real foods.60 Whether these effects are because of underlying biological differences or are a result of familiarity and habit (ie, “you like what you eat” not just “you eat what you like”) is unknown.

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STUDYING TASTE PERCEPTION WITHIN CONTEXT OF REAL FOODS

Many food ingredients are multifunctional, performing numerous roles within the food matrix. In ice cream, for example, fat acts both as a carrier for molecules that contribute to flavor (eg, vanillin) and as a part of the physical structure that is critical to its desirable melting properties. Likewise, common table salt (sodium chloride) not only adds saltiness to bread, which is its most obvious role, but also stabilizes the cross-linking of proteins that are critical for texture. Sodium ions (not saltiness per se) also reduce bitterness via a peripheral mechanism.61,62 Sugars such as sucrose or fructose impart sweetness, but they can also contribute to viscosity and water binding. This ability to bind water makes the water unavailable to microorganisms, and that is the reason why energy-dense foods such as maple syrup and honey are shelf stable.63

This multiplicity of ingredient functions greatly complicates efforts to systematically study how taste perception potentially influences ingestive behavior and food choice. That is, changing a single ingredient typically alters multiple sensory properties of a food. The complexity discourages many researchers from working with real foods because it causes a loss of experimental control. Instead, researchers may choose to work with simple aqueous solutions. However, free-living individuals do not generally consume table salt or plain sucrose in water. This means that studies that use simplified model systems generally lack ecological validity. Indeed, Rose Marie Pangborn, a pioneering sensory researcher, strongly cautioned against trying to generalize to real foods on the basis of model systems (Suzanne Pecore; email communication on May 6, 2016). Many early attempts in the literature that tried to link sensation to diet or health outcomes were largely unsuccessful.64,65 In hindsight, many of these failures may have been because of the reductionism of the experimental conditions (understandability motivated by a desire for experimental control or logistical limitations) rather than a true absence of a relationship between taste and food choice. If there were truly no connection between chemosensation and food choice, this raises 2 key questions: (1) Why do consumers consistently indicate “taste” is the main driver of their food choices?66 and (2) Why does the food industry spend millions of dollars each year formulating and reformulating products, if not to drive intake (and sales)?67

The complexity of multiple and interactive sensory properties of ingredients discourages many researchers from working with real foods because it causes a loss of experimental control.

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LEVERAGING INTERACTIONS BETWEEN BITTERNESS AND SWEETNESS TO SUPPORT INTAKE

When discussing taste influences on the affective responses to and consumption of real foods, there is a key psychophysical phenomenon, mixture suppression, that needs to be considered. Mixture suppression describes the observation that when 2 qualitatively different stimuli are mixed, the perceptual intensity of each quality in the mixture is lower than the intensity that would have resulted if the same stimuli were presented alone.68 In an early study of mixture suppression in adults, sucrose sweetness reduced the bitterness from caffeine, and a similar, albeit smaller, effect was seen for caffeine bitterness on sucrose sweetness.69 In another early example of mixture suppression, participants used magnitude estimation70,71 to quantify the sweetness and bitterness from a series of quinine and sucrose mixtures.72 When participants tasted a mixture containing both, the sweetness and bitterness were each reduced relative to the same concentration in isolation (Figure). For a mixture containing sucrose and quinine, the bitterness from quinine reduced the sweetness of the mixture by 14%, whereas the sweetness from sucrose reduced the bitterness of the mixture by 53%. Subsequent work indicated that mixture suppression is a central, perceptual phenomenon rather than some sort of inhibition in the periphery or physical interaction in the oral cavity.73 Today, it is known that sweetness reduces bitterness more than bitterness reduces sweetness,74 an asymmetry that is readily apparent when one looks back at data from earlier studies.69,72 Potentially more relevant to the acceptance of real foods, the reduction of bitterness shown in the Figure was also accompanied by a strong reduction in the disliking of the sample. On an unconstrained line scale where zero was neutral,72 the unmixed quinine had a mean pleasantness value of −23.6, whereas the mixture had a mean pleasantness of −1.2. That is, in the presence of some sweetness, the sample was rated near neutral, despite the bitterness that remained.


There are extremely limited data on mixture suppression in children, because the scaling methods used to assess it directly in adults are not developmentally or cognitively appropriate for children. However, there are 2 pieces of evidence that speak to this question indirectly. When children aged 12 to 41 months were given plexiglass lollipops coated with a mixture of a constant amount of sucrose and gum arabic along with an increasing concentration of a food grade bitterant, the mean mouthing time (in seconds) decreased in a dose-dependent manner. The data corresponded directly to the decrease in sweetness and increase in bitterness that were observed for the same lollipops given to adults.75 This suggests that ratings obtained from adults may potentially generalize to children, at least for mixture suppression. More recently, sucrose was shown to successfully reduce the taste intensity of 5 different bitterants in water using a forced choice task in children aged 5 to 12 years.76

Interactions between perceptions of sweetness and bitterness seen in common foods (as opposed to model systems) are also apparent. For example, the amount of bitterness that individuals experience from grapefruit juice varies with the TAS2R31 allele that they carry; even when given the exact same juice, some individuals experience more bitterness due to genetics.37,46 Consistent with the mixture suppression seen in model systems, the adults who experience more bitterness due to genetics also tend to show the opposite pattern for sweetness.46 That is, variation in a single bitter receptor gene can influence both bitterness and sweetness perception, because of mixture suppression. Unsurprisingly then, in adults, when sweetness is greater and bitterness is reduced, rated liking is higher.37,46,72 Elsewhere, statistically independent contributions of bitterness and sweetness on liking scores have been demonstrated in adults for beer, grapefruit juice, Brussels sprouts, and kale.14,77 Critically, these differences in liking are sufficient to influence intake, at least in adults.

These findings are also consistent with evidence from school-aged Danish children (9- to 11-year olds). Those who were more sensitive to bitterness consumed significantly less grapefruit juice in an ad libitum task. Perhaps more interestingly, these children consumed significantly more fruit juices (sea buckthorn and lingonberry) that contained added sucrose; this was interpreted as being consistent with mixture suppression.78 However, except for the Danish juice study, most studies have been conducted in adults and have only considered the endogenous sweetness and bitterness from individual foods which vary across people, presumably because of interactions of receptor genetics and mixture suppression. This raises a critical question: What happens to bitterness and/or the affective response to a bitter vegetable or a bitter medicine if we intentionally add a sweetener? Or as Mary Poppins might ask, “Can a spoonful of sugar help the vegetables go down?”

This raises a critical question: What happens to bitterness and/or the affective response to a bitter vegetable or a bitter medicine if we intentionally add a sweetener?

Polyphenols are a major class of plant bioactives that are widely believed to be health promoting. Unfortunately, polyphenols are commonly described as being bitter and astringent,79 and these sensations are a major barrier to their intake. For example, juices made from the polyphenol-rich chokeberry (aronia) are sour, astringent, bitter, and sweet,80 and juices made from the sea buckthorn are sour, astringent, and bitter.81 However, when sucrose is added to these juices, affective responses in adults increase substantially,80,81 although it should also be noted that this addition may not make the juices liked per se, only less disliked.

Regarding vegetable preferences, several studies using convenience samples of adults suggest that adding sweeteners can reduce bitterness and increase liking for sampled vegetables. This has been shown for broccoli, cauliflower, Brussels sprouts, asparagus, and kale. These effects do not depend on the energy content of the sweetener, because similar effects have been observed for both nutritive and nonnutritive sweeteners.82,83 Whether children experience similar effects with respect to bitterness, liking, or intake has not been fully explored.

Initial evidence from toddlers suggests that masking of bitterness in green beans with salt was effective for increasing intakes of the vegetable.84 When middle to upper class preschool children (3 to 5 years) were given an herbed low-energy–density dip, the amount of celery consumed increased 62%, and the amount of yellow squash increased 137%, relative to the same vegetables served plain. Whether this increase is because of the added herbs and spices or additional sweetness is unknown. However, it seems likely that mixture suppression may be involved, because the base of the low-fat dip contained both sugar and high fructose corn syrup. In a longer term exposure study, when 2- to 5-year-old children were given grapefruit juice sweetened with added sucrose 20 times, liking significantly increased for the children who had disliked unsweetened grapefruit juice at baseline; critically, even when the sucrose was later removed in follow-up testing (ie, unsweetened grapefruit juice was served), liking increased relative to baseline.85 In Danish children aged 22 to 38 months, average intake of artichoke heart puree sweetened with sucrose increased substantially over 10 exposures (14 to 148 g), and in a posttest with unsweetened artichoke puree, intake was 4.6 times greater than baseline, suggesting that increased acceptance generalizes back to the unsweetened vegetable partially but not completely. The changes for the added sucrose group were slightly less than the mere exposure group (5.8-fold increase in intake) and substantially larger than the high-energy density flavor-nutrient learning group (no change from baseline). Similar effects have also been observed in studies with French and British children. In all 3 studies, mere exposure and added sucrose each increased artichoke puree intake, whereas the data on flavor-nutrient learning were more mixed: increased energy density influenced intake in British but not Danish or French children. However, it should also be noted that approximately a third of the children tested in the Danish study (“noneaters”) failed to show any change over time, regardless of intervention group. This indicates that not all children respond equally and that mean effect sizes should be carefully considered with individual differences in mind. Increased intake of initially disliked vegetables has also been observed in children aged 15 to 56 months of age when apple puree (rather than sucrose) is used to provide additional sweetness. While most of these studies have typically been framed in terms of flavor-flavor learning (due to the inherent pleasantness of sweetness), these data are also generally consistent with reduced bitterness via mixture suppression. Additional work is needed to disentangle these 2 potential explanations.

Furthermore, reinforcing the importance of considering interactions between sweetness and bitterness in real foods is the observation that variation in the TAS2R38 bitter receptor gene seems to be related to preferences for both sucrose and real foods in children. In an ethnically diverse sample, children with 1 or 2 copies of the more functional allele (ie, those who experience more bitterness) preferred higher sucrose concentrations than did children with 2 copies of the less functional allele. Likewise, those with 2 copies of the more functional allele liked cereals and beverages with a higher sugar content than did the other children.54 Conversely, no relationship was seen between sugar preferences and taste receptor genotype in their mothers,54 suggesting culture or previous experience may partially override these effects in adulthood.

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EMERGING EVIDENCE SUGGESTS EVEN GREATER COMPLEXITY

Other biological factors beyond receptor function may also influence chemosensory phenotypes. Although they are largely unexplored, these biological factors may potentially influence ingestive behavior. Salivary composition has long been known to vary across people, and recent work suggests that this variability may influence chemosensation. For example, proteins found in saliva were reportedly associated with acceptance of bitter stimuli in young infants.86 Although they are beyond the scope of this review, salivary flow and composition also seem to influence astringency,87–89 starch perception,90,91 and possibly fat perception and liking.92 These observed differences in chemosensory responses may have implications for individual variations in children’s food acceptance patterns. The complexity of the multiple sensory systems that are involved in flavor perception, the multitude of compounds that are found in our environment that are ingested, and the differences in how these compounds perform within different food complexes all underscore the need for additional research.

Observed differences in chemosensory responses may have implications for individual variations in children’s food acceptance patterns.

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CONCLUSIONS

Current evidence suggests that the addition of sugar or salt may improve children’s liking and intake of initially disliked bitter foods. In preschoolers, several studies have suggested pairing bitter foods with more preferred flavors (sweetness, salt, and fat) may improve liking and consumption, at least for some children.93–95 Critically, after conditioning, increased liking and intake seems to generalize back to the plain, unsweetened version of the bitter food.93–95 This suggests that the added salt or sweetener can be removed once acceptance or liking has increased. However, other recent studies have reported little to no effect,96–98 so the collective body of evidence needs to be interpreted cautiously, and additional data are needed to resolve these conflicting reports. Particular attention needs to be given to the foods that are offered, the flavors that are paired with bitter foods, and the inclusion or exclusion of competing, more preferred foods.

Current evidence suggests that addition of salt or sugar may improve children’s liking and intake of initially disliked bitter foods.

Although increases in children’s liking and consumption have resulted from pairing bitter foods with salt (via peripheral blocking), sugar (either via mixture suppression or the simple pleasantness of sweetness), or fat (via physiochemical effects), all of these strategies are at odds with clear recommendations to limit sugar, sodium, and fat in children’s diets.99 Reframed, the questions that come to mind are: (1) Is it is tolerable or appropriate to alter food tastes to improve acceptance for a longer term goal of improving dietary variety, particularly for the individual who is more responsive to bitterness?50; (2) What are the costs and benefits of learning that a food can be enjoyed if it is slightly (as opposed to overwhelmingly) sweetened?; and 3) If learning can be used to increase liking for a single bitter food, how might this generalize to others? Once a preference is established, it would seem important to learn whether the preference might change with age, cognitive capacity, or even be moderated by activity level and energy state. Currently, there is little research that explores whether children’s preference of sweet and salt taste intensity can be modified by dietary exposure and experience. Studies that focus on individual variation in sweet and bitter taste response will be important because they may highlight strategies to more effectively promote acceptance of healthful foods and reduce consumption of foods that are excessively sweetened.17

Strong evolutionary drives encourage almost all mammals to consume sweet foods, and humans have added salt, sugar, and fat to foods for centuries to improve their palatability. However, mounting evidence indicates that individuals should limit their intake of these ingredients because of their adverse effects on health. Conversely, low-energy–density foods rich in polyphenols and/or fiber are frequently underconsumed because of lower palatability. The perceived dichotomy between “delicious” and “healthy” is rapidly learned by young children; most parents have heard some version of “No Daddy, I want something yummy, not something healthy!” This apparent contradiction raises very difficult questions about how to best balance innate pleasure-seeking drives against a need for diets that lead to optimal health. Is it reasonable to expect children (or adults) to stoically eat disliked vegetables, or is acceptable or appropriate to add a small pinch of salt or sugar, if these “forbidden” ingredients help overcome initial and innate aversions for nutrient-rich foods? For parents, is cauliflower in a cheese sauce a better choice, nutritionally speaking, over cauliflower that is steamed, served plain, and then tossed into the trash uneaten? What are the best strategies to develop of lifelong food preferences and eating habits that promote health? Answering such questions empirically with data that integrate sensory biology and ingestive behavior is critical if we are to give parents, policy makers, and food manufacturers appropriate guidance on how best to support health promoting dietary habits.

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REFERENCES

1. American Academy of Pediatrics Committee on Nutrition. Pediatric Nutrition Handbook. 6th ed. Elk Grove Village, IL: American Academy of Pediatrics; 2009.
2. Warwick ZS. Development of taste preferences: implications for nutrition and health. Nutr Today. 1990;25(2):15–18.
3. Duffy VB. Variation in oral sensation: implications for diet and health. Curr Opin Gastroenterol. 2007;23(2):171–177.
4. Boltong A, Keast RS, Aranda SK. A matter of taste: making the distinction between taste and flavor is essential for improving management of dysgeusia. Support Care Cancer. 2011;19(4):441–442.
5. Boltong A, Keast R. Chemosensory science in the context of cancer treatment: implications for patient care. Chemosens Percept. 2015;8(3):117–125.
6. Moskowitz HR. The sweetness and pleasantness of sugars. Am J Psychol. 1971;84(3):387–405.
7. Chapter 3: lactose content of milk and milk products. Am J Clin Nutr. 1988;48(4):1099–1104.
8. Bingham PM, Stevens-Tuttle D, Lavin E, Acree T. Odorants in breast milk. Arch Pediatr Adolesc Med. 2003;157(10):1031.
9. de Snoo K. Das trinkende kind im uterus. Gynecol Obstet Invest. 1937;105(2-3):88–97.
10. Steiner JE. Facial expressions of the neonate infant indicating the hedonics of food-related chemical stimuli. In: Weiffenbach JM, ed. Taste and Development: The Genesis of Sweet Preference. Bethesda, MD: US Department of Health, Education, and Welfare; 1977:173–189.
11. Steiner JE, Glaser D, Hawilo ME, Berridge KC. Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates. Neurosci Biobehav Rev. 2001;25(1):53–74.
12. Beauchamp GK, Mennella JA. Flavor perception in human infants: development and functional significance. Digestion. 2011;83(suppl 1):1–6.
13. Zinner SH, McGarvey ST, Lipsitt LP, Rosner B. Neonatal blood pressure and salt taste responsiveness. Hypertension. 2002;40(3):280–285.
14. Lanier SA, Hayes JE, Duffy VB. Sweet and bitter tastes of alcoholic beverages mediate alcohol intake in of-age undergraduates. Physiol Behav. 2005;83(5):821–831.
15. Schwartz C, Issanchou S, Nicklaus S. Developmental changes in the acceptance of the five basic tastes in the first year of life. Br J Nutr. 2009;102(9):1375–1385.
16. Maone TR, Mattes RD, Bernbaum JC, Beauchamp GK. A new method for delivering a taste without fluids to preterm and term infants. Dev Psychobiol. 1990;23(2):179–191.
17. Mennella JA, Bobowski NK, Reed DR. The development of sweet taste: from biology to hedonics. Rev Endocr Metab Disord. 2016;17(2):171–178.
18. Coldwell SE, Mennella JA, Duffy VB, et al. Gustation assessment using the NIH Toolbox. Neurology. 2013;80(11 suppl 3):S20–S24.
19. Desor JA, Beauchamp GK. Longitudinal changes in sweet preferences in humans. Physiol Behav. 1987;39(5):639–641.
20. Mennella JA, Finkbeiner S, Lipchock SV, Hwang LD, Reed DR. Preferences for salty and sweet tastes are elevated and related to each other during childhood. PLoS One. 2014;9(3):e92201.
21. De Graaf C, Zandstra EH. Sweetness intensity and pleasantness in children, adolescents, and adults. Physiol Behav. 1999;67(4):513–520.
22. Drewnowski A. Sensory control of energy density at different life stages. Proc Nutr Soc. 2000;59(2):239–244.
23. Sullivan SA, Birch LL. Pass the sugar, pass the salt: experience dictates preference. Dev Psychol. 1990;26(4):546–551.
24. Messer E. Some like it sweet: estimating sweetness preferences and sucrose intakes from ethnographic and experimental data. Am Anthropol. 1986;88(3):637–647.
25. Reed DR, Tanaka T, McDaniel AH. Diverse tastes: genetics of sweet and bitter perception. Physiol Behav. 2006;88(3):215–226.
26. Glendinning JI. Is the bitter rejection response always adaptive? Physiol Behav. 1994;56(6):1217–1227.
27. Garcia J, Hankins WG. The evolution of bitter and the acquisition of toxiphobia. In: Denton DA, Coghlan JP, eds. Olfaction and Taste: 5th Symposium. New York, NY: Academic Press, Inc; 1975:39–45.
28. Duffy VB, Bartoshuk LM, Striegel-Moore R, Rodin J. Taste changes across pregnancy. Ann N Y Acad Sci. 1998;855:805–809.
29. Mennella JA, Pepino MY, Duke FF, Reed DR. Age modifies the genotype-phenotype relationship for the bitter receptor TAS2R38. BMC Genet. 2010;11:60.
30. Cowart BJ, Yokomukai Y, Beauchamp GK. Bitter taste in aging: compound-specific decline in sensitivity. Physiol Behav. 1994;56(6):1237–1241.
31. Yeomans MR, Durlach PJ, Tinley EM. Flavour liking and preference conditioned by caffeine in humans. Q J Exp Psychol B. 2005;58(1):47–58.
32. Risso D, Tofanelli S, Morini G, Luiselli D, Drayna D. Genetic variation in taste receptor pseudogenes provides evidence for a dynamic role in human evolution. BMC Evol Biol. 2014;14:198.
33. Meyerhof W, Batram C, Kuhn C, et al. The molecular receptive ranges of human TAS2R bitter taste receptors. Chem Senses. 2010;35(2):157–170.
34. Kim UK, Drayna D. Genetics of individual differences in bitter taste perception: lessons from the PTC gene. Clin Genet. 2005;67(4):275–280.
35. Bufe B, Breslin PA, Kuhn C, et al. The molecular basis of individual differences in phenylthiocarbamide and propylthiouracil bitterness perception. Curr Biol. 2005;15(4):322–327.
36. Hayes JE, Bartoshuk LM, Kidd JR, Duffy VB. Supertasting and PROP bitterness depends on more than the TAS2R38 gene. Chem Senses. 2008;33(3):255–265.
37. Hayes JE, Feeney EL, Nolden AA, McGeary JE. Quinine bitterness and grapefruit liking associate with allelic variants in TAS2R31. Chem Senses. 2015;40(6):437–443.
38. Nolden AA, McGeary JE, Hayes JE. Differential bitterness in capsaicin, piperine, and ethanol associates with polymorphisms in multiple bitter taste receptor genes. Physiol Behav. 2016;156:117–127.
39. Dotson CD, Wallace MR, Bartoshuk LM, Logan HL. Variation in the gene TAS2R13 is associated with differences in alcohol consumption in patients with head and neck cancer. Chem Senses. 2012;37(8):737–744.
40. Allen AL, McGeary JE, Knopik VS, Hayes JE. Bitterness of the non-nutritive sweetener acesulfame potassium varies with polymorphisms in TAS2R9 and TAS2R31. Chem Senses. 2013;38(5):379–389.
41. Soranzo N, Bufe B, Sabeti PC, et al. Positive selection on a high-sensitivity allele of the human bitter-taste receptor TAS2R16. Curr Biol. 2005;15(14):1257–1265.
42. Wooding S, Gunn H, Ramos P, Thalmann S, Xing C, Meyerhof W. Genetics and bitter taste responses to goitrin, a plant toxin found in vegetables. Chem Senses. 2010;35(8):685–692.
43. Sandell MA, Breslin PA. Variability in a taste-receptor gene determines whether we taste toxins in food. Curr Biol. 2006;16(18):R792–R794.
44. Thalmann S, Behrens M, Meyerhof W. Major haplotypes of the human bitter taste receptor TAS2R41 encode functional receptors for chloramphenicol. Biochem Biophys Res Commun. 2013;435(2):267–273.
45. Duffy VB, Davidson AC, Kidd JR, et al. Bitter receptor gene (TAS2R38), 6-n-propylthiouracil (PROP) bitterness and alcohol intake. Alcohol Clin Exp Res. 2004;28(11):1629–1637.
46. Hayes JE, Wallace MR, Knopik VS, Herbstman DM, Bartoshuk LM, Duffy VB. Allelic variation in TAS2R bitter receptor genes associates with variation in sensations from and ingestive behaviors toward common bitter beverages in adults. Chem Senses. 2011;36(3):311–319.
47. Shen Y, Kennedy OB, Methven L. Exploring the effects of genotypical and phenotypical variations in bitter taste sensitivity on perception, liking and intake of brassica vegetables in the UK. Food Qual Pref. 2016;50:71–81.
48. Duffy VB, Hayes JE, Davidson AC, Kidd JR, Kidd KK, Bartoshuk LM. Vegetable intake in college-aged adults is explained by oral sensory phenotypes and TAS2R38 genotype. Chemosens Percept. 2010;3(3–4):137–148.
49. Sandell M, Hoppu U, Mikkilä V, et al. Genetic variation in the hTAS2R38 taste receptor and food consumption among Finnish adults. Genes Nutr. 2014;9(6):433.
50. Hayes JE, Feeney EL, Allen AL. Do polymorphisms in chemosensory genes matter for human ingestive behavior? Food Qual Prefer. 2013;30(2):202–216.
51. Running CA, Hayes JE. Individual differences in multisensory flavor perception. In: Piqueras-Fiszman B, Spence C, eds. Multisensory Flavor Perception: From Fundamental Neuroscience Through to the Marketplace. Duxford, UK: Woodhead Publishing, Ltd.; 2016:185–210.
52. Keller KL, Adise S. Variation in the ability to taste bitter thiourea compounds: implications for food acceptance, dietary intake, and obesity risk in children. Annu Rev Nutr. 2016;36:157–182.
53. Roudnitzky N, Bufe B, Thalmann S, et al. Genomic, genetic and functional dissection of bitter taste responses to artificial sweeteners. Hum Mol Genet. 2011;20(17):3437–3449.
54. Mennella JA, Pepino MY, Reed DR. Genetic and environmental determinants of bitter perception and sweet preferences. Pediatrics. 2005;115(2):e216–e222.
55. Boughter JD Jr, Bachmanov AA. Behavioral genetics and taste. BMC Neurosci. 2007;8(suppl 3):S3.
56. Bachmanov AA, Bosak NP, Floriano WB, et al. Genetics of sweet taste preferences. Flavour Fragr J. 2011;26(4):286–294.
57. Hwang LD, Zhu G, Breslin PA, Reed DR, Martin NG, Wright MJ. A common genetic influence on human intensity ratings of sugars and high-potency sweeteners. Twin Res Hum Genet. 2015;18(4):361–367.
58. Pangborn RM. Individual variation in affective responses to taste stimuli. Psychon Sci. 1970;21(2):125–126.
59. Lundgren B, Jonsson B, Pangborn RM, et al. Taste discrimination vs hedonic response to sucrose in coffee beverage. an interlaboratory study. Chem Senses. 1978;3(3):249–265.
60. Kim J-Y, Prescott J, Kim K-O. Patterns of sweet liking in sucrose solutions and beverages. Food Qual Prefer. 2014;36:96–103.
61. Gillette M. Flavor effects of sodium chloride. Food Technol. 1985;39(6):47–52.
62. Breslin PA, Beauchamp GK. Salt enhances flavour by suppressing bitterness. Nature. 1997;387(6633):563.
63. Norrish RS. An equation for the activity coefficients and equilibrium relative humidities of water in confectionery syrups. Int J Food Sci Tech. 1966;1(1):25–39.
64. Enns MP, Van Itallie TB, Grinker JA. Contributions of age, sex and degree of fatness on preferences and magnitude estimations for sucrose in humans. Physiol Behav. 1979;22(5):999–1003.
65. Pangborn RM, Pecore SD. Taste perception of sodium chloride in relation to dietary intake of salt. Am J Clin Nutr. 1982;35(3):510–520.
67. Hayes JE. Measuring sensory perception in relation to consumer behavior. In: Delarue J, Lawlor JB, Rogeaux M, eds. Rapid Sensory Profiling Techniques and Related Methods: Applications in New Product Development and Consumer Research. Cambridge, UK: Woodhead Publishing; 2015:53–70.
68. Keast RSJ, Breslin PAS. An overview of binary taste-taste interactions. Food Qual Pref. 2003;14(2):111–124.
69. Kamen JM, Pilgrim FJ, Gutman NJ, Kroll BJ. Interactions of suprathreshold taste stimuli. J Exp Psychol. 1961;62:348–356.
70. Moskowitz H. Magnitude estimation: notes on what, how, when, and why to use it. J Food Qual. 1977;1(3):195–227.
71. Stevens SS. The direct estimation of sensory magnitudes-loudness. Am J Psychol. 1956;69(1):1–25.
72. Lawless HT. The pleasantness of mixtures in taste and olfaction. Sens Processes. 1977;1(3):227–237.
73. Lawless HT. Evidence for neural inhibition in bittersweet taste mixtures. J Comp Physiol Psychol. 1979;93(3):538–547.
74. Green BG, Lim J, Osterhoff F, Blacher K, Nachtigal D. Taste mixture interactions: suppression, additivity, and the predominance of sweetness. Physiol Behav. 2010;101(5):731–737.
75. Lawless HT, Hammer LD, Corina MD. Aversions to bitterness and accidental poisonings among preschool children. J Toxicol Clin Toxicol. 1982;19(9):951–964.
76. Mennella JA, Reed DR, Mathew PS, Roberts KM, Mansfield CJ. “A spoonful of sugar helps the medicine go down”: bitter masking by sucrose among children and adults. Chem Senses. 2015;40(1):17–25.
77. Dinehart ME, Hayes JE, Bartoshuk LM, Lanier SL, Duffy VB. Bitter taste markers explain variability in vegetable sweetness, bitterness, and intake. Physiol Behav. 2006;87(2):304–313.
78. Hartvig D, Hausner H, Wendin K, Bredie WL. Quinine sensitivity influences the acceptance of sea-buckthorn and grapefruit juices in 9- to 11-year-old children. Appetite. 2014;74:70–78.
79. Fleming EE, Ziegler GR, Hayes JE. Check-all-that-apply (CATA), sorting, and polarized sensory positioning (PSP) with astringent stimuli. Food Qual Prefer. 2015;45:41–49.
80. Duffy VB, Rawal S, Park J, Brand MH, Sharafi M, Bolling BW. Characterizing and improving the sensory and hedonic responses to polyphenol-rich aronia berry juice. Appetite. 2016;107:116–125.
81. Tang X, Kalviainen N, Tuorila H. Sensory and hedonic characteristics of juice of sea buckthorn (Hippophae rhamnoides L.) origins and hybrids. LWT-Food Sci Technol. 2001;34(2):102–110.
82. Wilkie LM, Phillips EDC, Wadhera D. Sucrose and non-nutritive sweeteners can suppress the bitterness of vegetables independent of PTC taster phenotype. Chemosens Percept. 2013;6(3):127–139.
83. Sharafi M, Hayes JE, Duffy VB. Masking vegetable bitterness to improve palatability depends on vegetable type and taste phenotype. Chemosens Percept. 2013;6(1):8–19.
84. Bouhlal S, Issanchou S, Nicklaus S. The impact of salt, fat and sugar levels on toddler food intake. Br J Nutr. 2011;105(4):645–653.
85. Capaldi ED, Privitera GJ. Decreasing dislike for sour and bitter in children and adults. Appetite. 2008;50(1):139–145.
86. Morzel M, Chabanet C, Schwartz C, Lucchi G, Ducoroy P, Nicklaus S. Salivary protein profiles are linked to bitter taste acceptance in infants. Eur J Pediatr. 2014;173(5):575–582.
87. Horne J, Hayes J, Lawless HT. Turbidity as a measure of salivary protein reactions with astringent substances. Chem Senses. 2002;27(7):653–659.
88. Fleming EE, Ziegler GR, Hayes JE. Salivary protein levels as a predictor of perceived astringency in model systems and solid foods. Physiol Behav. 2016;163:56–63.
89. Dinnella C, Recchia A, Tuorila H, Monteleone E. Individual astringency responsiveness affects the acceptance of phenol-rich foods. Appetite. 2011;56(3):633–642.
90. Perry GH, Dominy NJ, Claw KG, et al. Diet and the evolution of human amylase gene copy number variation. Nat Genet. 2007;39(10):1256–1260.
91. Mandel AL, Peyrot des Gachons C, Plank KL, Alarcon S, Breslin PA. Individual differences in AMY1 gene copy number, salivary α-amylase levels, and the perception of oral starch. PLoS One. 2010;5(10):e13352.
92. Neyraud E, Palicki O, Schwartz C, Nicklaus S, Feron G. Variability of human saliva composition: possible relationships with fat perception and liking. Arch Oral Biol. 2012;57(5):556–566.
93. Capaldi-Phillips ED, Wadhera D. Associative conditioning can increase liking for and consumption of brussels sprouts in children aged 3 to 5 years. J Acad Nutr Diet. 2014;114(8):1236–1241.
94. Fisher JO, Mennella JA, Hughes SO, Liu Y, Mendoza PM, Patrick H. Offering “dip” promotes intake of a moderately-liked raw vegetable among preschoolers with genetic sensitivity to bitterness. J Acad Nutr Diet. 2012;112(2):235–245.
95. Havermans RC, Jansen A. Increasing children’s liking of vegetables through flavour-flavour learning. Appetite. 2007;48(2):259–262.
96. Caton SJ, Blundell P, Ahern SM, et al. Learning to eat vegetables in early life: the role of timing, age and individual eating traits. PLoS One. 2014;9(5):e97609.
97. Caton SJ, Ahern SM, Remy E, Nicklaus S, Blundell P, Hetherington MM. Repetition counts: repeated exposure increases intake of a novel vegetable in UK pre-school children compared to flavour-flavour and flavour-nutrient learning. Br J Nutr. 2013;109(11):2089–2097.
98. Anzman-Frasca S, Savage JS, Marini ME, Fisher JO, Birch LL. Repeated exposure and associative conditioning promote preschool children’s liking of vegetables. Appetite. 2012;58(2):543–553.
99. Vos MB, Kaar JL, Welsh JA, et al. Added sugars and cardiovascular disease risk in children: a scientific statement from the American Heart Association [published online ahead of print August 22, 2016]. Circulation. 2016.

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