Relation between CT scan findings and human sense of smell

Relation between CT scan findings and human sense of smell

Relation b e t w e e n CT scan findings and human sense of smell SEOK-CHAN HONG, MD, DONALD A. LEOPOLD,MD, PATRICKJ. OLIVERIO, MD, MARK L. BENSON,MO, ...

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Relation b e t w e e n CT scan findings and human sense of smell SEOK-CHAN HONG, MD, DONALD A. LEOPOLD,MD, PATRICKJ. OLIVERIO, MD, MARK L. BENSON,MO, DAVID MELLITS,ScD, SHIRLEYA. QUASKEY,BS,and S. JAMESZINREICH,MD, Seoul, South Korea, Baltimore, Maryland, and Fairmount and Wheeling, West Virginia

Symptom questionnaires were obtained from 106 patients immediately before nasal and sinus computed tomography scans at the Johns Hopkins Outpatient Center. Their scans were analyzed by two otolaryngologists and three neuroradiologists by using a semiobjective rating system of the size and opacity of 36 anatomic areas. Patients estimated their own left and right sense of smell as excellent, diminished, or absent. Results of the data are as follows: (I) There is no correlation between smell ability and size of the nasal and sinus structures. This indicates that there is no gross effect of the bulging of sinuses into the nasal airway; (2) As a rule, opacity of only left-sided anatomic structures was correlated with both left and right sense of smell (p < 0.01). This suggests that our subjects were using their left smell receptors preferentially, to the exclusion of and in place of the right smell receptors; and (3) Total, not partial, opacity of the left olfactory cleft, frontal recess, or ethmoidal infundibulum was correlated with decreased sense of smell. This suggests that these anterior structures in the region of the olfactory cleft do affect airflow, but complete obstruction of these spaces is needed. Possible explanations for the effect of opacified sinuses on the sense of smell include (I) The presence of fluid or thickened mucosa in the sinuses may interfere with perceived olfactory ability by changing nasal airflow patterns or odorant access to receptors; (2) There may be olfactory receptors inside the sinuses; and (3) There may be a relation between the trigeminal receptors in the sinuses and the olfactory system. (Otolaryngol Head Neck Surg 1998; 118:183-6.)

D e c r e a s e d olfactory ability is often noted in those with nasal obstruction associated with an allergic or infectious rhinitis. Patients with chronic rhinosinusitis also complain of a fluctuating olfactory loss. Although most of these losses have been assumed to be caused by obstruction of airflow through the olfactory cleft, this has not been shown in living human subjects. Additionally, the location of the olfactory receptors in the human nasal cavity is not fully understood, 1 and airflow outside the olfactory cleft may be important for olfaction. 2 Patients having computed tomographic (CT) scans of their nasal and sinus cavities present an excellent From the Departments of Otolaryngology-Headand Neck Surgery, Kon-Kuk University Hospital (Dr. Hong) and Johns Hopkins Medical Institutions (Dr. Leopold), Departments of Radiology, Johns Hopkins Medical Institutions (Dr. Zinreich) and Wheeling Hospital (Dr. Benson), Department of Neurology, Johns Hopkins Medical Institutions (Drs. Mellits and Quaskey), and Radiology Consultants Association (Dr. Oliverio). Reprint requests: Donald A. Leopold, MD, Johns Hopkins Medical Institutions, Department of Otolaryngology-Head and Neck Surgery, 4940 EasternAve., Baltimore, MD 21224. Copyright 9 1998 by the AmericanAcademy of OtolaryngologyHead and Neck SurgeryFoundation, Inc. 0194-5998/98/$5.00 + 0 23/1/78796

opportunity to study this relation between nasal anatomy and the sense of smell. CT scanning is the mainstay of imaging for nasal, sinus, and olfactory dysfunctions because it provides the best images of the bones, cartilage, and soft tissues in this area. In addition, the patient's assessment of current olfactory status can be obtained at the time of the scan. METHODS

One hundred six patients referred for nasal and sinus CT scans at the Johns Hopkins Outpatient Center completed questionnaires on their symptoms immediately before imaging. These patients were referred by various physicians, usually otolaryngologists, because of nasal and sinus symptoms or findings on nasal examination or both. On the questionnaire, the patients were asked to describe their own left and right sense of smell as excellent, diminished, or absent at that time. Although some of these patients may have had a neural origin for their perceived olfactory loss, this should not have correlated with anatomic factors. Their CT scans were analyzed by two otolaryngologists and three neuroradiologists by using a semiobjective rating system of the size, shape, and opacity of 36 anatomic areas (Table 1). One form was completed on 183

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Table 1. A n a t o m i c f a c t o r s a n d historical i t e m s considered Size and opacity of: Pateney of: R & L Frontal sinuses R & L Frontal recesses R & L Agger nasi cells R & L Olfactory clefts R & L Ethmoid bullae R & L Ethmoid infundibuli R & L Concha bullosae R & L Nasal cavity R & L Hailer cells R & L Anterior ethmoids Presence and degree oi: R & L Anterior middle meati R & L Congested nasal R & L Maxillary sinuses mucosa R & L Posterior ethmoids R & L Nasal septal spurs R & L Sphenoid sinuses R & L Thickened bone R & L Previous surgery

Table 2. R e l a t i o n b e t w e e n t h e sense o f smell* a n d t h e l o g o f p e r c e n t a g e o p a c i t y o f m u l t i p l e sinus areas % Opacity variables

R smell p values

L smell p values

R Frontal sinus R Agger nasi cell R Ethmoid bulla R Concha bullosa R Hailer cell R Anterior ethmoid R Ant middle meatus R Maxillary sinus R Posterior ethmoid R Sphenoid / Frontal sinus L Agger nasi cell L Ethmoid bulla L Concha bullosa L Hailer ceil L Anterior ethmoid L Ant middle meatus L Maxillary sinus L Posterior ethmoid L Sphenoid sinus

NS NS NS NS NS NS NS NS NS <0.01 <0.01 NS NS NS NS NS NS <0.001 NS <0.001

NS NS NS NS NS NS NS NS NS NS <0.01 <0.01 <0.01 NS NS <0.01 NS <0.001 NS <0.01

NS, Nonsignificant(p > 0.01) *Smell rated excellent,diminished,or absent. Univariateanalysiswith t tests for continuousvariables.

each scan by using a consensus of the reviewers' judgments, with disagreements resolved by voting. The size of the various structures was judged to be small, medium, or large, and the opacity was rated as a percentage, with 100% being totally occluded. In the data analysis, those few sinuses that were absent (never developed) were included with the "small" size group or the 100% opacity group. In the "size" and "other" analyses (Tables 1 and 3), the three smell groups were combined into "excellent" and "any loss of smell" to allow use of the chi-square test and to maximize any possible contribution of size or patency. In the "opacity" analysis (Table 2), a log transform was

done to normalize the percentage opacity data, and it was evaluated as a continuous variable. Chi-square tests, t tests, and analysis of variance (ANOVA) were used to examine the relation between the CT scan anatomic data and the patient's olfactory assessments. Stepwise logistic regression analysis was used to assess the relation of the CT variables to smell and to rate the order of their importance in concert. Because the patients' estimates of their own olfactory abilities are not so rigorous as olfactometry, and because the estimates of anatomy are not so accurate as measurement, the data were generally assessed as significant at p < 0.01 to minimize overinterpretation of the data. RESULTS

1. There was no significant correlation between the perceived smell ability and the size of the sinus cavities. 2. As a rule, opacity of only left-sided anatomic structures was correlated with both left and right sense of smell (Table 2). There was one correlation between opacification of the right sphenoid and the right sense of smell. Because the sphenoid ostium is near the nasopharynx, this may represent mixing of the left and right nasal airstreams. 3. Total, but not partial, opacity of the left olfactory cleft, frontal recess, or ethmoidal infundibulum was correlated with decreased sense of smell (Table 3). 4. Logistic-regression analysis showed that the right smell was most correlated with the patency of the left olfactory cleft (p < 0.001) and whether the left ethmoidal bulla was more or less than 10% opacifled (p < 0.05). The left smell was most correlated with the percentage opacity of the left maxillary sinus (p < 0.001) and the degree of projection of a septal spur into the left nasal cavity (p < 0.05). DISCUSSION

We were somewhat surprised that our data showed no statistically significant relation between the size of the sinus cavities and the sense of smell, especially in light of previous work that suggested that olfactory ability did vary with the airway anatomy. 2 In his 1988 CT scan study, Leopold 2 proposed that the region between the lower anterior middle turbinate and the septum may control the flow to the olfactory receptors higher in the nasal cavity. Leopold's study, however, measured airway size, whereas this analysis looked at the sizes of the bony sinuses. Our data suggest that there is no gross effect of the bulging or shrinking of

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sinuses or turbinates into the nasal airway. It may be that the "lateral wall" anatomy of the nasal cavity, which "grows" into place, allows a functional airway to form around it. The logistic-regression analysis did show that the projection of a septal spur into the left nasal cavity was correlated with a decreased left sense of smell. Although the exact area and degree of this airway narrowing was not measured in our study, this concept is in accord with previously discussed 1988 study of Leopold2 and the Vainio-Mattila 1974 study 3 correlating nasal examinations and tested olfactory ability. Perhaps airway narrowing from the septal or "medial" side of the nasal airway does affect olfactory ability. Septal shape can be determined by either growth or trauma. We did not obtain information regarding nasal trauma in our subjects, however, so further analysis of growth versus trauma is not possible. The importance of this in clinical practice still needs to be determined, because in our experience and as reported by Dory and Frye,4 patients who have had septoplasty have never noted a clinically significant improvement in their olfactory ability after surgery. It is somewhat surprising that assessment of nasal airway patency has no statistically significant correlation with smell (Table 3). Schneider and Wolf's observations 5 of the anterior nasal airways and Leopold's 2 1988 CT scan analyses suggest that they could be correlated. An explanation of this apparent discrepancy is that our nasal patency evaluations were visual assessments of the entire nasal cavity on CT scans, not assessments or measurements of specific regions. The second unexpected finding of this study is the correlation of only left-sided sinus opacity with both right and left sense of smell. This suggests two possibilities: (1) our subjects were generally anosmic on the right side and were unaware of it (highly unlikely), or (2) their central nervous systems are preferentially "paying attention to" their left olfactory receptors to the exclusion of the right ones. As can be seen in Tables 2 and 3, our data are very clear in this. It has been known that people differentiate poorly between right and left olfactory ability. 6 What is new is that people may be spending much of their day using only one olfactory side, possibly the left. Hornung et al.7 suggested that human subjects have a better side for olfactory performance, and that it is the side where they get the better perception for the largest number of odorants. In their study, they also found more people using their left nostrils. They speculated that there are more right-handed people, and with the majority of olfactory information entering the central nervous system with-

Table 3. Association b e t w e e n patency, presence, a n d d e g r e e of other a n a t o m i c regions a n d smell* Other variables

R smell p values

L smell p values

R Frontal recess patency R Olfactory cleft patency R Ethmoid infundibulum patency R Nasal cavity patency R Nasal mucosal congestion degree R Septum spur degree R Thickened bone degree

NS NS NS NS NS NS NS

NS NS NS NS NS NS NS

R Evidence of prev surg L Frontal recess patency L Olfactory cleft patency L Ethmoid infundibulum patency L Nasal cavity patency L Nasal mucosal congestion degree L Septum spur degree L Thickened bone degree L Evidence of prev surg

NS <0.01 <0.01 <0.01 NS NS NS NS NS

NS <0.001 <0.01 <0.01 NS NS NS NS NS

*Smell classified as "excellent"or "any loss." Chi-squaretests for categoric variables. NS, Nonsignificant(p > 0.01).

out crossing, perhaps people with a dominant left hemisphere (right-handers) would show a dominant left nostill. 8 Unfortunately, we did not record the handedness of the patients in our study. On the contrary, several studies suggested right nostril dominance. Zatorre and Jones-Gotman, 9 in a study with healthy young adults, found that olfactory discrimination was better in the right nostril, although no differences in detection thresholds were found. Bellas et al. 1~and Jones-Gotman and Zatorre 11 found decreases in odor memory and olfactory detection in patients who had had partial right brain excisions, usually for epilepsy. It may be that a person's self-perception of olfactory performance (the task we asked our patients to perform) occurs in the opposite hemisphere of the brain from detection and memory. The finding in this study that total but not partial opacification of the olfactory cleft recess was correlated with olfactory ability was not surprising. It is reasonable that complete airflow blockage of odorants to this area would diminish olfactory ability. Opacification in the frontal recess correlating with decreased olfactory ability, however, suggests that airflow must go through this area toward the olfactory cleft. Studies on nasal airflow have suggested that the airflow to the olfactory cleft moves from anterior to posterior in this area) 2 Alternatively, it may suggest that there are olfactory receptors in this anterior area. 1 Opacification in sinus regions more distant from the olfactory cleft also were found to correlate with decreased olfactory ability (Tables 2 and 3). The ostia

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of the anterior ethmoid and maxillary sinuses and the ethmoidal infundibulum are all near that place between the septum and the middle turbinate that has some control of upper nasal airflow. 2 The ostia of the sphenoid similarly lies adjacent to the nasal airstream in the sphenoethmoid recess. Perhaps the small amount of edema that occurs in the nasal mucosa near an opacified sinus can divert airflow streams away from the olfactory cleft. In addition, there may be a change in the nasal or olfactory mucus layer caused by the discharge from an opacified sinus, which interferes with the sorption or transport of odorants on their way to the olfactory receptors. Finally, there may be olfactory receptors in human paranasal sinuses. There are olfactory receptors in the ethmoid sinuses of nonhuman mammals like dogs and rodents. During human ethmoid sinus surgery, the white olfactory nerves can sometimes be seen along the lateral aspect of the upper middle turbinates. It is unclear whether there are actual receptors inside the human paranasal sinuses, or whether the inflammation associated with thickened mucosa can affect the function of the adjacent olfactory nerves. Overall this study suggests that there is still much to learn about ordinary functioning of the human olfactory system. This would include the anatomy of the receptor location in the nasal cavity, the dynamics of

the flow of odorants to those receptors, and how the information obtained by those receptors is processed. REFERENCES 1. Leopold DA, Schwob JE, Hummel T, Kobal G, Knecht M, Hong SC. Anterior distribution of human olfactory neuroepithelium [abstract]. Chem Senses 1995;20:729. 2. Leopold DA. The relationship between nasal anatomy and human olfaction. Laryngoscope 1988;98(11):1232-8. 3. Vainio-MattilaJ. Correlations of symptoms and signs in random sampling study.Acta Otolaryngol Suppl (Stockh) 1974;318:18793. 4. Dory RL, Frye R. Influence of nasal obstruction on smell function. Otolaryngol Clin North Am 1989;22(2):397-411. 5. Schneider RA, Wolf S. Relation of olfactory acuity to nasal membrane function. J Appl Physiol 1960;15(5):914-20. 6. Schneider RA, Schmidt CE. Dependency of olfactory localization on non-olfactory cues. Physiol Behav 1976;2:305-9. 7. Hornung DE, Leopold DA, Mozell MM, Sheehe PR, Youngentob SL. Impact of left and right nostril olfactory abilities on binasal olfactory performance. Chem Senses 1990;15(2): 233-7. 8. Koelega HS. Olfaction and sensory asymmetry. Chem Senses Flavours 1979;4:89-95. 9. Zatorre RJ, Jones-Gotman M. Right-nostril advantage for discrimination of odors. Percep Psychophy 1990;47(6):526-31. 10. Bellas DN, Novelly RA, Eskenazi B. Olfactory lateralization and identification in right hemisphere lesion and control patients. Neurophysiologia 1989;27(9):1187-91. 11. Jones-Gotman M, Zatorre RJ. Odor recognition memory in humans: role of fight temporal and orbitofrontal regions. Brain Cognition 1993;22(2):182-98. 12. Scherer PW, Hahn II, Mozell MM. The biophysics of nasal airflow. Otolaryngol Clin North Am 1989;22(2):265-77.

Vestibular Rehabilitation This conference, sponsored by the Office of Continuing Medical Education of the University of Michigan Medical School, will be held April 30-May 1, 1998, at Towsley Center, University of Michigan, Ann Arbor, Mich. Course codirectors are Neil T. Shepard, PbD, and Steven A. Telian, MD. Credit hours in category 1 of the Physicians Recognition Award of the AMA will be announced. Application has been submitted to the American Osteopathic Association for accreditation. Other credits by specialty may apply. For further information, contact Joyce Robertson, Registrar, Towsley Center for Continuing Medical Education, Department of Medical Education Professions, P.O. Box 1157, Ann Arbor, MI 48106-1157; phone (313)763-1400 or (800)800-0666; fax (313)936-1641.