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Effects of diversity in olfactory environment on children’s sense of smell


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Diversity in children’s everyday olfactory environment may affect the development of their olfactory abilities and odor awareness. To test this, we collected data on olfactory abilities using the Sniffin’ 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 effects of age and verbal fluency on children’s performance. We found that children’s odor identification and discrimination scores differed as a function of parental odor awareness. Although these effects were rather small, they were commensurate in size with those of gender and age. To the best of our knowledge, this study is the first to present evidence that diversity in children’s olfactory environment affects variability 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. Fulltext is available as of February 13, 2018 at
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SCientifiC RepoRts | (2018) 8:2937 | DOI:10.1038/s41598-018-20236-0
Eects of diversity in olfactory
environment on children’s sense of
Lenka Martinec Nováková
1,2, Jitka Fialová 2,3 & Jan Havlíček
Diversity in children’s everyday olfactory environment may aect the development of their olfactory
abilities and odor awareness. To test this, we collected data on olfactory abilities using the Snin’
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 eects of age and verbal uency on the children’s performance. We found
that the children’s odor identication and discrimination scores diered as a function of parental odor
awareness. Although these eects 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 aects 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” (hereaer 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 eective inhalation of odor stimuli10, not age itself. Gender (or sex) is another commonly used proxy for
individual dierences in olfaction, but simply identifying oneself (or being identied) as male, female, or other
can hardly suce 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 classications11,12. us,
although sex/gender is routinely cited as the second most important demographic factor inuencing olfaction,
and gender dierences in olfaction have been sought by a myriad of researchers13, investigations of specic, con-
crete factors inuencing normal olfactory function, some of which may align with thesex/gender classication,
seem a more productive approach. ese cover, among others, such varied but overlapping and interconnected
areas as genetic outt14, nasal anatomy15, brain anatomy16, respiratory-related physiology17, reproductive hor-
mone inuences18, cognitive functions19, crossmodal interactions20, and cultural inuences21.
Curiously enough, one factor that is being rather overlooked when it comes to interindividual dierences but
is otherwise granted close attention as far as cultural dierences are concerned, is diversity in olfactory environ-
ments and the formative eect of odor exposure. It is widely acknowledged that dierences in olfaction between
individuals coming from dierent cultures stem from long-term, frequent exposure to certain odors within spe-
cic contexts22. ese, in turn, not only come to acquire culturally specic meanings23, but may also be perceived
as more readily identiable 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 dierences 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@
Received: 17 October 2017
Accepted: 12 January 2018
Published: xx xx xxxx
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at which the eects of living in diverse olfactory environments are manifested but they are also sure to give rise to
interindividual dierences 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 dicult to quantify, hence the scarcity of studies on this topic. e rationale behind
this line of inquiry are the eects of perceptual learning, a phenomenon whereby sensory experience brings about
changes in brain function and behavior2931. 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 variationin everyday olfactory environments, most
evidence comes from studies with untrained individuals who underwent a specic 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 identication and discrimination indisputably benet from olfactory training/exposure
in a signicant way33. Findings on olfactory sensitivity are, however, rather contradictory3436. 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 specic anosmia in the case of the16-androstenes39,40. e evidence on the eect 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 identication and awareness on the other44.
We believe that developmental inquiry would particularly benet from considering the formative poten-
tial of odor exposure. e one thing that should make it far more eective (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 signicant 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 modied through the lifestyles we adopt4853. Behaviors and lifestyles may be transmitted
across generations5456 and various aspects of children’s lifestyles are heavily inuenced by their parents57. us,
family appears to play the most crucial role not only in familiarization with specic 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 childrens 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 aect 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 eects 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 ospring 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 acategorical
principal component analysis, we obtained four components of thechildren’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 eects 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 childrens identication, 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.
Eects of diversity of olfactory environment and demographic variables on children’s olfaction
imputed data. A repeated-measures MANOVA showed no signicant within-subject dierences but a mul-
titude of between-subject ones. As can be seen in detail from Table1, these were related, as expected, to age,
gender, and verbal uency, but also to the degree of averaged parental odor awareness. Multivariate tests yielded
eect 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 eect 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 eects of
gender and parental odor awareness pertained to children’s odor identication and discrimination, with Cohens
f 2 ranging between 0.04 and 0.09, indicating eects small in size, but still of “practical” signicance65. Namely,
better olfactory identication and discrimination performance was observed in girls and children whose parents
reported greater odor awareness. Furthermore, thechildrens age at study commencement modestly aected odor
identication and threshold, Cohen’s f 2 = 0.07 and 0.03, respectively, with theolder children exhibiting better
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odor identication and higher sensitivity. Finally, verbal uency had a medium to large eect on thechildren’s
odor awareness, Cohen’s f 2 = 0.31. Specically, thechildren who produced more words on the verbal uency test
received higher scores in the interview.
Eects of diversity of olfactory environment and demographic variables on children’s olfaction
– non-imputed data. As can also be seen from Table1, analyses on non-imputed data (N = 59, 26 boys)
yielded seemingly slightly dierent results. Although this analysis did not show any signicant eect of repeated
measures or interactions involving them, either, it diered from the previous one in that the eect of age and
parental odor awareness waned in terms of theformal level of signicance, while that of the rst component of
odor exposure, named “Food diversity and aroma, appeared. However, as statistical signicance largely depends
on sample size66, which was sub-optimal in the case of non-imputed data, it is advisable to focus on aninterpre-
tation of the eect sizes instead. A quick look at Table1 and comparison of Fig.1 with Supplementary FigureS1
will reveal that the relationship with parental odor awareness remained the same, while the eects 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 eect, 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 identication and exhibited greater odor awareness. Inspection of the other, non-signicant
eects will conrm that they were not dramatically dierent from those in theimputed 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 dierence from those obtained onthe imputed data in terms of eect sizes.
In the present study, we expected that childrens olfactory abilities, particularly odor identication and discrim-
ination, and odor awareness, would be inuenced 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
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
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
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
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
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
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
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
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
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
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 eects (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
theF-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. Signicant
eects (p < 0.05) are highlightedin italics.
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this hypothesis, we found that thechildren’s olfaction was aected by environmental inuences, whether concep-
tualized in terms of parental odor awareness (identication and discrimination, imputed data, small eects) or
parental assessments of thechildren’s olfactory environments (identication and odor awareness, non-imputed
data, medium eects). 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 identication and discrimination scores were on
average higher in girls and the former were also higher in older children, as was olfactory sensitivity. ese eects
were fairly small but still of “practical” signicance. Quite large, on the other hand, was the eect of verbal uency
on thechildren’s odor awareness.
As expected, parental reports of the children’s odor exposure inuenced their ospring’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 dierent inventories of odor exposure were used, diering
slightly in the former and completely in the latter case, in which, moreover, self-reports were provided and a
dierent measure of odor awareness (Odor Awareness Scale)67 was used due to a completely dierent 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 inuence some of the olfactory abilities. As mentioned above, if perceptual learning can bring about
tangible results aer arelatively brief exposure in the laboratory, in real-life settings with its long-term and per-
vasive eects, the opposite would actually be quite surprising. Also, in the latter case, and especially in children,
powerful inuences 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, specic social inuences
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 identication
(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 eective 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 laboratory38,7375 and in professionals (mainly perfumers, wine and beer experts) as compared to naïve
individuals34,35,76. Importantly, the eects 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 inuenced 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 dierentiation for novel odorants related in odor quality or functional
group were also observed aer 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. Dierences
in activation patterns were also observed between individuals with varying levels of olfactory or avour experi-
ence8284. 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
dierent strategies to process odors. Duration of practice and hence the level of expertise only aected 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 eort 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 specic, 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 eects 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 inuence on the proliferative activity of progenitor cells
in the subventricular zone, they did aect the number of newborn neurons in the main olfactory bulb, which,
aer 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 specic, 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 aected 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, aer that, they were able
to do so. is improvement was not specic to the odors they had been exposed to. Hence, there is converging
evidence from multiple empirical methods suggesting that olfactory enrichment aects 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 thechildren 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 haveencouraged their children, overtly or covertly, to make an eort 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 dier-
ing in motivation may be exposed to dierential 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.
Specically 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 theparents 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
havebeen eager to share this knowledge with the interviewer. us, they may not only or necessarily havelived
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, signicant association between theparental and chil-
dren’s odor awareness, which was not the case in the present study (see Supplementary FigureS1).
Among the ndings routinely reported in the literature on the development of the sense of smell was the eect
of gender on odor identication and discrimination24,62,9093. However, a number of studies nevertheless failed to
nd it28,45,61,9498. Since statistical signicance largely depends on sample size66, this discrepancy may be caused by
dierences in sample size, while the eect, 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 gender99101. What is more, between-gender dierences in olfaction may be obscured by gender (non)
conformity or sex-atypicality102. erefore, the focus should shi to concrete factors inuencing normal olfactory
function which tend to align with the sex/gender classication. As noted in the introduction, the majority of
developmental studies nevertheless lend little insight into what the actual causes of these gender/sex dierences
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 eect vanished when verbal prociency (verbal age
and olfactory verbal uency) was controlled for. Another factor might be gender dierences 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 dier depending on whether the child was a boy or a girl and girls did not outperform boys
on either of the two identication tests or on the discrimination one45. More developmental studies are needed to
identify other factors which may help explain the gender dierence in olfactory abilities.
Further, odor identication and threshold were mildly inuenced bythe children’s age at the commence-
ment of the study. is is also routinely reported for odor identication24,61,97, 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 eective 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 eect of verbal uency on theodor awarenessscores. is
is in line with thendings in the original use of the measure62, but not with those in two subsequent studies45,106.
Dierences 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 signicantly so, as the comparison of standard deviations indicated.
Dierent 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 eect size did not even reach the recommended minimum for social sci-
ence data to be regarded at least as small, but of “practical” signicance65. 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 aer children start school.
is is because there may be other moderating or mediating factors at play, aecting 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 childrens olfactory
environment aects variation in their olfactory abilities and odor awareness. Although these eects were small
to medium at best, they were actually commensurate in size with those of demographic variables standardly
reported to inuence 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 leaets to thechildren’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 dier 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 dierence 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 inuenza season. erefore, possible seasonal eects
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on olfactory performance were not taken into account. As can be seen from Table2, 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 theFaculty 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 identication, discrimination, and threshold. is is one of the
most widely used tests of olfactory performance, based on pen-like odor dispensing devices. e Snin’ 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 dierence
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
Identication 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
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 dierence
(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
Identication 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
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 dierence between 1st
and 2nd testing, Snin’ Sticks TDI (threshold, discrimination, identication), 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 dierences between boys and
girls, and their eect sizes expressed as Cohens d. Signicant ndings are highlighted in italics. No corrections
have been made for running multiple tests. Please note that the identication test was only comprised of 12
instead of the original 16 items.
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Odor Identication. e 16-item identication 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, coee, apple, clove, pineapple, rose, anise, and sh (exact chemicals are not specied
by the manufacturer). In the original version of the test cued identication 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 identication test, with higher scores indicating better identication performance. Prior to the
identication 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 dierentiate 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 dierentiate 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 aer 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 identication and childrens 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 signicant 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. Specically, most children tended
to disregard the items to be ranked and oered 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 Table2. e amended version of the questionnaire
used in this study is enclosed in Supplementary TableS2.
Odor Awareness Scale (OAS). To assess individual dierences 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 eect of odors on mood (“When a room has an unpleasant smell, does it inuence 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?”), eect
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,” “oen,” “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 childrens
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 Snin’ Sticks odor identication 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 TableS3. 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 acategorical 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 eect, and inclusion of these items in the CATPCA invariably led to a marked drop in
thepercentage of variance accounted for and a structure of loadings dicult 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 theanalysis. 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 of153 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. Avariable principal normalization
method was selected. Dimensions in solution were determined upon multiple trials to obtain the most inter-
pretable structure of loadings. Specically, 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 signicant and useful for interpretation purposes111. is
is roughly in accord with another recommendation of Stevens111 on component loadings with respect to sample
size. Specically, for N > 140 at α = 0.01, component loadings of about 0.434 or slightly less should be considered
statistically signicant. 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 Table3.
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 briey 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, theassumption 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 dierences were tested
with t-tests. e r and t statistics were converted to Cohen’s d aer 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,
animputation of missing values was performed rst. To achieve this, themissForest 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 dierence (error)119. Default settings were used117,120. Subsequent
multiple t-tests and Pearson’s product-moment correlations did not show any dierence 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 dierences 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-signicant aer controlling for the dierence between the ages at study commencement and com-
pletion. is was true for both theimputed and non-imputed data. eCOBEL, identication, 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 dierences between means was computed aer Rosnow and Rosenthal121.
Partial eta squared produced by SPSS was converted to Cohen’s f 2 aer Cohen63; see also IBM Support122.
Data Availability. e dataset generated and analysed during the present study is available in the Open
Science Framework:
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Component Item Loading
Food diversity and aroma
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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e authors would like to express their gratitude to Markéta Sobotková for her help with data collection and
Lydie Kubicová for herassistance 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 Specic
Academic Research project (Specický vysokoškolský výzkum, SVV) number 260 469 (“Adaptivní mechanismy
v lidské psychice”) realized at the Faculty of Humanities, Charles University, andby 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 andJH 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 conict 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
Competing Interests: e authors declare no competing interests.
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Supplementary resource (1)

February 2018
Lenka Martinec Nováková · Jitka Fialová · Jan Havlicek
... Several odour identification tests have been developed, and it is known that odour identification ability increases through childhood (1)(2)(3)(4)(5)(6)(7)(8)(9) . Olfaction can affect important aspects of life, including brain function, the choice of a future partner (10,11) , and other social activities (10)(11)(12) ; hence, the identification of factors affecting olfaction is important and of significant interest. ...
... Additionally, cultural differences are known to affect the results (8,12) . In adults, it is known that sex (1-5, 7-9, 11-12) , height (2) , weight (2) , body mass index (BMI) (2,4,13) , and sex hormones (2,12) There have been several reports on odour identification and environmental factors in children. ...
... Additionally, cultural differences are known to affect the results (8,12) . In adults, it is known that sex (1-5, 7-9, 11-12) , height (2) , weight (2) , body mass index (BMI) (2,4,13) , and sex hormones (2,12) There have been several reports on odour identification and environmental factors in children. Studies suggest that smoking or passive smoking may affect olfaction in children (4,12) , and those children who help with cooking, are exposed to domestic animals, or have siblings tend to be aware of and are able to recognise related odours (11) . ...
Background: Olfaction plays an important role in our daily and social lives, both as adults and as children. This study assessed whether the ability to identify odours increases with age, as well as the ability in various age groups and the factors involved. Methods: The survey was performed in 2017 on 697 Japanese children (366 girls and 331 boys) aged 6-18 years who lived in Tsunan, Niigata Prefecture, Japan by using the 'Open Essence', a card-type odour identification test. We collected information regarding age, sex, and physical characteristic. We also inquired whether participants had siblings or if members of the family smoked, and whether they had conversations about odour at home. Statistical analysis was performed to evaluate the factors affecting odour identification abilities. Results: The results showed that the odour identification abilities of children increase with age, and children who have daily conversations about odours at home have better odour identification abilities. Conclusions: Odour identification ability increases with age. In addition, our findings suggest that conversation may positively affect odour identification. Hence, it is important for children to be exposed to an environment where they develop an interest in smells for better growth of their olfactory identification ability.
... Current and prior olfactory related behaviors were associated with individual OAS scores (39) . Importantly, the OAS score is related to the degree and diversity (41) of odor exposure (42) . One advantage of the OAS is the wide coverage of situations with odor, such as eating and drinking, civilization, nature and human. ...
... Besides, it is necessary to control the influence of some factors during the process of interviewing, such as language fluency of the interviewer, and guide the children to answer (41,62) . The gender differences revealed by the COBEL had indicated that the stronger odor-orientation of human females is established in childhood (61) . ...
Purpose: Although neglected by science for a long time, the sense of olfaction has received increasing attention from research areas including psychology, neuroscience, clinical medicine and nutrition. With the rise of psychophysical and neuroimaging re- search into olfaction, psychometric tools (e.g. questionnaires and scales) are the basis for the quantitative exploration of inter-in- dividual variability regarding olfactory related responses. The current systematic review is to summarize existing olfaction related questionnaires and/or scales. Methods: Peer-reviewed literature on scales and questionnaires related to perception of odors were searched from online databa- ses (PubMed, Web of Science and PsycINFO). Twenty-one articles that meet the following criteria were included in the review: "hu- man species", "no physical odor stimuli" and "describing the original development of the tool", and "with specific focus on olfaction or odor related responses or behaviors". The psychometric properties, advantages and possible disadvantages were discussed. Results: Existing psychometric measures focus on various aspects of olfactory related responses and behaviors, including af- fective experiences of odor perception, awareness and attitude towards olfaction, olfactory function and the quality of life change due to olfactory dysfunction, and the ability to create vivid mental odor images. While most of them have been tested to have good reliability and validity, some were relatively time-consuming due to the number of questionnaire items. Besides, although many measures have been used in clinical populations, few have provided information on the predictive validity regarding effecti- veness of clinical intervention on changes of certain responses or behaviors. Summary: The current review provides an overview of olfactory related questionnaires and scales, highlighting the emotional and affective impact of olfaction and the impact on quality of life due to olfactory dysfunction. With growing interest in olfaction as an important sense, the development and use of psychometrically sound measurements in conjunction with objective assess- ments will advance our understanding of human olfaction and olfactory dysfunction. The review provides a guide for researchers and clinicians alike to select olfactory scales suitable for olfactory research with different experimental purposes and specific samples.
... Participants' propensity to notice smells and act on them in everyday contexts was evaluated using the 32-item Odor Awareness Scale (OAS) [42]. It was translated into Czech by LMN and Jaroslava Varella Valentova and used in several prior studies [56,57]. Items pertain to the tendency to pay attention to odours ('When you visit someone else's house, do you notice how it smells?'), to seek olfactory stimulation ('Do you sniff a new book?'), and to the effects of chemoreception on mood ('Do you feel cheerful or happy when you pick up a pleasant odour in the air?'), self-grooming ('The smell of smoke or food is still lingering in your clothes from the night before. ...
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Mental activity in sleep may involve visual and auditory content but chemosensory (olfactory and gustatory) experiences are less common and underexplored. The aim of the study was to identify olfaction-related factors that may affect the occurrence of chemosensory dream content. Specifically, we investigated the effects of all-night exposure to an ambient odour, par-ticipants’ appraisal of the present olfactory environment, their general propensity to notice odours and act on them (i.e., odour awareness), and olfactory acuity. Sixty pre-screened healthy young adults underwent olfactory assessment, completed a measure of odour awareness, and spent three nights in weekly intervals in a sleep laboratory. The purpose of the first visit was to adapt them to the experimental setting. On the second visit, half of them were exposed to the smell of vanillin or thioglycolic acid and the other half to the odourless control condition. On the third visit, they received control or stimulation in a balanced order. On each visit, data were col-lected twice: once from the first rapid eye movement (REM) stage that occurred after 3 a.m., and then shortly before getting up, usually from a non-REM stage. The volunteers were asked to report the presence of sensory dream content and to assess their current olfactory environment. Exposure, participants’ assessments of the ambient odour, or olfactory acuity did not affect re-ports of chemosensory content, but they were more frequent in individuals with greater odour awareness. This finding may have implications for treatment when such experiences become unwanted and bothersome.
Moving beyond the “canned” lens on literacies dominant in contemporary literacy studies in Malawi, this study connects theoretical perspectives on sensory and critical literacies to original empirical data on children’s lived “olfactory literacies”. We focus on situational and locally experienced odours in two classrooms in semi-urban Malawi. We present findings from interviews and drawings with 25 children who shared their olfactory preferences with the local researcher. Children’s views were supplemented with the researcher’s and teachers’ evaluations of the olfactory qualities of their classroom environments. Our study advances the field by being the first to unite theoretical provocations on sensory literacies in global child research with critical and empirical insights into children’s local olfactoscapes.
People with profound intellectual and multiple disabilities (PIMD) present intense and complex support needs as well as major motor, communicative, and cognitive limitations. The protocols presented in this chapter describe detailed practical procedures in order to evaluate the food, sensory, and emotional spheres of people with PIMD, taking the sense of smell (discrimination, habituation) and its relations with the emotional system (preferences) as an input modality. The protocols are designed to meet three conditions: (1) to respect the basic methodological principles required for all scientific research, which constitutes the common language of researchers and guarantees the objectivity, rigor, and verifiability of the approach; (2) to form a consistent experimental setting, from study conceptualization to data collection and coding, appropriate for the participants’ characteristics; and (3) build on the person’s ecological environment, in particular the cues allowing the person to be comfortable, safe, and secure, which contributes to the person’s successful participation in and completion of the research.
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Introduction The human sense of smell has different functions which can be categorized as “food,” “social,” and “environment.” Different questionnaires about the importance of olfaction in adults are available, but little attention has been paid to children and adolescents. Therefore, we aimed to develop a questionnaire about children’s personal significance of olfaction (ChiPSO). Methods The questionnaire was developed in two steps. The first questionnaire included 33 statements about the importance of olfactory information in daily life — covering three subscales “food,” “environment,” and “social” administered to 191 participants (mean age: 14.4 ± 1.7 years). The five best fitting items of each subscale were chosen for the final 15-item questionnaire. In the second part, we administered the developed questionnaire to 208 children and adolescents (mean age: 11.5 ± 3.5 years) who additionally underwent olfactory testing to investigate the association between olfactory function and questionnaire results. Participants were separated in two age groups: (i) 6–11 years (children), (ii) 12–17 years (adolescents). Results A significant influence of age on the total ChiPSO score and all three subscales with adolescents scoring higher than children was found. Additionally, there was a significant influence of sex in adolescents on total ChiPSO score and subscales “social” and “food” with girls scoring higher than boys. Conclusion We report an association between questionnaires results and olfactory performance. Additionally, olfactory information seems to be more important to adolescents compared to children and girls compared to boys. Implications The ChiPSO questionnaire is a practical tool to evaluate the importance of olfactory information in children and adolescents aged 6–17 years.
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Background Olfaction provides information on very important dimensions of the environment; however the olfactory abilities of children and young people with profound intellectual and multiple disabilities (PIMD) remain largely unknown. This within-subjects study explores olfactory detection abilities in children with PIMD. Method Twenty-two children and young people with PIMD (7–18 years) were presented with 18 medium intensity odours and an odourless control stimulus. Odorants were presented one by one in a randomised order. The neutral stimulus was presented prior to each odorant. Participants' responses were measured using 21 behavioural indicators. Results Results show that participants make a clear distinction between odorous and neutral conditions, between food and non-food, and between pleasant and unpleasant odours. The detection abilities are manifested by several behaviours, in particular by the duration of the head alignment on the odorant. Conclusions This study shows that participants detect the stimuli and act differently depending on the category.
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Objective Olfaction influences nutrition, safety, and the cognitive development of children. Presently there are few olfactory tests for children, and normative reference values are generally lacking. In this study, we validate the Pediatric Smell Wheel® (PSW) to evaluate olfactory function in Brazilian children. Methods We modified and validated the PSW, a test developed in the United States, for administration in Brazil, and established normative data for Brazilian children. The validation process consisted of five phases: First, we identified odorants familiar to Brazilian children. Second, we established the test-retest reliability of the Brazilian PSW test that employed these odorants. Third, we compared the test scores of healthy children to those microsmic from adenoid hypertrophy. Fourth, we examined the test’s ability to detect improvement in olfactory function before and after adenoidectomy. Finally, we determined a normative 10th percentile cut point for defining microsmia in a sample of 169 healthy Brazilian children between 5 and 12 years of age. Results Eleven odors were identified for inclusion in the test. The test-retest reliability was modest (r = 0.54, p < 0.001), although likely attenuated based on the inclusion of only data from children with normal function. The test clearly differentiated the olfactory function of children with adenoid hypertrophy from that of healthy children and demonstrated the return of function after adenoidectomy. An overall score <7 was found useful in defining hyposmia, although additional age-related cut-points were also defined. Conclusion A Brazilian version of the PSW was developed and validated and found to be efficacious in detecting smell dysfunction in children ranging in age from 5 to 12 years. Level of evidence 1b (Diagnosis).
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Children’s olfactory performance is associated with temperament but whether there is a link with olfactory reactivity and awareness is not known. In adults negative affectivity is linked to reactivity to environmental odours but it is not clear whether these associations extend to children. We aimed to investigate the effect of temperamental factors on olfactory reactivity and awareness. In so doing, we controlled for the effect of parenting styles on temperamental assessment and of verbal fluency on children’s olfactory reactivity and awareness. We hypothesised that children with a high degree of negative affectivity would show greater olfactory reactivity and awareness. 129 children (62 boys, mean age 6.83 ± 0.40 years) were interviewed about their olfactory reactivity and awareness in everyday life using the established Children’s Olfactory Behavior in Everyday Life questionnaire (COBEL). Parents assessed their child’s temperament using the 94-item short form of the Children's Behavior Questionnaire. We found that the relationship between negative affectivity and total COBEL scores varied between the genders: there was a positive, medium to large effect in boys and a negative, small one in girls. Future studies should include behavioural observations of temperament to gain insight into temperamental factors affecting olfactory reactivity and awareness. Fulltext freely available as of August 21, 2017 at
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Since the 1970s, research into ‘Intersex’ has been a central fascination for feminist theorists seeking to make arguments about how men and women are created as social/gender categories. Intersexualization: The Clinic and the Colony takes the case of Olympic runner Caster Semenya as a starting point to explore the issue of determining sex, and the ways in which intersexuality is a ‘threat’ to the distinction between men/women, homosexuality/heterosexuality and white/black. By focusing on the 1950s and the 40 years after, Eckert shows how what she calls intersexualization began in psycho-medical research at the Johns Hopkins Hospital in Baltimore and UCLA, and has from there spread into cross-cultural anthropological accounts conducted in Papua New Guinea and the Dominican Republic. With cross-cultural intersexualization having been largely neglected in recent literature on intersex, this timely volume describes how such intersexualization derives from the combination of medicalization and pathologization through two crucial parts. The first part, “The Clinic,” describes historical psycho-medical material engaging with hermaphroditism ranging from Greek Mythology up to today. This is followed by “The Colony,” which analyzes, in several close-readings, cross-cultural anthropological, sexological and psychoanalytical accounts contributing to cross-cultural intersexualization. Enclosing a wide range of inter-and transdisciplinary approaches to heteronormative and dichotomously organized frames of knowledge and organization, this volume is essential reading for upper-undergraduate and post-graduate students within the fields of gender studies, social studies of medicine, anthropology, science and technology studies, cultural studies, sociology, and history of medicine.
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A body of research predominantly in young adults has suggested a link between olfactory perception, especially sensitivity, and personality characteristics, particularly Neuroticism. Nevertheless, it is not clear whether these associations are present outside this particular age range and whether they involve other olfactory abilities, such as odor identification and discrimination. Also, implicit in such investigations is the assumption of the generalizability of such links, in which case they should already be found in young children and involve general, constitutionally based differences in reactivity and self-regulation, that is, temperament. On the one hand, extrapolating from studies with adults to children, those scoring high on Negative Affectivity, which broadly maps onto Neuroticism, should outperform the low-scoring ones. On the other hand, well-developed self-regulatory processes referred to as Effortful Control, which modulate the expression of such tendencies and manifest themselves in the ability to voluntarily sustain focus on a task, shift attention from one task to another, initiate action and inhibit it, might also contribute to better olfactory performance. Aim and Hypotheses The aim of the present study was to investigate the effect of the temperamental factors on olfactory performance. Namely, we hypothesized that superior olfactory performance would be delivered by children relatively higher on Negative Affectivity as well as those exhibiting greater self-regulation. Methods Odor identification and discrimination in 143 children (72 boys) aged six to eight years were assessed with the Sniffin' Sticks, controlling for their verbal fluency. Parents provided reports of their children's temperament by means of the short form of the Children's Behavior Questionnaire. The potential influence of parental responsiveness and demands on temperamental attributions were controlled for with hypothetical vignettes representing parenting styles. Results There was an effect of Effortful Control (but not Negative Affectivity) on the total identification (but not discrimination) scores. Namely, children who were perceived as more capable of self-regulation exhibited higher odor identification scores. Girls did not outperform boys on either of the olfactory tests but were perceived by their parents as more capable of self-regulation. Conclusions Our findings indirectly point to the effect of self-regulatory processes on odor identification in young children. However, they did not corroborate the idea that individuals varying in neuroticism differ in terms of olfactory performance. Given the narrow age range of children recruited in the present study, further studies with preadolescent and adolescent participants are needed to gain more insight into the nature of these relationships. The final publication is available at: Springer via
This book represents the proceedings from a conference that took place in Dallas in the spring of 1999 which was entitled "Pediatric Gender Assignment - A Critical Reappraisal". Some participants rightfully argued that the conference really focused on the issue of pediatric gender assignment, and that reassignment was not applied in most cases. Their comments were reflected in the title of this monograph. This multidisciplinary meeting was sponsored by a conference grant from the National Institutes of Health, and a broad inquiry into this complex topic took place from many points of view. Basic scientists offered insight into mechanisms of sexual differentiation of the gonads, physical phenotype and imprinting of the central nervous system. Endocrinologists reviewed their experience in diagnosis and management, surgeons described traditional as well as innovative approaches, and there was strong representation from the ethical and behavioral sciences. In putting together such a panel, it was essential that we identify a cast of speakers who could address their viewpoints with strong convictions, and yet not let their passions render the meeting counter productive. We were not disappointed. While many differing points of view were firmly expressed by the panelists and audience, all viewpoints were accorded the respect they deserved. The concept behind the meeting and this book really originated in 1997 shortly after Diamond and Sigmundson published their long term follow up study of the John/Joan case.
in 1951 Oellinek, 1951), until the conference held at the University of Warwick in 1986 there has previously never been a joint meeting of the industrial and academic disciplines relating to the sense of smell. Each year brings the launchings of many new perfumes; the respective national perfumery societies hold meetings; conferences on the sense of smell take place. These events involve the exchange of important knowledge relating to perfumes but the information remains largely isolated. The Warwick Olfaction Research Group is unusual in that it is led by two people, one of whom is a practising perfumer with an understanding of what it means to be asked to create a perfume, and the other a psychologist with an expertise in the area of emotion. Our interaction (Dodd and Van Toller, 1983) was a potent stimulus to hold the First International Conference on the Psychology of Perfumery. The main purpose of the meeting was to see if there was a framework that would knit the area together into a coherent set of ideas and also to give new perspectives to the study of perfumes. We invited speakers from all areas of the discipline. Thus, the meeting brought together people from the fragrance industry, academics and aromatherapists into a forum for debate. Besides the scientific basis of smell and perfumery, other important topics, including the important one of educating the general public about; olfaction and perfume, were discussed.
Over time, family life has lost ground in Western societies. Migration, fewer children per family, the emancipation of women and children, the rise of the number of divorces and other factors have contributed to a process of individualization, which, at least in Western Europe, has caused family bonds to grow less important (NWO 2003). In response to the question ‘who am I?’, fewer people are likely to refer to the family in which they were raised as the defining factor, while more will point to their own particular choices and achievements. Most look at themselves primarily as an individual rather than as a family member. In combination with this development, the naturalness of the family bond and contact among relatives — out of a sense of duty or habit — has increasingly been replaced with a preference for self-chosen contacts. With some relatives, one is in touch, but other relatives one rarely meets if at all.