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Clinical Observation  |  Open Access  |  29 May 2022

Olfactory and gustatory dysfunctions in patients with COVID-19 in Wuhan, China

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Ageing Neur Dis 2022;2:8.
10.20517/and.2022.09 |  © The Author(s) 2022.
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Abstract

The coronavirus disease 2019 (COVID-19) is spreading all over the world. The main symptoms of COVID-19 include fever, cough, fatigue, and myalgia. However, there are few reports on olfactory and gustatory dysfunctions in patients with COVID-19. Our objective was to investigate the incidence of olfactory and gustatory dysfunctions in patients with COVID-19 infection in Wuhan, China. In this retrospective study, we collected 81 confirmed cases of COVID-19 from the Renmin Hospital of Wuhan University from February 2020 to March 2020, and analyzed the demographic characteristics, clinical manifestations (including olfactory and gustatory dysfunctions), laboratory findings, and comorbidities. In total, 81 confirmed COVID-19 patients were enrolled in this study (38 males and 43 females). The study showed that the most prevalent symptoms included cough, myalgia, and loss of appetite. On admission, 25 (30.9%) of all patients reported either olfactory dysfunction (OD) or gustatory dysfunction (GD), and 7 (8.6%) reported both OD and GD. Overall, 13.6% and 25.9% of all patients reported OD and GD, respectively. OD and GD were not associated with disease severity. Pearson correlation analysis identified some factors that are correlated with OD and GD, including headache or dizziness (r = 0.342, P = 0.002), dark urine (r = 0.256, P = 0.021), IgM titer (r = 0.305, P = 0.01), and diabetes (r = 0.275, P = 0.013). Multivariate adjusted logistic analysis showed that patients with headache or dizziness (OR = 7.382, 95%CI: 1.028-53.022) and diabetics (OR = 6.871, 95%CI: 1.096-43.086) were at higher risk of developing OD. In addition, patients with high IgM titers (OR = 1.006, 95%CI: 1.000-1.006) and diabetes (OR = 4.335, 95%CI: 1.098-17.287) were at high risk of developing GD. In 81.8% of the cases with OD and 28.6% of the cases with GD, the symptoms lasted for at least one month after discharge. In addition, 3.6% of inpatients without OD developed OD after discharge. These findings suggest that OD and GD are common in COVID-19. These symptoms appear early during the course of the disease and may last for one month. The incidence of OD and GD is related to neurological manifestations, diabetics, and IgM titers.

Keywords

COVID-19, SARS-CoV-2, smell, taste, infection

INTRODUCTION

Coronavirus disease 2019 (COVID-19), an infectious disease caused by the acute respiratory syndrome coronavirus-2 (SARS-CoV-2), has spread globally. As of March 20, 2022, there have been more than 464 million confirmed cases of COVID-19 globally[1]. Early epidemiological investigations show that the basic reproduction number (R0) of SARS-CoV-2 is estimated to be about 2.2 (range, 1.4-6.5)[2]. The high spread and low fatality rate of COVID-19 made it a global pandemic. COVID-19 has become the largest pandemic since the H1N1 flu outbreak in 1918. Early genetic tests emphasized that the genome sequence identity of SARS-CoV-2 and SARS-CoV is 79.5%. Both viruses infect cells through angiotensin-converting enzyme 2 (ACE2)[3,4]. The similarity of the gene sequence and infection route suggests that SARS-CoV-2 and SARS-CoV have similar clinical manifestations. Similar to SARS, the most common symptoms of COVID-19 are fever, cough, sputum, fatigue, and myalgia[5-7]. Complications of COVID-19 involve multiple systems, such as the cardiovascular system, digestive system, and nervous system[8-10]. Current research mainly focuses on central nervous system complications such as cerebrovascular diseases and acute encephalopathy[10], while less is known about the peripheral nervous system complications. Symptoms in the head and neck such as dry eyes, tearing, and smell and taste disturbances were reported in COVID-19 patients and believed to be related to the neurophagy of the virus[11-12]. It is worth noting that SARS-CoV can be detected 60-66 h after infection and is most abundant in the olfactory bulb[13]. In addition, the virus may enter the brain through the olfactory bulb. Viral antigens can also be detected in brain areas connected to the olfactory bulb, such as the piriform nucleus and subliminal leather, basal ganglia, and midbrain[14,15].

The purpose of this study was to investigate the incidence of olfactory and taste disorders in confirmed COVID-19 cases and to analyze the risk factors related to olfactory and gustatory dysfunctions in order to provide clues for the clinical diagnosis and treatment of COVID-19.

METHODS

Patient enrollment and data collection

This descriptive study included 81 inpatients diagnosed with COVID-19 in the Renmin Hospital of Wuhan University, Wuhan, China. The diagnosis of COVID-19 was based on clinical symptoms, computed tomography (CT), real-time RT-PCR, and next-generation sequencing. The patient’s admission date was from February 1 to March 3, 2020. All patients participating in this study lived in Wuhan during the COVID-19 outbreak. Two well-trained investigators collected the data including demographic characteristics, clinical characteristics (including medical history, comorbidities, and symptoms), preliminary laboratory findings, treatment, and clinical outcomes.

According to the SARS-CoV-2 diagnosis and treatment guidelines (Versions 3-7) issued by the National Health Commission of China, the severity of COVID-19 patients was defined. Severe cases were designated when the patients fit one of the following criteria: (1) respiratory distress with respiratory rate ≥ 30/min; (2) oxygen saturation ≤ 93% at rest; (3) arterial partial oxygen pressure (PaO2)/oxygen absorption concentration (FiO2) ≤ 300 mmHg; (4) respiratory failure that needs mechanical ventilation; or (5) shock or organ failure requiring ICU care.

Procedures

Two investigators collected the information on epidemiology, clinical symptoms, laboratory test results, treatment, and clinical outcomes. Laboratory tests included routine blood examination (including white blood cells, lymphocytes, and platelets), coagulation function, lactate dehydrogenation, and immune indicators (including lymphocyte differential counts and inflammatory factors). Participants were interviewed by telephone and were asked to report their olfactory and gustatory dysfunctions at the time of hospitalization and one month after discharge. Two years after discharge, those with olfactory and gustatory dysfunctions one month after discharge were re-interviewed to report their smell and taste status. Verbal informed consent was obtained from all participants or their legal guardians. The severity of symptoms was graded as totally normal, mild, moderate, and severe. Totally normal means that respondents rated smell and taste as “Good” or “Unaffected”, mild dysfunction means the patient hardly noticed a smell and taste reduction, moderate dysfunction means there was a noticeable reduction, and severe dysfunction means the patient reported an almost complete loss of smell and taste. Patients with olfactory and gustatory dysfunctions before contracting COVID-19 were excluded, and so were patients with a diagnosis of chronic rhinitis, Alzheimer’s disease (AD), or Parkinson’s disease (PD) on admission. We also asked patients during the telephone interview whether they had a history of chronic rhinitis, AD, or PD. These patients might experience olfactory and gustatory dysfunctions, which could affect the study results. Cases with unsuccessful follow-ups were excluded.

Statistical analysis

Continuous variables were described as medians and interquartile range (IQR), and categorical variables were described as frequency rates and percentages. We used the chi-square (χ2) test or the Fisher’s exact test to compare categorical data. Mann-Whitney-Wilcoxon test was applied to compare non-normally continuous variables. Pearson correlation analysis was used to examine the correlations between olfactory/gustatory dysfunctions and all indicators (including epidemiology, clinical symptoms, laboratory test results, treatment, and disease severity). The sample size varied due to missing data, and missing data were not imputed. The analyses regarding different factors were based on non-missing data. Multivariate adjusted logistic regression models were adopted to analyze the factors influencing olfactory and gustatory dysfunction in patients with COVID-19. All statistical analyses were performed using SPSS software (V.23.0). Two-tailed P values were considered statistically significant at < 0.05. This study was approved by the Hospital Ethics Committee of the Renmin Hospital of Wuhan University (WDRY2020-K136).

RESULTS

Demographic characteristics in COVID-19

The demographic characteristics, clinical manifestations, and comorbidities are shown in Table 1. Of the 81 patients, 63 cases were diagnosed as non-severe and 18 cases were severe. The median age was 58 years (IQR, 50.0-68.5 years). The median age of the severe group was 11.5 years older than that of the non-severe group. Males accounted for 46.9% (38 of 81) of the total patients. However, males accounted for 66.7% (12 of 18) of patients in the severe group compared with 41.3% (26 of 63) of the non-severe group. These results suggest that males and older patients are more likely to develop into severe cases, which is consistent with other reports[16]. On admission, the most common clinical manifestations were fever (72.8%) and respiratory symptoms (70.4%), while chest pain, fatigue, gastrointestinal symptoms, dark urine, and headache or dizziness accounted for 27.2%, 37%, 27.2%, 19.8%, and 14.8% of the patients, respectively. Compared with the non-severe group, the severe group had a higher proportion of dark urine (17.5% vs. 27.8%), suggesting a potential relationship between urinary system dysfunction and disease severity. Among the 81 cases, 51.9% had at least one comorbidity, including hypertension, diabetes, coronary heart disease, stroke, cancers, and chronic pulmonary diseases. Compared with the non-severe group, more patients in the severe group had a history of stroke (0% vs. 5.6%) and coronary heart disease (1.6% vs. 11.1%), suggesting that patients with cardiovascular and cerebrovascular diseases are more likely to develop severe illness. The above findings are consistent with previous studies[17-19].

Table 1

Demographic characteristics of the 81 patients with COVID-19

Clinical characteristics and symptomsAll patients (n = 81)Disease severity
Non-severeSevere
(n = 63)(n = 18)
Age, median (IQR) - years58 (50.00-68.50)57 (49.00-67.00)68.5 (56.25-77.25)
Age groups - No., %
     < 6551 (63.0)45 (71.4)6 (33.3)
     ≥ 6530 (37.0)18 (28.6)12 (66.7)
Gender - No., %
     Male38 (46.9)26 (41.3)12 (66.7)
     Female43 (53.1)37 (58.7)6 (33.3)
Symptoms or signs - No., %
     Fever on admission59 (72.8)46 (73.0)12 (72.2)
     Chest distress22 (27.2)19 (30.2)3 (16.7)
     Fatigue30 (37.0)23 (36.5)7 (38.9)
     Headache or dizziness12 (14.8)9 (14.3)3 (16.7)
     Respiratory symptoms57 (70.4)45 (71.4)12 (66.7)
     Gastrointestinal symptoms22 (27.2)17 (27.0)5 (27.8)
     Dark urine16 (19.8)11 (17.5)5 (27.8)
Coexisting disorders - No., %
     Any42 (51.9)30 (47.6)12 (66.7)
     Hypertension23 (28.4)17 (27.0)6 (33.3)
     Diabetes15 (18.5)12 (19.0)3 (16.7)
     Coronary heart disease3 (3.7)1 (1.6)2 (11.1)
     Stroke1 (1.2)0 (0.0)1 (5.6)
     Cancer*6 (7.4)4 (6.3)2 (11.1)
     Chronic pulmonary disease#7 (8.6)5 (7.9)2 (11.1)

Olfactory and gustatory dysfunctions in COVID-19

Table 2 summarizes the incidence of olfactory dysfunction (OD) and gustatory dysfunction (GD) when the patients were admitted to the hospital. On admission, 30.9% of all patients reported an altered sense of smell or taste. Overall, 13.6% and 25.9% reported OD and GD, respectively, while 8.6% reported both OD and GD. The incidence of OD in the severe group (11.1%) was not significantly different from that in the non-severe group (14.3%). Compared with the non-severe group, the incidence of GD was lower in the severe group (28.6% vs. 16.7%). However, OD and GD do not seem to be related to the severity of the disease (Fisher’s exact test, P < 0.05).

Table 2

The incidence of olfactory and gustatory dysfunctions in patients with different disease severity

Disease severityOlfactory dysfunctionGustatory dysfunctionOD and GDAny
TotalMildModerateSevereTotalMildModerateSevere
Non-severe - n/%9 (14.3)*5 (7.9)1 (1.6)3 (4.8)18 (28.6)*8 (12.7)7 (11.1)3 (4.8)5 (7.9)*22 (34.9)*
Severe2 (11.1)0 (0.0)1 (5.6)1 (5.6)3 (16.7)1 (5.6)1 (5.6)1 (5.6)2 (11.1)3 (16.7)
All patients11 (13.6)5 (6.2)2 (2.5)4 (4.9)21 (25.9)9 (11.1)8 (9.9)4 (4.9)7 (8.6)25 (30.9)

The factors related to OD and GD are summarized in Table 3. We considered general conditions, symptoms, comorbidities, and laboratory tests and calculated the Pearson correlation coefficient. Some factors were positively correlated with OD, including headache or dizziness (r = 0.342, P = 0.002), dark urine (r = 0.256, P = 0.021), IgM titer (r = 0.305, P = 0.01), and diabetes (r = 0.275, P = 0.013). These factors were also positively correlated to GD (all r > 0.2, P < 0.05). The IgG titers were not significantly related to patients with OD (r = 0.083, P = 0.496) or GD (r = 0.164, P = 0.176). However, IgG titers were associated with the incidence of patients with either OD or GD (r = 0.269, P < 0.05).

Table 3

Factors associated with olfactory and gustatory dysfunctions in COVID-19

FactorsODGDOD or GD
rP valuerP valuerP value
Headache or dizziness0.3420.0020.3080.0050.2480.026
Dark urine0.2560.0210.2730.0140.2730.014
IgM0.3050.010.2380.0460.2510.035
IgG0.0830.4960.1640.1760.2690.024
Diabetes0.2750.0130.2980.0070.3010.006

The association between various factors and the risk of olfactory and gustatory dysfunction in patients with COVID-19 is shown in Table 4. In the multivariate adjusted logistic regression model, patients with headache and dizziness (adjusted OR = 7.382, 95%CI: 1.028-53.022) were more likely to have olfactory dysfunction than those without headache and dizziness. Patients with diabetes had a higher risk of olfactory dysfunction compared to those without diabetes (adjusted OR = 6.871, 95%CI: 1.096-43.086). In the logistic regression analysis of gustatory dysfunctions, patients with high IgM titers had a higher risk of developing gustatory dysfunctions compared to those with low IgM titers (adjusted OR = 1.003, 95%CI: 1.000-1.006). In addition, patients with diabetes had a higher risk of developing GD compared to patients without diabetes (adjusted OR = 4.335, 95%CI: 1.098-17.287). Similarly, when OD and GD were treated as one symptom, patients with diabetes (adjusted OR = 7.963, 95%CI: 1.557-37.515) and patients with higher IgM titers (adjusted OR = 1.006, 95%CI: 1.001-1.010) had a higher probability of developing this symptom.

Table 4

Multivariate adjusted logistic regression of olfactory and gustatory dysfunctions

VariablesβSEWaldAdjusted OR95%CIP
OD
     Headache or dizziness1.9991.0063.9497.3821.028-53.0220.047
     Dark urine0.6561.0400.3971.9270.251-14.7960.528
     IgM0.0020.0021.8671.0020.999-1.0060.172
     IgG-0.0010.8983.6715.5910.961-32.5150.055
     Diabetes1.9270.9374.2346.8711.096-43.0860.040
     Constant-3.2580.75918.412
GD
     Headache or dizziness1.3580.7892.9633.8900.828-18.2630.085
     Dark urine0.4320.8060.2871.5400.317-7.4720.592
     IgM0.0030.0024.0581.0031.000-1.0060.044
     IgG0.0010.0020.4801.0010.998-1.0040.488
     Diabetes1.4710.7034.3874.3351.098-17.2870.036
     Constant-2.0980.53115.591
OD or GD
     Headache or dizziness1.2970.8412.3873.6590.704-19.0260.123
     Dark urine0.3380.8680.1511.4020.256-7.6840.697
     IgM0.0060.0026.9611.0061.001-1.0100.008
     IgG0.0030.0022.5261.0030.999-1.0070.112
     Diabetes2.0400.7146.3697.9631.557-37.5150.012
     Constant-2.4790.58917.727

Table 5 describes the incidence of OD and GD one month after the patients were discharged from the hospital. Six patients had residual GD, and eleven patients reported OD. Of patients with OD or GD during hospitalization, 48.0% still complained of OD or GD one month after discharge. In patients with no OD or GD during hospitalization, 3.6% developed OD or GD after discharge. Continued follow-up of these patients with OD or GD showed that, in 60% (6 of 10) of the cases with OD and 20% (1 of 5) of the cases with GD, the symptoms lasted for at least two years; in 20% (2 of 10) of the cases with OD, symptoms aggravated. One OD patient and one GD patient lost in follow-up were excluded. We also analyzed the relationship between treatment and the incidences of olfactory and urinary dysfunction after discharge [Supplementary Table 1] and found that treatments had no effect on the clinical outcomes of OD and GD after patients were discharged, suggesting that the OD and GD are most likely primary symptoms caused by SARS-CoV-2, rather than the side effects of drugs.

Table 5

The clinical outcomes of olfactory and gustatory dysfunctions in COVID-19 patients

During hospitalizationAfter discharged*
ODGDOD and GDOD or GD
(n = 11)(n = 6)(n = 3)(n = 14)
None - n/%2 (3.6)0 (0.0)0 (0.0)2 (3.6)
OD9 (81.8)3 (27.3)3 (27.3)9 (81.8)
GD6 (28.6)6 (28.6)3 (14.3)9 (42.9)
OD and GD6 (85.7)3 (42.9)3 (42.9)6 (85.7)
Any9 (36.0)6 (24.0)3 (12.0)12 (48.0)

DISCUSSION

This retrospective descriptive study included 81 confirmed cases of COVID-19 and focused on the OD and GD in COVID-19 patients in Wuhan. On admission or during hospitalization, patients self-reporting OD, GD, and both accounted for 13.6%, 25.9%, and 8.6% of all subjects, respectively. The incidence of OD and GD in the severe cases was not significantly different from the non-severe cases, suggesting OD and GD are not related to the severity of the disease. In addition, 48.0% of patients had persistent OD or GD after the other clinical manifestations of COVID-19 disappeared. Continued follow-up showed that, in 20% of the cases with OD, symptoms even aggravated two years after infection.

There are currently few studies on the incidence of OD and GD in patients with COVID-19[20]. One study found that 5.1% of COVID-19 patients reported hyposmia[21]. Compared with this study, we found a higher rate of hyposmia (13.6%). A multicenter European study reported that 85.6% and 88.0% of patients suffer from olfactory and gustatory dysfunctions, respectively[22]; this result indicates that, compared with Asian patients, gustatory dysfunctions are more common in European patients. Notably, a recent study found that the prevalence of smell and taste dysfunction in COVID-19 patients has dropped significantly with the advent of the Omicron variant[23]. Thus, the different strains of the virus may have distinct effects on olfactory and gustatory dysfunction.

The reasons for the different incidences of OD and GD may be as follows: (1) Quantitative measurement is more sensitive than self-report. Studies have shown that only 35% of patients are aware of their olfactory deficits[24]. (2) The different affinity of the virus to different populations may lead to clinical differences among patients in different regions. A study showed that ACE2 mutations reduce the correlation between human ACE2 and SARS-CoV S-protein, thereby reducing the chance of infection[25]. ACE2 polymorphisms and the differences in expression levels between Asian and European populations may explain the difference in olfactory dysfunction between Asian and European populations[26]. (3) Different strains of the virus may cause different clinical manifestations.

Pearson correlation coefficient showed that headache or dizziness, dark urine, IgM, and diabetes all showed a positive correlation with OD and GD (all P < 0.05). We noted that chronic rhinitis and certain neurodegenerative diseases may directly lead to taste or smell disorders. In this study, such patients were excluded. Headache or dizziness are the most common symptoms of the nervous system. In a previous report, the incidence of headache and dizziness in COVID-19 patients were 13.1% and 16.8%, respectively[21]. OD and GD are positively related to dizziness and headache. It has been reported that ACE2 is highly expressed in the nasal goblet and ciliated cells[27]. The virus may infect the olfactory nerve early and cause OD before other neurological manifestations. OD and GD were also significantly related to dark urine. This may suggest that dark urine, similar to OD/GD, is a sign of early infection and damage to the urinary system. IgM is an early antibody produced by the immune system after infection. The interaction of infectivity, virulence, and immune response may explain the positive correlation between IgM and OD/GD. Consistent with other results, diabetes was significantly correlated with smell dysfunction[28]. The infection might exacerbate potential nerve damage in diabetic patients. In addition, multivariate adjusted logistic analysis showed that patients with headache or dizziness and diabetics were at higher risk of developing olfactory dysfunction, while patients with high IgM titers and diabetes were at high risk of developing gustatory dysfunction, which is consistent with the results of the above Pearson correlation coefficient.

One month or more after discharge, some patients still suffered from OD and GD. A few patients who did not have OD or GD during hospitalization developed these symptoms after discharge. Considering the damage caused by the virus to the olfactory or gustatory nerve, this may be one of the possible sequelae of COVID-19 patients. It is worth noting that SARS-CoV can be detected 60-66 h after infection and is most abundant in the olfactory bulb[29]. While the infection routes of SARS-CoV-2 and SARS-CoV are similar, OD may be an early symptom of COVID-19. Early screening of people with OG and GD, early detection of virus infections, and early isolation of COVID-19 patients can help prevent the spread of COVID-19.

In conclusion, we found that OD and GD are common symptoms of COVID-19. They appear early during the disease and may last from one month to even two years. Headache or dizziness, IgM titers, and diabetes are correlated with the occurrence of OD and GD. This retrospective study has some limitations. First, we collected self-reported data, which may lead to information bias. Second, the sample size was relatively small and geographically limited. We only recruited 81 confirmed cases of COVID-19 in our database since COVID-19 infectious was effectively controlled in Wuhan in early 2020. The cases reported here represent what happened to the first batch of patients in China. Third, grading bias might exist since we did not perform objective smell and taste tests. Fourth, as patients with other infectious diseases were not included in the control group, it could not be determined whether COVID-19 had a more severe and longer-lasting impact on taste and smell than other infectious diseases.

DECLARATIONS

Authors’ contributions

Full access to all of the data in the study, take responsibility for the integrity of the data and the accuracy of the data analysis, and wrote the manuscript: Zou L

The acquisition of data: Yu T, Zhang Y

Reviewed literature and gave technical support: Dai L

Conceived and supervised the project: Zhang Z, Zhang Z

All authors read and approved the submission of the manuscript.

Availability of data and materials

All analyzed data of this study are included within the article.

Financial support and sponsorship

This work was supported by grants from the National Natural Science Foundation of China (No. 81822016 and 81771382) and Medical Science Advancement Program of Wuhan University (No. TFLC2018001).

Conflicts of interest

All authors declared that there are no conflicts of interest.

Ethical approval and consent to participate

This study was approved by the Hospital Ethics Committee of the Renmin Hospital of Wuhan University [WDRY2020-K136].

Consent for publication

All patients agreed to participate in this study.

Copyright

© The Author(s) 2022.

Supplementary Materials

REFERENCES

1. WHO Coronavirus (COVID-19) Dashboard. Available from: https://www.who.int/redirect-pages/page/novel-coronavirus-(covid-19)-situation-dashboard [Last accessed on 26 May 2022].

2. Adhikari SP, Meng S, Wu YJ, et al. Epidemiology, causes, clinical manifestation and diagnosis, prevention and control of coronavirus disease (COVID-19) during the early outbreak period: a scoping review. Infect Dis Poverty 2020;9:29.

3. Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 2020;579:270-3.

4. Dutta K. Allosteric site of ACE-2 as a drug target for COVID-19. ACS Pharmacol Transl Sci 2022;5:179-82.

5. do Nascimento IJ, O’Mathúna DP, von Groote TC, et al; International Network of Coronavirus Disease 2019 (InterNetCOVID-19). Coronavirus disease (COVID-19) pandemic: an overview of systematic reviews. BMC Infect Dis 2021;21:525.

6. da Rosa Mesquita R, Francelino Silva Junior LC, Santos Santana FM, et al. Clinical manifestations of COVID-19 in the general population: systematic review. Wien Klin Wochenschr 2021;133:377-82.

7. Neto AR, Carvalho ARB, Oliveira EMN, Magalhães RLB, Moura MEB, Freitas DRJ. Symptomatic manifestations of the disease caused by coronavirus (COVID-19) in adults: systematic review. Rev Gaucha Enferm 2021;42:e20200205.

8. Zheng YY, Ma YT, Zhang JY, Xie X. COVID-19 and the cardiovascular system. Nat Rev Cardiol 2020;17:25960.

9. Han C, Duan C, Zhang S, et al. Digestive symptoms in COVID-19 patients with mild disease severity: clinical presentation, stool viral RNA testing, and outcomes. Am J Gastroenterol 2020;115:916-23.

10. Portela-Sánchez S, Sánchez-Soblechero A, Melgarejo Otalora PJ, et al. Neurological complications of COVID-19 in hospitalized patients: the registry of a neurology department in the first wave of the pandemic. Eur J Neurol 2021;28:3339-47.

11. Meduri A, Oliverio GW, Mancuso G, et al. Ocular surface manifestation of COVID-19 and tear film analysis. Sci Rep 2020;10:20178.

12. Freni F, Meduri A, Gazia F, et al. Symptomatology in head and neck district in coronavirus disease (COVID-19): a possible neuroinvasive action of SARS-CoV-2. Am J Otolaryngol 2020;41:102612.

13. Netland J, Meyerholz DK, Moore S, Cassell M, Perlman S. Severe acute respiratory syndrome coronavirus infection causes neuronal death in the absence of encephalitis in mice transgenic for human ACE2. J Virol 2008;82:7264-75.

14. Leyva-Grado VH, Churchill L, Wu M, et al. Influenza virus- and cytokine-immunoreactive cells in the murine olfactory and central autonomic nervous systems before and after illness onset. J Neuroimmunol 2009;211:73-83.

15. Wheeler DL, Athmer J, Meyerholz DK, Perlman S. Murine olfactory bulb interneurons survive infection with a neurotropic coronavirus. J Virol 2017;91:e01099-17.

16. Grasselli G, Zangrillo A, Zanella A, et al. COVID-19 Lombardy ICU Network. Baseline characteristics and outcomes of 1591 patients infected with SARS-CoV-2 admitted to ICUs of the lombardy region, Italy. JAMA 2020;323:1574-81.

17. Zhang JJ, Dong X, Cao YY, et al. Clinical characteristics of 140 patients infected with SARS-CoV-2 in Wuhan, China. Allergy 2020;75:1730-41.

18. Guan WJ, Ni ZY, Hu Y, et al. China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 2020;382:1708-20.

19. Wang D, Hu B, Hu C, et al. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 2020;323:1061-9.

20. Ghods K, Alaee A. Olfactory and taste disorders in patients suffering from Covid-19, a review of literature. J Dent (Shiraz) 2022;23:1-6.

21. Mao L, Jin H, Wang M, et al. Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol 2020;77:683-90.

22. Lechien JR, Chiesa-Estomba CM, De Siati DR, et al. 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;277:2251-61.

23. Boscolo-Rizzo P, Tirelli G, Meloni P, et al. Coronavirus disease 2019 (COVID-19)-related smell and taste impairment with widespread diffusion of severe acute respiratory syndrome-coronavirus-2 (SARS-CoV-2) Omicron variant. Int Forum Allergy Rhinol 2022; doi: 10.1002/alr.22995.

24. Giacomelli A, Pezzati L, Conti F, et al. Self-reported olfactory and taste disorders in patients with severe acute respiratory coronavirus 2 infection: a cross-sectional study. Clin Infect Dis 2020;71:889-90.

25. Li W, Zhang C, Sui J, et al. Receptor and viral determinants of SARS-coronavirus adaptation to human ACE2. EMBO J 2005;24:1634-43.

26. Cao Y, Li L, Feng Z, et al. Comparative genetic analysis of the novel coronavirus (2019-nCoV/SARS-CoV-2) receptor ACE2 in different populations. Cell Discov 2020;6:11.

27. Sungnak W, Huang N, Bécavin C, Berg M. HCA Lung Biological Network. SARS-CoV-2 entry genes are most highly expressed in nasal goblet and ciliated cells within human airways. ArXiv 2020;arXiv:2003.06122v1.

28. 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;10:944-50.

29. Weiss SR, Navas-Martin S. Coronavirus pathogenesis and the emerging pathogen severe acute respiratory syndrome coronavirus. Microbiol Mol Biol Rev 2005;69:635-64.

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Zou L, Yu T, Zhang Y, Dai L, Zhang Z, Zhang Z. Olfactory and gustatory dysfunctions in patients with COVID-19 in Wuhan, China. Ageing Neur Dis 2022;2:8. http://dx.doi.org/10.20517/and.2022.09

AMA Style

Zou L, Yu T, Zhang Y, Dai L, Zhang Z, Zhang Z. Olfactory and gustatory dysfunctions in patients with COVID-19 in Wuhan, China. Ageing and Neurodegenerative Diseases. 2022; 2(2): 8. http://dx.doi.org/10.20517/and.2022.09

Chicago/Turabian Style

Zou, Li, Ting Yu, Yangyang Zhang, Lijun Dai, Zhaohui Zhang, Zhentao Zhang. 2022. "Olfactory and gustatory dysfunctions in patients with COVID-19 in Wuhan, China" Ageing and Neurodegenerative Diseases. 2, no.2: 8. http://dx.doi.org/10.20517/and.2022.09

ACS Style

Zou, L.; Yu T.; Zhang Y.; Dai L.; Zhang Z.; Zhang Z. Olfactory and gustatory dysfunctions in patients with COVID-19 in Wuhan, China. Ageing. Neur. Dis. 2022, 2, 8. http://dx.doi.org/10.20517/and.2022.09

About This Article

© The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, sharing, adaptation, distribution and reproduction in any medium or format, for any purpose, even commercially, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

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Ageing and Neurodegenerative Diseases
ISSN 2769-5301 (Online)

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