Journal Article

Received: 9 September 2020 | Revised: 27 November 2020 | Accepted: 5 January 2021 DOI: 10.1002/jmv.26784

R E S E A R C H A R T I C L E

COVID‐19 with and without anosmia or dysgeusia: A case‐control study

Nishanth Dev1 | Jhuma Sankar2 | Nitesh Gupta3 | Ramesh Chand Meena1 |

Charanjit Singh1 | D. K. Gupta1 | M. K. Sen3

1Department of Medicine, VMMC &

Safdarjung Hospital, Delhi, India

2Department of Pediatrics, All India Institute

of Medical Sciences, Delhi, India

3Department of Pulmonology and critical

care, VMMC & Safdarjung Hospital, Delhi,

India

Correspondence

Nishanth Dev, Department of Medicine,

VMMC & Safdarjung Hospital, Delhi 110029,

India.

Email: [email protected]

Abstract

Various new clinical signs and symptoms, such as dysfunction of smell (anosmia) and

taste (dysgeusia) have emerged ever since the coronavirus disease 2019 (COVID‐19) pandemic begun. The objective of this study was to identify the clinical presentation

and factors associated with 'new loss/change of smell (anosmia) or taste (dysgeusia)'

at admission in patients positive by real time polymerase chain reaction for SARS‐ CoV‐2 infection. All adult COVID‐19 patients with new onset anosmia or dysgeusia at admission were included in study group. Equal number of age and gender matched

COVID‐19 patients without anosmia or dysgeusia at admission were included in the control group. A total of 261 COVID‐19 patients were admitted during the study period of which 55 (21%) had anosmia and or dysgeusia. The mean (SD) age was 36

(13) years and majority were males (58%, n = 32). Comorbidity was present in 38% of

cases (n = 21). Anosmia and dysgeusia were noted in more than 1/5th of the cases.

Anosmia (96%, n = 53) was more common than dysgeusia (75%, n = 41). Presence of

both ansomia and dysgeusia was noted in 71% of patients (n = 39). On comparing the

cases with the controls, on univariate analysis, fever (higher in cases), rhinitis (lower in

cases), thrombocytopenia, elevated creatinine and bilirubin (all higher in cases) were

significantly associated with anosmia or dysgeusia. On multivariate analysis, only

rhinitis (odds ratio [OR]: 0.28; 95% confidence interval [CI]: 0.09–0.83; p = .02)

thrombocytopenia (OR: 0.99; 95% CI: 0.99–0.99; p = .01) and elevated creatinine

(OR: 7.6; 95% CI: 1.5–37.6; p = .01) remained significant. In this retrospective study of

COVID‐19 patients, we found anosmia and dysgeusia in more than 1/5th of the cases. Absence of rhinitis, low platelet counts and elevated creatinine were associated with

anosmia or dysgeusia in these patients.

K E Y W O R D S

anosmia, COVID‐19, dysgeusia, rhinitis, SARS‐CoV‐2

1 | INTRODUCTION

The current pandemic of coronavirus disease (COVID‐19) caused by severe acute respiratory syndrome coronavirus 2 (SARS‐CoV‐2) continues to evolve and perplex the clinicians across the globe.

Various new clinical signs and symptoms have emerged ever since

the pandemic begun. The expanding list of various clinical manifes-

tations also includes dysfunction of smell and taste i.e. anosmia and

dysgeusia.1 Various case reports and case series have highlighted the

same and explored its pathophysiology.2

J Med Virol. 2021;93:2499–2504. wileyonlinelibrary.com/journal/jmv © 2021 Wiley Periodicals LLC | 2499

Although the exact pathophysiology of these symptoms has not

been established, various animal models have demonstrated high

levels of angiotensin converting enzyme (ACE2) proteins expression

by nasal and olfactory support cells which is used by the SARS‐CoV‐2 to infect the cells.3 Many believe these symptoms to be part of the

neurological manifestations of COVID‐19 with evidence suggesting propagation of the virus through the olfactory pathway.4

The increasing evidence of olfactory or gustatory dysfunction as

potential early symptoms of COVID‐19 infection has also prompted the Centers for Disease Control and Prevention to add ‘‘new loss of taste or

smell’’ to its list of COVID‐19 symptoms.5 Despite the recognition of anosmia and dysgeusia as an important clinical symptom and sign of

COVID‐19, there is paucity of data describing various clinical features, co‐morbidities and clinical outcome associated with anosmia and dys- geusia in patients with COVID‐19. In this retrospective case control study, we aim to identify clinical presentation and factors associated

with of new onset anosmia and/or dysgeusia at admission in COVID‐19 patients admitted to a tertiary care center in North India.

2 | MATERIALS AND METHODS

Design and setting: We conducted this retrospective case control study

of prospectively collected data at our tertiary care center Medical col-

lege and hospital in North India between May 1st and June 15th, 2020.

2.1 | Participants

Cases: All laboratory confirmed COVID‐19 patients greatert than 17 years of age with clinical presentation of “new loss/change of

taste or smell” at admission during the study period were included in

the study group.

Controls: Equal number of age and gender matched COVID‐19 patients without clinical presentation of “new loss/change of taste or

smell” at admission were included in the control or comparison group.

We excluded those with pre‐existing history of anosmia and/or dysgeusia, nasal or oral illness, neurodegenerative disorder, on che-

motherapy or radiotherapy. Patients who were unable to give history,

transferred out, absconded were also excluded from the study. The

study was approved by the Institutional Ethics Committee and patient

consent was waived off owing to the retrospective nature of the study.

2.2 | Definitions used in the study

• Anosmia was defined as temporary or permanent loss of the

ability to detect one or more smells.

• Dysgeusia was defined as distortion of the sense of taste.

Methods: Case records of patients with SARS‐CoV‐2 infection admitted to the COVID wards from May 1st to June 15th, 2020 were

retrieved. Information retrieved included demographic features, such

as age, gender, duration of illness, signs, and symptoms at admission,

laboratory parameters, treatment received, and discharge or death

from hospital were recorded.

Statistical analysis: Data were entered into Microsoft Excel 2013

and analyzed using Stata 11 (Stata Corp.). Missing values of clinical and

laboratory variables were assumed to be normal for the purpose of

statistical analysis. Continuous variables are presented as mean (SD), or

median (interquartille range [IQR]) as appropriate. Categorical variables

are presented as absolute numbers (%). Continuous variables were

compared using either independent Student's t test or Wilcoxon rank‐ sum test (based on the distribution of the data). Categorical data were

compared using χ2 test or Fischer's exact test as appropriate. For as-

sessing the factors associated with anosmia or dysgeusia (we combined

anosmia and/or dysgeusia for this purpose), univariate analysis followed

by multivariate analysis of key variables including age, gender, presence

of underlying co‐morbidities, key clinical features and laboratory para- meters was performed. In the multivariate model by logistic regression,

only those variables that were clinically relevant and did not result in

multicollinearity were included as the independent variables.6

3 | RESULTS

3.1 | Baseline characteristics

The case records of 261 COVID‐19 patients were screened during the study period. A total of 55 patients who were eligible were en-

rolled in the study group. An equal number of age and gender mat-

ched patients fulfilling the inclusion and exclusion criteria were

enrolled in the control group. The baseline characteristics of the

enrolled patients are described in Table 1. The mean (SD) age was

TABLE 1 Demographic profile of the cases and control

Variables Case n = 55

Control

n = 55 p Value

Age (years) (mean, SD) 36 (13) 36 (13) .96

Gender (male) 32 (58%) 32 (58%) 1

History of contact with

COVID‐19 patient 16 (29%) 17 (31%) .9

Comorbidity

• Diabetes 02 (3.6%) 04 (7%) .06

• Hypertension 07 (13%) 03 (5%)

• Diabetes and hypertension 05 (9%) 03 (5%)

• Hypothyroidism 07 (13%) 01 (2%)

• Tuberculosis 00 01 (2%)

• Chronic Kidney disease 00 01 (2%)

• Bronchial asthma 00 03 (5%)

• None 34 (62%) 39 (71%)

Lifestyle

• Smoker 14 (25%) 10 (18%) .35

• Alcoholic 12 (22%) 06 (11%) .12

Abbreviation: COVID‐19, coronavirus disease 2019.

2500 | DEV ET AL.

36 (13) years and majority were men (n = 32, 58%) in both the

groups. Comorbidities was present in 38 per cent (n = 21) of patients

in the study group and 29 percent (n = 16) in the comparison group

(p = .06). Hypertension and hypothyroidism were the commonest co‐ morbidity in the study group (13% each) where as diabetes mellitus

was the commonest in the control group (7%). Twenty five percent of

the study subjects (n = 14) and 18% percent (n = 10) of the control

group had history of smoking. Twenty two percent in the study group

(n = 12) and 11% in the comparison group (n = 06) consumed alcohol.

There was no difference in the baseline characteristics between the

groups. History of contact with a COVID‐19 patient was found in 29% (n = 16) and 31% (n = 17) in cases and control respectively.

3.2 | Comparison of clinical and laboratory parameters between the “cases” and “controls”

On evaluation of the 55 patients with olfactory and gustatory

symptoms, anosmia (96%, n = 53) was more common than dysgeusia

(75%, n = 41). Presence of both ansomia and dysgeusia was noted in

71% of the patients (n = 31). Fever was present in 75% (n = 41) and

51% (n = 28) in the “cases” and “controls,” respectively (p = .01).

Rhinitis was higher in controls (n = 20, 36%) as than cases (n = 09,

16%; p = .017). The clinical and laboratory features of the cases and

controls are described in Table 2. The median (IQR) duration of

anosmia and dysgeusia was 7 (4, 10) days and 7 (5, 2) days in the

“cases” and “controls,” respectively.

The mean (SD) of serum bilirubin was 0.9 mg/dl (0.25) in the

study group and 0.6 mg/dl (0.2) in the comparison group (p < .0001).

Serum creatinine level was higher in the “cases” with median (IQR)

value of 0.9 mg/dl (0.8, 1.2) as compared to 0.8 mg/dl (0.6, 0.9)

(p = .0001). A statistically significant difference was also seen in the

platelet count (p = .0009). The median (IQR) platelet count was lower

in the “cases” (1.5 lakh/mm3 [1, 2.2]) as compared to “controls” (1.94

lakh/mm3 [1.53, 2.56]). About 1/4thof the patients had an abnormal

chest X‐ray in both the groups. The disease severity of patients enrolled was comparable

in both the groups. The cases had 18% (n = 10) in the moderate

category as compared to 22% (n = 12) in the control group with

p = .63. None of the subjects in either category had severe disease.

The presence of moderate category disease was not found to be

significantly associated with development of anosmia and/or

dysgeusia (odds ratio [OR], 0.79; 95% confidence interval [CI],

0.31–2.03; p = .64).

On comparing cases with controls, in univariate analysis, fever

(higher in cases), rhinitis (lower in cases), thrombocytopenia, ele-

vated creatinine and bilirubin (all higher in cases) were significantly

associated with anosmia or dysgeusia as described in Table 3.

TABLE 2 Clinical, laboratory features, treatment details, and outcomes

Variables Case, n = 55 Control, n = 55 p Value

Clinical features

• Fever 41 (75%) 28 (51%) .01

• Cough 29 (53%) 23 (42%) .25

• Dyspnoea 15 (27%) 15 (27%) 1

• Rhinitis 09 (16%) 20 (36%) .017

• Anosmia 53 (96%) 00 –

• Dysgeusia 41 (75%) 00 –

• Anosmia and dysgeusia 39 (71%) 00 –

Duration in days (mean, SD)

• Anosmia 07 (3) – –

• Dysgeusia 07 (2) – –

Laboratory features

• Haemoglobin (g/dl) (mean, SD) 12 (2) 13 (2) .07

• Total leucocyte count/mm3 (median, IQR) 5600 (4500, 7800) 5900 (4800, 6800) .84

• Platelets (in lakh)/mm3 (median, IQR) 1.5 (1, 2.2) 1.94 (1.53, 2.56) .0009

• Creatinine (mg/dl) (median, IQR) 0.9 (0.8, 1.2) 0.8 (.6, 0.9) .0001

• Bilirubin (mg/dl) (mean, SD) 0.9 (0.25) 0.6 (0.2) <.0001

• Chest X‐ray (infiltrates) 13 (24%) 15 (27%) .66

Treatment received

• Oxygen therapy 10 (18%) 12 (22%) .63

• Antibiotics 34 (62%) 31 (56%) .56

Duration of hospital stay in days (mean, SD) 11 (02) 13 (03) .001

Discharged 55 (100%) 55 (100%) 1

Abbreviation: IQR, interquartile range.

DEV ET AL. | 2501

3.3 | Multivariate analysis of factors associated with anosmia or dysgeusia

On multivariate analysis of factors associated with anosmia or dys-

geusia we found rhinitis (OR, 0.28; 95% CI, 0.09–0.83); p = .02)

thrombocytopenia (OR, 0.99; 95% CI, 0.99–0.99; p = .01) and elevated

creatinine (OR, 7.6; 95% CI, 1.5–37.6; p = .01) to be factors significantly

associated with anosmia or dysgeusia as described in Table 4.

3.4 | Treatment and clinical course

About two‐third of the cases (62%, n = 34) and half (56%, n = 31) of the controls received antibiotics. About one‐fifth (20%) of patients required oxygen supplementation in both groups. The mean (SD) duration of

hospital stay in the “cases” was 11 days (02) as compared to 13 days

(03) in the “controls” (p = .001). No mortality occurred in either groups.

4 | DISCUSSION

COVID‐19 is mostly asymptomatic with an estimated figure of 40%–45%.7 The common presenting features are fever, cough, sore

throat, dyspnea, and myalgia.8 New signs or symptoms including

olfactory and gustatory dysfunctions are increasingly being ob-

served. Our study highlights the presence of these two dysfunctions

in patients with COVID‐19 in almost 21% of patients. The reported prevalence of olfactory dysfunction in various case series have ran-

ged from 5.14% to as high as 98.33% whereas the reported pre-

valence of gustatory dysfunction has ranged from 5.61% to 92.65%.9

In a Chinese cohort the frequency of neurological manifestations was

noticed in 214 COVID‐19 patients, anosmia in 11 (5.1%) patients and ageusia in 12 (5.6%) patients.10 Presence of gustatory and olfactory

dysfunction was found in 19.38% cases in a case series which is

similar to our study.11 However, olfactory and gustatory dysfunction

was reported in 75% and 92.65% respectively by Bénézit et al.12 The

significantly higher figures could be attributed to the fact that fewer

number of patients included in the study. Highly variable figures of

taste and smell dysfunction may also be attributed to presence of

variable strains of SARS‐CoV‐2 in various countries as well as varying pathogenicity for the nasal cavity by different strains.

A meta‐analysis has also reported that higher prevalence was demonstrated when validated instruments were used and

self‐reports generally underestimated its incidence.9

While most studies have been either case series or cross sec-

tional, only two case control studies have been done on the subject

till date. Moein et al.13 conducted olfactory function tests on 60

COVID‐19 patients and compared with age and gender matched

TABLE 3 Univariate analysis of factors associated with anosmia or dysgeusia Variables

Anosmia/dysgeusia,

n = 55

No anosmia/dysgeusia,

n = 55 p Value

Baseline

Age (years) (mean, SD) 36 (13) 36 (13) 1

Gender (male) 32 (58) 32 (58) 1

Comorbidity (yes/no) 21 (38%) 16 (29) .08

Lifestyle

• Smoker 14 (25%) 10 (18%) .35

• Alcoholic 12 (22%) 06 (11%) .12

Clinical features

• Fever 41 28 .01

• Cough 29 23 .25

• Dyspnoea 15 15 1

• Rhinitis 09 20 .01

Laboratory features

• Haemoglobin (g/dl) (mean, SD) 12 (2) 113 (2) .07

• Total leucocyte count/mm3

(median, IQR)

5600 (4500, 7800) 5900 (4800, 6800) .84

• Platelets (in lakh)/mm3

(median, IQR)b 1.5 (1, 2.2) 1.94 (1.53, 2.56) .0009

• Creatinine (mg/dl) (median, IQR) 0.9 (0.8, 1.2) 0.8 (0.6, 0.9) .0001

• Bilirubin (mg/dl)a (mean, SD) 0.9 (0.25) 0.6 (0.2) <.0001

• Chest X‐ray (infiltrates) 13 (24%) 15 (27%) .66

Note: Data presented as number (%) unless specified otherwise.

Abbreviation: IQR, interquartile range. aElevated in “3 cases” and “1 control,” respectively. b27 “cases” and 13 “controls” had thrombocytopenia.

2502 | DEV ET AL.

historical control from a previous study. Although pronounced

olfactory dysfunction was demonstrated, no meaningful relationships

between olfactory function test scores and sex, disease severity, or

comorbidities could be demonstrated. In another case control study

which included 79 COVID‐19 cases and 40 controls (patients posi- tive for influenza polymerase chain reaction (historical control

sample), new onset taste and smell dysfunction were significantly

higher amongst cases (31, 39.2%) than in the control group (5, 12.5%)

(adjusted OR, 21.4; CI, 2.77–165.4; p = .003)].14 While these studies

have made attempts to study certain factors associated with olfac-

tory dysfunctions, our study is probably the first attempt to identify

various demographic and clinical factors associated with olfactory

and gustatory dysfunction. Thrombocytopenia and elevated serum

creatinine levels were associated significantly with presence of an-

osmia or dysgeusia. While renal derangements have been associated

with these dysfunctions, its sudden onset in COVID‐19 patients re- mains unanswered. Another feature identified in the current study is

significantly lower incidence of rhinitis in patients with anosmia or

dysgeusia. Rhinitis was also found to have significant associated on

multivariate analysis as well. While anosmia or dysgeusia have been

found to be higher in patients with rhinitis due to nasal congestion

and obstruction, certain other studies have suggested affinity of

certain viruses for structures of the olfactory sensory epithelium as a

causative mechanism.15 Its lower incidence in COVID‐19 patients with rhinitis in our study also suggests towards a complex patho-

physiology which is yet to be elucidated.

Anosmia has already been reported in various viral illnesses in-

cluding other coronavirus infections; however, it has been identified

only recently as a presenting manifestation in COVID‐19 patients.16

The exact pathophysiology is not clear till date, with various hypoth-

esis and animal models suggesting trans‐neural penetration through the olfactory bulb.17 It has also been demonstrated that ACE‐2 re- ceptor used by SARS‐CoV‐2 to bind and penetrate into the cell, is also expressed on the epithelial cells of the oral cavity.18 Another plausible

mechanism involves cellular receptor neuropilin‐1, which is abun- dantly expressed in the respiratory and olfactory epithelium.19 It has

been demonstrated to significantly potentiate SARS‐CoV‐2 infectivity. Our study demonstrates that anosmia and dysgeusia are fairly

frequent in patients with SARS‐CoV‐2 infection and may precede

the onset of full‐blown clinical disease. From an epidemiological perspective during a pandemic, further investigations using vali-

dated tools on nonhospitalized infected patients are required to

ascertain if these symptoms, although nonspecific, can prove to be

an important tool in identification of asymptomatic COVID‐19 patients.

Ours is the first case control study from one of the worst ef-

fected countries from COVID‐19. It is also the first attempt to study various factors associated with anosmia/and or dysgeusia in COVID‐ 19 patients. Limitation of the study includes non‐usage of validated tool to assess theses dysfunctions.

5 | CONCLUSION

Anosmia and dysgeusia are fairly common in patients with SARS‐ CoV‐2 infection and may precede the onset of full‐blown clinical disease. Prospective study with large sample size using validated

tools is required to identify the true incidence and various factors

associated with these clinical presentations.

CONFLICT OF INTERESTS

The authors declare that there are no conflict of interests.

AUTHOR CONTRIBUTIONS

Nishanth Dev, Jhuma Sankar, Nitesh Gupta, Ramesh Chand Meena,

Charanjit Singh, D. K. Gupta, and M. K. Sen conceived the study.

Nishanth Dev, Jhuma Sankar, Nitesh Gupta, Ramesh Chand Meena,

and M. K. Sen collected the data. Data verified by Nishanth Dev,

Jhuma Sankar, Nitesh Gupta, Ramesh Chand Meena, Charanjit

Singh, D. K. Gupta, and M. K. Sen. Nishanth Dev and Jhuma Sankar

cleaned data. Nishanth Dev and Jhuma Sankar did statistical ana-

lyses. Nishanth Dev, Jhuma Sankar, Nitesh Gupta, Ramesh Chand

Meena, Charanjit Singh, D. K. Gupta, and M. K. Sen drafted the

manuscript.

DATA AVAILABILITY STATEMENT

The data that support the findings of this study are available from

the corresponding author upon reasonable request.

TABLE 4 Multivariate analysis of factors associated with anosmia or dysgeusia

Variables

Anosmia/

dysgeusia (n = 55)

No anosmia/no

dysgeusia (n = 55)

Adjusted OR (95% CI),

p value p Value

o Age in years (mean, SD) 36 (13) 36 (13) 0.98 (0.94,1.02) .38

o Gender (male) (n, %) 32 (58%) 32 (58%) 1.09 (0.41, 2.9) .85

o Co‐morbidity (yes/no) 21 (38%) 16 (29%) 0.9 (0.68, 1.19) .47 o Fever 41 (75%) 28 (51%) 2.28 (0.87, 5.9) .09

o Rhinitis 09 (16%) 20 (36%) 0.28 (0.09, 0.83) .02

o Haemoglobin (g/dl) (mean, SD) 12 (2) 13 (2) 0.84 (0.66, 1.08) .18

o Platelets (in lakh)/mm3 (median, IQR) 1.5 (1, 2.2) 1.94 (1.53, 2.56) 0.99 (0.99, 0.99) .01

o Creatinine (mg/dl) (median, IQR) 0.9 (0.8, 1.2) 0.8 (0.6, 0.9) 7.6 (1.5, 37.6) .01

Abbreviations: CI, confidence interval; IQR: Interquartile range; OR, odds ratio.

DEV ET AL. | 2503

ORCID

Nishanth Dev http://orcid.org/0000-0003-2486-6725

Jhuma Sankar https://orcid.org/0000-0002-9807-6550

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How to cite this article: Dev N, Sankar J, Gupta N,

et al. COVID‐19 with and without anosmia or dysgeusia: A case‐control study. J Med Virol. 2021;93:2499‐2504. https://doi.org/10.1002/jmv.26784

2504 | DEV ET AL.