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Systematic Review

Anosmia and dysgeusia in SARS-CoV-2 infection: incidence and effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - a systematic review and meta-analysis

[version 1; peer review: 2 approved, 1 approved with reservations]
Endang Mutiawati
https://orcid.org/0000-0002-5116-2881
1,2, Marhami Fahriani
https://orcid.org/0000-0003-0452-3485
3, Sukamto S. Mamada
https://orcid.org/0000-0002-7813-2164
4, [...] Jonny Karunia Fajar
https://orcid.org/0000-0002-0309-5813
3,5, Andri Frediansyah
https://orcid.org/0000-0003-4923-2948
6, Helnida Anggun Maliga
https://orcid.org/0000-0002-3702-6306
7, Muhammad Ilmawan
https://orcid.org/0000-0002-9459-609X
7, Talha Bin Emran
https://orcid.org/0000-0003-3188-2272
8, Youdiil Ophinni
https://orcid.org/0000-0001-9443-1538
9, Ichsan Ichsan
https://orcid.org/0000-0002-8903-9977
3,10, Nasrul Musadir1,2, Ali A. Rabaan
https://orcid.org/0000-0002-6774-9847
11, Kuldeep Dhama
https://orcid.org/0000-0001-7469-4752
12, Syahrul Syahrul
https://orcid.org/0000-0002-7873-8713
1,2, Firzan Nainu
https://orcid.org/0000-0003-0989-4023
4, Harapan Harapan
https://orcid.org/0000-0001-7630-8413
3,10,13
Endang Mutiawati
https://orcid.org/0000-0002-5116-2881
1,2, Marhami Fahriani
https://orcid.org/0000-0003-0452-3485
3, [...] Sukamto S. Mamada
https://orcid.org/0000-0002-7813-2164
4, Jonny Karunia Fajar
https://orcid.org/0000-0002-0309-5813
3,5, Andri Frediansyah
https://orcid.org/0000-0003-4923-2948
6, Helnida Anggun Maliga
https://orcid.org/0000-0002-3702-6306
7, Muhammad Ilmawan
https://orcid.org/0000-0002-9459-609X
7, Talha Bin Emran
https://orcid.org/0000-0003-3188-2272
8, Youdiil Ophinni
https://orcid.org/0000-0001-9443-1538
9, Ichsan Ichsan
https://orcid.org/0000-0002-8903-9977
3,10, Nasrul Musadir1,2, Ali A. Rabaan
https://orcid.org/0000-0002-6774-9847
11, Kuldeep Dhama
https://orcid.org/0000-0001-7469-4752
12, Syahrul Syahrul
https://orcid.org/0000-0002-7873-8713
1,2, Firzan Nainu
https://orcid.org/0000-0003-0989-4023
4, Harapan Harapan
https://orcid.org/0000-0001-7630-8413
3,10,13
PUBLISHED 21 Jan 2021
Author details Author details
OPEN PEER REVIEW
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This article is included in the Emerging Diseases and Outbreaks gateway.

This article is included in the Coronavirus collection.

Abstract

Background: The present study aimed to determine the global prevalence of anosmia and dysgeusia in coronavirus disease 2019 (COVID-19) patients and to assess their association with severity and mortality of COVID-19. Moreover, this study aimed to discuss the possible pathobiological mechanisms of anosmia and dysgeusia in COVID-19.
Methods: Available articles from PubMed, Scopus, Web of Science, and preprint databases (MedRxiv, BioRxiv, and Researchsquare) were searched on November 10th, 2020. Data on the characteristics of the study (anosmia, dysgeusia, and COVID-19) were extracted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline. Newcastle–Ottawa scale was used to assess research quality. Moreover, the pooled prevalence of anosmia and dysgeusia were calculated, and the association between anosmia and dysgeusia in presence of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) was assessed using the Z test.
Results: Out of 32,142 COVID-19 patients from 107 studies, anosmia was reported in 12,038 patients with a prevalence of 38.2% (95% CI: 36.5%, 47.2%); whereas, dysgeusia was reported in 11,337 patients out of 30,901 COVID-19 patients from 101 studies, with prevalence of 36.6% (95% CI: 35.2%, 45.2%), worldwide. Furthermore, the prevalence of anosmia was 10.2-fold higher (OR: 10.21; 95% CI: 6.53, 15.96, p < 0.001) and that of dysgeusia was 8.6-fold higher (OR: 8.61; 95% CI: 5.26, 14.11, p < 0.001) in COVID-19 patients compared to those with other respiratory infections or COVID-19 like illness. To date, no study has assessed the association of anosmia and dysgeusia with severity and mortality of COVID-19.
Conclusion: Anosmia and dysgeusia are prevalent in COVID-19 patients compared to those with the other non-COVID-19 respiratory infections. Several possible mechanisms have been hypothesized; however, future studies are warranted to elucidate the definitive mechanisms of anosmia and dysgeusia in COVID-19.
Protocol registration: PROSPERO CRD42020223204.

Keywords

anosmia, COVID-19, dysgeusia, predictor, SARS-CoV-2

Corresponding author: Endang Mutiawati
Competing interests: No competing interests were disclosed.
Grant information: The author(s) declared that no grants were involved in supporting this work.
Copyright:  © 2021 Mutiawati E et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
How to cite: Mutiawati E, Fahriani M, Mamada SS et al. Anosmia and dysgeusia in SARS-CoV-2 infection: incidence and effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - a systematic review and meta-analysis [version 1; peer review: 2 approved, 1 approved with reservations]. F1000Research 2021, 10:40 (https://doi.org/10.12688/f1000research.28393.1) First published: 21 Jan 2021, 10:40 (https://doi.org/10.12688/f1000research.28393.1) Latest published: 21 Jan 2021, 10:40 (https://doi.org/10.12688/f1000research.28393.1)

Introduction

Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), was initially identified in late December 2019 in Wuhan, Hubei Province, Republic of China1,2. This viral pandemic rapidly spread worldwide, infecting more than 60 million people, causing more than 1 million deaths3, and severely affecting the global healthcare system4,5. Several drugs have been repurposed for treating COVID-195-9; however, no drug has been recommended or approved by the World Health Organization (WHO). The common symptoms of COVID-19 include dry cough, fever, dyspnea, fatigue, anorexia, diarrhea, chest pain, headache, and muscle ache10,11. In particular, two manifestations have been increasingly identified among asymptomatic people that later tested positive for the presence of SARS-CoV-2: anosmia and dysgeusia12. Remarkably, previous studies reported that these olfactory issues were reported in 11.8% of COVID-19 cases before other symptoms occured13-15.

Anosmia, a severe condition of hyposmia, is a part of olfactory dysfunction where the person is unable to sense smell or detect odor16. Dysgeusia is a sensory dysfunction where the individual loses the perception of taste17. The British Association of Otorhinolaryngology reported that both dysfunctions varied from 3-20% among COVID-19 patients18. A previous study among 42 patients revealed that more than a third presented anosmia and dysgeusia19. A higher percentage of anosmia and dysgeusia cases were also reported20. Furthermore, another study reported that anosmia in COVID-19 is related to the enlargement of bilateral olfactory bulb edema21.

This evidence may be crucial in the present COVID-19 pandemic. As the real-time reverse transcriptase polymerase chain reaction (RT-PCR) test has certain limitations for screening, the manifestation of anosmia and dysgeusia could be used as an early warning for practitioners or clinicians to build a rationale to reach a firm conclusion on patients with SARS-CoV-2 infection22,23. Additionally, a recent study reported that anosmia and dysgeusia are among the earliest symptoms observed in COVID-19 patients24; however, in-depth analysis of this dysfunction and its relation to the pathogenesis, severity, and mortality of COVID-19 is missing from the literature. Thus, the present study aimed to summarize the global evidence of anosmia and dysgeusia among COVID-19 patients, in order to assess their association with the severity and mortality of the disease, and provide a comprehensive review related to the possible pathogenesis of anosmia and dysgeusia in SARS-CoV-2 infection.

Methods

Registration and protocol

To comprehensively calculate the cumulative prevalence of anosmia and dysgeusia in SARS-CoV-2 infection worldwide, a systematic review was conducted following guideline of Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)25. The protocol of this systematic review has been registered at PROSPERO (CRD42020223204).

Eligibility criteria of studies

All articles reporting anosmia and dysgeusia as the symptom of COVID-19 were included. COVID-19 case was defined by a positive RT-PCR for SARS-CoV-2 from either nasopharyngeal swab, oropharyngeal swab, bronchoalveolar lavage, or cerebrospinal fluid. All cross-sectional, retrospective, and prospective studies that randomly sampled COVID-19 cases from community or hospitals were considered eligible; whereas case reports and case series, including all editorials, reviews, and commentaries, were excluded. Studies targeting specific groups such as pregnant females, children, and other groups, were excluded. Only articles written in English during 2019-2020 were included.

Information sources and search strategy

Three bibliographical databases (PubMed, Scopus, and Web of Science) and three preprint databases (MedRxiv, BioRxiv, and Researchsquare) were used to identify the potential articles (as of November 10th, 2020). The search criteria were as follows. PubMed ([Title] “SARS-CoV-2” OR “COVID-19” OR “Wuhan coronavirus” OR “Wuhan virus” OR “novel coronavirus” OR “nCoV” OR “severe acute respiratory syndrome coronavirus 2” OR “coronavirus disease 2019 virus” OR “2019-nCoV” OR “2019 novel coronavirus” OR “severe acute respiratory syndrome coronavirus 2” OR “coronavirus” OR “coronaviruses” OR “SARS 2” OR “2019-nCoV acute respiratory disease” OR “novel coronavirus pneumonia” OR “COVID”) AND ([All] “Anosmia” OR “smell loss” OR “smell dysfunction” OR “smell impairment” OR “hyposmia” OR “dysosmia” OR “olfactory dysfunction” OR “olfactory disorder”) AND (“dysgeusia” OR “taste loss” OR “taste dysfunction” OR “taste impairment” OR “gustatory dysfunction” OR “gustatory disorder” OR “hypogeusia” OR “ageusia”). Scopus ([Title] “SARS-CoV-2” OR “COVID-19” OR “Wuhan coronavirus” OR “Wuhan virus” OR “novel coronavirus” OR “nCoV” OR “severe acute respiratory syndrome coronavirus 2” OR “coronavirus disease 2019 virus” OR “2019-nCoV” OR “2019 novel coronavirus” OR “severe acute respiratory syndrome coronavirus 2” OR “coronavirus” OR “coronaviruses” OR “SARS 2” OR “2019-nCoV acute respiratory disease” OR “novel coronavirus pneumonia” OR “COVID”) AND ([All] “Anosmia” OR “smell loss” OR “smell dysfunction” OR “smell impairment” OR “hyposmia” OR “dysosmia” OR “olfactory dysfunction” OR “olfactory disorder”) AND (“dysgeusia” OR “taste loss” OR “taste dysfunction” OR “taste impairment” OR “gustatory dysfunction” OR “gustatory disorder” OR “hypogeusia” OR “ageusia”). Web of Science ([Title] “SARS-CoV-2” OR “COVID-19” OR “Wuhan coronavirus” OR “Wuhan virus” OR “novel coronavirus” OR “nCoV” OR “severe acute respiratory syndrome coronavirus 2” OR “coronavirus disease 2019 virus” OR “2019-nCoV” OR “2019 novel coronavirus” OR “severe acute respiratory syndrome coronavirus 2” OR “coronavirus” OR “coronaviruses” OR “SARS 2” OR “2019-nCoV acute respiratory disease” OR “novel coronavirus pneumonia” OR “COVID”) AND ([All] “Anosmia” OR “smell loss” OR “smell dysfunction” OR “smell impairment” OR “hyposmia” OR “dysosmia” OR “olfactory dysfunction” OR “olfactory disorder”) AND ([All] “dysgeusia” OR “taste loss” OR “taste dysfunction” OR “taste impairment” OR “gustatory dysfunction” OR “gustatory disorder” OR “hypogeusia” OR “ageusia”).

Moreover, we searched the preprint servers MedRxiv, BioRxiv, and Researchsquare for non-peer-reviewed articles. Data were extracted from the articles as well as supplementary materials. Reference lists from the eligible articles were retrieved for further relevant studies.

Study selection and data extraction

The information of identified articles was imported into EndNote X9 (Thompson Reuters, Philadelphia, PA, USA). Duplicates between databases were removed. To identify eligible studies, the retrieved articles were screened based on title and abstract. The potentially eligible studies were then fully reviewed by two authors (MF and JKF). After reviewing the full texts, the eligibility of each study was decided.

Information of study characteristics, study site, study design, number of patients with anosmia, number of patients with dysgeusia, and COVID-19 characteristics such as number of patients, severity, and outcome were collected.

Outcomes

The primary outcomes were: (a) the global incidence of anosmia in COVID-19 patients; (b) the global incidence of dysgeusia in COVID-19 patients; (c) the association of anosmia with the severity of COVID-19; (d) the association of dysgeusia with the severity of COVID-19; (e) the association of anosmia with mortality of COVID-19; and (f) the association of dysgeusia with mortality of COVID-19. Moreover, this review was conducted to provide the possible pathogenesis of anosmia and dysgeusia in SARS-CoV-2 infection.

Data synthesis

The cumulative prevalence rate of anosmia and dysgeusia was calculated for COVID-19 cases by dividing the number of COVID-19 cases with anosmia by the total number of COVID-19 cases with and without anosmia, and was expressed as a percentage (%) with 95% confidence intervals (95% CI). Pooled odds ratios (OR) and 95% CI were calculated to assess the association of anosmia and the occurrence of SARS-CoV-2 compared to non-SARS-CoV-2 respiratory infections. The same method was used for dysgeusia. The pooled OR and 95% CI were presented in a forest plot.

Risk of bias assessment

Critical assessment was conducted for the study setting and diagnosis of SARS-CoV-2 to reduce the bias. The Newcastle-Ottawa scale (NOS)26 was used as critical appraisals to assess the quality of eligible studies. Prior to analysis, gathered data from studies were evaluated for heterogeneity and potential publication bias.

Statistical analysis

To assess the association between anosmia or dysgeusia and the presence of SARS-CoV-2, Z test was performed (p < 0.05 was considered statistically significant). Q test was used to evaluate the heterogeneity among studies, and the data with heterogeneity was analyzed using a random effect model. The reporting and publication bias were assessed using Egger’s test and a funnel plot (p < 0.05 was considered having potential for publication bias). The data were analyzed using Review Manager version 5.327.

Results

Study eligibility results

In total, 691 articles (660 reviewed articles and 31 preprint articles) were identified through the databases; of these, 182 articles were removed as duplicates. An additional 287 articles were excluded following a screening process of the titles and abstracts due to irrelevant studies, leaving 222 references (Figure 1). Full-texts of the remaining 222 references were retrieved and screened for eligibility, and this process excluded an additional 115 references as the inclusion criteria was not met. This exclusion included articles with no access28,29, RT-PCR not clearly stated in the text30-45, case reports46-97, case seriess98-113, repeated datasetss114-118, and studies in specific groups119-130. A complete assessment was conducted for 107 references.

f24054be-abc2-4d08-be8c-1ece881b6f7d_figure1.gif

Figure 1. Flowchart of the result of literature search according to PRISMA.

The meta-analysis included 107 studies to calculate the prevalence of anosmia in COVID-19 patients. Additionally, 6 studies were excluded while calculating the prevalence of dysgeusia in COVID-19, thus leaving 101 eligible studies. In total, 20 and 16 studies were included to assess the association of anosmia and dysgeusia with the COVID-19 occurrence, respectively.

The prevalence of anosmia and dysgeusia in COVID-19

To calculate the prevalence of anosmia in COVID-19 cases, 107 studies were included comprising 32,142 COVID-19 patients, and anosmia was reported in 12,038 patients with a global pooled prevalence of 38.2% (95% CI: 36.5%, 47.2%). The list of the studies and the prevalence of anosmia in each study are presented in Table 1.

In total, 30,901 COVID-19 patients from 101 studies were included to calculate the prevalence of dysgeusia in COVID-19. Dysgeusia was identified in 11,337 out of 30,901 COVID-19 patients resulting in a cumulative prevalence of 36.6% (95% CI: 35.2%, 45.2%). The individual studies and the prevalence of dysgeusia from each study are listed in Table 2.

Table 1.

The prevalence of anosmia among COVID-19 patients around the globe.

Study DesignCountryCOVID-19Prevalence (%)95%CIRef
AnosmiaTotal
RetrospectiveSingapore5330517.3813.12, 21.63131
ProspectiveTurkey92931.0314.20, 47.87119
ProspectiveFrance3122513.789.27, 18.28132
Case controlSpain257931.6521.39, 41.90133
RetrospectiveTaiwan4232113.089.39, 16.77134
Case controlCanada6913451.4943.03, 59.95135
Case controlUS6010159.4149.83, 68.98136
RetrospectiveItaly132136.102.89, 9.32137
Cross sectionalUS405967.8055.87, 79.72138
Cross sectionalSpain13819770.0563.65, 76.45139
Cross sectionalBrazil53965582.2979.37, 85.21140
RetrospectivePakistan43013.331.17, 25.50141
RetrospectiveSpain9037524.0019.68, 28.32142
ObservationalEurope997142070.2167.83, 72.59143
ProspectiveSouth Korea6817239.5332.23, 46.84144
ProspectiveFrance6219731.4724.99, 37.96145
RetrospectiveUSA4525117.9313.18, 22.67146
RetrospectiveItaly142263.6443.53, 83.74147
Cross sectionalIndia6223026.9621.22, 32.69148
Cross sectionalUS2216813.107.99, 18.20149
Cross sectionalHongkong398346.9936.25, 57.73150
RetrospectiveFrance5411447.3738.20, 56.53151
RetrospectiveJapan193259.3842.36, 76.39152
ProspectiveTaiwan7821735.9429.56, 42.33153
ProspectiveTurkey1817210.475.89, 15.04154
RetrospectiveItaly178420.2411.65, 28.83155
ProspectiveItaly4010837.0427.93, 46.14156
Cross sectionalEgypt809683.3375.88, 90.79157
RetrospectiveKenya27978735.4532.11, 38.79158
Cross sectionalGermany297339.7328.50, 50.95159
ProspectiveUK1402.500.00, 7.34160
Cross sectionalIndia12165518.4715.50, 21.45161
Cross sectionalFrance14029946.8241.17, 52.48162
RetrospectiveFrance5411447.3738.20, 56.53163
ProspectiveIran229223.9115.20, 32.63164
RetrospectiveUS5850911.398.63, 14.16165
Cross sectionalSpain284562.2248.06, 76.39166
Cross sectionalBrazil287338.3627.20, 49.51167
ProspectiveTurkey15726259.9253.99, 65.86168
RetrospectiveFrance175530.9118.70, 43.12169
Cross sectionalUK34457959.4155.41, 63.41170
RetrospectiveSomalia246040.0027.60, 52.40171
ProspectiveUS184242.8627.89, 57.82172
ProspectiveTurkey3314323.0816.17, 29.98173
RetrospectiveChina112145.142.18, 8.10174
RetrospectiveBrazil812080.660.20, 1.12175
RetrospectiveUS3506.000.00, 12.58176
Cross sectionalIndia263916.654.18, 9.12177
RetrospectiveChina348639.5329.20, 49.87178
RetrospectiveFrance377052.8641.16, 64.55179
Cross sectionalItaly345462.9650.08, 75.84180
RetrospectiveUK8014156.7448.56, 64.92181
ProspectiveItaly447261.1149.85, 72.37182
RetrospectiveBelgium274757.4543.31, 71.58183
Case controlIsrael31618.750.00, 37.88184
Case controlTurkey508161.7351.14, 72.31185
RetrospectiveChina, France Germany15439439.0934.27, 43.90186
RetrospectiveMalaysia3114521.3814.71, 28.05187
RetrospectiveEurope35741785.6182.24, 88.98188
RetrospectiveItaly2910029.0020.11, 37.89189
CohortItaly12615183.4477.52, 89.37190
Cross sectionalSwitzerland6310361.1751.75, 70.58191
Case controlItaly264360.4745.85, 75.08192
RetrospectiveGermany809187.9181.21, 94.61193
ProspectiveIsrael7811269.6461.13, 78.16194
CohortIndia2922512.898.51, 17.27195
Case controlTurkey4411637.9329.10, 46.76196
RetrospectiveTurkey5515535.4827.95, 43.02197
RetrospectiveFrance1442373738.5937.03, 40.15198
RetrospectiveSouth Korea53281.520.20, 2.85199
ProspectiveUS234650.0035.55, 64.45200
Cross sectionalSpain465879.3168.89, 89.74201
Cross sectionalGermany223464.7148.64, 80.77202
CohortUS14527353.1147.19, 59.03203
RetrospectiveEurope32041.470.00, 3.12204
CohortUS3231810.066.76, 13.37205
ProspectiveSouth Korea389319112.1911.06, 13.33206
ProspectiveFrance8111570.4362.09, 78.78207
RetrospectiveChina3019615.3110.27, 20.35208
RetrospectiveIran9610096.0092.16, 99.84209
RetrospectiveQatar1914113.487.84, 19.11210
Cross sectional2210022.0013.88, 30.12211
Cross sectionalFrance12939033.0828.41, 37.75212
Case controlIndia117414.866.76, 22.97213
RetrospectiveTurkey529119744.1941.38, 47.01214
Case controlIsrael7611267.8659.21, 76.51215
Cross sectionalCanada315655.3642.34, 68.38216
RetrospectiveUS7516944.3836.89, 51.87217
RetrospectiveChina134117211.439.61, 13.26218
CohortUS151778.474.37, 12.58219
Cross sectionalGreece297936.7126.08, 47.34220
Cross sectionalSaudi Arabia2812821.8814.71, 29.04221
Cross sectionalItaly28350855.7151.39, 60.03222
Cross sectionalItaly23735566.7661.86, 71.66223
Cross sectionalSpain263183.8770.92, 96.82224
Cross sectionalSpain45484653.6650.30, 57.02225
ProspectiveItaly8413860.8752.73, 69.01226
Case controlBrazil235740.3527.61, 53.09227
Case controlIran596098.3395.09, 100.00228
RetrospectiveUS19894920.8618.28, 23.45229
ProspectiveItaly465092.0084.48, 99.52230
Cross sectionalTurkey7122331.8425.72, 37.95231
ProspectiveItaly446765.6754.30, 77.04232
ProspectiveIndia627681.5872.86, 90.29233
Cross sectionalBrazil15917988.8384.21, 93.44234
RetrospectiveGlobal1324169877.9776.00, 79.95235
RetrospectiveItaly4611141.4432.28, 50.61236

Table 2.

The prevalence of dysgeusia among COVID-19 patients around the globe.

Study designCountryCOVID-19Prevalence (%)95%CIRef
DysgeusiaTotal
RetrospectiveSingapore5330517.3813.12, 21.63131
ProspectiveTurkey62920.695.95, 35.43119
Case controlSpain297936.7126.08, 47.34133
RetrospectiveTaiwan4232113.089.39, 16.77134
Case controlCanada6913451.4943.03, 59.95135
Case controlUS6010159.4149.83, 68.98136
RetrospectiveItaly62132.820.59, 5.04137
Cross sectionalUS425971.1959.63, 82.74138
Cross sectionalSpain12819764.9758.31, 71.64139
ProspectiveBrazil50265576.6473.40, 79.88140
RetrospectivePakistan43013.331.17, 25.50141
RetrospectiveSpain9037524.0019.68, 28.32142
Cross sectionalEurope770142054.2351.63, 56.82143
ProspectiveSouth Korea5817233.7226.66, 40.79144
ProspectiveFrance5619728.4322.13, 34.73145
RetrospectiveUSA4125116.3311.76, 20.91146
RetrospectiveItaly142263.6443.53. 83.74147
Cross sectionalIndia2523010.876.85. 14.89148
Cross sectionalUS151688.934.62, 13.24149
Cross sectionalHongkong368343.3732.71, 54.04150
RetrospectiveFrance5411447.3738.20. 56.53151
RetrospectiveJapan183256.2539.06, 73.44152
ProspectiveTaiwan7821735.9429.56, 42.33153
ProspectiveTurkey111726.402.74, 10.05154
RetrospectiveItaly268430.9521.07, 40.84155
ProspectiveItaly6610861.1151.92, 70.31156
ProspectiveIran667686.8479.24, 94.44122
RetrospectiveKenya27978735.4532.11, 39.79158
Cross sectionalGermany297339.7328.50, 50.95159
Cross sectionalFrance12429941.4735.89, 47.05162
RetrospectiveFrance465485.1975.71, 94.66163
ProspectiveIran159216.308.76, 23.85164
RetrospectiveIllinois8150915.9112.74, 19.09165
Cross sectionalBrazil297339.7328.50, 50.95167
ProspectiveTurkey15726259.9253.99, 65.86168
RetrospectiveFrance175530.9118.70, 43.12169
Cross sectionalUK34457959.4155.41, 63.41170
RetrospectiveSomalia176028.3316.93, 39.74171
ProspectiveUS244257.1442.18, 72.11172
ProspectiveTurkey5114335.6627.81, 43.52173
RetrospectiveChina122145.612.52, 8.69174
RetrospectiveBrazil312080.250.00, 0.53175
RetrospectiveIllinois55010.001.68, 18.32176
RetrospectiveChina122145.612.52, 8.69237
Cross sectionalIndia353918.956.12, 11.78177
RetrospectiveChina338638.3728.09, 48.65178
RetrospectiveFrance347048.5736.86, 60.28179
Cross sectionalItaly345462.9650.08, 75.84115
RetrospectiveUK8914163.1255.16, 71.08181
ProspectiveItaly397254.1742.66, 65.68182
Case controlTurkey435282.6972.41, 92.97125
ProspectiveBelgium378643.0232.56, 53.49238
RetrospectiveBelgium64712.773.23, 22.31183
Case controlIsrael31618.750.00, 37.88184
Case controlTurkey228127.1617.47, 36.85185
RetrospectiveChina, France Germany10039425.3821.08, 29.68186
RetrospectiveMalaysia3414523.4516.55, 30.34187
RetrospectiveEurope34241782.0178.33, 85.70188
RetrospectiveItaly4110041.0031.36, 50.64189
CohortItaly13515189.4084.49, 94.31190
Cross sectionalSwitzerland6710365.0555.84, 74. 26191
ProspectiveIsrael8211273.2165.01, 81.42194
CohortIndia3922517.3312.39, 22.28195
Case controlturkey4811641.3832.42, 50.34196
Retrospectiveturkey2515516.1310.34, 21.92197
RetrospectiveFrance1389373737.1735.62, 38.72198
Cross sectionalIran374975.5163.47, 87.55129
ProspectiveNA47675163.3859.94, 66.83239
RetrospectiveSouth Korea33280.910.00, 19.94199
Cross sectionalSpain515887.9379.55, 96.31201
CohortUS14527353.1147.19, 59.03203
RetrospectiveEurope32041.470.00, 3.12204
CohortUS243187.554.64, 10.45205
ProspectiveSouth Korea353319111.069.97, 12.15206
ProspectiveFrance8111570.4362.09, 78.78207
RetrospectiveChina2319611.737.23, 16.24208
RetrospectiveQatar2814119.8613.27, 26.44210
Cross sectionalIndia4010040.0030.40, 49.60211
Cross sectionalFrance13039033.3328.65, 38.01212
RetrospectiveTurkey526119743.9441.13, 46.75214
Case controlIsrael8011271.4363.06, 79.80215
Cross sectionalCanada325657.1444.18, 70.10216
RetrospectiveUS7016941.4233.99, 48.85217
RetrospectiveChina242117220.6518.33, 22.97218
CohortUS151778.474.37, 12.58219
Cross sectionalGreece227927.8517.96, 37.73220
Cross sectionalSaudi Arabia2812821.8814.71, 29.04221
Cross sectionalItaly32150863.1958.99, 67.38222
Cross sectionalItaly23235565.3560.40, 70.30223
Cross sectionalSpain43112.901.10, 24.70224
Cross sectionalSpain44284652.2548.88, 55.61225
ProspectiveItaly5613840.5832.39, 48.77226
Case controlBrazil5578.771.43, 16.12227
Case controlIran146023.3312.63, 34.04228
ProspectiveItaly355070.0057.30, 82.70230
Cross sectionalTurkey7722334.5328.29, 40.77231
ProspectiveItaly176725.3714.95, 35.79232
ProspectiveIndia647684.2176.01, 92.41233
Cross sectionalBrazil15917988.8384.21, 93.44234
RetrospectiveGlobal1149168768.1165.89, 70.33235
RetrospectiveItaly6611159.4650.33, 68.59236

Association of anosmia and the occurrence of COVID-19

In total, 20 studies comprising 1,213 COVID-19 cases with anosmia and 2,735 non-COVID-19 patients (mostly COVID-19-like symptoms with negative RT-PCR for SARS-CoV-2) were analyzed to investigate the association between anosmia and the occurrence of COVID-19. Data suggested that anosmia was 10.2-fold more prevalent in patients with COVID-19 compared to those with COVID-19 like illness, OR 10.21 (95% CI: 6.53, 15.96) with p < 0.001 (Figure 2).

f24054be-abc2-4d08-be8c-1ece881b6f7d_figure2.gif

Figure 2. Forest plot of the association between anosmia and the risk of COVID-19 (OR: 10.21; 95%CI: 6.53, 15.96; p<0.001; Egger’ p=0.8340; heterogeneity p<0.001; I-squared 79.33%).

Association of dysgeusia and the occurrence of COVID-19

In total, 16 studies comprising 1,342 COVID-19 cases with dysgeusia and 1,990 patients with other respiratory illness (COVID-19 like illness with negative RT-PCR for SARS-CoV-2) were included to assess the association between dysgeusia and the occurrence of COVID-19. Data suggested that dysgeusia was 8.6-fold more prevalent in patients with COVID-19 compared to those with other respiratory illness, with OR 8.61 (95% CI: 5.26, 14.11) and p<0.001 (Figure 3).

f24054be-abc2-4d08-be8c-1ece881b6f7d_figure3.gif

Figure 3. Forest plot of the association between dysgeusia and the risk of COVID-19 (OR: 8.61; 95%CI: 5.26, 14.11; p<0.001; Egger’ p=0.8220; heterogeneity p<0.001; I-squared 81.03%).

Association of anosmia and dysgeusia with COVID-19 severity and mortality

Limited studies have assessed the association between anosmia and dysgeusia and the severity and mortality of COVID-19 cases. One study linked anosmia with a lower fatality rate and a lower ICU admission240.

Discussion

Anosmia and dysgeusia in COVID-19 patients

The pooled prevalence of anosmia in our systematic review was 38.2% of 32,142 COVID-19 cases. This result was almost thrice the initial prevalence reported from Wuhan, China174,208. This suggests that anosmia is a potential indicator of SARS-CoV-2 infection, and may be useful for screening and early identification of COIVD-19 patients, particularly asymptomatics241. Some countries, such as the UK and US have used anosmia as an indicator for preventive measure, wherein COVID-19 patient with anosmia should commence self-isolation242-244.

Anosmia is not only present in COVID-19 patients, but also in patients with other respiratory diseases such as influenza, parainfluenza, Eipstein Barr virus, picornavirus, and rhinovirus245-248. However, our study demonstrated that the prevalence of anosmia was 10.2-fold higher in COVID-19 patient than that in non-COVID-19 patient. During the previous pandemics, such as severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome (MERS), anosmia was rarely reported249. Only one study reported persistent anosmia after 2 years of recovery from SARS250. Another study reported that anosmia in COVID-19 patients varied based on ethnicity; anosmia in Caucasian is three times more prevalent than in Asian population251.

Dysgeusia was initially reported in 11.7% of patients who were discharged from Wuhan hospital, which persisted for at least four weeks. This result was lower than ours (36.6% out of 30,901 COVID-19 cases), which might be attributable to either lower dysgeusia prevalence in China or underestimation of this symptom itself208. Moreover, the prevalence of dysgeusia in COVID-19 patients was 8.6-fold higher than that in non-COVID-19 like illness. Herpes zoster and HIV have also been linked to gustatory dysfunction252,253. Furthermore, another study reported that anosmia and dysgeusia have 82.5% predictive value for positive SARS-CoV-2 RT-PCR254.

Possible pathogenesis of anosmia in COVID-19

Several mechanisms have been proposed to explain the emergence of anosmia in COVID-19 patients.

a. Obstruction in the nasal airway

As several viral infections in the respiratory system display blockage of nasal airway or nasal congestion, this hypothesis was initially proposed. According to this mechanism, the interaction between the odorants and olfactory receptors is inhibited by certain obstructions, thereby impairing the subsequent smelling processes255. This condition results in anosmia. The obstruction could be caused by nasal discharge or by inflammation occurring in the nasal cavity256; however, this hypothesis can be presumably ruled out. Moreover, several studies reported that anosmia is more prevalent than nasal congestion in COVID-19 patients188,256-259. Interestingly, the incidence of rhinorrhea and nasal obstruction in SARS-CoV-2 infection is lower than other coronaviruses such as SARS-CoV and MERS-CoV260.

Furthermore, presumably, nasal obstruction is a secondary mechanism by which anosmia is induced in COVID-19 patients as the obstruction in viral infection typically occurs as a subsequent event after damage in the mucociliary system, thereby inhibiting the nasal discharge and leading to nasal obstruction. In certain viral infections, the mucociliary system operated by ciliated cells is impaired. A previous study reported that human coronavirus (HCoV) disrupted the nasal ciliated respiratory epithelium leading to impaired mucociliary escalator system261.

b. Damage in olfactory sensory neurons

Smelling processes commence when the odorants bind to the olfactory sensory neurons (OSNs) in the olfactory epithelium located in the nasal cavity, which subsequently transmits this information through their axons to the olfactory bulb in the brain262. According to this concept, a viral attack on the receptor neurons eventually creates disturbances in the sense of smell; however, this hypothesis remains under debate as several recent studies reported the absence of angiotensin-converting enzyme 2 (ACE2) and transmembrane protease serine 2 (TMPRSS), the key factors for the virus to enter the cell263, in the OSNs264-267. These findings are supported by another study carried out by Bryche et al., who demonstrated that SARS-CoV-2 was not detected in the OSNs of hamsters266.

Moreover, after comparing the duration between anosmia incidence in COVID-19 patients and the normal cellular regeneration process, this proposed mechanism should be reconsidered. Several studies reported that COVID-19-related anosmia disappeared within 1-2 weeks, whereas regeneration of dead OSNs requires more than 2 week time period188,206,255,262,268. This discrepancy results in a temporary conclusion that COVID-19-related anosmia is not directly associated with the impairment of the OSNs.

c. Olfactory center damage in the brain

The aforementioned dysfunction of OSNs and the mechanism by which SARS-CoV-2 directly affects the olfactory center via axonal transport of the neuron remains unclear, as the OSN lacks ACE2 and TMPRSS2 which hinders viral entry into the cell264-267. Nevertheless, the possibility of olfactory center disruption caused by SARS-CoV-2 should not be overlooked as the cause of anosmia, since a previous study concluded that human ACE2 (hACE2)-transgenic mice suffered from brain infection after intranasal inoculation with SARS-CoV269. The study found that the brain infection commenced from the olfactory bulb, which is the axonal trajectory pathway of the OSNs269. This finding suggests that SARS-CoV-2 might also first utilize another structure in the nasal cavity before it is transported into the OSNs.

d. Olfactory supporting cells dysfunction

As OSN does not express ACE2 and TMPRSS2, the virus should use another pathway to infect the olfactory system. Numerous studies have established the expression of these SARS-CoV-2 entry proteins in several supporting cells in olfactory epithelium, that is, Bowman’s gland cells, horizontal basal cells, olfactory bulb pericytes, mitral cells, sustentacular cells, and microvillar cells264-267. Of these supporting cells, the sustentacular cells have gained immense attention as the initial site of SARS-CoV-2 infection in the olfactory epithelium. In addition to their higher expression of ACE2 and TMPRSS2 than the others, sustentacular cells are located on the surface of the nasal cavity making them vulnerable to exposure to the external environment264,267.

Notably, sustentacular cells act as supporting cells and promote olfactory neuron in the olfactory system. These cells detoxify harmful odorants, promote odorant-receptor binding, and provide nutritional substances to support the action of olfactory receptor neurons255,264. Considerably, it is plausible to suggest that any damage occurring in sustentacular cells will in turn affect the olfactory epithelium and produce anosmia.

The corresponding regeneration time to the recovery of anosmia also supports the notion that sustentacular cell damage relates to anosmia caused by SARS-CoV-2. As the replenishment of dead OSNs does not correspond to the duration of COVID-19-related anosmia within 1-2 weeks, the regeneration of sustentacular cells seems to be in line with that time frame264,266,268.

Furthermore, this hypothesis is supported by a recent study conducted by Bryche et al., who reported that SARS-CoV-2 was accumulated in sustentacular cells but not in the OSNs266. The olfactory epithelial damage and sustentacular cell loss occurred 2 days after instilling SARS-CoV-2 intranasally in golden Syrian hamsters266.

e. Inflammation-related olfactory epithelium dysfunction

It is worth noting that the cytokine storm in COVID-19 is strongly associated with organ dysfunctions, including OSNs232. The dysfunction in this structure can lead to disturbance in the sense of smell270. Torabi et al. suggested that proinflammatory cytokines, particularly tumor necrosis factor a (TNF-α), may lead to COVID-19-induced anosmia271. Another proinflammatory cytokine, interleukin-6 (IL-6), increased in cases presenting with anosmia232,272.

The mechanism used by these cytokines, in particular IL-6, to produce anosmia is not fully understood. Cazzolla et al. suggested that this effect can be caused by either peripheral or central action of the cytokines232. In the periphery, IL-6 may induce apoptosis of ciliary neuronal cells in the olfactory epithelium272, whereas in its central action, the olfactory center in the brain is attacked by the cytokine as a result of virus infection232.

Possible pathogenesis of dysgeusia in COVID-19

Although gustatory impairment is always displayed concomitantly with olfactory dysfunction, this symptom has a relatively different mechanism and is often distantly linked to the latter symptom. Several hypotheses have been proposed to explain the mechanism behind the emergence of dysgeusia in COVID-19 patients.

a. The subsequent effect of cranial nerves dysfunction

Considering the close relationship between the olfactory and gustatory system both peripherally and centrally, smell and taste dysfunction in COVID-19 often occurs concomitantly256,273. This hypothesis describes dysgeusia as a secondary event of olfactory dysfunction274; however, several studies revealed that the percentage of dysgeusia in COVID-19 patients is higher than symptoms related to olfactory dysfunction188,275. Based on this finding, another mechanism may be involved in inducing SARS-CoV-2-related dysgeusia. Furthermore, COVID-19-induced dysgeusia could also occur when there is certain damage in the cranial nerves responsible for gustatory transmission (cranial nerve VII, IX, and X)276. Among these nerves, SARS-CoV-2 exposure to cranial nerve VII has gained immense attention. Based on this hypothesis, the virus initially colonizes the nasopharynx structure, then moves to the Eustachian tube, and eventually reaches the middle ear where the virus gets access to chorda tympani and causes dysgeusia276.

b. Zinc deficiency

Another interesting hypothesis underlying dysgeusia in COVID-19 is related to zinc deficiency276. This hypothesis was developed as zinc is an important mineral in carbonic anhydrase, which is pivotal in maintaining taste sensation277. Interestingly, one study reported that zinc level in patients with SARS-CoV-2 infection was significantly lower compared to that in the healthy control groups278. Alterations in the sense of taste after being treated with certain treatments, such as irradiation in cancer patients279,280, could be prevented by zinc supplementation. Moreover, dengue fever virus and human immunodeficiency virus replication could be inhibited by zinc chelation281,282. Furthermore, pharmacological agents influencing ACE2 activity are associated with taste disturbances283,284.

Nevertheless, this effect does not relate to zinc deficiency as these drugs do not influence both serum and salivary zinc concentrations284. Further investigation needs to be carried out to reveal the role of zinc in dysgeusia associated with COVID-19.

c. SARS-CoV-2-bound sialic acid

SARS-CoV-2 may produce dysgeusia via interaction with sialic acid receptors232,274,285. Sialic acid plays a pivotal role in the taste processing pathway as it is a component of the normal salivary composition286. Moreover, reduced amount of sialic acid impairs the ability to taste287. An in silico study revealed that SARS-CoV-2 could interact with the sialic acid receptor through its spike protein288. Previously, MERS-CoV was also reported to interact with this receptor289. Following this occupancy, the gustatory threshold increases, while gustatory particles degrade at a higher rate274,287.

d. Direct attack on several oral sites

A previous study investigated the expression of ACE2 in various tissues in the oral cavity and found that the tongue had higher ACE2 expression in comparison to other tissues, such as buccal and gingival tissues290. This finding raised a hypothesis that SARS-CoV-2 could directly attack the taste buds in the tongue, initiating inflammatory responses, and would eventually alter the sense of taste276. It is proposed that the Toll-like receptor-mediated cascade and apoptosis are the subsequent events that could lead to taste dysfunction276,291.

A previous study investigating SARS-CoV infection in rhesus macaques revealed that, initially, the salivary gland was attacked by the virus292. As the human salivary gland expresses a high level of ACE2293, it is reasonable to pay more attention to the vulnerability of this gland against SARS-CoV-2 exposure. Disruption in the activity of the salivary gland would produce either imbalance in salivary composition or impairment of salivary flow, which could ultimately result in dysgeusia276.

Conclusions

Out of 32,142 and 30,901 COVID-19 cases studied for anosmia and dysgeusia, respectively, the prevalence of anosmia was approximately 38.2%, whereas that of dysgeusia was 36.6%. Both of these symptoms were more common in COVID-19 compared to other respiratory infections (approximately 10 and 9 times, respectively). Several mechanisms have been proposed to explain the emergence of anosmia in COVID-19 patients including nasal airway obstruction, damage in OSNs, olfactory center damage in the brain, dysfunction of olfactory supporting cells, and inflammation-related olfactory epithelium dysfunction. Furthermore, some possible pathogenesis of dysgeusia in SARS-CoV-2 infection has been proposed including cranial nerve dysfunction, zinc deficiency, virion interaction, and direct attack of the virus to several oral sites.

Data availability

Undelying data

All data underlying the results are available as part of the article and no additional source data are required.

Reporting guidelines

Figshare: PRISMA checklist for ‘Anosmia and dysgeusia in SARS-CoV-2 infection: Incidence, effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - A systematic review and meta-analysis’, https://doi.org/10.6084/m9.figshare.13323080.v1294.

Data are available under the terms of the Creative Commons Attribution 4.0 International license (CC-BY 4.0).

Acknowledgement

Authors would like to thank HT Editorial Services in assisting the writing process.

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Mutiawati E, Fahriani M, Mamada SS et al. Anosmia and dysgeusia in SARS-CoV-2 infection: incidence and effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - a systematic review and meta-analysis [version 1; peer review: 2 approved, 1 approved with reservations] F1000Research 2021, 10:40 (https://doi.org/10.12688/f1000research.28393.1)
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ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
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Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
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Reviewer Report 23 Mar 2021
Mahir Gachabayov, Department of Surgery, New York Medical College, Valhalla, NY, USA 
Approved
VIEWS 16
https://doi.org/10.5256/f1000research.31412.r80213
Thank you for an interesting systematic review.
This systematic review and meta-analysis aimed at evaluating the rate of anosmia and dysgeusia in patients with confirmed COVID-19 and their association with disease severity and mortality. 
The research question makes ... Continue reading
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Gachabayov M. Reviewer Report For: Anosmia and dysgeusia in SARS-CoV-2 infection: incidence and effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - a systematic review and meta-analysis [version 1; peer review: 2 approved, 1 approved with reservations]. F1000Research 2021, 10:40 (https://doi.org/10.5256/f1000research.31412.r80213)
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https://f1000research.com/articles/10-40/v1#referee-response-80213
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Reviewer Report 22 Mar 2021
Seyi Samson Enitan, Department of Medical Laboratory Science, Babcock University, Ilishan-Remo, Nigeria 
Approved
VIEWS 19
https://doi.org/10.5256/f1000research.31412.r80214
The present study examined the global prevalence of anosmia and dysgeusia in COVID-19 patients, their association with severity and mortality of COVID-19, as well as the possible pathobiological mechanisms of anosmia and dysgeusia in COVID-19. Authors reported a global prevalence ... Continue reading
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Enitan SS. Reviewer Report For: Anosmia and dysgeusia in SARS-CoV-2 infection: incidence and effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - a systematic review and meta-analysis [version 1; peer review: 2 approved, 1 approved with reservations]. F1000Research 2021, 10:40 (https://doi.org/10.5256/f1000research.31412.r80214)
The direct URL for this report is:
https://f1000research.com/articles/10-40/v1#referee-response-80214
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Reviewer Report 16 Feb 2021
Cissy B. Kartasasmita, Department of Child Health, Faculty of Medicine, Universitas Padjadjaran, Bandung, Indonesia 
Approved with Reservations
VIEWS 32
https://doi.org/10.5256/f1000research.31412.r77883
Objectives of study
‘"The present study aimed to summarize the global evidence of anosmia and dysgeusia among COVID-19 patients, in order to assess their association with the severity and mortality of the disease, and provide a comprehensive review related ... Continue reading
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HOW TO CITE THIS REPORT
Kartasasmita CB. Reviewer Report For: Anosmia and dysgeusia in SARS-CoV-2 infection: incidence and effects on COVID-19 severity and mortality, and the possible pathobiology mechanisms - a systematic review and meta-analysis [version 1; peer review: 2 approved, 1 approved with reservations]. F1000Research 2021, 10:40 (https://doi.org/10.5256/f1000research.31412.r77883)
The direct URL for this report is:
https://f1000research.com/articles/10-40/v1#referee-response-77883
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Approved
The paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations
A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved
Fundamental flaws in the paper seriously undermine the findings and conclusions

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  1. Cissy B. Kartasasmita, Universitas Padjadjaran, Bandung, Indonesia
  2. Seyi Samson Enitan, Babcock University, Ilishan-Remo, Nigeria
  3. Mahir Gachabayov, New York Medical College, Valhalla, USA

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    Alongside their report, reviewers assign a status to the article:
    Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
    Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
    Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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