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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 62:1287-1293 (2007)
© 2007 The Gerontological Society of America

Good News for Elderly Persons: Olfactory Pleasure Increases at Later Stages of the Life Span

Katrin Markovic, Udo Reulbach, Agapi Vassiliadu, Jens Lunkenheimer, Birgit Lunkenheimer, Rita Spannenberger and Norbert Thuerauf

Department of Psychiatry and Psychotherapy, University of Erlangen-Nuremberg, Germany.

Address correspondence to Katrin Markovic, MD, Arbeitsgruppe/Laborbereich Sensorik, Psychiatrische und Psychotherapeutische Klinik, Universität Erlangen-Nuernberg, Schwabachanlage 6, 91054 Erlangen, Germany. E-mail: katrin.markovic{at}psych.imed.uni-erlangen.de


   Abstract
Top
 Abstract
Material and Methods
 Results
 Discussion
 References
 
Background. Numerous studies have been conducted collecting normative values dependent on age for the three major components of the Sniffin' Stick Test (threshold of n-butanol, and identification and discrimination of odors). Less is known about the influence of age on the hedonic and intensity evaluation of odors. Thus, the objective of this study was to analyze the influence of age on the hedonic and intensity estimates in a large human population.

Methods. Two hundred one single data sets established the Hedonic Database of Smell-Franconia (HeDoS-F) with the parameters age, gender, odor threshold, odor discrimination, oder identification, intensity estimates, and hedonic estimates (median age: 39 years, interquartile range: 28, minimum age: 19, maximum age: 83, men: 103, women: 98). For olfactory testing the Sniffin' Stick Test was used, and hedonic and intensity estimates were registered using visual analogue rating scales. For statistical analysis, we separated the study population into three age groups (19–39 years, 40–59 years, and ≥ 60 years), and parametric and nonparametric tests were calculated.

Results. We found a significant influence of age on threshold, discrimination, and identification with a decrease in the higher age class. Over all odors the summed intensity estimates did not depend on age, whereas the summed relative hedonic estimates increased with the beginning of the fifth decade.

Conclusion. Our study suggests that, for perceived odors, olfactory pleasure increases at later stages of the life span, whereas the perceived intensity of odors remains stable.

Olfactory sensitivity changes with age, and numerous studies have been conducted collecting normative values dependent on age for the three major components of the Sniffin' Stick Test (threshold of n-butanol, and identification and discrimination of odors). Especially for the elderly population, a significant loss of olfactory function could be demonstrated. Several studies using the Sniffin' Stick Test or the UPSIT (University of Pennsylvania Smell Identification Test) demonstrated that olfactory testing is also suited to improve the diagnosis of neurodegenerative diseases like idiopathic Parkinson's disease or Alzheimer's disease even at very early stages (1–5). Olfactory disturbances were also reported for multiple sclerosis (6,7). Despite the widespread application of olfactory testing in health and disease, little is known about the intensity and hedonic evaluation (evaluation as pleasant or unpleasant) of odors. The observation that intensity and hedonic evaluation are poorly investigated in health and disease is even more surprising because reduced intensity and altered hedonic perception are regarded as severe impairments of lifestyle and quality of life. The impact of olfactory sensitivity and of the hedonic evaluation of odors on eating enjoyment and on food consumption revealed controversial results. On the one hand, about 70% of patients with chemosensory loss reported decreased eating enjoyment and about 60% reported dietary alterations (8). On the other hand, it has been surprisingly difficult to document a loss of eating enjoyment in healthy elderly people despite the known decline in olfactory sensitivity at higher ages (9). In the elderly population, Schiffman and Warwick (10) reported an increased liking and intake of foods with enhanced flavors (e.g., carrots with added carrot flavor) (10). This behavior can be explained by an increase of pleasantness for specific flavors but also by compensating a decreased olfactory sensitivity for the flavors. Besides physiological changes of odor sensitivity and perception during the life span, it is well known that prefrontal brain damage often significantly impacts hedonic tone (11,12). Taken together, all these findings show that the hedonic evaluation of odors in health and disease is worth being investigated.

In order to understand hedonic perception, it is helpful to emphasize the relationship of olfactory hedonic evaluation to emotion. Emotional and olfactory processing seem to be closely linked (13), and involuntary categorization of odors by their hedonic perceptions is a likely and an early process during odor perception (14). This view is in line with the theory of emotion proposed by Zajonc (15) that affective evaluations of environmental stimuli happen quickly and are more primitive than are cognitive evaluations. Zajonc's theory challenged the earlier theory of Lazarus (16), who suggested that the primitive evaluation of a stimulus is, first of all, cognitive. In accordance with the view of Zajonc, Dijksterhuis and colleagues (17) concluded that the hedonic processing of odor stimuli is an emotional, rather than an analytical, task.

Bridging the gap between the established standard parameters of smell tests and higher cortical aspects of smell, we extended the Sniffin' Stick Test with regard to standardized registrations of intensity and hedonic estimates. Our study of a large human population aimed at investigating (i) the effect of age on the emotional categorization of pleasant, neutral, and aversive standard odors and (ii) the time course of olfactory intensity perception over the life span in comparison with the time course of olfactory sensitivity.

We also intended to create a helpful tool for olfactory hedonic and intensity evaluation in health and disease by establishing intensity and hedonic estimates as further components of the Sniffin' Stick Test. We used visual analogue rating scales, as frequently described in psychophysical studies of smell (18–22), to register hedonic and intensity estimates. In contrast to categorical testing instruments as, e.g., the questionnaire by Dravnieks and colleagues (23), visual analogue rating scales allow for the quantification of single items as requested in our study (24,25).


   MATERIAL AND METHODS
Top
 Abstract
 Material and Methods
Results
 Discussion
 References
 
Participants
Two hundred one healthy individuals participated in our sensory measurements establishing the Hedonic Database of Smell-Franconia (HeDoS-F) release 1.0. The database provided 201 single data sets with the parameters age, gender, odor threshold, odor discrimination, odor identification, intensity estimates, and hedonic estimates (median age: 39 years, interquartile range: 28, minimum age: 19 years, maximum age: 83 years, men: 103, women: 98). The sensory measurements consisted of the Sniffin' Stick Test (26) extended by the assessment of intensity and hedonic estimates. All experimental procedures were clearly explained, and participants provided written informed consent prior to the testing sessions. Participants were free to interrupt the testing sessions at any time. The study was performed in accordance with the Declaration of Helsinki of 1975 and was approved by the Ethics Committee of the University of Erlangen-Nuremberg.

Olfactory Testing
Odor thresholds for n-butanol were assessed using a single-staircase, triple-forced choice algorithm. Sixteen dilutions were prepared in a geometric series starting from a 4% n-butanol solution (dilution ratio 1:2 in deionized aqua conservata as diluent). Three pens ("triplets") were presented in a randomized order, with two containing the solvent and the third the odorant at a certain dilution. The participants' task was to identify the pen containing the odorant. Triplets were presented at intervals of 20 seconds. Reversal of the staircase was triggered when the odor was correctly identified in two successive trials. Thresholds were defined as means of the last four of seven staircase reversal points. The participants' scores ranged between 0 and 16.

In the odor-discrimination task, triplets were presented in a randomized order, with two containing the same odorant and the third a different odorant. Participants had to determine which of the three pens smelled different. The triplets were presented every 20–30 seconds. The interval between the presentations of the individual pens of a triplet was approximately 3 seconds. As a total of 16 triplets were tested, the participants' scores ranged from 0 to 16. When measuring odor thresholds and odor discrimination, participants were blindfolded to prevent visual identification of some of the odorant-containing pens.

Odor identification was assessed by means of 16 common odors (orange, shoe leather, cinnamon, peppermint, banana, lemon, licorice, turpentine, garlic, coffee, apple, clove, pineapple, rose, anise, and fish). Using a multiple choice task, participants identified individual odorants from a list of four descriptors. The interval between odor presentations was 20–30 seconds. Again, the participants' scores ranged from 0 to 16. We registered the hedonic and intensity estimates following the presentation of each single odor by means of a visual analogue rating scale presented on paper. The relative scaling for ‘unpleasantness/pleasantness’ was –100 to +100 and for ‘very low intensity/very high intensity’ 0 to +200 visual analogue rating units (VARU) were represented by a physical length of 200 mm on each scale. Participants marked the perceived intensity and the hedonic perception with a pencil on the scales presented. We converted and digitized the registered estimates offline to VARUs for the subsequent statistical analysis described below.

Statistical Methods
The data set HeDoS-F release 1.0 was used for statistical analysis. In order to exclude uneven gender distributions of the data set, we tested for differences in the age of women and men (Mann–Whitney U test) and for differences in gender distribution within the applied three age groups mentioned below (chi-square test).

For the subsequent data analysis we concentrated on age differences and calculated the statistical analysis over the intensity and hedonic estimates in order to determine the significant influence of age on both parameters. Participants were separated into three age groups (19–39, 40–59, or ≥ 60 years). Using the method of Kolmogorov–Smirnov, we tested for normal distribution of the data. Based on the results of this test, parametric (analysis of variance; ANOVA) or nonparametric (Kruskal–Wallis test) analyses were calculated subsequently. All statistical tests were two-sided. The significance level was set at {alpha} = 0.05. All calculations were performed by using the statistical software package SPSS for Windows 12 (SPSS Inc., Chicago, IL). In threshold, odor discrimination, and identification, the Kruskal–Wallis test was used for all data for the analysis of the three components of the Sniffin' Stick Test.

Intensity estimates.-- Intensity estimates were analyzed as positive values of a monopolar analogue rating scale (absolute values, range: 0–200 VARU). An ANOVA was calculated for the summed intensity estimates of all odors. For the analysis of the intensity estimates of each single odor, the Kruskal–Wallis test was used.

Hedonic estimates.-- Hedonic estimates were analyzed in two different ways: (i) as negative/positive values of a bipolar analogue rating scale (relative values, range: –100 to +100 VARU; the negative scale/value indicates unpleasantness and the positive scale/value indicates pleasantness) and (ii) as positive values representing the distance from 0 on the bipolar rating scale (absolute values/magnitude of estimates, range: 0–100 VARU). An ANOVA was calculated for all summed relative and absolute hedonic estimates of all odors and for the relative hedonic estimates of each single odor except the hedonic estimates of the "fish" odor. For the relative hedonic estimates of that odor and for all absolute hedonic estimates of each single odor, nonparametric analyses (Kruskal–Wallis test) were performed.


   RESULTS
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 Abstract
 Material and Methods
 Results
Discussion
 References
 
Consistency of Data
The age of female (median: 41.5 years; interquartile range: 29.25 years) and male (median: 36 years; interquartile range: 25 years) participants did not differ significantly (Mann–Whitney U; z = –1.13, p =.26). Moreover, the sex distribution within the three age groups was not significantly different (chi-square test; {chi}2 = 4.3, df = 2, p =.12).

We found a significant influence of age on threshold (Kruskal–Wallis, {chi}2 = 11.1, p =.004), discrimination ({chi}2 = 8.7, p =.013), and identification ({chi}2 = 31.8, p <.001) with a decrease in the higher age groups (Figure 1).


Figure 01
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  		Figure 1. Means and standard errors of the mean of the standard parameters of the Sniffin' Stick Test (threshold for n-butanol, discrimination, and identification). A (black column): 19–39 years (n = 102), B (gray column): 40–59 years (n = 66), C (white column): ≥60 years (n = 33)

 
Intensity Estimates
No association between the summed intensity estimates of all odors and age could be observed (ANOVA; F = 2.3, p = 0.10) (Figure 2). In contrast, the intensity estimates of the single odors "lemon" (Kruskal–Wallis; {chi}2 = 13.5, p =.001), "garlic" ({chi}2 = 15.2, p =.001), and "fish" ({chi}2 = 11.8, p =.003) were significantly associated with age (Figure 3).


Figure 02
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  		Figure 2. Means and standard errors of the mean of the summed intensity estimates over all odors and the summed relative hedonic estimates over all odors. A (black column): 19–39 years (n = 102), B (gray column): 40–59 years (n = 66), C (white column): ≥60 years (n = 33). VARU = visual analogue rating unit

 

Figure 03
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  		Figure 3. Means and standard errors of the mean of the intensity estimates of the single odors "lemon," "garlic," and "fish," A (black column): 19–39 years (n = 102), B (gray column): 40–59 years (n = 66), C (white column): ≥60 years (n = 33). VARU = visual analogue rating unit

 
Hedonic Estimates
The summed relative hedonic estimates of all odors were significantly associated with age (ANOVA; F = 8.2, p <.001) (Figure 2). Significant age differences of the relative hedonic estimates could be observed for the single odors "turpentine" (ANOVA; F = 3.7, p =.027), "garlic" (F = 6.1, p =.003), "clove" (F = 11.6, p <.001), "rose" (F = 6.6, p =.002), and "fish" (Kruskal–Wallis; {chi}2 = 25.1, p <.001) (Figure 4).


Figure 04
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  		Figure 4. Means and standard errors of mean of the relative hedonic estimates of the single odors "garlic," "turpentine," "fish," "clove," and "rose." A (black column): 19–39 years (n = 102), B (gray column): 40–59 years (n = 66), C (white column): ≥60 years (n = 33). VARU = visual analogue rating unit

 
Regarding the absolute values for hedonic estimates, we found no significant age-dependence for the summed absolute hedonic estimates of all odors (ANOVA; F = 0.4, p =.70, data not shown), whereas the hedonic estimates of the single odors "lemon" (Kruskal–Wallis; {chi}2 = 8.2, p =.017), "garlic" ({chi}2 = 11.1, p =.004) and "fish" ({chi}2 = 18.5, p <.001) were significantly different between the three age groups (Figure 5).


Figure 05
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  		Figure 5. Means and standard errors of mean of the absolute hedonic estimates of the single odors "lemon," "garlic," and "fish." A (black column): 19–39 years (n = 102), B (gray column): 40–59 years (n = 66), C (white column): ≥60 years (n = 33). VARU = visual analogue rating unit

 

   DISCUSSION
Top
 Abstract
 Material and Methods
 Results
 Discussion
References
 
A variety of publications in recent decades report that an age-dependent decrease in olfactory sensitivity and severe olfactory deficits like hyposmia or anosmia significantly increase at a higher age (18,27–30). Despite these deficits, our study demonstrates for the first time, to our knowledge, an increase in an olfactory ability—the ability to perceive olfactory pleasure—at an older age. Our consistent results suggest a general central mechanism shifting the olfactory hedonic estimates of elderly persons to a more pleasant range.

Further analyses of our study population revealed a significant increase in odor thresholds and a significant decrease in discrimination and identification ability in the higher age classes. This finding is in accordance with those from numerous previous studies as mentioned above. We successfully extended the Sniffin' Stick Test by registering olfactory intensity and hedonic estimates using standardized bipolar analogue ratings scales. Our study of a large human popluation of 201 participants (data sets) revealed that the overall hedonic estimate for the sum of all odors was 12.0 ± 17.0 VARU (unpleasantness/pleasantness scale: range = –100 to +100), indicating that the test is relatively balanced for pleasant and unpleasant odors. Generally, our data characterized the extended Sniffin' Stick Test as a helpful tool suited to investigate olfactory hedonic and intensity evaluation. However, a prerequisite for the hedonic and intensity test is the clear perception of the standard odors, i.e., the presentation of the odors at suprathreshold concentrations. Thus, participants with relevant smell deficits or anosmia—just being more frequent at a higher age—could not be included in our study. This exclusion of older participants because of more frequent smell deficits or anosmia also implies that very elderly persons are less (> 80 years) or not at all (> 83 years) represented in this study. Our measurements represent the first assessment of hedonic and intensity estimates using the extended Sniffin' Stick Test. The comparability with other studies could be limited by other standard odors selected for the testing batteries and/or by differences in odor presentation.

Our study revealed that the intensity evaluation of odors was more stable for the life span investigated than were olfactory detection, discrimination, and identification. We interpret this finding that intensity evaluation is a simpler and independent task whereas odor identification is related to semantic memory, and odor detection and discrimination depend on attention. For a small subgroup of single odors (3 of 16 odors: lemon, garlic, fish), we found a significant decline of perceived intensity with age, demonstrating that the time course of intensity estimates is not uniform for all odors. Some investigators found age-related differences in the ratings of the intensity of suprathreshold odors as well, with elderly participants perceiving odors to be less intense (31–34). Other researchers reported smaller (or no) age differences in suprathreshold measures than in threshold measures (35). Our results mentioned above show that an influence of age on the perception of intensity may also depend on the selection of single odors. This observation can also explain some of the controversy about the effect of age on the perception of olfactory intensity.

The hedonic evaluation of odors by analogue rating scales provides information about the span of estimates (absolute values) and the polarity (pleasantness/unpleasantness) of the hedonic evaluation (relative values). We found a statistically significant influence of age on the relative values of the overall hedonic estimates, whereas the absolute values of hedonic estimates and the intensity estimates were not age dependent for the life span investigated. At the level of single odors, we found a statistically significant influence of age on the relative hedonic estimates for 5 of 16 odors (clove, garlic, rose, turpentine, fish). For the time course of the hedonic estimates over all odors and for the five single odors a similar pattern over the life span arose with a significant higher olfactory pleasantness (or a significant lower unpleasentness) beginning with the fifth decade. Our data for the odorant "rose" are in accordance with reports on the National Geographic Smell Survey [for a review, see (26)]. Our data for "clove" demonstrate a switch of polarity from unpleasant to pleasant with age. This example receives special importance, because the hedonic categorization in olfaction is probably the most important criterion for odor grouping (36) and olfactory stimuli are experienced primarily in terms of their hedonic tone (37).

Changes of absolute hedonic values only reached statistical significance for the three single odors "lemon," "garlic," and "fish," with the highest spans for the youngest age group. This finding could indicate that the affective reactivity is most emphasized at a younger age. Olfactory neuroimaging research has revealed that the processing of olfactory information relies heavily on neuroanatomic structures within the limbic system, such as the amygdala, enthorinal cortex, and insula (38,39). In a similar vein, it has been proposed that emotionally highly reactive individuals show a higher activation within the limbic system (40,41).

Besides inborn and biological factors, cohort effects were discussed in order to explain age differences in the hedonic evaluation of odors. Wysocki and Pelchat (42) reported that the acceptance of the spicy, clove-like odor "eugenol" increased through the fourth decade and then began to decline. Decades ago, eugenol was used as an anesthetic during dental procedures. With increasing age, there may be a decreased acceptance to eugenol because associations between its odor and dental visits may intervene (42). Two studies in smokers and nonsmokers provided evidence of a relationship between the experience with the pharmacological action of S-(–)-nicotine and its hedonic rating (pleasantness/unpleasantness) (22,43). Smokers perceived the S-(–)-isomer as being more pleasant (or less unpleasant) than nonsmokers perceived it to be. The difference in hedonic estimates has been explained by a conditioning mechanism between the sensory stimulus and the pleasant pharmacological actions of S-(–)-nicotine. All these observations show that the hedonic evaluation of an odor also depends on learning mechanisms, for example, conditioning mechanisms, and thus on the personal odor environment.

Summarizing our results clearly demonstrated that the intensity evaluation over all odors is relatively stable over the life span investigated, whereas the hedonic evaluation of odors significantly shifts to higher olfactory pleasantness (or a significantly lower unpleasentness) beginning with the fifth decade. This shift of olfactory pleasantness at older age also implies that the valence (hedonic evaluation) of an odor represents a dynamic process varying over the entire life span. Our findings are relevant for the sensory life quality of the elderly population, but its importance goes far beyond that scope. Our study gives clear evidence of a general central mechanism regulating the perception of olfactory pleasure in an age-dependent manner. The increase in olfactory pleasure at a higher age can also be interpreted as a natural development during the evolution of man because it protects, e.g., against malnutrition during a period of reduced availability of food at a higher age.


   Acknowledgments
Top
 Abstract
 Material and Methods
 Results
 Discussion
 References
 
This research was supported by DFG (German Research Foundation) grant TH 500/3-1.

We thank Susanne Schroeder-Thuerauf (Melanchthon-Gymnasium Nuremberg) for helpful suggestions during the preparation of the manuscript.


   Footnotes
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 Abstract
 Material and Methods
 Results
 Discussion
 References
 
Decision Editor: Luigi Ferrucci, MD, PhD

Received September 12, 2006

Accepted March 15, 2007


   References
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 Abstract
 Material and Methods
 Results
 Discussion
 References
 

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