Evaluation of children and adults with post-COVID-19 persistent smell, taste and trigeminal chemosensory disorders: A hospital based study

Sherifa Ahmed Hamed, Eman Bahaa Kamal-Eldeen, Mohamed Azzam Abdel-Razek Ahmed, Sherifa Ahmed Hamed, Eman Bahaa Kamal-Eldeen, Mohamed Azzam Abdel-Razek Ahmed

Abstract

Background: Smell disorders are the most frequent persistent coronavirus disease 2019 (COVID-19) complications.

Aim: To describe the patterns and characteristics of persistent smell and taste disorders in Egyptian patients.

Methods: Assessment was done to 185 patients (adults = 150, age: 31.41 ± 8.63 years; children = 35; age: 15.66 ± 1.63 years). Otolaryngology and neuropsychiatric evaluations were done. Measurements included: A clinical questionnaire (for smell and taste); sniffin' odor, taste and flavor identification tests and the Questionnaire of Olfactory Disorders-Negative Statements (sQOD-NS).

Results: Duration of disorders was 11.53 ± 3.97 ms (6-24 ms). Parosmia (n = 119; 64.32%) was developed months after anosmia (3.05 ± 1.87 ms). Objective testing showed anosmia in all, ageusia and flavor loss in 20% (n = 37) and loss of nasal and oral trigeminal sensations in 18% (n = 33) and 20% (n = 37), respectively. Patients had low scoring of sQOD-NS (11.41 ± 3.66). There were no specific differences in other demographics and clinical variables which could distinguish post-COVID-19 smell and taste disorders in children from adults.

Conclusion: The course of small and taste disorders are supportive of the nasal and oral neuronal compromises. Post-COVID-19 taste and trigeminal disorders were less frequent compared to smell disorders. Post-COVID-19 flavor disorders were solely dependent on taste and not smell disorders. There were no demographics, clinical variables at onset or specific profile of these disorders in children compared to adults.

Keywords: Ageusia; Anosmia; Parosmia; Post-COVID-19 complications; Quality of life; Trigeminal sensory loss.

Conflict of interest statement

Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.

©The Author(s) 2023. Published by Baishideng Publishing Group Inc. All rights reserved.

Figures

Figure 1
Figure 1
Demographics, laboratory and treatment characteristics of the studied patients. A: This study included 96 (51.9%) females and 89 (48.1%) males; B: The majority were rural residents (64.9%, n = 120), while 35.1% (n = 65) were urban residents; C: The majority were of low socioeconomic status (51.9%, n = 96), while 31.4% (n = 58) and 16.8% (n = 31) were of middle and high socioeconomic states, respectively; D: Investigations done by patients included serology and complete blood count (70.3%, n = 130, polymerase chain reaction (23.2%) and computed tomography-chest (17.3%, n = 32). While 39.5% (n = 73) did not do any investigations. E: The received pharmacotherapies and interventions to treat chemosensory disorders included local steroids (47.6%, n = 88), vitamins and supplements (46.5%, n = 86), olfactory training (22.7%, n = 42) and systemic steroids (12.4%, n = 23), while 22.7% of the patients (n = 42) did not receive any therapy. PCR: Polymerase chain reaction; CBC: Complete blood count; CT: Computed tomography.
Figure 2
Figure 2
General, systemic and ear, nose and throat manifestations of viral infection of the studied patients. ENT: Ear, nose and throat.
Figure 3
Figure 3
Manifestations of smell, taste, flavor and trigeminal sensory disorders of the studied patients.
Figure 4
Figure 4
Types of parosmia and dysgeusia/distortion of flavor in the studied patients.

References

    1. Koyama S, Ueha R, Kondo K. Loss of Smell and Taste in Patients With Suspected COVID-19: Analyses of Patients' Reports on Social Media. J Med Internet Res. 2021;23:e26459.
    1. Blomberg B, Mohn KG, Brokstad KA, Zhou F, Linchausen DW, Hansen BA, Lartey S, Onyango TB, Kuwelker K, Sævik M, Bartsch H, Tøndel C, Kittang BR Bergen COVID-19 Research Group, Cox RJ, Langeland N. Long COVID in a prospective cohort of home-isolated patients. Nat Med. 2021;27:1607–1613.
    1. Roge I, Smane L, Kivite-Urtane A, Pucuka Z, Racko I, Klavina L, Pavare J. Comparison of Persistent Symptoms After COVID-19 and Other Non-SARS-CoV-2 Infections in Children. Front Pediatr. 2021;9:752385.
    1. Yan Q, Qiu D, Liu X, Guo X, Hu Y. Prevalence of Smell or Taste Dysfunction Among Children With COVID-19 Infection: A Systematic Review and Meta-Analysis. Front Pediatr. 2021;9:686600.
    1. Buonsenso D, Martino L, Morello R, De Rose C, Valentini P. Chronic Olfactory Dysfunction in Children with Long COVID: A Retrospective Study. Children (Basel) 2022;9
    1. Niklassen AS, Draf J, Huart C, Hintschich C, Bocksberger S, Trecca EMC, Klimek L, Le Bon SD, Altundag A, Hummel T. COVID-19: Recovery from Chemosensory Dysfunction. A Multicentre study on Smell and Taste. Laryngoscope. 2021;131:1095–1100.
    1. Boscolo-Rizzo P, Hummel T, Hopkins C, Dibattista M, Menini A, Spinato G, Fabbris C, Emanuelli E, D'Alessandro A, Marzolino R, Zanelli E, Cancellieri E, Cargnelutti K, Fadda S, Borsetto D, Vaira LA, Gardenal N, Polesel J, Tirelli G. High prevalence of long-term olfactory, gustatory, and chemesthesis dysfunction in post-COVID-19 patients: a matched case-control study with one-year follow-up using a comprehensive psychophysical evaluation. Rhinology. 2021;59:517–527.
    1. Lechien JR, Vaira LA, Saussez S. Prevalence and 24-month recovery of olfactory dysfunction in COVID-19 patients: A multicentre prospective study. J Intern Med. 2023;293:82–90.
    1. 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. Prevalence and 6-month recovery of olfactory dysfunction: a multicentre study of 1363 COVID-19 patients. J Intern Med. 2021;290:451–461.
    1. American Academy of Otolaryngology–Head and Neck Surgery. Anosmia as a potential marker of COVID-19 infection - an update. Apr 1, 2020 [cited 6 June 2020]. Available from:
    1. American Academy of Otolaryngology-Head and Neck Surgery (AAO-HNS) Anosmia Reporting tool. 2020. [cited 28 September 2021]. Available from: .
    1. Chapurin N, Totten DJ, Chaballout B, Brennan J, Dennis S, Lubner R, Chowdhury NI, Turner JH, Trone T, Chandra RK. Differential olfactory outcomes in COVID-19: A large healthcare system population study. Int Forum Allergy Rhinol. 2022;12:108–111.
    1. Biadsee A, Dagan O, Ormianer Z, Kassem F, Masarwa S, Biadsee A. Eight-month follow-up of olfactory and gustatory dysfunctions in recovered COVID-19 patients. Am J Otolaryngol. 2021;42:103065.
    1. Estiri H, Strasser ZH, Brat GA, Semenov YR Consortium for Characterization of COVID-19 by EHR (4CE), Patel CJ, Murphy SN. Evolving phenotypes of non-hospitalized patients that indicate long COVID. BMC Med. 2021;19:249.
    1. Sasinka M, Plenta I, Pavlovic M, Izakovic V, Kaiserová E, Páleníková O, Stubna J. [Complications of immunosuppresive therapy in chronic nephropathies in children] Cesk Pediatr. 1976;31:122–126.
    1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814–1820.
    1. Bryche B, St Albin A, Murri S, Lacôte S, Pulido C, Ar Gouilh M, Lesellier S, Servat A, Wasniewski M, Picard-Meyer E, Monchatre-Leroy E, Volmer R, Rampin O, Le Goffic R, Marianneau P, Meunier N. Massive transient damage of the olfactory epithelium associated with infection of sustentacular cells by SARS-CoV-2 in golden Syrian hamsters. Brain Behav Immun. 2020;89:579–586.
    1. Sia SF, Yan LM, Chin AWH, Fung K, Choy KT, Wong AYL, Kaewpreedee P, Perera RAPM, Poon LLM, Nicholls JM, Peiris M, Yen HL. Pathogenesis and transmission of SARS-CoV-2 in golden hamsters. Nature. 2020;583:834–838.
    1. Letko M, Marzi A, Munster V. Functional assessment of cell entry and receptor usage for SARS-CoV-2 and other lineage B betacoronaviruses. Nat Microbiol. 2020;5:562–569.
    1. Yee KK, Costanzo RM. Changes in odor quality discrimination following recovery from olfactory nerve transection. Chem Senses. 1998;23:513–519.
    1. Iwema CL, Fang H, Kurtz DB, Youngentob SL, Schwob JE. Odorant receptor expression patterns are restored in lesion-recovered rat olfactory epithelium. J Neurosci. 2004;24:356–369.
    1. Pushpass RG, Pellicciotta N, Kelly C, Proctor G, Carpenter GH. Reduced Salivary Mucin Binding and Glycosylation in Older Adults Influences Taste in an In Vitro Cell Model. Nutrients. 2019;11
    1. World Health Organization. Laboratory testing for 2019 novel coronavirus (2019-nCoV) in suspected human cases. Interim guidance. Jan 17, 2020. [cited 3 April 2023]. Available from: .
    1. El-Gilany A, El-Wehady A, El-Wasify M. Updating and validation of the socioeconomic status scale for health research in Egypt. East Mediterr Health J. 2012;18:962–968.
    1. Rawal S, Hoffman HJ, Honda M, Huedo-Medin TB, Duffy VB. The Taste and Smell Protocol in the 2011-2014 US National Health and Nutrition Examination Survey (NHANES): Test-Retest Reliability and Validity Testing. Chemosens Percept. 2015;8:138–148.
    1. Oleszkiewicz A, Taut M, Sorokowska A, Radwan A, Kamel R, Hummel T. Development of the Arabic version of the "Sniffin' Sticks" odor identification test. Eur Arch Otorhinolaryngol. 2016;273:1179–1184.
    1. Mattos JL, Edwards C, Schlosser RJ, Hyer M, Mace JC, Smith TL, Soler ZM. A brief version of the questionnaire of olfactory disorders in patients with chronic rhinosinusitis. Int Forum Allergy Rhinol. 2019;9:1144–1150.
    1. Fortunato F, Martinelli D, Iannelli G, Milazzo M, Farina U, Di Matteo G, De Nittis R, Ascatigno L, Cassano M, Lopalco PL, Prato R. Self-reported olfactory and gustatory dysfunctions in COVID-19 patients: a 1-year follow-up study in Foggia district, Italy. BMC Infect Dis. 2022;22:77.
    1. Stephenson T, Allin B, Nugawela MD, Rojas N, Dalrymple E, Pinto Pereira S, Soni M, Knight M, Cheung EY, Heyman I CLoCk Consortium, Shafran R. Long COVID (post-COVID-19 condition) in children: a modified Delphi process. Arch Dis Child. 2022;107:674–680.
    1. Elvan-Tuz A, Karadag-Oncel E, Kiran S, Kanik-Yuksek S, Gulhan B, Hacimustafaoglu M, Ozdem-Alatas S, Kuyucu N, Ozdemir H, Egil O, Elmas-Bozdemir S, Polat M, Bursal-Duramaz B, Cem E, Apaydin G, Teksam O TURK-COVID-19-Anosmia Study Group; LAS VEGAS study investigators, PROVE Network and the Clinical Trial Network of the European Society of Anaesthesiology. Prevalence of Anosmia in 10.157 Pediatric COVID-19 Cases: Multicenter Study from Turkey. Pediatr Infect Dis J. 2022;41:473–477.
    1. Sorokowski P, Karwowski M, Misiak M, Marczak MK, Dziekan M, Hummel T, Sorokowska A. Sex Differences in Human Olfaction: A Meta-Analysis. Front Psychol. 2019;10:242.
    1. Moein ST, Hashemian SM, Mansourafshar B, Khorram-Tousi A, Tabarsi P, Doty RL. Smell dysfunction: a biomarker for COVID-19. Int Forum Allergy Rhinol. 2020;10:944–950.
    1. Pecoraro V, Negro A, Pirotti T, Trenti T. Estimate false-negative RT-PCR rates for SARS-CoV-2. A systematic review and meta-analysis. Eur J Clin Invest. 2022;52:e13706.
    1. Song WL, Zou N, Guan WH, Pan JL, Xu W. Clinical characteristics of COVID-19 in family clusters: a systematic review. World J Pediatr. 2021;17:355–363.
    1. Ilyicheva TN, Netesov SV, Gureyev VN. COVID-19, Influenza, and Other Acute Respiratory Viral Infections: Etiology, Immunopathogenesis, Diagnosis, and Treatment. Part I. COVID-19 and Influenza. Mol Gen Microbiol Virol. 2022;37:1–9.
    1. Cain WS, Murphy CL. Interaction between chemoreceptive modalities of odour and irritation. Nature. 1980;284:255–257.
    1. Schwab J, Jensen CD, Fjaeldstad AW. Sustained Chemosensory Dysfunction during the COVID-19 Pandemic. ORL J Otorhinolaryngol Relat Spec. 2021;83:209–218.
    1. Parma V, Ohla K, Veldhuizen MG, Niv MY, Kelly CE, Bakke AJ, Cooper KW, Bouysset C, Pirastu N, Dibattista M, Kaur R, Liuzza MT, Pepino MY, Schöpf V, Pereda-Loth V, Olsson SB, Gerkin RC, Rohlfs Domínguez P, Albayay J, Farruggia MC, Bhutani S, Fjaeldstad AW, Kumar R, Menini A, Bensafi M, Sandell M, Konstantinidis I, Di Pizio A, Genovese F, Öztürk L, Thomas-Danguin T, Frasnelli J, Boesveldt S, Saatci Ö, Saraiva LR, Lin C, Golebiowski J, Hwang LD, Ozdener MH, Guàrdia MD, Laudamiel C, Ritchie M, Havlícek J, Pierron D, Roura E, Navarro M, Nolden AA, Lim J, Whitcroft KL, Colquitt LR, Ferdenzi C, Brindha EV, Altundag A, Macchi A, Nunez-Parra A, Patel ZM, Fiorucci S, Philpott CM, Smith BC, Lundström JN, Mucignat C, Parker JK, van den Brink M, Schmuker M, Fischmeister FPS, Heinbockel T, Shields VDC, Faraji F, Santamaría E, Fredborg WEA, Morini G, Olofsson JK, Jalessi M, Karni N, D'Errico A, Alizadeh R, Pellegrino R, Meyer P, Huart C, Chen B, Soler GM, Alwashahi MK, Welge-Lüssen A, Freiherr J, de Groot JHB, Klein H, Okamoto M, Singh PB, Hsieh JW GCCR Group Author, Reed DR, Hummel T, Munger SD, Hayes JE. More Than Smell-COVID-19 Is Associated With Severe Impairment of Smell, Taste, and Chemesthesis. Chem Senses. 2020;45:609–622.
    1. Blankenship ML, Grigorova M, Katz DB, Maier JX. Retronasal Odor Perception Requires Taste Cortex, but Orthonasal Does Not. Curr Biol. 2019;29:62–69.e3.
    1. Chaudhari N, Roper SD. The cell biology of taste. J Cell Biol. 2010;190:285–296.
    1. Hannum ME, Koch RJ, Ramirez VA, Marks SS, Toskala AK, Herriman RD, Lin C, Joseph PV, Reed DR. Taste loss as a distinct symptom of COVID-19: a systematic review and meta-analysis. Chem Senses. 2022;47
    1. Chen B, Akshita J, Han P, Thaploo D, Kitzler HH, Hummel T. Aberrancies of Brain Network Structures in Patients with Anosmia. Brain Topogr. 2020;33:403–411.
    1. Ferreli F, Gaino F, Russo E, Di Bari M, Rossi V, De Virgilio A, Di Stadio A, Spriano G, Mercante G. Long-term olfactory dysfunction in COVID-19 patients: 18-month follow-up study. Int Forum Allergy Rhinol. 2022;12:1078–1080.
    1. Vaira LA, Hopkins C, Petrocelli M, Lechien JR, Chiesa-Estomba CM, Salzano G, Cucurullo M, Salzano FA, Saussez S, Boscolo-Rizzo P, Biglioli F, De Riu G. Smell and taste recovery in coronavirus disease 2019 patients: a 60-day objective and prospective study. J Laryngol Otol. 2020;134:703–709.
    1. Deng J, Zhou F, Hou W, Silver Z, Wong CY, Chang O, Huang E, Zuo QK. The prevalence of depression, anxiety, and sleep disturbances in COVID-19 patients: a meta-analysis. Ann N Y Acad Sci. 2021;1486:90–111.
    1. Bagheri S, Ghobadimoghadam S. Safety and Health Protection of Health Care Workers during the COVID-19 Pandemic. Int J Community Based Nurs Midwifery. 2020;8:362–363.
    1. Abdelhafiz AS, Ali A, Maaly AM, Mahgoub MA, Ziady HH, Sultan EA. Predictors of post-COVID symptoms in Egyptian patients: Drugs used in COVID-19 treatment are incriminated. PLoS One. 2022;17:e0266175.
    1. Maier EC, Saxena A, Alsina B, Bronner ME, Whitfield TT. Sensational placodes: neurogenesis in the otic and olfactory systems. Dev Biol. 2014;389:50–67.
    1. de Melo GD, Lazarini F, Levallois S, Hautefort C, Michel V, Larrous F, Verillaud B, Aparicio C, Wagner S, Gheusi G, Kergoat L, Kornobis E, Donati F, Cokelaer T, Hervochon R, Madec Y, Roze E, Salmon D, Bourhy H, Lecuit M, Lledo PM. COVID-19-related anosmia is associated with viral persistence and inflammation in human olfactory epithelium and brain infection in hamsters. Sci Transl Med. 2021;13
    1. Zazhytska M, Kodra A, Hoagland DA, Frere J, Fullard JF, Shayya H, McArthur NG, Moeller R, Uhl S, Omer AD, Gottesman ME, Firestein S, Gong Q, Canoll PD, Goldman JE, Roussos P, tenOever BR, Jonathan B Overdevest, Lomvardas S. Non-cell-autonomous disruption of nuclear architecture as a potential cause of COVID-19-induced anosmia. Cell. 2022;185:1052–1064.e12.
    1. Murai A, Iwata R, Fujimoto S, Aihara S, Tsuboi A, Muroyama Y, Saito T, Nishizaki K, Imai T. Distorted Coarse Axon Targeting and Reduced Dendrite Connectivity Underlie Dysosmia after Olfactory Axon Injury. eNeuro. 2016;3
    1. Lechien JR, Chiesa-Estomba CM, De Siati DR, Horoi M, Le Bon SD, Rodriguez A, Dequanter D, Blecic S, El Afia F, Distinguin L, Chekkoury-Idrissi Y, Hans S, Delgado IL, Calvo-Henriquez C, Lavigne P, Falanga C, Barillari MR, Cammaroto G, Khalife M, Leich P, Souchay C, Rossi C, Journe F, Hsieh J, Edjlali M, Carlier R, Ris L, Lovato A, De Filippis C, Coppee F, Fakhry N, Ayad T, Saussez S. 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. Genovese F, Tizzano M. Microvillous cells in the olfactory epithelium express elements of the solitary chemosensory cell transduction signaling cascade. PLoS One. 2018;13:e0202754.
    1. Xu H, Zhong L, Deng J, Peng J, Dan H, Zeng X, Li T, Chen Q. High expression of ACE2 receptor of 2019-nCoV on the epithelial cells of oral mucosa. Int J Oral Sci. 2020;12:8.
    1. Gadanec LK, McSweeney KR, Qaradakhi T, Ali B, Zulli A, Apostolopoulos V. Can SARS-CoV-2 Virus Use Multiple Receptors to Enter Host Cells? Int J Mol Sci. 2021;22
    1. Sun XL. The role of cell surface sialic acids for SARS-CoV-2 infection. Glycobiology. 2021;31:1245–1253.
    1. Choudhury A, Mukherjee S. In silico studies on the comparative characterization of the interactions of SARS-CoV-2 spike glycoprotein with ACE-2 receptor homologs and human TLRs. J Med Virol. 2020;92:2105–2113.

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