 |
|
Clinical Assessment of Retronasal Olfactory Function
Stefan Heilmann, MD;
Gundel Strehle;
Kati Rosenheim;
Michael Damm, MD;
Thomas Hummel, MD
Arch Otolaryngol Head Neck Surg. 2002;128:414-418.
ABSTRACT
| |
Objectives To develop a test kit for the simple assessment of retronasal olfactory
function and to compare orthonasal and retronasal olfactory function in healthy
subjects and patients with olfactory disorders.
Design and Patients We tested 230 individuals with normosmia, hyposmia, and anosmia using
grocery-available powders. Initially, 30 different substances were investigated.
Subjects identified each substance using a list with 4 verbal items (forced
choice). After preliminary experiments, 20 items were selected according to
the degree to which they were identified by normosmic and anosmic subjects.
Orthonasal olfactory function was assessed psychophysically using "sniffin'
sticks," which includes tests for odor identification, discrimination, and
butanol odor thresholds. In addition, anosmia was confirmed electrophysiologically
by means of olfactory-evoked potentials.
Results In healthy subjects, there was a test-retest reliability correlation
of r27 = 0.76 for retronasal olfactory
function, which is similar to other odor identification tests. Retronasal
testing in normosmic subjects allowed for the discrimination of sex-related
differences, with women scoring higher than men (P
= .007), and the identification of a slight decrease with age (r120 = -0.20; P = .03). Orthonasal
and retronasal identification of odors was found to correlate (r86 = 0.78; P<.001). Retronasal
testing allowed for the discrimination between normosmia, hyposmia, and anosmia
(P<.001). In addition, retronasal performance
of anosmic patients appeared to improve with duration of anosmia (P = .03). No difference was found between patients with anosmia of
different origin.
Conclusion Results of the present investigation indicate that the assessment of
retronasal olfactory function is possible using oral stimulus presentation.
INTRODUCTION
IN EVERYDAY LIFE, olfactory-mediated sensations are often confused with
gustatory-mediated sensations. Retronasally perceived odors are referred to
the oral cavity rather than to the olfactory epithelium. In fact, in some
languages the word taste is used to refer to both
the olfactory and gustatory components of food. Rozin1
described the sense of smell in terms of a duality, with orthonasal smelling
referring to the outside world and retronasal smelling referring to the inside
world. Differences between these perceptually different worlds are only partly
understood. In fact, hedonic evaluation may be completely different for the
same olfactory component when applied either orthonasally or retronasally,
which is observed, for example, with cheese or fish.1
Patients with a loss of smell often report gustatory deficits as the
first and most prominent symptom, indicating a reduced capacity to identify
and appreciate foods.2 Hence, patients experience
their olfactory deficit by means of a procedure similar to a retronasal smell
test. Despite this fact, retronasal smelling so far has received far less
attention than its orthonasal counterpart. Thus, the aims of this study were
(1) to develop a test kit for the simple assessment of retronasal olfactory
testing that resembles everyday challenges to retronasal olfactory identification
abilities and (2) to compare orthonasal and retronasal olfactory function
in healthy subjects and patients with olfactory disorders.
SUBJECTS, MATERIALS, AND METHODS
To assess retronasal olfactory function, we tested 230 individuals with
normosmia (n = 120), hyposmia (n = 37), and anosmia (n = 73) (Table 1). Investigations were performed according to the Declaration
of Helsinki on biomedical studies involving human subjects (Summerset West
Amendment). Most normosmic subjects were students at the medical schools of
the University of Dresden, Dresden, Germany, and the University of Cologne,
Köln, Germany (see Table 1
for subject characteristics). In addition, we investigated patients reporting
to the Smell Dysfunction Clinic at the Department of Otorhinolaryngology of
the University of Dresden. None of the participants received any form of financial
compensation.
|
|
|
|
Table 1. Characteristics of Investigated Patients
|
|
|
Orthonasal olfactory function was assessed psychophysically using "sniffin'
sticks,"3 which involves tests for butanol
odor threshold, odor discrimination, and identification. Results of the 3
subtests were also presented as a composite score derived from the sum of
the results obtained for threshold, discrimination, and identification measures
(TDI score). This score allows a diagnosis in terms of anosmia, hyposmia,
or normosmia.4 Anosmia was additionally confirmed
electrophysiologically by means of olfactory-evoked potentials.5
Controls were included on the basis of reports of normal olfactory function
and normal test results in either an olfactory screening test (n = 71)6 or the whole sniffin' sticks test battery (n = 49).3 As sniffin' sticks are a well-investigated means to
assess orthonasal olfactory function, the comparison with the new retronasal
test battery was thought to be useful, especially because the present investigation
was primarily concerned with the clinical validity of a new test for retronasal
olfactory function.
For retronasal stimulation, grocery store condiments and food items
available in powder form were used (eg, spices, instant drinks, and instant
soups; Table 2). The substances
were applied using squeezable plastic vials with a 6-cm long spout. Substances
were selected according to their texture (ie, nonsticky, small grains) and
the degree to which they are known in the general population. Subjects were
free to sample as much stimulant as needed for identification. This approach
also minimized the problem of standardizing the area of stimulation, differences
in tongue, or oral cavity size. In a typical trial, through the wide-opened
mouth, the experimenter placed approximately 0.05 g on the middle of the tongue
inside the oral cavity. Before application of the first stimulant and after
each trial, subjects rinsed with tap water; this helped to minimize interindividual
differences in salivation, which might interfere with the release of the odorants.
The procedure was self-timed, although test intervals were usually 1 minute
due to rinsing. Each substance was identified by means of a closed set with
4 verbal items using a forced-choice procedure (subjects also indicated the
taste of the substances, the results of which will be reported elsewhere).
Responses were not analyzed with regard to "near" or "far" misses. All descriptors
used indicated odors that had previously been shown to be familiar to more
than 75% of a test population.3 Scores were
obtained by adding the number of correct identifications of retronasal stimuli.
For investigations of the test-retest reliability, subjects without nasal
pathologic features were tested twice at an interval of 1 to 7 days.
|
|
|
|
Table 2. Grocery-Available Powders Used for Retronasal Olfactory Testing
|
|
|
Results were analyzed with SPSS 9.0 for Windows (SPSS Inc, Chicago,
Ill). Because olfactory sensitivity varies as a function of age,7
subjects were separated into 4 age groups (groups A-D). Ages of subjects in
the groups were as follows: group A, 6 to 15 years; group B, 16 to 35 years;
group C, 36 to 55 years; group D, older than 55 years. To explore olfactory
sensitivity in relation to age and sex, data were submitted to analyses of
variance using the general linear model and multifactorial design analysis
of variance with "between-subject factors," "group," and "sex" with Bonferroni
post hoc tests. Correlations were performed using Pearson statistics. The 
level was .05.
RESULTS
From 30 items used for retronasal testing, 20 were selected according
to the degree to which they could be identified (Table 3). Specifically, substances that were poorly recognized by
normosmic subjects (ie, caraway, anise, blueberry, almond, sour cherry, bacon,
mustard, and coconut; identification rate in normosmic subjects <70%) and
substances that were identified to a similar degree by hyposmic, anosmic,
and normosmic subjects (ie, lemon and pepper) were left out. All results reported
in this section relate to the test based on 20 items only (compare with Table 2).
|
|
|
|
Table 3. Percentage of Correct Identifications of Items Used for Retronasal
Olfactory Testing
|
|
|
In healthy subjects, there was a test-retest reliability correlation
of r27 = 0.76 for retronasal olfactory
function (Figure 1). Results for
retronasal testing in normosmic subjects (55 men and 65 women; mean age, 33.5
years) allowed for the discrimination of sex-related differences, with women
scoring higher than men (t120 = 2.77; P = .007), and the identification of a slight age-related
decrease (r120 = -0.20; P = .03).
|
|
|
|
Figure 1. Correlation of scores for retronasal
olfactory testing obtained for test and retest. Data from healthy subjects
only (r27 = 0.76). The width of a bubble
relates linearly to the number of data points included in the bubble.
|
|
|
The correlation between retronasal olfactory function and scores for
the 3 orthonasal tests for normosmic and hyposmic subjects varied between r86 = 0.78 for odor identification (P<.001), r86 = .61 for odor
discrimination (P<.001), and r86 = 0.57 for butanol thresholds (P<.001)
(Figure 2).
|
|
|
|
Figure 2. Correlation between scores for
retronasal testing and tests of orthonasal olfactory function (A, orthonasal
odor identification; B, orthonasal odor discrimination; and C, orthonasal
butanol odor thresholds; higher scores indicate higher olfactory sensitivity).
When considering data from both normosmic and hyposmic patients, the coefficient
of correlation was largest for retronasal and orthonasal odor identification
(r86 = 0.78; P<.001).
In contrast, coefficients of correlation between scores for retronasal olfactory
function and orthonasal odor discrimination (r86 = 0.61; P<.001) and butanol thresholds
(r86 = 0.57; P<.001)
were lower.
|
|
|
Retronasal testing allowed for the discrimination between normosmic,
hyposmic, and anosmic subjects (F2,227 = 279; P<.001). Specifically, there was almost no overlap between scores
of anosmic (score of 12.3 at the 95th percentile) and normosmic (score of
13 at the 5th percentile) subjects, whereas scores of hyposmic subjects exhibited
overlap with both anosmic and normosmic subjects (Table 4).
|
|
|
|
Table 4. Descriptive Statistics of Results for Retronasal Olfactory
Testing
|
|
|
Retronasal identification scores in anosmic patients improved slightly
with duration of anosmia (in this analysis all patients with congenital olfactory
loss were excluded; in addition, only those patients in whom the duration
of olfactory loss was known were taken into consideration). Patients were
divided in 2 groups with duration of olfactory loss of 2 years or less (n
= 26; mean [range] age, 58 [28-89] years) and more than 2 years (n = 34; mean
[range] age, 56 [22-84] years). When duration of anosmia was 2 years or less,
patients scored lower compared with patients with longer duration of anosmia
(duration  2 years: mean ± SEM score of 7.9 ± 0.4; duration
>2 years: mean ± SEM score of 9.3 ± 0.4; t58 = 2.18; P = .03).
COMMENT
A number of factors are known to be involved in the retronasal perception
of olfactory stimuli. It has been shown that adequate orthonasal olfactory
function is a prerequisite for good retronasal olfactory performance.8 However, in some cases good orthonasal olfactory function
goes along with impaired retronasal smelling. This may be due to oral conditions
influencing retronasal perception.8 In addition,
mouth movements, mastication, and swallowing are known to influence the perception
of retronasal stimuli.9-10 Pierce
and Halpern11 reported that odor identification
is better when stimuli were presented orthonasally compared with retronasal
odor presentation. This was partly improved by training. That is, subjects
using a certain breathing technique to enhance retronasal stimulation scored
higher in retronasal identification tasks. However, retronasal odor identification
abilities still did not reach the level of orthonasal odor identification.
It was hypothesized that this difference was due to the differential efficacy
in odor presentation to the olfactory epithelium.
Apart from these factors, information-processing patterns and interactions
with other oral senses may influence the evaluation of olfactory information
obtained via the retronasal route (eg, as demonstrated in the poster by Fast
et al12). Different hypotheses have been presented
on interactions between taste and smell.13-18
Gillan15 compared both odor-odor and taste-taste
mixtures with odor-taste mixtures. He was able to show that suppression between
senses was smaller than suppression induced by mixtures stimulating the same
sensory system. Burdach et al16 reported that
measured sensitivity to stimuli decreased when odor-taste mixtures were administered.
This means that thresholds might increase as a consequence of suppression
caused by a combination of different stimuli. On the other hand, when magnitude
estimation procedures were used for the classification of stimuli, a number
of authors reported an independent contribution of smell and taste to overall
intensity.13-14,17-18
The test used in the present study addressed retronasal stimulation
similar to everyday challenges. Specifically, subjects were allowed to distribute
the powders intraorally, perform masticationlike movements, and to swallow
(compare with the articles by Burdach and Doty9
and Harrison et al 10). However, the "real-life
stimuli" used in the present study not only activated the olfactory system,
but additionally provided sensations mediated by the gustatory and trigeminal
systems. Based on this sensory information, some of the stimulants (eg, lemon)
could be identified by more than 80% of the anosmic patients. After excluding
these substances from the test, it appeared that olfactory-mediated information
was a major factor in the identification of the 20 substances that remained
in the test. This hypothesis is supported by the separation of anosmic, hyposmic,
and normosmic subjects, which was possible by means of the 20-item retronasal
test kit. The use of stimuli that do not specifically activate the olfactory
system is also applied in most tests of orthonasal odor identification (eg,
the University of Pennsylvania Smell Identification Test19).
In these tests, it is fundamentally assumed that the identification of most
odors is possible through some degree of olfactory function but to a much
smaller degree through, for example, trigeminal sensitivity.
The discrimination between different degrees of olfactory loss is also
the prerequisite for clinical applications of this test. In addition, its
test-retest reliability correlation of r27
= 0.76 is similar to other olfactory tests using a similar number of items.
For example, a 12-item odor identification reached a coefficient of correlation
of 0.71,20 and a 16-item odor identification
test reached a coefficient of correlation of 0.73.3
Also, it has to be considered that the coefficient of correlation for test
and retest was established in a relatively homogeneous population with little
interindividual variance. Thus, it can be assumed that the coefficient of
correlation would be higher if different populations had been examined (eg,
normosmic and hyposmic subjects), which will be investigated in future studies.
About the test's validity, it also allowed for the identification of
effects related to both age and sex. This indicates that retronasal function
follows the course of well-known, age-related changes in orthonasal olfactory
function.7 In addition, the better performance
of women in orthonasal olfactory testing has been described frequently21-23; this appears to
be equally present in retronasal olfactory testing. Previous studies already
described the decline of retronasal olfactory function with age, using solely
the oral presentation of ethyl butyrate with unpinched or pinched nose (thus
switching retronasal smelling on and off)24
or using a single food ingredient (marjoram).25
Our study extended these findings with regard to retronasal odor identification.
Most interestingly, retronasal identification abilities of anosmic patients
appeared to improve slightly with duration of anosmia. In an adaptive sense,
patients seem to become more efficient in terms of the use of gustatory and/or
trigeminal information. It may be speculated that this indicates cross-modal
plasticity as it has been hypothesized to occur, for example, for visual processing
in congenitally deaf subjects.26
In conclusion, results of the present investigation indicate that the
assessment of retronasal olfactory function is possible using oral stimulus
presentation. Future developments will focus on an extension of the number
of test items used to improve its sensitivity.
AUTHOR INFORMATION
Accepted for publication September 10, 2001.
We would like to thank John Prescott, PhD, University of Otago, Dunedin,
New Zealand, for his thoughtful comments on earlier versions of the manuscript.
We also would like to thank our referees for their most helpful suggestions.
Corresponding author: Thomas Hummel, MD, Department of Otorhinolaryngology,
University of Dresden Medical School, Fetscherstr 74, 01307 Dresden, Germany
(e-mail: thummel{at}rcs.urz.tu-dresden.de).
From the Department of Otorhinolaryngology, University of Dresden Medical
School, Dresden, Germany (Drs Heilmann and Hummel and Mss Strehle and Rosenheim);
and the Department of Otorhinolaryngology, University of Cologne, Köln,
Germany (Dr Damm).
REFERENCES
| |
1. Rozin P. "Taste-smell confusions" and the duality of the olfactory sense. Percept Psychophys. 1982;31:397-401.
ISI
| PUBMED
2. Deems DA, Doty RL, Settle RG, et al. Smell and taste disorders: a study of 750 patients from the University
of Pennsylvania Smell and Taste Center. Arch Otolaryngol Head Neck Surg. 1991;117:519-528.
FULL TEXT
|
ISI
| PUBMED
3. Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G. "Sniffin' sticks": olfactory performance assessed by the combined testing
of odor identification, odor discrimination and olfactory threshold. Chem Senses. 1997;22:39-52.
FREE FULL TEXT
4. Kobal G, Klimek L, Wolfensberger M, et al. Multicenter investigation of 1,036 subjects using a standardized method
for the assessment of olfactory function combining tests of odor identification,
odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol. 2000;257:205-211.
FULL TEXT
| PUBMED
5. Kobal G, Hummel T. Olfactory and intranasal trigeminal event-related potentials in anosmic
patients. Laryngoscope. 1998;108:1033-1035.
FULL TEXT
|
ISI
| PUBMED
6. Kobal G, Hummel T, Sekinger B, Barz S, Roscher S, Wolf S. "Sniffin' sticks": screening of olfactory performance. Rhinology. 1996;34:222-226.
PUBMED
7. Schiffman S. Changes in taste and smell with age: psychophysical aspects. In: Ordy JM, Brizzee K, eds. Sensory Systems and
Communication in the Elderly. New York, NY: Raven Press; 1979:227-246.
8. Duffy VB, Cain WS, Ferris AM. Measurement of sensitivity to olfactory flavor: application in a study
of aging and dentures. Chem Senses. 1999;24:671-677.
FREE FULL TEXT
9. Burdach KJ, Doty RL. The effects of mouth movements, swallowing, and spitting on retronasal
odor perception. Physiol Behav. 1987;41:353-356.
FULL TEXT
| PUBMED
10. Harrison M, Campell S, Hills BP. Computer simulation of flavor release from solid foods in the mouth. J Agric Food Chem. 1998;46:2736-2743.
FULL TEXT
11. Pierce J, Halpern BP. Orthonasal and retronasal odorant identification based upon vapor phase
input from common substances. Chem Senses. 1996;21:529-543.
FREE FULL TEXT
12. Fast K, Tie K, Bartoshuk LM, Kveton JF, Duffy VB. Unilateral anesthesia of the chorda tympani nerve suggests taste may
localize retronasal olfaction. Poster presented at: 22nd Annual Conference of the Association for
Chemoreception Science; April 2000; Sarasota, Fla.
13. Murphy C, Cain WS. Taste and olfaction: independence vs interaction. Physiol Behav. 1980;24:601-605.
FULL TEXT
| PUBMED
14. Garcia-Medina MR. Flavor-odor taste interactions in solutions of acetic acid and coffee. Chem Senses. 1981;6:13-22.
FREE FULL TEXT
15. Gillan DJ. Taste-taste, odor-odor, and taste-odor mixtures: greater suppression
within than between modalities. Percept Psychophys. 1983;33:183-185.
ISI
| PUBMED
16. Burdach KJ, Kroeze JH, Koster EP. Nasal, retronasal, and gustatory perception: an experimental comparison. Percept Psychophys. 1984;36:205-208.
ISI
| PUBMED
17. Hornung DE, Enns MP. The contributions of smell and taste to overall intensity: a model. Percept Psychophys. 1986;39:385-391.
ISI
| PUBMED
18. Hornung DE, Enns MP. Odor-taste mixtures. Ann N Y Acad Sci. 1987;510:86-90.
ISI
| PUBMED
19. Doty RL. The Smell Identification Test Administration Manual. 3rd ed. Haddon Heights, NJ: Sensonics Inc; 1995.
20. Doty RL, McKeown DA, Lee WW, Shaman P. A study of the test-retest reliability of ten olfactory tests. Chem Senses. 1995;20:645-656.
FREE FULL TEXT
21. Cain WS. Odor identification by males and females: prediction vs performance. Chem Senses. 1982;7:129-142.
FREE FULL TEXT
22. Cometto-Muniz E, Noriega G. Gender differences in the perception of pungency. Physiol Behav. 1985;34:385-389.
FULL TEXT
| PUBMED
23. Yousem DM, Maldjian JA, Siddiqi F, et al. Gender effects on odor-stimulated functional magnetic resonance imaging. Brain Res. 1999;818:480-487.
FULL TEXT
|
ISI
| PUBMED
24. Stevens JC, Cain WS. Smelling via the mouth: effect of aging. Percept Psychophys. 1986;40:142-146.
ISI
| PUBMED
25. Cain WS, Reid F, Stevens JC. Missing ingredients: aging and the discrimination of flavor. J Nutr Elder. 1990;9:3-15.
26. Wolff AB, Thatcher RW. Cortical reorganization in deaf children. J Clin Exp Neuropsychol. 1990;12:209-221.
ISI
| PUBMED
RELATED ARTICLE
Archives of Otolaryngology–Head & Neck Surgery Reader's Choice: Continuing Medical Education
Arch Otolaryngol Head Neck Surg. 2002;128(4):465-466.
FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
|
Synergy and Masking in Odor Mixtures: An Electrophysiological Study of Orthonasal vs. Retronasal Perception
Ishii et al.
Chem Senses 2008;33:553-561.
ABSTRACT
| FULL TEXT
Retronasal and Orthonasal Olfactory Ability After Laryngectomy
Leon et al.
Arch Otolaryngol Head Neck Surg 2007;133:32-36.
ABSTRACT
| FULL TEXT
Olfactory Function Assessed With Orthonasal and Retronasal Testing, Olfactory Bulb Volume, and Chemosensory Event-Related Potentials
Rombaux et al.
Arch Otolaryngol Head Neck Surg 2006;132:1346-1351.
ABSTRACT
| FULL TEXT
Mechanical Obstruction of the Olfactory Cleft Reveals Differences Between Orthonasal and Retronasal Olfactory Functions
Pfaar et al.
Chem Senses 2006;31:27-31.
ABSTRACT
| FULL TEXT
Differences Between Orthonasal and Retronasal Olfactory Functions in Patients With Loss of the Sense of Smell
Landis et al.
Arch Otolaryngol Head Neck Surg 2005;131:977-981.
ABSTRACT
| FULL TEXT
Intranasal Concentrations of Orally Administered Flavors
Frasnelli et al.
Chem Senses 2005;30:575-582.
ABSTRACT
| FULL TEXT
|
