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Decreased nasal nitric oxide levels: a potential marker of decreased olfactory discrimination in chronic rhinosinusitis

Published online by Cambridge University Press:  27 October 2021

L Zhang ,
F Fang ,
L Yao ,
H Sun ,
X Zhan ,
M Lu  and
Y Wei
L Zhang
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Beijing Anzhen Hospital, Capital Medical University, Beijing, China
F Fang
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Beijing Anzhen Hospital, Capital Medical University, Beijing, China Key Laboratory of Upper Airway Dysfunction-Related Cardiovascular Diseases, Beijing Institute of Heart, Lung and Blood Vessel Diseases, Beijing Anzhen Hospital, Beijing, China
L Yao
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Beijing Anzhen Hospital, Capital Medical University, Beijing, China
H Sun
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Beijing Anzhen Hospital, Capital Medical University, Beijing, China Key Laboratory of Upper Airway Dysfunction-Related Cardiovascular Diseases, Beijing Institute of Heart, Lung and Blood Vessel Diseases, Beijing Anzhen Hospital, Beijing, China
X Zhan
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Beijing Anzhen Hospital, Capital Medical University, Beijing, China
M Lu
Affiliation:
Department of Otolaryngology – Head and Neck Surgery, Beijing Anzhen Hospital, Capital Medical University, Beijing, China
Y Wei*
Affiliation:
Department of Otorhinolaryngology Head and Neck Surgery, Capital Institute of Pediatrics, Beijing, China
*
Author for correspondence: Dr Y Wei, Department of Otolaryngology – Head and Neck Surgery, Capital Institute of Pediatrics, Beijing, China E-mail: weiyongxiang6261@163.com
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Abstract

Objective

This study aimed to investigate the association of nasal nitric oxide and olfactory function.

Method

A cross-sectional study was performed in 117 adults, including 91 patients with chronic rhinosinusitis and 26 healthy controls. Scores on the 22-item Sino-Nasal Outcomes Test, Lund-Mackay scale and Lund-Kennedy scale were recorded to assess severity of disease. All participants were screened for common inhaled and food allergens. Nasal nitric oxide and fractional exhaled nitric oxide testing, acoustic rhinometry and anterior rhinomanometry testing were performed to measure nasal function. The validated Sniffin’ Sticks test battery was used to assess olfactory function.

Results

Higher nasal nitric oxide was an independent protective factor for odour discrimination and odour threshold in participants with chronic rhinosinusitis after adjusting for age, gender, drinking, smoking, 22-item Sino-Nasal Outcomes Test, Lund-Mackay score, Lund-Kennedy score, immunoglobulin E and the second minimal cross-sectional area by acoustic rhinometry. Nasal nitric oxide also showed high discrimination in predicting impaired odour discrimination. In addition, nasal nitric oxide was lower in older participants, those with higher Lund-Mackay or Lund-Kennedy scores and higher with elevated total serum immunoglobulin E concentrations above a threshold of 0.35 kU/l.

Conclusion

Higher nasal nitric oxide is associated with better odour discrimination in chronic rhinosinusitis and is modulated by age, degree of allergy and severity of chronic rhinosinusitis.

Keywords

Nitric OxideSmellSinusitis
Type
Main Article
Information
The Journal of Laryngology & Otology , Volume 136 , Issue 5 , May 2022 , pp. 419 - 426
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of J.L.O. (1984) LIMITED

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Footnotes

Dr Y Wei takes responsibility for the integrity of the content of the paper

References

Fokkens, WJ, Lund, VJ, Mullol, J, Bachert, C, Alobid, I, Baroody, F et al. EPOS 2012: European position paper on rhinosinusitis and nasal polyps 2012. A summary for otorhinolaryngologists. Rhinology 2012;50:1–12Google ScholarPubMed
Soler, ZM, Kohli, P, Storck, KA, Schlosser, RJ. Olfactory impairment in chronic rhinosinusitis using threshold, discrimination, and identification scores. Chem Senses 2016;41:713–19CrossRefGoogle ScholarPubMed
Rombaux, P, Potier, H, Bertrand, B, Duprez, T, Hummel, T. Olfactory bulb volume in patients with sinonasal disease. Am J Rhinol 2008;22:598–601CrossRefGoogle ScholarPubMed
Han, P, Whitcroft, KL, Fischer, J, Gerber, J, Cuevas, M, Andrews, P et al. Olfactory brain gray matter volume reduction in patients with chronic rhinosinusitis. Int Forum Allergy Rhinol 2017;7:551–6CrossRefGoogle ScholarPubMed
Whitcroft, KL, Cuevas, M, Haehner, A, Hummel, T. Patterns of olfactory impairment reflect underlying disease etiology. Laryngoscope 2017;127:291–5CrossRefGoogle ScholarPubMed
Whitcroft, KL, Cuevas, M, Andrews, P, Hummel, T. Monitoring olfactory function in chronic rhinosinusitis and the effect of disease duration on outcome. Int Forum Allergy Rhinol 2018;8:769–76CrossRefGoogle Scholar
Pifferi, M, Bush, A, Rizzo, M, Tonacci, A, Cicco, MD, Piras, M et al. Olfactory dysfunction is worse in primary ciliary dyskinesia compared with other causes of chronic sinusitis in children. Thorax 2018;73:980–2CrossRefGoogle ScholarPubMed
Elsherif, HS, Landis, BN, Hamad, MH, Hugentobler, M, Bahig, SM, Gamaa, AM et al. Olfactory function and nasal nitric oxide. Clin Otolaryngol 2007;32:356–60CrossRefGoogle ScholarPubMed
American Thoracic Society, European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide. Am J Respir Crit Care Med 2005;171:912–30CrossRefGoogle Scholar
Hummel, T, Sekinger, B, Wolf, SR, Pauli, E, Kobal, G. ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 1997;22:39–52CrossRefGoogle ScholarPubMed
Ewan, P W, Coote, D. Evaluation of a capsulated hydrophilic carrier polymer (the ImmunoCAP) for measurement of specific IgE antibodies. Allergy 1990;45:22–9CrossRefGoogle ScholarPubMed
Clement, P A, Gordts, F. Consensus report on acoustic rhinometry and rhinomanometry. Rhinology 2005;43:169–79Google ScholarPubMed
Oleszkiewicz, A, Schriever, VA, Croy, I, Hähner, A, Hummel, T. Updated Sniffin'Sticks normative data based on an extended sample of 9139 subjects. Eur Arch Otorhinolaryngol 2019;276:719–28CrossRefGoogle Scholar
Schlosser, RJ, Desiato, VM, Storck, KA, Nguyen, SA, Hill, JB, Washington, BJ et al. A community-based study on the prevalence of olfactory dysfunction. Am J Rhinol Allergy 2020;34:661–70CrossRefGoogle Scholar
Delgado-Losada, ML, Delgado-Lima, AH, Bouhaben, J. Spanish validation for olfactory function testing using the sniffin'sticks olfactory test: threshold, discrimination, and identification. Brain Sci 2020;10:943CrossRefGoogle Scholar
Gupta, N, Drusch, J, Landis, BN, Hummel, T. Nasal nitric oxide levels do not allow for discrimination between olfactory loss due to various etiologies. Laryngoscope 2013;123:311–14CrossRefGoogle Scholar
Hedner, M, Larsson, M, Arnold, N, Zucco, GM, Hummel, T. Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol 2010;32:1062–7CrossRefGoogle ScholarPubMed
Stopfer, M, Bhagavan, S, Smith, BH, Laurent, G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 1997;390:70–4CrossRefGoogle ScholarPubMed
Hosler, J S, Buxton, K L, Smith, B H. Impairment of olfactory discrimination by blockade of GABA and nitric oxide activity in the honey bee antennal lobes. Behav Neurosci 2000;114:514–25CrossRefGoogle ScholarPubMed
Pietrobon, M, Zamparo, I, Maritan, M, Franchi, SA, Pozzan, T, Lodovichi, C. Interplay among cGMP, cAMP, and Ca2+ in living olfactory sensory neurons in vitro and in vivo. J Neurosci 2011;31:8395–405CrossRefGoogle ScholarPubMed
Teyke, T, Gelperin, A. Olfactory oscillations augment odor discrimination not odor identification by Limax CNS. Neuroreport 1999;10:1061–8CrossRefGoogle Scholar
Gupta, D, Gulati, A, Singh, I, Tekur, U. Endoscopic, radiological, and symptom correlation of olfactory dysfunction in pre-and postsurgical patients of chronic rhinosinusitis. Chem Senses 2014;39:705–10CrossRefGoogle ScholarPubMed
Li, C, Jiang, J, Kim, K, Otto, BA, Farag, AA, Cowart, BJ et al. Nasal structural and aerodynamic features that may benefit normal olfactory sensitivity. Chem Senses 2018;43:229–37CrossRefGoogle ScholarPubMed
Hummel, T, Whitcroft, KL, Andrews, P, Altundag, A, Cinghi, C, Costanzo, RM et al. Position paper on olfactory dysfunction. Rhinol Suppl 2017;54:1–30CrossRefGoogle ScholarPubMed
Ishizuka, T, Hisada, T, Kamide, Y, Aoki, H, Seki, K, Honjo, C et al. The effects of concomitant GERD, dyspepsia, and rhinosinusitis on asthma symptoms and FeNO in asthmatic patients taking controller medications. J Asthma Allergy 2014;7:131–9CrossRefGoogle ScholarPubMed
Kharitonov, SA, Rajakulasingam, K, O'Connor, B, Durham, SR, Barnes, PJ. Nasal nitric oxide is increased in patients with asthma and allergic rhinitis and may be modulated by nasal glucocorticoids. J Allergy Clin Immunol 1997;99:58–64Google ScholarPubMed
Oliver, J D, Lim, K G, O'Brien, E K. Correlation of exhaled nasal nitric oxide with sinus computed tomography and sinonasal outcome test scores: a cross-sectional pilot study. Am J Rhinol Allergy 2018;32:533–8CrossRefGoogle ScholarPubMed
Lee, JM, McKnight, CL, Aves, T, Yip, J, Grewal, AS, Gupta, S et al. Nasal nitric oxide as a marker of sinus mucosal health in patients with nasal polyposis. Int Forum Allergy Rhinol 2015;5:894–9CrossRefGoogle ScholarPubMed
Colantonio, D, Brouillette, L, Parikh, A, Scadding, GK. Paradoxical low nasal nitric oxide in nasal polyposis. Clin Exp Allergy 2002;32:698–701CrossRefGoogle ScholarPubMed