The Effect of Anatomic Clearance Between Tongue and SoftPalate on Retronasal Olfactory Function

Aytug Altundag & Murat Salihoglu & Melih Cayonu &

Hakan Tekeli & Gurkan Kayabasoglu

Received: 8 September 2013 /Accepted: 5 January 2014 /Published online: 15 January 2014# Springer Science+Business Media New York 2014

Abstract Research shows that odorants travel to the olfactoryreceptors by two routes. Oral conditions, mouth movements,mastication, and swallowing are known to influence the per-ception of retronasal stimuli. The dimension of the anatomicalclearance between the soft palate and tongue might affect theretronasal olfaction because retronasal olfaction is only possi-ble when the soft palate–tongue barrier is opened. Therefore,in this present study, our aim is to evaluate the effect of theanatomical clearance between tongue and soft palate onretronasal olfactory function. After rating the mallampatiscore for the classification of the clearance between tongueand soft palate, the “Sniffin’ Sticks” test for orthonasal olfac-tion and retronasal olfactory testing were performed. Thestudy was carried out on 276 subjects, and the mean age ofthe participants was 27 years ranging from 19 to 53 years. Theparticipants were divided into two groups: Group 1 includedparticipants with mallampati Class 1 and 2 scores; Group 2included participants with mallampati Class 3 and 4 scores.

This study clearly shows that the dimensional differences inthe anatomical clearance between the soft palate and tonguehad no effects on retronasal olfaction.

Keywords Retronasal olfaction . “Sniffin’ Sticks” . Tongue .

Palate . Swallowing

Introduction

Research shows that odorants travel to the olfactory receptorsby two routes (Fig. 1). Sniffing brings odorants through thenostrils into the nasal cavity (orthonasal olfaction); chewingand swallowing force odorants emitted by foods upward,behind the palate, into the nasal cavity from the rear of themouth (retronasal olfaction). There are clear differences be-tween orthonasal and retronasal olfaction in neuronal process-ing and perception so that these two pathways convey twodistinct sensory signals (Buettner et al. 2001; Landis et al.2005; Pfaar et al. 2006; Rombaux et al. 2006 and 2007;Bojanowski and Hummel 2012).

Approximately 5 % of the general population is anosmic,but about 15 % have a reduced sense of smell (Murphy et al.2002; Vennemann et al. 2008; Landis and Hummel 2006). Asignificant number of patients complain of a reduction in theirsense of smell, so it becomes important to reveal the factorsthat can influence both orthonasal olfaction and retronasalolfaction. Despite this fact, retronasal olfaction so far hasreceived far less attention than its orthonasal counterpart.There are numerous studies about pathologies causing con-ductive orthonasal olfaction dysfunction (Simopoulos et al.2012; Becker et al. 2012; Schriever et al. 2013; Nguyen et al.2012; Garzaro et al. 2012; Haxel et al. 2011). However, thereis little data about the factors affecting the retronasal odorsfrom reaching the olfactory mucosa.

A. Altundag (*)Division of Otorhinolaryngology, Istanbul Surgery Hospital,Istanbul 34365, Sisli, Turkeye-mail: aaltundagkbb@gmail.com

M. SalihogluDepartment of Otorhinolaryngology,GulhaneMilitary Medicine Academy Haydarpaşa Training Hospital,Uskudar, Istanbul 34668, Turkey

M. CayonuDepartment of Otorhinolaryngology, Amasya University Trainingand Research Hospital, Amasya 05100, Turkey

H. TekeliDepartment of Neurology, Gulhane Military Medicine AcademyHaydarpasa Training Hospital, Uskudar, Istanbul 34668, Turkey

G. KayabasogluDepartment of Otorhinolaryngology, Sakarya University Trainingand Research Hospital, Adapazarı, Turkey

Chem. Percept. (2014) 7:40–45DOI 10.1007/s12078-014-9162-7

Oral conditions, mouth movements, mastication, andswallowing are known to influence the perception ofretronasal stimuli (Heilmann et al. 2002; Welge-Lüssen et al.2009; Hummel 2008). It is found that adenoid vegetation,narrowing the patency of retropalatal area, has negative effectson retronasal olfaction (Konstantinidis et al. 2005). Likewise,the dimension of the anatomical clearance between the softpalate and tonguemight affect the retronasal olfaction becauseretronasal olfaction is only possible when the soft palate-tongue barrier is opened (Buettner et al. 2001 and 2002).Therefore, in this present study, our aim is to evaluate theeffect of the anatomical clearance between tongue and softpalate on retronasal olfactory function.

Material and Methods

This study was approved by the Clinical Research EthicsCommittee of the Istanbul Cerrahpasa Medical Faculty(10.05.13-83045809/11274) and conducted at otorhinolaryn-gology clinics of the Gulhane Military Medicine AcademyHaydarpaşa Training Hospital and Istanbul Surgery Hospital.Informed consent was obtained from all participating subjects.Volunteers with signs of nasal polyposis or rhinosinusitis andwith a history of subjective olfactory dysfunction were ex-cluded from the study.

Also, volunteers with Grade 2, 3 or 4 tonsil hypertrophy,according to Friedman tonsil grading (Friedman et al. 1999),were excluded from the study. Only volunteers with Grade 1tonsil size, which implied tonsils hidden within the pillars,were included in the study in order to minimize the tissueeffect of the palatine tonsil.

For the classification of the clearance between tongue andsoft palate, the modified mallampati classification was used.

The modified mallampati classification was assessed as de-scribed (Mallampati et al. 1985; Samsoon and Young 1987)(Fig. 2). The procedure involved asking the patient to com-fortably rest in a seated position with the mouth open and thetongue protruding without phonation, providing visualizationof the oropharyngeal isthmus. Based on the what was ob-served, four classifications were assigned: Class 1 allowedthe observer to examine the entire uvula and tonsils or pillars;Class 2 allowed observation of the uvula but not the tonsils;Class 3 allowed observation of the soft palate but not theuvula; Class 4 allowed observation of the hard palate only.

After rating the Friedman tongue position, the “Sniffin’Sticks” olfactory test and retronasal olfactory test were con-ducted with 276 patients. No patient loss occurred during thetest processes.

Psychophysical testing of orthonasal olfactory functionwas performed with the validated “Sniffin’ Sticks” test. Odor-ants were presented in commercially available felt-tip pens(“Sniffin’ Sticks”, Burghart GmbH, Wedel, Germany)(Hummel et al. 1997; Kobal et al. 2000). For odor presenta-tion, the pen’s cap was removed by the experimenter forapproximately 3 s, and the tip of the pen was placed approx-imately 1.0–2.0 cm in front of the nostrils. The test consists ofone threshold and two suprathreshold subtests, namely a testfor olfactory thresholds of n-butanol, a test for odor discrim-ination (16 triplets with two different odors), and one for odoridentification (16 common odors, presented in a four-alternative, forced-choice procedure). The maximum scoreof each subtest was 16, resulting in a maximum compositescore of 48 (TDI [threshold, discrimination, and identifica-tion] score) (Wolfensberger et al. 2000). This score allows adiagnosis of anosmia, hyposmia, or normosmia. In thosepatients where orthonasal lateralized testing had been per-formed, results for the best nostril were used for furtherstatistical evaluations (Hummel et al. 2007). None of thesubjects was excluded from the study according to the TDIscore.

For retronasal olfactory testing, a standardized, validatedtest was used (Heilmann et al. 2002). The test is based onidentification of odorized powders or granules presented to theoral cavity (e.g., spices, instant drinks, and instant soups;Table 1). The substances were applied to the midline of thetongue on fenestrated plastic sticks. Subjects were free tosample as much stimulant as needed for identification. Thisapproach also minimized the problem of standardizing thearea of stimulation, differences in tongue, or oral cavity size.In a typical trial, the experimenter placed approximately0.05 g on the middle of the tongue inside the oral cavity. Afteradministration of each powder, participants rinsed theirmouths with tap water. The procedure was self-timed. Eachsubstance was identified by means of a closed set with fourverbal items using a forced-choice procedure. The test resultwas a sum score of the correctly identified stimuli.

Fig. 1 The retronasal and orthonasal routes of olfaction

Chem. Percept. (2014) 7:40–45 41

Statistical Analysis

Data analysis was performed by SPSS 21.0 (StatisticalPackage for Social Sciences, SPSS Inc., Chicago, IL,USA). The normal distribution of considered variables wasfirst evaluated using the Shapiro–Wilk test. Data was shownas mean±standard deviation for continuous variables, andthe number of cases was used for categorical variables.Demographic data of the subjects were compared by T orchi-square tests. The T test was used to evaluate the rela-tionship between independent variables and retronasal ol-factory testing scores. The effect of gender and palategrading on retronasal olfactory scores was examined witha linear regression model. Correlational analyses were cal-culated according to Pearson. The level of significance wasset at 0.05.

Results

The study was carried out on 276 subjects, and the mean ageof the participants was 27±7.7 years ranging from 19 to53 years. The participants were divided into two groups:Group 1 included participants with mallampati Class 1 and 2scores; Group 2 included participants with mallampati Class 3and 4 scores. There were no differences between the groups interms of age, cigarette smoking, and alcohol consumption.However, there were statistically significant differences interms of gender between the two groups.

Table 2 summarizes the characteristics of each of the var-iables of interest by groups. Differences in retronasal olfactionscores were not significant between the two groups. The effectof mallampati scoring on retronasal olfactory scores was notfound to be significant by linear regression model (p=0.24).

Fig. 2 Modified mallampaticlassification (1–4)

Table 1 Odorized powder orgranules used for retronasal ol-factory testing

42 Chem. Percept. (2014) 7:40–45

Target item Distracter items Brand name (distributor name and city Location)

Ginger Mustard, paprika, curry Zencefil (Doğasal®, Ankara)Grapefruit Lemon, sour cherry, red currant Grapefruit (Firmenich®, İstanbul)Bread Sauerkraut, pizza, garlic Rusk bread (Etimek®, Bilecik)

Milk Vanilla, banana, coconut Süttozu (Pınar®, İstanbul)Strawberry Apple, red currant, tangerine Çilek (Ori®, İstanbul)Vanilla Cherry, banana, honey Vanilin (Dr. Oetker®, İzmir)Orange Raspberry, strawberry, cherry Portakal (Ori®, İstanbul)Onion Chives, salami, smoked ham Soğan (Arifoğlu®, İstanbul)Cocoa Caramel, muscat, juniper Kakao (Dr. Oetker®, İzmir)Celery Chives, parsley, carrots Kereviz kök granül (Kurucum®, Isparta)

Mushrooms Bread, fish, white wine Mushrooms (Firmenich®, İstanbul)Paprika Ginger, curry, mustard Karabiber (Bağdat®, Ankara)Coffee Cinnamon, muscat, cocoa Türk Kahvesi (Ülker®, İzmir)Smoked ham Fish, bread, chives Smoked ham (Firmenich®, İstanbul)Cloves Anise, caraway, dill Karanfil (Arifoğlu®, İstanbul)Garlic Ham, chives, celery Sarımsak Granül (Bağdat®, Ankara)Muscat Cinnamon, coffee, cocoa Muscat (Firmenich®, İstanbul)Curry Mustard, cheese, cucumber Köri (Bağdat®, Ankara)Cinnamon Honey, caramel, cocoa Tarçın (Doğasal®, Ankara)Raspberry Peach, pineapple, white grapes Raspberry (Firmenich®, İstanbul)

Also, there was no correlation between gender and retronasalolfactory scores (p=0.57).

There was a significant negative correlation betweensmoking and retronasal olfactory scores (p<0.001, r=0.26)and also between smoking and all of the “Sniffin’ Sticks”subtests, namely threshold, discrimination, and identificationscores (p<0.001, r=0.21; p<0.001, r=0.25; p=0.001, r=0.2respectively) (Fig. 3).

There was a significant positive correlation between the“Sniffin’ Sticks” subtest total score (TDI) and retronasal testolfactory scores, independent of the grouping according to themallampati classification (p<0.001, r=0.7) (Fig. 4).

Discussion

The oral cavity is a three-dimensional place where retronasalolfactory perception and taste perception start. This cavity iscontinuous with pharynx posteriorly at the oropharyngeal isth-mus, and so it is potentially connected to the nasal cavity by theway of nasopharynx. The oropharyngeal isthmus can be openedor closed by surrounding soft tissues, which include the soft

palate and tongue. The oral cavity in healthy adults is generallyconnected to the nasal passages whenever the person is notspeaking, swallowing, or choosing to produce a velopharyngealclosure (Buettner et al. 2001 and 2002). The air phase of theodorants derived from liquid or solid foods in the oral cavityreaches the nasal passages through the oropharyngeal isthmusduring the exhale portion of each natural breathing cycle thatoccurs during lip closure and normal lingual manipulation ordental chewing of food (Deibler et al. 2001).

The relation between olfactory function and nasal airflowdisturbances has been examined in several studies. However,anatomical barriers, which may affect the flow of odor mole-cules from oral cavity to the nasal passages, have not yet beenstudied. So in this current investigation, the question is wheth-er the anatomical clearance between the tongue and soft palateaffects the flow of odor molecules from oral cavity to the nasalcavity or not.

To answer this question, we planned a study in which thevolunteers were grouped according to modified mallampaticlassification. This scoring system is widely used for evaluat-ing the clearance of oropharyngeal isthmus in patients withobstructive sleep apnea and before the induction of anesthesia.Although the mallampati classification is done while the pa-tient is conscious in a sitting position, this scoring systemhelps the clinicians to predict the airway patency during therelaxation period of sleep and general anesthesia. In a similarway, although the dimension of the oral cavity and the move-ments of the tongue are quite variable during swallowing anddeglutition, the mallampati classification makes it easier topredict the anatomical clearance between soft palate andtongue during swallowing.

The volunteers with size 2, 3 or 4 tonsil hypertrophy wereexcluded from the study in order to minimize the tissue effectof palatine tonsil. The olfactory system was checked by thevalidated “Sniffin’ Sticks” test to detect whether volunteershad a sense of smell impairment or not. Since the adequateorthonasal olfaction is a prerequisite for good retronasal

Table 2 Comparison of the two groups (Group 1 included participantswith mallampati classes 1 and 2; group 2 included participants withmallampati classes 3 and 4)

Characteristics Group 1 Group 2 p value

Age 27.5±7.5 26.1±8 0.2

Male gender/N 145/191 78/85 0.002

Smoking (%) 83 (44 %) 39 (46 %) 0.7

Alcohol usage (%) 37 (19 %) 13 (15 %) 0.4

Retronasal olfactory test scores 16 ±2.6 15.4 ±2.4 0.09

TDI scores 31.2±7.8 29.2±9.9 0.1

Fig. 3 Box plot model of retronasal olfactory testing (Rno) score, totalscore of “Sniffin’ Sticks” subtests (TDI), odor threshold (T), odor dis-crimination (D), and odor identification (I) scores according to the habitof smoking

Fig. 4 Scatter plot model with linear regression for the “Sniffin’ Sticks”subtests total score (TDI) and retronasal olfactory testing score

Chem. Percept. (2014) 7:40–45 43

olfaction, the “real life stimuli” used in this study, and shownin Table 1, not only activated the olfactory system, but addi-tionally provided sensations mediated by the gustatory andtrigeminal systems.

Also, the stimuli used for the orthonasal odor identificationtest do not specifically activate the olfactory system. Theidentification of most odors is possible through some degreeof olfactory function but sometimes at comparable degreesthrough trigeminal sensitivity. However, the assessment ofretronasal olfaction is possible using oral stimulus presenta-tion (Heilmann et al. 2002). According to the retronasal ol-factory testing, our study clearly shows that the dimensionaldifferences in the anatomical clearance between the soft palateand tongue have no effects on retronasal olfaction.

The retronasal olfactory perception is more sophisticatedthan the orthonasal counterpart as it requires adequate masti-cation to release olfactory volatiles, which are pumpedretronasally to the olfactory region by sufficient mouth andswallowing movements (Welge-Lüssen et al. 2009; Hummel2008). Differences in relation to the perception of stimuli,either orthonasally or retronasally, are at least to a certaindegree due to differences in airflow pattern. It is known thatmild changes in nasal anatomy may produce large differencesin the perception of odors (Nguyen et al. 2012; Garzaro et al.2012). The influence of flow characteristics on olfactory per-ception is not yet fully understood; it appears to be clear thatairflow plays a major role in the perceptual differences be-tween stimuli presented in the back or in the anterior portionof the nose. Our investigation is a basic clinical study aboutthe soft palate–tongue anatomy and its effect on retronasalolfaction. However, basic studies such as the effect of palatinetonsillar hypertrophy or swallowing dysfunction on retronasalolfaction are still lacking in the literature.

Conclusion

The perception of foods is based on the interaction betweenortho- and retronasal smell, taste, trigeminal activation, andtexture, so it is difficult to investigate one of these factors inisolation. That is why retronasal olfaction has received lessattention than the orthonasal olfaction until recently. Technicalproblems excluded retronasal olfactory testing from routineclinical practice. This study shows that the anatomical varia-tions in the dimension of the clearance between the soft palateand tongue have no effect on retronasal olfaction. However,further studies are needed in order to determine factors affect-ing the retronasal olfaction.

Compliance with Ethics Requirements

Conflict of Interest The authors state that they have no funding,financial relationships, or conflicts of interest.

All procedures followed were in accordance with the ethical standardsof the responsible committee on human experimentation (institutional andnational) and with the Helsinki Declaration of 1975, as revised in 2008.Informed consent was obtained from all patients for being included in thestudy. This study was approved by the Clinical Research Ethics Committeeof the Istanbul Cerrahpasa Medical Faculty (10.05.13-83045809/11274).

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