INTERNATIONAL SYMPOSIUM ON OLFACTION AND TASTE

Evaluating the Prevalence of OlfactoryDysfunction in a Pediatric Population

Pamela Dalton,a Julie A. Mennella,a Beverly J. Cowart,a,b

Christopher Maute,a Edmund A. Pribitkin,b

and James S. Reillyc

aMonell Chemical Senses Center, Philadelphia, Pennsylvania, USAbThomas Jefferson University, Philadelphia, Pennsylvania, USA

cNemours/A.I. duPont Hospital for Children, Wilmington, Delaware, USA

Although smell loss has several potential etiologies (e.g., head trauma, allergic rhinitis,and enlarged adenoids) that are common among children, studies evaluating the preva-lence of olfactory dysfunction in the pediatric population are rare. Several challengesconfront the clinician or researcher hoping to evaluate odor identification ability inyoung children. Children are likely to be unfamiliar with many of the odor stimuli usedin adult tests and have limited ability to read and identify labels to select from alterna-tive choices, which is the typical adult response option. Consequently, specialized formsof olfactory tests must be developed for this population. Based on the format of the SanDiego Odor Identification Test1 and the delivery system of the Brief Smell IdentificationTest,2 we are developing a short form odor identification test utilizing standardizedodor stimuli in which participants match 6 odorants to pictures of the odor source. Thepilot version of this test is being administered to children between the ages of 3–17 aspart of the pre-surgical intake evaluation at the A.I. duPont Hospital for Children andas part of basic research studies at the Monell Center. The hospital study populationis broad and includes children undergoing ear, nose, and throat surgery as well as con-trols subjects (children undergoing general surgery), with approximately 50 children perweek eligible for evaluation. To improve correct interpretation of the results, stimulusfamiliarity is evaluated by having the child’s parent/guardian also complete the test andanswer a short questionnaire about the child’s experience with the various odor stimuli.The challenges confronted in studying this clinical population as well as extrapolationto larger populations will be discussed.

Key words: olfaction; odor identification; children; evaluation; NIH Toolbox

Introduction

Our sense of smell provides informationabout our environment and food quality thatis critical to our health and safety, a nutritiousdiet, and psychological well-being. Althoughsmell loss has several potential etiologies (e.g.,head trauma, allergic rhinitis, and enlargedadenoids) that are common among children,

Address for correspondence: Pamela Dalton, Monell Chemical SensesCenter, 3500 Market Street, Philadelphia, PA 19104. Voice: 267-519-4810; fax: 215-898-2084. pdalton@pobox.upenn.edu

studies evaluating the prevalence of olfactorydysfunction in the pediatric population are rare.Moreover, of the available tests for evaluatingolfactory function in adults, children are likelyto be unfamiliar with many of the odor stim-uli used and have limited ability to read andidentify labels to select from alternative choices,which is the typical adult response option. Con-sequently, specialized forms of olfactory testsmust be developed for this population. Basedon the format of the San Diego Odor Identifi-cation Test (SDOIT)1 and the delivery systemof the Brief Smell Identification Test (B-SIT),2

International Symposium on Olfaction and Taste: Ann. N.Y. Acad. Sci. 1170: 537–542 (2009).doi: 10.1111/j.1749-6632.2009.03919.x c© 2009 New York Academy of Sciences.

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this paper reviews the development of a shortform odor identification test utilizing standard-ized odor stimuli suitable for administration tochildren between 3 and 17 years of age.

Why Study Olfactionin Children?

Routine evaluations of visual and auditoryacuity are performed in childhood in order toidentify deficits in sensory abilities that may im-pair normal development and learning. Giventhe importance of vision and hearing to normalfunctioning, it is not surprising that specializedtests for evaluating pediatric populations havebeen developed.3–5 In contrast, tests of olfac-tory function for very young children are nei-ther routinely available nor administered. Thislikely represents an oversight in our appreci-ation of the importance of the olfactory sys-tem for identifying hazards in our environmentand ensuring nutritious food choices. Given theevidence that olfactory learning may be par-ticularly robust during childhood,6 identifyingdeficits in this age group could be important fornormal development.

Although congenital anosmia is estimated tobe a relatively rare occurrence,7 there are anumber of conditions that may occur in earlychildhood that can lead to either partial or to-tal loss or distortion in olfactory ability. For ex-ample, the olfactory system is particularly vul-nerable to head injuries which may sever theolfactory nerve and result in a complete lossof olfactory ability. Even swelling in this areacan prove temporarily disabling to the sense ofsmell. Several studies of children have shownmeasurable deficits in children with head in-jury or traumatic brain injury and the degreeof performance decrement is associated withthe severity of the head trauma.8,9 Conditionswhich produce significant nasal congestion ornasal passage obstructions, such as allergies orenlarged adenoids, may also impair olfactorysensitivity. A study of children before and afteradenoidectomy revealed that performance on

an odor identification test improved followingthe procedure.10

Beyond these known risk factors, there maybe additional disease or environmental fac-tors that can impact olfactory ability amongyoung children. As one example, animal stud-ies have demonstrated that a variety of heavymetals (e.g., cadmium, manganese) that comeinto contact with the olfactory epithelium canbe taken up in the primary olfactory neuronsand be transported to the olfactory bulbs andeven further into other areas of the brain.11,12

Given the large number of children who arestill exposed to lead dust in their home en-vironment, we might expect to observe someimpact on olfactory performance among chil-dren with high blood lead levels. For these rea-sons, there is increasing interest and impetusto screen children at an early age for olfactoryfunction.

The NIH Toolbox

The NIH Toolbox for assessment of neu-rological and behavioral function is a projectfunded by the NIH Blueprint for NeuroscienceResearch, an initiative sponsored by 16 NIHinstitutes, centers, and offices that support neu-roscience research.13 The goal of the NIH Tool-box project is to develop brief but comprehen-sive measurement tools for assessing cognitivefunction, emotional health, sensory, and motorfunction across the entire lifespan. The Toolboxaims to be responsive to the needs of researchersin a variety of settings, but with particular em-phasis on measuring outcomes in clinical trialsand functional status in large epidemiologicaland longitudinal studies.

The tests which will ultimately be includedin the Toolbox must meet a number of specificcriteria. They must be brief, easy to use and ad-minister in a variety of settings and with differ-ent subgroups, but psychometrically sound. Ad-ditionally, they must be available for use withoutintellectual property issues and at minimal costto the users, who may be incorporating items

Dalton et al.: Olfactory Tests for Pediatric Populations 539

from the Toolbox as only a subset of measuresto be used in their overall study.

The Toolbox project has placed special em-phasis on developing or modifying tests foruse among pediatric populations, recognizingthat few standardized tests exist to assess nor-mal children for motor and sensory function.Moreover, in many of the motor and sensorydomains, there is a general reliance on proxyreporting and national “norms” if they do ex-ist, are typically based on English-speakingpopulations.

Issues in the Developmentof Pediatric Olfactory

Assessment Tools

There are numerous challenges to evaluatingolfactory function among children, particularlyin the age ranges from 3 to 5 years old.

• There are no tests which have been val-idated or provide normative data amongchildren this young.

• Most of the existing tests utilize odor stim-uli that would be unfamiliar to many chil-dren. In fact, the cultural and experientialspecificity of certain items in many odoridentification tests limit their use acrossdiverse populations, and often necessitatethe development of culture-specific testversions.14,15

• The cognitive and linguistic demands ofmany existing tests confound the interpre-tation of the results from young children.

• Children’s attentional resources also needto be considered in limiting the num-ber of items in a test, even while recog-nizing that the reliability and specificityof any test increases with the number ofitems.

Chemosensory researchers who have workedextensively with young children have arguedthat age-appropriate, game-like tasks that arefun for children and minimize the impact ofcognitive and language development are nec-

essary in order to ensure that what is beingmeasured is olfactory ability, not cognition.16,17

Hedonic judgments disguised as a game (forexample, give odors you like to Big Bird, odorsyou don’t like to Oscar the Grouch) have beenshown to be reliable methods for children asyoung as 3 years of age. In slightly older chil-dren, matching odors to pictures is a suc-cessful method, provided the child has expe-rience with the particular odor stimuli beingevaluated.18

For purposes of the Toolbox effort, we iden-tified several published or commercially avail-able tests which could serve as the buildingblocks for a pediatric specific test that meetsthe Toolbox criteria. The B-SIT2 is a 12-itemscratch and sniff test representing a subset ofthe items from the 40-item Smell Identifica-tion Test (SIT). Items in the B-SIT have beenselected to have broader cross-cultural familiar-ity. The micro-encapsulated stickers provide anefficient and easy way to administer standard-ized odor stimuli and individuals are asked toselect from four possible labels and determinewhich one best corresponds to the source ofwhat they smell. The test has excellent reliabil-ity (> 0.80) and although less specificity than itsparent (the 40-item SIT), can be administeredto adults and older children in under 5 min.However, data on this test exist only for chil-dren aged 5 and older, and performance forchildren aged 5–9 is similar to adults in theireighth decade where true deficits in olfactionare known to exist.19 This raises the questionas to whether the test is actually measuring ol-factory ability among children this young orwhether cognitive or language confounds areresponsible for the relatively poor performance.In addition to the linguistic response require-ments in the current version, however, the costsof this commercially available test may limit itsuse in studies where olfaction is not the primaryendpoint.

Recognizing that instrument costs in largescale epidemiological trials could producean obstacle to their adoption, Murphy andcolleagues1 developed a version of odor

540 Annals of the New York Academy of Sciences

identification test using grocery store itemswhich are then placed in opaque plastic bot-tles. In the SDOIT, eight everyday items aresniffed and matched to the appropriate linedrawing (out of 20 possible), keeping costslow and removing the reading and languageissue which can confound the assessment inyoung children. Performance on this test isquite good and reliability is high (> 0.80).However, given that the test uses actual fooditems, concerns about standardization of stim-uli and the need for investigators to pre-pare the stimuli themselves may prove tobe barriers to the use of this test in manysituations.

Based on the existing tests and methodolo-gies, the goal of the olfactory domain team wasto refine a child-specific test that utilizes stan-dard, easily obtained stimuli, can be adminis-tered in less than 5 min, uses both pictures andwords as response options and maintains goodreliability, sensitivity, and specificity.

The Toolbox Pediatric OdorIdentification Test

The version of the test that is currently un-der development uses items which have beenidentified as highly familiar to children in the5–9 year age group. Our goal is to identify up to6 items whose odors are readily recognized bymost American children from 3 to 9 years oldand that can be easily depicted in picture form.Currently, there are two versions of the test,each containing six odor stimuli. Table 1 liststhe odor stimuli and identifies which of themare used in the SDOIT and the B-SIT. Forstandardization purposes and ease of adminis-tration, we have produced micro-encapsulatedversions of each odorant in a sticker formatwhich can be scratched by the administrator orthe test taker to release the odor.

The test uses both pictures and words of eachstimulus as response options. The high resolu-tion quality of the pictures will enable us toconform to the Toolbox format by having the

Table 1. Odor Stimuli

Set A Set B

Bananab Peanut Buttera

Lemona,b Chocolatea,b

Play DohTM1Flowerb

Coffeea Minta

Cinnamona,b Play DohTMa

Bubble Guma GrapeaUsed in the San Diego Odor Identification Test.bUsed in the Brief Smell Identification Test.

children view the picture alternatives and re-spond on a touch screen to facilitate data collec-tion. To ensure that the pictures are recognizedappropriately, children are first given a pretestin which they are asked to point to the picturethat the experimenter names. If they incorrectlyidentify a picture, they are told the correct nameand given the opportunity to point to the cor-rect picture again. If they fail to identify thepicture after feedback, responses to that itemwill be disregarded.

For each odor stimulus, there are four re-sponse options shown: one is correct and threeare distractors. Among the distractors, how-ever, one is categorically or perceptually sim-ilar to the correct item (i.e., chocolate versuscoffee) and is considered a “near-miss.” Theother two are very dissimilar and are consideredtrue distractors. This methodology is based onthe Monell-Jefferson Chemosensory ClinicalResearch Center (CCRC) odor identificationtest20 and allows us to determine if the child canidentify the perceptual features of the odor suf-ficiently to classify it as a similar odor source. Aswith the Monell-Jefferson CCRC test, correctresponses are given a score of “1” while near-misses are given a score of 0.5. This mod-ification also allows us to obtain additionalresolution on a test with a small number ofitems.

Finally, the use of picture and word responseoptions will enable us to conform to the Tool-box format by having the children view andselect response alternatives on a touch screento facilitate data collection.

Dalton et al.: Olfactory Tests for Pediatric Populations 541

Test Plan and Populations

Children between the ages of 3 and 17 will betested, with a particular emphasis on obtainingsufficient numbers of children in the 3–9 yearrange. To determine familiarity with the odorstimuli, the accompanying parent or guardianwill also take the same version of the test as thechild and answer a questionnaire about theirand the child’s familiarity with the food or odoritems on the test. This will allow us to correctlyinterpret whether misses on the test are due tounfamiliarity with the odor stimulus or a truemeasure of olfactory dysfunction. The parentor guardian will also complete a short healthquestionnaire for the child focusing on condi-tions that are known to impair olfactory ability,such as allergic status, frequency of colds, andprior head injuries.

We are currently testing at two sites: the pre-operative outpatient facility at the A.I. duPontHospital for Children in Wilmington, Delawareand at the Monell Chemical Senses Centerin Philadelphia, PA. At the duPont Hospi-tal, patients are drawn from the DelawareValley region having a pediatric populationof 2.2 million children under the age of 18.Approximately 14,000 children per year un-dergo procedures at this facility and 12,500 ofthose go through the pre-op outpatient facil-ity where testing will take place. Of those un-dergoing surgery, 35% have ear-, nose-, andthroat-related surgery and this is the pop-ulation among which we might expect tosee some olfactory disturbances. Our currentplan estimates that 50 children and their par-ent/guardian can be evaluated each week, andwithin the hospital network, additional sites canbe recruited as needed.

At the Monell Center, children are drawnfrom the Philadelphia metropolitan area. Frompast experience, approximately 600 childrenare tested annually in other studies. The brevityof this olfactory assessment makes it easy to ap-pend to existing studies to increase the clinicalpopulation sample. An additional advantage atthe Monell Center, however, is that there are

Table 2. Odor Identification Results Stratified byage Group across the two Stimulus Sets

Age Group n # Correct (of 6)

3–5 30 2.936–8 44 3.779–11 35 3.9012–14 14 4.0815–17 16 4.09

fewer time constraints on testing than at thehospital site.

The preliminary results from pretesting atboth the duPont Hospital and the Monell Cen-ter have shown that children as young as 3 yearsold can complete the pretest and the olfactorytest well within a 5-min period and appear tobe enjoying the game-like experience. Childrenaged 6 and up, complete the odor identificationportion of the test in less than 2 min. Table 2presents a brief summary of the preliminary re-sults, stratified according to age group. Summa-rizing across both stimulus sets, the number ofcorrect responses increases with age categories.However, the initial analysis suggests that cer-tain items are better recognized among eventhe oldest age group than others and the out-come of these results will be the most importantfor determining the final stimulus selection.

The current plan is to continue the pretestingphase in order to determine the optimal stimu-lus selection, at which time the test stimuli willbe finalized. Following that, the collection ofnormative data for children at all age groupswill take place at multiple sites, including thosealready identified.

Summary

Increased awareness of the role of the olfac-tory system for safety, adequate nutrition andmany aspects of quality of life should impelfar more widespread evaluation of this sensoryability across large population groups. Evalua-tions of young children and identification of anydeficits may be particularly important if critical

542 Annals of the New York Academy of Sciences

periods for olfactory system development existas have been shown for the gustatory system.6,17

The support from the NIH Toolbox providesa significant opportunity to develop, validate,and provide normative data for evaluation ofolfactory function. The emphasis on the de-velopment of pediatric-specific tests which canbe readily incorporated into large-scale clinicaltrials or epidemiological studies is a significantopportunity to advance our understanding ofolfactory function and dysfunction across thelifespan.

Acknowledgments

Supported by the NIH Blueprint for Neuro-science Research, NIH contract No.: HHS-N-260-2006-00007-C, and by the Nemours Foun-dation. The authors wish to acknowledge theassistance of Ms. Carly Jornlin for data collec-tion and the work of the other members of theNIH Toolbox Olfaction Team for their contri-butions to instrument development and selec-tion: Richard Doty, Robert Frank, Julie Men-nella, and Claire Murphy.

Conflicts of Interest

The authors declare no conflicts of interest.

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