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Erschienen in: BMC Infectious Diseases 1/2021

Open Access 01.12.2021 | COVID-19 | Research article

Clinical characteristics and outcome of influenza virus infection among adults hospitalized with severe COVID-19: a retrospective cohort study from Wuhan, China

verfasst von: Xunliang Tong, Xiaomao Xu, Guoyue Lv, He Wang, Anqi Cheng, Dingyi Wang, Guohui Fan, Yue Zhang, Yanming Li

Erschienen in: BMC Infectious Diseases | Ausgabe 1/2021

Abstract

Background

Coronavirus disease 2019 (COVID-19) is an emerging infectious disease that rapidly spreads worldwide and co-infection of COVID-19 and influenza may occur in some cases. We aimed to describe clinical features and outcomes of severe COVID-19 patients with co-infection of influenza virus.

Methods

Retrospective cohort study was performed and a total of 140 patients with severe COVID-19 were enrolled in designated wards of Sino-French New City Branch of Tongji Hospital between Feb 8th and March 15th in Wuhan city, Hubei province, China. The demographic, clinical features, laboratory indices, treatment and outcomes of these patients were collected.

Results

Of 140 severe COVID-19 hospitalized patients, including 73 patients (52.14%) with median age 62 years were influenza virus IgM-positive and 67 patients (47.86%) with median age 66 years were influenza virus IgM-negative. 76 (54.4%) of severe COVID-19 patients were males. Chronic comorbidities consisting mainly of hypertension (45.3%), diabetes (15.8%), chronic respiratory disease (7.2%), cardiovascular disease (5.8%), malignancy (4.3%) and chronic kidney disease (2.2%). Clinical features, including fever (≥38 °C), chill, cough, chest pain, dyspnea, diarrhea and fatigue or myalgia were collected. Fatigue or myalgia was less found in COVID-19 patients with IgM-positive (33.3% vs 50/7%, P = 0.0375). Higher proportion of prolonged activated partial thromboplastin time (APTT) > 42 s was observed in COVID-19 patients with influenza virus IgM-negative (43.8% vs 23.6%, P = 0.0127). Severe COVID-19 Patients with influenza virus IgM positive have a higher cumulative survivor rate than that of patients with influenza virus IgM negative (Log-rank P = 0.0308). Considering age is a potential confounding variable, difference in age was adjusted between different influenza virus IgM status groups, the HR was 0.29 (95% CI, 0.081–1.100). Similarly, difference in gender was adjusted as above, the HR was 0.262 (95% CI, 0.072–0.952) in the COX regression model.

Conclusions

Influenza virus IgM positive may be associated with decreasing in-hospital death.
Hinweise

Supplementary Information

The online version contains supplementary material available at https://​doi.​org/​10.​1186/​s12879-021-05975-2.
Xunliang Tong and Xiaomao Xu contributed equally to this work.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Abkürzungen
APTT
Activated partial thromboplastin time
CDC
Centers for disease control and prevention
COVID-19
Coronavirus disease 2019
ECMO
Extracorporeal membrane oxygenation
eGFR
Estimated glomerular filtration rate
ELISA
Enzyme-linked immunosorbent assay
FiO2
Fraction of inspired oxygen
HA
Hemagglutinin
HFNC
High-flow nasal cannula
ILI
Influenza like illness
IQR
Interquartile range
LDH
Lactate dehydrogenase
MV
Mechanical ventilation
NMV
Noninvasive methods of mechanical ventilation
NT-proBNP
N-terminal pro brain natriuretic peptide
PaO2
Partial pressure of oxygen
PT
Prothrombin time
RT-PCR
Reverse-transcriptase–polymerase chain-reaction
SARS-CoV
Severe acute respiratory syndrome- coronavirus
SARS-CoV-2
Severe acute respiratory syndrome- coronavirus − 2
WHO
World Health Organization
ALT
Alanine transaminase
AST
Aspartate aminotransferase
CRP
C-reactive protein
IL-6
Interleukin-6
FIB
Fibrinogen
NMV
Non-invasive mechanical ventilation
IMV
Invasive mechanical ventilation

Background

In December 2019, a novel coronavirus with high similarity to the coronavirus responsible for severe acute respiratory syndrome (SARS-CoV) appeared and was later named as SARS-CoV-2 [13]. In 2020, the World Health Organization (WHO) announced that the pandemic of Coronavirus disease 2019 (COVID-19) has constituted a public health emergency of international concern [4].
Previous studies have focused primarily on COVID-19 patients’ clinical features with fever accompanied with respiratory and/or gastrointestinal symptoms, and so on [5, 6], which were highly similar to the clinical manifestation of influenza like illness (ILI). ILI may occur in population as co-infection of SARS-CoV-2 and influenza virus during the pandemic. Sustained surveillance of ILI has been implemented by Centers for Disease Control and Prevention (CDC) [79] and the co-infection of influenza viruses and SARS-CoV-2 was possible at 2019–2020 influenza season [2, 10]. According to previous study, influenza virus-specific antibody responses following influenza infection rises in HA-specific serum IgM (86 to 94%) antibodies after primary influenza virus infection in adults [11]. Therefore, HA-specific serum IgM can be identified as the marker of influenza virus infection in COVID-19 patients. The aims of this study were to describe the clinical features and outcomes of hospitalized COVID-19 patients, who were also positive of influenza virus IgM.

Methods

Study design

This was a retrospective cohort study which was performed during Feb 8th to March 15th at wards designated for patients with COVID-19 in the Sino-French New City Branch of Tongji Hospital in Wuhan city, Hubei province, China. Total of 140 patients diagnosed of COVID-19 pneumonia was enrolled from two wards managed by multidisciplinary team from Beijing Hospital and First Hospital attached to Jilin University (Fig. 1). The study was approved by Ethics Committee of Beijing Hospital (2020BJYYEC-046-01).
The inclusion criteria: throat-swab specimen from upper respiratory tract that were obtained and tested by RT-PCR for confirmation of SARS-CoV-2 as the same protocol described previously [1, 12]; pneumonia confirmed by thoracic CT scan [13], an oxygen saturation (SaO2) of 94% or less while they were breathing ambient air or a ratio of the partial pressure of oxygen (PaO2) to the fraction of inspired oxygen (FiO2) at or below 300 mmHg [14]. Exclusion criteria included without examined influenza virus IgM in the first 24 h in hospital, sudden death within 24 h.

Data collection

All the data from electronic medical records were reviewed by experienced physicians separately and checked by 2 physicians independently. The baseline of clinical data was recorded in the first 24 h after administration and all interventions and the highest level of oxygen support during hospitalization were recorded.
Throat swab samples were collected for SARS-CoV-2 detection from patients by local Centers for Disease Control and Prevention, local health institutions. The PCR re-examination was conducted by throat-swab specimens after clinical remission of symptoms, including fever, cough, and dyspnea. A patient was allowed to discharge if he was clinical improvement and two throat-swab samples negative for SARS-CoV-2 RNA obtained at least 24 h apart [14]. Peripheral blood samples from patients were taken for identification of influenza virus-specific antibody IgM which responses following influenza infection and detected by indirect immunofluorescence assay (Respiratory tract 8 joint detection kit; EUROIMMUN, Inc., Germany) [11, 15, 16].

Statistical analysis

Descriptive analyses of the variables were expressed as median (interquartile range [IQR]) or number (%) and compared using Mann-Whitney test. Categorical data were compared using X2 test or the Fisher exact test, where appropriate. The patients’ characteristics of deaths verses discharged and death/discharge & influenza IgM positive/negative were also described and shown in Supplementary Table 1 and 2. Kaplan-Meier curve was portrayed by influenza virus IgM positive/negative to describe the cumulative survival rate of COVID-19 patients. COX regression model was fitted to investigate the association between influenza virus IgM positive and the in-hospital death. To avoid overfitting, at most two covariates were allowed to the model and we adjusted for age and gender respectively in the model. Adjusted hazard ratios (aHRs) and 95% confidence intervals (95% CIs) were then estimated. All tests were 2-sides, and a P value less than .05 was considered statistically significant. All analyses were performed with SPSS, version 23.0 (IBM inc.).

Results

Baseline characteristics

A total of 140 adult patients confirmed with COVID-19 from designated hospital was enrolled in this study, with 73 patients (52.14%) were identified as influenza virus IgM-positive. 76 (54.4%) of the COVID-19 patients were males. The median age of patients with influenza virus-IgM negative was 66 years (IQR, 55 to 70 years), older than patients with influenza virus IgM-positive (median age 62, IQR, 47 to 70 years, P = 0.1118). Chronic comorbidities consisting mainly of hypertension (45.3%), diabetes (15.8%), chronic respiratory disease (7.2%), cardiovascular disease (5.8%), malignancy (4.3%) and chronic kidney disease (2.2%). Clinical features, including fever (≥38 °C), chill, cough, chest pain, dyspnea, diarrhea and fatigue or myalgia were collected. Fatigue or myalgia was less found in COVID-19 patients with IgM-positive (33.3% vs 50/7%, P = 0.0375). (Table 1).
Table 1
Clinical Characteristics of COVID-19 Patients with and Without Influenza IgM positive
Study Population
With Influenza IgM positive (n = 73)
Without Influenza IgM positive (n = 67)
Total (n = 140)
P value
Demographic
 Gender, Male
39 (53.4)
37 (55.2)
76 (54.3)
0.8310
 Age, media (IQR), yrs
62.0 (47.0, 70.0)
66.0 (55.0, 70.0)
65.0 (48.5, 70.0)
0.1118
Comorbidities
 Hypertension
32/70 (45.7)
30/67 (44.8)
62/137 (45.3)
0.9122
 Diabetes
12/72 (16.7)
10/67 (14.9)
22/139 (15.8)
0.7787
 Chronic respiratory disease
5/72 (6.9)
5/67 (7.5)
10/139 (7.2)
0.9060
 Cardiovascular disease
5/72 (6.9)
3/67 (4.5)
8/139 (5.8)
0.5301
 Malignancy
3/72 (4.2)
3/67 (4.5)
6/139 (4.3)
0.9282
 Chronic kidney disease
2/72 (2.8)
1/67 (1.5)
3/139 (2.2)
0.5983
Signs and symptoms
 Fever
55 (75.3)
53 (79.1)
108 (77.1)
0.5964
 Highest temperature, °C
38.5 (38.0, 39.0)
38.7 (38.2, 39.0)
38.5 (38.0, 39.0)
0.1274
 Chills
13 (17.8)
19 (28.4)
32 (22.9)
0.1375
 Cough
41/72 (56.9)
44/67 (65.7)
85/139 (61.2)
0.2915
 Productive cough
20/72 (27.8)
25/67 (37.3)
45/139 (32.4)
0.2299
 Chest pain/Chest congestion
19/72 (26.4)
13/67 (19.4)
32/139 (23.0)
0.3283
 Dyspnea
21/72 (29.2)
29/67 (43.3)
50/139 (36.0)
0.0831
 Diarrhea
18 (24.7)
25 (37.3)
43 (30.7)
0.1049
 Fatigue or myalgia
24/72 (33.3)
34/67 (50.7)
58/139 (41.7)
0.0375
Laboratory findings, median (IQR)
 White blood cells, × 109/mL
5.7 (4.2, 6.8)
5.7 (4.6, 7.9)
5.7 (4.4, 7.2)
0.3226
 Neutrophils, × 109/mL
3.9 (2.5, 4.8)
4.0 (2.6, 5.9)
3.9 (2.5, 5.3)
0.3600
 Lymphocytes, ×109/mL
1.2 (0.9, 1.6)
1.1 (0.8, 1.5)
1.1 (0.8, 1.5)
0.3826
 Lymphocytes< 0.8 × 109/mL
18/73 (24.7)
18/66 (27.3)
36/139 (25.9)
0.7252
 Red blood cells, × 1012/mL
4.1 (3.6, 4.6)
4.0 (3.7, 4.4)
4.0 (3.7, 4.5)
0.4502
 Platelets, ×109/ mL
230.0 (173.0, 292.0)
253.0 (169.0, 340.0)
235.0 (169.0, 312.0)
0.3622
 Platelets< 100 × 109/mL
5/73 (6.8)
6/66 (9.1)
11/139 (7.9)
0.6249
 Hemoglobin, g/L
122.0 (114.0, 137.0)
125.5 (113.0, 137.0)
123.0 (113.0, 137.0)
0.9143
 ALT, U/L
23.0 (17.0, 40.0)
22.5 (15.0, 41.0)
23.0 (16.0, 41.0)
0.7373
 AST, U/L
26.0 (19.0, 37.0)
30.0 (19.0, 41.0)
28.0 (19.0, 39.0)
0.3370
 Albumin, g/L
36.1 (32.2, 38.3)
35.0 (31.4, 37.1)
35.2 (31.7, 38.1)
0.2945
 Creatinine, μmol/L
70.0 (60.0, 89.5)
70.0 (59.0, 87.0)
70.0 (59.0, 89.0)
0.8596
 LDH, U/L
268.5 (204.0, 329.5)
287.0 (235.0, 351.0)
281.0 (212.0, 334.0)
0.2419
 LDH > 245 U/L
44/72 (61.1)
47/65 (72.3)
91/137 (66.4)
0.1658
 Troponin> 15.6 pg/mL, No (%)
7/51 (13.7)
12/56 (21.4)
19/107 (17.8)
0.2977
 NT-proBNP, pg/mL
140.0 (60.0, 334.0)
157.0 (64.0, 459.0)
151.0 (63.0, 411.0)
0.2883
 NT-proBNP≥247 pg/mL, No (%)
29/57 (50.9)
35/58 (60.3)
64/115 (55.7)
0.3069
 CRP, mg/L
21.3 (4.1, 49.2)
34.7 (9.1, 73.4)
27.2 (6.1, 69.8)
0.1281
 CRP ≥ 1 mg/L, No (%)
57/61 (93.4)
47/49 (95.9)
104/110 (94.5)
0.5651
 IL-6, pg/mL
9.8 (4.2, 21.1)
6.8 (3.6, 23.2)
9.4 (3.9, 23.2)
0.5603
 IL-6 ≥ 7 pg/mL, No (%)
25/42 (59.5)
15/35 (42.9)
40/77 (51.9)
0.1450
 Ferritin, μg/L
522.1 (320.5, 729.0)
630.5 (310.2, 1519.9)
562.6 (320.5, 986.5)
0.0964
 Ferritin> 150 μg/L, No (%)
39/43 (90.7)
33/35 (94.3)
72/78 (92.3)
0.5495
 PT, s
13.7 (13.2, 14.3)
13.8 (13.4, 14.2)
13.8 (13.3, 14.3)
0.9762
 APTT, s
39.6 (35.8, 42.0)
39.5 (37.8, 45.8)
39.6 (36.6, 44.3)
0.0243
 APTT> 42 s, No (%)
17/72 (23.6)
28/64 (43.8)
45/136 (33.1)
0.0127
 FIB, g/L
4.9 (3.9, 6.0)
5.3 (4.3, 6.2)
5.0 (4.1, 6.1)
0.2374
 D-Dimer, μg/mL
0.7 (0.5, 1.7)
1.2 (0.5, 2.1)
1.0 (0.5, 2.0)
0.2371
 D-Dimer≥0.5 μg/mL, No (%)
53/73 (72.6)
45/64 (70.3)
98/137 (71.5)
0.7669
Note. Data are presented as n (%) or median (IQR, interquartile range) for each parameter. P values were calculated by chi-square test, Fisher’s exact test, or Mann-Whitney U test, where appropriate
Abbreviations IQR interquartile range, ALT alanine aminotransferase, AST aspartate aminotransferase, LDH lactic Acid dehydrogenase, CRP C-reactive protein, IL-6 interleukin-6, PT prothrombintime, APTT activated partial thromboplastin time, FIB fibrinogen

Laboratory findings

Higher proportion of prolonged activated partial thromboplastin time (APTT) > 42 s was observed in COVID-19 patients with influenza virus IgM-negative (43.8% vs 23.6%, P = 0.0127). (Table 1) Counts of lymphocytes and platelets were significantly lower, while aspartate aminotransferase (AST), creatinine, lactate dehydrogenase (LDH), troponin, NT-proBNP, C-reactive protein (CRP), interleukin-6 (IL-6), ferritin, prothrombin time (PT), APTT and D-Dimer were significantly higher in dead cases (all P < 0.05). (Supplementary Table 1).

Treatment and outcomes

43.6% of the patients received nasal cannula, 2.1% oxygen mask, 49.3% non-invasive mechanical ventilation (NMV)/high-flow nasal cannula (HFNC) and 8.6% invasive mechanical ventilation (IMV)/extracorporeal membrane oxygenation (ECMO). Compound Methoxamine capsule were used in more patients with influenza IgM positive than the other group (23.3% vs 9.0%, P = 0.0222). (Table 2) higher levels of respiratory support were more seen in dead patients, especially those with influenza IgM positive. (supplementary Table 1 and supplementary Table 2)
Table 2
Treatment and prognosis of COVID-19 Patients with and Without Influenza IgM positive
Study Population
With influenza IgM positive (n = 73)
Without influenza IgM positive (n = 67)
Total (n = 140)
P value
Treatment in hospital
 Oxygen Therapy
 Nasal Cannula
32 (43.8)
29 (43.3)
61 (43.6)
0.9475
 Oxygen Mask
1 (1.4)
2 (3.0)
3 (2.1)
0.5069
 NMV/High-flow nasal cannula
35 (47.9)
34 (50.7)
69 (49.3)
0.7405
 IMV/ECMO
7 (9.6)
5 (7.5)
12 (8.6)
0.6535
 Drugs
  Oseltamivir
33 (45.2)
23 (34.3)
56 (40.0)
0.1894
  Arbidol
53 (72.6)
47 (70.1)
100 (71.4)
0.7482
  Compound Methoxamine capsule
17 (23.3)
6 (9.0)
23 (16.4)
0.0222
Clinical outcomes
 CURB-65
   
0.0397
  Low risk
65 (89.0)
50 (74.6)
115 (82.1)
  Medium risk
6 (8.2)
8 (11.9)
14 (10.0)
  High risk
2 (2.7)
9 (13.4)
11 (7.9)
 Duration of viral shedding, days
26.0 (20.0, 32.0)
25.0 (21.0, 32.0)
25.5 (20.5, 32.0)
0.9694
 Hospital length of stay, days
13.0 (10.0, 18.0)
14.0 (10.0, 17.0)
13.0 (10.0, 18.0)
0.9084
 Time from illness onset to discharge, days
27.0 (22.0, 35.0)
27.0 (21.0, 33.0)
27.0 (22.0, 33.5)
0.6208
 Death,No (%)
   
0.0276
  Discharge
70 (95.9)
57 (85.1)
127 (90.7)
  Death
3 (4.1)
10 (14.9)
13 (9.3)
According to the score of CURB-65, more COVID-19 patients with influenza IgM positive group were in low to moderate risk level (P = 0.0397). No differences were observed in the duration of viral shedding, the length of hospital stay and time from illness onset to discharge between groups. 9.3% of the patients died in hospital and the rate of death was significantly lower in patients with IgM positive than those with IgM negative (4.1% vs 14.9%, P = 0.0276). (Table 2).
Severe COVID-19 Patients with influenza virus IgM positive have a higher cumulative survivor rate than that of patients with influenza virus IgM negative (Log-rank P = 0.0308). Considering age is a potential confounding variable, difference in age was adjusted between different influenza virus IgM status groups, the HR was 0.29 (95% CI, 0.081–1.100). Similarly, difference in gender was adjusted as above, the HR was 0.262 (95% CI, 0.072–0.952) in the COX regression model. (Fig. 2).

Discussion

In this retrospective cohort study, we described the clinical features and outcomes of hospitalized COVID-19 patients with different influenza virus IgM status. We found that influenza virus IgM positive may be associated with decreasing in-hospital death. Fatigue and myalgia were less presented in COVID-19 patients with influenza virus IgM positive. It is the first time for influenza virus IgM to be a prognostic factor of COVID-19.
Previous studies reported cases with co-infection of SARS-CoV-2 and influenza showed the implications of co-infection during the pandemic area [1720]. It was necessary to assess the effect of the SARS-CoV-2 and influenza co-infection in clinical outcomes. Previous studies demonstrated that influenza virus-specific IgM antibody responses follow primary influenza virus infection in adults [11, 21]. Serological confirmation of a clinical diagnosis is by demonstration of greater rise in functional strain specific antibody titer. Specific neutralizing antibody can be detected from about 10 to 14 days post infection, reaches a plateau at around 28 days and decreased to normal level around a month and a half. This test uses nucleocapsid antigens that are type-specific and can distinguish A from B and C infections. Due to the huge task of rapid tests for SARS-CoV-2 and the absence of widely available testing methods, thousands of patients were diagnosed of COVID-19 without identification of co-infection pathogens at the initial period. During the epidemic of seasonal influenza and other respiratory illness, our concern is on the possibility of the co-infection of virus. Therefore, influenza virus IgM antibody may help us review these cases. The outbreak of COVID-19 may occur during influenza season, which brings difficulty in prevention, diagnosis and treatment. Increasing number of literatures has been demonstrating that influenza virus infection may trigger non-neutralizing antibodies responses which also binds to pathogens as diverse as HIV-1, herpes simplex virus and Ebola [2228]. Some other researches showed that influenza vaccination could reduce cardiovascular morbidity and mortality in patients with COVID-19 [29] Therefore, some potential mechanisms including active immunity or passive immunity may involve in the virus immunity for exhibition its protective effects. In this study, influenza virus IgM positive showed as a protective effector in severe COVID-19 patients associated with better prognosis and higher cumulative survivor rate. Considering the potential confounding variables, age and gender were adjusted between different influenza virus IgM status groups, respectively. After that, the potential protective effects influenza virus IgM positive in severe COVID-19 patients were observed If patients are suspected ILI, especially suffering from virus infection, a prompt test, like a one-time diagnostic panel for the respiratory virus nucleic acid, antigen or serological detection of virus specific IgM/ IgG, should be the first step with an expanded detectable rang towards confirming diagnosis, which help in making early and effective prevention and treatment strategy.
The strengths of this study include adults hospitalized with diagnosis of COVID-19, the retrospective cohort design, standardized patient screening in the participating, and centralized confirmation of respiratory viruses and other laboratory indices. Our study has several limitations. Firstly, a large number of patients were continually being admitted to hospital, but the sample size of our study is still limited. Secondly, our study was conducted in a local hospital in Wuhan, which may result in biases. Especially consideration of influenza season, it may become epidemic of different type in different regions. Thirdly, this cohort study did not last for a long time. Missing information of death status at discharge and initial influenza virus IgM status may influence the demographics and available clinical characteristics between included and excluded patients. Thus, the results may partly help us recognize co-infection of influenza and SARS-CoV-2. Further studies focused on the co-infectious pathogens, the treatment and prevention will be needed.

Conclusions

Influenza virus IgM positive may be associated with decreasing in-hospital death. The co-infection of SARS-CoV-2 and influenza virus may occur by causing a crisis and we need to improve our understanding for confronting it in the future.

Acknowledgments

The authors thank Academician Chen Wang for his guidance and assistance with this work.

Declarations

The study was approved by Ethics Committee of Beijing Hospital (2020BJYYEC-046-01).
Not applicable.

Competing interests

The authors declare that they have no competing interests.
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Literatur
1.
Zurück zum Zitat Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579(7798):270–3. https://doi.org/10.1038/s41586-020-2012-7.CrossRefPubMedPubMedCentral Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020;579(7798):270–3. https://​doi.​org/​10.​1038/​s41586-020-2012-7.CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Yan R, Zhang Y, Li Y, Xia L, Guo Y, Zhou Q. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science (New York, NY). 2020;367(6485):1444–8.CrossRef Yan R, Zhang Y, Li Y, Xia L, Guo Y, Zhou Q. Structural basis for the recognition of SARS-CoV-2 by full-length human ACE2. Science (New York, NY). 2020;367(6485):1444–8.CrossRef
5.
Zurück zum Zitat Wang C, Horby PW, Hayden FG, Gao GF. A novel coronavirus outbreak of global health concern. Lancet (London, England). 2020;395(10223):470–3.CrossRef Wang C, Horby PW, Hayden FG, Gao GF. A novel coronavirus outbreak of global health concern. Lancet (London, England). 2020;395(10223):470–3.CrossRef
6.
Zurück zum Zitat Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, Liu L, Shan H, Lei CL, Hui DSC, du B, Li LJ, Zeng G, Yuen KY, Chen RC, Tang CL, Wang T, Chen PY, Xiang J, Li SY, Wang JL, Liang ZJ, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Zhong NS, China Medical Treatment Expert Group for Covid-19, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382(18):1708–20. https://doi.org/10.1056/NEJMoa2002032.CrossRefPubMed Guan WJ, Ni ZY, Hu Y, Liang WH, Ou CQ, He JX, Liu L, Shan H, Lei CL, Hui DSC, du B, Li LJ, Zeng G, Yuen KY, Chen RC, Tang CL, Wang T, Chen PY, Xiang J, Li SY, Wang JL, Liang ZJ, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Zhong NS, China Medical Treatment Expert Group for Covid-19, et al. Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med. 2020;382(18):1708–20. https://​doi.​org/​10.​1056/​NEJMoa2002032.CrossRefPubMed
7.
Zurück zum Zitat Bedford T, Riley S, Barr IG, Broor S, Chadha M, Cox NJ, Daniels RS, Gunasekaran CP, Hurt AC, Kelso A, Klimov A, Lewis NS, Li X, McCauley JW, Odagiri T, Potdar V, Rambaut A, Shu Y, Skepner E, Smith DJ, Suchard MA, Tashiro M, Wang D, Xu X, Lemey P, Russell CA, et al. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature. 2015;523(7559):217–20. https://doi.org/10.1038/nature14460.CrossRefPubMedPubMedCentral Bedford T, Riley S, Barr IG, Broor S, Chadha M, Cox NJ, Daniels RS, Gunasekaran CP, Hurt AC, Kelso A, Klimov A, Lewis NS, Li X, McCauley JW, Odagiri T, Potdar V, Rambaut A, Shu Y, Skepner E, Smith DJ, Suchard MA, Tashiro M, Wang D, Xu X, Lemey P, Russell CA, et al. Global circulation patterns of seasonal influenza viruses vary with antigenic drift. Nature. 2015;523(7559):217–20. https://​doi.​org/​10.​1038/​nature14460.CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Wu X, Cai Y, Huang X, Yu X, Zhao L, Wang F, Li Q, Gu S, Xu T, Li Y, et al. Co-infection with SARS-CoV-2 and Influenza A Virus in Patient with Pneumonia, China. Emerg Infect Dis. 2020;26:6. Wu X, Cai Y, Huang X, Yu X, Zhao L, Wang F, Li Q, Gu S, Xu T, Li Y, et al. Co-infection with SARS-CoV-2 and Influenza A Virus in Patient with Pneumonia, China. Emerg Infect Dis. 2020;26:6.
12.
Zurück zum Zitat Liang WH, Guan WJ, Li CC, Li YM, Liang HR, Zhao Y, Liu XQ, Sang L, Chen RC, Tang CL, Wang T, Wang W, He QH, Chen ZS, Wong SS, Zanin M, Liu J, Xu X, Huang J, Li JF, Ou LM, Cheng B, Xiong S, Xie ZH, Ni ZY, Hu Y, Liu L, Shan H, Lei CL, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Cheng LL, Ye F, Li SY, Zheng JP, Zhang NF, Zhong NS, He JX, et al. Clinical characteristics and outcomes of hospitalised patients with COVID-19 treated in Hubei (epicenter) and outside Hubei (non-epicenter): a Nationwide analysis of China. Eur Respir J. 2020;55(6):2000562. https://doi.org/10.1183/13993003.00562-2020.CrossRefPubMedPubMedCentral Liang WH, Guan WJ, Li CC, Li YM, Liang HR, Zhao Y, Liu XQ, Sang L, Chen RC, Tang CL, Wang T, Wang W, He QH, Chen ZS, Wong SS, Zanin M, Liu J, Xu X, Huang J, Li JF, Ou LM, Cheng B, Xiong S, Xie ZH, Ni ZY, Hu Y, Liu L, Shan H, Lei CL, Peng YX, Wei L, Liu Y, Hu YH, Peng P, Wang JM, Liu JY, Chen Z, Li G, Zheng ZJ, Qiu SQ, Luo J, Ye CJ, Zhu SY, Cheng LL, Ye F, Li SY, Zheng JP, Zhang NF, Zhong NS, He JX, et al. Clinical characteristics and outcomes of hospitalised patients with COVID-19 treated in Hubei (epicenter) and outside Hubei (non-epicenter): a Nationwide analysis of China. Eur Respir J. 2020;55(6):2000562. https://​doi.​org/​10.​1183/​13993003.​00562-2020.CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Cao B, Wang Y, Wen D, Liu W, Wang J, Fan G, Ruan L, Song B, Cai Y, Wei M, Li X, Xia J, Chen N, Xiang J, Yu T, Bai T, Xie X, Zhang L, Li C, Yuan Y, Chen H, Li H, Huang H, Tu S, Gong F, Liu Y, Wei Y, Dong C, Zhou F, Gu X, Xu J, Liu Z, Zhang Y, Li H, Shang L, Wang K, Li K, Zhou X, Dong X, Qu Z, Lu S, Hu X, Ruan S, Luo S, Wu J, Peng L, Cheng F, Pan L, Zou J, Jia C, Wang J, Liu X, Wang S, Wu X, Ge Q, He J, Zhan H, Qiu F, Guo L, Huang C, Jaki T, Hayden FG, Horby PW, Zhang D, Wang C, et al. A trial of Lopinavir-ritonavir in adults hospitalized with severe Covid-19. N Engl J Med. 2020;382(19):1787–99. https://doi.org/10.1056/NEJMoa2001282.CrossRefPubMed Cao B, Wang Y, Wen D, Liu W, Wang J, Fan G, Ruan L, Song B, Cai Y, Wei M, Li X, Xia J, Chen N, Xiang J, Yu T, Bai T, Xie X, Zhang L, Li C, Yuan Y, Chen H, Li H, Huang H, Tu S, Gong F, Liu Y, Wei Y, Dong C, Zhou F, Gu X, Xu J, Liu Z, Zhang Y, Li H, Shang L, Wang K, Li K, Zhou X, Dong X, Qu Z, Lu S, Hu X, Ruan S, Luo S, Wu J, Peng L, Cheng F, Pan L, Zou J, Jia C, Wang J, Liu X, Wang S, Wu X, Ge Q, He J, Zhan H, Qiu F, Guo L, Huang C, Jaki T, Hayden FG, Horby PW, Zhang D, Wang C, et al. A trial of Lopinavir-ritonavir in adults hospitalized with severe Covid-19. N Engl J Med. 2020;382(19):1787–99. https://​doi.​org/​10.​1056/​NEJMoa2001282.CrossRefPubMed
20.
Zurück zum Zitat Kondo Y, Miyazaki S, Yamashita R, Ikeda T. Coinfection with SARS-CoV-2 and influenza A virus. BMJ Case Rep. 2020;13:7.CrossRef Kondo Y, Miyazaki S, Yamashita R, Ikeda T. Coinfection with SARS-CoV-2 and influenza A virus. BMJ Case Rep. 2020;13:7.CrossRef
24.
Zurück zum Zitat Kohl S, Loo LS, Pickering LK. Protection of neonatal mice against herpes simplex viral infection by human antibody and leukocytes from adult, but not neonatal humans. J Immunol (Baltimore, Md : 1950). 1981;127(4):1273–5. Kohl S, Loo LS, Pickering LK. Protection of neonatal mice against herpes simplex viral infection by human antibody and leukocytes from adult, but not neonatal humans. J Immunol (Baltimore, Md : 1950). 1981;127(4):1273–5.
25.
Zurück zum Zitat Kohl S, Loo LS. Protection of neonatal mice against herpes simplex virus infection: probable in vivo antibody-dependent cellular cytotoxicity. J Immunol (Baltimore, Md : 1950). 1982;129(1):370–6. Kohl S, Loo LS. Protection of neonatal mice against herpes simplex virus infection: probable in vivo antibody-dependent cellular cytotoxicity. J Immunol (Baltimore, Md : 1950). 1982;129(1):370–6.
26.
Zurück zum Zitat Wang K, Tomaras GD, Jegaskanda S, Moody MA, Liao H-X, Goodman KN, Berman PW, Rerks-Ngarm S, Pitisuttithum P, Nitayapan S, et al. Monoclonal Antibodies, Derived from Humans Vaccinated with the RV144 HIV Vaccine Containing the HVEM Binding Domain of Herpes Simplex Virus (HSV) Glycoprotein D, Neutralize HSV Infection, Mediate Antibody-Dependent Cellular Cytotoxicity, and Protect Mice from Ocular Challenge with HSV-1. J Virol. 2017;91:19. Wang K, Tomaras GD, Jegaskanda S, Moody MA, Liao H-X, Goodman KN, Berman PW, Rerks-Ngarm S, Pitisuttithum P, Nitayapan S, et al. Monoclonal Antibodies, Derived from Humans Vaccinated with the RV144 HIV Vaccine Containing the HVEM Binding Domain of Herpes Simplex Virus (HSV) Glycoprotein D, Neutralize HSV Infection, Mediate Antibody-Dependent Cellular Cytotoxicity, and Protect Mice from Ocular Challenge with HSV-1. J Virol. 2017;91:19.
27.
Zurück zum Zitat Gunn BM, Yu W-H, Karim MM, Brannan JM, Herbert AS, Wec AZ, Halfmann PJ, Fusco ML, Schendel SL, Gangavarapu K, et al. A Role for Fc Function in Therapeutic Monoclonal Antibody-Mediated Protection against Ebola Virus. Cell Host Microbe. 2018;24:2.CrossRef Gunn BM, Yu W-H, Karim MM, Brannan JM, Herbert AS, Wec AZ, Halfmann PJ, Fusco ML, Schendel SL, Gangavarapu K, et al. A Role for Fc Function in Therapeutic Monoclonal Antibody-Mediated Protection against Ebola Virus. Cell Host Microbe. 2018;24:2.CrossRef
28.
Zurück zum Zitat Saphire EO, Schendel SL, Fusco ML, Gangavarapu K, Gunn BM, Wec AZ, Halfmann PJ, Brannan JM, Herbert AS, Qiu X, et al. Systematic Analysis of Monoclonal Antibodies against Ebola Virus GP Defines Features that Contribute to Protection. Cell. 2018;174:4.CrossRef Saphire EO, Schendel SL, Fusco ML, Gangavarapu K, Gunn BM, Wec AZ, Halfmann PJ, Brannan JM, Herbert AS, Qiu X, et al. Systematic Analysis of Monoclonal Antibodies against Ebola Virus GP Defines Features that Contribute to Protection. Cell. 2018;174:4.CrossRef
Metadaten
Titel
Clinical characteristics and outcome of influenza virus infection among adults hospitalized with severe COVID-19: a retrospective cohort study from Wuhan, China
verfasst von
Xunliang Tong
Xiaomao Xu
Guoyue Lv
He Wang
Anqi Cheng
Dingyi Wang
Guohui Fan
Yue Zhang
Yanming Li
Publikationsdatum
01.12.2021
Verlag
BioMed Central
Schlagwort
COVID-19
Erschienen in
BMC Infectious Diseases / Ausgabe 1/2021
Elektronische ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-021-05975-2

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