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Test for screening olfactory function in children
International Journal of Pediatric Otorhinolaryngology 77 (2013) 418–423
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Test for screening olfactory function in children Karolina Dz˙aman a,*, Beata Zielnik-Jurkiewicz b, Dariusz Jurkiewicz c, Marta Molin´ska-Glura d a
ENT Department, Czerniakowski Hospital in Warsaw, 19/25 Stepinska St., 00-739 Warsaw, Poland ENT Department, The Prof. Jan Bogdanowicz Children’s Hospital in Warsaw, 4/24 Nieklanska St., 03-924 Warsaw, Poland c ENT Department, Military Institute of Medicine in Warsaw, 128 Szaserow St., 04-141 Warsaw, Poland d Department of Computer Science and Statistics, Poznan University of Medical Sciences, 79 Da˛browskiego St., 60-529 Poznan, Poland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 August 2012 Received in revised form 3 December 2012 Accepted 4 December 2012 Available online 9 January 2013
Objective: The research determining odors recognizable by children from Poland and Eastern Europe has not been widely described in the literature. The aim of the study was to determine the odors recognizable by Polish children which could be used in a screening olfactory test. Methods: The study was performed in Children’s Hospital in Warsaw. Ninety-one children aged from 2.9 years to 10 years (SD = 5.6 years) were examined, 85 (93.4%) of which completed a full olfactory test. Children were separated into three age groups. The olfactory test consisted of 21 odors. Results: The analysis of the results of all children’s examinations showed statistically significant influence of age on the number of odors identified (p = 0.0001; r = 0.676). The olfactory test score enabled identification of 6 odors to be included in the screening test: bubble gum, lemon, cola, mint, toffee, fish. Correct identification of at least 4 out of them was accepted as a norm and was achieved by 96.5% of children. Conclusions: Olfactory evaluation is possible for children as young as 3 years old. Child’s age influences the number of odors recognized and the specific odors recognition depends also on the home place geographic location and eating habits. Eastern European children most often recognized the following odors: bubble gum, lemon, cola, mint, toffee and fish, as so these odors were considered for olfactory screening test. The 6 odors test has good ability to generalize performance to olfactory status, has normative data and good validity and reliability, is fast, easy and inexpensive to administer. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Smell Odor Olfactory screening Children sense examination Smell identification test
1. Introduction Reception of smell information in children undergoes alterations that begin in early childhood. Research indicates that humans develop the ability to react to olfactory stimuli already during their fetal life. Infants and little children are able to smell and distinguish odors [1], that are a major source of information about food and the surrounding environment [2,3]. Contact with an increasing number of various aromas during human’s lifetime stimulates development and improvement of olfactory function. Scent’s learning lasts the whole life. It is acknowledged that child’s ability to name and remember olfactory stimuli is less developed than in adults as children’s lexicon is too little to define scents [3]. There has never been a census to count the number of people who complain of problems with their senses of smell, but researchers estimate that about 6% percent of the population have loss of smell [4] As yet, there does not appear to have been any
* Corresponding author at: 12 Wiejska St., 05-500 Jozefoslaw, Poland. Tel.: +48 608781068. E-mail address: [email protected] (K. Dz˙aman). 0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2012.12.001
reports of the prevalence of anosmia in children but that appears to be substantially lower than that reported for adults. Whether congenital anosmia (include Kallman’s syndrome) accounts for many cases of children with anosmia remains to be determined. There are a number of conditions occur in early childhood that can lead to either partial or total loss or distortion in olfactory ability. For example, the olfactory system is particularly sensitive to head injuries which may sever the olfactory nerve and result in a complete loss of olfactory ability. Roberts and Simcox [5] found 75% of children with a severe traumatic brain injury suffering from anosmia. Many cases of significant nasal obstructions, such as allergies or enlarged adenoids may also impair olfactory sensitivity. Beyond these known risk factors, there may be additional disease or environmental factors that can impact olfactory ability among young children as dust in their home, chronic rhinosinusitis disease and cystic fibrosis [6]. Olfactory examinations are most frequently conducted in grown or older children. Doctors seldom undertake to asses olfaction in small children. It results from the lack of tools adjusted to examine olfaction in this age group, as well as from the difficulties connected with cooperation with a small patient. Therefore, the methods for olfaction evaluation in children are most frequently borrowed from the methodology applicable to
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adults who are equipped with rich and perfectly developed lexicon for defining scents [7,8]. Diagnosis conducted in such a way, however, raises various doubts, as it is known that all tests for examining a population in developmental age should take into consideration stages of child’s mental development, child’s ability to focus attention as well as possessed lexicon. Thus, by using odor identification tests for adults or older children, younger patients are deliberately excluded. It is frequently the case that doctors do not examine the olfactory function in small children considering the results to be not very reliable [9]. It seems, however, that an adequately designed olfactory test may serve as a dependable assessment of olfactory function in children [10]. For these reasons, we are interested in development of test to screen children at an early age for olfactory function. A grave problem while conducting an olfactory examination in the group of children is selecting test odors. The stimuli have to be well-known and frequently encountered in the child’s surroundings for the possibility of recognizing them by a little patient. Aromas surrounding a child in its everyday life differ depending on the country of origin and culinary traditions of a certain region of the world. Tests based on odors easily recognizable by residents of a certain country may cause trouble for children from a different region of the world [11]. Research determining odors recognizable by children from Poland and Eastern Europe has not been widely described in the literature. Therefore, the aim of the study was to determine the odors recognizable by Polish children which could be used in a screening olfactory test. Moreover, the correlation between olfactory test results and child’s age was examined. 2. Methods Ninety one children admitted to the Prof. Jan Bogdanowicz Children’s Hospital in Warsaw were included in the analyses, that
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after a case history and laryngology examination showed no symptoms of olfaction disorders or any illnesses that could influence the functioning of olfaction. The examined children range from 2.9 years to 10 years, 85 children (93.4%) completed a full olfactory test and only those were put through the analysis (43 girls, 42 boys). The remaining 6 persons did not complete the examination due to either parent’s shortage of time (3 persons) or impossibility of further concentration of child’s attention (3 persons). Having taken the age of children into consideration, they were separated into three groups: Group I – (37 persons; 20 girls, 17 boys) children below the age of 5, (av. 4 years, SD = 0.48); Group II – (30 persons; 14 girls, 16 boys) children from 5 years to 7 years old, (av. 5.74 years, SD = 0.52) Group III – (18 persons; 9 girls, 9 boys) children over 7 up to 10 years old, (av. 8.87 years, SD = 0.64) Different quantity of children in these groups is a result that nasal patency disturbances have been more often noticed in older children which excluded them from the study (e.g. nasal septum deviation, chronic rhinosinusitis, antrochoanal polyps). The test consisted of 21 odors (Table 1), chosen from stimuli used in the most well-known olfactory tools: Sniffin Stick test [12], UPSIT [13], CCCRC [14], CC-SIT [11]. The aromas were placed in bottles made from dark glass which were labeled with codes. After having unscrewed a cap, a bottle was moved for 3 s over nostrils, in a distance of about 2 cm from nostrils. At the same time a child was shown 3 pictures and was asked to indicate a picture that best illustrates the odor. The name of the odor under the picture was read out loudly each time. The olfactory stimuli were presented in 20 s intervals at the minimum, in a different order for each child. The test was done each time by the same doctor. The examination was conducted in a quiet room and took about 10 min. For the results to be more reliable, a parent provided information on the things a particular
Table 1 Odor identification by children in three age groups. Odors
Strawberry Pineapple Lemon Apple Rose Chocolate Cola Vanilla Cinnamon Toffee Licorice Anise Bubble gum Garlic Mint Banana Peach Orange Coffee Cake Fish An average number of recognized aromas
GROUP I <5 years old (37 persons)
GROUP II 5–7 years old (30 persons)
GROUP III 7–10 years old (18 persons)
3 years 4 years Summary 2 years 2 persons 14 persons 21 persons persons (% of the group)
5 years 6 years Summary 16 persons 14 persons persons (% of the group)
7 years 8 years 9 years 10 years Summary 4 persons 6 persons 6 persons 2 persons persons (% of the group)
0 1 1 0 0 1 1 0 1 2 2 2 1 0 1 1 1 1 1 1 1
12 10 16 3 5 11 16 10 14 16 12 5 11 13 14 9 13 11 13 7 14
4 4 4 2 2 4 4 4 4 4 4 4 4 4 4 2 2 4 4 4 4
6 6 9 7 5 6 10 8 7 12 8 6 13 11 9 10 5 9 7 8 14
17 10 21 9 2 14 19 12 16 15 13 4 20 14 19 13 12 15 17 17 13 13.16
23 17 31 16 7 21 30 20 24 29 23 12 34 25 29 24 18 25 25 26 28
(62.2%) (45.9%) (83.8%) (43.2%) (18.9%) (56.8%) (81.1%) (54.1%) (64.9%) (78.4%) (62.2%) (32.4%) (91.9%) (67.6%) (78.4%) (64.9%) (48.6%) (67.6%) (67.6%) (70.3%) (75.7%)
12 14 9 7 9 12 14 12 14 14 10 5 14 10 14 12 11 7 11 12 11 15.63
24 24 25 10 14 23 30 22 28 30 22 10 25 23 28 21 24 18 24 19 25
(80.0%) (80.0%) (83.3%) (33.3%) (46.7%) (76.7%) (100%) (73.3%) (93.3%) (100%) (73.3%) (33.3%) (83.3%) (76.7%) (93.3%) (70.0%) (80.0%) (60.0%) (80.0%) (63.3%) (83.3%)
2 2 2 6 6 6 6 6 6 6 6 6 6 6 6 4 2 2 6 6 6
4 6 6 4 4 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
0 2 2 0 0 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 18.67
10 14 14 12 12 18 18 18 18 18 18 18 18 18 18 14 12 14 18 18 18
(55.6%) (77.8%) (77.8%) (66.7%) (66.7%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (77.8%) (66.7%) (77.8%) (100%) (100%) (100%)
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odor can be associated with when it comes to a particular child. After having obtained an answer, a guessed name of the odor was marked without denoting it as right or wrong. All data were entered and maintained in a Statview database and analyzed using STATISTICA 6pl Program. Calculations of Chisquared Pearson’s correlation coefficient (C) and linear correlation (r) were used in the assessment of interrelations within the data. 3. Results The statistical analysis was employed to examine the influence of sex and age on the obtained olfactory test result. Sex influenced neither the number (p = 0.597; C = 0.090), nor the type of identified stimuli (p > 0.05). The analysis of the results of all children’s examinations showed statistically significant influence of age on the number of odors identified (p = 0.0001; r = 0.676). Only in the group of the oldest children, above the age of 7, no correlation of age with the olfactory test result was observed (p = 0.453; r = 0.189). The average number of the odors correctly identified by all children was 15 (72%): group I – 13 (62.%), group II – 16 (76%), group III – 19 (90%). Percentage distribution of children who identified a particular number of odors in each group is presented in Table 1. The most recognized stimuli by all the children were the odor of cola, bubble gum and toffee (the correct answers provided respectively by 91.8%; 90.6%; 90.6% of subjects), and the least recognized were the aromas of rose and apple (respectively 39%; 45% of subjects) (Fig. 1). Among 21 odors tested by 85 children, the 75% recognizability threshold was exceeded by 9 odors in average (Fig. 1), (gr. I – 6 odors, gr. II – 13 odors, gr. III – 17 odors).
The analysis of all children’s responses after exposing them to smell of bubble gum, lemon, cola, mint, toffee and fish (proposed screening test) showed that – 40 persons (47%) correctly recognized all 6 odors, 31 (36.5%) – 5 odors, 11 (13%) – 4 odors, and 3 (3,5%) – 3 odors. A norm widely accepted by other authors is also implemented in the present study. As a result, the correct identification of 75% of test odors, that is at least 4 out of 6 olfactory stimuli used in the screening test, was accepted as a norm. The threshold was exceeded and thus the norm was achieved by 96.5% of the examined children. The screening test results in relation to the children’s age has been shown in Fig. 2. Reliability and validity of the final -6 odors test were made on the assumption that satisfactory level of specific odor recognize was 90% with statistical analysis based on test Z for proportion. Additional validation of the final test was carried out on a group of 30 children (10 children from each group). Those children were given to recognize the 6 odors test in 4-fold repetitions in order to determine whether the odor is recognizable every time. After familiarizing children with 6 scents, the odors were tested again but mixed, so the same odor cannot be recognized one by one. Revalidation - after 2weeks period validation was repeated to confirm its effectiveness. Diagnostic validation data obtained from each group have been shown in Table 2. The test was useful in children aged about 3 years and older. There was an appreciable age trend in the variability of the scores on the identification task (Table 2). Only for one odor – fish aroma, in the youngest group of children we noticed statistically significant difference in odor recognition level compare to satisfactory level on the assumption (90% efficacy level). But if we took under consideration the 80% level specific odor recognition was with a good efficacy in each group of children. Additional validation of the 6 odors test in 4-fold repetitions has received similar data. Results on the 6 odors test from healthy children showed satisfactory test–retest reliability, split-half reliability and validity. We compared the age trends in variability of scores on the 6 odors test with those on an odorant identification task, using a
Fig. 1. Recognizing particular odors by all the children. The odors recognized by at least 75% of the children were labeled in cyan. (For interpretation of the references to color in the artwork, the reader is referred to the web version of the article.)
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100% 6
90% 80% 70%
18 14
60%
6 odors
20
50%
5 odors 4 odors
40% 30%
3 odors
7
20%
6
10% 0%
4
5
3
group II
group I
group III
Fig. 2. The screening test results in relation to the children’s age. Determined amount of children in each group have recognized indicated quantity of odors in the screening test. Children labeled in yellow did not meet the specified norm. (For interpretation of the references to color in the artwork, the reader is referred to the web version of the article.)
Table 2 Data of test Z for proportion for 6-odors test. 6-odors test
Cola Toffee Chewing gum Mint Lemon Fish
Group I
Group II
Group III
Recognition
Error
Test Z for proportion (p value)
Recognition
Error
Test Z for proportion (p value)
Recognition
Error
Test Z for proportion (p value)
30 29 34 29 31 28
7 8 3 8 6 9
0.142 0.0548 0.972 0.054 0.319 0.018
30 30 25 28 25 25
0 0 5 2 5 5
1 1 0.350 0.822 0.350 0.350
18 18 18 18 14 18
0 0 0 0 4 0
1 1 1 1 0.196 1
weighted linear regression analysis. It showed statistically significant influence of age on the olfactory test result.
4. Discussion There have been no reports on the olfactory function disturbances prevalence in children but many cases of children with anosmia remain to be determined. Individual patients and their parents are seldom aware of olfactory deficits and concluded that formal assessment of olfactory function is imperative. Evaluations of young children and identification of any deficits may be particularly important if critical periods for olfactory system development exist as have been shown for the gustatory system [15,16]. Thus we were interested in development of test to screen children at an early age for olfactory function. Most of the existing tests utilize odor stimuli that would be unfamiliar to many children that limits their use across diverse populations, and necessitate the development of culture-specific test versions. The presented results of the examination determine the types of odors that Polish children aged from 2.9 to 10 years were able to identify. From among 21 odors used in the most well-known olfactory tests only 6 (smell of: cola, bubble gum, toffee, mint, fish and lemon) were identified by the youngest children (2.9–5 years old) with the frequency of 75% making it possible to include them in screening tests. Thus, those may serve as screening olfactory examination for Polish children (Table 1). Recognizing an odor by 75% of a healthy population is thought to be the threshold to include the odor in the olfactory test [12]. The number of commonly identified odors was increasing with age, and therefore it is possible to extend the 6-element olfactory test by other olfactory stimuli which were recognized in 75% of the instances in a particular age group. The test can be extended by 7
odors in the group of 5–7 years old and by 11 odors in the group of children above 7 years old (Table 1). A surprising result was a low identification rate of apple and rose smell – stimuli included in many well-known olfactory tests [17] (Sniffin Stick test, CC-SIT). That confirms that the examination methods cannot be uncritically transferred from an adult population into children’s population. The results obtained alter our knowledge about children olfactory screening. Many researchers believe that olfactory assessment based on psychophysical tests is possible only for children that are more than 5 years old, and for younger patients different measures are proposed [18]. These include, however, less available and often still experimental examinations, i.e. olfactory-evoked cortical potential [3,19]. It probably results from a significant peculiarity of tools employed in examining children. The present study describes the methodology of conducting olfactory tests on children. It could be more acceptable by a little patient as possible and give more reliable results of olfactory function assessment. We tried to use the UPSIT, pen-like odor test and Elsberg-Levy olfactometry to asses olfactory function in children but it was very difficult thus we have been looking for more suitable test. Based on our experience the number of stimuli employed in tools for examining children has to be fewer than in respective tools used for adults due to the examination’s duration as well as children’s quicker lack of concentration and boredom caused by the examination. Performing the test as a game exercise – a guessing game with colorful pictures that make children connect them with odors – assures the increase of examination’s reliability. Hence, in the present study the authors tried to create a test that could be easy and quick to conduct, treated by a child as a game and finally minimalizing the influence of verbal and cognitive abilities on the outcome. The name of the odor under the picture was read
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out loudly each time. Based on our previous experiences we found out that the list of odors presented on paper is not effective in children, because some of the children aged between 2, 9 and 10 years old could not read yet. Verbally read out name of a specific odor was not enough as well because some of the odors e.g. mint was colligated to a toothpaste or refresh - sweets but the term ‘‘mint’’ itself or image of a mint leaf – was unknown to many children. Thus for much more reliable results, a parent provided information about such products which can be related to specific odors and asked to give a brief instructions on the proper choice of the picture that could be best recognized by a child. From among 21 odors only the most easily recognizable by children were selected: in group I – 6 odors, in group II – 13 odors, and in group III – 17 odors. Only 6 children (6.6%) from the group of 91 did not complete the examination due to either parent’s lack of time for continuing the examination (3 persons) or child’s lack of concentration (3 persons). These were the youngest children (group aged 2.9–5 years). The data differ from data collected by other authors. Hummel et al. [3] in a group of patients aged from 3 to 5 obtained 44% of unfinished tests. Perhaps it results from using Sniffin Stick test intended to examine an adult population for the olfactory evaluation of children [17]. From the authors’ experience it follows that this test is unsuitable for children’s examination. The time of conducting the Sniffin Stick test is too long (about 30 min) and as was confirmed in our research, this test includes odors unfamiliar to children. The presented single 21-odor examination took about 10 min, and screening test composed of 6 odors took 3– 4 min. That is a few times shorter than the Sniffin Stick test. Other researchers have similar observations [19]. The aim of authors was simplification of the method. Despite the fact that this leads to diminishing the knowledge about functioning of olfaction, it seems to be a more adequate method to evaluate olfaction in little children. The choice of stimuli employed in the examination was based on the odors used in the most popular olfactory tests. Children were able to identify on average 15 (72%) odors from 21 presented. This result indicates that a part of the aromas commonly included in olfactory tests is not sufficiently wellknown to the children in this part of Europe. The set of six the most recognized odors seems to be the most suitable for a quick evaluation of olfaction in Polish children. The results obtained after exposition to some stimuli – e.g. anise, apple or rose – were situated at the very border of recognizability, what is significant mainly in a context of using these odors in olfactory examination of children by some authors [17,20]. In accordance with other authors’ reports [18] the number of correctly identified stimuli by children was significantly increasing along with age (an average number of correct answers in group I – 13, in group II – 16, and in group III – 19). The evaluation of olfactory function in children provides many problems resulting mainly from the lack of satisfactory diagnosis methods. The presented examination results enable creating a test for screening olfactory function in children from this part of Europe and simultaneously they confirm that uncritical mapping of olfactory tools for diagnosing adults onto children’s population raises controversies and doubts when it comes to the validity of such proceedings. The 6-odors test was developed to address the need for a culturally valid odor-identification test for clinical use on the Polish population. Six odorous test stimuli were selected that were relatively identifiable, familiar, strong in intensity according to healthy participants. Four response alternatives were then selected for each final test stimulus based on a confusion matrix of identification rates obtained from healthy participants, in a manner that controlled for task difficulty.
5. Conclusions The aim of the present article was to determine the possibility of olfactory examination in children and to identify the aromas that are recognizable by Polish children. The results obtained suggest that olfactory examinations conducted by psychophysical methods are possible to execute in small children, yet the tests need to be strictly adjusted to an age group. The article presents a proposal of the olfactory screening test in which the aromas that were the most easily recognized by children from this part of Europe are included. The research conducted confirms the influence of age on the number of recognized odors as well as the lack of significant differences in olfactory test results when it comes to sex of subjects. 1. Olfactory evaluation is possible in children as young as 3 years old. Child’s age influences the number of odors recognized. 2. The odors that were most easily recognized by children were: bubble gum, lemon, cola, mint, toffee and fish. Those odors may be used in an olfactory screening test. 3. The 6 odors test has good ability to generalize performance to olfactory status, has normative data and good validity and reliability, is fast, easy and inexpensive to administer.
Conflict of interest statement The authors have no conflicts of interest to disclose. Role of the funding source No external funding was secured for this study. Patient consent and ethics The study got the Ethics Committee approval no 99/WIM. Acknowledgements We express thanks to Jaskulski Aromaty JAR company from Warsaw for donating the odors necessary for conducting the research. References [1] C.G. Pomares, J. Schirrer, V. Abadie, Analysis of the olfactory capacity of healthy children before language acquisition, J. Dev. Behav. Pediatr. 23 (4) (2002) 203–207. [2] B. Schaal, T. Hummel, R. Soussignan, Olfaction in the fetal and premature infant: functional status and clinical implications, Clin. Perinatol. 31 (2) (2004) 261–285. [3] T. Hummel, M. Bensafi, J. Nikolaus, M. Knecht, D.G. Laing, B. Schaal, Olfactory function in children assessed with psychophysical and electrophysiological techniques, Behav. Brain Res. 180 (2) (2007) 133–138. [4] A. Bra¨merson, L. Johansson, L. Ek, S. Nordin, M. Bende, Prevalence of olfactory dysfunction: the Skovde population-based study, Laryngoscope 114 (4) (2004) 733–737. [5] M.A. Roberts, A.F. Simcox, Assessing olfaction following pediatric traumatic brain injury, Appl. Neuropsychol. 3 (2) (1996) 86–88. [6] D.G. Laing, J.E. Armstrong, M. Aitken, A. Carroll, F.J. Wilkes, A.L. Jinks, et al., Chemosensory function and food preferences of children with cystic fibrosis, Pediatr. Pulmonol. 45 (8) (2010) 807–815. [7] R.A. Frank, M.F. Dulay, K.A. Niergarth, R.C. Gesteland, A comparison of the sniff magnitude test and the University of Pennsylvania Smell Identification Test in children and nonnative English speakers, Physiol. Behav. 81 (3) (2004) 475–480. [8] F.R. Karsz, A. Vance, V.A. Anderson, P.G. Brann, S.J. Wood, C. Pantelis, et al., Olfactory impairments in child attention-deficit/hyperactivity disorder, J. Clin. Psychiatry 69 (9) (2008) 1462–1468. [9] R.A. Richman, E.M. Post, P.R. Sheehe, H.N. Wright, Olfactory performance during childhood. I. Development of an odorant identification test for children, J. Pediatr. 121 (6) (1992) 908–911. [10] P. Dalton, J.A. Mennella, B.J. Cowart, C. Maute, E.A. Pribitkin, J.S. Reilly, Evaluating the prevalence of olfactory dysfunction in a pediatric population, Ann. N. Y. Acad. Sci. 1170 (2009) 537–542. [11] R.L. Doty, A. Marcus, W.W. Lee, Development of the 12-item cross-cultural Smell Identification Test (CC-SIT), Laryngoscope 106 (1996) 353–356.
K. Dz˙aman et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 418–423 [12] T. Hummel, B. Sekinger, S.R. Wolf, E. Pauli, G. Kobal, ’Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification. odor discrimination and olfactory threshold, Chem. Senses 22 (1) (1997) 39–52. [13] R.L. Doty, U. Agrawal, The shelf life of the University of Pennsylvania Smell Identification Test (UPSIT), Laryngoscope 99 (4) (1989) 402–404. [14] W.S. Cain, J.F. Gent, R.B. Goodspeed, G. Leonard, Evaluation of olfactory dysfunction in the Connecticut Chemosensory Clinical Research Center, Laryngoscope 98 (1) (1988) 83–88. [15] J.A. Mennella, C.P. Jagnow, G.K. Beauchamp, Prenatal and postnatal flavor learning by human infants, Pediatrics 107 (6) (2001) 88. [16] J.A. Mennella, G.K. Beauchamp, Olfactory preferences in children and adults, in: D.G. Laing, R.L. Doty, W. Breipohl (Eds.), The Human Sense of Smell, vol. 1991, Springer-Verlag, New York, 1992, pp. 167–180.
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[17] I. Konstantinidis, S. Triaridis, A. Triaridis, I. Petropoulos, K. Karagiannidis, G. Kontzoglou, How do children with adenoid hypertrophy smell and taste? Clinical assessment of olfactory function pre- and post-adenoidectomy, Int. J. Pediatr. Otorhinolaryngol. 69 (10) (2005) 1343–1349. [18] D.G. Laing, C. Segovia, T. Fark, O.N. Laing, A.L. Jinks, J. Nikolaus, et al., Tests for screening olfactory and gustatory function in school-age children, Otolaryngol. Head Neck Surg. 139 (1) (2008) 74–82. [19] M. Knecht, J. Nikolaus, K.B. Huttenbrink, Olfactory function in children – results from psychophysical and electrophysiological investigations, HNO – Inf. 29 (2004) 122. [20] A. Obre˛bowski, Z. Obre˛bowska-Karsznia, M. Gawlin´ski, Smell and taste in children with simple obesity, Int. J. Pediatr. Otorhinolaryngol. 55 (3) (2000) 191–196.
Contents lists available at SciVerse ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Test for screening olfactory function in children Karolina Dz˙aman a,*, Beata Zielnik-Jurkiewicz b, Dariusz Jurkiewicz c, Marta Molin´ska-Glura d a
ENT Department, Czerniakowski Hospital in Warsaw, 19/25 Stepinska St., 00-739 Warsaw, Poland ENT Department, The Prof. Jan Bogdanowicz Children’s Hospital in Warsaw, 4/24 Nieklanska St., 03-924 Warsaw, Poland c ENT Department, Military Institute of Medicine in Warsaw, 128 Szaserow St., 04-141 Warsaw, Poland d Department of Computer Science and Statistics, Poznan University of Medical Sciences, 79 Da˛browskiego St., 60-529 Poznan, Poland b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 1 August 2012 Received in revised form 3 December 2012 Accepted 4 December 2012 Available online 9 January 2013
Objective: The research determining odors recognizable by children from Poland and Eastern Europe has not been widely described in the literature. The aim of the study was to determine the odors recognizable by Polish children which could be used in a screening olfactory test. Methods: The study was performed in Children’s Hospital in Warsaw. Ninety-one children aged from 2.9 years to 10 years (SD = 5.6 years) were examined, 85 (93.4%) of which completed a full olfactory test. Children were separated into three age groups. The olfactory test consisted of 21 odors. Results: The analysis of the results of all children’s examinations showed statistically significant influence of age on the number of odors identified (p = 0.0001; r = 0.676). The olfactory test score enabled identification of 6 odors to be included in the screening test: bubble gum, lemon, cola, mint, toffee, fish. Correct identification of at least 4 out of them was accepted as a norm and was achieved by 96.5% of children. Conclusions: Olfactory evaluation is possible for children as young as 3 years old. Child’s age influences the number of odors recognized and the specific odors recognition depends also on the home place geographic location and eating habits. Eastern European children most often recognized the following odors: bubble gum, lemon, cola, mint, toffee and fish, as so these odors were considered for olfactory screening test. The 6 odors test has good ability to generalize performance to olfactory status, has normative data and good validity and reliability, is fast, easy and inexpensive to administer. ß 2012 Elsevier Ireland Ltd. All rights reserved.
Keywords: Smell Odor Olfactory screening Children sense examination Smell identification test
1. Introduction Reception of smell information in children undergoes alterations that begin in early childhood. Research indicates that humans develop the ability to react to olfactory stimuli already during their fetal life. Infants and little children are able to smell and distinguish odors [1], that are a major source of information about food and the surrounding environment [2,3]. Contact with an increasing number of various aromas during human’s lifetime stimulates development and improvement of olfactory function. Scent’s learning lasts the whole life. It is acknowledged that child’s ability to name and remember olfactory stimuli is less developed than in adults as children’s lexicon is too little to define scents [3]. There has never been a census to count the number of people who complain of problems with their senses of smell, but researchers estimate that about 6% percent of the population have loss of smell [4] As yet, there does not appear to have been any
* Corresponding author at: 12 Wiejska St., 05-500 Jozefoslaw, Poland. Tel.: +48 608781068. E-mail address: [email protected] (K. Dz˙aman). 0165-5876/$ – see front matter ß 2012 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2012.12.001
reports of the prevalence of anosmia in children but that appears to be substantially lower than that reported for adults. Whether congenital anosmia (include Kallman’s syndrome) accounts for many cases of children with anosmia remains to be determined. There are a number of conditions occur in early childhood that can lead to either partial or total loss or distortion in olfactory ability. For example, the olfactory system is particularly sensitive to head injuries which may sever the olfactory nerve and result in a complete loss of olfactory ability. Roberts and Simcox [5] found 75% of children with a severe traumatic brain injury suffering from anosmia. Many cases of significant nasal obstructions, such as allergies or enlarged adenoids may also impair olfactory sensitivity. Beyond these known risk factors, there may be additional disease or environmental factors that can impact olfactory ability among young children as dust in their home, chronic rhinosinusitis disease and cystic fibrosis [6]. Olfactory examinations are most frequently conducted in grown or older children. Doctors seldom undertake to asses olfaction in small children. It results from the lack of tools adjusted to examine olfaction in this age group, as well as from the difficulties connected with cooperation with a small patient. Therefore, the methods for olfaction evaluation in children are most frequently borrowed from the methodology applicable to
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adults who are equipped with rich and perfectly developed lexicon for defining scents [7,8]. Diagnosis conducted in such a way, however, raises various doubts, as it is known that all tests for examining a population in developmental age should take into consideration stages of child’s mental development, child’s ability to focus attention as well as possessed lexicon. Thus, by using odor identification tests for adults or older children, younger patients are deliberately excluded. It is frequently the case that doctors do not examine the olfactory function in small children considering the results to be not very reliable [9]. It seems, however, that an adequately designed olfactory test may serve as a dependable assessment of olfactory function in children [10]. For these reasons, we are interested in development of test to screen children at an early age for olfactory function. A grave problem while conducting an olfactory examination in the group of children is selecting test odors. The stimuli have to be well-known and frequently encountered in the child’s surroundings for the possibility of recognizing them by a little patient. Aromas surrounding a child in its everyday life differ depending on the country of origin and culinary traditions of a certain region of the world. Tests based on odors easily recognizable by residents of a certain country may cause trouble for children from a different region of the world [11]. Research determining odors recognizable by children from Poland and Eastern Europe has not been widely described in the literature. Therefore, the aim of the study was to determine the odors recognizable by Polish children which could be used in a screening olfactory test. Moreover, the correlation between olfactory test results and child’s age was examined. 2. Methods Ninety one children admitted to the Prof. Jan Bogdanowicz Children’s Hospital in Warsaw were included in the analyses, that
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after a case history and laryngology examination showed no symptoms of olfaction disorders or any illnesses that could influence the functioning of olfaction. The examined children range from 2.9 years to 10 years, 85 children (93.4%) completed a full olfactory test and only those were put through the analysis (43 girls, 42 boys). The remaining 6 persons did not complete the examination due to either parent’s shortage of time (3 persons) or impossibility of further concentration of child’s attention (3 persons). Having taken the age of children into consideration, they were separated into three groups: Group I – (37 persons; 20 girls, 17 boys) children below the age of 5, (av. 4 years, SD = 0.48); Group II – (30 persons; 14 girls, 16 boys) children from 5 years to 7 years old, (av. 5.74 years, SD = 0.52) Group III – (18 persons; 9 girls, 9 boys) children over 7 up to 10 years old, (av. 8.87 years, SD = 0.64) Different quantity of children in these groups is a result that nasal patency disturbances have been more often noticed in older children which excluded them from the study (e.g. nasal septum deviation, chronic rhinosinusitis, antrochoanal polyps). The test consisted of 21 odors (Table 1), chosen from stimuli used in the most well-known olfactory tools: Sniffin Stick test [12], UPSIT [13], CCCRC [14], CC-SIT [11]. The aromas were placed in bottles made from dark glass which were labeled with codes. After having unscrewed a cap, a bottle was moved for 3 s over nostrils, in a distance of about 2 cm from nostrils. At the same time a child was shown 3 pictures and was asked to indicate a picture that best illustrates the odor. The name of the odor under the picture was read out loudly each time. The olfactory stimuli were presented in 20 s intervals at the minimum, in a different order for each child. The test was done each time by the same doctor. The examination was conducted in a quiet room and took about 10 min. For the results to be more reliable, a parent provided information on the things a particular
Table 1 Odor identification by children in three age groups. Odors
Strawberry Pineapple Lemon Apple Rose Chocolate Cola Vanilla Cinnamon Toffee Licorice Anise Bubble gum Garlic Mint Banana Peach Orange Coffee Cake Fish An average number of recognized aromas
GROUP I <5 years old (37 persons)
GROUP II 5–7 years old (30 persons)
GROUP III 7–10 years old (18 persons)
3 years 4 years Summary 2 years 2 persons 14 persons 21 persons persons (% of the group)
5 years 6 years Summary 16 persons 14 persons persons (% of the group)
7 years 8 years 9 years 10 years Summary 4 persons 6 persons 6 persons 2 persons persons (% of the group)
0 1 1 0 0 1 1 0 1 2 2 2 1 0 1 1 1 1 1 1 1
12 10 16 3 5 11 16 10 14 16 12 5 11 13 14 9 13 11 13 7 14
4 4 4 2 2 4 4 4 4 4 4 4 4 4 4 2 2 4 4 4 4
6 6 9 7 5 6 10 8 7 12 8 6 13 11 9 10 5 9 7 8 14
17 10 21 9 2 14 19 12 16 15 13 4 20 14 19 13 12 15 17 17 13 13.16
23 17 31 16 7 21 30 20 24 29 23 12 34 25 29 24 18 25 25 26 28
(62.2%) (45.9%) (83.8%) (43.2%) (18.9%) (56.8%) (81.1%) (54.1%) (64.9%) (78.4%) (62.2%) (32.4%) (91.9%) (67.6%) (78.4%) (64.9%) (48.6%) (67.6%) (67.6%) (70.3%) (75.7%)
12 14 9 7 9 12 14 12 14 14 10 5 14 10 14 12 11 7 11 12 11 15.63
24 24 25 10 14 23 30 22 28 30 22 10 25 23 28 21 24 18 24 19 25
(80.0%) (80.0%) (83.3%) (33.3%) (46.7%) (76.7%) (100%) (73.3%) (93.3%) (100%) (73.3%) (33.3%) (83.3%) (76.7%) (93.3%) (70.0%) (80.0%) (60.0%) (80.0%) (63.3%) (83.3%)
2 2 2 6 6 6 6 6 6 6 6 6 6 6 6 4 2 2 6 6 6
4 6 6 4 4 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6
0 2 2 0 0 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 2 18.67
10 14 14 12 12 18 18 18 18 18 18 18 18 18 18 14 12 14 18 18 18
(55.6%) (77.8%) (77.8%) (66.7%) (66.7%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (77.8%) (66.7%) (77.8%) (100%) (100%) (100%)
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odor can be associated with when it comes to a particular child. After having obtained an answer, a guessed name of the odor was marked without denoting it as right or wrong. All data were entered and maintained in a Statview database and analyzed using STATISTICA 6pl Program. Calculations of Chisquared Pearson’s correlation coefficient (C) and linear correlation (r) were used in the assessment of interrelations within the data. 3. Results The statistical analysis was employed to examine the influence of sex and age on the obtained olfactory test result. Sex influenced neither the number (p = 0.597; C = 0.090), nor the type of identified stimuli (p > 0.05). The analysis of the results of all children’s examinations showed statistically significant influence of age on the number of odors identified (p = 0.0001; r = 0.676). Only in the group of the oldest children, above the age of 7, no correlation of age with the olfactory test result was observed (p = 0.453; r = 0.189). The average number of the odors correctly identified by all children was 15 (72%): group I – 13 (62.%), group II – 16 (76%), group III – 19 (90%). Percentage distribution of children who identified a particular number of odors in each group is presented in Table 1. The most recognized stimuli by all the children were the odor of cola, bubble gum and toffee (the correct answers provided respectively by 91.8%; 90.6%; 90.6% of subjects), and the least recognized were the aromas of rose and apple (respectively 39%; 45% of subjects) (Fig. 1). Among 21 odors tested by 85 children, the 75% recognizability threshold was exceeded by 9 odors in average (Fig. 1), (gr. I – 6 odors, gr. II – 13 odors, gr. III – 17 odors).
The analysis of all children’s responses after exposing them to smell of bubble gum, lemon, cola, mint, toffee and fish (proposed screening test) showed that – 40 persons (47%) correctly recognized all 6 odors, 31 (36.5%) – 5 odors, 11 (13%) – 4 odors, and 3 (3,5%) – 3 odors. A norm widely accepted by other authors is also implemented in the present study. As a result, the correct identification of 75% of test odors, that is at least 4 out of 6 olfactory stimuli used in the screening test, was accepted as a norm. The threshold was exceeded and thus the norm was achieved by 96.5% of the examined children. The screening test results in relation to the children’s age has been shown in Fig. 2. Reliability and validity of the final -6 odors test were made on the assumption that satisfactory level of specific odor recognize was 90% with statistical analysis based on test Z for proportion. Additional validation of the final test was carried out on a group of 30 children (10 children from each group). Those children were given to recognize the 6 odors test in 4-fold repetitions in order to determine whether the odor is recognizable every time. After familiarizing children with 6 scents, the odors were tested again but mixed, so the same odor cannot be recognized one by one. Revalidation - after 2weeks period validation was repeated to confirm its effectiveness. Diagnostic validation data obtained from each group have been shown in Table 2. The test was useful in children aged about 3 years and older. There was an appreciable age trend in the variability of the scores on the identification task (Table 2). Only for one odor – fish aroma, in the youngest group of children we noticed statistically significant difference in odor recognition level compare to satisfactory level on the assumption (90% efficacy level). But if we took under consideration the 80% level specific odor recognition was with a good efficacy in each group of children. Additional validation of the 6 odors test in 4-fold repetitions has received similar data. Results on the 6 odors test from healthy children showed satisfactory test–retest reliability, split-half reliability and validity. We compared the age trends in variability of scores on the 6 odors test with those on an odorant identification task, using a
Fig. 1. Recognizing particular odors by all the children. The odors recognized by at least 75% of the children were labeled in cyan. (For interpretation of the references to color in the artwork, the reader is referred to the web version of the article.)
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100% 6
90% 80% 70%
18 14
60%
6 odors
20
50%
5 odors 4 odors
40% 30%
3 odors
7
20%
6
10% 0%
4
5
3
group II
group I
group III
Fig. 2. The screening test results in relation to the children’s age. Determined amount of children in each group have recognized indicated quantity of odors in the screening test. Children labeled in yellow did not meet the specified norm. (For interpretation of the references to color in the artwork, the reader is referred to the web version of the article.)
Table 2 Data of test Z for proportion for 6-odors test. 6-odors test
Cola Toffee Chewing gum Mint Lemon Fish
Group I
Group II
Group III
Recognition
Error
Test Z for proportion (p value)
Recognition
Error
Test Z for proportion (p value)
Recognition
Error
Test Z for proportion (p value)
30 29 34 29 31 28
7 8 3 8 6 9
0.142 0.0548 0.972 0.054 0.319 0.018
30 30 25 28 25 25
0 0 5 2 5 5
1 1 0.350 0.822 0.350 0.350
18 18 18 18 14 18
0 0 0 0 4 0
1 1 1 1 0.196 1
weighted linear regression analysis. It showed statistically significant influence of age on the olfactory test result.
4. Discussion There have been no reports on the olfactory function disturbances prevalence in children but many cases of children with anosmia remain to be determined. Individual patients and their parents are seldom aware of olfactory deficits and concluded that formal assessment of olfactory function is imperative. Evaluations of young children and identification of any deficits may be particularly important if critical periods for olfactory system development exist as have been shown for the gustatory system [15,16]. Thus we were interested in development of test to screen children at an early age for olfactory function. Most of the existing tests utilize odor stimuli that would be unfamiliar to many children that limits their use across diverse populations, and necessitate the development of culture-specific test versions. The presented results of the examination determine the types of odors that Polish children aged from 2.9 to 10 years were able to identify. From among 21 odors used in the most well-known olfactory tests only 6 (smell of: cola, bubble gum, toffee, mint, fish and lemon) were identified by the youngest children (2.9–5 years old) with the frequency of 75% making it possible to include them in screening tests. Thus, those may serve as screening olfactory examination for Polish children (Table 1). Recognizing an odor by 75% of a healthy population is thought to be the threshold to include the odor in the olfactory test [12]. The number of commonly identified odors was increasing with age, and therefore it is possible to extend the 6-element olfactory test by other olfactory stimuli which were recognized in 75% of the instances in a particular age group. The test can be extended by 7
odors in the group of 5–7 years old and by 11 odors in the group of children above 7 years old (Table 1). A surprising result was a low identification rate of apple and rose smell – stimuli included in many well-known olfactory tests [17] (Sniffin Stick test, CC-SIT). That confirms that the examination methods cannot be uncritically transferred from an adult population into children’s population. The results obtained alter our knowledge about children olfactory screening. Many researchers believe that olfactory assessment based on psychophysical tests is possible only for children that are more than 5 years old, and for younger patients different measures are proposed [18]. These include, however, less available and often still experimental examinations, i.e. olfactory-evoked cortical potential [3,19]. It probably results from a significant peculiarity of tools employed in examining children. The present study describes the methodology of conducting olfactory tests on children. It could be more acceptable by a little patient as possible and give more reliable results of olfactory function assessment. We tried to use the UPSIT, pen-like odor test and Elsberg-Levy olfactometry to asses olfactory function in children but it was very difficult thus we have been looking for more suitable test. Based on our experience the number of stimuli employed in tools for examining children has to be fewer than in respective tools used for adults due to the examination’s duration as well as children’s quicker lack of concentration and boredom caused by the examination. Performing the test as a game exercise – a guessing game with colorful pictures that make children connect them with odors – assures the increase of examination’s reliability. Hence, in the present study the authors tried to create a test that could be easy and quick to conduct, treated by a child as a game and finally minimalizing the influence of verbal and cognitive abilities on the outcome. The name of the odor under the picture was read
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out loudly each time. Based on our previous experiences we found out that the list of odors presented on paper is not effective in children, because some of the children aged between 2, 9 and 10 years old could not read yet. Verbally read out name of a specific odor was not enough as well because some of the odors e.g. mint was colligated to a toothpaste or refresh - sweets but the term ‘‘mint’’ itself or image of a mint leaf – was unknown to many children. Thus for much more reliable results, a parent provided information about such products which can be related to specific odors and asked to give a brief instructions on the proper choice of the picture that could be best recognized by a child. From among 21 odors only the most easily recognizable by children were selected: in group I – 6 odors, in group II – 13 odors, and in group III – 17 odors. Only 6 children (6.6%) from the group of 91 did not complete the examination due to either parent’s lack of time for continuing the examination (3 persons) or child’s lack of concentration (3 persons). These were the youngest children (group aged 2.9–5 years). The data differ from data collected by other authors. Hummel et al. [3] in a group of patients aged from 3 to 5 obtained 44% of unfinished tests. Perhaps it results from using Sniffin Stick test intended to examine an adult population for the olfactory evaluation of children [17]. From the authors’ experience it follows that this test is unsuitable for children’s examination. The time of conducting the Sniffin Stick test is too long (about 30 min) and as was confirmed in our research, this test includes odors unfamiliar to children. The presented single 21-odor examination took about 10 min, and screening test composed of 6 odors took 3– 4 min. That is a few times shorter than the Sniffin Stick test. Other researchers have similar observations [19]. The aim of authors was simplification of the method. Despite the fact that this leads to diminishing the knowledge about functioning of olfaction, it seems to be a more adequate method to evaluate olfaction in little children. The choice of stimuli employed in the examination was based on the odors used in the most popular olfactory tests. Children were able to identify on average 15 (72%) odors from 21 presented. This result indicates that a part of the aromas commonly included in olfactory tests is not sufficiently wellknown to the children in this part of Europe. The set of six the most recognized odors seems to be the most suitable for a quick evaluation of olfaction in Polish children. The results obtained after exposition to some stimuli – e.g. anise, apple or rose – were situated at the very border of recognizability, what is significant mainly in a context of using these odors in olfactory examination of children by some authors [17,20]. In accordance with other authors’ reports [18] the number of correctly identified stimuli by children was significantly increasing along with age (an average number of correct answers in group I – 13, in group II – 16, and in group III – 19). The evaluation of olfactory function in children provides many problems resulting mainly from the lack of satisfactory diagnosis methods. The presented examination results enable creating a test for screening olfactory function in children from this part of Europe and simultaneously they confirm that uncritical mapping of olfactory tools for diagnosing adults onto children’s population raises controversies and doubts when it comes to the validity of such proceedings. The 6-odors test was developed to address the need for a culturally valid odor-identification test for clinical use on the Polish population. Six odorous test stimuli were selected that were relatively identifiable, familiar, strong in intensity according to healthy participants. Four response alternatives were then selected for each final test stimulus based on a confusion matrix of identification rates obtained from healthy participants, in a manner that controlled for task difficulty.
5. Conclusions The aim of the present article was to determine the possibility of olfactory examination in children and to identify the aromas that are recognizable by Polish children. The results obtained suggest that olfactory examinations conducted by psychophysical methods are possible to execute in small children, yet the tests need to be strictly adjusted to an age group. The article presents a proposal of the olfactory screening test in which the aromas that were the most easily recognized by children from this part of Europe are included. The research conducted confirms the influence of age on the number of recognized odors as well as the lack of significant differences in olfactory test results when it comes to sex of subjects. 1. Olfactory evaluation is possible in children as young as 3 years old. Child’s age influences the number of odors recognized. 2. The odors that were most easily recognized by children were: bubble gum, lemon, cola, mint, toffee and fish. Those odors may be used in an olfactory screening test. 3. The 6 odors test has good ability to generalize performance to olfactory status, has normative data and good validity and reliability, is fast, easy and inexpensive to administer.
Conflict of interest statement The authors have no conflicts of interest to disclose. Role of the funding source No external funding was secured for this study. Patient consent and ethics The study got the Ethics Committee approval no 99/WIM. Acknowledgements We express thanks to Jaskulski Aromaty JAR company from Warsaw for donating the odors necessary for conducting the research. References [1] C.G. Pomares, J. Schirrer, V. Abadie, Analysis of the olfactory capacity of healthy children before language acquisition, J. Dev. Behav. Pediatr. 23 (4) (2002) 203–207. [2] B. Schaal, T. Hummel, R. Soussignan, Olfaction in the fetal and premature infant: functional status and clinical implications, Clin. Perinatol. 31 (2) (2004) 261–285. [3] T. Hummel, M. Bensafi, J. Nikolaus, M. Knecht, D.G. Laing, B. Schaal, Olfactory function in children assessed with psychophysical and electrophysiological techniques, Behav. Brain Res. 180 (2) (2007) 133–138. [4] A. Bra¨merson, L. Johansson, L. Ek, S. Nordin, M. Bende, Prevalence of olfactory dysfunction: the Skovde population-based study, Laryngoscope 114 (4) (2004) 733–737. [5] M.A. Roberts, A.F. Simcox, Assessing olfaction following pediatric traumatic brain injury, Appl. Neuropsychol. 3 (2) (1996) 86–88. [6] D.G. Laing, J.E. Armstrong, M. Aitken, A. Carroll, F.J. Wilkes, A.L. Jinks, et al., Chemosensory function and food preferences of children with cystic fibrosis, Pediatr. Pulmonol. 45 (8) (2010) 807–815. [7] R.A. Frank, M.F. Dulay, K.A. Niergarth, R.C. Gesteland, A comparison of the sniff magnitude test and the University of Pennsylvania Smell Identification Test in children and nonnative English speakers, Physiol. Behav. 81 (3) (2004) 475–480. [8] F.R. Karsz, A. Vance, V.A. Anderson, P.G. Brann, S.J. Wood, C. Pantelis, et al., Olfactory impairments in child attention-deficit/hyperactivity disorder, J. Clin. Psychiatry 69 (9) (2008) 1462–1468. [9] R.A. Richman, E.M. Post, P.R. Sheehe, H.N. Wright, Olfactory performance during childhood. I. Development of an odorant identification test for children, J. Pediatr. 121 (6) (1992) 908–911. [10] P. Dalton, J.A. Mennella, B.J. Cowart, C. Maute, E.A. Pribitkin, J.S. Reilly, Evaluating the prevalence of olfactory dysfunction in a pediatric population, Ann. N. Y. Acad. Sci. 1170 (2009) 537–542. [11] R.L. Doty, A. Marcus, W.W. Lee, Development of the 12-item cross-cultural Smell Identification Test (CC-SIT), Laryngoscope 106 (1996) 353–356.
K. Dz˙aman et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 418–423 [12] T. Hummel, B. Sekinger, S.R. Wolf, E. Pauli, G. Kobal, ’Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification. odor discrimination and olfactory threshold, Chem. Senses 22 (1) (1997) 39–52. [13] R.L. Doty, U. Agrawal, The shelf life of the University of Pennsylvania Smell Identification Test (UPSIT), Laryngoscope 99 (4) (1989) 402–404. [14] W.S. Cain, J.F. Gent, R.B. Goodspeed, G. Leonard, Evaluation of olfactory dysfunction in the Connecticut Chemosensory Clinical Research Center, Laryngoscope 98 (1) (1988) 83–88. [15] J.A. Mennella, C.P. Jagnow, G.K. Beauchamp, Prenatal and postnatal flavor learning by human infants, Pediatrics 107 (6) (2001) 88. [16] J.A. Mennella, G.K. Beauchamp, Olfactory preferences in children and adults, in: D.G. Laing, R.L. Doty, W. Breipohl (Eds.), The Human Sense of Smell, vol. 1991, Springer-Verlag, New York, 1992, pp. 167–180.
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[17] I. Konstantinidis, S. Triaridis, A. Triaridis, I. Petropoulos, K. Karagiannidis, G. Kontzoglou, How do children with adenoid hypertrophy smell and taste? Clinical assessment of olfactory function pre- and post-adenoidectomy, Int. J. Pediatr. Otorhinolaryngol. 69 (10) (2005) 1343–1349. [18] D.G. Laing, C. Segovia, T. Fark, O.N. Laing, A.L. Jinks, J. Nikolaus, et al., Tests for screening olfactory and gustatory function in school-age children, Otolaryngol. Head Neck Surg. 139 (1) (2008) 74–82. [19] M. Knecht, J. Nikolaus, K.B. Huttenbrink, Olfactory function in children – results from psychophysical and electrophysiological investigations, HNO – Inf. 29 (2004) 122. [20] A. Obre˛bowski, Z. Obre˛bowska-Karsznia, M. Gawlin´ski, Smell and taste in children with simple obesity, Int. J. Pediatr. Otorhinolaryngol. 55 (3) (2000) 191–196.