10 1093@chemse@bjz011

Weanling infants prefer the odors of green vegetables, cheese and fish when their mothers
consumed these foods during pregnancy and/or lactation
Downloaded from https://academic.oup.com/chemse/advance-article-abstract/doi/10.1093/chemse/bjz011/5341973 by guest on 25 February 2019

Sandra Wagner1, Sylvie Issanchou1, Claire Chabanet1, Christine Lange1, Benoist Schaal1, Sandrine
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Monnery-Patris1
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Affiliation: 1Centre des Sciences du Goût et de l'Alimentation, AgroSup Dijon, CNRS, INRA, Université
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Bourgogne Franche-Comté, F-21000 Dijon, France.
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Correspondence to be sent to: Sandrine Monnery-Patris, Inra, Centre des Sciences du Goût et de
l’Alimentation, 17 rue Sully, BP 86510 Dijon cedex, France. email: Sandrine.Monnery-Patris@inra.fr

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© The Author(s) 2019. Published by Oxford University Press. All rights reserved. For permissions,
please e-mail: journals.permissions@oup.com
Abstract
Infants' olfactory experience begins before birth and extends after birth through milk and

complementary foods. Until now, studies on the effects of chemosensory experience in utero and/or
through human milk focused on experimentally controlled exposure to only one target food bearing
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a specific odor quality and administered in sizeable amounts. The present study aimed to assess
whether early olfactory experience effect was measurable in everyday conditions of maternal food
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intake during pregnancy and lactation, and of infant intake at weaning, leading to expose the infant
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to corresponding odors as fetus, neonate, and infant up to 8 and 12 months of age. Infants’ early
food exposures were assessed by asking mothers to fill out diaries about their food consumption
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during pregnancy and breastfeeding, and about their infant’s consumption during complementary
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feeding. To test odor liking, odorants representing a priori pleasant and unpleasant food odors, as
well as odorless stimuli, were presented. The infant’s exploratory behavior toward odorized bottles
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and non-odorized control bottles was measured in terms of mouthing duration, which is thought to
reflect attraction and/or appetence. At age 8 months only, positive correlations were found between
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liking of some unpleasant odors and early exposure to these odors through mother’s diet. No
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correlations were found between infants’ liking of the pleasant odors and early exposures to the
foods bearing these odors. This study highlights that early exposure to unpleasant food odors may
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increase subsequent liking (or reduce subsequent dislike) of these food odors at least until the age of
8 months.
Key words: Olfaction, amniotic fluid, breast milk, complementary feeding, liking, perinatal
exposure.
Introduction
In human infants, as in other mammalian infants, olfactory experience begins well before direct
exposure to solid foods and related odorous constituents (Schaal 2015, 2016). Some odor-active

compounds from the pregnant and lactating mother’s diet are indeed transferred into the prenatal
environment and into mother's milk (Hauser et al. 1985; Mennella 1995; Mennella and Beauchamp
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1999; Mennella et al. 1995). Such olfactory cues passing the placenta are detectable by the fetus
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(Marlier et al. 2001; Schaal 2015) as they subsequently influence the newborns’ reactions to
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corresponding odor in aerial conditions of stimulation (Hepper 1995; Schaal et al. 2000). For instance,
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human fetuses born to mothers who have eaten anise-flavored foods exhibit after birth higher
appetence and attraction to the odor of anethole than non-exposed infants (Schaal et al. 2000).
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Similarly, odorants transferred from the mothers’ diet to her breast milk are detected by infants and
influence their suckling behavior (Mennella and Beauchamp 1991a, b; 1993 a, b; 1996, 1999). The
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effect of early experience also extends to the period of weaning or complementary feeding when
infants begin to be directly exposed to solid foods. For example, infants whose mothers drank carrot
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juice during pregnancy or breastfeeding exhibit fewer negative facial responses than unexposed
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infants when they were fed cereals prepared with carrot juice than when they were fed cereals
prepared with water (Mennella et al. 2001). Prenatal odor experience has been shown to influence
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behavior even after several years; thus, 8 to 9 year-old children whose mothers consumed garlic
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during pregnancy eat significantly more garlic-flavored potato purée than non-exposed children
(Hepper et al. 2013). Early odor experience during milk-feeding has also been shown to influence
odor selectivity for more than one year (Delaunay-El Allam et al. 2010) and even into adulthood (e.g.,
Haller et al. 1999).
Food-related odors are known to be important drivers of food liking and consumption in adults
(Engel et al. 2006; Font-i-Furnols 2012; Jaeger et al. 2012) and, before, during, and after actual
ingestion, they provoke a cascade of psychophysiological and metabolic responses (Mattes 1997;
Yeomans 2006). Thus, olfaction may have a rather essential role in the control of the appetence and
intake dimensions of eating behavior. Converging results exist in children and infants. For example,
food neophobia is more a matter of olfactory reactivity than of taste reactivity, suggesting that the
appreciation and rejection of unfamiliar foods, which is common in children and infants, may be

prevalently caused by odor cues (Monnery-Patris et al. 2015). Therefore, it is relevant to better
understand how and when early experience with food-related odorants in the pre-weaning (amniotic
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and lacteal) environment influences the appetitive value of odors conveyed in solid foods.
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The aim of the present study was to investigate the relative influence of exposure in the early
succession of niches constituted by the amniotic, lacteal, and the initial post-lacteal food
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environments on the liking of food-related odor in 8 and 12 month-old French infants. In France, 100
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% of infants aged on average 8 months have been repeatedly exposed to foods other than human
and/or formula milks (Turberg-Romain et al. 2007). By age 12 months, the infants’ food repertoire
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has begun to progressively shift from baby foods to table foods (Briefel et al. 2004). Thus, 8 and 12
months can be considered as key ages for the establishment of the food repertoire.
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The couple of previous studies focusing on the prenatal shaping of odor liking assessed
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subsequent effects in the very short term of several hours or days (Hepper 1995; Schaal et al. 2000).
The present study aimed to investigate longer-term effects in attempting to assess whether such
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early exposure effects occur in conditions where the infants are introduced to a wide panel of foods
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that characterizes the culture of their parents. Most studies investigating early odor or flavor
exposure required indeed that participant pregnant or lactating mothers ingest one specific food in
consequent amounts [e.g., 300 mL of carrot juice 4 days/week during 3 weeks (Mennella et al. 2001);
75 g of hummus with 30 mg d-carvone every third day over a period of 28 days (Hausner et al.
2010)]. The originality of the present study was thus to evaluate the consequence of early odor
exposure on the infant through the mothers’ spontaneous consumption of a wide spectrum of foods,
without inducing them to consume any specific foods bearing a given dominant odor. Spontaneous
diets were recorded during late pregnancy and lactation and for the infant, during the first months of
diversified feeding. Early exposure to given odor qualities was inferred from the foods eaten by
mothers (late fetal and lacteal periods) or infants (early post-lacteal period). When the infants were 8
and 12 months of age, their responses to different odor qualities conveyed by several categories of

foods were measured to evaluate the magnitude of odor exposure on their hedonic responses to
related odors.
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Because previous studies suggest positive effects of early odor exposure on later odor
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liking in infants (Hepper 1995; Mennella et al. 2001; Schaal 2016; Schaal et al. 2000), we
hypothesized that the more frequently infants were exposed to the target olfactory stimuli
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during the three periods described above, the higher their subsequent liking of
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corresponding odors.
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Experimental
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Participants
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The present data were collected in the context of the ‘Observatory of Food preferences in Infants
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and Children’ (OPALINE study), which aims to understand the formation of food preferences from
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birth up to 2 years of age. Participating mothers were recruited before or during the last trimester of
pregnancy using leaflets left at health professionals and in daycare centers. To be included in the
cohort, both parents had to be older than 18 years (legal age of majority), and their infant had to be
void of any previous medical complication.
The aims and methods of the study were explained to both parents in great detail, after which
they gave their written informed consent. The study was conducted in accordance with the
Declaration of Helsinki for human experimentation and was approved by the local ethics committee
(Comité Consultatif de Protection des Personnes dans la Recherche Biomédicale de Bourgogne).
Mother-infant dyads (n=235) participated in olfactory testing when the infants were 8 and 12

months old (at the mean ages (± SD) of 239 ± 13 days, and 372 ± 12 days, respectively). The mothers
had a mean age (± SD) of 32 ± 4 years when infants where 8 months old. The infants were devoid of
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any oro-nasal affections (cold or allergy) at the time of the tests. Only the infants for whom mothers
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provided complete information on their diet during pregnancy and breastfeeding, and on their
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infant’s diet during complementary feeding, were entered into the analyses. Thus, the data set
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included data of 100 mother-infant dyads at the infants’ age of 8 months. Their demographic
characteristics are described in Table 1. Complete data were available at 12 months for 71 of these
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100 mother-infant dyads.
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Measurement of infants’ odor liking

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Odor stimuli
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The stimuli consisted of 8 odorants selected to represent diverse food qualities. Based on previous
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literature on early odor preferences (Wagner et al. 2013), 4 odorants were selected to represent
foods considered a priori as pleasant (strawberry, peach/apricot, apple, and vanilla), and 4 odorants
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represented foods considered a priori as unpleasant (2-isobutyl-3-methoxypyrazine, trimethylamine,
dimethyl disulfide, butyric acid) [see Table 2 for the correspondence between odorants and
associated foods]. Control stimuli consisted of mineral oil. All the stimuli were soaked in 11 x 5 cm
strips of scentless absorbent (3M, Liège, Belgium) placed in the bottom of nipple-less, transparent
infant-ergonomic bottles (12 x 6 cm, opening diameter of 2.3 cm; Tex, Carrefour, France).
Procedure of the olfactory tests
The procedure of the olfactory tests, which is described in full details elsewhere (Wagner et al. 2013),
is only summarized here. Infants were individually welcomed in the presence of one parent in a

laboratory room dedicated to infant testing. To control for the infants’ hunger state, parents were
asked not to feed them 1.5 hour before the visit to the lab. Parents’ compliance with this instruction
was checked before the beginning of the testing session by asking when they last fed their infant. To
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accustom the infants to the room and experimenters, a familiarization phase took place before
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engaging the tests.
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For the tests themselves, the infants were exposed to 4 series of 3 test-bottles, sequentially
ordered to present them a scentless control, a pleasant, and an unpleasant odor (Wagner et al.
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2013). This order of presentation was chosen to avoid the infant refusing to pursue the test after
smelling first an unpleasant odor as was noted in previous studies (Schmidt and Beauchamp 1988)
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and in our own pilot tests. Exposure to a bottle meant that a given bottle was put under the nose of
the infant during 5 s and then placed on the table in front of the infant who was left free to explore it
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by any means. Within series of bottle triplets, bottles were presented separately during 60 s with a
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15-s interval between bottles. Between each series of bottle triplets, we managed a 5- to 15-min
break.
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Behavioral analyses and odor-liking scores
All odor tests were videotaped for subsequent analysis of the infants’ spontaneous exploratory
behavior toward the bottles. We focused on “mouthing” behavior, which was previously shown to be
a reliable indicator of hedonic discrimination in infants within the age range considered (Delaunay-El
Allam et al. 2010; Mennella and Beauchamp 1998; Soussignan et al. 1997). Mouthing behavior was
defined as direct contact between the infant’s perioral and/or perinasal areas with the opening of
the bottle. The videos were analyzed frame-by-frame with the Observer software (Noldus,
Wageningen, The Netherlands) by trained observers who were blind to the nature of the odor
conveyed by the bottle. Ten video sequences were randomly selected to check inter-observer
reliability in coding mouthing behavior. The average percentage of agreement was higher than 0.90.

When relevant, mouthing duration was corrected by the duration of inaccessibility of the bottle (for
example, if dropped onto the floor).
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The analysis was restricted to the infants who mouthed the bottles for a combined total duration of
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at least 10 seconds. Thus, the data corresponding to 10 infants at 8 months of age and to 7 infants at
12 months of age were not considered.
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For each test odorant, mouthing duration was converted into an odor liking score. These scores were
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defined as the ratio between mouthing duration for the odorized bottle and the sum of mouthing
durations for the odorized bottle and corresponding control bottle in a triplet. Whereas a score of 0.5
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indicates indifference for the odorant, a score higher than 0.5 indicates attraction and a score lower
than 0.5 indicates avoidance of the odorant compared to the control.

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Recording of dietary data for deriving of odor exposure data

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Mothers were asked to fill out food diaries during pregnancy, breastfeeding, and the period of infant
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complementary feeding. The diaries were organized by day (for 7 consecutive days) and by meal. A
very detailed description of the meal was required to allow a precise characterization of odor, taste
and flavor of the food items composing each meal. Mothers were also asked to give details about the
ingredients and seasonings for home-made preparations and to provide the label with the list of
ingredients for commercial dishes (Lange et al. 2007). The instructions were detailed to the mothers
during individual sessions, and the diaries included written instructions with examples.
Maternal diet during pregnancy and breastfeeding
Mothers had to indicate in a qualitative way all the food or beverage items they consumed each day
during one week of the 8th gestational month, and during the 4 weeks of the last gestational month

(depending on the infant’s gestational age at birth, there were records for 1 to 4 weeks). The
mothers also completed such diaries daily during one week per month during the breastfeeding
period. For the analyses, we considered first the breastfeeding period from birth to 7 months in
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order to take into account all exposures up to the first olfactory test at 8 months; then we considered
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the breastfeeding period from birth to 11 months included, to take into account all exposures up to
the second olfactory test at 12 months. For the infants who were not breastfed, the breastfeeding
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exposure was set to 0.
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Infant diet during complementary feeding
The mothers were asked to complete diaries daily about their infants’ qualitative consumption of
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foods during one week per month. As the olfactory tests occurred at 8 and 12 months of age, we
derived the food exposure data from two periods: the target infant’s beginning of complementary
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feeding (as decided and reported by the mother) to 7 months, and then from the beginning of
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complementary feeding to 11 months.

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Selection of food items for deriving infant odor exposure
The frequency at which each infant was exposed to given odorants over the three periods studied
was derived from the mothers’ and infants’ dietary diaries. We extracted from these diaries all food
items carrying dominant odor qualities corresponding to the test odorants. The number of
consumption occurrences was calculated from the mothers’ diaries for each food category and each
period (pregnancy and breastfeeding). The number of occurrences of infants’ direct exposure to
given food odor stimuli was inferred for each food category from the infants’ ingestion of non-milk
foods.

For the odorants characteristic of apple, strawberry, peach/apricot and vanilla, all food items
composed of apple, strawberry, peach, apricot or vanilla or related artificial aromas were selected
from the diaries. For the other odorants, three chemical data bases of volatile compounds were
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systematically screened to assess their presence in food items reported in the diaries: the Flavor-
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Base© 2010 (http://www.leffingwell.com), the VCF Database 14.1 available through TNO Triskelion
(VCF Volatile Compounds in Food), and the CSGA odor database. Each test odorant was associated
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with one food category, except for dimethyl disulfide that was associated with two food categories.
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The correspondences between the test odorants and the food items containing them used for infant
exposure inference are presented in Table 2.

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Statistical analyses
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The statistical analyses were carried out using the R software version 3.0.1.
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Odor liking
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At each time point, we calculated the individual median odor liking scores for pleasant odors and for
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unpleasant odors. A paired Wilcoxon test was performed to assess whether the median odor liking
scores were significantly different between a priori unpleasant and a priori pleasant odors. Kendall
correlations were calculated to assess whether odor liking scores at 8 and 12 months were
correlated. As positive correlations were expected based on previous studies, unilateral tests were
performed.
Mothers’ food consumption during pregnancy and breastfeeding
Friedman tests were performed to assess whether there were significant differences of
consumptions between the food categories; when the Friedman test was significant Wilcoxon test

for paired data with Bonferroni corrections were performed to compare the different food categories
two by two. To assess the continuity of food consumption during pregnancy and breastfeeding,
Kendall correlations were calculated between the consumption of each food category during
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pregnancy and during breastfeeding. As positive correlations were expected, unilateral tests were
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performed.
Relationships between odor liking and early exposures

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The relationships between early exposures during each period and odor liking scores of the related
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odorant at 8 months (and 12 months) were assessed by calculating Kendall correlations. The
relationships were also assessed for the cumulative periods of exposure, i.e., prenatal plus lactational
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and, prenatal plus lactational and complementary feeding. According to our hypothesis, positive
correlations were expected between early exposure and odor liking score, justifying the use of
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unilateral tests.
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Results
Liking of food odors
The bottles containing odorants considered as unpleasant were mouthed for marginally shorter
durations than the bottles containing pleasant odorants at 8 months [P = 0.09 – median (Q1-Q3) for
pleasant/unpleasant stimuli were: 0.41 (0.26-0.55)/ 0.39 (0.08-0.51)] and at 12 months, even if the
difference was not significant (P = 0.11), the duration of mouthing [median (Q1-Q3)] for the a priori
pleasant odors was 0.45 (0.18-0.53) versus 0.35 (0.24-0.47) for the a priori unpleasant odors.
For the 71 infants for which data were available at 8 and 12 months, their individual liking scores for

all odorants at the two age points were not correlated (all P-values > 0.11).
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Food items consumed during pregnancy and breastfeeding
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The occurrences of mothers’ consumption differed between the target food categories during
pregnancy (Friedman = 452.7, p<0.0001) and during breastfeeding (Friedman = 452.8, p<0.0001). The
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mothers’ most consumed food category (Figure 1A) during pregnancy was “apple products”
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(occurrence: median, Q1, Q3 = 33.5, 21, 47), whereas “vanilla desserts” was one of the least
consumed food categories (occurrence: median, Q1, Q3 = 6, 2, 11). During breastfeeding, a similar
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pattern was found (Figure 1B): the most consumed food category were “apple products”
(occurrence: median, Q1, Q3 = 20.5, 4, 48.5), while “strawberry products” (occurrence: median, Q1,
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Q3 = 3, 0, 9.5), “vanilla desserts” (occurrence: median, Q1, Q3 = 4, 0, 9.25) and “sulfurous cheeses”
(occurrence: median, Q1, Q3 = 4, 0, 10) were amongst the least consumed food categories. It is
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worth noting that consumption patterns during pregnancy and breastfeeding were weakly but
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significantly correlated for each food category (Kendall correlations between 0.16 and 0.34, all P-
values < 0.01), suggesting a qualitative consistency in mothers’ consumption during pregnancy and
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the postpartum period.
[insert Fig. 1 about here]

Food exposures during complementary feeding
The occurrences of infants’ consumption differed between the target food categories from the
beginning of complementary feeding (which is variable and depends on the mother’s decision) to 7

months (Friedman = 392.9, P < 0.0001) and to 11 months (Friedman = 408.0, P < 0.0001). From the
beginning of complementary feeding to 7 months, the food categories studied were introduced to at
least 25% of the infants, except for fish, sulfurous cheeses and butyric cheeses, which were only
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introduced to 9, 2 and 6 infants, respectively. Among the other food categories considered here
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(Figure 2A), the infants were the most exposed to “apple products” [occurrence: median (Q1-Q3) = 6
(3-12)], and the least exposed to “vanilla desserts” [occurrence: median (Q1-Q3) = 0 (0-1)]. From the
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beginning of complementary feeding to 11 months (Figure 2B), all the food categories studied were
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introduced to at least 89% of infants. Infants were the most exposed to “apple products”
[occurrence: median (Q1-Q3) = 27 (17.5-32)], and the least exposed to sulfurous and butyric cheeses
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[occurrence: median (Q1-Q3) = 0 (0-0) for both categories) and to fish (occurrence: median (Q1-Q3) =
0 (0-0.5)].
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[insert Fig. 2 about here]

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Relationships between early exposures and subsequent odor liking
Relationships between in utero exposure and subsequent odor liking
At 8 months, infants whose mothers reported eating more green vegetables during pregnancy
displayed higher liking scores for the corresponding odorant (Table 3). Additionally, in utero exposure
to sulfurous cheese odor led to a marginally significant correlation with the odor liking score for
dimethyl disulfide odor at 8 months. No significant correlations were found between in utero
exposures and the corresponding odor liking scores at 12 months (Table 4).
Relationships between breastfeeding exposure and subsequent odor liking

Infants whose mothers reported eating more green vegetables during their breastfeeding period
displayed a higher liking of the corresponding odor at 8 months (Table 3). Additionally, exposure to
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fish odor during breastfeeding led to a marginally significant correlation with the odor liking score for
trimethylamine odor at 8 months. No significant correlations were found between exposures during
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breastfeeding and the corresponding odor liking scores at 12 months (Table 4).
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Relationships between complementary feeding exposure and subsequent odor liking
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Direct exposures of infants to the real foods during complementary feeding were not correlated with
odor liking scores at 8 or 12 months (Tables 3 and 4).

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Relationships between the cumulative periods of exposure and subsequent odor liking
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Exposure to green vegetables odor during the perinatal period (i.e., cumulating exposures in utero
and during breastfeeding) led to a significant correlation with green vegetables odor liking score at 8
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months (tau = 0.28, P <0.001). A significant correlation was also found for this odor when we
considered cumulative exposures during the perinatal period and complementary feeding (tau =
0.27, P <0.001).
Regarding the other odors, no significant correlations were found between the perinatal exposure or
the cumulated exposures over the perinatal and complementary feeding periods and the
corresponding odor liking scores at 12 months.

Discussion
This study aimed to assess longitudinally the association between early exposure to specific dietary

odorants, inferred from the diet consumed spontaneously by the pregnant-lactating mother and by
the weanling infant, and subsequent liking of these odors. The relationship between maternal food
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consumption during pregnancy and breastfeeding and her infant’s subsequent liking for
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corresponding odors was based on the assumption that odorous compounds of the mother’s diet are
transferred to the fetus through the placenta and to the nursling through milk. Based on previous
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studies on human fetuses and neonates (Hepper 1995; Mennella et al. 2001; Schaal et al. 2000), we
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hypothesized that the perinatal olfactory experience linked with the mother’s ingestion of a given
food leads to higher liking for related food odors at a later age.
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In the conditions of the present study, such exposure-liking relationships were found significant
only for unpleasant odor qualities, and only at 8 months. Prenatal or lactational exposure to foods
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bearing unpleasant odors was associated with increased liking (or reduced disliking) responses of
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related odorants. However, similar odor exposure-liking relationships did not reach significance when
the food exposure occurred during complementary feeding. Importantly, no relationships were
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found between exposures to foods bearing pleasant odor qualities and the liking of related odors.
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Thus, the present study brought only partial support to the hypothesis that early olfactory
experience would lead to an enhanced liking of a related odor separately from the context of the
entire food flavor.

In utero and breastfeeding exposures in relation with odor liking at 8 months
No significant relationships were uncovered between the mothers’ gestational and lactational
consumption frequency of foods carrying pleasant odors and the infants’ later liking for the pleasant
odors at 8 and 12 months of age. Three out of the 4 pleasant odorants considered in the present
study conveyed fruity odors. The rate of trans-placental and mammary transfer of compounds

carrying fruity notes has not yet been systematically analyzed, although isolated evidence indicates
that a fruity-smelling ester is only weakly traced into human milk (Hausner et al. 2008). Nevertheless,
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one study indicated that 4 to 8 month-old infants express higher acceptance of peaches when they
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have been breastfed (as opposed to formula-fed), the authors explaining this result by the fruit-rich
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diet of breastfeeding mothers in their study (Forestell and Mennella 2007).
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By contrast, prenatal exposure to odorants characteristic of green vegetables positively
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influenced the infants’ liking of the corresponding unpleasant odor at 8 months. A similar significant
positive correlation was noted with lactational exposure to green vegetable odorants, and so was it
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when the cumulative perinatal exposure (in utero and during breastfeeding) was considered. The
compound used here to represent green vegetable odor, 2-isobutyl-3-methoxypyrazine, has been
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found in human milk although without controlling whether the mothers effectively ingested green
vegetables (Buettner 2007). Our results are inconsistent with the results of Forestell and Mennella
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(2007). They found no clear evidence for any influence of lactating mothers’ consumption of green
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beans on infants’ acceptance of this vegetable at the time of complementary feeding and explained
their results by the low rate of consumption of green beans by the mothers and the fact that being
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exposed to the odor is not sufficient.
Other significantly positive exposure/liking relationships were reached in the present study for
sulfurous cheeses and for fish, but only when infants’ liking of the corresponding odors was assessed
at 8 months. The exposure to cheese was linked with ensuing liking for the cheesy odor dimethyl
disulfide only when the mother consumed cheese while pregnant. Similarly, a liking for the fishy odor
trimethylamine only emerged after maternal ingestion of fish during the breastfeeding period. To our
knowledge, the odorant related to sulfurous cheeses, namely dimethyl disulfide, has not been
identified in amniotic fluid, or in human milk after the ingestion of raw garlic by mothers (Scheffler et
al. 2016). However, these authors identified several garlic-derived metabolites, one of which (allyl
methyl sulfide) having a pronounced garlic-like odor. Trimethylamine, the compound used here to

represent fish odor, was found in both amniotic fluid and milk (Lichtenberger et al. 1991).
Despite the fact that food intakes by the mothers during pregnancy and breastfeeding were
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correlated, the highlighted relationships regarding the two periods of early exposures do not concern
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the same foods. Moreover, when considering the cumulative exposure over the in utero and
breastfeeding periods, no relationships were noted for fish or sulfurous cheeses. This raises the
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question of potentially variable rates of transfer of dietary odorants or their metabolites through the
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placenta and the mammary systems, of differential solvent properties of amniotic fluid and milk for
various odor-active compounds, and/or of heterogeneous consequences of chemosensory exposure

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during earliest phases of development of the olfactory tract.

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Relationships between exposures during complementary feeding and odor liking at 8 months
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In the present conditions, no significant associations were found between food exposures during
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complementary feeding and odor liking at 8 months. Thus, the most recent olfactory exposure
through direct feeding does not appear to be the strongest determinant of infants’ odor liking. For
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fish, sulfurous cheeses and butyric cheeses, it may be explained by the fact that these 3 food
categories were introduced to less than 10 infants. For the other food categories, one possibility
might be that the time elapsed between the last food exposures and the olfactory test was too short.
Previous studies suggest indeed that a time interval of less than 4 days between the end of exposure
and the test can affect food acceptance score negatively, by the hypothetical effect of sensory
specific satiety or sensory boredom (Mennella and Beauchamp 1999; Mennella et al. 2006).
Absence of relationships between early exposures and odor liking at 12 months
At 12 months, the relationships between food exposures during the different periods considered in

our study (prenatal, breastfeeding, complementary feeding) and ensuing odor liking by infants
appeared to weaken or to vanish. Several explanations may be proposed for this result. First, the
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method used to gauge odor liking may be less adequate in 12 month-olds than in 8 month-olds who
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just begun the transition to post-lacteal foods and, hence, remain more reliably demonstrative in
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their behavior toward the test-bottles. Nevertheless, this explanation is unlikely since the infants
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differentiated pleasant and unpleasant stimuli similarly at 12 months and at 8 months. Second, the
effect of exposures during the prenatal period or during the breastfeeding period may be limited in
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time. This is supported by studies showing that breastfeeding exposure confers an initial advantage
on food acceptance during complementary feeding, but this advantage wanes when other ways
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enabling infants to experience flavors operate, such as the direct, repeated exposure to the dietary
flavors (Hausner et al. 2010; Maier et al. 2007) without presumable attenuation by maternal and/or
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fetal metabolism. Moreover, there is another study finding that the effect of early exposure on
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infants’ preferences for basic tastes was evident in younger children still eating baby foods but was
no longer evident in older children who have started to be offered table foods (Mennella et al. 2009).
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Third, as noted above, phenomena of sensory specific satiety or of sensory boredom could explain
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the absence of effect between the most recent exposure to complementary feeding foods and liking
responses to corresponding odors. Finally, in studies demonstrating lengthily persisting effects of
olfactory experience in utero or during breastfeeding (Delaunay-El Allam et al. 2010; Hepper et al.
2013; Mennella et al. 2001), the amount of exposure by the mothers was controlled and relatively
high (Mennella et al. 2001). Therefore, it is possible that the persistent effects of early exposure are
only found after a long and repeated exposure to specific and relatively intense odorants.
The fact that significant relationships were found only between very early exposure to given food
odorants, namely, in utero and breastfeeding, and odor liking at 8 months may point to a sensitive
period for the encoding of concurrent odors or flavors. These results are in line with previous
experimental studies which demonstrated that the last weeks of pregnancy, as well as the first weeks

of the breastfeeding period (Mennella et al. 2001), are optimal for the perception and long term
memorization of chemosensory cues (Delaunay-El Allam et al. 2010; Hepper 1995; Hepper et al.
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2013; Schaal et al. 2000).
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Limitations of the study
The findings of this study should be interpreted in light of potential limitations. The prenatal and
an
breast milk exposures to the different target odorants were inferred from the spontaneous food
M
intake reported by mothers during pregnancy and breastfeeding, respectively. This study is
composed of a first phase of unsupervised odor/flavor exposure recording by mothers and a second
ed
phase of measurement of ensuing effects in infants. Thus, no causality can be inferred and other
non-controlled factors might account for the observed relationships. For example, a genetic
pt
predisposition of the parents could have been transmitted to their infant and could have influenced
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infant odor liking. It is also known that the transfer of volatile compounds of mothers’ diet to the
amniotic fluid or breast milk may differ between compounds and between mothers (Hausner et al.
Ac
2008; Schaal 2005) and this could explain that different associations were found for the exposure in
utero and during breastfeeding. However, considering the number of mothers who participated in
the study, it would not have been possible to analyze the composition in volatile compounds in the
breast milk of each mother during the whole breastfeeding period, and analyzing the amniotic fluid
composition was not at all possible. During the complementary feeding period, odor exposures were
inferred from the occurrences of consumption because mothers were not asked to report the
quantities of the different foods eaten by the infants. However, one may wonder which parameter
(number of occurrences, frequency, intensity of each exposure) is the most significant to describe the
effect of olfactory exposure on odor liking. Otherwise, despite some limitations of the olfactory test,
such as presentation in triplet which are discussed elsewhere (Wagner et al. 2013), the strength of
the present study lays in the recording of the usual food intake of a large range of foodstuffs by

mothers in the last months of pregnancy or while breastfeeding, and for the infants during the
complementary feeding period, followed by an experiment conducted with a quite large number of
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infants.
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In conclusion, the present study highlights a positive association of prenatal and postnatal
olfactory exposure and enhanced liking, or reduced disliking, of odors later in life. Specifically, early
an
chemosensory exposures to green vegetables, sulfurous cheeses, and fish in utero and/or during
breastfeeding correlate positively with responses indicating acceptance of related dominant odors at
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the beginning of complementary feeding. From a practical point of view, our work is important
regarding the long-term persistence of perinatal odor impressions and the transmission of food
ed
culture. Further, it gives new highlights to promote the early exposure and acceptance of foods
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recommended for their health benefits (e.g., Anzman-Frasca et al. 2018).

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Funding
This work was supported by the Conseil Régional Bourgogne, Franche-Comté (PARI grant) and the
FEDER (European Funding for Regional Economic Development), the Institut Fédératif de Recherche
92, and the Agence Nationale de la Recherche under the ‘Programme National de Recherche en
Alimentation et Nutrition Humaine’ (project ANR-06-PNRA-028, OPALINE). The present study,
labelled by Vitagora® (The Taste, Nutrition and Health Innovation Pole), was also supported by grants
from Blédina, Nestlé, Symrise and Cedus. The present work was part of a PhD work (S. Wagner)
supported by a grant funded by the Nutrition, Chemical Food Safety and Consumer Behavior Division
of INRA (the French National Institute for Agronomical Research) and the Conseil Régional
Bourgogne, Franche-Comté.

Acknowledgements
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The authors wish to thank the infants and parents who took part in the present study, and also C.
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Laval for recruitment, A.Vincent, A. Fornerol, R. Bouhalassa, E. Szleper, J. Pierard, V. Feyen, F. Durey;
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V. De Anfrasio for the odor liking data collection; C. Gulluscio for behavioral analyses; S. Jacob and S.
Crevoisier for the food liking data collection; and the whole OPALINE team for support and advice.
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The authors thank Symrise, IFF and Firmenich for graciously providing the odorants.
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Table 1. Characteristics of mothers and infants (n=100)
Infants
Gender (N girl / N boy) 42 / 58

Feeding mode at birth (N)*
Exclusive bottle-feeding 12
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Exclusive breastfeeding 81
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Bottle- and breastfeeding 5
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Duration of exclusive breastfeeding (days; mean ± SD) 90 ± 60
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Duration of total breastfeeding (days; mean ± SD) 170 ± 152
Age at onset of complementary feeding (days; mean ± 164 ± 27

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SD)
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*This information is missing for 2 infants.

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Table 2. Correspondences between the qualities of the test odorants and the foods conveying similar
qualities
Test odorant Food category Foods given to infants
Food items containing vanillin, such as

a
Vanillin Vanilla desserts vanilla cakes or cookies, vanilla dairy
products

Apple, Food items containing apple,
b
Apple Apple products such as apple compote or apple pie,
apple juice
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Peach, Apricot, Food items containing
c Peach or apricot
Peach/apricot peach or apricot, such as peach cake or
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products
apricot pie, peach/apricot juice
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Strawberry, Food items containing
d
Strawberry Strawberry products strawberry, such as strawberry yoghurt
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or pie, strawberry syrup
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Dried cod, whitefish, herring in oil, dog

d fish, fresh salmon, tuna, sardine,
Trimethylamine Fish
mackerel, fish soup, shellfish, sea shell,
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breaded fish
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Raclette, Emmental, Gruyère, Comté,

Beaufort, Mont d'or, Saint Marcellin,
Camembert, Brie, Cantal, Morbier,
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a
Butyric acid Butyric cheeses Tomme, Saint Nectaire, Munster,
Epoisses, blue cheese, Cancoillotte,
 
sheep cheese, Bonbel , Babybel , Port
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
Salut
Garlic and chives cheese, Cancoillotte,

d
Dimethyl disulfide Sulfurous cheeses Camembert, Munster, Epoisses, blue
cheese
Broccoli, cabbage, cauliflower, Brussels

d
Dimethyl disulfide Sulfurous vegetables sprouts, leek, chive, garlic, onion,
shallot, capers
a
2-isobutyl-3-methoxypyrazine Green vegetables Green pepper, green bean, salad, peas
a
Purchased from Sigma-Aldrich, Saint Quentin Fallavier, France; b provided by Firmenich, Geneva, Switzerland; c provided by IFF, Dijon, France;
d
provided by Symrise, Clichy la Garenne, France.

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Table 3. Kendall correlations (unilateral tests) between odor liking scores for each odorant at 8 months and early exposures to the corresponding odors

(significant correlations are shown in bold).
Odorants Food Infants* Liking score** Pregnancy Breastfeeding Complementary
category
feeding
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Medians τ P τ P τ P
(Q1-Q3) value value value
Odors considered a priori as unpleasant
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Trimethylamine Fish 72 0.51 (0.33-0.67) -0.09 0.85 0.12 0.07 -0.15 0.93
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Butyric acid Cheeses 79 0.39 (0-0.71) 0.04 0.31 -0.02 0.61 -0.07 0.76
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Dimethyl disulfide Sulfurous 0.12 0.06 -0.04 0.71 -0.06 0.75
cheeses
81 0.41 (0.13-0.64)
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Dimethyl disulfide Sulfurous -0.01 0.54 -0.12 0.94 -0.12 0.91
vegetables
2-isobutyl-3- Green 79 0.51 (0.33-0.81) 0.30 <0.001 0.16 0.02 -0.07 0.79
methoxypyrazine vegetables
Odors considered a priori as pleasant

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Vanillin Vanilla 86 0.51 (0.28-0.72) 0.09 0.11 -0.05 0.73 -0.03 0.64
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Apple Apple 77 0.54 (0.32-0.74) 0.07 0.18 0.05 0.28 -0.06 0.76
Peach/apricot Peach/apricot 75 0.54 (0.28-0.75) -0.04 0.69 -0.05 0.72 0.06 0.23
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Strawberry Strawberry 76 0.48 (0.19-0.67) 0.07 0.18 0.03 0.36 0.002 0.49
*The number of infants varied between 72 and 86 because, in some cases, infants did not complete the olfactory test because they became fussy during the session, thus
data were missing for some odorants.

** A score of 0.5 indicates indifference for the odorant, a score higher than 0.5 indicates attraction and a score lower than 0.5 indicates avoidance of the odorant compared
to the control. Here, none of liking scores was significantly different from 0.5.
Table 4. Kendall correlations (unilateral tests) between odor liking scores for each odorant at 12 months and early exposures to the corresponding odors

(Statistically significant results are shown in bold).
Odorants Food Infants* Liking score** Pregnancy Breastfeeding Complementary
category
feeding
Medians (Q1-Q3) τ P τ P τ P
value value value
Odors considered a priori as unpleasant
Trimethylamine Fish 52 0.43 (0.12-0.57) 0.11 0.12 -0.04 0.67 0.08 0.23
Butyric acid Cheeses 58 0.42 (0.25-0.64) 0.07 0.23 -0.001 0.50 -0.11 0.85
Dimethyl disulfide Sulfurous -0.13 0.92 -0.17 0.96 -0.10 0.83

cheeses
Dimethyl disulfide Sulfurous 58 0.40 (0.12-0.6 -0.22 0.99 -0.26 0.99 -0.05 0.69
vegetables
2-isobutyl-3- Green 60 0.50 (0.18-0.82) -0.17 0.97 -0.01 0.56 -0.17 0.96
methoxypyrazine vegetables
Odors considered a priori as pleasant
Vanillin Vanilla 58 0.48 (0.26-0.69) 0.07 0.22 -0.16 0.95 -0.04 0.65
Apple Apple 60 0.49 (0.32-0.79) 0.02 0.40 -0.09 0.85 -0.02 0.59
Peach/apricot Peach/apricot 60 0.46 (0.21-0.67) 0.07 0.21 -0.01 0.54 0.08 0.20
Strawberry Strawberry 59 0.49 (0.29-0.74) -0.11 0.89 0.06 0.26 -0.06 0.75
*The number of infants varied between 52 and 60 because, in some cases, infants did not complete the olfactory test because they became fussy during the session, thus
data were missing for some odorants.

** A score of 0.5 indicates indifference for the odorant, a score higher than 0.5 indicates attraction and a score lower than 0.5 indicates avoidance of the odorant compared
to the control. Here, none of liking scores was significantly different from 0.5.
Titles and legends for the figures
Fig. 1. Box-plots depicting the number of occurrences of mothers’ consumption for the different

target food categories during the 2 last months of pregnancy from which infants’ in utero exposure to
odorant stimuli were inferred (A) and during breastfeeding from which infants’ exposure to odorant
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stimuli through human milk were inferred (B). For each box-plot, the bottom and the top of the box
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represent respectively the 25th and 75th percentiles and the line within the box the median. The 95%
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confidence intervals of the medians are represented. The food categories with a different letter have
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significant different medians (paired Wilcoxon tests with Bonferroni correction, P < 0.05).
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Fig. 2. Box-plots depicting food exposures between the beginning of complementary feeding and 7
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months (A) and between the beginning of complementary feeding and 11 months (B). The 95%
confidence intervals of the medians are represented. The food categories with a different letter have
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significant different medians (paired Wilcoxon tests with Bonferroni correction, P < 0.05).
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Figure 1
A B

Vanilla desserts d d
Apple products a a
Peach/apricot products b d
Strawberry products d d
Fish d d
Butyric cheeses c b a
Sulfurous cheeses d d
Sulfurous vegetables c b b
Green vegetables c c
0 20 40 60 80 100 0 20 40 60 80 100 120

Number of occurrences of Number of occurrences of
consumption during pregnancy consumption during breastfeeding
Figure 2
A B
Vanilla desserts c d

Apple products a a
Peach/apricot products b b
Strawberry products c c
Fish d e
Butyric cheeses d e
Sulfurous cheeses d e
Sulfurous vegetables c dc
Green vegetables b c b
0 5 10 15 20 25 30 0 10 20 30 40 50 60
Number of occurrences of exposure between Number of occurrences of exposure between
the beginning of complementary feeding the beginning of complementary feeding
and 7 months and 11 months

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Weanling infants prefer the odors of green vegetables, cheese and fish when their mothers

consumed these foods during pregnancy and/or lactation

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l’Alimentation, 17 rue Sully, BP 86510 Dijon cedex, France. email: Sandrine.Monnery-Patris@inra.fr

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Haller et al. 1999).

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void of any previous medical complication.

(Comité Consultatif de Protection des Personnes dans la Recherche Biomédicale de Bourgogne).

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Measurement of infants’ odor liking

represented foods considered a priori as unpleasant (2-isobutyl-3-methoxypyrazine, trimethylamine,

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Behavioral analyses and odor-liking scores

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example, if dropped onto the floor).

12 months of age were not considered.

than 0.5 indicates avoidance of the odorant compared to the control.

Recording of dietary data for deriving of odor exposure data

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complementary feeding to 11 months.

Selection of food items for deriving infant odor exposure

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exposure inference are presented in Table 2.

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Relationships between odor liking and early exposures

Liking of food odors

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the postpartum period.

[insert Fig. 1 about here]

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[insert Fig. 2 about here]

Relationships between early exposures and subsequent odor liking

Relationships between in utero exposure and subsequent odor liking

Relationships between breastfeeding exposure and subsequent odor liking

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odor liking scores at 8 or 12 months (Tables 3 and 4).

corresponding odor liking scores at 12 months.

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entire food flavor.

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exposed to the odor is not sufficient.

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various odor-active compounds, and/or of heterogeneous consequences of chemosensory exposure

during earliest phases of development of the olfactory tract.

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responses to corresponding odors. Finally, in studies demonstrating lengthily persisting effects of

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recommended for their health benefits (e.g., Anzman-Frasca et al. 2018).

Alimentation et Nutrition Humaine’ (project ANR-06-PNRA-028, OPALINE). The present study,

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and cooked cauliflower consumption. Appetite. 46:263-269.

vanillin on food preference later in life. Chem Senses. 24:465-467.

pre-natal ingestion of spicy foods. Eur J Pediatr. 144:403.

flavour compounds into human breast milk. Physiol Behav. 95:118-124.

of a novel dietary flavour compound. Clin Nutr. 29:141-148.

Downloaded from https://academic.oup.com/chemse/advance-article-abstract/doi/10.1093/chemse/bjz011/5341973 by guest on 25 February 2019

prenatal garlic experience. Dev Psychobiol. 55:568-574.

Sensory Science Symposium, August 12-16, 2007, Minneapolis, USA.