Top

Neurological Sciences

Published in:

Open Access 01-12-2021 | COVID-19 | COVID-19

Qualitative smell/taste disorders as sequelae of acute COVID-19

Authors: Tommaso Ercoli, Carla Masala, Ilenia Pinna, Gianni Orofino, Paolo Solla, Lorenzo Rocchi, Giovanni Defazio

Published in: Neurological Sciences | Issue 12/2021

Abstract

Background

Qualitative smell/taste disorders (such as phantosmia, parosmia, phantogeusia, and parageusia) have not yet been fully characterized in patients who had COVID-19, whereas quantitative disturbances (i.e., reduction/loss of smell/taste) have been widely investigated.

Objective

To simultaneously assess the presence of both quantitative and qualitative smell/taste dysfunctions in patients who suffered from COVID-19.

Methods

We enrolled 17 consecutive patients who suffered from COVID-19 over the last 6 months and 21 healthy controls, matched for sex and age. After a negative nasopharyngeal swab, the Sniffin’ Sticks Test and the Taste Strips were used to assess olfactory and taste function, respectively. At the same time, the presence of phantosmia, parosmia, phantogeusia, and parageusia was investigated with a standardized questionnaire.

Results

Qualitative disturbances of smell and/or taste were found in 6/17 (35.3%) patients. Phantosmia was reported in 2/17 (11.8%) patients and parosmia in 4/17 (23.5%). There were no significant differences in smell test scores between patients who reported phantosmia and/or parosmia and patients who did not. Phantogeusia was described in 3/17 (17.6%) patients, and parageusia was identified in 4/17 (23.5%) patients. All tested patients were normogeusic.

Conclusion

Around one-third of patients who recover from COVID-19 may have persistent qualitative dysfunction in smell/taste domains. Detection of phantogeusia in long-term COVID-19 patients represents a further novel finding. Further investigation is needed to better characterize the pathophysiology of phantosmia, parosmia, phantogeusia, and parageusia in patients who had COVID-19.

Vaira LA, Hopkins C, Salzano G, Petrocelli M, Melis A, Cucurullo M, Ferrari M, Gagliardini L, Pipolo C, Deiana G, Fiore V, De Vito A, Turra N, Canu S, Maglio A, Serra A, Bussu F, Madeddu G, Babudieri S et al (2020) Olfactory and gustatory function impairment in COVID-19 patients: Italian objective multicenter-study. Head Neck 42:1560–1569. https://doi.org/10.1002/hed.26269CrossRefPubMed

Lechien JR, Chiesa-Estomba CM, Hans S, Barillari MR, Jouffe L, Saussez S (2020) Loss of smell and taste in 2013 European patients with mild to moderate COVID-19. Ann Intern Med 173:672–675. https://doi.org/10.7326/M20-2428CrossRefPubMed

Hummel T, Whitcroft KL, Andrews P, Altundag A, Cinghi C, Costanzo RM, Damm M, Frasnelli J, Gudziol H, Gupta N, Haehne A, Holbrook E, Hong SC, Hornung D, Huttenbrink KB, Kamel R, Kobayashi M, Konstantinidis I, Landis BN et al Position paper on olfactory dysfunction. Rhinol J 54(2017):1–30. https://doi.org/10.4193/Rhino16.248

Carfì A, Bernabei R, Landi F (2020) Persistent symptoms in patients after acute COVID-19. JAMA 324:603. https://doi.org/10.1001/jama.2020.12603CrossRefPubMedPubMedCentral

Lechien JR, Chiesa-Estomba CM, Beckers E, Mustin V, Ducarme M, Journe F, Marchant A, Jouffe L, Barillari MR, Cammaroto G, Circiu MP, Hans S, Saussez S (2021) Prevalence and 6-month recovery of olfactory dysfunction: a multicentre study of 1363 COVID-19 patients. J Intern Med:1–11. https://doi.org/10.1111/joim.13209

National Institute for Health and Care Excellence, R.C. of G. Practitioners, H.I. Scotland (2020) COVID-19 rapid guideline : managing the long-term effects of COVID-19, NICE Guidel. 1–35.

İşlek A, Balcı MK (2021) Phantosmia with COVID-19 related olfactory dysfunction: report of nine case. Indian J Otolaryngol Head Neck Surg. https://doi.org/10.1007/s12070-021-02505-z

Muroni A, Murru MR, Sechi M, Ercoli T, Marrosu F, Bentivoglio AR, Petracca M, Maria Scaglione CL, Soliveri P, Cocco E, Pedron M, Murgia M, Deriu M, Cuccu S, Ulgheri L, Zuccato C, Defazio G (2020) Prevalence of Huntington’s disease in Southern Sardinia, Italy. Park Relat Disord 80:54–57. https://doi.org/10.1016/j.parkreldis.2020.09.011CrossRef

Ercoli T, Lutzoni L, Orofino G, Muroni A, Defazio G (2021) Functional neurological disorder after COVID-19 vaccination. Neurol Sci:2–3. https://doi.org/10.1007/s10072-021-05504-8

10.

World Health Organization, Clinical management of COVID-19: interim guidance, 27 May 2020, World Health Organization, Geneva PP - Geneva, n.d. https://apps.who.int/iris/handle/10665/332196

11.

Howell J, Costanzo RM, Reiter ER (2018) Head trauma and olfactory function. World J Otorhinolaryngol - Head Neck Surg 4:39–45. https://doi.org/10.1016/j.wjorl.2018.02.001CrossRefPubMedPubMedCentral

12.

Defazio G, Fabbrini G, Erro R, Albanese A, Barone P, Zibetti M, Esposito M, Pellicciari R, Avanzino L, Bono F, Eleopra R, Bertolasi L, Altavista MC, Cotelli MS, Ceravolo R, Scaglione C, Bentivoglio AR, Cossu G, Moja MC et al (2020) Does acute peripheral trauma contribute to idiopathic adult-onset dystonia? Parkinsonism Relat Disord 71:40–43. https://doi.org/10.1016/j.parkreldis.2020.01.002CrossRefPubMed

13.

Pellegrino R, Farruggia MC, Small DM, Veldhuizen MG (2021) Post-traumatic olfactory loss and brain response beyond olfactory cortex. Sci Rep 11:4043. https://doi.org/10.1038/s41598-021-83621-2CrossRefPubMedPubMedCentral

14.

Tinazzi M, Geroin C, Erro R, Marcuzzo E, Cuoco S, Ceravolo R, Mazzucchi S, Pilotto A, Padovani A, Romito LM, Eleopra R, Zappia M, Nicoletti A, Dallocchio C, Arbasino C, Bono F, Pascarella A, Demartini B, Gambini O, Modugno N, Olivola E, Bonanni L, Antelmi E, Zanolin E, Albanese A, Ferrazzano G, Micco R, Lopiano L, Calandra-Buonaura G, Petracca M, Esposito M, Pisani A, Manganotti P, Stocchi F, Coletti Moja M, Antonini A, Ercoli T, Morgante F (2021) Functional motor disorders associated with other neurological diseases: beyond the boundaries of “organic” neurology. Eur J Neurol 1–7. https://doi.org/10.1111/ene.14674.

15.

Tinazzi M, Geroin C, Marcuzzo E, Cuoco S, Ceravolo R, Mazzucchi S, Pilotto A, Padovani A, Romito LM, Eleopra R, Zappia M, Nicoletti A, Dallocchio C, Arbasino C, Bono F, Magro G, Demartini B, Gambini O, Modugno N et al (2021) Functional motor phenotypes: to lump or to split? J Neurol. https://doi.org/10.1007/s00415-021-10583-w

16.

Herr T, Hummel T, Vollmer M, Willert C, Veit B, Gamain J, Fleischmann R, Lehnert B, Mueller JU, Stenner A, Kronenbuerger M (2020) Smell and taste in cervical dystonia. J Neural Transm 127:347–354. https://doi.org/10.1007/s00702-020-02156-4CrossRefPubMed

17.

Doty RL (2012) Olfaction in Parkinson’s disease and related disorders. Neurobiol Dis. https://doi.org/10.1016/j.nbd.2011.10.026

18.

Tinazzi M, Erro R, Mascia MM, Esposito M, Ercoli T, Ferrazzano G, Di Biasio F, Pellicciari R, Eleopra R, Bono F, Bertolasi L, Barone P, Scaglione CLM, Pisani A, Altavista MC, Cotelli MS, Ceravolo R, Cossu G, Zibetti M et al (2020) Demographic and clinical determinants of neck pain in idiopathic cervical dystonia. J Neural Transm 127:1435–1439. https://doi.org/10.1007/s00702-020-02245-4CrossRefPubMed

19.

Liu G, Zong G, Doty RL, Sun Q (2016) Prevalence and risk factors of taste and smell impairment in a nationwide representative sample of the US population: a cross-sectional study. BMJ Open 6:e013246. https://doi.org/10.1136/bmjopen-2016-013246CrossRefPubMedPubMedCentral

20.

Solla P, Masala C, Liscia A, Piras R, Ercoli T, Fadda L, Hummel T, Haenher A, Defazio G (2019) Sex-related differences in olfactory function and evaluation of possible confounding factors among patients with Parkinson’s disease. J Neurol. https://doi.org/10.1007/s00415-019-09551-2

21.

Landis BN, Welge-Luessen A, Brämerson A, Bende M, Mueller CA, Nordin S, Hummel T (2009) “Taste strips”—a rapid, lateralized, gustatory bedside identification test based on impregnated filter papers. J Neurol 256:242–248. https://doi.org/10.1007/s00415-009-0088-yCrossRefPubMed

22.

Solla P, Masala C, Pinna I, Ercoli T, Loy F, Orofino G, Fadda L, Defazio G (2021) Frequency and determinants of olfactory hallucinations in Parkinson’s disease patients. Brain Sci 11:841. https://doi.org/10.3390/brainsci11070841CrossRefPubMedPubMedCentral

23.

Defazio G, Ercoli T, Erro R, Pellicciari R, Mascia MM, Fabbrini G, Albanese A, Lalli S, Eleopra R, Barone P, Marchese R, Ceravolo R, Scaglione C, Liguori R, Esposito M, Bentivoglio AR, Bertolasi L, Altavista MC, Bono F et al (2020) Idiopathic non-task-specific upper limb dystonia, a neglected form of dystonia. Mov Disord 35:2038–2045. https://doi.org/10.1002/mds.28199CrossRefPubMed

24.

Ercoli T, Defazio G, Muroni A (2019) Cerebellar syndrome associated with thyroid disorders. Cerebellum 18:932–940. https://doi.org/10.1007/s12311-019-01059-9CrossRefPubMed

25.

Dagostino S, Ercoli T, Gigante AF, Pellicciari R, Fadda L, Defazio G (2019) Sensory trick in upper limb dystonia. Park Relat Disord. https://doi.org/10.1016/j.parkreldis.2019.01.006

26.

Mastrangelo A, Bonato M, Cinque P (2021) Smell and taste disorders in COVID-19: from pathogenesis to clinical features and outcomes. Neurosci Lett 748:135694. https://doi.org/10.1016/j.neulet.2021.135694CrossRefPubMedPubMedCentral

27.

Nalbandian A, Sehgal K, Gupta A, Madhavan MV, McGroder C, Stevens JS, Cook JR, Nordvig AS, Shalev D, Sehrawat TS, Ahluwalia N, Bikdeli B, Dietz D, Der-Nigoghossian C, Liyanage-Don N, Rosner GF, Bernstein EJ, Mohan S, Beckley AA et al (2021) Post-acute COVID-19 syndrome. Nat Med 27:601–615. https://doi.org/10.1038/s41591-021-01283-zCrossRefPubMed

28.

Bonfils P, Avan P, Faulcon P, Malinvaud D (2005) Distorted odorant perception. Arch Otolaryngol Neck Surg 131:107. https://doi.org/10.1001/archotol.131.2.107CrossRef

29.

Masala C, Käehling C, Fall F, Hummel T (2019) Correlation between olfactory function, trigeminal sensitivity, and nasal anatomy in healthy subjects. Eur Arch Oto-Rhino-Laryngol 276:1649–1654. https://doi.org/10.1007/s00405-019-05367-yCrossRef

30.

Douek E (1970) Some abnormalities of smell. J Laryngol Otol 84:1185–1191. https://doi.org/10.1017/S0022215100072935CrossRefPubMed

31.

RB GJG, Catalanotto FA (1986) Clinical characteristics of patients with taste and smell disorders. In: Meiselman HL, Rivlin RS (eds) Ed. Clin. Meas. OfTaste Smell. Macmillan, NewYork, pp 451–466

32.

Ciurleo R, De Salvo S, Bonanno L, Marino S, Bramanti P, Caminiti F (2020) Parosmia and neurological disorders: a neglected association. Front Neurol 11:1–7. https://doi.org/10.3389/fneur.2020.543275CrossRef

33.

Ren AL, Digby RJ, Needham EJ (2021) Neurological update: COVID-19. J Neurol. https://doi.org/10.1007/s00415-021-10581-y

34.

Chiu A, Fischbein N, Wintermark M, Zaharchuk G, Yun PT, Zeineh M (2021) COVID-19-induced anosmia associated with olfactory bulb atrophy. Neuroradiology 63:147–148. https://doi.org/10.1007/s00234-020-02554-1CrossRefPubMed

35.

Kandemirli SG, Altundag A, Yildirim D, Tekcan Sanli DE, Saatci O (2021) Olfactory bulb MRI and paranasal sinus CT findings in persistent COVID-19 anosmia. Acad Radiol 28:28–35. https://doi.org/10.1016/j.acra.2020.10.006CrossRefPubMed

36.

Hajjij A, Benslima N, Aasfara J, Bensouda H, Mahi M, Benariba F (2021) MRI of the olfactory tract in a case of post-COVID-19 persistent anosmia. Integr J Med Sci 8:1–3. https://doi.org/10.15342/ijms.2021.406CrossRef

37.

Torabi A, Mohammadbagheri E, Akbari Dilmaghani N, Bayat AH, Fathi M, Vakili K, Alizadeh R, Rezaeimirghaed O, Hajiesmaeili M, Ramezani M, Simani L, Aliaghaei A (2020) Proinflammatory cytokines in the olfactory mucosa result in COVID-19 induced anosmia. ACS Chem Neurosci 11:1909–1913. https://doi.org/10.1021/acschemneuro.0c00249CrossRefPubMed

38.

Belvisi D, Pellicciari R, Fabbrini A, Costanzo M, Pietracupa S, De Lucia M, Modugno N, Magrinelli F, Dallocchio C, Ercoli T, Terravecchia C, Nicoletti A, Solla P, Fabbrini G, Tinazzi M, Berardelli A, Defazio G (2020) Risk factors of Parkinson disease: simultaneous assessment, interactions, and etiologic subtypes. Neurology 95:e2500–e2508. https://doi.org/10.1212/WNL.0000000000010813CrossRefPubMedPubMedCentral

39.

Merello M, Bhatia KP, Obeso JA (2021) SARS-CoV-2 and the risk of Parkinson’s disease: facts and fantasy. Lancet Neurol 20:94–95. https://doi.org/10.1016/S1474-4422(20)30442-7CrossRefPubMed

40.

Makhoul K, Jankovic J (2021) Parkinson’s disease after COVID-19. J Neurol Sci 422:117331. https://doi.org/10.1016/j.jns.2021.117331CrossRefPubMed

Title: Qualitative smell/taste disorders as sequelae of acute COVID-19
Authors: Tommaso Ercoli
Carla Masala
Ilenia Pinna
Gianni Orofino
Paolo Solla
Lorenzo Rocchi
Giovanni Defazio
Publication date: 01-12-2021
Publisher: Springer International Publishing
Keywords: COVID-19
Taste Disorder
Anosmia
Published in: Neurological Sciences / Issue 12/2021
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI: https://doi.org/10.1007/s10072-021-05611-6

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Qualitative smell/taste disorders as sequelae of acute COVID-19

Abstract

Background

Objective

Methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Background

Objective

Methods

Results

Conclusion

Please log in to get access to this content

Other articles of this Issue 12/2021

A case of adult-onset leukoencephalopathy with axonal spheroids and pigmented glia (ALSP) with a high antinuclear antibody titer

Neuropsychiatric symptoms among young stroke survivors—frequency, patterns, and associated factors

A case of meningoencephalocele in the nasal cavity 6 years after skull base fracture

Efficacy of aspirin for sporadic vestibular schwannoma: a meta-analysis

Inter-individual variability in disease expression: the Tudor-Churchill spectrum

Face pareidolia is associated with right striatal dysfunction in drug-naïve patients with Parkinson’s disease