Heterogeneity in transmissibility and shedding SARS-CoV-2 via droplets and aerosols

  1. Paul Z Chen
  2. Niklas Bobrovitz
  3. Zahra Premji
  4. Marion Koopmans
  5. David N Fisman
  6. Frank X Gu  Is a corresponding author
  1. Department of Chemical Engineering & Applied Chemistry, University of Toronto, Canada
  2. Temerty Faculty of Medicine, University of Toronto, Canada
  3. Department of Critical Care Medicine, Cumming School of Medicine, University of Calgary, Canada
  4. O'Brien Institute of Public Health, University of Calgary, Canada
  5. Libraries & Cultural Resources, University of Calgary, Canada
  6. Department of Viroscience, Erasmus University Medical Center, Netherlands
  7. Division of Epidemiology, Dalla Lana School of Public Health, University of Toronto, Canada
  8. Division of Infectious Diseases, Temerty Faculty of Medicine, University of Toronto, Canada
  9. Institute of Biomedical Engineering, University of Toronto, Canada
5 figures, 2 tables and 1 additional file

Figures

Development of the systematic dataset.
Figure 2 with 2 supplements
Association of overdispersion in SARS-CoV-2, SARS-CoV-1 and A(H1N1)pdm09 transmissibility with heterogeneity in respiratory viral load (rVL).

Meta-regression of dispersion parameter (k) with the standard deviation (SD) of rVLs from contributing studies with low risk of bias (Pearson’s r = −0.73). Pooled estimates of k were determined from …

Figure 2—figure supplement 1
Meta-regression between dispersion in SARS-CoV-2, SARS-CoV-1 and A(H1N1)pdm09 transmissibility and heterogeneity in respiratory viral load (rVL).

Meta-regression of dispersion parameter (k) with the standard deviation (SD) of rVLs from all contributing studies (Pearson’s r = −0.26). Pooled estimates of k were determined from the literature. …

Figure 2—figure supplement 2
Meta-analysis of respiratory viral loads (rVLs) of SARS-CoV-2, SARS-CoV-1 and influenza A(H1N1)pdm09 during the estimated infectious period.

Random-effects meta-analyses comparing the expected rVLs for COVID-19, SARS and A(H1N1)pdm09 cases during the infectious period. Quantitative specimen measurements were used to estimate rVLs, which …

Figure 3 with 5 supplements
Subgroup analyses of SARS-CoV-2 respiratory viral load (rVL) during the infectious period.

Random-effects meta-analyses comparing the expected rVLs of adult (≥18 years old) COVID-19 cases with pediatric (<18 years old) ones (top) and symptomatic/presymptomatic infections with asymptomatic …

Figure 3—figure supplement 1
Risk-of-bias sensitivity analysis of between-study heterogeneity for SARS-CoV-2 respiratory viral load (rVL) during the estimated infectious period.

Random-effects meta-analyses, based on the risk of bias of contributing studies, of the expected rVLs of COVID-19 cases during the infectious period. Quantitative rVLs refer to virus concentrations …

Figure 3—figure supplement 2
Risk-of-bias sensitivity analysis of between-study heterogeneity for SARS-CoV-1 respiratory viral load (rVL) during the estimated infectious period.

Random-effects meta-analyses, based on the risk of bias of contributing studies, of the expected rVLs of SARS cases during the infectious period. Quantitative rVLs refer to virus concentrations in …

Figure 3—figure supplement 3
Risk-of-bias sensitivity analysis of between-study heterogeneity for A(H1N1)pdm09 respiratory viral load (rVL) during the estimated infectious period.

Random-effects meta-analyses, based on the risk of bias of contributing studies, of the expected rVLs of A(H1N1)pdm09 cases during the infectious period. Quantitative rVLs refer to virus …

Figure 3—figure supplement 4
Risk-of-bias sensitivity analysis of between-study heterogeneity for SARS-CoV-2 respiratory viral load (rVL) for adult COVID-19 cases during the estimated infectious period.

Random-effects meta-analyses, based on the risk of bias of contributing studies, of the expected rVLs of adult (≥18 years old) COVID-19 cases during the infectious period. Quantitative rVLs refer to …

Figure 3—figure supplement 5
Risk-of-bias sensitivity analysis of between-study heterogeneity for SARS-CoV-2 respiratory viral load (rVL) for symptomatic/presymptomatic COVID-19 cases during the estimated infectious period.

Random-effects meta-analyses, based on the risk of bias of contributing studies, of the expected rVLs of symptomatic/presymptomatic (≥18 years old) COVID-19 cases during the infectious period. …

Figure 4 with 5 supplements
Heterogeneity and kinetics of SARS-CoV-2 respiratory viral load (rVL).

(A) Estimated distribution of rVL for SARS-CoV-2 (N = 3834 samples from N = 26 studies) and A(H1N1)pdm09 (N = 512 samples from N = 10 studies) throughout the infectious periods. (B, C) Estimated …

Figure 4—figure supplement 1
Respiratory viral loads for SARS-CoV-2, SARS-CoV-1 and A(H1N1)pdm09 best conform to Weibull distributions.

(AD) Normal (p≤0.01) (A), lognormal (p≤0.01) (B), gamma (p≤0.005) (C) and Weibull (p>0.10, not significant [NS]) (D) probability plots for individual sample data of SARS-CoV-2 respiratory viral …

Figure 4—figure supplement 2
Case heterogeneity in respiratory viral loads (rVLs) across viruses, COVID-19 subgroups and disease course.

(A–C) Estimated rVLs of SARS-CoV-2 (A), SARS-CoV-1 (B) and A(H1N1)pdm09 (C) across case percentile (cp) throughout the infectious periods. (DG) Estimated SARS-CoV-2 rVLs for adult (D), pediatric (E)…

Figure 4—figure supplement 3
Descriptive parameters for respiratory viral loads based on individual sample data.
Figure 4—figure supplement 4
Model parameters describing SARS-CoV-2 kinetics during respiratory infection.
Figure 4—figure supplement 5
Kinetics of SARS-CoV-2 and airway epithelial cells during respiratory infection.

(A, B) Estimated kinetics of uninfected (blue) and productively infected (red) airway epithelial cells (left axis) and SARS-CoV-2 (right axis) in the respiratory tract, as shown in linear (A) and …

Figure 5 with 5 supplements
Heterogeneity in shedding SARS-CoV-2 via droplets and aerosols.

(A, B) Estimated likelihood of respiratory particles containing viable SARS-CoV-2 when expelled by the mean (top) or 98th case percentile (cp) (bottom) COVID-19 cases at −1 (A) or 1 (B) days from …

Figure 5—figure supplement 1
Likelihood of respiratory particles containing SARS-CoV-2 or A(H1N1)pdm09.

(A–E) Estimated likelihood that droplets and aerosols contain viable SARS-CoV-2 when expelled by the 25th case percentile (cp) (A), mean (B), 65th cp (C), 80th cp (D) or 90th cp (E) for COVID-19 …

Figure 5—figure supplement 2
Rate profiles for particle expelled by respiratory activities.

(A–D) Rate profiles of particles expelled while talking (A), singing (B), breathing (C) and coughing (D). (E) Comparison of the rate profiles of aerosol emission from singing and different …

Figure 5—figure supplement 3
Heterogeneity in shedding SAR-CoV-2 via talking, breathing and coughing.

(A–C) Case heterogeneity in the total SARS-CoV-2 shedding rate (over all particle sizes) by talking at a moderate amplitude (A), breathing (B) or coughing (C) for COVID-19 cases across the …

Figure 5—figure supplement 4
Heterogeneity in infectiousness for COVID-19 and A(H1N1)pmd09 cases during the infectious period.

(A, B) Estimated time for a A(H1N1)pdm09 case to expel one virion via only aerosols (A) or either droplets or aerosols (B) by talking, singing, breathing or coughing. (C, D) Estimated time for a …

Figure 5—figure supplement 5
Heterogeneity in shedding A(H1N1)pdm09 via droplets and aerosols.

(A–D) Case heterogeneity in the total A(H1N1)pdm09 shedding rates while talking (A), singing (B), breathing (C) and coughing (D) during the infectious period. Data represent estimated rates for …

Tables

Appendix 1—table 1
Characteristics of contributing studies.
Study*CountryNo. of cases included (no. of specimens)No. of pediatric cases (no. of specimens)No. of asymptomatic cases (no. of specimens)Disease caused by virus (WHO case definition)Treatments given (type)†Individual data extracted (diluent volume reported)Adjusted viral load§ (type of specimen)Weight, % (meta-analysis category)||Weight, % (meta-regression)Risk of bias
Argyropoulos et al., 2020USA205 (205)00COVID-19 (confirmed)N/ANo (no)Yes (NPS)3.80 (V), 5.09 (A), 3.98 (S/Ps)2.13********
Baggio et al., 2020Switzerland405 (405)58 (58)0COVID-19 (confirmed)N/AYes (no)Yes (NPS)3.84 (V), 5.14 (A), 13.9 (P), 3.88 (S/Ps)4.20*******
Fajnzylber et al., 2020USA- (31)00COVID-19 (confirmed)Yes (remdesivir)Yes (yes)Yes (NPS, OPS)
No (Spu)
3.45 (V), 4.62 (A), 3.76 (S/Ps)0.32********
Hung et al., 2020South Korea2 (8)1 (6)0COVID-19 (confirmed)N/AYes (no)Yes (NPS, OPS)2.53 (V), 4.06 (S/Ps)0.08******
Hung et al., 2020South Korea12 (27)12 (27)3 (7)COVID-19 (confirmed)N/AYes (no)Yes (NPS)3.43 (V), 17.5 (P), 4.10 (S/Ps), 14.3 (As)0.28********
Hung et al., 2020China41 (310)00COVID-19 (confirmed)Yes (control group: lopinavir ritonavir, antimicrobial treatment for secondary bacterial infection as indicated clinically, hydrocortisone for those requiring oxygen support)No (no)Yes (NPS, OPS, POS)3.81 (V), 5.10 (A), 3.81 (S/Ps)3.22*********
Hurst et al., 2020USA133 (133)54 (54)52 (52)COVID-19 (confirmed)Yes (remdesivir)Yes (no)Yes (NPS)3.77 (V), 15.3 (P), 3.88 (S/Ps), 21.6 (As)1.38********
Iwasaki et al., 2020Japan5 (5)00COVID-19 (confirmed)N/AYes (no)Yes (NPS)2.53 (V), 3.37 (A), 4.12 (S/Ps)0.05****
Kawasuji et al., 2020Japan16 (16)--COVID-19 (confirmed)Yes (antivirals, antibiotics – specifics not reported)Yes (no)Yes (NPS)3.15 (V)0.18*****
L'Huillier et al., 2020Switzerland23 (23)23 (23)0COVID-19 (confirmed)N/AYes (no)Yes (NPS)2.91 (V), 14.7 (P), 3.73 (S/Ps)0.24********
Lavezzo et al., 2020Italy103 (110)2 (3)49 (49)COVID-19 (confirmed)N/AYes (yes)Yes (NPS, OPS)3.77 (V), 5.03 (A), 11.57 (P), 3.57 (S/Ps), 21.8 (As)1.14*******
Lennon et al., 2020USA2200 (2,200)18 (18)2200 (2200#)COVID-19 (confirmed)N/ANo (yes)Yes (NPS)3.88 (V), 5.20 (A), 24.0 (As)22.84*********
Lucas et al., 2020USA24 (33)00COVID-19 (confirmed)Yes (tocilizumab for moderate and severe patients, glucocorticoid and vasopressor for severe patients)Yes (yes)Yes (NPS)3.51 (V), 4.69 (A), 4.08 (S/Ps)0.34*******
Mitjà et al., 2020Spain148 (296)00COVID-19 (confirmed)N/ANo (no)Yes (NPS)3.81 (V), 5.10 (A), 3.93 (S/Ps)3.07*********
Pan et al., 2020China75 (104)-0COVID-19 (confirmed)N/AYes (no)Yes (OPS)
No (Spu)
3.45 (V), 2.50 (S/Ps)1.24****
Peng et al., 2020China6 (6)00COVID-19 (confirmed)Yes (arbidol, lopinavir, ritonavir, interferon alfa-2b inhalation)Yes (no)Yes (OPS)3.03 (V), 4.05 (A), 4.02 (S/Ps)0.06********
Perera et al., 2020China- (36)0-COVID-19 (confirmed)Yes lopinavir-ritonavir alone, combination lopinavir-ritonavir and ribavirin, ribavirin and β interferon, β interferon alone, combination ribavirin, β interferon, and tocilizumab, and corticosteroidYes (no)Yes (NPA, NPS, OPS, Spu)3.23 (V), 4.32 (A)0.39****
Shi et al., 2020China103 (103)00COVID-19 (confirmed)No (samples drawn before antivirals given)Yes (no)Yes (NPS, OPS)3.87 (V), 5.18 (A), 4.34 (S/Ps)1.07*****
Shrestha et al., 2020USA171 (171)00COVID-19 (confirmed)Yes (indicated no hydroxychloroquine or other COVID-19-related treatments were used)Yes (no)Yes (NPS)3.79 (V), 5.07 (A), 3.86 (S/Ps)1.78*******
To et al., 2020China23 (51)00COVID-19 (confirmed)N/AYes (yes)Yes (ETA, POS)3.37 (V), 4.51 (A), 3.25 (S/Ps)0.53*********
van Kampen et al., 2021The Netherlands- (154)00COVID-19 (confirmed)Yes (lopinavir-ritonavir with or without ribavirin and/or interferon beta 1b)Yes (yes)Yes (NPS, Spu)3.80 (V), 5.09 (A), 4.10 (S/Ps)1.60********
Vetter et al., 2020Switzerland5 (63)00COVID-19 (confirmed)Yes (paracetamol, alfuzosin, ibuprofen, enoxaparin, amoxicillin clarithromycin, piperacillin, tazobactam, lopinavir, ritonavir, folic acid)Yes (yes)Yes (NPS, OPS)3.68 (V), 4.93 (A), 4.14 (S/Ps)0.65*********
Wölfel et al., 2020Germany9 (136)01 (4)COVID-19 (confirmed)N/AYes (yes)Yes (NPS, OPS)
No (Spu)
3.76 (V), 5.03 (A), 3.93 (S/Ps)1.38*******
Wyllie et al., 2020USA40 (42)-9 (9)COVID-19 (confirmed)N/AYes (yes)Yes (NPS)3.55 (V), 4.75 (A), 4.00 (S/Ps), 18.3 (As)0.44*******
Xu et al., 2020China7 (14)7 (14)1 (1)COVID-19 (confirmed)Yes (α-interferon oral spray, azithromycin)Yes (no)Yes (NPS)3.40 (V). 17.3 (P), 4.1 (S/Ps)0.15********
Yonker et al., 2020USA17 (17)14 (14)0COVID-19 (confirmed)N/AYes (no)Yes (NPS)2.58 (V), 9.79 (P), 3.28 (S/Ps)0.18******
Zhang et al., 2020bChina9 (9)00COVID-19 (confirmed)N/AYes (no)Yes (NPS, OPS)2.97 (V), 3.97 (A), 3.68 (S/Ps)0.09********
Zheng et al., 2020China- (19)00COVID-19 (confirmed)Yes (gamma globulin, glucocorticoids, antibiotics, antiviral combination of interferon α inhalation, lopinavir-ritonavir combination, arbidol, favipiravir, and darunavir-cobicistat)Yes (no)Yes (POS, Spu)3.66 (V), 4.90 (A), 4.23 (S/Ps)0.20*******
Zou et al., 2020China14 (55)01 (4)COVID-19 (confirmed)N/AYes (no)Yes (NPS, OPS)3.64 (V), 4.87 (A), 3.65 (S/Ps)0.57*******
Chen et al., 2006China154 (154#)00SARS (confirmed)N/AYes (no)Yes (NPS)14.0 (V)1.59********
Chu et al., 2004**China11 (11)00SARS (confirmed)Yes (control group: ribavirin, hydrocortisone, methylprednisolone)Yes (yes)Yes (NPS)8.6 (V)0.11*********
Chu et al., 2005China57 (57)00SARS (confirmed)N/AYes (yes)Yes (NPA)13.3 (V)0.59*********
Cheng et al., 2004China59 (59)00SARS (confirmed)Yes (amoxicillin-clavulanate, azithromycin, levofloxacin, ribavirin, hydrocortisone, prednisolone, methylprednisolone)Yes (yes)Yes (NPA)13.4 (V)0.61*********
Hung et al., 2004China60 (60)00SARS (confirmed)N/ANo (yes)Yes (NPA)13.5 (V)0.62*******
Peiris et al., 2003**China14 (42)00SARS (confirmed)Yes (ribavirin, hydrocortisone, prednisolone, methylprednisolone)Yes (no)Yes (NPA)13.4 (V)0.44********
Poon et al., 2003China40 (40)00SARS (confirmed)N/ANo (yes)Yes (NPA)11.3 (V)0.42*****
Poon et al., 2004China- (43)00SARS (confirmed)N/ANo (yes)Yes (NPA)12.5 (V)0.45*******
Rodrigues Guimarães Alves et al., 2020Brazil86 (86)-15 (15)A(H1N1)pdm09 (confirmed)Yes (oseltamivir)No (yes)Yes (NPA, NPS, OPS)3.7 (V)0.89*****
Chan et al., 2011China58 (58)00A(H1N1)pdm09 (confirmed)Yes (oseltamivir, zanamivir, peramivir)Yes (no)Yes (NPA, NPS, OPS)3.7 (V)0.60******
Cheng et al., 2010China60 (60)-0A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (no)Yes (NPA)3.7 (V)0.62******
Cowling et al., 2010China45 (54)22 (31)0A(H1N1)pdm09 (confirmed)Yes (oseltamivir)Yes (yes)Yes (NPS, OPS)3.7 (V)0.56*********
Duchamp et al., 2010France209 (209)209 (209)0A(H1N1)pdm09 (confirmed)Yes (oseltamivir, zanamivir)No (yes)Yes (NPS)3.8 (V)2.17*****
Esposito et al., 2011Italy74 (282)74 (282)0A(H1N1)pdm09 (confirmed)NoYes (yes)Yes (NPS)3.8 (V)2.93*******
Hung et al., 2010China87 (87)-0A(H1N1)pdm09 (confirmed)Yes (oseltamivir)Yes (no)Yes (NPA, NPS)3.8 (V)0.90******
Ip et al., 2016China17 (20)7 (-)0A(H1N1)pdm09 (confirmed)N/AYes (no)Yes (NPS, OPS)3.6 (V)0.21*******
Ito et al., 2012Japan34 (34)-0A(H1N1)pdm09 (confirmed)No (pretreatment samples)Yes (yes)Yes (NPS)3.7 (V)0.35*****
Killingley et al., 2010United Kingdom12 (21)-0A(H1N1)pdm09 (confirmed)Yes (oseltamivir)Yes (yes)Yes (NPS)3.5 (V)0.22********
Launes et al., 2012Spain47 (47)47 (47)0A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (no)Yes (NPA)3.7 (V)0.49*******
Lee et al., 2011aChina48 (48)00A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (no)Yes (NPA)3.7 (V)0.50********
Lee et al., 2011aSingapore578 (578)231 (231)0A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (no)Yes (NPS)3.8 (V)6.00*********
Li et al., 2010aChina581 (581)522 (522)0A(H1N1)pdm09 (confirmed)Yes (oseltamivir)No (no)Yes (OPS)3.8 (V)6.03********
Li et al., 2010bChina27 (59)-0A(H1N1)pdm09 (confirmed)No (control group no treatment)No (no)Yes (NPA, NPS, OPS)3.7 (V)0.61*******
Loeb et al., 2012Canada97 (218)-- (17)A(H1N1)pdm09 (confirmed)NoNo (no)Yes (NPS)3.8 (V)2.26*******
Lu et al., 2012China13 (25)-0A(H1N1)pdm09 (confirmed)Yes (oseltamivir, zanamivir)Yes (no)Yes (NPS)3.5 (V)0.26*******
Meschi et al., 2011Italy533 (533)00A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (no)Yes (NPS)3.8 (V)0.92*********
Ngaosuwankul et al., 2010China12 (33)-0A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (yes)Yes (NPA, NPS, OPS)3.6 (V)0.34******
Rath et al., 2012Germany27 (41)27 (41)0A(H1N1)pdm09 (confirmed)Yes (oseltamivir)Yes (yes)Yes (NPS)3.7 (V)0.43*********
Suess et al., 2010Germany51 (129)12 (-)1 (1)A(H1N1)pdm09 (confirmed)Yes (oseltamivir)No (no)Yes (NPA, NPS, OPS)3.8 (V)1.34********
Thai et al., 2014Vietnam33 (123)16 (-)5 (28)A(H1N1)pdm09 (confirmed)Yes (oseltamivir)Yes (yes)Yes (NPS)3.8 (V)1.28*********
To et al., 2010aChina50 (50)00A(H1N1)pdm09 (confirmed)Yes (oseltamivir, zanamivir, inotropes)No (no)Yes (NPA, NPS)3.6 (V)0.52******
To et al., 2010bChina22 (22)-0A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (no)Yes (NPA, NPS, OPS)3.4 (V)0.23*****
Watanabe et al., 2011Japan251 (251)251 (251)0A(H1N1)pdm09 (confirmed)No (pretreatment samples)No (yes)Yes (NPA)3.8 (V)2.61**********
Wu et al., 2012China64 (89)-0A(H1N1)pdm09 (confirmed)Yes (oseltamivir)No (yes)Yes (NPS)3.7 (V)5.53*******
Yang et al., 2011China251 (251)-0A(H1N1)pdm09 (confirmed)N/ANo (yes)Yes (OPS)3.8 (V)6.57*****
  1. *Data shown as ‘-' were not obtained from the paper or authors.

    Responses of ‘N/A’ indicate that no details were reported on treatment for COVID-19 in the study.

  2. For studies reporting specimen measurements as individual sample data (either in numerical or graphical formats), the sample data was extracted for analysis.

    §Specimen measurements were converted to rVLs based on the dilution factor for specimens in transport media.

  3. ||Abbreviations for random-effects meta-analyses: virus meta-analysis (V), adult subgroup (A), pediatric subgroup (P), symptomatic/presymptomatic subgroup (S/Ps) and asymptomatic subgroup (As).

    The hybrid JBI critical appraisal checklist was used, with more stars indicating lower risk of bias. Studies were considered to have low risk of bias if they met the majority of the items (≥6/10 items). Results from each study are shown in Appendix 1—table 2.

  4. #For these studies, 2147 (Lennon et al., 2020) and 134 (Chen et al., 2006) individual specimen measurements were obtained for the individual sample datasets.

    **For Chu et al., 2004, only specimen measurements at 20 DFSO were collected as 5–15 DFSO were specimens reported in Peiris et al., 2003.

  5. NPS: nasopharyngeal swab; OPS, oropharyngeal swab; Spu: sputum; POS, posterior oropharyngeal saliva; NPA: nasopharyngeal aspirate; ETA: endotracheal aspirate; DFSO: days from symptom onset; rVL: respiratory viral load.

Appendix 1—table 2
Assessment of risk of bias based on the hybrid JBI critical appraisal checklist.
Checklist items*
Study12345678910
Argyropoulos et al., 2020YYYYNYYNYY
Baggio et al., 2020YYYYNYYNNY
Fajnzylber et al., 2020YYYYNYYYNY
Hung et al., 2020NYNYNYYNYY
Hung et al., 2020YYYYNYYNYY
Hung et al., 2020YYYYYYYNYY
Hung et al., 2020YYYYNYYNYY
Iwasaki et al., 2020YNUUNYYNNY
Kawasuji et al., 2020YYUUNYYNNY
L'Huillier et al., 2020YYYYNYYNYY
Lavezzo et al., 2020YYNYNYYNYY
Lennon et al., 2020YYYYYYYNYY
Lucas et al., 2020YYUUNYYYYY
Mitjà et al., 2020YYYYYYYNYY
Pan et al., 2020YNUUNYYNNY
Peng et al., 2020YYYYNYYNYY
Perera et al., 2020YNUUNYYNNY
Shi et al., 2020YYUUNYYNNY
Shrestha et al., 2020NYYYNYYNYY
To et al., 2020YYYYNYYYYY
van Kampen et al., 2021YYYYNYYNYY
Vetter et al., 2020YYYYNYYYYY
Wölfel et al., 2020YYNUNYYYYY
Wyllie et al., 2020YYUYNYYYNY
Xu et al., 2020YYYYNYYNYY
Yonker et al., 2020YYNUNYYNYY
Zhang et al., 2020bYYYYNYYNYY
Zheng et al., 2020YYYYNYYNNY
Zou et al., 2020NYYYNYYNYY
Chen et al., 2006YYYYNYYNYY
Chu et al., 2004YYYYNYYYYY
Chu et al., 2005YYYYNYYYYY
Cheng et al., 2004YYYYNYYYYY
Hung et al., 2004YYUUNYYYYY
Peiris et al., 2003YYYYNYYNYY
Poon et al., 2003YNUUNYYYNY
Poon et al., 2004YNYYNYYYNY
Rodrigues Guimarães Alves et al., 2020YNUUNYYYNY
Chan et al., 2011YYUUNYYNYY
Cheng et al., 2010YNYYNYYNNY
Cowling et al., 2010YYYYNYYYYY
Duchamp et al., 2010YYUUNYYYNN
Esposito et al., 2011YYYUNYYYNY
Hung et al., 2010NYYYNYYNNY
Ip et al., 2016YYYUNYYNYY
Ito et al., 2012YNUUNYYYNY
Killingley et al., 2010YYYYNYYYNY
Launes et al., 2012YYYYNYYNNY
Lee et al., 2011aYYYYNYYNYY
Lee et al., 2011aYYYYYYYNYY
Li et al., 2010aYYYYNYYNYY
Li et al., 2010bYYYYNYYNNY
Loeb et al., 2012YYYYNYYNNY
Lu et al., 2012YYYYNYYNNY
Meschi et al., 2011YYYYYYYNYY
Ngaosuwankul et al., 2010YYUUNYYYNY
Rath et al., 2012YYYYNYYYYY
Suess et al., 2010YYYYNYYNYY
Thai et al., 2014YYYYNYYYYY
To et al., 2010aYYUUNYYNYY
To et al., 2010bYYUUNYYNNY
Watanabe et al., 2011YYYYYYYYYY
Wu et al., 2012YYYUNYYYNY
Yang et al., 2011YNUUYYYNNY
  1. *Descriptions of each item are included in the hybrid JBI critical appraisal checklist (Appendix). Y (green), U (yellow) and N (red) represent yes, unclear and no, respectively.

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