Olfactory Cleft Measurements and COVID-19-Related Anosmia

Aytug Altundag, Duzgun Yıldırım, Deniz Esin Tekcan Sanli, Melih Cayonu, Sedat Giray Kandemirli, Ahmet Necati Sanli, Ozge Arici Duz, Ozlem Saatci, Aytug Altundag, Duzgun Yıldırım, Deniz Esin Tekcan Sanli, Melih Cayonu, Sedat Giray Kandemirli, Ahmet Necati Sanli, Ozge Arici Duz, Ozlem Saatci

Abstract

Objective: This study aimed to investigate the differences in olfactory cleft (OC) morphology in coronavirus disease 2019 (COVID-19) anosmia compared to control subjects and postviral anosmia related to infection other than severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2).

Study design: Prospective.

Setting: This study comprises 91 cases, including 24 cases with anosmia due to SARS-CoV-2, 38 patients with olfactory dysfunction (OD) due to viral infection other than SARS-CoV-2, and a control group of 29 normosmic cases.

Methods: All cases had paranasal sinus computed tomography (CT), and cases with OD had magnetic resonance imaging (MRI) dedicated to the olfactory nerve. The OC width and volumes were measured on CT, and T2-weighted signal intensity (SI), olfactory bulb volumes, and olfactory sulcus depths were assessed on MRI.

Results: This study showed 3 major findings: the right and left OC widths were significantly wider in anosmic patients due to SARS-CoV-2 (group 1) or OD due to non-SARS-CoV-2 viral infection (group 2) when compared to healthy controls. OC volumes were significantly higher in group 1 or 2 than in healthy controls, and T2 SI of OC area was higher in groups 1 and 2 than in healthy controls. There was no significant difference in olfactory bulb volumes and olfactory sulcus depths on MRI among groups 1 and 2.

Conclusion: In this study, patients with COVID-19 anosmia had higher OC widths and volumes compared to control subjects. In addition, there was higher T2 SI of the olfactory bulb in COVID-19 anosmia compared to control subjects, suggesting underlying inflammatory changes. There was a significant negative correlation between these morphological findings and threshold discrimination identification scores.

Level of evidence: Level 4.

Keywords: COVID-19; SARS-CoV-2; Sniffin’ Sticks; anosmia; olfactory cleft; volume; width.

Conflict of interest statement

Disclosures: Competing interests: None.

Sponsorships: None.

Funding source: None.

Figures

Figure 1.
Figure 1.
Section through the parasagittal plane of the cribriform plate: cross section from the front one-third to the back two-thirds section perpendicular to the horizontal plane, the plan in which the coronal plan image was obtained.
Figure 2.
Figure 2.
Axial image depicting the total volume of the olfactory cleft (thick-edged rectangle, cm3) and mean density within the voxel of interest (thin double-line edged rectangle).
Figure 3.
Figure 3.
Grayscale and color window coronal T2 cleft magnetic resonance image. The mean region of interest signal intensity value was measured by taking the olfactory cleft mucosa along the height extending from the cleft top to 10 mm inferior.
Figure 4.
Figure 4.
Flowchart of the findings.

References

    1. Guan WJ, Ni ZY, Hu Y, et al.. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382:1708-1720.
    1. Cheng X, Liu J, Li N, et al.. Otolaryngology providers must be alert for patients with mild and asymptomatic COVID-19. Otolaryngol Head Neck Surg. 2020;162:809-810.
    1. Vaira LA, Salzano G, Deiana G, De Riu G. Anosmia and ageusia: common findings in COVID-19 patients. Laryngoscope. 2020;130:1787.
    1. Lechien JR, Chiesa-Estomba CM, De Siati DR, et al.. Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): a multicenter European study. Eur Arch Otorhinolaryngol. 2020;277:2251-2261.
    1. Tong JY, Wong A, Zhu D, Fastenberg JH, Tham T. The prevalence of olfactory and gustatory dysfunction in COVID-19 patients: a systematic review and meta-analysis. Otolaryngol Head Neck Surg. 2020;163:3-11.
    1. Parma V, Ohla K, Veldhuizen MG, et al.. More than smell—COVID-19 is associated with severe impairment of smell, taste, and chemesthesis [published online June 20, 2020]. Chem Senses.
    1. Hummel T, Whitcroft KL, Andrews P, et al.. Position paper on olfactory dysfunction. Rhinol Suppl. 2017;54:1-30.
    1. Lee DY, Lee WH, Wee JH, Kim JW. Prognosis of postviral olfactory loss: follow-up study for longer than one year. Am J Rhinol Allergy. 2014;28:419-422.
    1. Huart C, Philpott C, Konstantinidis I, et al.. Comparison of COVID-19 and common cold chemosensory dysfunction [published online August 19, 2020]. Rhinology.
    1. Gengler I, Wang JC, Speth MM, Sedaghat AR. Sinonasal pathophysiology of SARS-CoV-2 and COVID-19: a systematic review of the current evidence. Laryngoscope Investig Otolaryngol. 2020;5:354-359.
    1. Altundag A, Temirbekov D, Haci C, Yildirim D, Cayonu M. Olfactory cleft width and volume: possible risk factors for postinfectious olfactory dysfunction [published online February 6, 2020]. Laryngoscope.
    1. 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;22:39-52.
    1. Kobal G, Klimek L, Wolfensberger M, et al.. Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol. 2000;257:205-211.
    1. Wolfensberger M, Schnieper I, Welge-Lüssen A. Sniffin’Sticks: a new olfactory test battery. Acta Otolaryngol. 2000;120:303-306.
    1. Hummel T, Kobal G, Gudziol H, Mackay-Sim A. Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol. 2007;264:237-243.
    1. Tekeli H, Altundağ A, Salihoğlu M, Cayönü M, Kendirli MT. The applicability of the “Sniffin’ Sticks” olfactory test in a Turkish population. Med Sci Monit. 2013;19:1221-1226.
    1. Worley ML, Schlosser RJ, Soler ZM, Dubno JR, Eckert MA. Age-related differences in olfactory cleft volume in adults: a computational volumetric study. Laryngoscope. 2019;129:E55-E60.
    1. Li M, Sharbel DD, White B, Y, Tadros S, Kountakis SE. Reliability of the supraorbital ethmoid cell vs Keros classification in predicting the course of the anterior ethmoid artery. Int Forum Allergy Rhinol. 2019;9:821-824.
    1. Jahanshahlu L, Rezaei N. Central nervous system involvement in COVID-19 [published online May 22, 2020]. Arch Med Res.
    1. Saghazadeh A, Rezaei N. Towards treatment planning of COVID-19: rationale and hypothesis for the use of multiple immunosuppressive agents: anti-antibodies, immunoglobulins, and corticosteroids. Int Immunopharmacol. 2020;84:106560.
    1. Yazdanpanah N, Saghazadeh A, Rezaei N. Anosmia: a missing link in the neuroimmunology of coronavirus disease 2019 (COVID-19) [published online August 10, 2020]. Rev Neurosci.
    1. Bunyavanich S, Do A, Vicencio A. Nasal gene expression of angiotensin-converting enzyme 2 in children and adults. JAMA. 2020;323:2427-2429.
    1. Hoffmann M, Kleine-Weber H, Schroeder S, et al.. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell. 2020;181:271-280.
    1. Brann DH, Tsukahara T, Weinreb C, et al.. Non-neuronal expression of SARS-CoV-2 entry genes in the olfactory system suggests mechanisms underlying COVID-19–associated anosmia. Sci Adv. 2020;6:1-19.
    1. Bilinska K, Jakubowska P, Von Bartheld CS, Butowt R. Expression of the SARS-CoV-2 entry proteins, ACE2 and TMPRSS2, in cells of the olfactory epithelium: identification of cell types and trends with age. ACS Chem Neurosci. 2020;11:1555-1562.
    1. Butowt R, Bilinska K. SARS-CoV-2: Olfaction, brain infection, and the urgent need for clinical samples allowing earlier virus detection. ACS Chem Neurosci. 2020;11:1200-1203.
    1. Rombaux P, Mouraux A, Bertrand B, Nicolas G, Duprez T, Hummel T. Olfactory function and olfactory bulb volume in patients with postinfectious olfactory loss. Laryngoscope. 2006;116:436-439.
    1. Mueller A, Rodewald A, Reden J, Gerber J, von Kummer R, Hummel T. Reduced olfactory bulb volume in posttraumatic and postinfectious olfactory dysfunction. Neuroreport. 2005;16:475-478.
    1. Laurendon T, Radulesco T, Mugnier J, et al.. Bilateral transient olfactory bulb edema during COVID-19-related anosmia. Neurology. 2020;95:224-225.
    1. Sarbu N, Shih RY, Jones RV, Horkayne-Szakaly I, Oleaga L, Smirniotopoulos JG. White matter diseases with radiologic-pathologic correlation. Radiographics. 2016;36:1426-1447.
    1. Chetrit A, Lechien JR, Ammar A, et al.. Magnetic resonance imaging of COVID-19 anosmic patients reveals abnormalities of the olfactory bulb: preliminary prospective study [published online July 30, 2020]. J Infect.
    1. Mao L, Jin H, Wang M, et al.. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 2020;77:1-9.

Source: PubMed

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