Acta Oto-Laryngologica. 2015; 135: 258–263
ORIGINAL ARTICLE
Simple assessment of olfaction in patients with chronic rhinosinusitis
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BYUNG GUK KIM, JEONG-HOON OH, HA NA CHOI & SO YOUNG PARK Department of Otorhinolaryngology-Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul, Korea
Abstract Conclusion: The brief-smell identification test (B-SIT) can substitute for the butanol threshold test (BTT) in screening of anosmia and postoperative assessment of olfactory outcomes in patients with chronic rhinosinusitis (CRS). A time-effective test battery composed of B-SIT and the visual analog scale (VAS) can be implemented for simple olfactory assessment in any otolaryngology clinic. Objectives: Anosmia is a distinct clinical entity requiring special attention. Unpredictable olfactory outcomes after surgery make preoperative assessment more important. We compared the results of the BTT, B-SIT, and VAS to investigate whether B-SIT or VAS can substitute for BTT in screening of anosmia and postoperative follow-up. Methods: We collected data on 68 CRS patients who had bilateral CRS and underwent endoscopic sinus surgery. Olfactory performance was graded using the BTT: normosmia, hyposmia, or anosmia. VAS and B-SIT were also performed. All tests were repeated 6 months after surgery. Postoperative improvement was defined by an increase of the BTT score ‡ 2. Results: The B-SIT and VAS scores of the anomics were significantly lower than those of the normosmics. B-SIT discriminated anosmia with high specificity. Within the improvement group, postoperative increase of B-SIT/VAS score showed significance. However, neither the B-SIT nor the VAS differentiated between no change and deterioration of olfaction.
Keywords: Anosmia, brief-smell identification test, butanol threshold test, endoscopic sinus surgery, visual analog scale
Introduction Decreased sense of smell is a frequent complaint of patients with chronic rhinosinusitis (CRS). Anosmia should be regarded as a distinct clinical entity requiring special attention in the evaluation of CRS patients because of the problems of safety and quality of life. Although olfactory impairment secondary to CRS has been known to be the most treatable form of the olfactory disorders, the outcomes after sinus surgery depend on the varied contribution from two pathophysiologic mechanisms: conductive impairment from the mechanical obstruction of the nasal passages and sensorineural impairment from the toxic inflammatory mediators causing neuronal damage in the olfactory mucosa [1]. After endoscopic sinus surgery (ESS), residual hyposmia remains in most of the patients despite olfactory improvement [2], and
olfaction deteriorates occasionally by the mechanisms related to the risks inherent in nasal surgery [3]. Therefore, the unpredictable olfactory outcomes make preoperative evaluation of the baseline olfactory function more important. Quantitative assessment of the olfactory function, which has relied on threshold determination or odor identification, has become increasingly common in clinical practice due to the development of various standardized olfactory tests [4]. The butanol threshold test (BTT) is one part of the Connecticut Chemosensory Clinical Research Center (CCCRC) test [5]. It has been widely used and is regarded as one of the most accurate methods that reflect the olfactory status [6]. However, the detailed threshold test requires a relatively long test time and trained personnel, while identification tests take less time and can be self-administered. The 12-item brief-smell
Correspondence: So Young Park MD PhD, Department of Otorhinolaryngology-Head and Neck Surgery, St Paul’s Hospital, College of Medicine, The Catholic University of Korea, Wangsan-ro 180, Dongdaemoon-gu, Seoul 130-709, Republic of Korea. Tel: +82 2 961 4526. E-mail: [email protected]
(Received 11 August 2014; accepted 28 September 2014) ISSN 0001-6489 print/ISSN 1651-2251 online 2015 Informa Healthcare DOI: 10.3109/00016489.2014.974288
Acta Otolaryngol Downloaded from informahealthcare.com by Kainan University on 04/09/15 For personal use only.
Olfactory testing in patients with chronic rhinosinusitis identification test (B-SIT), also known as the crosscultural smell identification test (CCSIT), is a validated scratch-and-sniff semiquantitative test at the suprathreshold level performed in less than 5 min [7,8]. One weakness of the B-SIT is poor differentiation between subclasses of dysfunction due to few stimuli [4]. The visual analog scale (VAS) provides a self-rating subjective measure of olfactory function. Nowadays, various olfactory tests are routinely performed in more and more rhinology clinics at the clinician’s convenience. The authors have employed an olfactory test battery composed of BTT, B-SIT, and VAS in the clinical setting of CRS. In the present study, the results of three tests were compared to investigate whether the B-SIT or VAS can substitute for BTT in screening of CRS-related anosmia and evaluation of postoperative outcomes in terms of olfaction. Material and methods Subjects Clinical data on bilateral CRS patients who underwent ESS between January 2007 and December 2011 were retrospectively collected with the approval of the Institutional Review Board of The Catholic University of Korea St Paul’s Hospital. All subjects had CRS with or without polyps and fulfilled the diagnostic criteria for adult CRS recommended by the American Academy of Otolaryngology-Head and Neck Surgery Foundation [9]. Patients who completed both preoperative and postoperative olfactory tests were included in this study. Those with the following conditions were excluded from the analysis: older than 65 years, asthma, previous nasal surgery, and other suspected causes of olfactory disorders such as head trauma or viral infection. Surgery (bilateral ESS) was performed by a single surgeon (the first author) after a failure of antibiotic treatment. None of the patients was given topical or systemic steroids preoperatively. Olfactory tests and grouping Olfactory thresholds were measured using 1-butanol sniff bottles as described by Cain et al. [5]. Our modification was the highest concentration. We started from 100% concentration (dilution step 0) and prepared successive dilutions by a factor of 1/ 3 up to step 11. Dilution step 3 equaled 4% aqueous concentration. Four consecutive correct choices marked the threshold, namely the BTT score. After threshold determination for the right nostril, testing switched to the left with the other nostril blocked. The
259
olfactory performance of a nostril was graded as normosmia, hyposmia, or anosmia based on the report of the developer [5]: BTT scores of 9–11 were normosmia; 5–8, hyposmia; 0–4, anosmia. Then subjects were assigned to one of the three olfactory groups – normosmic, hyposmic, or anosmic – preoperatively according to the performance of the better functioning nostril. Olfactory thresholds of both nostrils independently contribute to an individual’s olfaction and the mixed outcome of the two separate performances is likely to follow the better functioning nostril in a bilateral smelling mode. Postoperative olfactory outcomes were divided into three categories according to the changes in the BTT score. The test-retest reliability of the CCCRC test has been reported to be very high (0.92) [10]. Improvement was defined by an increase of the score ‡ 2, no changes, and deterioration by a decrease of ‡ 2. Subjects were assigned to one of the three outcome groups postoperatively. For subjective olfactory assessment, patients were asked to indicate their sense of smell on a 10-point VAS: 0 represented the absence of smell sensation and 10 represented the best sense of smell. For assessment of odor identification, we used a commercially available test kit, the Smell Identification TestTM (Sensonics, Inc., Haddon Heights, NJ, USA) that consists of 12 odorants presented with a scratch-and-sniff technique. For a given item, the patients were forced to choose one odor quality from four alternatives provided. The B-SIT score was defined as the number of correct choices. VAS and B-SIT were performed in a bilateral smelling mode. All tests were repeated at 6 months after surgery. Statistical analysis SPSS 18.0 software (IBM Corp., NY, USA) was used for data analysis and a two-tailed p value of < 0.05 was considered to be significant. Pearson’s correlation coefficient was obtained between the BTT and VAS/B-SIT scores pre- and postoperatively. Preoperative VAS and B-SIT scores were compared across the three olfactory groups (normosmic, hyposmic, and anosmic) using one-way analysis of variance (ANOVA) with the Tukey post hoc test. After ESS, pre- and postoperative BTT/VAS/B-SIT scores were compared within each outcome group, i.e. improvement, no changes, and deterioration, using the Wilcoxon signed rank test. Results Sixty-eight patients met the inclusion criteria (45 men and 23 women; aged 12–65 years). The number of
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Figure 1. Pre- and postoperative correlations between BTT and VAS/B-SIT scores. B-SIT, brief-smell identification test; BTT, butanol threshold test; VAS, visual analog scale. Error bars indicate SEM.
patients with bilateral normosmia/hyposmia/anosmia was 11/9/36, respectively. Eight patients had unilateral normosmia and contralateral hyposmia; four patients had anosmia and hyposmia. The preoperative Pearson correlation coefficient between the BTT and VAS scores of all subjects was 0.483 (p = 0.000); between the BTT and B-SIT scores it was 0.704 (p = 0.000). The postoperative Pearson correlation coefficient between the BTT and VAS scores of all subjects was 0.434 (p = 0.000); between the BTT and B-SIT scores it was 0.605 (p = 0.000) (Figure 1). Nineteen (28%) patients were normosmic, 13 (19%) were hyposmic, and 36 (53%) were anosmic. The mean (SD) BTT scores of the normosmic, hyposmic, and anosmic groups were 10.4 (1.0), 6.5 (1.3), and 1.4 (1.5), respectively. The preoperative mean (SD) VAS scores were 7.5 (1.6), 6.0 (1.9), and 4.3 (3.2) in the normosmic, hyposmic, and anosmic groups, respectively. The post hoc test revealed differences between the normosmic and anosmic groups (p = 0.000). The preoperative mean (SD) B-SIT scores of the normosmic/hyposmic/anosmic groups were 9.0 (1.6)/8.3 (2.3)/3.7 (3.9), respectively. The scores were significantly different between the normosmic and anosmic groups (p = 0.000), and between the hyposmic and anosmic groups (p = 0.000) by the post hoc test (Figure 2). After ESS, the improvement group comprised 28 (41.2%) subjects, the no changes group, 23 (33.8%), and the deterioration group, 17 (25.0%) (Figure 3A).
According to the VAS score, 18 (26.5%) subjects showed an increase of ‡ 2 points; 35 (51.5%), no changes; 15 (22.1%), a decrease of ‡ 2 points (Figure 3B). With the B-SIT score, 19 (27.9%) subjects showed an increase of ‡ 2 points; 39 (57.4%), no changes; 10 (14.7%), a decrease of ‡ 2 points (Figure 3C). Within the improvement group, preand postoperative mean (SD) BTT scores were 2.7 (2.7) and 7.9 (2.0) (p = 0.000); pre- and postoperative VAS scores, 5.3 (3.0) and 6.5 (2.0) (p = 0.019); pre- and postoperative B-SIT scores, 5.2 (4.3) and
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Normosmia (n = 19)
VAS (0–10) Hyposmia (n = 13)
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Figure 2. Comparison of BTT/VAS/B-SIT scores across normosmic, hyposmic, and anosmic groups. B-SIT, brief-smell identification test; BTT, butanol threshold test; VAS, visual analog scale. *p = 0.000.
Olfactory testing in patients with chronic rhinosinusitis A
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Acta Otolaryngol Downloaded from informahealthcare.com by Kainan University on 04/09/15 For personal use only.
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Figure 3. Postoperative olfactory outcomes.
7.8 (2.8) (p = 0.002), respectively. Within the no changes group, pre- and postoperative BTT scores were 4.8 (4.8) and 4.7 (4.8) (p = 0.317); pre- and postoperative VAS scores, 4.8 (3.3) and 4.9 (3.6) (p = 0.808); pre- and postoperative B-SIT scores, 5.2 (4.1) and 4.6 (3.8) (p = 0.259), respectively. Within
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the deterioration group, pre- and postoperative BTT scores were 8.5 (2.7) and 4.4 (2.9) (p = 0.000); pre- and postoperative VAS scores, 6.8 (2.0) and 6.5 (2.1) (p = 0.225); pre- and postoperative B-SIT scores, 8.7 (1.7) and 9.2 (1.8) (p = 0.231), respectively (Figure 4).
Improvement group (n = 28) p = 0.002
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Figure 4. Comparison of pre- and postoperative BTT/VAS/B-SIT scores within each outcome group. B-SIT, brief-smell identification test; BTT, butanol threshold test; VAS, visual analog scale. Error bars indicate SEM.
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Discussion In the present study, we compared VAS/B-SIT with BTT to demonstrate its potential to screen anosmia. Anosmia secondary to CRS was diagnosed by using BTT, a standardized olfactory threshold test. Toledano et al. reported that the CCCRC test is as valid as the CCSIT to be administered in patients with nasal polyposis [10]. In methodology, we conversely thought that BTT is more appropriate for the basic test to be compared because the B-SIT provides no detailed information on the olfactory threshold. Most of the subjects (82.4%) showed the same olfactory performances in both nostrils. Weak, but significant positive correlations were observed between the BTT and VAS scores preoperatively (r = 0.483) and 6 months postoperatively (r = 0.434); moderate positive correlations were observed between the BTT and B-SIT scores, pre- and postoperatively (r = 0.704 and 0.605). Briner et al. reported a higher pre-/postoperative correlation coefficient of 0.81/0.68 than ours between the VAS and butanol scores [11]. Nguyen et al. documented moderate correlations between the self-ratings and olfactory test scores before and after surgery (both r = 0.66) [12]. Welge-Luessen et al. reported a similar correlation between the self-ratings and measures of olfactory function (r = 0.57) [13]. However, the various results cannot easily be compared because most olfactory studies have employed different tests and methods. Subjective ratings are not always in agreement with the olfactory testing results. It has been documented that many patients with CRS do not realize the presence of their olfactory disorders; 58% of all patients with CRS noticed preoperative olfactory deficits, while 83% were identified to have deficits by olfactory tests [14]. That may partly explain the weak positive correlations between the VAS and BTT scores of our results. Both B-SIT and VAS scores were significantly lower in the anosmics than in normosmics, and the B-SIT scores were also lower in the anosmics than in the hyposmics. BTT score differences across the three groups must be expected naturally because the BTT score itself was the standard for grouping. The means (95% confidence intervals, CI) of the B-SIT and VAS scores of the anomics were 3.7 (2.4–5.0) and 4.3 (3.2– .4), respectively. When the score 5 (the maximum value of 95% CI) was considered as the cut-off point of anosmia, our results indicated that CRS patients who presented with either a B-SIT score £ 5 or a VAS score £ 5 are likely to have anosmia. With this criterion, the sensitivity/specificity of B-SIT was 63.9/ 93.8% and the the sensitivity/specificity of VAS was 63.9/71.9%. The B-SIT showed especially high
specificity, while the sensitivities of both tests were the same. After ESS, the mean BTT score change was 5.2/ 4.1 in the improvement/deterioration groups. Within the improvement group, mean increase of the B-SIT/ VAS score after ESS was 2.6/1.2 with statistical significance, which probably implies that an increase of the B-SIT score ‡ 3 or the VAS score ‡ 2 can signify olfactory improvement after ESS. However, within the no changes and deterioration groups, pre- and postoperative B-SIT/VAS scores were similar. In other words, neither the B-SIT and nor the VAS differentiated between no change and deterioration of olfaction. Lack of attention to olfaction in daily life [15], probably because of improvement of the other troubling CRS symptoms such as obstruction and rhinorrhea, may be the reason why deterioration was not detected by VAS. The mechanism by which the B-SIT scores remained unchanged in spite of the threshold deterioration is still unclear. It might be explained by the low number of stimuli in the test. We conclude that the B-SIT can substitute for the BTT in screening of anosmia and postoperative assessment of olfactory outcomes in CRS patients. A B-SIT score £ 5 may indicate anosmia with high specificity, and an increase of the score ‡ 3 may indicate postoperative improvement. VAS can be complementary to B-SIT with moderate sensitivity and specificity. Furthermore, we suggest that a timeeffective test battery composed of B-SIT and VAS can be implemented for simple olfactory evaluation in any otolaryngology clinic. Acknowledgment This work was partly supported by a 2014 grant from the alumni association of the Department of Otorhinolaryngology-Head and Neck Surgery, College of Medicine, The Catholic University of Korea. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
References [1] Raviv JR, Kern RC. Chronic sinusitis and olfactory dysfunction. Otolaryngol Clin North Am 2004;37:1143–57. [2] Litvack JR, Mace JC, Smith TL. Does olfactory function improve after endoscopic sinus surgery? Otolaryngol Head Neck Surg 2009;140:312–19. [3] Kimmelman CP. The risk to olfaction from nasal surgery. Laryngoscope 1994;104:981–8. [4] Doty RL. Office procedures for quantitative assessment of olfactory function. Am J Rhinol 2007;21:460–73.
Olfactory testing in patients with chronic rhinosinusitis
Acta Otolaryngol Downloaded from informahealthcare.com by Kainan University on 04/09/15 For personal use only.
[5] Cain WS, Gent JF, Goodspeed RB, Leonard G. Evaluation of olfactory dysfunction in the Connecticut chemosensory clinical research center. Laryngoscope 1988;98:83–8. [6] Briner HR, Jones N, Simmen D. Olfaction after endoscopic sinus surgery: long-term results. Rhinology 2012;50:178–84. [7] Doty RL. Development of the 12-item cross-cultural smell identification test (CC-SIT). Laryngoscope 1996;106:353–6. [8] Doty RL. Olfaction and its alteration by nasal obstruction, rhinitis, and rhinosinusitis. Laryngoscope 2001;111:409–23. [9] Rosenfeld RM, Andes D, Bhattacharyya N, Cheung D, Eisenberg S, Ganiats TG, et al. Clinical practice guideline: adult sinusitis. Otolaryngol Head Neck Surg 2007;137:S1– 31. [10] Toledano A, González E, Rodríguez G, Galindo N. The validity of CCCRC test in patients with nasal polyposis. Rhinology 2007;45:54–8.
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[11] Briner HR, Jones N, Simmen D. Olfaction after endoscopic sinus surgery: long-term results. Rhinology 2012;50:178–84. [12] Nguyen DT, Nguyen-Thi PL, Jankowski R. How does measured olfactory function correlate with self-ratings of the sense of smell in patients with nasal polyposis? Laryngoscope 2012;122:947–52. [13] Welge-Luessen A, Hummel T, Stojan T, Wolfensberger M. What is the correlation between ratings and measures of olfactory function in patients with olfactory loss? Am J Rhinol 2005;19:567–71. [14] Delank KW, Stoll W. Olfactory function after functional endoscopic sinus surgery for chronic sinusitis. Rhinology 1998;36:15–19. [15] Gudziol V, Lotsch J, Hahner A, Zahnert T, Hummel T. Clinical significance of results from olfactory testing. Laryngoscope 2006;116:1858–63.
ORIGINAL ARTICLE
Simple assessment of olfaction in patients with chronic rhinosinusitis
Acta Otolaryngol Downloaded from informahealthcare.com by Kainan University on 04/09/15 For personal use only.
BYUNG GUK KIM, JEONG-HOON OH, HA NA CHOI & SO YOUNG PARK Department of Otorhinolaryngology-Head and Neck Surgery, College of Medicine, The Catholic University of Korea, Seoul, Korea
Abstract Conclusion: The brief-smell identification test (B-SIT) can substitute for the butanol threshold test (BTT) in screening of anosmia and postoperative assessment of olfactory outcomes in patients with chronic rhinosinusitis (CRS). A time-effective test battery composed of B-SIT and the visual analog scale (VAS) can be implemented for simple olfactory assessment in any otolaryngology clinic. Objectives: Anosmia is a distinct clinical entity requiring special attention. Unpredictable olfactory outcomes after surgery make preoperative assessment more important. We compared the results of the BTT, B-SIT, and VAS to investigate whether B-SIT or VAS can substitute for BTT in screening of anosmia and postoperative follow-up. Methods: We collected data on 68 CRS patients who had bilateral CRS and underwent endoscopic sinus surgery. Olfactory performance was graded using the BTT: normosmia, hyposmia, or anosmia. VAS and B-SIT were also performed. All tests were repeated 6 months after surgery. Postoperative improvement was defined by an increase of the BTT score ‡ 2. Results: The B-SIT and VAS scores of the anomics were significantly lower than those of the normosmics. B-SIT discriminated anosmia with high specificity. Within the improvement group, postoperative increase of B-SIT/VAS score showed significance. However, neither the B-SIT nor the VAS differentiated between no change and deterioration of olfaction.
Keywords: Anosmia, brief-smell identification test, butanol threshold test, endoscopic sinus surgery, visual analog scale
Introduction Decreased sense of smell is a frequent complaint of patients with chronic rhinosinusitis (CRS). Anosmia should be regarded as a distinct clinical entity requiring special attention in the evaluation of CRS patients because of the problems of safety and quality of life. Although olfactory impairment secondary to CRS has been known to be the most treatable form of the olfactory disorders, the outcomes after sinus surgery depend on the varied contribution from two pathophysiologic mechanisms: conductive impairment from the mechanical obstruction of the nasal passages and sensorineural impairment from the toxic inflammatory mediators causing neuronal damage in the olfactory mucosa [1]. After endoscopic sinus surgery (ESS), residual hyposmia remains in most of the patients despite olfactory improvement [2], and
olfaction deteriorates occasionally by the mechanisms related to the risks inherent in nasal surgery [3]. Therefore, the unpredictable olfactory outcomes make preoperative evaluation of the baseline olfactory function more important. Quantitative assessment of the olfactory function, which has relied on threshold determination or odor identification, has become increasingly common in clinical practice due to the development of various standardized olfactory tests [4]. The butanol threshold test (BTT) is one part of the Connecticut Chemosensory Clinical Research Center (CCCRC) test [5]. It has been widely used and is regarded as one of the most accurate methods that reflect the olfactory status [6]. However, the detailed threshold test requires a relatively long test time and trained personnel, while identification tests take less time and can be self-administered. The 12-item brief-smell
Correspondence: So Young Park MD PhD, Department of Otorhinolaryngology-Head and Neck Surgery, St Paul’s Hospital, College of Medicine, The Catholic University of Korea, Wangsan-ro 180, Dongdaemoon-gu, Seoul 130-709, Republic of Korea. Tel: +82 2 961 4526. E-mail: [email protected]
(Received 11 August 2014; accepted 28 September 2014) ISSN 0001-6489 print/ISSN 1651-2251 online 2015 Informa Healthcare DOI: 10.3109/00016489.2014.974288
Acta Otolaryngol Downloaded from informahealthcare.com by Kainan University on 04/09/15 For personal use only.
Olfactory testing in patients with chronic rhinosinusitis identification test (B-SIT), also known as the crosscultural smell identification test (CCSIT), is a validated scratch-and-sniff semiquantitative test at the suprathreshold level performed in less than 5 min [7,8]. One weakness of the B-SIT is poor differentiation between subclasses of dysfunction due to few stimuli [4]. The visual analog scale (VAS) provides a self-rating subjective measure of olfactory function. Nowadays, various olfactory tests are routinely performed in more and more rhinology clinics at the clinician’s convenience. The authors have employed an olfactory test battery composed of BTT, B-SIT, and VAS in the clinical setting of CRS. In the present study, the results of three tests were compared to investigate whether the B-SIT or VAS can substitute for BTT in screening of CRS-related anosmia and evaluation of postoperative outcomes in terms of olfaction. Material and methods Subjects Clinical data on bilateral CRS patients who underwent ESS between January 2007 and December 2011 were retrospectively collected with the approval of the Institutional Review Board of The Catholic University of Korea St Paul’s Hospital. All subjects had CRS with or without polyps and fulfilled the diagnostic criteria for adult CRS recommended by the American Academy of Otolaryngology-Head and Neck Surgery Foundation [9]. Patients who completed both preoperative and postoperative olfactory tests were included in this study. Those with the following conditions were excluded from the analysis: older than 65 years, asthma, previous nasal surgery, and other suspected causes of olfactory disorders such as head trauma or viral infection. Surgery (bilateral ESS) was performed by a single surgeon (the first author) after a failure of antibiotic treatment. None of the patients was given topical or systemic steroids preoperatively. Olfactory tests and grouping Olfactory thresholds were measured using 1-butanol sniff bottles as described by Cain et al. [5]. Our modification was the highest concentration. We started from 100% concentration (dilution step 0) and prepared successive dilutions by a factor of 1/ 3 up to step 11. Dilution step 3 equaled 4% aqueous concentration. Four consecutive correct choices marked the threshold, namely the BTT score. After threshold determination for the right nostril, testing switched to the left with the other nostril blocked. The
259
olfactory performance of a nostril was graded as normosmia, hyposmia, or anosmia based on the report of the developer [5]: BTT scores of 9–11 were normosmia; 5–8, hyposmia; 0–4, anosmia. Then subjects were assigned to one of the three olfactory groups – normosmic, hyposmic, or anosmic – preoperatively according to the performance of the better functioning nostril. Olfactory thresholds of both nostrils independently contribute to an individual’s olfaction and the mixed outcome of the two separate performances is likely to follow the better functioning nostril in a bilateral smelling mode. Postoperative olfactory outcomes were divided into three categories according to the changes in the BTT score. The test-retest reliability of the CCCRC test has been reported to be very high (0.92) [10]. Improvement was defined by an increase of the score ‡ 2, no changes, and deterioration by a decrease of ‡ 2. Subjects were assigned to one of the three outcome groups postoperatively. For subjective olfactory assessment, patients were asked to indicate their sense of smell on a 10-point VAS: 0 represented the absence of smell sensation and 10 represented the best sense of smell. For assessment of odor identification, we used a commercially available test kit, the Smell Identification TestTM (Sensonics, Inc., Haddon Heights, NJ, USA) that consists of 12 odorants presented with a scratch-and-sniff technique. For a given item, the patients were forced to choose one odor quality from four alternatives provided. The B-SIT score was defined as the number of correct choices. VAS and B-SIT were performed in a bilateral smelling mode. All tests were repeated at 6 months after surgery. Statistical analysis SPSS 18.0 software (IBM Corp., NY, USA) was used for data analysis and a two-tailed p value of < 0.05 was considered to be significant. Pearson’s correlation coefficient was obtained between the BTT and VAS/B-SIT scores pre- and postoperatively. Preoperative VAS and B-SIT scores were compared across the three olfactory groups (normosmic, hyposmic, and anosmic) using one-way analysis of variance (ANOVA) with the Tukey post hoc test. After ESS, pre- and postoperative BTT/VAS/B-SIT scores were compared within each outcome group, i.e. improvement, no changes, and deterioration, using the Wilcoxon signed rank test. Results Sixty-eight patients met the inclusion criteria (45 men and 23 women; aged 12–65 years). The number of
B. G. Kim et al. 12
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Figure 1. Pre- and postoperative correlations between BTT and VAS/B-SIT scores. B-SIT, brief-smell identification test; BTT, butanol threshold test; VAS, visual analog scale. Error bars indicate SEM.
patients with bilateral normosmia/hyposmia/anosmia was 11/9/36, respectively. Eight patients had unilateral normosmia and contralateral hyposmia; four patients had anosmia and hyposmia. The preoperative Pearson correlation coefficient between the BTT and VAS scores of all subjects was 0.483 (p = 0.000); between the BTT and B-SIT scores it was 0.704 (p = 0.000). The postoperative Pearson correlation coefficient between the BTT and VAS scores of all subjects was 0.434 (p = 0.000); between the BTT and B-SIT scores it was 0.605 (p = 0.000) (Figure 1). Nineteen (28%) patients were normosmic, 13 (19%) were hyposmic, and 36 (53%) were anosmic. The mean (SD) BTT scores of the normosmic, hyposmic, and anosmic groups were 10.4 (1.0), 6.5 (1.3), and 1.4 (1.5), respectively. The preoperative mean (SD) VAS scores were 7.5 (1.6), 6.0 (1.9), and 4.3 (3.2) in the normosmic, hyposmic, and anosmic groups, respectively. The post hoc test revealed differences between the normosmic and anosmic groups (p = 0.000). The preoperative mean (SD) B-SIT scores of the normosmic/hyposmic/anosmic groups were 9.0 (1.6)/8.3 (2.3)/3.7 (3.9), respectively. The scores were significantly different between the normosmic and anosmic groups (p = 0.000), and between the hyposmic and anosmic groups (p = 0.000) by the post hoc test (Figure 2). After ESS, the improvement group comprised 28 (41.2%) subjects, the no changes group, 23 (33.8%), and the deterioration group, 17 (25.0%) (Figure 3A).
According to the VAS score, 18 (26.5%) subjects showed an increase of ‡ 2 points; 35 (51.5%), no changes; 15 (22.1%), a decrease of ‡ 2 points (Figure 3B). With the B-SIT score, 19 (27.9%) subjects showed an increase of ‡ 2 points; 39 (57.4%), no changes; 10 (14.7%), a decrease of ‡ 2 points (Figure 3C). Within the improvement group, preand postoperative mean (SD) BTT scores were 2.7 (2.7) and 7.9 (2.0) (p = 0.000); pre- and postoperative VAS scores, 5.3 (3.0) and 6.5 (2.0) (p = 0.019); pre- and postoperative B-SIT scores, 5.2 (4.3) and
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Normosmia (n = 19)
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Figure 2. Comparison of BTT/VAS/B-SIT scores across normosmic, hyposmic, and anosmic groups. B-SIT, brief-smell identification test; BTT, butanol threshold test; VAS, visual analog scale. *p = 0.000.
Olfactory testing in patients with chronic rhinosinusitis A
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Figure 3. Postoperative olfactory outcomes.
7.8 (2.8) (p = 0.002), respectively. Within the no changes group, pre- and postoperative BTT scores were 4.8 (4.8) and 4.7 (4.8) (p = 0.317); pre- and postoperative VAS scores, 4.8 (3.3) and 4.9 (3.6) (p = 0.808); pre- and postoperative B-SIT scores, 5.2 (4.1) and 4.6 (3.8) (p = 0.259), respectively. Within
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the deterioration group, pre- and postoperative BTT scores were 8.5 (2.7) and 4.4 (2.9) (p = 0.000); pre- and postoperative VAS scores, 6.8 (2.0) and 6.5 (2.1) (p = 0.225); pre- and postoperative B-SIT scores, 8.7 (1.7) and 9.2 (1.8) (p = 0.231), respectively (Figure 4).
Improvement group (n = 28) p = 0.002
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Figure 4. Comparison of pre- and postoperative BTT/VAS/B-SIT scores within each outcome group. B-SIT, brief-smell identification test; BTT, butanol threshold test; VAS, visual analog scale. Error bars indicate SEM.
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Discussion In the present study, we compared VAS/B-SIT with BTT to demonstrate its potential to screen anosmia. Anosmia secondary to CRS was diagnosed by using BTT, a standardized olfactory threshold test. Toledano et al. reported that the CCCRC test is as valid as the CCSIT to be administered in patients with nasal polyposis [10]. In methodology, we conversely thought that BTT is more appropriate for the basic test to be compared because the B-SIT provides no detailed information on the olfactory threshold. Most of the subjects (82.4%) showed the same olfactory performances in both nostrils. Weak, but significant positive correlations were observed between the BTT and VAS scores preoperatively (r = 0.483) and 6 months postoperatively (r = 0.434); moderate positive correlations were observed between the BTT and B-SIT scores, pre- and postoperatively (r = 0.704 and 0.605). Briner et al. reported a higher pre-/postoperative correlation coefficient of 0.81/0.68 than ours between the VAS and butanol scores [11]. Nguyen et al. documented moderate correlations between the self-ratings and olfactory test scores before and after surgery (both r = 0.66) [12]. Welge-Luessen et al. reported a similar correlation between the self-ratings and measures of olfactory function (r = 0.57) [13]. However, the various results cannot easily be compared because most olfactory studies have employed different tests and methods. Subjective ratings are not always in agreement with the olfactory testing results. It has been documented that many patients with CRS do not realize the presence of their olfactory disorders; 58% of all patients with CRS noticed preoperative olfactory deficits, while 83% were identified to have deficits by olfactory tests [14]. That may partly explain the weak positive correlations between the VAS and BTT scores of our results. Both B-SIT and VAS scores were significantly lower in the anosmics than in normosmics, and the B-SIT scores were also lower in the anosmics than in the hyposmics. BTT score differences across the three groups must be expected naturally because the BTT score itself was the standard for grouping. The means (95% confidence intervals, CI) of the B-SIT and VAS scores of the anomics were 3.7 (2.4–5.0) and 4.3 (3.2– .4), respectively. When the score 5 (the maximum value of 95% CI) was considered as the cut-off point of anosmia, our results indicated that CRS patients who presented with either a B-SIT score £ 5 or a VAS score £ 5 are likely to have anosmia. With this criterion, the sensitivity/specificity of B-SIT was 63.9/ 93.8% and the the sensitivity/specificity of VAS was 63.9/71.9%. The B-SIT showed especially high
specificity, while the sensitivities of both tests were the same. After ESS, the mean BTT score change was 5.2/ 4.1 in the improvement/deterioration groups. Within the improvement group, mean increase of the B-SIT/ VAS score after ESS was 2.6/1.2 with statistical significance, which probably implies that an increase of the B-SIT score ‡ 3 or the VAS score ‡ 2 can signify olfactory improvement after ESS. However, within the no changes and deterioration groups, pre- and postoperative B-SIT/VAS scores were similar. In other words, neither the B-SIT and nor the VAS differentiated between no change and deterioration of olfaction. Lack of attention to olfaction in daily life [15], probably because of improvement of the other troubling CRS symptoms such as obstruction and rhinorrhea, may be the reason why deterioration was not detected by VAS. The mechanism by which the B-SIT scores remained unchanged in spite of the threshold deterioration is still unclear. It might be explained by the low number of stimuli in the test. We conclude that the B-SIT can substitute for the BTT in screening of anosmia and postoperative assessment of olfactory outcomes in CRS patients. A B-SIT score £ 5 may indicate anosmia with high specificity, and an increase of the score ‡ 3 may indicate postoperative improvement. VAS can be complementary to B-SIT with moderate sensitivity and specificity. Furthermore, we suggest that a timeeffective test battery composed of B-SIT and VAS can be implemented for simple olfactory evaluation in any otolaryngology clinic. Acknowledgment This work was partly supported by a 2014 grant from the alumni association of the Department of Otorhinolaryngology-Head and Neck Surgery, College of Medicine, The Catholic University of Korea. Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.
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