Trimethylaminuria

Anyone who has observed infants for any period of time can testify to the intense activity occurring in and around their mouths--a primary site for learning in the first few months of life. During feeding, or while mouthing objects such as their hands and toys, infants learn to discriminate the varying features of their new world. They use the sense of touch to discriminate between textures, and the senses of taste and smell to discriminate flavors. Before they are even able to crawl, infants have learned much about their sensory world.

Knowledge of flavor perception in the human infant has expanded substantially over the past few decades. It is now widely recognized that newborn infants are not passive receptacles for flavors--rather, they avidly accept some, while decidedly rejecting others.

Through human and other animal studies, we have also learned that the flavor aspects of foods eaten by mothers are transmitted through their milk to their infants, with the odor of garlic being a good example.(1)(2) These studies suggest that mother's milk is a potentially rich source of flavor experiences, affording breastfed infants an early opportunity to learn about the "flavor" of their culture. That is, American, African, East Indian, Asian, Middle Eastern, European, and Hispanic children alike may all become familiarized with the spicing and seasoning of their mother's diet, long before solid foods are ever introduced.

Other animal studies suggest that these early flavor experiences affect later food acceptability. The research shows that young animals prefer the flavor of the foods eaten by their mothers during nursing(3)(4)(5)(6)(7) and that their young are also more likely to accept unfamiliar foods if they have experienced a variety of flavors during suckling.(8)

In contrast to the potentially variant chemosensory experiences of breastfed infants, bottlefed infants experience a constant set of flavors from standard infant formulas. Though receiving appropriate nutrition, bottlefed infants may be missing significant sensory experiences which, until recent times in human history, were common to all infants.

In this article we will discuss how amniotic fluid and human milk are potentially rich media for early flavor experiences. We will also discuss how the chemical senses of taste and smell change during infancy. First, however, we must establish a basic understanding of taste and smell and the differences between them.

WHAT IS FLAVOR?

The "flavor" we experience while eating foods is a product of two frequently confused chemical senses: taste or gustation and smell or olfaction.

Taste refers to the sensation occurring when chemicals stimulate taste receptors on the tongue and other parts of the oropharynx (Figure 1). Taste stimuli are often separated into a small number of "primary" tastes: sweet, salty, bitter, sour, and perhaps savory, the taste of "umami" or monosodium glutamate (MSG).

[CHART OMITTED]

Smell, on the other hand, occurs when chemicals stimulate olfactory receptors in the nasal cavity. Unlike the sense of taste, there may be many different classes of odor stimuli, perhaps thousands. Odors can reach the olfactory receptors in two ways: they can enter the nostril during inhalation (orthonasal route) or they can travel from the back of the nasopharynx toward the roof to the nasal cavity (retronasal route) during suckling in infants or chewing and swallowing in older children and adults (Figure 1).

Retronasal olfaction contributes significantly to the perception of flavor. For example, holding one's nose while eating interrupts retronasal olfaction and eliminates many of the subtleties of food, leaving only the taste components (sweet, salty, sour, bitter, and savory) remaining. The importance of smell in flavor perception is most clearly noted by head cold sufferers who lose the ability to discriminate common foods when olfactory receptors are blocked. Similarly, foods often taste better after individuals quit smoking because their sense of smell has improved,(9) allowing them to detect more subtleties of flavor. The role of smell in flavor is critical to enjoying foods like licorice, vanilla, and citrus, which can only be experienced through the sense of smell.

It should be noted that other properties of food (e.g., viscosity, temperature, irritation) are also very important to perceived flavor. However, little experimental work has been done in this area of infant flavor perception. Therefore, in this article, we will focus on the infant's senses of taste and smell.

DEVELOPING SENSITIVITIES AND PREFERENCES

The sensory world of the young infant differs from that of the adult in that the infant's sense of taste develops over time (Table 1). Specifically, sweet responses are evident prenatally, and major changes are not known to occur postnatally. Similarly, the rejection of sour taste is evidenced from birth onward, whereas salt and bitter sensitivities appear to change postnatally.

Table 1 Development Changes in the Infant's Response to Tastes(*)

(*)Infants' responses to various tastes solutions relative to water or diluent.

([dagger])Facial expressions suggest rejection, whereas intake studies suggest indifference.

([double dagger])Sucking measures suggest rejection, whereas intake and facial expression studies suggest indifference.

([sections])Preference seen only when MSG mixed with soup; MSG solution alone is rejected relative to plain water.

([paragraph])Preference emerges at approximately 4 months of age; before that, indifference or rejection depending on the methods used.

Less is known about how olfactory perceptions and preferences change over time. Clearly, infants are able to detect and discriminate among a wide variety of odors shortly after birth. However, it is not yet known whether they hedonically respond to differences in odor quality, viz., which odors infants find pleasant.

FETUS AND PREMATURE INFANTS

Studies on Taste. Taste cells first appear in the human fetus at 7 to 8 weeks' gestation, with morphologically mature cells appearing at about 14 weeks.(10) These receptors may be stimulated by the varying chemicals presented in the amniotic fluid when the fetus begins to swallow episodically at about the 12th week of gestation.(11)(12)

Studies on taste sensation in the preterm infant are rare, due, in part, to methodological limitations. When preterm infants, who had been fed exclusively via gastric tubes, were presented with minute amounts of either glucose or water solutions intraorally, they exhibited more nonnutritive sucking in response to the glucose than to the water.(13)

Because immature suck-swallow coordination puts premature infants at risk for aspirating fluids, reserchers at Monell have developed a new methodology that embeds taste substances in a nipple-shaped gelatin medium.(14) Small amounts of a substance are then released when the nipple is mouthed or sucked, eliminating the need for administering fluids during testing. Infants born preterm and tested between 33 and 40 weeks postconception produced more frequent, stronger sucking responses when offered a sucrosesweetened nipple, compared with a latex nipple.

The results from these studies indicate that, before birth, the human infant possesses a sensory apparatus that can detect sweet tastes.

Studies on Smell. Although the olfactory system is well developed before birth,(15) it is not know whether the fetus responds to olfactory stimuli. However, recent reports indicate that the environment in which the fetus lives--the amniotic fluid--can indeed be odorous. This odor can indicate certain disease states (such as maple syrup disease,(16) phenylketonuria,(17) and trimethylaminuria(18) or the types of foods eaten by the pregnant mother.(19) The fact that the amniotic fluid and the newborn's body can acquire the odor of a spicy meal the mother ingested before giving birth suggests that odorous compounds in her diet can be transferred to the amniotic fluid. Because the normal fetus swallows significant amounts of amniotic fluid during the latter stages of gestation(20) and has open airway passages that are bathed in amniotic fluid,(21) the fetus may be exposed to a unique olfactory environment. Studies on other animals reveal that adults prefer certain odors that were experienced in utero.(22) Whether similar mechanisms are operating in humans remains unknown.

NEWBORNS

Studies on Taste. Facial expressions, which suggest contentment and liking or discomfort and rejection, have been used to assess the newborn's responsiveness to taste stimuli in some of the earliest investigations on human taste development (Figure 2, A to D). During the first few hours of life, infants display relatively consistent, quality-specific facial expressions when the sweet tastes of sucrose (facial relaxation followed by positive mouth gaping; Figure 2A), the sour taste of concentrated citric acid (lip pursing and facial grimace; Figure 2B), and the bitter taste of concentrated quinine and urea (tongue protrusion and grimace; Figure 2C) are presented into the oral cavity.(23)(24)(25) No distinct facial response is evidenced with salt taste, however (Figure 2D). Infants also display distinct positive facial expressions, similar to those observed with sweetness, when tasting soup to which MSG has been added when compared with the soup diluent alone.(26) MSG alone does not appear to elicit those facial responses, however, raising the question of exactly what it is about the MSG-flavored soup that is of apparent positive hedonic value.

[CHART OMITTED]

Intake studies, which compare how much an infant consumes of a taste solution and a diluent solution during brief presentations, are the most frequent method used to evaluate taste preferences. Generally, intake studies use weaker concentrations of taste stimuli than do studies on facial expressions. If an infant ingests more of the taste solution than a diluent, for example, one can infer that (a) the infant can detect the taste and, with less certainty, (b) the infant prefers or likes the tastant more than the diluent.

Consistent with the findings for premature infants, these studies repeatedly demonstrate strong acceptance of sweet-tasting sugars by newborn infants. Newborns will respond to even dilute sweet solutions, and they can differentiate varying degrees of sweetnees and different kinds of sugars.(27) In contrast, they reject the sour taste of citric acid and are apparently indifferent to the taste of low to moderate concentrations of salt and the bitter taste of urea.(28)

Finally, as was the case for premature infants, newborn's sucking patterns have been used in taste research as an alternative to intake studies. These studies also indicate that sweet stimuli are positive and salt taste is negative, in that salt intake suppresses sucking relative to the infant's response to the diluent alone.(29)

Although each measure has its limitations, the convergence of research findings supports the conclusion that the ability to detect sweets is evident very early in human development and that its hedonic tone--that is, its pleasantness--is also well developed at birth. It is likely that the innate liking of sweets and rejection of bitter tastes in humans is a consequence of selection, favoring animals who consumed high-energy, vitamin-rich fruit and vegetable diets, while avoiding bitter, poisonous fruits and plants. Although the preference for sweet tastes appears to be innate, experience with them may also play an interacting role in development. There is, however, no evidence in humans that variations in early exposure to sweets permanently alters the preference for sweet-tasting foods.(30) Fewer studies on sour tastes have been conducted with newborn infants, but those that have been done suggest that sour-tasting substances are unpleasant. Because of the lack of research, it is not known whether there are developmental changes in sensitivity of preference for sourtasting compounds.

Conclusions regarding the neonate's response to bitter and salty tastes are more problematic. Newborns respond with highly negative facial expressions to concentrated quinine and urea (Figure 2), but they do not reject moderate concentrations of urea.(25) The reason for this difference remains unclear. Perhaps the newborn can detect bitter substances, but the ability to reject a substance or modulate intake will come as the infant matures. Further stdudies using a variety of bitter stimuli and additional behavioral measures could resolve this question. With regard to salt perception, stdudies measuring intake and facial expressions suggest that the newborn infant is indifferent to and may not detect salt. However, salt does appear to suppress some parameters of sucking in newborns. Here, too, more research is needed to clarify the newborn's response to salt. No studies suggest, however, that the taste of salt is attractive to the newborn infant.

Studies on Smell. Odor preferences in newborns are more difficult to assess. However, we do know that, shortly after birth, human infants are able to detect a wide variety of odors, with perhaps the most salient of these odors originating from the mother. Within hours after birth, mothers and infants can recognize each other through the sense of smell alone. Day-old breastfed infants spend more time orienting toward a breast pad previously worn by their lactating mothers than one worn by an unfamiliar lactating woman.(31)(32)(33) They move their head and arms less and suck more when they are exposed to their mother's odors.(34) This ability of breastfed infants to discriminate the odors of their mothers from those of other lactating women is not limited to odors emanating from the breast region. They can also discriminate odors originating from their mother's underarms and neck.

Interestingly, bottlefed infants do not discriminate their mothers' odors from those of an unfamiliar bottlefeeding mother.(33)(34) It has been suggested that breastfed infants are able to discriminate these odors because they, unlike bottlefed infants, have prolonged periods of skin contact with their mothers, and their nostrils are in close proximity to their mother's breasts and underarms during feeding. Recent studies, however, suggest that bottlefed infants also prefer the breast odors of lactating women.(35) Therefore, breast odors, or the volatile components of breast milk, may be particularly attractive to all newborns.

OLDER INFANTS

Studies on Taste. Babies beyond the neonatal period (1 to 24 months) have been most neglected in studies on taste development. Nonetheless, a few notable findings suggest that changes in taste responses occur during this time in development.

Studies conducted in Mexico focused on the responses of well-nourished and malnourished infants, aged 2 to 24 months, to determine whether the protein-calorie status of the infants affected their taste preferences.(36) At all ages, both the well-nourished and the malnourished infants preferred the sucrose but rejected the bitter (urea) and sour (citric acid) stimuli. The infants under the age of 1 year preferred the salty solutions, whereas those older than 1 year were indifferent to the salt.

Although newborn infants are indifferent to or reject salt relative to plain water, a developmental shift in salt acceptability has been supported in more recent studies of U.S. children, with whom preferential ingestion of salt water relative to plain wter first emerged at approximately 4 months of age.(37) It has been argued that experience with salty tastes probably does not play a major role in the shift from indifference or rejection of salt at birth to acceptance in later infancy.(37) Rather, this change in response may reflect postnatal maturation of central and/or peripheral mechanisms underlying salt taste perception. Thus the salt preference that emerges at approximately 4 months of age may be largely unlearned. Although animal model studies demonstrate that early alterations in sodium balance alters long-term salt preference behavior,(38) whether this occurs in humans is unknown.

A recent study on the infant's sensitivity to bitter taste revealed that relatively low concentrations of urea were not rejected in newborn infants, but rejection was evident among infants who were 14 to 180 days of age.(39) This is consistent with the idea that there is an early developmental change in bitterness perception or the ability to regulate the intake of bitter solutions. As a practical matter, it could explain why older infants reject bitter-tasting foods, such as green vegetables. Parents can expect a "learning period" when introducing these foods and anticipate a need to introduce them slowly, but consistently. With exposure, eventually these foods may be tolerated and even enjoyed.

Studies on Smell. During the past few years, research at Monell has focused on the early olfactory experiences of the human infant, using mother's milk as the medium for these experiences. As mentioned earlier, we have demonstrated that human milk, like the milk of other animals,(2) can acquire a wide variety of odors from the mother's diet. The breastfeeding infant's ability to detect the sensory changes in the mother's milk is suggested by the infant's altered suckling behavior when the milk is flavored, e.g., the infant feeds longer and sucks more overall when the milk is flavored with garlic.(1) The mouth movements made during suckling may facilitate the retronasal perception of the garlic volatiles in the milk, enhancing the infant's ability to "taste" the change.

The flavor of human milk is also altered when nursing women drink alcohol, a beverage that has been recommended for centuries to nursing mothers as an aid to lactation. Folklore relates that drinking small quantities of alcohol shortly before nursing increases milk yield, facilitates milk letdown, and relaxes both the mother and her baby. In recent studies, alcohol consumption by nursing mothers was shown to alter the flavor of the mothers' milk and the behavior of their infants during breast feeding.(40)(41) Unlike the response to garlic-flavored milk, the infants did not feed longer when the milk was flavored with alcohol. They did, however, consume significantly less alcohol-flavored milk--even though they sucked more during the initial minutes of the feedings. Whether the infants were responding to the altered milk flavor or whether the alcohol was having a pharmacological effect on the nursing mothers is the subject of present investigations. Whatever the case, it would seem that the recommendation for a nursing mother to drink a glass of beer or wine before nursing may actually be counterproductive. While the mother may be more relaxed after a drink, her baby will ingest less milk.

CONCLUSION

The flavor world of the breastfed infant is potentially much richer than previously thought. Because research shows that the senses of taste and smell are not only functioning in the human neonate but also change during development, breastfed infants may be afforded an opportunity to learn about the flavor of the foods of their people long before solids are introduced.

Based on a variety of animal model studies,(3)(4)(5)(6)(7)(8) an infant's prior exposure to flavors in mother's milk may actually increase the desirability of those flavors through familiarization. Unfamiliar foods, which are often not preferred by children, become preferred with repeated presentations and increased familiarity;(42) bitter tastes, such as green vegetables, are a notable example. Studies on other animals(8) also suggest that the experience with a variety of flavors during breastfeeding, in contrast to the invariant flavor experience during formula feeding, predisposes breastfed infants toward an increased willingness to accept unfamiliar flavors. Indeed, a recent study revealed that breastfed infants will consume more of a novel vegetable than will their formula-fed counterparts.(43)

Finally, recent studies indicate that 25% of bottlefed infants experience a change in formula during the first months of life, usually in response to nonspecific symptoms.(44) Perhaps, as Da Mota(45) has suggested, "this monotony, which is contrary to the most basic rule in dietary habits, might just prove too much for one in four babies."

As a relatively new and exciting area of study, many questions remain unanswered about the infant's sense of taste and smell. The long-term goals of research at Monell are to uncover whether exposure to flavors in the amniotic fluid or mother's milk affects the infant's later preferences, the development of food habits, and the infant's willingness to accept new foods at weaning or thereafter. Also worthy of study is how early feeding style (breast or bottle feeding) affects later behavior. This is especially relevant when considering amniotic fluid as a potential "flavor bridge" to breast milk, and then breast milk, as a bridge to solid foods.

Although much research is still needed to fully understand how the infant is affected by experiencing flavors in mother's milk, it is clear that human infants are not passive receptacles for flavored foods. Rather, they will avidly accept some flavors, while decidedly rejecting others. Because every baby is an individual, with his or her own likes and dislikes, parents should expect that their child will need time to learn to like some foods, though the child may never like others.

Parents who offer their babies and growing children a variety of foods will provide both a nutritious, well-balanced diet as well as an opportunity for their child's own personal tastes to develop.

HISTORY AND FOLKLORE OF NURSING

Clearly, the notion that flavors from a mother's diet can be transmitted to her milk is not a new one, since medical writings from the 14th century A.D. stated that if milk had an offensive odor, it could be made more pleasant if the woman drank fragrant wines or ate sweet foods. A diet of white bread, veal, mutton and poultry, and ripe fruits was recommended to keep her body open and her bile equally distributed. Pickles and spices and salted or seasoned meats, on the other hand, would cause her milk to become heated and acrimonious.

Up to the eighteenth century, breastfeeding was the predominant form of child nutrition. Before sanitary precautions were known, and before the differences between human milk and the raw milk of other animals were understood, the only successful substitute for a mother's milk was the milk of another human female. The wet nurse was usually a woman of lower social rank who had recently had a child and was supplied with milk. Her duties meant giving up the care of her own child to nurse the child of her social superior. The folklore surrounding the choice of a wet nurse is equally rich and colorful. It was believed that the characteristics of the nurse were imbibed by the child through the milk, and, therefore, careful selection was warranted. It was said that if the nurse hired was a promiscuous or evil-tempered woman, the child would suck in her vices through her milk. And, if she was red-haired, her milk would surely engender a treacherous mind in the child. It was better not to take anyone with red hair or freckles, but instead settle for a wholesome brown color.

Other animal milk was not even considered until the late 18th century, for surely if the temperament of a wet nurse could be imbibed by the breastfeeding child, imagine what characteristics the milk of a cow or goat would bring!

REFERENCES

Cone TE: Infant feeding in Europe. In: Bond et al. (eds), Infant and child feeding. New York: Academic Press, 1981.

Mixsell HR: A short history of infant feeding. Arch Pediatr 1916; 33:282--93.

Trumbach R: Mother's milk, wet nurses, and artificial foods. In: The rise of the egalitarian family. New York: Academic Press, 1978.

JEAN MAYER USDA HUMAN NUTRITION RESEARCH CENTER ON AGING (HNRCA) AT TUFTS

The U.S. Department of Agriculture's Human Nutrition Research Center on Aging at Tufts University, Boston, one of the leading research centers investigating the relationship between nutrition and well-being in the elderly, was named in memory of Jean Mayer, the late president of Tufts who was an internationally recognized nutritionist and health policy activist Dr. Mayer's words, "Nutrition is not just a science, it's an agenda," long have been a motto at Tufts and are exemplified in the work of the center researchers.

Dr. Mayer, who started waging war on hunger and poverty long before it became fashionable to do so, ws president of Tufts from 1976 to 1992, and served as the university's first chancellor until his death in 1993. He advised presidents Nixon, Ford, and Carter, and helped establish and expand the food stamp, school lunch, and other national and international nutrition programs. He advised the U.S. Congress, the United Nations' Food and Agriculture Organization, the World Health Organization, and the United Nations Children's Fund, among others.

Dr. Mayer positioned Tufts as a world-class institution in interdisciplinary approaches to fostering good nutrition, preventing famine, and addressing health issues and disease prevention worldwide. He was instrumental in establishing the nation's first graduate school of nutrition as well as the HNRCA. Shortly before he died, Dr. Mayer carried to the International Nutrition Conference in Rome his long-standing plea for an international convention to prevent the use of starvation as a military or political weapon, and to declare, once and for all, that freedom from hunger is a human right.

Established in 1980, the HNRCA is one of five national human nutrition research centers supported by the USDA's Agricultural Research Service to study the effect of nutrition on our health. More than 2,000 people each year are evaluated for admission to studies at the 15-story building in downtown Boston that houses nearly 50 research scientists and a staff of more than 200.

Some of the center's major research findings include:

* Documenting the benefits of exercise in the elderly.

* Demonstrating that vitamin C intake is positively related to high blood levels of highdensity lipoproteins.

* Identifying fat, protein, and gene markers in the blood that predict early heart disease.

* Noting that a hormonal form of vitamin D can influence skin aging.

* Finding that the skin's ability to synthesize vitamin D from sunlight decreases with age.

* Showing that a decreased ability to produce stomach acid, which occurs in at least 20 percent of the elderly, interferes with the absorption of several vitamins and minerals.

* Discovering that elderly women ingesting low levels of calcium lose minerals from the spine at a significantly greater rate than those whose intakes exceed the RDAs.

* Observing that calcium supplements, when taken with a meal, impair iron absorption.

* Showing that vitamin E may reverse age-related declines in immune responses.

REFERENCES

(1.)Mennella JA, Beauchamp GK. Maternal diet alters the sensory qualities of human milk and the nursling's behavior. Pediatrics 1991; 88:737--44.

(2.)Bassette R, Fung DYC, Mantha VR. Off-flavors in milk. CRC Crit Rev Food Sci Nutr 1986; 24:1--52.

(3.)Galef BG, Henderson PW. Mother's milk: a determinant of the feeding preferences of weaning rat pups. J Comp Physiol Psychol 1972; 78:213--19.

(4.)Campbell RG. A note on the use of feed flavour to stimulate the feed intake of weaner pigs. Anim Prod 1976; 23:417--19.

(5.)Mainardi M, Poli M, Valesecchi P. Ontogeny of dietary selection in weaning mice: effects of early experience and mother's milk. Biol Behav 1989; 14:185--94.

(6.)Nolte DL, Provenza FD. Food preferences in lambs after exposure to flavors in milk. Appl Anim Behav Sci 1991; 32:381--89.

(7.)Weunsch KL. Exposure to onion taste in mother's milk leads to enhanced preference for onion diet among weanling rats. J Gen Psychol 1978; 99:163--67.

(8.)Capretta PJ, Petersik JT, Stewart DJ. Acceptance of novel flavors is increased after early experience of diverse tastes. Nature 1975; 254:689--91.

(9.)Frye RE, Schwarz BS, Doty RL. Dose-related effects of cigarette smoking on olfactory function. JAMA 1990; 263:1233--6.

(10.)Bradley RM. Development of the taste bud and gustatory papillae in human fetuses. In: Bosma JF (ed), The third symposium on oral sensation and perception: the mouth of the infant. Spring-field, IL: Charles C Thomas, 1972:137--62.

(11.)Conel JL. The postnatal development of the human cerebral cortex: I. Cortex of the newborn. Cambridge, MA: Harvard University Press, 1939.

(12.)Liley AW. Disorders of amniotic fluid. In: Assali NS (ed), Pathophysiology of gestation: fetal placental disorders, vol. 2. New York: Academic Press, 1972:157--206.

(13.)Tatzer E, Schubert MT, Timischl W, Simbrunger G. Discrimination of taste and preference for sweet in premature babies. Early Hum Dev 1985; 12:23--30.

(14.)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; 23:179--91.

(15.)Bossey J. Development of olfactory and related structures in staged human embryos. Anat Embryol (Berlin) 1980; 161:225--36.

(16.)Menkes JH, Hurst PL, Craig JM. A new syndrome: progressive familial infantile cerebral dysfunction associated with an unusual urinary substance. Pediatrics 1954; 14:462--7.

(17.)Partington MW. The early symptoms of phenylketonuria. Pediatrics 1961; 27:465--73.

(18.)Lee CWG, Yu JS, Turner BB, Murray KE. Trimethylaminuria: fishy odors in children. N Engl J Med 1975; 295:937--8.

(19.)Hauser GJ, Chitayat D, Berbs L, Braver D, Mulbauer B. Peculiar odors in newborns and maternal prenatal ingestion of spicy foods. Eur J Pediatr 1985; 44:403.

(20.)Pritchard JA. Deglutition by normal and anencephalic fetuses. Obstet Gynecol 1965; 5:289--97.

(21.)Schaffer JP. The lateral wall of the cavum nasi in man with special reference to the various developmental stages. J Morphol 1910; 21:613--707.

(22.)Hepper PG. The amniotic fluid: an important priming role in kin recognition. Anim Behav 1987; 35:1343--6.

(23.)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. Washington, DC: US Government Printing Office, 1977:173--89.

(24.)Rosenstein D, Oster H. Differential facial responses to four basic tastes in newborns. Child Dev 1990; 59:1555--68.

(25.)Ganchrow JR, Steiner JE, Munif D. Neonatal facial expressions in response to different quality and intensities of gustatory stimuli. Infant Behav Dev 1983; 6:473--84.

(26.)Steiner JE. What the neonate can tell us about umami. In: Kawamura Y, Kare MR (eds), Umami: a basic taste. New York: Marcel Dekker, 1987:97--123.

(27.)Desor JA, Maller O, Turner RE. Preference for sweet in humans: infants, children and adults. In: Weiffenbach JM (ed), Taste and Development: The Genesis of Sweet Preference. Washington, DC: US Government Printing Office, 1977:161--72.

(28.)Desor JA, Maller O, Andrews K. Ingestive responses of human newborns to salty, sour and bitter stimuli. J Comp Physiol Psychol 1975; 89:966--70.

(29.)Crook, CK. Taste perception in the newborn infant. Infant Behav Dev 1978; 1:52--69.

(30.)Beauchamp GK, Moran MM. Dietary experience and sweet taste preference in human infants. Appetite 1982; 3:139--52.

(31.)Schaal B. Olfaction in infants and children: development and functional perspectives. Chem Senses 1988; 13:145--90.

(32.)MacFarlane AJ. Olfaction in the development of social preferences in the human neonate. Ciba Found Symp 1975; 33:103--17.

(33.)Cernoch JM, Porter RH. Recognition of maternal axillary odors by infants. Child Dev 1985; 56:1593--8.

(34.)Schaal B. Presumed olfactory exchanges between mother and neonate in humans. In: Le Camus J, Conier J (eds), Ethology and Psychology. Toulouse: Privat IEC 101--110, 1986.

(35.)Makin JIW. Bottle-feeding infants' responsiveness to lactating maternal breast and axillary odors (dissertation). Vanderbilt University, 1987.

(36.)Vasquez M, Pearson PB, Beauchamp GK. Flavor preferences in malnourished Mexican infants. Physiol Behav 1982; 28:513--9.

(37.)Beauchamp GK, Cowart BJ, Moran M. Developmental changes in salt acceptability in human infants. Dev Psychobiol 1986; 19:17--25.

(38.)Hill DL, Mistretta CM. Developmental neurobiology of salt taste sensations. Trends Neurosci 1990; 13:188--95.

(39.)Kajuira H, Cowart BJ, Beauchamp GK. Early developmental changes in bitter taste responses in human infants. Dev Psychobiol 1992; 25:375--86.

(40.)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--5.

(41.)Mennella JA, Beauchamp GK. Effects of beer on breast-fed infants. JAMA 1993; 269:1635--6.

(42.)Birch LL. Dimensions of preschool children's food preferences. J Nutri Educ 1979; 11:77--80.

(43.)Sullivan SA. Infant experience and acceptance of solid foods (dissertation). University of Illinois at Urbana-Champaign, 1992.

(44.)Taitz LS, Scholey W. Are babies more satisfied by casein based formulas? Arch Dis Child 1989; 64:619--21.

(45.)Da Mota HC. The taste of milk. Arch Dis Child 1990; 65:647.

COPYRIGHT 1994 Lippincott/Williams & Wilkins
COPYRIGHT 2004 Gale Group