International clinical assessment of smell: An international, cross‐sectional survey of current practice in the assessment of olfaction

Olfactory dysfunction (OD) is common and carries significant personal and societal burden. Accurate assessment is necessary for good clinical and research practice but is highly dependent on the assessment technique used. Current practice with regards to UK/international clinical assessment is unknown. We aimed to capture current clinical practice, with reference to contemporaneously available guidelines. We further aimed to compare UK to international practice.

Olfactory dysfunction (OD) affects $22% of the general adult population 1,2 -a figure likely set to increase due to the long-term chemosensory effects of COVID-19.4][5] Accordingly, olfaction and its disorders are the justified focus of clinical and research interest.
Appropriate assessment of olfaction is paramount for good clinical and research practice-enabling accurate diagnosis, therapeutic decision making and outcomes assessment.However, the current state of UK and international practice with regards to clinical assessment is unknown, with the last available UK data from 2009. 6][9][10] In particular, these guidelines recommend use of psychophysical testing, given evidence that subjective assessment correlates poorly with more objective chemosensory tests. 11Again, however, adherence to such guidelines is unknown.Furthermore, there have been no prior attempts to characterise geographical variations in practice.

| Objectives
We therefore performed the International Clinical Assessment of Smell (ICAS) Survey-the first comprehensive cross-sectional survey of UK and international clinical practice amongst ENT surgeons in the assessment of OD, with particular interest in psychophysical smell testing, and with reference to the only available international guidelines at time of survey-the Position Paper on Olfactory Dysfunction (PPOD).Finally, as we were particularly interested in practice variation between UK and international clinicians, we aimed to compare these geographical cohorts.

| Survey design/setting/participants
An anonymous online questionnaire was created targeting ENT surgeons who assess olfaction.The questionnaire was developed with the aid of a UK-based panel of four consultant rhinologists with special interest in olfaction, three consultant rhinologists/general ENT surgeons and a non-ENT surgeon (included for technical review).The inclusion of clinicians with varying interest in olfaction during development and piloting allowed better approximation of respondents within the target population. 12Item generation was performed in two steps: 1: guideline/supporting literature review and identification of assessment domains of interest; 2: simultaneous item generation/reduction. Step 2, as well as survey piloting, was performed during three iterative rounds of panel review.
Three main assessment domains were identified: A-psychophysical assessment (and barriers thereof); B-subjective assessment (patient reported outcome measures, 'PROMS'); C-imaging (MRI/other).Questions referred to routine practice-except for a separate stem on the effects of the pandemic-and were carefully worded to be clear, unambiguous and unbiased. 13During piloting, several topics were deemed highly specialist, so made optional (skippable using branching logic).
Copies of the PPOD 7 and BRS Consensus Guidelines on Management of New Onset Anosmia in the COVID Pandemic 14 were offered to respondents as incentives to complete the survey.
Following development, the survey was approved for distribution by the ENT-UK survey guardian and distributed electronically between May and June 2021 (cross-sectional non-probability sampling 12 ).
Reminder rounds were sent but read-receipts were not available.
Prior to international distribution, the survey underwent further review and piloting amongst an international panel of 10 further experts in olfaction, comprising members of the Clinical Olfactory Working Group (COWoG).Minor changes were made for international audiences (e.g., insurance) if needed, but no changes were made to existing questions that would prevent UK/international comparison.The survey was written in English.Distribution was facilitated by local panel members with circulation via professional society mailing lists where possible.International distribution took place between September 2021 and January 2022.
See Data S1 for further development details and full questionnaires.

| Ethical considerations
As a service evaluation/audit, this was not classified as research according to NHS HRA guidance.Audit registration for national/international distribution was approved by the Royal National ENT & Eastman Dental Hospitals (part of University College London Hospitals NHS Foundation Trust).Where required, further local permissions were obtained by distributing COWoG members.As all data were anonymous and 'non-sensitive', there were no data protection issues of note.Identical copies of the survey were provided in 'Microsoft Forms' (GDPR compliant)/'Google Forms'/'Survey Monkey' (ENT-UK), as required.

| Statistical analysis/reporting
Results are reported in line with the CROSS guidelines.As this was a service evaluation with no minimum significant difference available for the main outcome measures, a power calculation was not performed, and an a priori sample size was not set.
Quantitative data were analysed using GraphPad Prism.Data were assessed for normality and parametric/nonparametric tests used.If response rates to individual questions were lower than total respondents (due to dropout/branching logic), this is stated.Missing data were excluded from statistical analysis.Proportions are given for total respondent number or total response number, where answers were non-mutually exclusive.
For qualitative data analysis methods, please see Data S1.Subgroup analysis was performed for 'UK' and 'international' responses-comparison between cohorts was performed for the main assessment domains.

Key points
• The accuracy of olfactory assessment is dependent on the technique used.Current guidelines make recommendations on how to assess olfaction, including the use of psychophysical smell tests to improve accuracy.
• Current clinical practice in the assessment of olfactory dysfunction (OD) is unknown.Furthermore, geographical comparison of practice has not previously been performed.
• We performed an anonymous online survey of clinical practice in the assessment of OD, with reference to contemporaneously available guidelines, and with particular focus on psychophysical testing.
• Responses were obtained from 465 clinicians across 17 counties, with the largest cohort in the UK (217).Psychophysical testing and patient reported outcome measures were infrequently used-the former less so in the UK than internationally.Use of diagnostic MRI was, however, more common in the UK.
• We present recommendations to improve clinical practice in the assessment of olfaction and OD, including but not limited to increased education and funding for psychophysical testing.

| Sample population
Results were obtained from 465 respondents, of whom 217 were from the UK.The geographical distribution of remaining 'international' respondents (17 countries in total) is shown in Figure 1 Country-specific response rate varied from 1.4% to 72.5%, with lower rates being obtained where distribution was to mailing lists including multiple specialties/subspecialties (Table 1).As distribution method, response rates and proportion of 'rhinologists' varied geographically, direct country comparison was not performed, due to probable differences in selection bias.Instead, subgroup analysis T A B L E 1 Response rates and distribution methods.T A B L E 2 UK and international results for psychophysical assessment, imaging, and subjective assessment.

| Psychophysical testing
Within the UK, across all respondents, and within the rhinologist and non-rhinologist subgroups, the largest proportion of clinicians 'never' performed psychophysical testing in any of the clinical scenarios presented (covering diagnostics, outcomes and complications).Comparing rhinologist to non-rhinologist subgroups, a statistically significantly higher proportion of rhinologists 'always' or 'most of the time' performed testing during the initial assessment of OD as a presenting/ isolated symptom, before/after surgical intervention, and before/after surgical intervention that could cause OD as a complication (for full results and statistics-see Table 2).
For international respondents, there was greater variation in practice across assessment scenarios, and greater proportions of clinicians performing psychophysical testing, particularly within the rhinologist subgroup.When comparing rhinologist to non-rhinologist subgroups, statistically significantly higher proportions of rhinologists 'always', 'most of the time' or 'sometimes' performed psychophysical testing across all of the clinical scenarios presented (Table 2).
Comparing UK and international responses, in both rhinologist/ non-rhinologist subgroups, where statistically significant differences in proportions of testing were found, it was more frequently performed internationally (Table 2).Figure 2 compares UK/international psychophysical test use during the initial assessment of OD. Figure 3 shows country-specific diagnostic practice in rhinologist/nonrhinologist subgroups.
In both the UK and internationally, the most common type of test used was odour identification, followed by discrimination and threshold (UK-27.3%,12.9% and 6.7% of responses, respectively; international-38.4%,21.6% and 21.4%, respectively).The most common specific type of test was the 'Smell Identification Test' in the UK, the 'Sniffin' Sticks' internationally.
Barriers to routine psychophysical testing, as well as maximum acceptable duration of smell testing are shown in Figure 4.
Approximately one in five of both UK and international respondents had no knowledge/experience of psychophysical smell tests (21.8% and 18.6%, respectively).Across both cohorts, the most frequent source of knowledge was clinical experience, followed by selfdirected study, post-graduate training, courses, medical school and 'other'.Most respondents (UK-77.6%and international-63.3%) said they would like to receive training in use of psychophysical tests.

| Imaging
The highest proportions of UK respondents, overall and within rhinol- Note: Where individual question response rates were less than the total, this was due to either branching logic or dropout.Test statistic (parametric or non-parametric as appropriate) and associated p value given for statistically significant results (where p < .05).Statistical significance tested between groups as per headings (UK rhinologists vs. non-rhinologists; international rhinologists vs. non-rhinologists; UK vs. international rhinologists; UK vs. international non-rhinologists).Note-percentages shown rounded to one decimal place.Abbreviation: ns, non-statistically significant.
'sometimes' scanned, followed by 'most of the time'.There was no significant difference in frequencies of scanning between rhinologist or non-rhinologist subgroups (UK/internationally). Comparing UK and international practice, in both rhinologist/non-rhinologist subgroups, a significantly higher proportion of UK respondents 'always' scanned.
In both the UK/internationally, the most frequent aim of performing MRI scanning was to 'exclude neoplasm', followed by 'exclude non-neoplastic structural abnormality upstream of the OB' and 'assess OB (grosspresent/absent)'.More international respondents performed volumetric assessment than in the UK (16.4% vs. 8.4% of total responses, respectively).CT of the paranasal sinuses was the most frequent 'other' scan.

| PROMs
Across all clinicians, rhinologist and non-rhinologist subgroups, the highest proportion of respondents 'never' used PROMs during their initial assessment of OD, both in the UK and internationally (Table 2).
However, practice varied between rhinologist/non-rhinologists, with the latter group using PROMS more frequently.In both the UK and internationally, the 'SNOT-22' questionnaire was the most frequently used PROM.

| Further questions
Please see Data S1 for full results.

| DISCUSSION
To our knowledge, this is the first detailed international survey of clinical practice in the assessment of olfaction.Responses were received from 465 clinicians, with the largest cohort originating from the UK, and country-specific response rate ranging from 1.4% to 72.5%.
Assessment of OD can be performed using approaches ranging from subjective report to functional neuroimaging and electrophysiology.Subjective report can be captured through clinical history, anchored scales/questions, or more formally using validated PROMs.
These methods are important for understanding patient experience and calculating the minimal clinically important difference.6][17][18]  Interestingly, despite poor rates of psychophysical testing, PROMs were not used consistently in the UK.
Whilst comparisons between UK and international cohorts should be interpreted with care (see limitations section), in general, there were higher levels of psychophysical testing amongst international respondents, across all clinical scenarios.The most common barrier to routine psychophysical testing amongst international clinicians was 'insufficient time', though other issues surrounding service provision (including insufficient staff/hospital-related funding) were also common.Despite this, international respondents were more tolerant towards longer smell tests, with most choosing 5-15 min as maximum acceptable testing time.As in the UK, PROMs were not consistently used-though they were more so in the rhinologist subgroup.
Interestingly, in both the UK and international cohorts, 'refer on to specialist clinic' was an infrequent reason for not performing routine psychophysical testing.Furthermore, in both cohorts, $3/4 of respondents said they would like to receive further training in psychophysical testing.
Regarding imaging, a large proportion of UK-respondents 'always' performed MRI scanning of the brain/olfactory tract during the initial assessment of OD (31.3% of all respondents, 36.4% of rhinologists).
Compared with the UK, international respondents performed MRI scanning less frequently and with more variability-with 'sometimes' being the most frequently chosen response.MRI can be used to provide diagnostic (through identification of structural abnormalities, e.g., neoplasia or OB hypoÀ/aplasia) and/or prognostic information (through volumetric assessment of the OB or other structures).Whilst lack of hypothetical-aetiology information and relative subjectivity of the Likert-frequency terms used (particularly 'most of the time'/'sometimes'/'rarely') limits interpretation of our data, it is likely that the cohort of clinicians who 'always' scan contains two subgroups-those who perform MRI scanning to obtain prognostic information, and those who scan for more indiscriminate diagnostic purposes (supported by 'exclusion of neoplasm' being the most frequently chosen aim of scanning overall).In the latter subgroup, a more tailored approach could be encouraged through increased psychophysical testing, education and more comprehensive imaging guidelines. 7,19Such an approach could enable more cost-effective healthcare and limit patient burden, including associated indirect healthcare costs.At the Various other results of interest can be found in the main and Data S1 results section.

| Comparisons with other studies
To our knowledge, the only available UK data on the assessment of OD was published in 2007 and 2009. 6,20In these studies, 54.8% and 63% of respondents did not perform psychophysical testing for F I G U R E 4 UK and international barriers to routine psychophysical testing (bar chart, top -note N = total nonmutually exclusive responses) and maximum acceptable testing time (donut chart, bottom: for the assessment of (A) OD as a presenting/isolated symptom, (B) OD in association with another presenting symptom, (C) during the perioperative assessment of olfaction for a surgical intervention that could cause OD as a complication).Note-percentages shown rounded to one decimal place.

F
I G U R E 2 UK and international smell testing during initial assessment of olfactory dysfunction (OD).(i): Percent stacked column charts showing distribution of testing frequencies in the UK, all (excluding UK) and all (including UK) in rhinologist and non-rhinologist subgroups, for OD as a presenting/isolated symptom (A/C) or OD in association with another presenting symptom (B/D).(ii): Bar charts comparing distribution of testing frequencies between UK and all (excluding UK), for OD as a presenting/isolated symptom (A/C) or OD in association with another presenting symptom (B/D).Asterisks indicate statistically significant results-* p < .05,** p < .01,*** p < .001,**** p < .0001.Note-percentages shown rounded to one decimal place.F I G U R E 3 UK and international smell testing during initial assessment of olfactory dysfunction (OD).Percent stacked column charts showing distribution of testing frequencies in all countries with total respondents n ≥ 10 (from left to right in order of descending total (rhinologist + nonrhinologist) participant number), in rhinologist and non-rhinologist subgroups, for OD as a presenting/isolated symptom (A/C) or OD in association with another presenting symptom (B/D).Note-percentages shown rounded to one decimal place.time of survey, no imaging guidelines were available; however, the 2023 update to the PPOD now provides expert-agreed recommendations on scanning practice for different suspected aetiologies of OD.10 Future work should aim to interrogate imaging practice in more detail, through prospective auditing of aetiology-specific scanning and subsequent diagnostic/prognostic outcome yield.Ultimately, the establishment of evidence-based imaging practice amongst all clinicians is needed to ensure that patients receive access to appropriate investigations as standard. .
71ychophysical smell tests involve presentation of odour stimuli, with score based on the subject's perceptual response.They include the well-validated Smell Identification Test (also known as the 'SIT-40' or previously as the 'University of Pennsylvania Smell Identification Test'), which tests odour identification, and 'Sniffin' Sticks', which tests odour identification, discrimination and threshold.Such tests are reliable and accurate, and arguably represent the gold standard of clinical assessment.11Therefore, in the first (PPOD7), and subsequent sets of international guidelines, 8,9 a key recommendation is that subjective report should not be performed in isolation, but rather combined with psychophysical smell testing.This mirrors the standard of care that is expected during the assessment of hearing or