RISK FACTORS FOR OLFACTORY AND GUSTATORY DYSFUNCTIONS IN PATIENTS WITH SARS-COV-2 INFECTION
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Original Paper
Neuroepidemiology 2021;55:154–161 Received: December 13, 2020
Accepted: January 30, 2021
DOI: 10.1159/000514888 Published online: April 1, 2021
Risk Factors for Olfactory and
Gustatory Dysfunctions in Patients with
SARS-CoV-2 Infection
Francesca Galluzzi a Veronica Rossi b Cristina Bosetti c Werner Garavello a, b
aDepartment
of Otorhinolaryngology, San Gerardo Hospital, Monza, Italy; bDepartment of Otorhinolaryngology,
School of Medicine and Surgery, University of Milano-Bicocca, Monza, Italy; cDepartment of Oncology, Istituto di
Ricerche Farmacologiche Mario Negri IRCCS, Milan, Italy
Keywords lergy in particular was significantly associated with olfactory
Olfactory dysfunction · Gustatory dysfunction · SARS-CoV-2 · dysfunctions (multivariable OR 2.30, 95% CI 1.02–5.17). Sig-
COVID-19 · Risk factors nificant inverse associations were observed for patients
aged 60 years or more (multivariable OR 0.33, 95% CI 0.19–
0.57) and hospitalization (multivariable OR 0.22, 95% CI
Abstract 0.06–0.89). Considering gustatory dysfunctions, after allow-
Introduction: Smell and taste loss are characteristic symp- ance of other variables a significant direct association was
toms of SARS-CoV-2 infection. The aim of this study is to in- found for respiratory allergies (OR 2.24, 95% CI 1.03–4.86),
vestigate the prevalence and risk factors associated with ol- and an inverse association was found only for hospitalization
factory and gustatory dysfunctions in coronavirus disease (OR 0.21, 95% CI 0.06–0.76). Conclusion: Our study indicates
(COVID-19) patients. Methods: We conducted an observa- that current smoking and history of allergy (particularly re-
tional, retrospective study on 376 patients with documented spiratory) significantly increase the risk for smell loss in CO-
SARS-CoV-2 infection admitted to the San Gerardo Hospital VID-19 patients; the latter is also significantly associated to
in Monza, Italy, from March to July 2020. All patients an- taste loss. Hospitalization has an inverse association with the
swered a phone questionnaire providing information on risk of olfactory and gustatory dysfunctions, suggesting that
age, sex, smoking status, and clinical characteristics. Adjust- these may be symptoms characteristics of less severe SARS-
ed odds ratios (ORs) and corresponding 95% confidence in- CoV-2 infection. © 2021 S. Karger AG, Basel
tervals (CIs) were estimated through logistic regression
models including relevant covariates. Results: The preva-
lence of olfactory and gustatory dysfunctions in COVID-19
patients was 33.5 and 35.6%, respectively. Olfactory dysfunc- Introduction
tions were significantly directly associated with current
smoking and history of allergy, the multivariable ORs being Since December 2019, a pandemic infection caused by
6.53 (95% CI 1.16–36.86) for current smokers versus never a new coronavirus named SARS-CoV-2 spread from Wu-
smokers, and 1.89 (95% CI 1.05–3.39) for those with an al- han in China around the world due to the high contagious
lergy compared to those without any allergy. Respiratory al- transmission human-to-human. The coronavirus disease
karger@karger.com © 2021 S. Karger AG, Basel Correspondence to:
www.karger.com/ned Francesca Galluzzi, francescagalluzzi @ yahoo.it(COVID-19) is an infectious disease ranging from a mild Although in the literature smell and taste disorders are
to more severe respiratory disease, whose common symp- well-documented symptoms of SARS-CoV-2 infection,
toms are fever, cough, dyspnea, sore throat, arthralgia, little is known about how these may be related to other
malaise, vomiting, abdominal pain, and headache. More- patients’ characteristics, disease severity, or type of treat-
over, a large number of COVID-19 patients also reported ment. In this perspective, the aim of this study is to inves-
olfactory and taste dysfunctions, rarely associated with tigate the prevalence and the risk factors associated with
rhinorrhea and/or nasal obstruction [1, 2]. Current stud- olfactory and gustatory dysfunctions in patients with in-
ies among COVID-19 patients have shown a relationship fection of SARS-CoV-2.
between SARS-CoV-2 infection and smell (hyposmia or
anosmia) and taste (dysgeusia or ageusia) disorders,
though olfactory dysfunction seems to be more prevalent Materials and Methods
than gustatory dysfunction [3, 4]. These symptoms have
Study Population
caught early the attention of otolaryngologists all over the We conducted an observational retrospective study on pa-
world, so they recommended adding loss of smell and tients with documented SARS-CoV-2 infection admitted to San
taste as screening symptoms for SARS-CoV-2 infection Gerardo Hospital in Monza, Italy, from March to July 2020. In
[5, 6]. Currently, the WHO officially included them as particular, the present study included 2 samples of patients: pa-
symptoms of COVID-19 disease [7]. The pathophysiol- tients discharged from COVID-19 departments and patients with
SARS-CoV-2 infection admitted to the emergency department
ogy leading to chemosensory dysfunction in SARS-CoV-2 without hospitalization. The following inclusion criteria were
infection is still unknown, albeit 2 mechanisms have been considered: (1) laboratory-confirmed SARS-CoV-2 infection by
suggested: a conductive olfactory dysfunction related to reverse transcription PCR and (2) age ≥18 years old. The exclu-
inflammation and damage of the olfactory epithelium [8, sion criteria were (1) olfactory and/or gustatory disorders prior to
9] and a sensorineural olfactory dysfunction due to an the SARS-CoV-2 infection; (2) presence of comorbidities such as
sinonasal diseases, craniofacial trauma, neurologic, and psychiat-
injury of the central olfactory processing pathways [10, ric disorders; (3) previous neurosurgical, otorhinolaryngological,
11]. Regarding taste dysfunction, it has been speculated or maxillofacial surgery that cause alterations in sinonasal appa-
that SARS-CoV-2 may utilize the same pathways used by ratus; and (4) inability or impossibility to complete the phone
angiotensin-2 converting enzyme (ACE2) inhibitors questionnaire.
drugs through a complex mechanism which involves G- This study protocol was approved by the Ethics Committee
(Comitato Etico Brianza, number 3385/2020) and prior to enrol-
protein-coupled protein and sodium channel present in ment each patient was invited to participate and gave the consent
the taste buds. The SARS-CoV-2 infects cells through the to enter the study. This trial was registered on ClinicalTrials.gov
ACE2 receptors and inactivates these by blocking the (number NCT04427332).
transformation of chemical gustatory signals into action
potential, and consequently taste perception [12]. Recent Data Collected
All patients answered a phone questionnaire (see online sup-
data suggest a role of spike protein mutation D614G that pl. material; see www.karger.com/doi/10.1159/000514888 for all
became dominant during the pandemic progression from online suppl. material) administrated by a resident otorhinolar-
East Asia to Western countries. This viral genetic variant yngologist (R.V.). Patients provided information on sociodemo-
facilitates infection of chemosensory epithelia increasing graphic characteristics, including sex, age, cigarette smoking
smell and taste impairment in COVID-19 patients [13]. status, and the occurrence of hospitalization. They were asked
about the presence of allergy (respiratory allergies/other) or oth-
Hannum et al. [4] in a recent meta-analysis including er comorbidities, antiflu vaccination execution, and home ther-
34 studies and 19,746 patients with SARS-CoV-2 infec- apies or hospital treatments for COVID-19. Specifically, they
tion calculated an overall prevalence of smell loss of were asked to indicate which type of drugs (hydroxychloro-
50.2%; when pooled across studies that used objective quine, tocilizumab, low-molecular-weight heparin, antiviral,
tests the average prevalence rate was 76.7% while consid- nonsteroidal anti-inflammatory drugs, and steroids) and/or re-
spiratory supports they received (continuous positive airway
ering studies that utilized subjective measures the preva- pressure; oxygen therapy or endotracheal intubation). In addi-
lence rate was 44.6%. Another recent systematic review tion, medical records were consulted in order to verify the infor-
and meta-analysis including 38,198 patients diagnosed mation, particularly for patients with a more severe course of
with COVID-19 reported a prevalence of smell loss of disease. Drugs and/or other treatments performed during the
43.04% and taste loss of 44.62% [14]. Considering the hospitalization were carefully detailed, also through check of the
clinical records. To investigate COVID-19 symptoms, patients
Italian studies included, prevalence varied widely, from were asked about the onset and the types of symptoms (fever,
19.4% [15] to 92% [16]. cough, dyspnea, arthralgia, headache, rhinitis, abdominal symp-
toms, and smell and/or taste disorders). Patients who reported
Risk Factors for Smell and Taste Loss in Neuroepidemiology 2021;55:154–161 155
COVID-19 DOI: 10.1159/000514888Table 1. Characteristics of the study population Table 2. Prevalence and characteristics of olfactory and gustatory
dysfunctions
N %
N %
Age, years (mean, SD) 60.8 (12.6)
Sex Olfactory dysfunction
Female 139 37.0 No 250 66.5
Male 237 63.0 Yes 126 33.5
Smoking Symptoms at month 1
Never 292 80.0 No 339 90.2
Past 65 17.8 Yes 37 9.8
Current 8 2.2 Symptoms at month 3
Missing 11 No 369 98.1
Hospitalization Yes 7 1.9
No 20 5.3 Onset
Yes 356 94.7 1–7 days before first symptoms 13 10.3
Allergies Concomitant to first symptoms 66 52.4
No 300 81.3 1–10 days after first symptoms 47 37.3
Yes 69 18.7 Duration of symptoms (day; median, IQR) 15 (14–30)
1 55 14.9 Gustatory dysfunctions
≥2 14 3.8 No 242 64.4
Respiratory 32 8.7 Yes 134 35.6
Other 37 10.0 Symptoms at month 1
Missing 7 No 344 91.5
Comorbidities Yes 32 8.5
No 119 32.2 Symptoms at month 3
Yes 251 67.8 No 371 98.7
1 108 29.2 Yes 5 1.3
2 76 20.5 Onset
3 47 12.7 1–7 days before first symptoms 6 4.5
≥4 20 5.4 Concomitant to first symptoms 70 52.2
Missing 6 1–10 days after first symptoms 58 43.3
Missing 6 Duration of symptoms (day; median, IQR) 14 (10–21)
Antiflu vaccination
No 312 86.0 IQR, interquartile range.
Yes 51 14.0
Missing 13
Drugs for COVID-19
No 25 6.8 Statistical Analysis
Yes 343 93.2 We calculated means and standard deviations or median and
Missing 8 interquartile range (IQR) for continuous variables, and absolute
Therapies for COVID-19 and relative frequencies for dichotomous/categorical data. Uncon-
No 59 16.1 ditional multiple logic regression models were used to compute the
Yes 308 83.9 odds ratios (ORs) and corresponding 95% confidence intervals
CPAP† 155 42.2 (CIs). The models were adjusted for age, sex, smoking status, hos-
O2† 148 40.3 pitalization, allergies, comorbidities, antiflu vaccination, drugs for
EI† 5 1.4 COVID-19, and therapies COVID-19. The level of statistical sig-
Missing 9 nificance was set up to p valueTable 3. Association of olfactory dysfunctions according to various covariates
N % OR (95% CI)* p value* OR (95% CI)** p value**
Age, yearsTable 4. Association of gustatory dysfunctions according to various covariates
N % OR (95% CI)* p value* OR (95% CI)** p value**
Age (years)tion, in which there was a predominance of males, indi- found that smoking is most likely associated with the neg-
viduals over 60 years, and patients hospitalized with the ative progression and adverse outcomes of the disease.
severe COVID-19. Consistently with this, previous data They included study conducted in China and they calcu-
reported a decrease in the prevalence of smell and/or taste lated that smokers were 1.4 times more likely (RR = 1.4
dysfunctions with older age, male sex, and disease sever- 95% CI: 0.98–2.00) to have severe symptoms of CO
ity [14]. Interestingly, the reduction of olfactory function VID-19 and 2.4 times more likely to be admitted to an
with age is a well-known phenomenon, though an age- intensive care unit, need mechanical ventilation or die
related effect may be expected, a sudden loss should be compared to nonsmokers (RR = 2.4, 95% CI: 1.43–4.04).
noticeable also in older patients. Regarding the impact of Olfactory dysfunction is a characteristic neurologic
sex in patients with chemosensory dysfunctions, data are symptom of COVID-19 [20], Kabbani et al. [21] specu-
still contradictory. We found that males have a lower risk lated that nicotine exposure can increase the risk for CO-
to develop olfactory dysfunctions. A recent systematic re- VID-19 neuroinfection based on known functional inter-
view reported no gender differences [17], while another action between the nicotine receptor and ACE2. Specifi-
one suggested a lower, though not significantly, preva- cally, they suppose that smoking can promote SARS-CoV-2
lence of smell and/or taste dysfunctions in females than cellular entry through the upregulation of nicotine acetyl-
in males [14]. The above considerations suggest that choline receptor that augmented ACE2 expression in
women tend to develop chemosensory dysfunctions. To neurons and astrocytes. However, the association be-
explain this, various hypotheses have been proposed, in- tween smoking habits and smell and/or taste dysfunc-
cluding the location of ACE2 on the chromosome X, a tions in COVID-19 patients is still debated. Indeed, other
hormonal effect, or the fact that women are more atten- studies did not document statistically significant associa-
tive to olfactory perception [14, 18]. tions [22–24].
Though olfactory and taste dysfunctions are well-es- A significant increase in olfactory dysfunctions was
tablished symptoms of SARS-CoV-2 infection, informa- observed for allergic patients, especially in case of respira-
tion concerning their onset and duration varied among tory allergy. To our knowledge, few previous studies doc-
studies. We found that smell and/or taste loss in about umented the presence of allergy as comorbidities in CO-
half of patients occurred concomitantly to the firsts CO- VID-19 patients with smell loss [1, 2, 25]. The frequency
VID-19 symptoms. Borsetto et al. [3] in a recent system- of olfactory dysfunction in patients with allergic rhinitis
atic review and meta-analysis on 3,563 patients with CO- ranged from 20 to 40%, and its presence seems to increase
VID-19 calculated that in mildly-to-moderate symptom- with the severity of the disease [26]. Allergy might predis-
atic patients smell and/or taste disorders was concomitant pose to viral infections due to delayed and deficient of the
to firsts symptoms in 28% patients, preceded in 20%, and innate type 1 and 3 interferons and/or deficient epithelial
occurred after in 54% patients. Comparing these data, we barrier function. Moreover, viral infections, including in-
can suppose that the timing of the onset of chemosensory fections with coronaviruses, are associated with worsen-
dysfunctions may depend on the severity of COVID-19. ing of allergies by stimulation of type 2 immune response
Again, Bartheld et al. [14] estimated that the duration of [27]. However, the pathogenetic mechanism of interac-
smell and/or taste loss was relatively shorter (mean of 8–9 tion between SARS-CoV-2 virus and nasal epithelium in
days) than our findings (median of 14 and 15 days). allergic patients is still unknown. According to Wang et
Moreover, we have assessed that chemosensory dysfunc- al. [28], ACE2 expression in nasal tissue is not altered in
tions resolved at 3 months in 98% of patients. These data allergic rhinitis and the expression in airway epithelial
together support the hypotheses of a transitory pathoge- cells seems to be regulated by effect of IFN and type 2 in-
netic mechanism of damage such as olfactory neuron in- flammation.
jury, support-cell mediated dysfunction of the olfactory Finally, our analysis has shown that having comorbid-
epithelium or a virus-induced shot lasting immune re- ities, receiving respiratory support therapies for CO
sponse [8, 9]. VID-19, and particularly hospitalization were protective
The analysis of risk factors for chemosensory dysfunc- factors for the development of smell and/or taste dysfunc-
tions revealed a strong association between active smok- tions in hospitalized patients who usually presented mod-
ing and smell loss. This result should be interpreted with erate to severe COVID-19 disease. This suggests that
caution considering the small number of current smokers these symptoms may be characteristic of less severe
included. Vardavas et al. [19] in a systematic review SARS-CoV-2 infection as previously reported by Vacchi-
studying the relationship between smoke and COVID-19 ano and colleagues [29].
Risk Factors for Smell and Taste Loss in Neuroepidemiology 2021;55:154–161 159
COVID-19 DOI: 10.1159/000514888Among the limitations of our study, it should be con- Brianza, number 3385/2020) and prior to enrolment each patient
sidered that all data were self-reported and based on was invited to participate and gave the consent to enter the study.
This trial was registered on ClinicalTrials.gov (number
phone questionnaire; therefore, it was possible that pa- NCT04427332).
tients over/underestimated symptoms. In addition, pa-
tients were not assessed for smell and taste loss using
quantitative measures. Moreover, our study was retro- Conflict of Interest Statement
spective and involved patients with SARS-CoV-2 infec-
tion without a control group. The authors have no conflicts of interest to declare.
In conclusion, our study reports that olfactory and
gustatory dysfunctions are characteristics symptoms of
COVID-19 in about of third of patients. Current smokers Funding Sources
and allergic patients have significantly increased risk for
The authors did not receive any funding for this work.
smell loss. On the contrary, hospitalization reduces the
risk of olfactory and gustatory dysfunctions, suggesting
that these symptoms may be characteristic of less severe
Author Contributions
SARS-CoV-2 infection. Further studies are needed to elu-
cidate these preliminary data. Prof. Garavello and Dr. Galluzzi conceptualized and designed
the study, performed the literature search, analyzed data, and
drafted the work. Dr. Rossi performed the literature search, col-
Statement of Ethics lected data, and revised the manuscript. Dr. Bosetti analyzed data
and revised the work. All the authors approved the final manu-
The research was conducted ethically in accordance with the script as submitted and agree to be accountable for all aspects of
World Medical Association Declaration of Helsinki. This study the work.
protocol was approved by the Ethics Committee (Comitato Etico
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