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Characteristics of Olfactory Disorders in Relation to Major Causes of Olfactory Loss
Andreas F. P. Temmel, MD;
Christian Quint, MD;
Bettina Schickinger-Fischer, MD;
Ludger Klimek, MD;
Elisabeth Stoller;
Thomas Hummel, MD
Arch Otolaryngol Head Neck Surg. 2002;128:635-641.
ABSTRACT
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Objective To investigate the consequences of olfactory loss and explore specific
questions related to the effect of duration of olfactory loss, degree of olfactory
sensitivity, and cause of the olfactory loss.
Patients A total of 278 consecutive patients with hyposmia or anosmia were examined.
Results Causes of olfactory loss were categorized as follows: trauma (17%),
upper respiratory tract infection (URI) (39%), sinonasal disease (21%), congenital
anosmia (3%), idiopathic causes (18%), or other causes (3%). Our data suggest
that (1) recovery rate was higher in URI olfactory loss than in olfactory
loss from other causes; (2) likelihood of recovery seemed to decrease with
increased duration of olfactory loss; and (3) the elderly are more prone to
URI olfactory loss than younger patients. Regarding changes in quality of
life (QoL), we found that (1) in most patients olfactory loss caused food-related
problems; (2) loss in QoL did not change with duration of olfactory loss;
(3) younger patients had more complaints than older ones, and women had more
complaints than men; (4) complaint scores were higher in hyposmic patients
than in anosmic patients; and (5) self-rated depression did not relate to
measured olfactory function.
Conclusions Among many complaints of olfactory loss, the predominant ones were food
related. This loss in QoL seemed to be of greater importance in younger than
in older people, and women seem to be affected more strongly than men.
INTRODUCTION
LOSS OF olfactory function affects the patient's appreciation of food
and drink; it has an impact on safety (eg, detection of spoiled foods and
smoke); and it may also produce bodily insecurity: the patient's own body
odors are no longer self-perceived, which, in our clinical experience and
that of others,1 has led to an exaggeration
of patients' hygiene measures or the excessive use of perfume. However, the
loss of olfaction can be particularly insidious and escape detection because,
unlike loss of sight or hearing, it is not readily apparent to others. A good
example of this difficulty of detection is that patients with congenital anosmia
in our population did not discover their olfactory loss until after age 10
years. The present study was designed to investigate the consequences of olfactory
loss in daily life and to explore specific questions related to the effect
of the duration, degree, and causes of the olfactory disorder.
PATIENTS, MATERIALS, AND METHODS
We evaluated 278 consecutive patients (155 women, 123 men) with olfactory
loss who were either referred or directly sought help for olfactory disorders
at the departments of otorhinolaryngology of the University of Vienna, Austria,
and the University of Dresden, Germany. Subjects were between ages 14 and
86 years. The study was performed according to the principles of the Declaration
of Helsinki/Summerset West on biomedical research involving human subjects.
All patients were thoroughly examined by an experienced otorhinolaryngologist,
including detailed endoscopic investigation of the olfactory cleft. Whenever
a patient's history was unclear or the psychophysical olfactory test results
were ambiguous, the patient additionally underwent computed tomographic scans
of the nasal cavity, magnetic resonance imaging with a special focus on important
olfactory structures (eg, olfactory bulbs and tracts, olfactory sulcus), or
olfactory evoked potentials.2
CHEMOSENSORY TESTING
Psychophysical testing was performed by means of "Sniffin' Sticks"3-4 bilaterally, and it involved tests
for odor threshold (N-butanol), discrimination, and
identification. Results of the 3 subtests were presented as a sum of the results
obtained for threshold, discrimination, and identification measures (TDI score).4 If the TDI score was 31 or higher, the patient was
considered normosmic; with a score between 16 and 30, he or she was considered
hyposmic. With a score lower than 16, the patient was regarded as functionally
anosmic.4 Olfactory evaluation required approximately
30 minutes. Diagnostic criteria for the classification of the cause of the
olfactory disorder are given in Table 1.
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Table 1. Categorization of Patients According to History of Their Olfactory
Disturbance*
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QUESTIONNAIRE
A self-reporting questionnaire was used that contained mainly questions
regarding olfactory sensitivity and quality of life (QoL) issues. It had been
developed in collaboration with the Arbeitsgemeinschaft Olfaktologie/Gustologie
der Deutschen Gesellschaft für Hals-Nasen-Ohren Heilkunde, Kopf und Halschirurgie,
Dresden, Germany. Questions related to the subjective degree of olfactory
loss and associated difficulties such as cooking, eating, body hygiene, appetite,
problems in everyday life, ways to manage this handicap, and the subjective
degree of decrease of QoL. Both affirmative and symptom-based questions were
used. Questionnaires were filled in before commencement of olfactory tests.
After receiving detailed instructions by a member of the staff, the subjects
usually completed the forms in the waiting area.
STATISTICAL ANALYSIS
Statistical analyses were performed using SPSS 10.0 (SPSS Inc, Chicago,
Ill). Data were submitted to nonparametric statistical analysis including
Kruskal-Wallis, Mann-Whitney, and  2 tests. Correlational analyses
were performed using Spearman statistics. The minimum  level was .05.
Nonsignificant results are indicated as NS.
RESULTS
CHARACTERISTICS OF PATIENTS
A total of 278 patients were included (155 women, 123 men). All of them
had olfactory dysfunction as established by means of psychophysical testing;
151 were functionally anosmic, 127 were hyposmic. Major causes for olfactory
loss were upper respiratory tract infection (URI) (n = 102; 36%), sinonasal
disease (SND) (n = 60; 21%), trauma (n = 47; 17%), congenital anosmia (n =
9; 3%), and other causes including intoxication (solvents), abuse of nasal
decongestants, Parkinson disease, radiation, or cerebral infarction (n = 9;
3%). No reason for olfactory loss could be identified in 51 patients (18%)
(Figure 1); in at least 9 of these
patients who were older than 70 years, aging might have contributed to olfactory
loss.5
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Figure 1. Olfactory loss among our patients
was caused by upper respiratory tract infection (URI) (n = 102; 36%), sinonasal
disease (SND) (n = 60; 21%), trauma (n = 47; 17%), congenital anosmia (n =
9; 3%), and other causes (n = 9; 3%). No cause for olfactory loss could be
found in 51 patients (18%).
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RELATIONSHIP OF TEST SCORES TO CAUSES OF OLFACTORY LOSS
Results of the 3 different olfactory tests are shown in Table 2, separately for anosmic and hyposmic patients in relation
to the investigated causes of olfactory loss. When comparing results of hyposmic
patients in the 3 olfactory tests, we found no significant difference between
the 4 major causes (23<2.3; P>.51; Kruskal-Wallis test); in other words, the results pattern from
the 3 olfactory tests did not indicate the cause of the disorder.
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Table 2. Results for Butanol Odor Thresholds, Odor Discrimination,
and Odor Identification in Patients With Functional Anosmia and Hyposmia,
by Cause of Olfactory Loss*
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In URI olfactory loss, more patients were found to be hyposmic (n =
62) than anosmic (n = 40) (2 = 4.75; P
= .03). In contrast, for all other causes, this ratio was reversed (for SND,
28 hyposmic vs 32 anosmic [NS]; trauma, 15 hyposmic vs 32 anosmic [2 = 6.15; P = .01]; idiopathic cases, 18 hyposmic
vs 33 anosmic [2 = 4.41; P= .04];
other causes, 4 hyposmic vs 5 anosmic [NS]).
RELATIONSHIP BETWEEN SEX AND OLFACTORY DISORDER
A higher percentage of women (44%) than men (28%) suffered from URI
olfactory loss (2 = 11.3; P = .001).
These sex-related differences were not significant for SND (19% women vs 25%
men), trauma-related olfactory loss (12% women vs 24% men), or idiopathic
olfactory disorders (19% women vs 18% men). Approximately the same portion
of male and female patients suffered from hyposmia and anosmia (women, 73
with hyposmia vs 82 with anosmia; men, 54 with hyposmia vs 69 with anosmia).
RELATIONSHIP BETWEEN AGE AND OLFACTORY DISORDER
We categorized subjects into 3 age groups: group A, younger than 41
years (n = 60); group B, 41-60 years (n = 130); and group C, older than 60
years (n = 88). Different causes were present at different ratios in these
3 age groups. The highest percentage of URI olfactory disorders was seen in
older subjects (group A, 23%; group B, 31%; and group C, 55%). No such differences
were found for SND (A, 30%; B, 24%; and C, 13%), posttraumatic causes (A,
20%; B, 18%; and C, 14%), or idiopathic causes (group A, 15%; B, 22%; and
C, 15%) (Figure 2). Statistical
differences in the relative presence of the 4 most frequent causes were found
only for group C (2 = 46.38; P<.001).
The relative number of hyposmic patients was not significantly different in
different age groups (group A, 31 hyposmic vs 29 anosmic; group B, 56 hyposmic
vs 74 anosmic; group C, 40 hyposmic vs 48 anosmic).
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Figure 2. The highest percentage of olfactory
disorders related to upper respiratory tract infection (URI) was seen in older
subjects. No significant age-related differences were found for sinonasal
disease (SND) or posttraumatic or idiopathic causes of olfactory loss.
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RELATIONSHIP BETWEEN DURATION OF OLFACTORY DISORDER, CAUSE, AGE, AND
SEX
We categorized subjects into 3 duration groups of olfactory loss: group
A, less than 24 months; group B, 24-48 months; and group C, longer than 48
months. The presence of anosmia increased with duration of olfactory loss.
Specifically, most of the patients with the longest duration of olfactory
loss were anosmic (group C, 16 hyposmic vs 34 anosmic; 2 =
6.48; P = .01); no significant differences were found
between the frequencies of hyposmia and anosmia in group A (55 hyposmic vs
53 anosmic) or B (25 hyposmic vs 21 anosmic). In addition, the percentage
of patients with different causes of olfactory disorders was associated with
the duration of the disease. That is, URI olfactory disorders were most frequent
in duration groups A (56%) and B (57%) and least frequent in group C (26%).
The percentage of SND increased with increasing duration (group A, 5%; B,
9%; and C, 24%); similar findings were made for idiopathic olfactory loss
(group A, 14%; B, 4%; and C, 30%) but not for trauma (group A, 22%; B, 26%;
and C, 16%) or other causes (group A, 4%; B, 4%; and C, 4%). Accordingly,
statistics revealed that the percentages of the 4 most frequent causes were
significantly different when the duration of disease was shorter than 48 months
(group A, 2 = 66.2 with P<.001;
group B, 2 = 32.3 with P<.001),
but not when the duration of disease was longer than 48 months.
The percentage of women was found to be higher in duration group A (64%
women vs 36% men; 2 = 8.33; P = .004).
In duration groups B and C, men and women were more equally distributed (group
B, 44 women vs 57 men; group C, 46 women vs 54 men; NS).
SELF-RATINGS OF OLFACTORY AND GUSTATORY FUNCTION
Most of the examined patients fully completed the questionnaire. From
a total of 275 patients, 210 (76%) reported loss of olfactory sensitivity
and 210 patients (76%) reported altered sensitivity. Interestingly, although
11 (4%) of the 275 patients reported normal olfactory sensitivity, after testing
5 of these 11 were diagnosed as functionally anosmic, and the remaining 6
as hyposmic. These patients had been referred to the clinic by other otorhinolaryngologists
or by general practitioners who suspected olfactory loss; some of them also
came because relatives and/or spouses urged them to seek counseling. Most
of the patients also reported loss (150/231; 65%) or alteration (33/231; 14%)
of gustatory function.
PERCENTAGE DECREASE OF QoL
On average, patients reported a 20% decrease of QoL related to their
olfactory loss. These figures differed with causes: patients with URI olfactory
disorders (22%), SND (27%), trauma (19%), idiopathic causes (13%), or other
causes (13%) rated the loss of QoL to a similar degree (differences NS). Patients
with congenital anosmia indicated no loss (0%) in QoL. No significant difference
in QoL was found across age groups, indicating that decreased QoL was not
correlated with the duration of olfactory loss. Similarly, neither sex-related
(women, 21% vs men, 19%) nor age-related differences (age group A, 24%; B,
21%; and C, 15%) were seen in this measure of QoL. In hyposmic patients, the
self-rated decrease of QoL exhibited a low coefficient of correlation with
the subject's olfactory loss as measured by the TDI score (r115 = 0.22; P = .02).
DIFFICULTIES IN DAILY LIFE
Almost all patients reported difficulties in daily life due to their
olfactory disorders. Specifically, 73% complained of difficulties with cooking,
68% of mood changes, 56% of decreased appetite, 50% of eating spoiled food,
41% of too little perception of their own body odor, 30% of burning food,
and 8% of problems at work (Figure 3).
These complaints were added to create a complaint score (percentage of complaints
present); ie, presence of an individual complaint was valued as "1"; absence
of this complaint, "0." The maximum complaint score (all complaints present)
was 100%; the lowest score (no complaints) was 0%.
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Figure 3. Quality of life issues of patients
with olfactory loss: cooking indicates difficulties with cooking; mood, mood
changes; appetite, decreased appetite; spoiled food, eating of spoiled food
because of inability to smell spoilage; body odor, too little perception of
own body odor; burnt food, burning food while cooking because of inability
to detect burning odor; and work, work-related problems.
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Both age and sex had a significant effect on difficulties in daily life.
Specifically, the youngest patients had the highest degree of difficulties
(age group A, 54%; B, 53%; C, 38% [22 = 24.6; P<.001; Kruskal-Wallis test]) (Figure 4), and women mentioned more complaints than men (53% vs
42%, respectively; U = 6751; P<.001; Mann-Whitney test) (Figure
4). Duration of disease had no significant effect on the complaint
score (duration group A, 46%; B, 43%; and C, 46%). Similarly, the cause of
the olfactory disorder had no significant effect (URI, 46%; SND, 53%; trauma,
47%; and idiopathic causes, 51%).
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Figure 4. In the comparison of complaint
scores in relation to age, sex, and olfactory loss, the oldest patients had
the lowest number of difficulties (P<.001); women
mentioned more complaints than men (P<.001); and
anosmic patients had lower scores than hyposmic ones (P= .01).
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Anosmic patients had a lower complaint score than hyposmic ones (anosmia,
45%; hyposmia, 52%; U = 7881; P = .01; Mann-Whitney test) (Figure
4); however, there was no significant difference between anosmia
and hyposmia in QoL ratings (subjects with anosmia, 16%; subjects with hyposmia,
24%). In hyposmic patients, no significant correlation was found between the
complaint score and the patient's ability to smell (TDI score). In addition,
the complaint score and the self-rated QoL did not correlate very well (r242 = 0.18; P = .01).
Patients who reported depressed mood as a consequence of olfactory loss
had significantly higher complaint scores (depressed, 66%; nondepressed, 45%; U = 964; P<.001; Mann-Whitney
test) and higher self-ratings of loss of QoL (depressed, 44%; nondepressed,
29%; U = 1824; P = .001;
Mann-Whitney test). In contrast, there was no significant difference between
these 2 groups of patients regarding self-rated olfactory abilities (depressed,
22%; nondepressed, 22%) and TDI score (depressed, 16.2; nondepressed, 16.4).
COMMENT
The present study addresses 2 major issues: (1) specific characteristics
of olfactory disorders as related to their causes and (2) the effects of olfactory
disorders on daily life. Herein we discuss some of our more important findings.
DIFFERENT OLFACTORY SUBTESTS DO NOT SEEM TO DIFFERENTIATE BETWEEN CAUSES
OF OLFACTORY LOSS
The present data indicate that causes of olfactory loss have no significant
influence on results in odor thresholds, discrimination, and identification.
However, further research in larger populations is needed to investigate whether
the 3 tests of olfactory function differ in their sensitivity to olfactory
deficits in different age groups or in relation to the duration of the olfactory
loss.
PATIENTS MAY REPORT NORMAL OLFACTORY FUNCTION IN THE PRESENCE OF ANOSMIA
In the present study, 4% of the patients reported normal olfactory function
despite the presence of olfactory deficit. This indicates once more6-7 that olfactory testing is needed to
properly evaluate patients' olfactory abilities. Recently, it has also been
reported that 42% of 203 patients were unable to correctly rate olfactory
loss on a 4-point scale (normal, impaired but not absent, no ability, highly
sensitive).8 Thus, it seems that a simple interview
may provide entirely misleading information.
INDICATIONS FOR HIGHER RECOVERY RATE IN URI OLFACTORY LOSS
Among patients with URI olfactory loss, hyposmia was more common than
anosmia. In addition, duration of olfactory loss was found to be shorter in
URI olfactory disorders than in SND-related or idiopathic olfactory dysfunction.
These findings may relate to the relatively high rate of recovery found in
URI disorders.9-11
LIKELIHOOD OF RECOVERY DECREASES WITH INCREASING DURATION OF OLFACTORY
LOSS
The presence of anosmia was found to increase as the duration of the
olfactory loss increased. This is consistent with reports that late recovery
is relatively rare.12-13
ELDERLY PATIENTS ARE PRONE TO URI OLFACTORY LOSS
Consistent with other observations,9, 14-15
we found that URI olfactory loss was more frequent in patients 65 years or
older, whereas all other causes were almost equally distributed across the
ages. In addition, an age-related increase in the prevalence of olfactory
loss has been reported.16 The same study indicated
that olfactory dysfunction due to influenza and/or common colds and/or sinus
infection correlated negatively with age. Because the authors evaluated olfactory
loss in the context of URI and SND, this specific finding neither supports
nor contradicts the present observations. This higher incidence of URI olfactory
loss in elderly persons may relate to the age-related decrease of the size
of the olfactory epithelium,17-18
and thus to a higher vulnerability to the consequences of the infection.
DECREASE IN QoL MAY RELATE TO THE DEGREE OF OLFACTORY FUNCTION BEFORE
LOSS OF OLFACTORY ABILITIES
More than 70% of our population reported that the chemosensory disorder
interfered with their daily life activities, including food preparation and
intake. Both age and sex had a significant effect on difficulties in daily
life. Specifically, younger patients had more complaints than older ones,
and women had more than men. This may relate to the relative loss of olfactory
function, or, in other words, to the degree of olfactory function before its
loss. Specifically, as olfactory function is best in the young5
and better in women than in men,19 these initially
more sensitive groups are more likely to have the most complaints when olfactory
function is impaired. The higher significance of olfactory loss in relation
to sex may also be a factor in the shorter duration of olfactory loss in women
than in men. That is, women seem to find olfactory problems more disturbing
and thus may seek counseling sooner than men.
In terms of self-reported changes of quality of life, 42% of our population
indicated a decrease in QoL of more than 10%. In comparison, it has been reported
that 82% of subjects with hearing loss indicated a decreased QoL20;
24% of patients with hearing loss were reported to be depressed.21
In this context it should also be mentioned that our population is certainly
nonrepresentative of all people with olfactory loss. Most of our patients
report a high olfactory sensitivity prior to loss of olfactory function. Thus,
it may well be that patients with a lower degree of olfactory acuity prior
to loss may not even seek counseling.
DECREASE OF QoL DOES NOT CHANGE WITH DURATION OF OLFACTORY LOSS
Duration of olfactory loss did not seem to affect self-rated changes
in QoL. This result emphasizes the significance of smells for everyday life;
it also indicates that various coping strategies may be insufficient to deal
with this loss of olfactory-mediated sensations.22
COMPLAINT SCORES SEEM TO BE HIGHER IN HYPOSMIA THAN IN ANOSMIA
In the present study, hyposmic patients had higher complaint scores
than anosmic patients. What would explain this anomalous finding? One explanation
may relate to the reinforcing character of the occasional perception of odors
in hyposmia. It may serve as a constant reminder of the olfactory loss, like
an echo from an olfactory world that, although present, cannot be perceived.
Similar findings were reported elsewhere with regard to behavior of patients
with anosmia and hyposmia in an odor identification test.23
When looking at the effort different groups of patients took to release an
odor in a "scratch and sniff test," researchers found that hyposmic patients
scratch much harder than healthy controls. In contrast, anosmic patients seem
to be frustrated after only a few trials and scratch significantly less than
hyposmic patients. Other explanations may relate to the questionnaire itself;
ie, the outcome might have been different if questions were put differently.
This will be subject to further research.
SELF-RATED DEPRESSION SEEMINGLY DOES NOT RELATE TO MEASURED OLFACTORY
FUNCTION
Patients reporting to be depressed had higher complaint scores and higher
self-reported loss of QoL, but did not differ in terms of their TDI scores.
Here, it seems possible that the difference between olfactory sensitivity
prior to and after the loss of olfactory function might be the decisive factor
in this correlation. In other words, the relative loss of olfactory function
may relate to the development of a depressive state.24-25
Lifetime prevalence for any psychiatric morbidity ranges from 21% to
65%, and depression is among the most common. It has been reported that 28%
of patients with olfactory dysfunction have a feeling of vulnerability because
they have difficulties detecting spoiled foods, smoke, gas, or body odors.22 As many as 26% of patients with olfactory dysfunction
even reported disruption of their marital, sexual, and social relationships
in relation to their olfactory loss.20 In addition,
in a study using the Beck Depression Inventory and the revised symptom checklist
90, at least 17% of patients with olfactory loss suffered from moderate depression.22
OLFACTORY LOSS SEEMS TO PRODUCE FEW WORK-RELATED PROBLEMS
A relatively small number of patients indicated that problems of olfaction
interfered with their occupations. This might be because (1) older patients
were usually retired, and (2) our population did not include many patients
professionally involved in the analysis of odors (eg, the food or chemical
industries). On the other hand, one would like to think that, for example,
electricians would need to know when and where cables burn or car mechanics
would need to know whether this clear liquid was water or gasoline.22 While the present observations may be used as an
argument in the discussion regarding the relatively small financial compensation
of olfactory loss in legal cases, one must not forget specific professions
that strongly rely on an intact sense of smell (eg, perfumers or chefs).
OLFACTORY LOSS SEEMS TO PRODUCE MOSTLY FOOD-RELATED PROBLEMS
Food preparation and intake was a major problem in our population. Flavor
is a complex interaction of smell, taste, pH, temperature, texture, and sensitivity
of the oral cavity. However, patients often associate flavor with the sense
of taste only. Most patients with olfactory loss experience the loss of flavor
as a loss of taste and thus confuse olfactory and gustatory abilities.6
Some authors provide evidence olfactory dysfunction does not lead to
nutritional problems.26 When interviewed about
food preferences, only 24% of anosmic patients reported unchanged preferences.27 Many anosmic patients also reported that they forget
about the need to eat. Others reported weight loss (7%); still others reported
weight gain (14%).28 This is consistent with
our own experiences with anosmic patients who complain of weight gain; that
is, after having lost the most sophisticated sense to enjoy foods, some patients
with anosmia simply eat more sweet dishes to reward themselves after an uninteresting
dinner.
Olfactory loss produces numerous complaints. It severely affects the
lives of patients who report to specialized centers. This clearly indicates
the need for an increased research effort in the treatment of olfactory loss.
AUTHOR INFORMATION
Accepted for publication November 16, 2001.
We thank Kati Rosenheim and S. Pabinger for their help in acquisition
of the data; Ebba Héden-Blomqvist, MD, for her thoughtful comments
on the manuscript; and Elisabeth Pauli, PhD, for her help with the statistical
analysis of this investigation.
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 Vienna, Austria
(Drs Temmel, Quint, and Schickinger-Fischer); Deutsche Klinik für Diagnostik,
Wiesbaden (Dr Klimek), and the Department of Otorhinolaryngology, University
of Dresden Medical School, Dresden (Ms Stoller and Dr Hummel), Germany.
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