An investigation of retronasal testing of olfactory function in a Turkish population

Background

Recent research has shown that odorants travel to the olfactory receptors by 2 routes: sniffing brings odorants through the nostrils into the nasal cavity (orthonasal olfaction), and chewing and swallowing force odorants emitted by foods upward behind the palate and into the nasal cavity from the rear of the mouth (retronasal olfaction) [1–6]. Thus, the flavor of the food is perceived via the sense of the smell [7]. As a result, taste perception is known to mainly consist of the interaction of retronasal olfaction and gustatory stimuli [8].

Approximately 5% of the general population is anosmic, but about 15% have a reduced sense of smell [9–11]. A significant number of patients complain of a reduction in their sense of smell, so it becomes important to reveal the factors that can influence both orthonasal olfaction and retronasal olfaction. Despite this fact, retronasal smelling has thus far received significantly less attention than its orthonasal counterpart. There are numerous ways of assessing nasal chemosensory performance (e.g., the University of Pennsylvania Smell Identification Test, UPSIT [12], “Sniffin’ Sticks” [13,14], or measurements of event-related potentials [15]), which have been validated for various countries and populations. However, only 2 test kits – retronasal olfactory testing [16] and the Candy smell test [17] – have been developed and validated on patients in Germany for the simple assessment of retronasal olfactory testing that resembles everyday challenges to retronasal olfactory identification abilities.

The aim of this study was (1) to perform a preliminary study for validation of “retronasal olfactory testing” in the Turkish population to find the best way to evaluate smell and taste disorders in Turkey; (2) to determine if cultural differences make application of the test more difficult; and (3) to determine the flavors that participants had not yet tasted by using the survey method.

Material and Methods

STATISTICAL ANALYSIS:

Data analysis was performed using the Statistical Package for the Social Sciences (SPSS), version 21.0 (SPSS Inc., Chicago, IL). The normal distribution of considered variables was first evaluated using the Shapiro-Wilk test. Data are shown as mean ± standard deviation for continuous variables and the number of cases was used for categorical ones. Subjects were divided into 3 groups according to the Sniffin’ Sticks score (normosmia, hyposmia, and anosmia). In addition, to explore the retronasal olfactory sensitivity in relation to groups, age, gender, cigarette smoking, and alcohol consumption, data were submitted to variance of analysis using the general linear model with Bonferroni post hoc tests. Correlational analyses were calculated according to Pearson. The level of significance was set at 0.05.

Results

The study was carried out on 330 subjects, and the mean age of the participants was 26±7.3 years, ranging from 19 to 53 years. The participants were divided into 3 groups according to “Sniffin’ Sticks” scores: normosmia, hyposmia, and anosmia. There were no differences between the groups in terms of age, gender, and alcohol consumption. There were statistically significant differences in terms of cigarette smoking between the normosmia and anosmia groups.

Table 2 gives the summary of characteristics of each of the variables of interest by disease status. Significant differences in retronasal olfaction scores were detected among the anosmia, hyposmia, and normosmia groups with Bonferroni post hoc tests (p<0.002). There was a strong significant correlation between the TDI scores and retronasal olfactory test scores (p<0.001, r=0.82) (Figure 1). In addition, subtests of “Sniffin’ Sticks” (odor threshold, odor discrimination, and odor identification) had a significant correlation with retronasal olfactory testing (p<0.001, r=0.7; p<0.001, r=0.8; and p<0.001, r=0.78, respectively).

A significant effect of cigarette smoking on TDI and retronasal olfactory scores was found by the linear regression model, which was an inverse correlation between smoking with TDI and retronasal olfactory scores (p<0.001, r=0.25; p<0.001, r=0.27, respectively).

Retronasal olfactory testing allowed for discriminating between normosmic, hyposmic, and anosmic subjects. Specifically, there was almost no overlap between scores of anosmic (score of 11 at 95th percentile) and normosmic subjects (score of 14 at 5th percentile), whereas scores of hyposmic subjects exhibited overlap between both normosmic and anosmic subjects (Table 3).

In the normosmia group, some odorized powders or granules were consistently correctly identified while others less so (Table 4). Bread, strawberry, orange, onion, cocoa, paprika, coffee, and garlic were the odorized granules most reliably correctly identified, while smoked ham, ginger, curry, raspberry, and celery were most commonly mistaken. In the anosmia and hyposmia groups, as expected, a larger proportion of subjects wrongly identified odorants. Looking at the 2 groups together, smoked ham, ginger, celery, curry, and raspberry were the least well-recognized odorized granules from the 20 presented.

In addition, when the results of the “Sniffin’ Sticks” test were evaluated, it was found that turpentine, apple, leather, lemon, and liquorice were the most commonly mistaken odorants in the normosmia group. In the hyposmia and anosmia groups, as expected, a larger proportion of subjects wrongly identified odorants. Considering the 2 groups together, apple and turpentine were these least well-recognized odors from the 16 presented.

Considering the results of the survey, we found that at least half of our participants had no idea about the tastes of smoked ham, juniper, curry, ham, anise, and white wine (Figure 2).

Discussion

Retronasal olfactory testing is an important tool in the clinical assessment of taste and smell disorders. However, cultural differences make the use of odor or flavor identification tests more difficult in different countries, as was seen during validation studies of the “Sniffin’ Sticks” tests before, because it was strongly dependent on familiarity with these specific odors and flavors [20–22]. When applied to our population, the retronasal olfactory test appeared to perform well and there was a strong significant correlation between “Sniffin’ Sticks” olfactory test results and retronasal olfactory test results. However, when evaluating the descriptive statistics of the retronasal testing, we detected that the scores of hyposmic subjects exhibited overlap between both normosmic and anosmic subjects. Thus, we thought that retronasal olfactory test required some adaptations, especially in using different odorized powders or granules, to improve the performance of the test in differentiating between the patients with normosmia, hyposmia, and anosmia.

In our population, the odorized granules or powders most commonly mistaken by subjects with normal olfactory function were ginger (66%), smoked ham (53%), curry (41%), raspberry (38%), and celery (32%). For the subjects with anosmia and hyposmia, the most commonly mistaken odorized granules or powders were raspberry (98%), curry (81%), celery (80%), ginger (90%), smoked ham (73%), grapefruit, and mushroom (both 70%). A possible explanation for these results could be the similarity of distracters with the odorized powders or granules, as in the case of grapefruit (distracters are lemon, cherry, and grapes) and mushroom (distracters are bread, fish, and white wine).

Also, according to our survey, at least half of our population was unfamiliar with odorized powders or granules that are used in the retronasal olfactory testing, such as raspberry, curry, celery, ginger, and smoked ham. Ginger is widely used with honey because of ginger’s bitter taste, and that is why our population was not accustomed to its original taste. The participants confused its taste with paprika. Raspberry, curry, and celery are not used widely in any regions of Turkey. Raspberry was most often was confused with white grapes, curry with mustard, and celery with chives. In addition, smoked ham is not a product used in traditional Turkish kitchens. Most of the participants might have understood that it was a taste of meat, but the options offered in the test were not familiar, so they answered that they had no idea about the smoked ham item.

To overcome these problems, we propose a modification of the original list of flavors. According to Hummel et al., one of the criteria for the selection of odorants in healthy subjects was the >75% successful identification of individual odorants from a list of 4 descriptors [13]. In our study, we found that ginger, smoked ham, curry, raspberry, and celery were not sufficiently well-known in healthy Turkish subjects (Table 4). Therefore, we will use thyme, cumin, sausage, sesame, and banana, which are items frequently consumed in our society, in place of ginger, celery, smoked ham, curry, and raspberry, respectively (Table 5). Also, we propose a modification of the original list of distracters by excluding the unfamiliar ones to achieve more accurate results. We plan to evaluate the results of these modifications (Table 5) in the test in a further study testing retronasal olfactory function in both normal subjects and patients with an impaired sense of smell.

Our study has several limitations. One limitation is obviously the low number of female participants. It should be better to test both genders in a more representative numbers. Also, it would be better to show the test-re-test quality of the retronasal olfactory testing and the lack of test-re-test reliability is another limitation of the study. Thus, further studies with more participants and including both genders and all age groups are needed for presenting the retronasal olfactory function and flavor familiarity of the whole Turkish population.

Conclusions

These results provide the basis for routine clinical evaluation of patients with olfactory disorders using retronasal olfactory testing, which is a simple and easy-to-perform test of the retronasal olfaction in our sample of the Turkish population. Modifications of odorized powders or granules and distracters of the test, taking into account cultural differences, are likely to improve the performance of the test.