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In this study, a total of 11 patients with COVID-19 and OD were enrolled. Only one patient also had GD. All the patients were imported from other countries and treated in Xi’an No. 8 Hospital. During this period, a total of 246 imported COVID-19 cases were reported; thus, the proportion of OD among the overall imported case total was 4.5% (11/246).
The median patient age was 34 (IQR 23–46) years; 81.8% (9/11) were men, and 27.3% (3/11) had comorbidities (hypertension in two cases and hepatitis B in one case). Of the total OD cases, 54.5% (6/11) and 45.5% (5/11) had moderate and mild COVID-19, respectively. Of the 11 patients, 72.7% (8/11) had normal weight, 18.2% (2/11) were overweight, and 9.1% (1/11) had obesity. All the patients were diagnosed upon entering China; of these, 63.6% (7/11) were from Asia (two from Kazakhstan, three from Uzbekistan, and two from the United Arab Emirates), 18.2% (2/11) were from Africa (Angola and Liberia), and the other 18.2% (2/11) were from Europe (Belgium and the UK). Detailed characteristics are shown in Table 1 and Figure 1.
Table 1. Demographics, clinical characteristics, treatment outcomes, and follow up of 11 imported COVID-19 cases with olfactory dysfunction
Characteristics Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Case 10 Case 11 Age (years) 19 52 22 37 23 23 35 24 47 46 34 Gender Male Male Male Male Male Female Male Female Male Male Male Occupation Student Salary employee Student Semi-skilled employee Salary employee Unemployed Salary employee Student Salary employee Salary employee Semi-skilled employee Body mass index (kg/m2) 24.8 23.7 23.7 24.2 20.0 18.8 20.0 22.1 28.7 22.6 23.0 Comorbidity Hypertension Hypertension No No No No No No No Hepatitis B No Complication No No No Liver injury No No No No Liver injury No No Imported country Kazakhstan Kazakhstan Britain Liberia United Arab Emirates United Arab Emirates Uzbekistan Uzbekistan Angola Uzbekistan Belgium Clinical classification Mild Moderate Mild Moderate Mild Mild Moderate Mild Moderate Moderate Moderate Symptoms and signs Hyposmia Yes No No Yes Yes No Yes No Yes No Yes Anosmia No Yes Yes No No Yes No Yes No Yes No Hypogeusia No No No No No No Yes No No No No Fever No No No No No No No No No No Yes Cough No No No Yes No No Yes Yes No Yes Yes Fatigue No Yes No No No No No No No No No Rhinorrhea No No No No No No No No No No No Nasal congestion No No No No No Yes No No No No No Sore throat No No No Yes No Yes No Yes Yes No No Myalgia No No No No No No No No No No No Diarrhea No No No No No No No No Yes No No Treatment Antiviral Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Antibiotic No No No Yes No No No No Yes No Yes Traditional Chinese medicine Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Corticosteroids No No No Yes No No No No Yes No Yes Intravenous
immunoglobinNo Yes Yes Yes Yes No Yes No Yes Yes Yes Hepatoprotective
therapyNo No No Yes No Yes Yes Yes Yes Yes Yes Treatment outcome Cured Cured Cured Cured Cured Cured Cured Cured Cured Cured Cured Follow up 1-month OD No recovery* Recovery No recovery* Recovery Recovery No recovery* Recovery Partial recovery# Recovery Recovery Recovery Other sequelae Anxiety, fatigue, difficulty sleeping No No No No Throat discomfort, Fatigue, No No Fatigue Difficulty sleeping, Fatigue Throat discomfort Re-positive Yes No Yes No No Yes No No No No No 6-month OD Partial recovery# No Partial recovery# Recovery Recovery Partial recovery# Recovery Recovery OD Recovery Recovery Other sequelae Hair loss, anxiety, fatigue and difficulty sleeping No No No No Throat discomfort No No Fatigue Difficulty sleeping Throat discomfort, hair loss Re-positive No No No No No No No No No No No 12-month OD Partial recovery# Recovery Recovery Recovery Recovery Recovery Recovery Recovery Partial recovery# Recovery Recovery Other sequelae Hair loss, anxiety, fatigue, difficulty sleeping No No No No Throat discomfort No No Fatigue Difficulty sleeping Hair loss
, anxietyRe-positive No No No No No No No No No No No Note. *No recovery: patients with OD were considered that who do not report any improvement for smell for odors. #Partial recovery: patients with OD were considered that who subjectively start to smell some odors. OD, olfactory dysfunction. Figure 1. The clinical course of olfactory dysfunction in 11 imported COVID-19 cases. RT-PCR, reverse transcription polymerase chain reaction. Of note: Case 1 was hospitalized four times. Case 3 presented with anosmia before arrival in Xi’an (August 10, 2020), tested positive with RT-PCR, and was hospitalized. Cases 3 and 6 were hospitalized twice; both retested positive with RT-PCR after discharge and were considered mild cases at each admission. Case 7 had gustatory dysfunction in addition to olfactory dysfunction.
Of these patients, 54.5% (6/11) had hyposmia and 45.5% (5/11) had anosmia. Some 63.6% (7/11) (including the one patient reporting anosmia prior to entry) reported the onset of OD (four hyposmia and three anosmia) before or on the day of hospital admission; OD was reported as the initial symptom in those cases. Of those who reported OD as the initial symptom, 42.9% (3/7) presented OD as the only symptom. The other main symptoms included cough (5/11) and sore throat (4/11). However, none of the patients had rhinorrhea, generalized weakness, or myalgia. The patients’ symptoms and duration are shown in Table 1 and Figure 2.
Figure 2. Chronology of symptom onset and duration, RT-PCR, and serology testing of 11 imported COVID-19 cases with olfactory dysfunction. IgM, immunoglobulin M; RT-PCR, reverse transcription polymerase chain reaction; UAE, United Arab Emirates.
Table 2 shows the laboratory and radiological findings on admission. All patients had normal peripheral white blood cell counts and procalcitonin. The lymphocyte count was low in one patient, and more than one-third (36.4%, 4/11) had elevated erythrocyte sedimentation rates. Elevated levels of C-reactive protein, liver enzymes, and creatine kinase were present in two patients, elevated lactate dehydrogenase was found in one patient, and D-dimer was found in one patient.
Table 2. Laboratory and radiological findings of 11 imported COVID-19 cases with olfactory dysfunction, China
Variables Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Case 10 Case 11 Laboratory tests; (normal range) WBC count, ×109/L; (3.97–9.15) 7.02 6.38 7.99 7.55 4.07 7.75 5.69 5.85 5.59 4.25 4.18 Neutrophil count, ×109/L; (2.0–7.0) 3.65 3.73 4.35 4.58 2.66 4.38 3.82 2.57 3.28 2.84 2.94 Lymphocyte count, ×109/L; (0.8–4.0) 2.85 2.04 2.85 2.22 0.68 2.85 1.44 2.69 1.71 0.94 0.73(↓) Platelet count, ×109/ L; (85–303) 245 254 204 188 173 309(↑) 168 229.4 298 215 174 Hemoglobin, g/L; (131.0–172.0) 150 149 148 159.4 148 122 151 117 138 168 152.4 Prothrombin time, s; (11.0–15.0) 11.86 12.39 13.13 11.88 12.91 14.41 11.34 9.64(↓) 11.21 12.15 13.57 Activated partial thromboplastin
time, s; (24.0–38.0)34.66 39.37(↑) 35.03 36.14 35.38 33.35 33.11 31.86 33.78 29.35 32.38 D-dimer, μg/mL; (0.0–0.4) 0.21 0.16 0.08 0.39 0.21 0.26 0.35 0.4 0.11 0.44(↑) 0.35 Fibrinogen, g/dL; (2.0–4.0) 2.81 2.72 2.08 4.26(↑) 2.77 2.46 3.34 1.61(↓) 2.54 3.46 2.83 Albumin, g/L; (38.0–54.0) 46.5 45.38 44.99 40.39 46.02 47.44 41.98 37.62(↓) 42.72 46.8 45.3 Bilirubin, μmol/L; (5.1–19.0) 11.59 7.79 14.33 8.74 8.26 9.13 8.75 15.35 17.44 12.94 7.84 Alkaline phosphatase, U/L; (42–128) 95.73 81.34 83.87 50.31 70.71 69.35 78.39 37.42 80.94 103.5 65.4 ALT, U/L; (0.0–41.0) 19.87 15.5 17.35 26.3 9.73 14.42 132.15(↑) 6.17 102.83(↑) 25.1 10.9 AST, U/L; (0.0–37.0) 18.22 20.18 19.82 23.07 14.09 13.79 69.11(↑) 11.51 48.13(↑) 36.8 14.4 Urea, mmol/L; (1.7–8.3) 4.64 6.09 4.95 3.66 4.37 2.53 4.76 2.62 4.95 5.61 3.81 Creatinine, μmol/L; (70–115) 79.44 108.36 83.57 111.13 79.58 47.4 82.66 54.5 73.98 101.2 100.3 Sodium, mmol/L; (137–147) 142.85 141.74 141.05 135.35(↓) 141.74 141.01 139.36 143.16 141.22 143.6 139.5 Potassium, mmol/L; (3.5–5.3) 4.54 3.82 3.77 3.81 3.91 3.8 4.02 4.23 3.85 3.69 4.23 Creatine kinase, U/L; (24–190) 110.3 155 262.53(↑) 144.77 138.13 58.98 51.6 74.35 339.18(↑) 67.6 127 LDH, U/L; (115–220) 145.66 195.84 153.28 202.75 143.77 155.58 240.54(↑) 145.99 190.02 178.2 190.7 CRP, mg/L; (0.0–6.0) 1.28 2.11 0.77 11.77(↑) 1.01 0.33 3.09 0.2 1.5 0.1 9.4(↑) ESR, mm/h; (0.0–15.0) 5.0 8.0 4.0 21.0(↑) 8.0 7.0 40.0(↑) 20.0(↑) 7.0 41.0(↑) 6.0 Procalcitonin, ng/L; (0.0–0.5) < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 Blood glucose, mmol/L; (3.36–6.11) 4.56 5.15 5.31 4.63 5.33 4.17 4.61 3.7 5.21 6.45(↑) 7.15(↑) Chest CT findings No abnormal lesions Yes No Yes No Yes Yes No Yes No No No Bilateral pulmonary lesions No No No Yes No No No No No No No Unilateral pulmonary lesions No Yes No No No No Yes No Yes Yes Yes Note. ALT, alanine aminotransferase; AST, aspartate aminotransferase; CRP, C-reactive protein; CT, computerized tomography; ESR, erythrocyte sedimentation rate; LDH, lactate dehydrogenase; WBC, white blood cell; ↑ above normal range; ↓ below normal range. Available relevant laboratory data, CT findings, and treatment at admission are presented. -
All the patients received a combined treatment of traditional Chinese medicine (primarily lung cleansing and detoxifying decoction) and Western medicine. In terms of Western medicine, 100% of the patients received an antiviral treatment (primarily Abidol and interferon-α), 72.7% (8/11) received intravenous immunoglobin treatment (thymalfasin), 63.6% (7/11) received hepatoprotective therapy (compound glycyrrhizin or glutathione), and 27.3% (3/11) received antibiotic (ceftriaxone or ceftazidime) and corticosteroid (methylprednisolone) treatment (Table 1).
All the patients recovered and were discharged; none developed aggravation during hospitalization. 72.7% (8/11) had full or partial recovery at discharge, and the median duration was 9 (IQR 4.75 to 17.75) days; most improvements occurred in the first 2 weeks [in 7/9 patients (77.8%)] after onset. See the clinical course of the 11 patients in Figure 1.
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Of the 11 cases, 72.7% (8/11) had recovered completely or recovered partially at the 1-month follow-up; 45.5% (5/11) of patients reported at least one sequela; 3 cases had more than two sequelae, such as anxiety, fatigue, difficulty sleeping, and throat discomfort; and 3 cases had been recurrent.
At the 6-month follow-up, 54.5% (6/11) had recovered completely and 27.3% (3/11) had recovered partially; however, one recovered patient with OD developed OD again, with long-term fatigue. Of the aforementioned sequelae at the 1-month follow-up, one patient had hair loss. There were no recurrent cases.
In terms of OD recovery at the 12-month follow-up, all the patients had a favorable outcome, including 81.8% (9/11) who recovered completely and 18.2% (2/11) who recovered partially. 45.5% (5/11) of the patients reported at least one sequela, and there were no recurrent cases (Figure 1 and Table 1).
doi: 10.3967/bes2022.056
A Case Series of Olfactory Dysfunction in Imported COVID-19 Patients: A 12-Month Follow-Up Study
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Abstract:&These authors contributed equally to this work.
Objective The scientific community knows little about the long-term influence of coronavirus disease 2019 (COVID-19) on olfactory dysfunction (OD). With the COVID-19 pandemic ongoing worldwide, the risk of imported cases remains high. In China, it is necessary to understand OD in imported cases. Methods A prospective follow-up design was adopted. A total of 11 self-reported patients with COVID-19 and OD from Xi’an No. 8 Hospital were followed between August 19, 2021, and December 12, 2021. Demographics, clinical characteristics, laboratory and radiological findings, and treatment outcomes were analyzed at admission. We surveyed the patients via telephone for recurrence and sequelae at the 1-, 6-, and 12-month follow-up. Results Eleven patients with OD were enrolled; of these, 54.5% (6/11) had hyposmia and 45.5% (5/11) had anosmia. 63.6% (7/11) reported OD before or on the day of admission as their initial symptom; of these, 42.9% (3/7) described OD as the only symptom. All patients in the study received combined treatment with traditional Chinese medicine and Western medicine, and 72.7% (8/11) had partially or fully recovered at discharge. In terms of OD recovery at the 12-month follow-up, 45.5% (5/11) reported at least one sequela, 81.8% (9/11) had recovered completely, 18.2% (2/11) had recovered partially, and there were no recurrent cases. Conclusions Our data revealed that OD frequently presented as the initial or even the only symptom among imported cases. Most OD improvements occurred in the first 2 weeks after onset, and patients with COVID-19 and OD had favorable treatment outcomes during long-term follow-up. A better understanding of the pathogenesis and appropriate treatment of OD is needed to guide clinicians in the care of these patients.
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Figure 1. The clinical course of olfactory dysfunction in 11 imported COVID-19 cases. RT-PCR, reverse transcription polymerase chain reaction. Of note: Case 1 was hospitalized four times. Case 3 presented with anosmia before arrival in Xi’an (August 10, 2020), tested positive with RT-PCR, and was hospitalized. Cases 3 and 6 were hospitalized twice; both retested positive with RT-PCR after discharge and were considered mild cases at each admission. Case 7 had gustatory dysfunction in addition to olfactory dysfunction.
Table 1. Demographics, clinical characteristics, treatment outcomes, and follow up of 11 imported COVID-19 cases with olfactory dysfunction
Characteristics Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Case 10 Case 11 Age (years) 19 52 22 37 23 23 35 24 47 46 34 Gender Male Male Male Male Male Female Male Female Male Male Male Occupation Student Salary employee Student Semi-skilled employee Salary employee Unemployed Salary employee Student Salary employee Salary employee Semi-skilled employee Body mass index (kg/m2) 24.8 23.7 23.7 24.2 20.0 18.8 20.0 22.1 28.7 22.6 23.0 Comorbidity Hypertension Hypertension No No No No No No No Hepatitis B No Complication No No No Liver injury No No No No Liver injury No No Imported country Kazakhstan Kazakhstan Britain Liberia United Arab Emirates United Arab Emirates Uzbekistan Uzbekistan Angola Uzbekistan Belgium Clinical classification Mild Moderate Mild Moderate Mild Mild Moderate Mild Moderate Moderate Moderate Symptoms and signs Hyposmia Yes No No Yes Yes No Yes No Yes No Yes Anosmia No Yes Yes No No Yes No Yes No Yes No Hypogeusia No No No No No No Yes No No No No Fever No No No No No No No No No No Yes Cough No No No Yes No No Yes Yes No Yes Yes Fatigue No Yes No No No No No No No No No Rhinorrhea No No No No No No No No No No No Nasal congestion No No No No No Yes No No No No No Sore throat No No No Yes No Yes No Yes Yes No No Myalgia No No No No No No No No No No No Diarrhea No No No No No No No No Yes No No Treatment Antiviral Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Antibiotic No No No Yes No No No No Yes No Yes Traditional Chinese medicine Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Corticosteroids No No No Yes No No No No Yes No Yes Intravenous
immunoglobinNo Yes Yes Yes Yes No Yes No Yes Yes Yes Hepatoprotective
therapyNo No No Yes No Yes Yes Yes Yes Yes Yes Treatment outcome Cured Cured Cured Cured Cured Cured Cured Cured Cured Cured Cured Follow up 1-month OD No recovery* Recovery No recovery* Recovery Recovery No recovery* Recovery Partial recovery# Recovery Recovery Recovery Other sequelae Anxiety, fatigue, difficulty sleeping No No No No Throat discomfort, Fatigue, No No Fatigue Difficulty sleeping, Fatigue Throat discomfort Re-positive Yes No Yes No No Yes No No No No No 6-month OD Partial recovery# No Partial recovery# Recovery Recovery Partial recovery# Recovery Recovery OD Recovery Recovery Other sequelae Hair loss, anxiety, fatigue and difficulty sleeping No No No No Throat discomfort No No Fatigue Difficulty sleeping Throat discomfort, hair loss Re-positive No No No No No No No No No No No 12-month OD Partial recovery# Recovery Recovery Recovery Recovery Recovery Recovery Recovery Partial recovery# Recovery Recovery Other sequelae Hair loss, anxiety, fatigue, difficulty sleeping No No No No Throat discomfort No No Fatigue Difficulty sleeping Hair loss
, anxietyRe-positive No No No No No No No No No No No Note. *No recovery: patients with OD were considered that who do not report any improvement for smell for odors. #Partial recovery: patients with OD were considered that who subjectively start to smell some odors. OD, olfactory dysfunction. Table 2. Laboratory and radiological findings of 11 imported COVID-19 cases with olfactory dysfunction, China
Variables Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Case 10 Case 11 Laboratory tests; (normal range) WBC count, ×109/L; (3.97–9.15) 7.02 6.38 7.99 7.55 4.07 7.75 5.69 5.85 5.59 4.25 4.18 Neutrophil count, ×109/L; (2.0–7.0) 3.65 3.73 4.35 4.58 2.66 4.38 3.82 2.57 3.28 2.84 2.94 Lymphocyte count, ×109/L; (0.8–4.0) 2.85 2.04 2.85 2.22 0.68 2.85 1.44 2.69 1.71 0.94 0.73(↓) Platelet count, ×109/ L; (85–303) 245 254 204 188 173 309(↑) 168 229.4 298 215 174 Hemoglobin, g/L; (131.0–172.0) 150 149 148 159.4 148 122 151 117 138 168 152.4 Prothrombin time, s; (11.0–15.0) 11.86 12.39 13.13 11.88 12.91 14.41 11.34 9.64(↓) 11.21 12.15 13.57 Activated partial thromboplastin
time, s; (24.0–38.0)34.66 39.37(↑) 35.03 36.14 35.38 33.35 33.11 31.86 33.78 29.35 32.38 D-dimer, μg/mL; (0.0–0.4) 0.21 0.16 0.08 0.39 0.21 0.26 0.35 0.4 0.11 0.44(↑) 0.35 Fibrinogen, g/dL; (2.0–4.0) 2.81 2.72 2.08 4.26(↑) 2.77 2.46 3.34 1.61(↓) 2.54 3.46 2.83 Albumin, g/L; (38.0–54.0) 46.5 45.38 44.99 40.39 46.02 47.44 41.98 37.62(↓) 42.72 46.8 45.3 Bilirubin, μmol/L; (5.1–19.0) 11.59 7.79 14.33 8.74 8.26 9.13 8.75 15.35 17.44 12.94 7.84 Alkaline phosphatase, U/L; (42–128) 95.73 81.34 83.87 50.31 70.71 69.35 78.39 37.42 80.94 103.5 65.4 ALT, U/L; (0.0–41.0) 19.87 15.5 17.35 26.3 9.73 14.42 132.15(↑) 6.17 102.83(↑) 25.1 10.9 AST, U/L; (0.0–37.0) 18.22 20.18 19.82 23.07 14.09 13.79 69.11(↑) 11.51 48.13(↑) 36.8 14.4 Urea, mmol/L; (1.7–8.3) 4.64 6.09 4.95 3.66 4.37 2.53 4.76 2.62 4.95 5.61 3.81 Creatinine, μmol/L; (70–115) 79.44 108.36 83.57 111.13 79.58 47.4 82.66 54.5 73.98 101.2 100.3 Sodium, mmol/L; (137–147) 142.85 141.74 141.05 135.35(↓) 141.74 141.01 139.36 143.16 141.22 143.6 139.5 Potassium, mmol/L; (3.5–5.3) 4.54 3.82 3.77 3.81 3.91 3.8 4.02 4.23 3.85 3.69 4.23 Creatine kinase, U/L; (24–190) 110.3 155 262.53(↑) 144.77 138.13 58.98 51.6 74.35 339.18(↑) 67.6 127 LDH, U/L; (115–220) 145.66 195.84 153.28 202.75 143.77 155.58 240.54(↑) 145.99 190.02 178.2 190.7 CRP, mg/L; (0.0–6.0) 1.28 2.11 0.77 11.77(↑) 1.01 0.33 3.09 0.2 1.5 0.1 9.4(↑) ESR, mm/h; (0.0–15.0) 5.0 8.0 4.0 21.0(↑) 8.0 7.0 40.0(↑) 20.0(↑) 7.0 41.0(↑) 6.0 Procalcitonin, ng/L; (0.0–0.5) < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 < 0.05 Blood glucose, mmol/L; (3.36–6.11) 4.56 5.15 5.31 4.63 5.33 4.17 4.61 3.7 5.21 6.45(↑) 7.15(↑) Chest CT findings No abnormal lesions Yes No Yes No Yes Yes No Yes No No No Bilateral pulmonary lesions No No No Yes No No No No No No No Unilateral pulmonary lesions No Yes No No No No Yes No Yes Yes Yes Note. ALT, alanine aminotransferase; AST, aspartate aminotransferase; CRP, C-reactive protein; CT, computerized tomography; ESR, erythrocyte sedimentation rate; LDH, lactate dehydrogenase; WBC, white blood cell; ↑ above normal range; ↓ below normal range. Available relevant laboratory data, CT findings, and treatment at admission are presented. -
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