4 Food, Folklore, and Flavor Preference Development
4.4 EARLY FLAVOR LEARNING .1 Amniotic Fluid
The environment in which the fetus lives, the amnion, can indeed be odorous. Its odor can indicate certain disease states, such as maple syrup disease or trimethylaminuria [36, 37]. In 1985, a case study report was published describing four infants who presented
with peculiar body odors on delivery. Although each infant tested negative for syn-dromes that are associated with peculiar body odors, all were born to women who had ingested a spicy meal (e.g., cumin, fenugreek, curry) prior to delivery [14].
In the mid-1990s, an experimental study was conducted that revealed that the diet of the mother could alter the odor of amniotic fluid in humans [38]. Amniotic samples were collected from women undergoing routine amniocentesis. The women were ran-domized to one of two groups, in which they consumed either essential oil of garlic or placebo capsules approximately 45 min prior to the amniocentesis. The amniotic fluid from a portion of the sample was then evaluated by a trained sensory panel of adults who were screened for normal olfactory functioning. The results were unequivocal. Panelists judged the odor of the amniotic fluid of the women who consumed the garlic capsules as smelling stronger and more garlic-like than the amniotic fluid samples from the women who consumed the placebos. Since odor is an important component of flavor perception, these data provided the first experimental evidence that the amniotic fluid may provide infants with their first exposure to flavors within the mothers’ diets.
That these flavor changes in amniotic fluid are perceived by fetuses and bias their preferences after birth was later demonstrated in a study conducted in Northern Ireland [39]. The response to the odor of garlic was assessed in two groups of infants: one group had mothers who consumed garlic-containing foods on a regular basis during the last month of pregnancy, whereas the other group did not. Between 15 and 24 h after birth, newborns were given a two-choice test between a cotton swab that contained garlic and an unadulterated cotton swab. The infants whose mothers consumed garlic before their birth oriented their head slightly more toward the cotton swab that smelled like garlic, whereas the infants whose mothers avoided garlic expressed their aversion for the garlic odor by orienting their heads more to the unadulterated swab than to the garlic swab.
A similar study was later conducted in France [40], but here the response to anise odors was assessed in infants whose mothers either regularly consumed anise-flavored foods and sweets, or those who did not consume anise-flavored foods. In this study, newborns of mothers who regularly consumed anise mouthed more and spent more time orienting toward a swab containing anise odor relative to the unadulterated swab and displayed fewer facial responses of distaste (e.g., brow lowering, cheek raising, nose wrinkling, gaping) toward the anise odor when compared with the infants whose mothers did not consume such flavored foods and sweets.
Taken together, these data suggest that neonates can respond positively to flavor volatiles that are experienced prenatally. However, experimental studies in which sub-jects are randomized to different treatment groups are considered the gold standard in research because they control for all extraneous variables, thereby permitting cause–effect inferences [41]. To this end, the first experimental study on how experience with flavors in amniotic fluid and mothers’ milk affects infants’ responses to these flavors is presented in the next section. But first, we review the evidence that reveals that like amniotic fluid, human milk provides the potential for a rich source of varying chemosensory experiences.
4.4.2 Breast Milk
Over the past 15 years, psychophysical research studies have revealed that like the milk of other mammals, human milk changes as a function of the dietary choices
Chapter 4 / Food, Folklore, and Flavor Preference Development 59 of the mother (for review, see [42]). Using a within-subjects design, milk samples were obtained from lactating women at fixed intervals before and after they ingested a particular food or beverage on one testing day and placebo during the other. These milk samples were placed individually in plastic squeeze bottles to minimize any vis-ual differences in the milk samples, and all possible pairs of samples were presented to trained sensory panelists who were blind to the experimental condition. Using a forced-choice procedure, the panelists were asked to indicate which bottle of the pair
“smelled stronger” or like the flavor under study. In general, panelists indicated that significant increases in the intensity of the milk odor occurred within a half hour to an hour after the mother consumed the flavor under study, with the intensity of the flavor decreasing thereafter. No such changes occurred on the days the mothers consumed the placebos. To date these psychophysical studies have revealed that a wide variety of volatiles either ingested (e.g., alcohol [43], garlic [44], vanilla [45], carrot [46]) or inhaled (i.e., tobacco [47]) by the lactating mother are transmitted to her milk.
Not only can infants detect these flavor changes in the milk, but other experimental studies revealed that they develop preferences for flavors experienced in amniotic fluid or mother’s milk [46]. Pregnant women who planned on breastfeeding their infants were randomly assigned to one of three groups. The women consumed either 300 ml of carrot juice or water for 4 days per week for three consecutive weeks during the last trimester of pregnancy and then again during the first 2 months of lactation. The mothers in one group drank carrot juice during pregnancy and water during lacta-tion, mothers in a second group drank water during pregnancy and carrot juice during lactation, whereas those in the control group drank water during both pregnancy and lactation. Approximately 4 weeks after the mothers began complementing their infants’ diet with cereal, and before they had ever been fed foods or juices containing the flavor of carrots, the infants were videotaped as they were fed, in counterbalanced order, cereal prepared with water during one test session and cereal prepared with carrot juice during another.
Similar to the results of previous studies [39, 40], infants who had exposure to the flavor of carrots in amniotic fluid behaved differently in response to that flavor in a food base than did nonexposed control infants. Specifically, previously exposed infants displayed fewer negative facial expressions while eating the carrot-fla-vored cereal when compared with the plain cereal. They were also perceived by their mothers as enjoying the carrot-flavored cereal more when compared with the plain cereal. Postnatal exposure had similar consequences, thus highlighting the importance of a varied diet for both pregnant and lactating women. These findings provide the first experimental demonstration that prenatal or postnatal exposure to a flavor enhances the acceptance and enjoyment of that flavor in a food during weaning in humans [46].
The finding of enhanced acceptance of a flavor experienced in amniotic fluid and mothers’ milk is not unique to humans, since similar findings have been observed in a wide variety of mammals such as dogs [48], rabbits [49], lambs [50], and rodents [51, 52]. The redundancy of dietary information transmitted during pregnancy and lactation may be important biologically because it provides complementary routes for the animal to learn about the types of foods available in the environment, should the mother’s diet
change between pregnancy and lactation. At weaning, young animals are faced with learning what to eat and how to forage. Exposure to dietary flavors in amniotic fluid and mother’s milk may be one of several ways that mothers teach their young what foods are “safe.” Consequently, young animals tend to choose a diet similar to that of their mothers when faced with their first solid meal. Such flavor learning is adaptive since these flavors tend to be associated with nutritious foods, or at least the foods the mother has access to, and hence they will likely be the foods to which young animals will have the earliest exposure during weaning.