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Eects of diversity in olfactory
environment on children’s sense of
smell
Lenka Martinec Nováková
1,2, Jitka Fialová 2,3 & Jan Havlíček
2,3
Diversity in children’s everyday olfactory environment may aect the development of their olfactory
abilities and odor awareness. To test this, we collected data on olfactory abilities using the Snin’
Sticks and odor awareness with Children’s Olfactory Behaviors in Everyday Life Questionnaire in 153
preschool children and retested them one and a half year later. Parents completed an inventory on
children’s exposure to a variety of odors and on their own odor awareness using the Odor Awareness
Scale. We controlled for the eects of age and verbal uency on the children’s performance. We found
that the children’s odor identication and discrimination scores diered as a function of parental odor
awareness. Although these eects were rather small, they were commensurate in size with those of
gender and age. To the best of our knowledge, this study is the rst to present evidence that diversity
in children’s olfactory environment aects variation in their olfactory abilities and odor awareness. We
suggest that future studies consider the long-term impact of perceptual learning out of the laboratory
and its consequences for olfactory development.
One of the best-documented phenomena in olfactory research is the great degree of interindividual variability in
olfactory performance1 and metacognition2, also referred to as “odor awareness and reactivity” (hereaer referred
to as “odor awareness” for short) or “attitudes towards the sense of smell”. Accounts of how this variability in
olfactory perception arises are nonetheless still far from complete. e demographic factor routinely listed in the
rst place is age3,4. However, the passing of time (or age) itself is not what drives developmental changes but can
only be employed as a proxy for the actual causal mechanisms. For instance, children’s olfactory abilities mature
as they grow up, but this is most likely caused by growing experience with odors and improving linguistic abili-
ties5,6, broadening working memory span7, improving recognition memory8,9, changes in nasal aerodynamics and
more eective inhalation of odor stimuli10, not age itself. Gender (or sex) is another commonly used proxy for
individual dierences in olfaction, but simply identifying oneself (or being identied) as male, female, or other
can hardly suce as an explanation. e numerous factors that underlie genotypic and phenotypic sex and gender
are involved in a complex interplay, and may or may not converge to allow simplifying classications11,12. us,
although sex/gender is routinely cited as the second most important demographic factor inuencing olfaction,
and gender dierences in olfaction have been sought by a myriad of researchers13, investigations of specic, con-
crete factors inuencing normal olfactory function, some of which may align with thesex/gender classication,
seem a more productive approach. ese cover, among others, such varied but overlapping and interconnected
areas as genetic outt14, nasal anatomy15, brain anatomy16, respiratory-related physiology17, reproductive hor-
mone inuences18, cognitive functions19, crossmodal interactions20, and cultural inuences21.
Curiously enough, one factor that is being rather overlooked when it comes to interindividual dierences but
is otherwise granted close attention as far as cultural dierences are concerned, is diversity in olfactory environ-
ments and the formative eect of odor exposure. It is widely acknowledged that dierences in olfaction between
individuals coming from dierent cultures stem from long-term, frequent exposure to certain odors within spe-
cic contexts22. ese, in turn, not only come to acquire culturally specic meanings23, but may also be perceived
as more readily identiable or categorizable, pleasant, familiar, and more (or less) intense by members of one
culture than of another21,24,25. Moreover, such variation in experience with odors may result in cross-cultural
variation in certain olfactory abilities26 and olfactory metacognition24,27,28. Cross-cultural dierences are one level
1Department of Anthropology, Faculty of Humanities, Charles University, U Kříže 8, 158 00, Prague 5 – Jinonice,
Czech Republic. 2National Institute of Mental Health, Topolová 748, 250 67, Klecany, Czech Republic. 3Department
of Zoology, Faculty of Science, Charles University, Viničná 7, 128 44, Prague 2, Czech Republic. Correspondence and
requests for materials should be addressed to L.M.N. (email: lenka.novakova@s.cuni.cz)
Received: 17 October 2017
Accepted: 12 January 2018
Published: xx xx xxxx
OPEN
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SCientifiC RepoRts | (2018) 8:2937 | DOI:10.1038/s41598-018-20236-0
at which the eects of living in diverse olfactory environments are manifested but they are also sure to give rise to
interindividual dierences in olfaction within a given culture.
e ways in which odor exposure in everyday life shapes an individual’s olfactory abilities and metacognition,
i.e. odor awareness, are rather dicult to quantify, hence the scarcity of studies on this topic. e rationale behind
this line of inquiry are the eects of perceptual learning, a phenomenon whereby sensory experience brings about
changes in brain function and behavior29–31. Perceptual learning can occur by means of training, i.e. directed,
focused program of instruction, or experience, which consists in unstructured exposure to a wide variety of stim-
uli32. Due to methodological problems with assessment of variationin everyday olfactory environments, most
evidence comes from studies with untrained individuals who underwent a specic olfactory training program
in the laboratory and from those with experts, mostly perfumers and wine tasters. Altogether these studies show
that the abilities of odor identication and discrimination indisputably benet from olfactory training/exposure
in a signicant way33. Findings on olfactory sensitivity are, however, rather contradictory34–36. On the one hand,
repeated exposure to a given odor in some untrained individuals may lead to heightened sensitivity to it37,38 as
well as to alleviation of specic anosmia in the case of the16-androstenes39,40. e evidence on the eect of odor
expertise on odor awareness is more limited. If it is to be conceptualized as including olfactory imagery capac-
ity41,42, this indeed seems higher in fragrance experts than in non-expert controls43. Other than that, there is a
study showing a link between self-reported exposure to food odors and avors in childhood and adulthood on
the one hand and odor identication and awareness on the other44.
We believe that developmental inquiry would particularly benet from considering the formative poten-
tial of odor exposure. e one thing that should make it far more eective (and hence its consequences even
more tangible) than any professional training or exposure within laboratory settings is its long-term and per-
vasive nature. Despite that, it has actually rarely been considered at all. To date, the only two studies in chil-
dren to employ some assessment of their everyday olfactory environment reported mixed results. In a sample
of Namibian 8–15-year-olds, Saxton et al.28 did not nd a signicant link between self-reported olfactory envi-
ronment (as assessed by questions on the number of siblings, number of animals, and cooking frequency) and
odor awareness or olfactory abilities. However, as the authors note, the sample size was quite small (N = 52) and
more sensitive measures of individual odor exposure may have been needed. ese were used in a recent study
by Martinec Nováková and Vojtušová Mrzílková45, who showed that the degree of preschool children’s odor
exposure in everyday contexts, as assessed by their parents, predicted their odor awareness, but not olfactory
abilities. Self- or parental reports of what a child’s everyday olfactory environment smells like is one approach
to assess odor exposure. Another, not yet employed in previous studies, is information on those who participate
in shaping it, especially the parents. Of course, certain aspects of our olfactory environments and acuity of the
sense of smell are non-negotiable and more or less given by the geographic location and place of residence46,47 but
others can be actively modied through the lifestyles we adopt48–53. Behaviors and lifestyles may be transmitted
across generations54–56 and various aspects of children’s lifestyles are heavily inuenced by their parents57. us,
family appears to play the most crucial role not only in familiarization with specic odors, but also in formation
of olfaction-related attitudes, practices, and behaviors and so on. Perhaps most notably, this is the case as regards
dietary habits58 or moralization of certain olfaction-related activities, such as smoking59, or odors, such as per-
sonal (body) odors60. Hence, including information on parental odor awareness may help shed additional light
on children’s everyday olfactory environments and how these shape the development of their olfactory abilities
and odor awareness.
In the present study, we were interested in how children’s everyday olfactory environment and parental odor
awareness aect the development of their olfactory abilities and odor awareness. To achieve this, we collected
olfactory data in over 150 preschool children and retested them one and a half year later. In so doing, we con-
trolled for the eects of age and verbal uency, which were found to modulate children’s olfactory abilities24,61 and
odor awareness62. We hypothesized that children of parents who reported higher self-assessed odor awareness
and greater exposure of their ospring to diverse olfactory stimuli would outperform their peers on odor identi-
cation and discrimination and also exhibit greater odor awareness, regardless of gender. First, using acategorical
principal component analysis, we obtained four components of thechildren’s odor exposure. Second, due to a
fair amount of missing data, imputation of missing values was performed. Finally, using a multivariate repeated
measures analysis of variance (MANOVA) model, we tested for the eects of children’s gender (between-subject
factor), age at the rst session, verbal uency, four components of odor exposure, and averaged mother’s and
father’s odor awareness (covariates) on children’s identication, discrimination, and threshold scores as well as
their odor awareness (within-subject variables). We decided to err on the side of caution and performed this
analysis on both the imputed dataset and the original one.
Results
Eects of diversity of olfactory environment and demographic variables on children’s olfaction –
imputed data. A repeated-measures MANOVA showed no signicant within-subject dierences but a mul-
titude of between-subject ones. As can be seen in detail from Table1, these were related, as expected, to age,
gender, and verbal uency, but also to the degree of averaged parental odor awareness. Multivariate tests yielded
eect sizes of Cohen’s f 2 ranging between 0.10 and 0.12, except for verbal uency, for which it was 0.33. According
to Cohen63 and Murphy et al.64, the eect sizes of age, gender, and parental odor awareness can be thought of as
small to medium, while that of verbal uency was medium to large. Univariate tests showed that the eects of
gender and parental odor awareness pertained to children’s odor identication and discrimination, with Cohen’s
f 2 ranging between 0.04 and 0.09, indicating eects small in size, but still of “practical” signicance65. Namely,
better olfactory identication and discrimination performance was observed in girls and children whose parents
reported greater odor awareness. Furthermore, thechildren’s age at study commencement modestly aected odor
identication and threshold, Cohen’s f 2 = 0.07 and 0.03, respectively, with theolder children exhibiting better
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odor identication and higher sensitivity. Finally, verbal uency had a medium to large eect on thechildren’s
odor awareness, Cohen’s f 2 = 0.31. Specically, thechildren who produced more words on the verbal uency test
received higher scores in the interview.
Eects of diversity of olfactory environment and demographic variables on children’s olfaction
– non-imputed data. As can also be seen from Table1, analyses on non-imputed data (N = 59, 26 boys)
yielded seemingly slightly dierent results. Although this analysis did not show any signicant eect of repeated
measures or interactions involving them, either, it diered from the previous one in that the eect of age and
parental odor awareness waned in terms of theformal level of signicance, while that of the rst component of
odor exposure, named “Food diversity and aroma”, appeared. However, as statistical signicance largely depends
on sample size66, which was sub-optimal in the case of non-imputed data, it is advisable to focus on aninterpre-
tation of the eect sizes instead. A quick look at Table1 and comparison of Fig.1 with Supplementary FigureS1
will reveal that the relationship with parental odor awareness remained the same, while the eects of gender and
age increased slightly from small to medium and that of verbal uency from medium bordering on large to large.
e only large eect, larger even than those of the demographic variables, was that of the rst component of odor
exposure. Namely, children exposed to more diverse food-related odors, as assessed by their parents, scored
higher on odor identication and exhibited greater odor awareness. Inspection of the other, non-signicant
eects will conrm that they were not dramatically dierent from those in theimputed data, either. Hence, even
though the results on the non-imputed data should be regarded with caution because of the small sample size, in
fact there was little dierence from those obtained onthe imputed data in terms of eect sizes.
Discussion
In the present study, we expected that children’s olfactory abilities, particularly odor identication and discrim-
ination, and odor awareness, would be inuenced by the diversity in their olfactory environments. In line with
Imputed data Non-imputed data
Gender Age Verbal
uency Parental
OA OE 1 OE 2 OE 3 OE 4 Gender Age Verbal
uency Parental
OA OE 1 OE 2 OE 3 OE 4
Multivariate tests
Pillai’s
Trace 0.087 0.102 0.249 0.105 0.043 0.016 0.034 0.016 0.193 0.135 0.299 0.061 0.374 0.105 0.079 0.002
F 3.363 3.990 11.679 4.150 1.584 0.590 1.233 0.579 2.809 1.829 5.007 0.762 7.015 1.378 1.329 0.020
p0.0120.004 <0.001 0.003 0.182 0.670 0.300 0.678 0.036 0.139 0.002 0.555 <0.001 0.256 0.415 0.999
Cohen’s
f 20.095 0.114 0.332 0.117 0.045 0.016 0.035 0.016 0.239 0.156 0.427 0.065 0.597 0.117 0.086 0.002
Univariate tests
Identication
F 8.013 9.991 0.271 5.648 2.832 0.184 2.489 0.106 6.341 5.734 2.143 0.938 13.913 0.473 0.833 0.001
p0.005 0.002 0.604 0.019 0.095 0.669 0.117 0.745 0.015 0.020 0.149 0.337 <0.001 0.495 0.366 0.982
Cohen’s
f 20.056 0.070 0.002 0.040 0.019 <0.001 0.017 0.001 0.127 0.115 0.043 0.018 0.279 0.009 0.016 <0.001
Discrimination
F 6.345 2.961 2.500 12.932 0.606 1.600 2.612 1.017 5.679 0.002 1.536 2.793 2.014 1.412 3.700 0.021
p0.013 0.087 0.116 <0.001 0.438 0.208 0.108 0.315 0.021 0.968 0.221 0.101 0.162 0.240 0.060 0.886
Cohen’s
f 20.044 0.020 0.017 0.089 0.004 0.011 0.018 0.007 0.114 <0.001 0.031 0.056 0.041 0.028 0.074 <0.001
reshold
F 1.890 4.959 0.027 0.396 0.931 0.090 0.068 1.325 0.099 0.043 0.002 0.165 0.043 <0.001 0.016 0.017
p 0.171 0.028 0.869 0.530 0.336 0.765 0.794 0.252 0.754 0.837 0.962 0.686 0.837 0.998 0.901 0.897
Cohen’s
f 20.013 0.034 <0.001 0.003 0.006 <0.001 <0.001 0.009 0.002 <0.001 <0.001 0.003 0.001 <0.001 <0.001 <0.001
COBEL
F 0.329 0.006 43.975 1.767 2.560 0.850 1.293 0.028 3.573 2.158 19.154 0.169 13.305 1.564 0.010 0.051
p 0.567 0.940 <0.001 0.186 0.112 0.358 0.257 0.868 0.065 0.148 <0.001 0.683 <0.001 0.217 0.922 0.822
Cohen’s
f 20.002 <0.001 0.305 0.012 0.017 0.006 0.009 <0.001 0.072 0.043 0.383 0.003 0.266 0.031 <0.001 0.001
Table 1. Results of repeated-measures analyses on imputed (N = 153, 76 M) and non-imputed (N = 59,
26 M) data. Shown are multivariate and univariate tests for between-subject eects (multivariate Pillai’s
Trace, F, p-value, and Cohen’s f 2 computed from SPSS-produced partial η2). In imputed data, df1 and df2 for
theF-statistic were 4, 141 and 1, 144 for multivariate and univariate tests, respectively, while in non-imputed
ones these were 4, 47 and 1, 50, respectively. OE1 = Food diversity and aroma, OE2 = Engagement in cooking
and household chores, OE3 = Scent intensity, and OE4 = Edible odors, awareness, and naming. Signicant
eects (p < 0.05) are highlightedin italics.
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this hypothesis, we found that thechildren’s olfaction was aected by environmental inuences, whether concep-
tualized in terms of parental odor awareness (identication and discrimination, imputed data, small eects) or
parental assessments of thechildren’s olfactory environments (identication and odor awareness, non-imputed
data, medium eects). Besides this, we also replicated some of the standard ndings in the literature on the devel-
opment of olfactory abilities and odor awareness. Namely, odor identication and discrimination scores were on
average higher in girls and the former were also higher in older children, as was olfactory sensitivity. ese eects
were fairly small but still of “practical” signicance. Quite large, on the other hand, was the eect of verbal uency
on thechildren’s odor awareness.
As expected, parental reports of the children’s odor exposure inuenced their ospring’s odor awareness, as
was the case in the study by Martinec Nováková and Vojtušová Mrzílková45 in preschool children and Nováková
et al.44 in young adults. is was despite the fact that dierent inventories of odor exposure were used, diering
slightly in the former and completely in the latter case, in which, moreover, self-reports were provided and a
dierent measure of odor awareness (Odor Awareness Scale)67 was used due to a completely dierent demo-
graphic. us, there is a mounting converging evidence that diversity in olfactory environment indeed may play
a role in how we regard and use our sense of smell, which cannot be simply explained by the fact that all meas-
ures (questionnaires, inventories) employed were completed by the same individuals, and hence the so-called
extreme response style68,69 might have been involved. Even more intriguing is the possibility that this diversity
may actually inuence some of the olfactory abilities. As mentioned above, if perceptual learning can bring about
tangible results aer arelatively brief exposure in the laboratory, in real-life settings with its long-term and per-
vasive eects, the opposite would actually be quite surprising. Also, in the latter case, and especially in children,
powerful inuences such as social reinforcement are likely to be at work. For instance, “good behaviour” such as
washing hands or ushing the toilet is reinforced with verbal praise by parents and teachers70. rough signs of
disapproval, advertising that heightens insecurities about bodily odors, and other channels that mediate negative
societal views of e.g. perspiration, children come to recognize odors that are unacceptable in social interactions
and learn to manage and mask them71 and even to moralize them60. In young children, specic social inuences
Figure 1. Matrix showing scatter plots of olfactory measures, age, verbal uency, parental odor awareness, and
odor exposure component 1 in the lower diagonal, their distributions on the diagonal and Pearson’s correlations
written in the upper diagonal in boys (N = 76) and girls (N = 77) in imputed data. MI = mean identication
(mean for the 1st and 2nd testing occasion), MD = mean discrimination, MT = mean threshold, MC = mean
total COBEL score, A = age at study commencement, VF = verbal uency, OAS = parental odor awareness
(mean for mothers and fathers), OE1 = rst component of odor exposure.
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also promote learning about novel odors and avors, acting to overcome early food neophobia72. ese and other
examples illustrate the crucial role of social environment in the long-term process of learning about odors, which
should make such exposure far more eective than any structured training in the laboratory.
is account is broadly in line with evidence of olfactory performance enhancement following olfactory train-
ing in the laboratory38,73–75 and in professionals (mainly perfumers, wine and beer experts) as compared to naïve
individuals34,35,76. Importantly, the eects of practice and experience need not be limited to the behavioral level,
i.e. performance on various olfactory tasks, but they also appear to be linked to structural and functional variation
in certain brain areas in experts and non-experts alike. is idea is supported by positive associations in healthy
naïve individuals between performance on various olfactory tasks and the olfactory bulb volume in adults16,77
and children and adolescents78, gray matter volume in the right orbitofrontal cortex16 as well as cortical thickness
of the right medial orbitofrontal cortex, right insula or areas around the central sulcus bilaterally79. From these
associations it follows that if olfactory function is positively inuenced by heightened exposure to a variety of
olfactory stimuli over the longer term, so should certain brain regions involved in olfactory processing. Direct
evidence of changes in brain activity following olfactory training or odor exposure is nevertheless rather limited.
In one of the few studies, Li et al.80 demonstrated that following aversive Pavlovian conditioning, chiral odor pairs
initially smelling the same became perceptually distinct, which was accompanied by spatial divergence of odor
activity patterns in the piriform cortex. Increased responses in the posterior piriform and medial orbitofrontal
cortices along with improved perceptual dierentiation for novel odorants related in odor quality or functional
group were also observed aer an exposure as short as 3.5 min to a target odorant. Importantly, perceptual dif-
ferentiation performance was predicted by the magnitude of activation of the orbitofrontal cortex81. Dierences
in activation patterns were also observed between individuals with varying levels of olfactory or avour experi-
ence82–84. For instance, in a study with professional and trainee perfumers83, higher activation in trainees relative
to professionals was observed in the right anterior insula during olfactory mental imagery and in the posterior
piriform cortex during this task as well as during passive odor perception, suggesting that the two groups used
dierent strategies to process odors. Duration of practice and hence the level of expertise only aected mental
imagery capacities, not passive odor perception: the higher the experience level, the weaker the activation of the
right posterior piriform cortex, the le orbitofrontal cortex and the le hippocampus. e authors suggested
that experts exhibit enhanced perceptual capacity and so require less eort to mentally imagine odors. Structural
changes in the brain in healthy individuals remain somewhat less investigated but seem to parallel the functional
ones. To be specic, in perfumers, whether trainees or professionals, there was an increase in gray matter volume
in the bilateral gyrus rectus/medial orbital gyrus relative to controls. Furthermore, the le-side volume of gray
matter in this orbitofrontal area that surrounds the olfactory sulcus as well as in the anterior piriform cortex was
positively correlated with the degree of experience of professional perfumers84.
Additional evidence of the eects of odor exposure on the brain comes from animal studies. For instance, in
the study by Rochefort et al.85, proliferation among neural progenitors and their survival in the main olfactory
bulb was investigated in mice housed in either a standard or an odor-enriched environment for 40 days. ey
found that while olfactory conditions did not have any inuence on the proliferative activity of progenitor cells
in the subventricular zone, they did aect the number of newborn neurons in the main olfactory bulb, which,
aer three weeks, was roughly doubled in the enriched group compared to the standard one. A nding even more
important from the perspective of the present study is that the increase of newborn neurons resulting from envi-
ronmental enrichment had functional consequences on olfactory behavioral performance. To be specic, in mice
exposed to the enriched environment, odor memory held circa four times longer than in the controls. In addition,
in the former group, recognition of an odor was not aected by an immediate presentation of a second, distractor
odor, as evidenced by the fact that odor-enriched mice spent less time investigating the rst odor during repeated
presentation despite the exposure to the distractor. In contrast, for the controls, the previously encountered odor
was as unfamiliar as the second odor. In another study, Mandairon and colleagues86 exposed rats to single odors
or to pairs of similar or dissimilar odors for one hour twice a day over 20 days. ey reported that while the rats
did not spontaneously discriminate similar odor pairs prior to the enrichment period, aer that, they were able
to do so. is improvement was not specic to the odors they had been exposed to. Hence, there is converging
evidence from multiple empirical methods suggesting that olfactory enrichment aects brain structure and func-
tion and olfactory performance. Future studies should employ the developmental perspective to elucidate the
environmental factors that contribute to enhanced olfactory function.
Nevertheless, an alternative account of why thechildren of parents who reported high odor awareness out-
performed others is that parents interested in the study or those who were high-achieving or careful about their
image may haveencouraged their children, overtly or covertly, to make an eort and perform well in any circum-
stances, regardless of the task at hand. Psychophysical tests of olfactory abilities require collaboration on the part
of the participant and an ability to adhere to oral instructions and very young children tend to lack the motivation
to comply with them87. As in the case of school performance and academic achievement, children seen as dier-
ing in motivation may be exposed to dierential parental motivation practices88, which, in turn, may perhaps be
linked more to parents’ general tendency to outperform, make a good impression, etc. than olfactory interests.
Specically in terms of the interview with children to gauge their odor awareness, some children may tend to
exaggerate their responses about unwanted odors and their control. ese children may be encouraged to do so,
if unknowingly, by parents who care about the impression they and their children give about socially desirable
behaviors in general. Even though theparents or other caregivers were not present during the interview, children
who (begin to) realize that (de)odorization is widely encouraged within the Western sociocultural context89 may
havebeen eager to share this knowledge with the interviewer. us, they may not only or necessarily havelived
in an environment which was richer in olfactory stimuli, it might be as well that their parents were very careful
about their image in this respect and, if unconsciously, passed this message onto their children. Nevertheless, if
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this account were to be correct, one would expect a strong, signicant association between theparental and chil-
dren’s odor awareness, which was not the case in the present study (see Supplementary FigureS1).
Among the ndings routinely reported in the literature on the development of the sense of smell was the eect
of gender on odor identication and discrimination24,62,90–93. However, a number of studies nevertheless failed to
nd it28,45,61,94–98. Since statistical signicance largely depends on sample size66, this discrepancy may be caused by
dierences in sample size, while the eect, in fact, tends to be quite small across studies. However, one should bear
in mind that the terms “sex” and “gender” can be understood in a number of ways, e.g. chromosomal, hormonal
or endocrine, gonadal, genital, body-type sex, sex of assignment and rearing, brain sex/gender, social and psy-
chological gender99–101. What is more, between-gender dierences in olfaction may be obscured by gender (non)
conformity or sex-atypicality102. erefore, the focus should shi to concrete factors inuencing normal olfactory
function which tend to align with the sex/gender classication. As noted in the introduction, the majority of
developmental studies nevertheless lend little insight into what the actual causes of these gender/sex dierences
may be. Some indicate that the female verbal superiority is likely to be one factor in children5,91,103 and adults104
alike. For instance, Monnery-Patris5 reported that the gender eect vanished when verbal prociency (verbal age
and olfactory verbal uency) was controlled for. Another factor might be gender dierences in the capacity to
comply with verbal instructions and sustain focus on the task at hand during psychophysical olfactory testing.
Martinec Nováková and Vojtušová Mrzílková94 hypothesised that girls might be better able to handle the testing
format. ey indeed found higher self-regulatory capacities in girls compared to boys, as assessed by the chil-
dren’s parents, i.e. superiority in terms of the ability to voluntarily sustain focus on a task, shi attention from one
task to another, initiate action, and inhibit it105. Yet, girls did not outperform boys on either of the olfactory tests
employed. Also, it has been suggested that females since infancy might be exposed to a greater variety of olfactory
stimuli in everyday life through certain olfaction-related activities44,45. In children, however, parental reports of
odor exposure did not dier depending on whether the child was a boy or a girl and girls did not outperform boys
on either of the two identication tests or on the discrimination one45. More developmental studies are needed to
identify other factors which may help explain the gender dierence in olfactory abilities.
Further, odor identication and threshold were mildly inuenced bythe children’s age at the commence-
ment of the study. is is also routinely reported for odor identication24,61,97, even though some studies suggest
otherwise28,45. In general, tasks which depend on lexical, semantic, or symbolic processes exhibit increments in
performance as children get older. Again, it is still unclear precisely what factors drive this development. Several
mutually non-exclusive factors will likely be involved, such as growing experience with odors and improving
linguistic abilities5,6, broadening working memory span7, improving recognition memory8,9, nasal aerodynamics
and more eective inhalation of odor stimuli10, etc. However, a comprehensive developmental study taking into
consideration multiple factors is still missing.
Finally, we also observed a medium to large positive eect of verbal uency on theodor awarenessscores. is
is in line with thendings in the original use of the measure62, but not with those in two subsequent studies45,106.
Dierences in variability in children’s odor awareness in the present and the two aforementioned studies cannot
be invoked to explain this discrepancy, since it was roughly similar. Verbal uency was more variable in the
slightly older children45,106 than here, but not signicantly so, as the comparison of standard deviations indicated.
Dierent sample sizes cannot account for this discrepancy, either, since the N for which verbal uency data was
available was actually about twice as large in the previous studies, in which nevertheless no link with children’s
odor awareness appeared. Besides, the eect size did not even reach the recommended minimum for social sci-
ence data to be regarded at least as small, but of “practical” signicance65. ere is thus a possibility worth further
exploration in future studies that the relationship between children’s odor awareness on the one hand and verbal
capacities on the other perhaps only exists at a certain age and vanishes some time aer children start school.
is is because there may be other moderating or mediating factors at play, aecting both of these variables, such
as being more accustomed to interacting and collaborating with adults in authority (e.g. a teacher, researcher),
which is crucial for performance both at school and within research settings.
To the best of our knowledge, this study is the rst to present evidence that diversity in children’s olfactory
environment aects variation in their olfactory abilities and odor awareness. Although these eects were small
to medium at best, they were actually commensurate in size with those of demographic variables standardly
reported to inuence olfaction, i.e. gender and age. We suggest that future studies consider the long-term impact
of perceptual learning out of the laboratory and its consequences for olfactory development.
Materials and Methods
Participants. e participants were 153 children of Czech origin (76 boys), mean age at study commence-
ment 5.76 ± 0.60 years, range 4.33–6.92 years, mean interval between sessions 18.86 ± 3.49 months. Namely,
there were 17 children younger than 5 years of age, 74 aged between 5 and 6 years of age, and 62 over 6 years of
age at the rst testing occasion. At the start of the study, we collected data in ve public mixed-sex kindergar-
tens in Prague and its suburbs. e kindergartens were attended by children from varied social backgrounds.
Kindergarten principals were contacted via telephone, e-mail, and in person to inform them about the planned
study. ose who had provided permission to perform the study on the kindergarten’s premises were asked to
pass the information on to the teachers, who distributed leaets to thechildren’s parents. We kept the e-mail
addresses and phone numbers the parents had provided to contact them later with an invitation for their children
to take part in a second testing. is time it took place either within the schools’ premises or at our department.
Girls and boys did not dier in terms of mean age or age distribution at the rst testing, t(151) = 1.90, p = 0.06
(boys: 5.67 ± 0.55 years, girls: 5.85 ± 0.63 years), or at the second one, t(151) = 0.573, p = 0.57 (boys: 7.32 ± 0.71
years, girls: 7.26 ± 0.60 years). Nor was there any dierence between boys and girls in the interval between the
two sessions, t(151) = 1.50, p = 0.14. Data collection took place in the late spring and early autumn, primarily
so as to minimize missing data due to dropout during the inuenza season. erefore, possible seasonal eects
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on olfactory performance were not taken into account. As can be seen from Table2, some of the measures were
nevertheless missing in some children, which is why N is given for each variable and analysis.
Ethics Statement. All procedures followed were in accordance with the ethical standards of the respon-
sible committee on human experimentation (institutional and national) and with the Helsinki Declaration
of 1975, as revised in 2008 (5). The study has been approved by the IRB of theFaculty of Science, Charles
University(Approval No. 2008/4). Written informed consent was obtained from the children’s parents and
oral informed consent was provided by the children in the presence of a teacher employed by the school. e
children-parents pairs each received 300 CZK (approx. 11 EUR) in compensation.
Olfactory Measures. General Considerations. The Sniffin’ Sticks test107, manufactured by Burghart
Messtechnik GmbH, was used to assess odor identication, discrimination, and threshold. is is one of the
most widely used tests of olfactory performance, based on pen-like odor dispensing devices. e Snin’ Sticks
test has been widely used by clinicians and researchers across Europe to test olfactory abilities in adults1 and chil-
dren24,90,95, including Czech ones28,45,94,108.
Boys Girls Tot a l Gender dierence
eoretical
range Mean SD Range NMean SD Range NMean SD Range N t(df) p d
First testing
Age (months) 70.22 7.57 53–83 76 68.04 6.65 52–83 77 69.12 7.18 52–83 153 −1.90 (151) 0.06 0.31
reshold 1–16 5.12 2.81 0.75–11.50 67 5.78 3.15 0.75–14 73 5.46 3.00 0.75–14 140 1.32 (138) 0.19 0.22
Discrimination 0–16 8.95 2.46 2–14 76 9.34 2.18 4–14 76 9.14 2.32 2–14 152 1.05 (150) 0.30 0.17
Identication 0–12 7.32 1.82 2–11 76 7.56 1.88 3–11 75 7.44 1.85 2–11 151 0.81 (149) 0.42 0.13
COBEL total 0–15 6.56 2.16 1.50–11 75 6.95 2.06 3–11 74 6.75 2.11 1.50–11 149 1.12 (147) 0.27 0.18
COBEL food 0–3 1.46 0.70 0–2.50 75 1.50 0.73 0–2.50 74 1.48 0.71 0–2.50 149 0.34 (147) 0.73 0.06
COBEL social 0–4 1.53 1.08 0–3.50 75 1.93 1.06 0–4 74 1.73 1.09 0–4 149 2.24 (147) 0.03 0.37
COBEL
environmental 0–8 3.57 1.09 1–5.50 75 3.52 1.13 1–6 74 3.54 1.11 1–6 149 −0.26 (147) 0.80 0.05
Second testing
Age (months) 87.85 8.53 69–104 76 87.12 7.23 69–103 77 87.48 7.89 69–104 153 −0.57 (151) 0.57 0.09
Age dierence
(months) 18.44 3.52 12–26 76 19.28 3.44 12–25 77 18.86 3.49 12–26 153 1.50 (151) 0.14 0.24
reshold 5.98 1.85 2–10 51 5.82 1.99 2–9.50 57 5.89 1.92 2–10 108 −0.44 (106) 0.66 0.08
Discrimination 10.16 2.54 5–16 62 11.13 2.47 5–15 63 10.65 2.54 5–16 125 2.16 (123) 0.03 0.39
Identication 7.40 1.75 2–11 63 8.18 1.60 5–12 62 7.78 1.72 2–12 125 2.60 (123) 0.01 0.47
COBEL total 6.53 2.03 2.50–11 61 7.02 2.34 2.50–13 62 6.78 2.20 2.50–13 123 1.24 (121) 0.22 0.22
COBEL food 1.59 0.69 0–2.50 61 1.55 0.78 0–2.50 62 1.57 0.74 0–2.50 123 −0.31 (121) 0.76 0.05
COBEL social 1.28 1.04 0–3.50 61 1.57 1.06 0–4 62 1.43 1.06 0–4 123 1.55 (121) 0.12 0.28
COBEL
environmental 3.66 1.07 1.50–5.50 61 3.90 1.30 2–7 62 3.78 1.19 1,50–7 123 1.12 (121) 0.27 0.20
Verbal uency 9.58 1.77 7–13 26 9.85 1.84 7–15 34 9.73 1.80 7–15 60 0.58 (58) 0.56 0.15
1 Food diversity
and aroma −0.04 0.93 −2.55–1.99 76 0.04 1.03 −2.42–1.99 77 0 0.98 −2.55–1.99 153 0.49 (151) 0.63 0.08
2 Engagement
in cooking and
household chores −0.21 0.97 −2.19–2.32 76 0.21 0.94 −1.66–2.67 77 0 0.98 −0.2.19–2.67 153 2.71 (151) <0.01 0.44
3 Scent intensity 0.01 0.97 −2.18–1.92 76 −0.01 0.99 −2.85–2.51 77 0 0.98 −0.2.85–2.51 153 −0.17 (151) 0.87 0.02
4 Edible odors,
awareness, and
naming −0.07 1.06 −2.58–2.30 76 0.07 0.88 −2.37–2.23 77 0 0.98 −0.2.58–2.30 153 0.85 (151) 0.40 0.14
Mother’s OAS 32–158 119.35 12.42 91–139 49 120.67 11.49 85–147 54 120.04 11.90 85–147 103 0.56 (101) 0.58 0.11
Father’s OAS 32–158 113.44 12.95 79–137 43 109.77 16.52 77–146 39 111.70 14.78 77–146 82 −1.13 (80) 0.26 0.25
Table 2. Mean ± SD, range, and valid N for the repeated measures of age in months, age dierence between 1st
and 2nd testing, Snin’ Sticks TDI (threshold, discrimination, identication), and COBEL (total and its food,
social, and environmental component). Further, verbal uency (2nd testing only), olfaction-related activities
(CATPCA object scores for the four factors), and mother’s and father’s odor awareness scores are shown in boys,
girls, and the total sample. Shown are also t statistics and degrees of freedom for dierences between boys and
girls, and their eect sizes expressed as Cohen’s d. Signicant ndings are highlighted in italics. No corrections
have been made for running multiple tests. Please note that the identication test was only comprised of 12
instead of the original 16 items.
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Odor Identication. e 16-item identication test (“blue”, as it is referred to by the manufacturer) consists
of odors familiar to the general European population, namely orange, leather, cinnamon, mint, banana, lemon,
licorice, turpentine, garlic, coee, apple, clove, pineapple, rose, anise, and sh (exact chemicals are not specied
by the manufacturer). In the original version of the test cued identication is employed, in which participants
select the verbal label of the target odor from a candidate list of four alternatives. e resulting score is the sum of
correct answers (maximum of 16). In the present study, the test was adapted to children who could not read yet
or were only beginning to learn reading. is was done by presenting both the targets and distractors in the form
of color pictures instead of verbal labels. e process of adaptation of the tests has been described in full detail in
Martinec Nováková and Vojtušová Mrzílková45. In short, children had been interviewed about their understand-
ing of both the target and distractor odor sources, upon which images depicting items most frequently associated
with the given verbal label were selected. ese interviews had also revealed that most children were rather unfa-
miliar with most of the spices (anise, cinnamon, clove, vanilla), menthol, and turpentine. us, items involving
these odor sources either as a target or distractor (items 3, 8, 12, and 15) were excluded, resulting in the maximum
score of 12 for the identication test, with higher scores indicating better identication performance. Prior to the
identication task, the researchers always made sure the children understood what the given picture depicted.
Odor presentation (sequence of odors presented, distance from the nostrils, exposure duration, etc.) was carried
out in a manner recommended by Hummel et al.107. e interval between odor presentations was circa 20 seconds.
Odor Discrimination. No alterations had to be made to the discrimination test. e test of odor discrimination
assesses the degree to which an individual can dierentiate between odors in suprathreshold concentrations. e
set comprises 16 triplets of odorized pens, of which two are identical, and the participant is asked to indicate the
odd one. e odorants used in the test and the order of presentation, which was followed, are given in Hummel
et al.107. Presentations of triplets were separated by circa 20 seconds. e score is the total of correct trials (0–16),
with higher scores indicating a better ability of odor discrimination.
Odor threshold. No alterations were made to the threshold test, either. e olfactory threshold refers to the
minimum concentration of a tested odorant that an individual is able to reliably dierentiate from a blank sample.
e set employed in the present study consisted of 16 dilution steps of n-butanol (targets), each of which formed a
triplet with two blanks. As recommended by Hummel et al.107, a single-staircase, three-alternative forced-choice
(3-AFC) method was used, in which, starting with the lowest concentration (dilution number 16), an ascending
(low to high concentration) series of even-numbered triplets was presented, with successful trials prompting
another presentation of the same triplet in a random order. Two successful trials in a row marked a turning point;
starting with the nearest lower concentration, a descending series of triplets was presented until the child failed
to detect the target. is marked a reversal towards the higher concentrations and, starting with the next higher
concentration, an ascending series of triplets was presented until two correct trials occurred, marking another
reversal. e testing was nished aer a total of 7 reversals was reached. e threshold score was computed as the
arithmetic mean of the dilution number at the last four reversals. Ranging from 1 to 16, higher scores indicate
greater olfactory sensitivity (i.e. lower threshold).
Verbal uency. Verbal uency is known to modulate mainly odour identication and children’s reports by
which their odor awareness is gauged24,28,62. It was tested using a Czech version of the category verbal uency
test adapted to children109. First, a training trial was conducted using the transport category, on which a child
was asked to name as many means of transport as possible. Understanding was assured by asking the child what
transport meant and by giving an example (e.g. a car). Next, the child was encouraged to name as many animals
as possible in 60 seconds, while the answers were being immediately written down by the researcher. Verbal u-
ency was only conducted at the second testing. e verbal uency score is the count of the items correctly named
(theoretical minimum of 0).
Questionnaires. Children’s Olfactory Behaviors in Everyday Life Questionnaire (COBEL). e children's
odor awareness was assessed by means of an interview based on the Children’s Olfactory Behaviors in Everyday
Life (COBEL) questionnaire62. Having been originally developed with 6- to 10-year-olds, it consists of 16 ques-
tions designed to evaluate self-reported awareness of odors in signicant everyday contexts, i.e. food, social,
and environmental. Each item was coded on a 3-point scale, rating the child as poorly (0), moderately (0.5), or
highly (1) olfaction-oriented in the given situation. Although it was used in a previous study with slightly older
Czech children28, in this age group it transpired that children did not fully understand the rating format of Item
3 (Senses in nature: “When you walk in nature, what do you prefer?”), which involved ranking the following
activities in order of preference: touching, smelling, watching, listening45,106. Specically, most children tended
to disregard the items to be ranked and oered their own response, which mostly involved “playing” or “running
around”. erefore, the item was excluded from the interview. us, the total COBEL score, computed as a sum
of the 15 items, ranged from 0 to 15. In addition to the total score, component scores for food (items 1, 2, and 16),
social (items 11, 12, 13, and 14), and environmental odors (items 4, 5, 6, 7, 8, 9, 10, and 15) were computed follow-
ing previous usage of COBEL24,28,62. e theoretical range for food, social, and environmental odors is thus 0 to 3,
0 to 4, and 0 to 8, respectively. e actual ranges are given in Table2. e amended version of the questionnaire
used in this study is enclosed in Supplementary TableS2.
Odor Awareness Scale (OAS). To assess individual dierences in odor awareness in parents (both mother and
father), the Czech version of the 32-item Odor Awareness Scale67 was administered. e teachers were asked to
distribute the Odor Awareness Scale only to parents who shared the household with each other and their child.
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e scale was translated by LMN and back-translation was produced by Jaroslava Varella Valentova. For previ-
ous usage in Czech participants see Nováková et al.44. is is a metacognitive measure to learn about people’s
self-assessments of their tendency to notice, pay attention, or attach importance to odors in certain everyday
situations, and their knowledge of how olfactory experiences shape their everyday behaviors. Items relate, for
instance, to the eect of odors on mood (“When a room has an unpleasant smell, does it inuence your mood?”),
evocation of memories by odors (“Do odors revive strong or vivid memories in you?”), olfactory distraction
(“When you are studying, or concentrated in general, do you get distracted by odors in the environment?”), eect
on product purchase (“Suppose you are at a supermarket where it smells bad. Is this a reason for you not to return
there?”), approach (“When someone has a pleasant body odor, do you nd him or her attractive?”), and avoidance
(“You are in a public space sitting close to someone who has an unpleasant smell. Do you look for another seat
if possible?”). irty of the 32 items are a ve-category response format (e.g. “always,” “oen,” “sometimes,” “sel-
dom,” and “never”), with greater frequency, degree, or probability scoring more points. e total score is obtained
by adding up the scores of the individual items, and can range between 32 and 158, with higher scores indicating
greater odor awareness. For subsequent analyses, the mother’s and father’s scores were averaged for each child.
Children’s Odor Exposure Inventory. Mothers were also asked to complete an inventory regarding their children’s
exposure to odors in various everyday contexts. It was based on the Olfactory Diversity Questionnaire (ODQ)110,
which provides parental reports of children’s odor exposure and lists items involving activities potentially rich
in olfactory stimulation. It has been reported to exhibit a moderate to strong association with children’s both
free and cued Snin’ Sticks odor identication scores110. Items include, for instance, raising the child’s aware-
ness of the surrounding odors, child’s exposure to exotic foods and a variety of herbs and spices, use of various
scented products, presence of natural sources of odor (e.g. animals) in the household, smoking, or air pollution
in the neighborhood. e complete list of the items is given in Supplementary TableS3. Several items were not
included in the analysis on the following grounds. Firstly, as regards the item Childcare (1), only 32% of mothers
(N = 47) indicated that their child had ever taken part in such an activity. Out of those, 57% (N = 27) responded
that the child only participated in childcare with a very low frequency of several times a month to less than once
a month (median = 1). Further, exploratory correlations preceding acategorical PCA (CATPCA) showed that
items Frequency of use of cosmetic products (2), those listing products/odor sources/hobbies/pets (items 14
through 17), and Breastfeeding (24) did not correlate with any other item. Since recoding to a yes/no response
format or rescaling had no eect, and inclusion of these items in the CATPCA invariably led to a marked drop in
thepercentage of variance accounted for and a structure of loadings dicult to interpret, these items were omit-
ted from the analysis. Finally, strength of environmental odor (19) and of odor from smoking at home (22, 23),
respectively, were excluded from theanalysis. In terms of environmental odor, only 31% of mothers indicated
that there were objects in the vicinity of their home which were a source of strong odor. Of these, over one fourth
(29%) nevertheless thought such an object emanated little to no odor. In most households (83%), the members
of the family did not smoke at home. Of those who did smoke at home or had neighbors whose smoking odors
penetrated to their household, 96% still perceived little to no odor.
To identify the components underlying the reports of odor exposure and to obtain component scores to be
used in the subsequent analyses, we performed a categorical principal component analysis (PCA) using the IBM
SPSS categorical PCA (CATPCA) Optimal Scaling option. Of the total of153 cases, 8 cases, in which the survey
had not been completed, were excluded from the analysis. e assumptions of the analysis were met, since an
exploration of correlations between the variables entered in the analyses showed that extreme multicollinearity
(>0.9) or singularity (=0.0) were not a problem, and all the data were positive integer. Ordinal and nominal
variables were scaled as such and the former were discretized by ranking. Avariable principal normalization
method was selected. Dimensions in solution were determined upon multiple trials to obtain the most inter-
pretable structure of loadings. Specically, eigenvalues were used as an indication of how many dimensions were
needed, following the general rule which states that the eigenvalue for a dimension should be larger than 1 when
all variables are either single nominal, ordinal, or numerical111,112. Joint plots of the category points showed that
the categories of variables were separated by the categorical principal components analysis clearly enough as
could be expected when the level was truly ordinal. e plot of the object scores revealed no outliers. A rule of
thumb was followed that only loadings sharing at least 15% of their variance with the components (i.e. loadings of
about 0.40 or greater) should be considered practically signicant and useful for interpretation purposes111. is
is roughly in accord with another recommendation of Stevens111 on component loadings with respect to sample
size. Specically, for N > 140 at α = 0.01, component loadings of about 0.434 or slightly less should be considered
statistically signicant. e CATPCA yielded four components: (i) Food diversity and aroma, (ii) Engagement in
cooking and household chores, (iii) Scent intensity, and (iv) Edible odors, awareness, and naming. e resulting
components and loadings are given in Table3.
Procedure. Parents and teachers were instructed to only encourage their children to attend the testing ses-
sions, scheduled between 9 a.m. and 3 p.m., when in good respiratory health. Testing took place in a secluded,
well-ventilated room without strong ambient odors. First, children were briey familiarized with the tasks, which
were presented as a game, and ensured that they could stop or quit at any time. e order of the olfactory tests,
interview based on COBEL, and verbal uency test was randomized across children. However, within the olfac-
tory tests, the stimuli were presented in the order recommended by Hummel et al.107. e sheer number of the
various olfactory tests and the interview presented a cognitive load that could only be alleviated by splitting them
over two sessions. erefore, each child was tested on two consecutive days or within a week at the very latest.
Each session took circa 30 minutes. e parents were sent the Odor Exposure Inventory and the Odor Awareness
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Scale to complete them at home, which they returned to the teacher. Parents or teachers were never present in the
room during the testing session.
Statistical Analysis. Analyses were carried out with SPSS 24.0113 and R114. Normality of the raw data was
checked, rstly, by visually examining the individual histograms of all relevant variables, secondly, by produc-
ing skewness and kurtosis values and their respective standard errors, from which z-scores were computed and
compared to the value of 1.96, as suggested by Field115, and, thirdly, with multiple Shapiro-Wilk’s W tests. Except
the two threshold measures, theassumption of normality was met. Hence, parametric tests were used. Bivariate
exploratory correlations involving interval variables or an interval and a dichotomous one were computed using
Pearson product-moment correlations. ose involving two ordinal, dichotomous, or an ordinal and a dichoto-
mous variable were calculated with Spearman’s rho, Phi, and Lambda, respectively. Gender dierences were tested
with t-tests. e r and t statistics were converted to Cohen’s d aer Cumming116. ere was a fair amount of miss-
ing data, which would render analysis across repeated measures only possible in 59 children (26 boys). erefore,
animputation of missing values was performed rst. To achieve this, themissForest package117 was used, avail-
able from the Comprehensive R Archive Network (CRAN) and run in the R114. Recommended particularly for
conducting multiple imputation of mixed data (numeric and factor variables in one data frame)118, it has been
compared to other imputation methods and found to have the least imputation error for both continuous and
categorical variables and the smallest prediction dierence (error)119. Default settings were used117,120. Subsequent
multiple t-tests and Pearson’s product-moment correlations did not show any dierence between the original and
imputed data in any of the variables or any change in relationships between variables within the imputed data
compared to the original data, respectively.
en, the relationship between children’s olfactory abilities and odor awareness, gender, age at study com-
mencement, components of odor exposure, verbal uency, and parental odor awareness was analysed using a
repeated-measures MANOVA, disregarding the interindividual dierences in the interval between the two meas-
urement occasions. is was done because correlations between the repeated measures did not markedly change
or turn non-signicant aer controlling for the dierence between the ages at study commencement and com-
pletion. is was true for both theimputed and non-imputed data. eCOBEL, identication, discrimination,
and threshold scores were entered as within-subject variables, gender was treated as a between-subject factor, and
the rest (age at the rst session, verbal uency, the four components of odor exposure, and mean parental odor
awareness) as covariates. Cohen’s d for dierences between means was computed aer Rosnow and Rosenthal121.
Partial eta squared produced by SPSS was converted to Cohen’s f 2 aer Cohen63; see also IBM Support122.
Data Availability. e dataset generated and analysed during the present study is available in the Open
Science Framework: osf.io/qhsw7.
References
1. Hummel, T., obal, G., Gudziol, H. & Macay-Sim, A. Normative data for the “Snin’ Stics” including tests of odor identication,
odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur. Arch.
Otorhinolaryngol. 264, 237–243,https://doi.org/10.1007/s00405-006-0173-0 (2007).
2. Dematte, M. L. et al. Individual variability in the awareness of odors: Demographic parameters and odor identication ability.
Chemosens. Percept.4, 175–185, https://doi.org/10.1007/s12078-011-9103-7 (2011).
3. Hawes, C. H. & Doty, . L. In e Neurology of Olfaction 1–58 (Cambridge University Press, 2009).
4. Doty, . L. & amath, V. e inuences of age on olfaction: a review. Front. Psy chol.5, 20, https://doi.org/10.3389/fpsyg.2014.00020
(2014).
Component Item Loading
Food diversity and aroma
(16.40%)
7 Strength of aroma 0.681
6 Seasoning 0.628
5 Foreign cuisines, exotic or
unusual foods 0.549
Engagement in cooking and
household chores (15.02%)
12 Household chores 0.695
4 Participation in meal preparation
and cooking 0.643
Scent intensity (11.81%)
3 Strength of scent of cosmetic
products 0.632
13 Strength of scent of household
products 0.402
11 Feasts 0.373
Edible odors, awareness, and
naming (9.88%)
10 Home baking −0.534
21 Attention to odors 0.493
8 Herbalism −0.488
20 Odor naming 0.483
9 Home processing of seasonal
produce −0.356
Table 3. An overview of the components (percentage of total variance), items, and loadings. Items with weak
loadings (<0.40) are given in italics at the component on which their loadings have been the highest.
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www.nature.com/scientificreports/
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5. Monnery-Patris, S., ouby, C., Niclaus, S. & Issanchou, S. Development of olfactory ability in children: sensitivity and
identication. Dev. Psychobiol. 51, 268–276, https://doi.org/10.1002/dev.20363 (2009).
6. Stevenson, . J., Mahmut, M. & Sundqvist, N. Age-related changes in odor discrimination. Dev. Psychol. 43, 253–260, https://doi.
org/10.1037/0012-1649.43.1.253 (2007).
7. Larjola, . & von Wright, J. Memory of odors: Developmental data. Percept. Mot. Skills 42, 1138–1138 (1976).
8. Hvastja, L. & Zanuttini, L. Odor memory and odor hedonics in children. Perception 18, 391–396, https://doi.org/10.1068/p180391
(1989).
9. Fran, . A., Brearton, M., ybalsy, ., Cessna, T. & Howe, S. Consistent avor naming predicts recognition memory in children
and young adults. Food Qual. Prefer.22, 173–178, https://doi.org/10.1016/j.foodqual.2010.09.009 (2011).
10. Mennella, J. A. & Beauchamp, G. . Developmental changes in nasal airflow patterns. Acta Otolaryngol. (Stockh.) 112,
1025–1031,https://doi.org/10.3109/00016489209137505 (1992).
11. Cohen-ettenis, P. T. & Pfäin, F. Transgenderism and intersexuality in childhood and adolescence: Making choices. (Sage, 2003).
12. Ecert, L. Intersexualization: e clinic and the colony. 248 (outledge, 2017).
13. Brand, G. & Millot, J. L. Sex dierences in human olfaction: Between evidence and enigma. Q. J. Exp. Psychol. B54, 259–270,
https://doi.org/10.1080/713932757 (2001).
14. naapila, A. et al. Genetic component of identication, intensity and pleasantness of odours: a Finnish family study. Eur. J. Hum.
Genet. 15, 596–602, https://doi.org/10.1038/sj.ejhg.5201804 (2007).
15. Damm, M. et al. Intranasal volume and olfactory function. Chem. Senses 27, 831–839, https://doi.org/10.1093/chemse/27.9.831
(2002).
16. Seubert, J., Freiherr, J., Frasnelli, J., Hummel, T. & Lundström, J. N. Orbitofrontal cortex and olfactory bulb volume predict distinct
aspects of olfactory performance in healthy subjects. Cereb. Cortex 23, 2448–2456, https://doi.org/10.1093/cercor/bhs230 (2013).
17. Zhao, . & Frye, . E. In Handbook of Olfaction and Gustation (ed. . L. Doty) Ch. 16, 355–374 (John Wiley & Sons, 2015).
18. Doty, . L. & Cameron, E. L. Sex dierences and reproductive hormone inuences on human odor perception. Physiol. Behav. 97,
213–228, https://doi.org/10.1016/j.physbeh.2009.02.032 (2009).
19. Hedner, M., Larsson, M., Arnold, N., Zucco, G. M. & Hummel, T. Cognitive factors in odor detection, odor discrimination, and
odor identication tass. J. Clin. Exp. Neuropsychol. 32, 1062–1067, https://doi.org/10.1080/13803391003683070 (2010).
20. Gottfried, J. A. & Dolan, . J. e nose smells what the eye sees: Crossmodal visual facilitation of human olfactory perception.
Neuron 39, 375–386,https://doi.org/10.1016/S0896-6273(03)00392-1 (2003).
21. Ayabe anamura, S. et al. Dierences in perception of everyday odors: a Japanese- German cross-cultural study. Chem. Senses 23,
31–38,https://doi.org/10.1093/chemse/23.1.31 (1998).
22. Engen, T. In Perfumery: e Psychology and Biology of Fragrance (ed S. Van Toller, Dodd, G. H.) 79–90 (Chapman & Hall, 1988).
23. Cain, W. S. & Johnson, F. Lability of odor pleasantness: inuence of mere exposure. Perception 7, 459–465 (1978).
24. Ferdenzi, C., Mustonen, S., Tuorila, H. & Schaal, B. Children’s awareness and uses of odor cues in everyday life: A Finland-France
comparison. Chemosens. Percept.1, 190–198, https://doi.org/10.1007/s12078-008-9020-6 (2008).
25. Ferdenzi, C. et al. Variability of aective responses to odors: Culture, gender, and olfactory nowledge. Chem. Senses 38, 175–186,
https://doi.org/10.1093/chemse/bjs083 (2013).
26. Soroowsa, A., Soroowsi, P., Hummel, T. & Huanca, T. Olfaction and environment: Tsimane’ of bolivian rainforest have lower
threshold of odor detection than industrialized German people. PLoS ONE 8, e69203, https://doi.org/10.1371/journal.
pone.0069203 (2013).
27. Seo, H. S. et al. Attitudes toward olfaction: A cross-regional study. Chem. Senses 36, 177–187, https://doi.org/10.1093/chemse/
bjq112 (2011).
28. Saxton, T. . et al. Sex dierences in olfactory behavior in Namibian and Czech children. Chemosens. Percept.7, 117–125, https://
doi.org/10.1007/s12078-014-9172-5 (2014).
29. Fahle, M. & Poggio, T. Perceptual Learning. (MIT Press, 2002).
30. Gilbert, C. D., Sigman, M. & Crist, . E. e neural basis of perceptual learning. Neuron 31, 681–697, https://doi.org/10.1016/
s0896-6273(01)00424-x (2001).
31. Goldstone, . L. Perceptual learning. Annu. Rev. Psychol. 49, 585–612, https://doi.org/10.1146/annurev.psych.49.1.585 (1998).
32. Gawel, . The use of language by trained and untrained experienced wine tasters. J. Sens. Stud.12, 267–284, https://doi.
org/10.1111/j.1745-459X.1997.tb00067.x (1997).
33. oyet, J.-P., Plailly, J., Saive, A.-L., Veyrac, A. & Delon-Martin, C. e impact of expertise in olfaction. Front. Psy chol.4, 928, https://
doi.org/10.3389/fpsyg.2013.00928 (2013).
34. Bende, M. & Nordin, S. Perceptual learning in olfaction: Professional wine tasters versus controls. Physiol. Behav. 62, 1065–1070,
https://doi.org/10.1016/s0031-9384(97)00251-5 (1997).
35. Parr, W. V., Heatherbell, D. & White, . G. Demystifying wine expertise: Olfactory threshold, perceptual sill and semantic
memory in expert and novice wine judges. Chem. Senses 27, 747–755, https://doi.org/10.1093/chemse/27.8.747 (2002).
36. Brand, G. & Brisson, . Lateralization in wine olfactory threshold detection: Comparison between experts and novices. Laterality
17, 583–596, https://doi.org/10.1080/1357650x.2011.595955 (2012).
37. abin, M. D. & Cain, W. S. Determinants of measured olfactory sensitivity. Percept. Psychophys. 39, 281–286, https://doi.
org/10.3758/BF03204936 (1986).
38. Dalton, P., Doolittle, N. & Breslin, P. A. S. Gender-specic induction of enhanced sensitivity to odors. Nat. Neurosci. 5, 199–200,
https://doi.org/10.1038/nn803 (2002).
39. Wysoci, C. J., Dorries, . M. & Beauchamp, G. . Ability to perceive androstenone can be acquired by ostensibly anosmic people.
Proc. Natl. Acad. Sci. USA 86, 7976–7978, https://doi.org/10.1073/pnas.86.20.7976 (1989).
40. Mainland, J. D. et al. Olfactory plasticity - One nostril nows what the other learns. Nature 419, 802–802, https://doi.
org/10.1038/419802a (2002).
41. Arshamian, A., Willander, J. & Larsson, M. Olfactory awareness is positively associated to odour memory. J. Cogn. Psychol.23,
220–226, https://doi.org/10.1080/20445911.2011.483226 (2011).
42. Vanhaudenhuyse, A. et al. Two distinct neuronal networs mediate the awareness of environment and of self. J. Cogn. Neurosci. 23,
570–578, https://doi.org/10.1162/jocn.2010.21488 (2011).
43. Gilbert, A. N., Crouch, M. & emp, S. E. Olfactory and visual mental imagery. J. Ment. Imagery 22, 137–146 (1998).
44. Nováová, L., Valentova, J. V. & Havlíče, J. Engagement in olfaction-related activities is associated with the ability of odor
identication and odor awareness. Chemosens. Percept.7, 56–67,https://doi.org/10.1007/s12078-014-9167-2 (2014).
45. Martinec Nováová, L. & Vojtušová Mrzílová, . Children’s exposure to odors in everyday contexts predicts their odor awareness.
Chemosens. Percept.9, 56–68, https://doi.org/10.1007/s12078-016-9205-3 (2016).
46. Calderon-Garciduenas, L. et al. Urban air pollution: Inuences on olfactory function and pathology in exposed children and young
adults. Exp. Toxicol. Pathol. 62, 91–102, https://doi.org/10.1016/j.etp.2009.02.117 (2010).
47. Philpott, C., Goodenough, P., Passant, C., obertson, A. & Murty, G. e eect of temperature, humidity and pea inspiratory
nasal ow on olfactory thresholds. Clin. Otolaryngol. 29, 24–31, https://doi.org/10.1111/j.1365-2273.2004.00760.x (2004).
48. atotomichelais, M. et al. e eect of smoing on the olfactory function. Rhinology 45, 273–280 (2007).
49. upp, C. I. et al. educed olfactory sensitivity, discrimination, and identication in patients with alcohol dependence. Alcohol.
Clin. Exp. Res.27, 432–439, https://doi.org/10.1097/01.alc.0000057945.57330.2c (2003).
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
12
SCientifiC RepoRts | (2018) 8:2937 | DOI:10.1038/s41598-018-20236-0
50. Islam, M. A. et al. Olfaction in eating disorders and abnormal eating behavior: a systematic review. Front. Psychol.6, https://doi.
org/10.3389/fpsyg.2015.01431 (2015).
51. Gobba, F. Olfactory toxicity: Long-term eects of occupational exposures. Int. Arch. Occup. Environ. Health 79, 322–331, https://
doi.org/10.1007/s00420-005-0043-x (2006).
52. uhn, P., Astruc, D., Messer, J. & Marlier, L. Exploring the olfactory environment of premature newborns: a French survey of health
care and cleaning products used in neonatal units. Acta Pae diat r. 100, 334–339, https://doi.org/10.1111/j.1651-2227.2010.02076.x
(2011).
53. Bridges, B. Fragrance: emerging health and environmental concerns. Flavour and Frag. J.17, 361–371, https://doi.org/10.1002/
.1106 (2002).
54. Ponthiere, G. Mortality, family and lifestyles. J. Fam. Econ. Issues 32, 175–190 (2011).
55. Bohace, J. & Mansuy, I. M. Molecular insights into transgenerational non-genetic inheritance of acquired behaviours. Nat. Rev.
Genet.16, 641–652, https://doi.org/10.1038/nrg3964 (2015).
56. Lane, M., ober, . L. & obertson, S. A. Parenting from before conception. Science 345, 756–760, https://doi.org/10.1126/
science.1254400 (2014).
57. Horstman, . & Smand, C. In Genetics from the laboratory to society: societal learning as an alternative to regulation (eds de Vries,
G. & Horstman, .) 90–117 (Palgrave Macmillan, 2008).
58. Mennella, J. A. & Ventura, A. . In Early nutrition: Impact on short- and long-term health Vol. 68 (eds van Goudoever, H.,
Guandalini, S. & leinman, . E.) 153–168 (arger, 2011).
59. ozin, P. & Singh, L. e moralization of cigarette smoing in the United States. J. Consum. Psychol.8, 321–337, https://doi.
org/10.1207/s15327663jcp0803_07 (1999).
60. Soo, M. L. M. & Stevenson, . J. e moralisation of body odor. Mankind Quart.47, 25–56 (2007).
61. Cameron, E. L. & Doty, . L. Odor identication testing in children and young adults using the smell wheel. Int. J. Pediatr.
Otorhinolaryngol. 77, 346–350, https://doi.org/10.1016/j.ijporl.2012.11.022 (2013).
62. Ferdenzi, C., Coureaud, G., Camos, V. & Schaal, B. Human awareness and uses of odor cues in everyday life: esults from a
questionnaire study in children. Int. J. Behav. Dev.32, 422–431, https://doi.org/10.1177/0165025408093661 (2008).
63. Cohen, J. Statistical Power Analysis for the Behavioral Sciences. 2 edn, (Lawrence Erlbaum Associates, Inc., 1988).
64. Murphy, . ., Myors, B. & Wolach, A. Statistical Power Analysis: A Simple and General Model for Traditional and Modern
Hypothesis Tests. 4 edn, (outledge, 2014).
65. Ferguson, C. J. An eect size primer: A Guide for clinicians and researchers. Prof. Psychol. Res. Pr.40, 532–538, https://doi.
org/10.1037/a0015808 (2009).
66. Cumming, G. e New Statistics: Why and How. Psychol. Sci. 25, 7–29, https://doi.org/10.1177/0956797613504966 (2014).
67. Smeets, M. A. M., Schierstein, H. N. J., Boelema, S. . & Lensvelt-Mulders, G. e Odor Awareness Scale: A new scale for
measuring positive and negative odor awareness. Chem. Senses 33, 725–734, https://doi.org/10.1093/chemse/bjn038 (2008).
68. Greenleaf, E. A. Measuring extreme response style. Public Opin. Q. 56, 328–351, https://doi.org/10.1086/269326 (1992).
69. Merrens, M. Generality and stability of extreme response style. Psychol. Rep. 27, 802–802, https://doi.org/10.2466/pr0.1970.27.3.802
(1970).
70. Cli, . & Millei, Z. Biopower and the “civilisation” of children’s bodies in a preschool bathroom: An Australian case study. Int. Soc.
Sci. J.62, 351–362, https://doi.org/10.1111/issj.12005 (2011).
71. Simes, M. . & Berg, D. H. Surreptitious learning: Menarche and menstrual product advertisements. Health Care Women Int. 22,
455–469, https://doi.org/10.1080/073993301317094281 (2001).
72. Addessi, E., Galloway, A. T., Visalberghi, E. & Birch, L. L. Specic social inuences on the acceptance of novel foods in 2-5-year-old
children. Appetite 45, 264–271, https://doi.org/10.1016/j.appet.2005.07.007 (2005).
73. abin, M. D. Experience facilitates olfactory quality discrimination. Percept. Psychophys. 44, 532–540, https://doi.org/10.3758/
bf03207487 (1988).
74. Jehl, C., oyet, J. P. & Holley, A. Odor discrimination and recognition memory as a function of familiarization. Percept. Psychophys.
57, 1002–1011, https://doi.org/10.3758/bf03205459 (1995).
75. Cain, W. S. Odor identication by males and females: predictions versus performance. Chem. Senses 7, 129–142, https://doi.
org/10.1093/chemse/7.2.129 (1982).
76. Zucco, G. M., Carassai, A., Baroni, M. . & Stevenson, . J. Labeling, identication, and recognition of wine-relevant odorants in
expert sommeliers, intermediates, and untrained wine driners. Perception 40, 598–607, https://doi.org/10.1068/p6972 (2011).
77. Buschhüter, D. et al. Correlation between olfactory bulb volume and olfactory function. Neuroimage 42, 498–502, https://doi.
org/10.1016/j.neuroimage.2008.05.004 (2008).
78. Hummel, T. et al. Correlation between olfactory bulb volume and olfactory function in children and adolescents. Exp. Brain Res.
214, 285–291, https://doi.org/10.1007/s00221-011-2832-7 (2011).
79. Frasnelli, J. et al. Neuroanatomical correlates of olfactory performance. Exp. Brain Res. 201, 1–11, https://doi.org/10.1007/s00221-
009-1999-7 (2010).
80. Li, W., Howard, J. D., Parrish, T. B. & Gottfried, J. A. Aversive learning enhances perceptual and cortical discrimination of
indiscriminable odor cues. Science 319, 1842–1845, https://doi.org/10.1126/science.1152837 (2008).
81. Li, W., Luxenberg, E., Parrish, T. & Gottfried, J. A. Learning to smell the roses: Experience-dependent neural plasticity in human
piriform and orbitofrontal cortices. Neuron 52, 1097–1108,https://doi.org/10.1016/j.neuron.2006.10.026 (2006).
82. Castriota-Scanderbeg, A. et al. The appreciation of wine by sommeliers: a functional magnetic resonance study of sensory
integration. Neuroimage 25, 570–578, https://doi.org/10.1016/j.neuroimage.2004.11.045 (2005).
83. Plailly, J., Delon-Martin, C. & oyet, J. P. Experience induces functional reorganization in brain regions involved in odor imagery
in perfumers. Hum. Brain Mapp. 33, 224–234, https://doi.org/10.1002/hbm.21207 (2012).
84. Delon-Martin, C., Plailly, J., Fonlupt, P., Veyrac, A. & oyet, J. P. Perfumers’ expertise induces structural reorganization in olfactory
brain regions. Neuroimage 68, 55–62, https://doi.org/10.1016/j.neuroimage.2012.11.044 (2013).
85. ochefort, C., Gheusi, G., Vincent, J. D. & Lledo, P. M. Enriched odor exposure increases the number of newborn neurons in the
adult olfactory bulb and improves odor memory. J. Neurosci. 22, 2679–2689, https://doi.org/10.3410/f.1005381.63306 (2002).
86. Mandairon, N., Stac, C., iselyczny, C. & Linster, C. Enrichment to odors improves olfactory discrimination in adult rats. Behav.
Neurosci. 120, 173–179, https://doi.org/10.1037/0735-7044.120a.173 (2006).
87. Hummel, T., oudnitzy, N. & empter, W. Intranasal trigeminal function in children. Dev. Med. Child Neurol. 49, 849–853,https://
doi.org/10.1111/j.1469-8749.2007.00849.x (2007).
88. Gottfried, A. E. In Handbook of motivation at school (eds Wentzel, . . & Wigeld, A.) Ch. 21, 463–475 (outledge, 2009).
89. MacPhee, M. Deodorized Culture: Anthropology of Smell in America. Arizona Anthropologist 8, 89–102 (1992).
90. enner, B. et al. e Candy Smell Test: A new test for retronasal olfactory performance. Laryngoscope 119, 487–495, https://doi.
org/10.1002/lary.20123 (2009).
91. ichman, . A., Post, E. M., Sheehe, P. . & Wright, H. N. Olfactory performance during childhood. I. Development of an odorant
identication test for children. J. Pe diatr. 121, 908–911,https://doi.org/10.1016/S0022-3476(05)80337-3 (1992).
92. Stevenson, . J., Sundqvist, N. & Mahmut, M. Age-related changes in discrimination of unfamiliar odors. Percept. Psychophys. 69,
185–192, https://doi.org/10.3758/bf03193741 (2007).
Content courtesy of Springer Nature, terms of use apply. Rights reserved
www.nature.com/scientificreports/
13
SCientifiC RepoRts | (2018) 8:2937 | DOI:10.1038/s41598-018-20236-0
93. van Spronsen, E., Ebbens, F. A. & Foens, W. J. Olfactory function in healthy children: Normative data for odor identication. Am.
J. Rhinol. Allergy 27, 197–201, https://doi.org/10.2500/ajra.2013.27.3865 (2013).
94. Martinec Nováová, L. & Vojtušová Mrzílová, . Temperamental inuences on children’s olfactory performance: e role of self-
regulation. Chemosens. Percept.9, 153–173, https://doi.org/10.1007/s12078-016-9216-0 (2016).
95. Soroowsa, A. et al. Changes of olfactory abilities in relation to age: odor identication in more than 1400 people aged 4 to 80
years. Eur. Arch. Otorhinolaryngol. 272, 1937–1944, https://doi.org/10.1007/s00405-014-3263-4 (2015).
96. ichman, . A., Sheehe, P. ., Wallace, ., Hyde, J. M. & Coplan, J. Olfactory performance during childhood. II. Developing a
discrimination tas for children. J. Ped iatr. 127, 421–426,https://doi.org/10.1016/S0022-3476(95)70074-9 (1995).
97. Schriever, V. A. et al. e “Snin’ ids” Test - A 14-item odor identication test for children. PLoS ONE 9, e101086, https://doi.
org/10.1371/journal.pone.0101086 (2014).
98. Dzaman, ., Zielni-Juriewicz, B., Juriewicz, D. & Molinsa-Glura, M. Test for screening olfactory function in children. Int. J.
Pediatr. Otorhinolaryngol. 77, 418–423, https://doi.org/10.1016/j.ijporl.2012.12.001 (2013).
99. arazis, . Fixing sex: Intersex, medical authority, and lived experience. 380 (Due University Press, 2008).
100. Zderic, S. A., Canning, D. A., Carr, M. C. & Snyder III, H. M. Pediatric gender assignment: A critical reappraisal. (Springer
Science+Business Media, 2002).
101. Fausto-Sterling, A. Sex/gender: Biology in a social world. (outledge, 2012).
102. Nováová, L., Valentova, J. V. & Havlíče, J. Olfactory performance is predicted by individual sex-atypicality, but not sexual
orientation. PLoS ONE 8, e80234, https://doi.org/10.1371/journal.pone.0080234 (2013).
103. ichman, . A., Wallace, . & Sheehe, P. . Assessment of an abbreviated odorant identication tas for children: a rapid screening
device for schools and clinics. Act a Pa edia tr. 84, 434–437, https://doi.org/10.1111/j.1651-2227.1995.tb13666.x (1995).
104. Öberg, C., Larsson, M. & Bacman, L. Dierential sex eects in olfactory functioning: e role of verbal processing. J. Int.
Neuropsychol. Soc. 8, 691–698, https://doi.org/10.1017/s1355617702801424 (2002).
105. Ahadi, S. A. & othbart, M. . In The developing structure of temperament and personality from infancy to adulthood (eds Halverson
Jr, C. F., ohnstamm, G. A. & Martin, . P.) 189–208 (Psychology Press, 2014).
106. Martinec Nováová, L., Vojtušová Mrzílová, . & ernerová, A. Gender dierences in inuences of temperament on olfactory
reactivity and awareness. Sci. Rep. 7, 8920, https://doi.org/10.1038/s41598-017-09231-z (2017).
107. Hummel, T., Seinger, B., Wolf, S. ., Pauli, E. & obal, G. ‘Snin’ Stics’: Olfactory performance assessed by the combined testing
of odor identification, odor discrimination and olfactory threshold. Chem. Senses 22, 39–52, https://doi.org/10.1093/
chemse/22.1.39 (1997).
108. Martinec Nováová, L., Plotěná, D., oberts, S. C. & Havlíče, J. Positive relationship between odor identication and aective
responses of negatively valenced odors. Front. Psychol.6, https://doi.org/10.3389/fpsyg.2015.00607 (2015).
109. Preiss, M. Verbální uence, metoda vyšetření pošození mozu u dětí a dospělých. Cesk. Psychol.41, 244–249 (1997).
110. Ferdenzi, C. Variations interindividuelles des comportements olfactifs chez les enfants de 6–12 ans, Université de Bourgogne, (2007).
111. Stevens, J. P. Applied Multivariate Statistics for the Social Sciences. (outledge, 2009).
112. IBM Corp.,IBM Knowledge Center (2017).
113. IBM SPSS Statistics for Windows v. 24 (IBM Corp., Armon, NY, 2016).
114. Development Core Team. A language and environment for statistical computing, (2008).
115. Field, A. Discovering Statistics Using SPSS. (SAGE Publications, 2005).
116. Cumming, G. Understanding e New Statistics: Eect Sizes, Condence Intervals, and Meta-Analysis. (outledge, 2012).
117. missForest: Nonparametric Missing Value Imputation using andom Forest v. 1.4 ( Foundation for Statistical Computing,
Vienna, Austria, 2013).
118. Starweather, J. A new recommended way of dealing with multiple missing values: Using missForest for all your imputation needs.
Benchmarks RSS Matters July 2014 (2014).
119. Waljee, A. . et al. Comparison of imputation methods for missing laboratory data in medicine. BMJ Open 3, https://doi.
org/10.1136/bmjopen-2013-002847 (2013).
120. Pacage ‘missForest’: Nonparametric Missing Value Imputation using andom Forest (Swiss Federal Institute of Technology,
Zürich, Switzerland, 2013).
121. osnow, . L. & osenthal, . Computing contrasts, eect sizes, and counternulls on other people’s published data: General
procedures for research consumers. Psychol. Methods 1, 331–340, https://doi.org/10.1037/1082-989x.1.4.331 (1996).
122. IBM Support.Eect Size: Relationship between partial Eta-squared, Cohen’s f, and Cohen’s d, http://www-01.ibm.com/support/
docview.wss?uid=swg21476421 (2016).
Acknowledgements
e authors would like to express their gratitude to Markéta Sobotková for her help with data collection and
Lydie Kubicová for herassistance with maintaining the participant database. We are very grateful to children
and their parents for their participation, and school principals and teachers for allowing us to perform the study
in school premises. is study is a result of research funded by the project LO1611 with nancial support from
the Ministry of Education, Youth, and Sports (MEYS) under the NPU I program. It has also been supported
by the Charles University Research Centre program No. 204056. Further, LMN was supported by the Specic
Academic Research project (Specický vysokoškolský výzkum, SVV) number 260 469 (“Adaptivní mechanismy
v lidské psychice”) realized at the Faculty of Humanities, Charles University, andby the PROGRES program
Q22 “Antropologická bádání v rámci přírodních, humanitních a historických věd” at the Faculty of Humanities,
Charles University within the Institutional Support for Long-Term Development of Research Organizations from
MEYS. JF andJH were supported by the Czech Science Foundation (18-15168S).e funding sources had no
involvement in study design, in the collection, analysis, and interpretation of data, in the writing of the report, or
in the decision to submit the article for publication. e authors declare that the research was conducted in the
absence of any commercial or nancial relationships that could be construed as a potential conict of interest.
Author Contributions
Conceived and designed the study: L.M.N. and J.H. Performed the study: L.M.N. and J.F. Analyzed the data:
L.M.N. Wrote the paper: L.M.N., J.F. and J.H.
Additional Information
Supplementary information accompanies this paper at https://doi.org/10.1038/s41598-018-20236-0.
Competing Interests: e authors declare no competing interests.
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