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Prevalence of post-COVID-19 symptoms in hospitalized and non-hospitalized COVID-19 survivors: A systematic review and meta-analysis

      Highlights

      • This meta-analysis quantitively analysed data from 29 peer-reviewed studies and 4 preprints.
      • The results showed that 63.2, 71.9 and 45.9% of the sample exhibited ≥one post-COVID symptoms 30, 60, or ≥90days after onset or hospitalization.
      • Fatigue and dyspnea were the most prevalent symptoms (pooled prevalence from 35% to 60%) depending on the follow-up period.
      • The prevalence of each post-COVID symptom in isolation dropped off 30days after (10–15%) but increased at 60days or longer after (40–60%) onset.

      Abstract

      Background

      Single studies support the presence of several post-COVID-19 symptoms; however, no meta-analysis differentiating hospitalized and non-hospitalized patients has been published to date. This meta-analysis analyses the prevalence of post-COVID-19 symptoms in hospitalized and non-hospitalized patients recovered from COVID-19

      . Methods

      MEDLINE, CINAHL, PubMed, EMBASE, and Web of Science databases, as well as medRxiv and bioRxiv preprint servers were searched up to March 15, 2021. Peer-reviewed studies or preprints reporting data on post-COVID-19 symptoms collected by personal, telephonic or electronic interview were included. Methodological quality of the studies was assessed using the Newcastle-Ottawa Scale. We used a random-effects models for meta-analytical pooled prevalence of each post-COVID-19 symptom, and I² statistics for heterogeneity. Data synthesis was categorized at 30, 60, and ≥90 days after

      . Results

      From 15,577 studies identified, 29 peer-reviewed studies and 4 preprints met inclusion criteria. The sample included 15,244 hospitalized and 9011 non-hospitalized patients. The methodological quality of most studies was fair. The results showed that 63.2, 71.9 and 45.9% of the sample exhibited ≥one post-COVID-19 symptom at 30, 60, or ≥90days after onset/hospitalization. Fatigue and dyspnea were the most prevalent symptoms with a pooled prevalence ranging from 35 to 60% depending on the follow-up. Other post-COVID-19 symptoms included cough (20–25%), anosmia (10–20%), ageusia (15–20%) or joint pain (15–20%). Time trend analysis revealed a decreased prevalence 30days after with an increase after 60days

      . Conclusion

      This meta-analysis shows that post-COVID-19 symptoms are present in more than 60% of patients infected by SARS-CoV‑2. Fatigue and dyspnea were the most prevalent post-COVID-19 symptoms, particularly 60 and ≥90 days after.

      Keywords

      1. Introduction

      The world is suffering a dramatic situation of catastrophic proportions due to the rapid worldwide spread of the coronavirus disease 2019 (COVID-19) caused by the pathogen acute respiratory syndrome coronavirus 2 (SARS-CoV-2) [
      • Zhu N.
      • Zhang D.
      • Wang W.
      • et al.
      A novel coronavirus from patients with pneumonia in China, 2019.
      ]. Symptoms associated with SARS-CoV-2 infection are heterogeneous and affect different systems such as respiratory (cough, sore throat, rhinorrhea, dyspnea), musculoskeletal (myalgias), gastrointestinal (diarrhoea, vomiting), and neurological (headaches, myopathy, ageusia, anosmia) [
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      ].
      Understandably, most literature has concentrated on the potential pathophysiology of the disease and on the management of acute cases at hospitalization periods. However, a second pandemic has emerged: post-COVID-19 sequalae and “long-haulers” [
      • Marshall M.
      The lasting misery of coronavirus long-haulers.
      ]. Since millions of people will survive to SARS-CoV-2 infection; the number of individuals suffering COVID-19 sequelae, i.e., long hauler, will dramatically increase with time [
      • Rubin R.
      As their numbers grow, COVID-19 “long haulers” stump experts.
      ]. Therefore, identification of the COVID-19 aftermaths will be crucial for healthcare professionals.
      Current evidence suggests the presence of a plethora of symptoms in subjects recovered from COVID-19. However, literature investigating the symptoms after SARS-CoV-2 infection is on its infancy in comparison with the literature available on the acute COVID-19 phase. Different terms are currently used for describing the presence of post-COVID-19 symptoms (e.g., post-COVID-19 syndrome, persistent post-COVID), being “long COVID” probably the most expanded term [
      • Nabavi N.
      Long covid: how to define it and how to manage it.
      ]. “Long COVID” is used to describe illness in people who have recovered from COVID-19 but still exhibit symptoms for far longer than would be expected [
      • Nabavi N.
      Long covid: how to define it and how to manage it.
      ]. In the last months, an increasing number of studies assessing the presence of post-COVID-19 symptoms have been published. In fact, a meta-analysis has been recently published as a preprint [
      • Lopez-Leon S.
      • Wegman-Ostrosky T.
      • Perelman C.
      • Sepulveda R.
      • Rebolledo P.A.
      • Cuapio A.
      • et al.
      More than 50 Long-term effects of COVID-19: a systematic review and meta-analysis.
      ]. This meta-analysis found that 80% of COVID-19 survivors exhibited at least one post-COVID-19 symptom, being fatigue (58%), headache (44%), attention disorders (27%), hair loss (25%), and dyspnea (24%) the most frequent [
      • Lopez-Leon S.
      • Wegman-Ostrosky T.
      • Perelman C.
      • Sepulveda R.
      • Rebolledo P.A.
      • Cuapio A.
      • et al.
      More than 50 Long-term effects of COVID-19: a systematic review and meta-analysis.
      ]. However, this review pooled prevalence rates without considering follow-up periods after symptoms and did not differentiate between hospitalized and non-hospitalized patients [
      • Lopez-Leon S.
      • Wegman-Ostrosky T.
      • Perelman C.
      • Sepulveda R.
      • Rebolledo P.A.
      • Cuapio A.
      • et al.
      More than 50 Long-term effects of COVID-19: a systematic review and meta-analysis.
      ]. These two considerations are highly important to properly determine the presence of post-COVID-19 symptoms [
      • Fernández-de-las-Peñas C.
      • Palacios-Ceña D.
      • Gómez-Mayordomo V.
      • Cuadrado M.L.
      • Florencio L.L.
      Defining post-COVID symptoms (post-acute COVID, long COVID, persistent post-COVID): an integrative classification.
      ].
      This study presents a systematic review and meta-analysis pooling prevalence data of post-COVID-19 symptoms differentiating between hospitalized and non-hospitalized COVID-19 survivors and analysing the prevalence of post-COVID-19 symptoms at different timepoints. The research questions of this systematic review and meta-analysis were: what is the prevalence of post-COVID-19 symptoms in individuals recovered from SARS-CoV-2 infection?, is there any difference in post-COVID-19 between hospitalized and non-hospitalized patients? and, what is the time-course of post-COVID-19 symptoms in the next months following SARS-CoV-2 infection?

      2. Methods

      This systematic review and meta-analysis adheres to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) statement as appropriate [
      • Liberati A.
      • Altman D.G.
      • Tetzlaff J.
      • Mulrow C.
      • Gøtzsche P.C.
      • Ioannidis J.P.A.
      • et al.
      The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration.
      ]. It was also prospectively registered in the Open Science Framework Registry database with the following link https://doi.org/10.17605/OSF.IO/ESWQZ.

      2.1 Systematic literature search

      Electronic literature searches were conducted on MEDLINE, CINAHL, PubMed, EMBASE, and Web of Science databases, as well as on preprint servers medRxiv and bioRxiv, for studies published to March 20, 2021. We also screened the reference list of the identified papers. Database search strategies were conducted with the assistance of an experienced health science librarian. Searches were limited to human studies by using the following terms: “long COVID syndrome”, “long COVID symptoms”, “long haul COVID”, “long hauler COVID”, “chronic COVID syndrome”, “chronic COVID symptoms”, “post-acute COVID syndrome”, “post-acute COVID symptoms”, “persistent COVID syndrome”, “post-COVID”, “COVID sequalae” OR “persistent COVID symptoms”. The inclusion/exclusion criteria were formulated by using the Population, Intervention, Comparison, Outcome (PICO) questions:
      Population: Adults (>18 years), positively diagnosed of SARS-CoV-2 infection with real-time reverse transcription-polymerase chain reaction (PCR) assay of nasopharyngeal/oral swab samples, during the first wave of the pandemic (from January 1 to June 30, 2020). We included both hospitalized and non-hospitalized patients.
      Intervention: Not applicable
      Comparison: Not applicable
      Outcomes: Monitorization or collection of the presence of multiple symptoms in COVID-19 survivors after SARS-CoV-2 infection, i.e., hospital discharge or symptoms onset, by either personal, telephonic, or electronical interview. Studies monitoring just changes in immunological, serological or radiological outcomes without assessment of post-COVID −19 symptoms were excluded.

      2.2 Screening process, study selection and data extraction

      This review/meta-analysis considered original research including observational cohort or case-control studies where samples of COVID-19 survivors, either hospitalized or non-hospitalized, were followed for the presence of symptoms for more than two weeks after infection. Based on pre-existing data and timeframes [
      • Fernández-de-las-Peñas C.
      • Palacios-Ceña D.
      • Gómez-Mayordomo V.
      • Cuadrado M.L.
      • Florencio L.L.
      Defining post-COVID symptoms (post-acute COVID, long COVID, persistent post-COVID): an integrative classification.
      ], we selected 30, 60, and ≥90 days after symptoms onset as pre-endpoints selected for the analysis. Editorials, opinion, and correspondence articles were excluded.
      Two authors reviewed the title and abstract of publications identified in the databases. First, the duplicates were removed. Second, title and abstract of the articles were screened for potential eligibility and posterior full-read text. Data including authors, country, sample size, clinical data, settings (hospitalization/no hospitalization), symptoms at onset, and post-COVID-19 symptoms at different follow-up periods were extracted from each study. Both authors had to achieve a consensus on data-extraction. Discrepancies between the reviewers at any stage of the screening process were resolved by asking a third author, if necessary.

      2.3 Methodological quality

      The methodological quality of the studies was independently assessed by two authors using the Newcastle-Ottawa Scale, a star rating system that evaluates the risk of bias of case-control and cohort studies [

      Wells G.A., Tugwell P., O'Connell D., Welch V., Peterson J., Shea B., et al. The newcastle-ottawa scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses 2015.

      ]. This scale, when applied to cohort studies, includes the following sections: case selection, comparability, and exposure. Case selection includes representativeness of cohort, selection of non-exposed cohort, ascertainment of exposure (case definition), and outcome of interest no present at start. Comparability evaluates the analysis of comparison (e.g., controlled for age, gender, or other factors) between groups (exposed and non-exposed). Exposure includes outcome assessment, long enough follow-up period, and adequate follow-up. In longitudinal cohort studies or case-control studies, a maximum of 9 stars can be awarded. In cross-sectional cohort studies, a maximum of 3 stars can be awarded. Studies scoring 3 are considered of good quality, those scoring 2 are of fair quality and studies scoring 1 are of poor quality [

      Wells G.A., Tugwell P., O'Connell D., Welch V., Peterson J., Shea B., et al. The newcastle-ottawa scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses 2015.

      ]. Methodological quality of the included studies was determined by two authors and the differences, if existed, were discussed. In the case of disagreement, a third researcher arbitrated a consensus decision.

      2.4 Data synthesis and analysis

      The meta-analysis was conducted with the R software 4.0.0 using meta and dmetar packages. Percentages and frequencies of each symptom at onset/hospitalization and each symptom were extracted from studies and an overall proportion was calculated reporting a single proportion using the metaprop function. We used a random-effects model because potential heterogeneity was expected. An I2 value ≥75% was considered to indicate serious heterogeneity. We were not able to assess funnel plot asymmetry due to an insufficient number of studies investigating the same post-COVID-19 symptom at a particular follow-up. We calculated sample size-weighted mean scores for each study reporting data alongside 95% confidence intervals (95%CI) in addition to any potential meta-analytical summary effect on the pooled prevalence data for each post-COVID-19 symptom. Data synthesis was categorized by time after onset/hospitalization into three follow-up periods (symptoms at 30 days, 60 days, and ≥90 days). To determine the time-course of post-COVID-19 symptoms over time (from onset to ≥90 days after), Freeman-Tukey double arcsine transformation was conducted using the escalc function in the metafor package. The rma.mv (meta-analytic multilevel random effect model with moderators via linear mixed-effect models) was used to carry out a multilevel metanalysis with three levels to identify time and time *subgroup effect. For meta-analyses of studies reporting outcomes at multiple time points, it may be reasonable to assume that the true effects are correlated over time according to an autoregressive structure; therefore, a heteroscedastic autoregressive (HAR) model was adopted. Grouping by gender was not possible due to lack of data (see discussion section).
      For quantitative data (age, days at hospital), overall means and standard deviations (SD) were calculated using the pool.groups function from the dmetar package. Median and interquartile range (IQR) were converted to mean and SD as described by Luo et al. [
      • Luo D.
      • Wan X.
      • Liu J.
      • Tong T.
      Optimally estimating the sample mean from the sample size, median, mid-range, and/or mid-quartile range.
      ]. When necessary, data were estimated from graphs with the GetData Graph Digitizer v.2.26.0.20 software.

      2.5 Role of the funding source

      There was no funding source for this study.

      2.6 Patient and public involvement

      Patients were not involved in the study since this was a meta-analysis of the literature.

      3. Results

      3.1 Study selection

      The selection process is shown in Fig. 1. The electronic search identified 15,577 potential titles. After removing duplicates and papers not directly related to post-COVID-19 symptoms, 64 studies remained. Twenty-six (n = 26) were excluded after title/abstract examination. One preprint was excluded because it analysed risk factors and clusters but not detailed specific post-COVID-19 symptoms [
      • Huang Y.
      • Pinto M.D.
      • Borelli J.L.
      • et al.
      COVID symptoms, symptom clusters, and predictors for becoming a long-hauler: looking for clarity in the haze of the pandemic.
      ]; one study was excluded because it was a case series [
      • Sofian M.
      • Velayati A.A.
      • Banifazl M.
      • et al.
      SARS-CoV2, a virus with many faces: a series of cases with prolonged persistence of COVID-19 symptoms.
      ]; another one because mortality rate, not post-COVID-19 symptoms, was analyzed [
      • Islam N.
      • Lewington S.
      • Kharbanda R.K.
      • Davies J.
      • Várnai K.A.
      • Lacey B.
      Sixty-day consequences of COVID-19 in patients discharged from hospital: an electronic health records study.
      ]; and the last one because it included children, not adults, with COVID-19 [
      • Ludvigsson J.F.
      Case report and systematic review suggest that children may experience similar long-term effects to adults after clinical COVID-19.
      ].
      Fig 1
      Fig. 1Preferred reporting items for systematic reviews and meta-analyses (PRISMA) flow diagram.
      A total of 29 published studies [
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      ,
      • Garrigues E.
      • Janvier P.
      • Kherabi Y.
      • et al.
      Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19.
      ,
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      ,
      • Halpin S.J.
      • McIvor C.
      • Whyatt G.
      • et al.
      Postdischarge symptoms and rehabilitation needs in survivors of COVID-19 infection: a cross-sectional evaluation.
      ,
      • Galván-Tejada C.E.
      • Herrera-García C.F.
      • Godina-González S.
      • et al.
      Persistence of COVID-19 symptoms after recovery in mexican population.
      ,
      • Stavem K.
      • Ghanima W.
      • Olsen M.K.
      • Gilboe H.M.
      • Einvik G.
      Persistent symptoms 1.5–6 months after COVID-19 in non-hospitalised subjects: a population-based cohort study.
      ,
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      ,
      • Xiong Q.
      • Xu M.
      • Li J.
      • et al.
      Clinical sequelae of COVID-19 survivors in Wuhan, China: a single-centre longitudinal study.
      ,
      • Huang C.
      • Huang L.
      • Wang Y.
      • et al.
      6-month consequences of COVID-19 in patients discharged from hospital: a cohort study.
      ,
      • Moreno-Pérez O.
      • Merino E.
      • Leon-Ramirez J.M.
      • et al.
      Post-acute COVID-19 syndrome. incidence and risk factors: a mediterranean cohort study.
      ,
      • Sykes D.L.
      • Holdsworth L.
      • Jawad N.
      • Gunasekera P.
      • Morice A.H.
      • Crooks M.G.
      Post-COVID-19 symptom burden: what is long-COVID and how should we manage it?.
      ,
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      ,
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      ,
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      ,
      • Kamal M.
      • Abo Omirah M.
      • Hussein A.
      • Saeed H
      Assessment and characterisation of post-COVID-19 manifestations.
      ,
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of long COVID.
      ,
      • Iqbal A.
      • Iqbal K.
      • Ali S.A.
      • et al.
      The COVID-19 sequelae: a cross-sectional evaluation of post-recovery symptoms and the need for rehabilitation of COVID-19 survivors.
      ,
      • Zhou M.
      • Cai J.
      • Sun W.
      • et al.
      Does Post-COVID-19 symptoms exist? A longitudinal study of COVID-19 sequelae in Wenzhou, China.
      ,
      • Venturelli S.
      • Benatti S.V.
      • Casati M.
      • et al.
      Surviving COVID-19 in Bergamo province: a post-acute outpatient re-evaluation.
      ,
      • Suárez-Robles M.
      • del Rosario Iguaran-Bermúdez M.
      • García-Klepizg J.L.
      • Lorenzo-Villalba N.
      • Méndez-Bailón M.
      Ninety days post-hospitalization evaluation of residual COVID-19 symptoms through a phone call check list.
      ,
      • L Morin
      • Savale L.
      • et al.
      Writing Committee for the COMEBAC Study Group
      Four-month clinical status of a cohort of patients after hospitalization for COVID-19.
      ,
      • Chopra V.
      • Flanders S.A.
      • O'Malley M.
      • Malani A.N.
      • Prescott H.C
      Sixty-day outcomes among patients hospitalized with COVID-19.
      ,
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      ,
      • Nehme M.
      • Braillard O.
      • Alcoba G.
      • et al.
      COVID-19 symptoms: longitudinal evolution and persistence in outpatient settings.
      ,
      • Tenforde M.W.
      • Kim S.S.
      • Lindsell C.J.
      • et al.
      Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network- united states.
      ,
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      ,
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      ,
      • Townsend L.
      • Dyer A.H.
      • Jones K.
      • et al.
      Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection.
      ,
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      ] and five medRxiv preprints [
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of Long-COVID: analysis of COVID cases and their symptoms collected by the COVID symptoms study app.
      ,
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      ,
      • Munblit D.
      • Bobkova P.
      • Spiridonova E.
      • et al.
      Risk factors for long-term consequences of COVID-19 in hospitalised adults in moscow using the isaric global follow-up protocol: stopcovid cohort study.
      ,
      • Perlis R.H.
      • Green J.
      • Santillana M.H.
      • et al.
      Persistence of symptoms up to 10 months following acute COVID-19 illness.
      ,

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      ] were initially included in the review/meta-analysis (Fig. 1). One preprint [
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of Long-COVID: analysis of COVID cases and their symptoms collected by the COVID symptoms study app.
      ] was excluded because the same study has been posteriorly published in a peer-reviewed journal [
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of long COVID.
      ]. Therefore, a total of 29 peer-reviewed studies [
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      ,
      • Garrigues E.
      • Janvier P.
      • Kherabi Y.
      • et al.
      Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19.
      ,
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      ,
      • Halpin S.J.
      • McIvor C.
      • Whyatt G.
      • et al.
      Postdischarge symptoms and rehabilitation needs in survivors of COVID-19 infection: a cross-sectional evaluation.
      ,
      • Galván-Tejada C.E.
      • Herrera-García C.F.
      • Godina-González S.
      • et al.
      Persistence of COVID-19 symptoms after recovery in mexican population.
      ,
      • Stavem K.
      • Ghanima W.
      • Olsen M.K.
      • Gilboe H.M.
      • Einvik G.
      Persistent symptoms 1.5–6 months after COVID-19 in non-hospitalised subjects: a population-based cohort study.
      ,
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      ,
      • Xiong Q.
      • Xu M.
      • Li J.
      • et al.
      Clinical sequelae of COVID-19 survivors in Wuhan, China: a single-centre longitudinal study.
      ,
      • Huang C.
      • Huang L.
      • Wang Y.
      • et al.
      6-month consequences of COVID-19 in patients discharged from hospital: a cohort study.
      ,
      • Moreno-Pérez O.
      • Merino E.
      • Leon-Ramirez J.M.
      • et al.
      Post-acute COVID-19 syndrome. incidence and risk factors: a mediterranean cohort study.
      ,
      • Sykes D.L.
      • Holdsworth L.
      • Jawad N.
      • Gunasekera P.
      • Morice A.H.
      • Crooks M.G.
      Post-COVID-19 symptom burden: what is long-COVID and how should we manage it?.
      ,
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      ,
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      ,
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      ,
      • Kamal M.
      • Abo Omirah M.
      • Hussein A.
      • Saeed H
      Assessment and characterisation of post-COVID-19 manifestations.
      ,
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of long COVID.
      ,
      • Iqbal A.
      • Iqbal K.
      • Ali S.A.
      • et al.
      The COVID-19 sequelae: a cross-sectional evaluation of post-recovery symptoms and the need for rehabilitation of COVID-19 survivors.
      ,
      • Zhou M.
      • Cai J.
      • Sun W.
      • et al.
      Does Post-COVID-19 symptoms exist? A longitudinal study of COVID-19 sequelae in Wenzhou, China.
      ,
      • Venturelli S.
      • Benatti S.V.
      • Casati M.
      • et al.
      Surviving COVID-19 in Bergamo province: a post-acute outpatient re-evaluation.
      ,
      • Suárez-Robles M.
      • del Rosario Iguaran-Bermúdez M.
      • García-Klepizg J.L.
      • Lorenzo-Villalba N.
      • Méndez-Bailón M.
      Ninety days post-hospitalization evaluation of residual COVID-19 symptoms through a phone call check list.
      ,
      • L Morin
      • Savale L.
      • et al.
      Writing Committee for the COMEBAC Study Group
      Four-month clinical status of a cohort of patients after hospitalization for COVID-19.
      ,
      • Chopra V.
      • Flanders S.A.
      • O'Malley M.
      • Malani A.N.
      • Prescott H.C
      Sixty-day outcomes among patients hospitalized with COVID-19.
      ,
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      ,
      • Nehme M.
      • Braillard O.
      • Alcoba G.
      • et al.
      COVID-19 symptoms: longitudinal evolution and persistence in outpatient settings.
      ,
      • Tenforde M.W.
      • Kim S.S.
      • Lindsell C.J.
      • et al.
      Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network- united states.
      ,
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      ,
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      ,
      • Townsend L.
      • Dyer A.H.
      • Jones K.
      • et al.
      Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection.
      ,
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      ] and four medRxiv preprints [
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      ,
      • Munblit D.
      • Bobkova P.
      • Spiridonova E.
      • et al.
      Risk factors for long-term consequences of COVID-19 in hospitalised adults in moscow using the isaric global follow-up protocol: stopcovid cohort study.
      ,
      • Perlis R.H.
      • Green J.
      • Santillana M.H.
      • et al.
      Persistence of symptoms up to 10 months following acute COVID-19 illness.
      ,

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      ] were included in the systematic review and meta-analysis.

      3.2 Sample characteristics

      The characteristics of the COVID-19 populations of the included studies are shown in Table 1. The total sample comprised 24,255 COVID-19 survivors (52.26% female; mean ± SD age: 47.8 ± 16.6 years); 15,244 were hospitalized (42.7% female; age: 48.6 ± 17.4) whereas 9011 (70.2% female; age: 44.3 ± 14.8) were non-hospitalized patients. The mean length of hospital stay due to SARS-CoV-2 infection was 12.5 days (SD 6.8). From those hospitalized, 402 patients (8%) required ICU admission (mean stay: 15 ± 14.6 days).
      Table 1Characteristics of the included studies investigating post-COVID-19 symptoms.
      StudyCountryParticipants (Male/Female)HospitalizationAge Mean (SD)Data assessmentDays onset to follow-up (median)
      Carvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      France150 (66 / 84)YES49 (15)Telephone30-60
      Garrigues et al. 2020
      • Garrigues E.
      • Janvier P.
      • Kherabi Y.
      • et al.
      Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19.
      France120 (73 / 47)YES63.2 (15.7)Telephone100
      Carfi et al 2020
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      Italy143 (90 / 53)YES56.5 (14.6)Face-to-face60
      Mandal et al. 2020
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      UK384 (239 / 145)YES59.9 (16.1)Telephone54
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      UK110 (68 / 42)YES60 IQR 46-73Face-to-face90
      Jacobs et al. 2020
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      Italy183 (112 / 71)YES57 IQR 48-68Telephone35
      Townsend et al. 2020
      • Townsend L.
      • Dyer A.H.
      • Jones K.
      • et al.
      Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection.
      Ireland128 (59 / 69)YES49.5 (15)Face-to-face63
      Wang et al. 2020
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      China131 (59 / 72)YES49 (36, 62)Face-to-face28
      Halpin et al. 2021
      • Halpin S.J.
      • McIvor C.
      • Whyatt G.
      • et al.
      Postdischarge symptoms and rehabilitation needs in survivors of COVID-19 infection: a cross-sectional evaluation.
      UK100 (54 / 46)YES66.66Telephone50
      Xiong et al. 2021
      • Xiong Q.
      • Xu M.
      • Li J.
      • et al.
      Clinical sequelae of COVID-19 survivors in Wuhan, China: a single-centre longitudinal study.
      China538 (245 / 293)YES52 IQR 41-62Telephone97
      Huang et al. 2021
      • Huang C.
      • Huang L.
      • Wang Y.
      • et al.
      6-month consequences of COVID-19 in patients discharged from hospital: a cohort study.
      China1,733 (897 / 836)YES57 IQR 47-65Face-to-face186
      Kamal et al. 2020
      • Kamal M.
      • Abo Omirah M.
      • Hussein A.
      • Saeed H
      Assessment and characterisation of post-COVID-19 manifestations.
      Egypt287 (103 /184)YES32.3 (8.5)Postal60
      Moreno-Pérez et al. 2021
      • Moreno-Pérez O.
      • Merino E.
      • Leon-Ramirez J.M.
      • et al.
      Post-acute COVID-19 syndrome. incidence and risk factors: a mediterranean cohort study.
      Spain277 (146 /131)YES56 (42-67.5)Face-to-face77
      Perlis et al. 2021
      • Perlis R.H.
      • Green J.
      • Santillana M.H.
      • et al.
      Persistence of symptoms up to 10 months following acute COVID-19 illness.
      USA5,437 (3,189/2,248)YES37.87 (11.92)Website60
      Jacobson et al. 2021
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      USA22 (14 /8)YES50.6 (15.1)Face-to-face138
      Sykes et al. 2021
      • Sykes D.L.
      • Holdsworth L.
      • Jawad N.
      • Gunasekera P.
      • Morice A.H.
      • Crooks M.G.
      Post-COVID-19 symptom burden: what is long-COVID and how should we manage it?.
      UK134 (88 / 46)YES59.6 (14)Virtual113
      Zhou et al. 2021
      • Zhou M.
      • Cai J.
      • Sun W.
      • et al.
      Does Post-COVID-19 symptoms exist? A longitudinal study of COVID-19 sequelae in Wenzhou, China.
      China89 (46 / 43)YES43 (31-52)Face-to-face21
      Venturelli et al. 2021
      • Venturelli S.
      • Benatti S.V.
      • Casati M.
      • et al.
      Surviving COVID-19 in Bergamo province: a post-acute outpatient re-evaluation.
      Italy767 (515/ 252)YES63 (13.6)Telephone81
      Suarez-Robles et al. 2021
      • Suárez-Robles M.
      • del Rosario Iguaran-Bermúdez M.
      • García-Klepizg J.L.
      • Lorenzo-Villalba N.
      • Méndez-Bailón M.
      Ninety days post-hospitalization evaluation of residual COVID-19 symptoms through a phone call check list.
      France134 (515 / 252)YES58.5 (18.5)Telephone90
      COMEBAC Study Group et al. 2021
      • L Morin
      • Savale L.
      • et al.
      Writing Committee for the COMEBAC Study Group
      Four-month clinical status of a cohort of patients after hospitalization for COVID-19.
      France478 (277 / 201)YES60.9 (16.1)Telephone113
      Mumblit et al. 2021
      • Munblit D.
      • Bobkova P.
      • Spiridonova E.
      • et al.
      Risk factors for long-term consequences of COVID-19 in hospitalised adults in moscow using the isaric global follow-up protocol: stopcovid cohort study.
      Russia2,649 (1,296/1,353)YES56 (46-66)Telephone217.5
      Chopra et al. 2021
      • Chopra V.
      • Flanders S.A.
      • O'Malley M.
      • Malani A.N.
      • Prescott H.C
      Sixty-day outcomes among patients hospitalized with COVID-19.
      USA1250 (648 / 602)YES62 (50-72)Telephone60
      Nehme et al. 2020
      • Nehme M.
      • Braillard O.
      • Alcoba G.
      • et al.
      COVID-19 symptoms: longitudinal evolution and persistence in outpatient settings.
      Switzerland669 (268 / 401)NO42.8 (13.7)Telephone40
      Tenforde et al. 2020
      • Tenforde M.W.
      • Kim S.S.
      • Lindsell C.J.
      • et al.
      Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network- united states.
      USA270 (130 / 140)NO42.5 IQR 31-54Telephone21
      Goertz et al. 2020
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      Netherland2113 (310 / 1,803)NO47 IQR 39-54.0Website80
      Galván-Tejada et al. 2020
      • Galván-Tejada C.E.
      • Herrera-García C.F.
      • Godina-González S.
      • et al.
      Persistence of COVID-19 symptoms after recovery in mexican population.
      Mexico219 (111 / 108)NONRFace-to-face30
      Stavem et al. 2020
      • Stavem K.
      • Ghanima W.
      • Olsen M.K.
      • Gilboe H.M.
      • Einvik G.
      Persistent symptoms 1.5–6 months after COVID-19 in non-hospitalised subjects: a population-based cohort study.
      Norway451 (198 / 253)NO49.8 (15.2)Postal/Web95
      Petersen et al. 2020
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      Faroe Islands180 (82 / 98)NO39.9 (19.4)Telephone120
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      USA357 (NR)NO56 IQR 18-89Electronic30-60-90
      Sudre et al. 2020
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of long COVID.
      Multi-country4,182 (1,192 / 2,990)NO42 (32-53)Website30-60
      Logue et al. 2021
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      USA177 (76 /101)NO48 (15.2)Electronic169
      Jacobson et al. 2021
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      Jacobson et al included both hospitalized and non-hospitalized patients
      USA96 (49 / 47)NO41.6 (12.5)Face-to-face115
      Iqbal et al 2021
      • Iqbal A.
      • Iqbal K.
      • Ali S.A.
      • et al.
      The COVID-19 sequelae: a cross-sectional evaluation of post-recovery symptoms and the need for rehabilitation of COVID-19 survivors.
      Pakistan158 (71 / 87)NO32.1 (12.4)Telephone38
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      USA135 (100 / 79)NO48 (37-57)Telephone3 to 36 weeks
      SD: standard deviation; IQR: Interquartile range; NR: Not Reported
      low asterisk Jacobson et al included both hospitalized and non-hospitalized patients
      Almost 50% of the total sample exhibited at least one pre-existing comorbidity (one: 26.3%, 95%CI 25.3–28.0%; two: 17.6%, 95%CI 15.1–20.5%; ≥ three: 25.6%, 95%CI 11.4 −47.8%) with hypertension (22.9%, 95%CI 16.2–31.5%) and obesity (22.2%, 95%CI 13.9 −33.5%) being the most prevalent. Pre-existing comorbidities were, in general, more prevalent in hospitalized patients than in non-hospitalized patients. Table 2 summarizes the pooled prevalence of demographic and clinical data of COVID-19 survivors separated by hospitalization. Hospitalization data were collected from medical records in all studies.
      Table 2Pooled means of demographic and clinical data differentiated by hospitalized (n=15,244) and non-hospitalized (n=9,011) COVID-19 patients.
      Hospitalized (n=15,244)Non-Hospitalized (n=9,011)
      Age, mean (SD), years
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      48.7 (17.4)N=12,595 - 22 studies44.3 (14.8)N=8,792 - 11 studies
      Gender, male/femalen (%)
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      9,189 (57.5%) /6,791 (42.5%)2,584 (29.7%) /6,107 (70.3%)
      Medical co-morbidities
      Without comorbidities
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      38.7% [30.9; 47.0]N= 2,799 / 977I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 88% - 2 studies
      55.2% [48.0; 62.2]N = 2,062 / 3,507I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 93% - 4 studies
      1 comorbidity27.7% [26.1; 29.4]N = 755 / 2,799I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 74% - 2 studies
      25.6% [24.0; 27.2]N = 726 / 2,838I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 61% - 3 studies
      2 comorbidities19.6% [18.3; 20.9]N = 698 / 3,566I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 0% - 3 studies
      15.8% [12.3; 20.0]N = 413 / 2,838I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 89% - 3 studies
      3 or more comorbidities29.6% [10.9; 59.0]N = 591 / 2,883I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 98% - 3 studies
      16.1% [12.2; 20.9]N = 44 / 274I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = N/A -1 study
      Obesity29.0% [21.2; 38.2]N = 841 / 3,687I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 96% - 5 studies
      12.7 [4.3; 32.0]N = 1,155 / 4,491I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 93% - 3 studies
      Hypertension
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      30.9% [21.6; 42.1]N = 3,548 / 9,127I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 98% - 15 studies
      13.0% [7.9; 20.7]N = 224 / 1,375I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 81% - 6 studies
      Diabetes
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      14.2% [9.8; 20.1]N = 1,557 / 9,128I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 97% - 15 studies
      4.1% [2.1; 8.1]N = 180 / 5,106I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 90% - 6 studies
      Heart Disease
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      11.6% [7.8; 17.0]N = 487 / 8,864I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 96% - 14 studies
      2.3% [1.3; 4.0]N = 100 / 4,929I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 78% - 5 studies
      Asthma9.3% [5.5; 15.4]N = 219 / 5,619I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 96% - 8 studies
      12.0% [8.8; 16.1]N = 562 / 5,245I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 89% - 5 studies
      COPD
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      6.0% [4.1; 8.7]N = 195 / 8,252I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 94% - 11 studies
      2.2% [1.2; 4.0]N = 10 / 454I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 0% - 2 studies
      Cancer4.4% [2.5; 7.7]N = 140 / 7,975I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 95% - 10 studies
      1.9% [0.8; 4.2]N = 6 / 315I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 0% - 2 studies
      Kidney disease
      Significant differences between non-hospitalized and hospitalized COVID-19 patients
      5.3% [2.7; 9.8]N = 567 / 7,504I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 98% - 10 studies
      0.6% [0.4; 0.9]N = 27 / 4,475I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 0% - 3 studies
      Immune Disorders3.3% [1.3; 7.3]N = 92 / 4,707I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 93% - 8 studies
      4.6% [3.0; 7.2]N = 19 / 409I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
       = 0% - 2 studies
      Stay at the hospital, mean (SD), days12.6 (6.8)N=7,299 - 15 studies
      ICU) admissionYes/No, n (%)Stay at ICU, mean (SD), days492 (8%)N=4,507 - 12 studies14.97 (14.6)N= 391 - 7 studies
      COPD: Chronic Obstructive Pulmonary Disease; ICU: Intensive Care Unit; SD: Standard Deviation
      low asterisk Significant differences between non-hospitalized and hospitalized COVID-19 patients

      3.3 Methodological quality

      Thirty studies (88%) were cross-sectional, just one was of good quality (3/3 stars), 28 were considered of fair quality (2/3 stars), and two of poor quality (1/3 stars). One was a longitudinal cohort study with high methodological quality (8/9 stars), and two were case-control studies of poor quality (5/9 stars, with 0 stars in the comparability domain). No disagreement between authors was observed. Table 3 presents the Newcastle-Ottawa Scale scores for each study and a summary of every item.
      Table 3Newcastle - ottawa quality assessment scale - quality appraisal cohort/cross-sectional studies.
      SelectionComparabilityExposure
      Cohort StudyRepresentativeness of exposed cohortSelection of non-exposed cohortAscertainment of exposureOutcome of interest nor present at startStudy controls for age/genderStudy controls for additional factorAssessment of outcomeLong enough follow-upAdequate follow-upScore
      Carvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      2/3
      Garrigues et al. 2020
      • Garrigues E.
      • Janvier P.
      • Kherabi Y.
      • et al.
      Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19.
      2/3
      Carfi et al 2020
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      2/3
      Mandal et al. 2020
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      2/3
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
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      Galván-Tejada et al. 2020
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      3.4 Symptoms at onset or hospital admission experienced by COVID-19 patients

      Supplementary Table summarizes which study assessed each COVID-19 onset symptom and each post-COVID-19 symptom. Sixteen studies (48.5%) collected the post-COVID-19 data by telephonic interviews, whereas ten studies (30%) collected data face-to-face interviews.
      Pooled data of symptoms at onset and post-COVID-19 symptoms experienced by the total sample, including both hospitalized and non-hospitalized COVID-19 patients, are shown in Table 4. In the total sample, the most common symptoms experienced at SARS-CoV-2 infection were fatigue (63.4%), cough (60.2%), fever (55.3%), ageusia (46.0%), anosmia (45.7%) and dyspnea (44.1%). Among hospitalized patients, the most common onset symptoms at hospital admission included cough (65.2%), fever (59.45%), fatigue (48.0%), dyspnea (50.9%), anosmia (34.3%) and ageusia (34.0%). In non-hospitalized patients, the most common onset symptoms were fatigue (71.89%), myalgia (59%), cough (56%), fever (52.5%), anosmia (51.9%), and ageusia (51.8%). Most pooled data showed high level of heterogeneity (I2≥75%).
      Table 4Pooled prevalence of symptoms at onset, and Post-COVID-19 Symptoms 30, 60, and ≥90 days after Onset/Hospitalization.
      Onset30 days after60 days after≥90 days dafter
      THNHTHNHTHNHTHNH
      Fever55.3%59.4%52.5%---------
      95%CI42.9; 67.133.7; 80.941.4; 63.4---------
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      98%99%98%---------
      Event/Total5,217/10,9673,172/6,5492,045 / 4,418---------
      Studies1567---------
      Dyspnea44.1%50.9%38.9%13.2%9.2%15.7%27.2%24.5%39.9%26.3%33.3%19.1%
      95%CI29.3; 60.125.8; 75.523.0; 57.56.6; 29.32.0; 33.07.7; 29.314.9; 44.412.7; 41.99.7; 80.39.4; 34.923.4; 45.09.4; 34.9
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      99%98.0%99%96%95%97%99%99%99%99%97%99%
      Event/Total3,123 /5,815483 / 1,3972,640 /4,418279 /1,74176 / 464203 / 1,2771,211/ 7,962792 / 7,246419 / 7162,617 /4,385483 / 4,3851,677 /3,314
      Studies178983510821587
      Fatigue63.4%48.0%71.9%11.7%7.7%#11.8%56.2%53.9%63.2%35.3%38.4%29.8%
      95%CI48.3; 76.228.8; 67.848.3; 76.23.1; 35.37.1; 8.06.5; 20.528.3; 80.740.5; 66.81.9; 99.325.3; 46.830.4; 47.412.3; 56.3
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      99%98%99%95%0%88%98.0%96%99%99%99%99%
      Event/Total3,531 /5,134458 / 1,1053,073 /4,029230 / 1,297114 / 403116/ 8941,295 /2,029740 / 1,319555 / 7104,409 /9,8761,753 /6,5672,000 /3,309
      Studies135863386217107
      Chest Pain16.5%10.1%28.0%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      6.6%1.1%10.9%23.6%21.0%28.5%9.4%7.7%14.9%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      95%CI8.0; 30.93.5; 25.614.4; 47.31.5; 25.20.0; 77.13.3; 30.611.9; 41.514.4; 29.75.8; 72.26.7; 13.15.2; 11.29.9; 21.7
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      99979994%100%97%98%84%99%94.6%93%89%
      Event/Total1,561 /3,990115 / 1,0721,446 /2,918106 / 83227 / 28179 / 551481 / 1,27131 / 560350 / 718920 / 8,945252 / 6,437553 / 2,508
      Studies9545235321394
      Myalgia37.0%15.6%59.0%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      4.9%2.0%9.6%#14.7%8.1%32.1%10.9%9.7%12.6%
      95%CI21.2; 56.14.3; 42.953.2; 64.61.3; 17.20.0; 27.87.0; 12.95.1; 35.53.5; 17.36.8; 75.36.6; 17.73.9; 22.07.8; 19.9
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      98%95%90%81%82%0%99%98%99%99%98%97%
      Event/Total2,556 /4,956258 / 1,2252,298 /3,73178 / 78941 / 40337 / 386660 / 6,570286 / 5,857374 / 7131,198 /5,286191 / 5,826878 / 3,312
      Studies13675325321477
      Headache36.7%11.8%51.6%7.4%1.1%11.0%19.8%11.3%48.2%6.3%3.6%10.9%
      95%CI18.5; 59.81.2; 60.332.9; 69.82.3; 21.50.0; 72.94.2; 25.75.3; 52.44.7; 24.83.1; 96.53.2; 12.01.3; 9.95.7; 19.7
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      98%99%99%95%99%97%99%99%99%99%97%97%
      Event/Total2,866 /4,889143 / 5672,723 /4,322142 / 1,37029 / 314113 / 1,056833 / 6,858312 / 6,144521 / 7141,157 /8,63795 / 5,775867 / 2,862
      Studies1484246421266
      Eye irritation15.3%17.7%13.9%7.0%5.3%#9.7%9.8%9.8%-5.1%-5.1%
      95%CI8.6; 25.69.0; 32.06.0; 28.83.4;24.62.2; 12.53.4; 24.65.9; 15.85.9; 15.8-1.4; 17.2-1.4; 17.2
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      96%93%97%88%68%94%N/AN/A97%-97%
      Event/Total688 / 3,24259 / 326629 / 2,91657 / 64917 / 27240 / 37714 / 14314 / 143-262 / 2,564-262 / 2,564
      Studies52342211-2-2
      Sputum18.9%14.8%25.5%4.7%4.7%-7.7%7.7%-6.5%3.4%#10.7%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      95%CI13.0; 26.79.2; 22.917.1; 36.10.0; 49.50.0; 49.5-3.9; 13.33.9; 13.3-3.1; 13.12.2; 5.14.5; 23.3
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      96%86%96%99%99%N/AN/A96%38%94%
      Event/Total1,025 /3,645156 / 995869 / 2,65049 / 40349 / 403-11 / 14311 / 143-413 / 2,96523 / 672390 / 2,293
      Studies74333-11-422
      Rhinitis27.3%#1.2%38.9%#0.1%0.0%0.006%7.3%7.3%-4.0%4.5%4.0%
      95%CI12.6; 49.60.0; 9.036.5; 41.30.002; 34.60.0; 1.00.003; 10.73.7; 14.03.7; 14.0-1.7; 9.30.1; 26.11.6; 9.8
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      31%99%15%99%N/AN/A94%94%-94%N/A95%
      Event/Total672 / 1,89243 / 274629 / 1,61811 / 3100 / 13111 / 179280 / 5,580280 / 5,580-65 / 2,7671 / 2264 / 2,745
      Studies82621122-615
      Sore Throat26.7%5.6%45.8%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      1.0%#1.5%0.6%15.2%4.2%#67.0%4.9%4.5%7.3%
      95%CI12.1; 49.10.1; 29.638.1; 53.70.3; 3.00.4; 5.90.01; 3.92.4; 56.43.7; 4.763.0; 70.82.7; 8.71.9; 10.22.0; 23.0
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      98%98%96%0%N/AN/A99%36%N/A98%9797%
      Event/Total1,975 /4,26971 / 8121,904/ 3,4573 / 3102 / 1311 / 179609 / 6,138235 / 5,580374 / 558692 / 5,523103/ 3,196589 / 3,196
      Studies936211321936
      Cough60.2%65.2%56.0%18.6%26.5%13.9%18.9%13.8%40.7%8.6%10.4%6.7%
      95%CI53.3; 66.854.2; 74.348.2; 63.510.6; 30.714.4; 43.86.2; 28.310.1; 32.68.3; 22.011.9; 77.85.3; 13.75.7; 18.33.0; 14.3
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      95%92%97%96%92%97%99%98%99%98.6%97%97%
      Event/Total3,438 /5,697838 / 1,3752,600 /4,322334/ 1,829153 / 553181/ 1,276812 / 7,293401 / 6,575411 / 7181,061 /8,219374 / 4,904687 / 3,315
      Studies15789454528157
      Anosmia45.7%34.4%51.9%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      16.5%11.1%#19.9%17.3%11.8%37.6%11.0%8.1%15.5%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      595%CI38.3; 53.224.9; 45.345.7; 58.19.9; 26.38.2; 15.010.3; 34.88.3; 32.17.4; 18.18.3; 80.28.0; 15.05.0; 12.912.5; 19.0
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      95.6%89%95%95%26%96%99%97%99%95%96%77%
      Event/Total1,927 /4,317197 / 5861,730 /3,731198 / 1,09937 / 333161 / 766840 / 7,191428 / 6,475412 / 716841 / 9.357302 / 6,042460 / 3,315
      Studies11476247521697
      Ageusia46.0%34.0%51.8%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      15.7%11.4%#18.3%9.0%8.939.6%10.0%7.6%13.2%
      95%CI37.3; 54.923.1; 46.943.7; 59.09.2; 25.68.4; 15.38.8; 34.16.3; 12.75.8; 13.45.9; 15.36.6; 15.13.8; 14.610.0; 17.1
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      95%91%96%96%32%97%94%95%N/A95%96%77%
      Event/Total2,031 /4,442161 / 4761,870 /3,966230 / 1,42838 / 333192 / 1,095377 / 6,354362 / 6,19815 / 156561 / 7,655176 / 4,697342 / 2,958
      Studies9366245411165
      Joint Pain30.0%32.0%28.7%6.9%6.8%7.3%19.0%22.9%10.4%10.3%9.4%11.2%
      95%CI20.1; 42.119.0; 48.717.0; 45.82.0; 21.12.7; 16.20.7; 46.810.7; 31.512.8; 37.46.5; 16.37.1; 14.75.0; 16.77.2; 17.1
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      95%94%95%96%85%97%81.9%91%N/A97%94%94%
      Event/Total1,348 /3,716145 / 4361,203 /3,280132 / 99640 / 42292 / 544168 / 714152 / 56016 / 154803 / 6,42080 / 3,382549 / 3,038
      Studies835633431945
      Diarrhoea23.9%14.1%36.0%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      4.1%4.2%3.3%#8.5%5.3%18.2%3.1%2.2%3.9%
      95%CI16.2; 33.86.1; 29.332.2; 40.01.7; 9.70.9; 17.51.9; 5.62.7; 23.72.5; 10.82.4; 67.01.9; 4.91.1; 4.32.3; 6.7
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      94%87%77%81%78%0%98%80%98%94%90%87%
      Event/Total1,669 /5,106223 / 1,3751,446 /3,73149 / 94536 / 55313 / 392331 / 1,26738 / 550293 / 717404 / 8,4591551 / 5,143249 / 3,316
      Studies147764253211447
      Vomiting7.5%2.7%#12.2%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      0.9%0.0%2.8%---0.8%0.3%1.3%#
      95%CI3.7; 14.50.1; 8.58.2; 17.80.05; 14.00.0; 1.00.3; 21.4---0.3; 2.20.01; 0.60.7; 2.3
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      958%64%95%77%N/A89%---83%N/A61%
      Event/Total361 / 3,68623 / 669338 / 3,01724 / 5290 / 13124 / 398---40 / 5,4487 / 2,60933 / 2,839
      Studies624312---514
      Nausea15.5%4.3%24.2%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      3.8%0.8%5.4%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      3.1%-3.1%4.9%-4.9%
      95%CI8.6; 26.21.1; 15.318.4; 31.01.5; 9.00.1; 5.22.8; 10.71.3; 7.3-1.3; 7.32.4; 9.5-2.4; 9.5
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      96%91%94%81%N/A82%N/A-N/A86%-86%
      Event/Total1,199 /4,51040 / 7791,159 /3,73139 / 7431 / 13138 / 6125 / 160-5 / 160280 / 2,769-280 / 2,769
      Studies10374131-15-5
      Skin Rashes5.7%-5.7%4.6%14.0%2.5%#6.7%9.4%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      2.5%2.7%3.0%2.4%
      95%CI4.1; 7.9-4.1; 7.91.6; 12.69.3; 20.50.1; 4.63.4; 12.76.9; 12.60.9; 6.71.8; 4.01.8; 5.11.3; 4.3
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      78%-78%91%N/A0%75%8%N/A76%83%76%
      Event/Total205 / 3,376-205 / 3,37631 / 54521 / 15010 / 39542 / 56938 / 4074 / 162179 / 7,303117 / 4,53262 / 2,771
      Studies6-6312221945
      Palpitations15.2%7.2%28.4%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      3.5%0.9%4.6%3.0%2.1%4.9%10.0%9.1%11.1%
      95%CI3.7; 45.80.1; 42.97.5; 65.91.7; 7.20.02; 33.32.9; 7.10.6; 13.80.1; 22.92.5; 9.66.4; 15.35.6; 14.55.1; 22.6
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      99%95%N/A90%99%0%85%91%N/A99%93%96%
      Event/Total1,320 /2,961141 / 6691,179 /2,29227 / 6759 / 28118 / 39423 / 57915 / 4178 / 1621,164 8,221459 / 5,711705 / 2,510
      Studies422422221954
      Confusion13.2%#9.6%14.3%8.0%#9.3%7.0%6.8%-6.8%8.7%9.1%8.0%
      95%CI11.3; 15.45.3; 17.012.0; 17.15.7; 11.15.8; 14.44.2; 11.23.8; 11.9-3.8; 11.95.3; 13.85.6; 14.53.4; 17.8
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      52.0%77%0%0%N/AN/A0%-0%99%93%98%
      Event/Total136 / 1,02832 / 303104 / 72532 / 398117 / 18315 / 21511 / 161-11 / 1611,174/ 8,672459 / 5,711715 / 2,961
      Studies4221111-11055
      Vertigo17.7%5.7%31.9%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      2.3%0.0%4.3%6.2%#6.3%6.2%7.9%4.2%12.6%
      Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      95%CI6.3; 40.70.0; 29.018.7; 48.90.6; 8.20.0; 1.02.7; 6.84.0; 9.63.3; 11.63.4; 11.23.8; 15.82.3; 7.55.9; 25.1
      I
      • Guan W.J.
      • Ni Z.Y.
      • Hu Y.
      • Liang W.H.
      • Ou C.Q.
      • He J.X.
      • et al.
      Clinical characteristics of coronavirus disease.
      98%92%98%0%N/A0%0%N/AN/A99%89%95%
      Event/Total1,250 /2,91827 / 2741,223 /2,64417 / 5240 / 13117 / 39319 / 3049 / 14310 / 161709 / 4,616115 / 2,203594 / 2,413
      Studies523312211523
      T: Total sample, H: Hospitalized COVID-19 patients; NH: Non-hospitalized COVID-19 patients; CI: Confidence interval
      low asterisk Statistically significant differences between hospitalized and non-hospitalized patients; # No heterogeneity between studies (I2<75%)
      Supplementary Table S1: Studies investigating each post-COVID-19 symptom at onset and at different follow-up periods.
      SymptomOnsetFollow-up Period
      3060>90
      FeverCarvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      Jacobs et al. 2020
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      Wang et al. 2020
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      Tenforde et al. 2020
      • Tenforde M.W.
      • Kim S.S.
      • Lindsell C.J.
      • et al.
      Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network- united states.
      Goertz et al. 2020
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      Stavem et al. 2020
      • Stavem K.
      • Ghanima W.
      • Olsen M.K.
      • Gilboe H.M.
      • Einvik G.
      Persistent symptoms 1.5–6 months after COVID-19 in non-hospitalised subjects: a population-based cohort study.
      Petersen et al. 2020
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Logue et al. 2021
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      Jacobson et al. 2021
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      ---
      DyspneaCarvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      Garrigues et al. 2020
      • Garrigues E.
      • Janvier P.
      • Kherabi Y.
      • et al.
      Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19.
      Carfi et al 2020
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      Mandal et al. 2020
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      Jacobs et al. 2020
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      Wang et al. 2020
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      Halpin et al. 2021
      • Halpin S.J.
      • McIvor C.
      • Whyatt G.
      • et al.
      Postdischarge symptoms and rehabilitation needs in survivors of COVID-19 infection: a cross-sectional evaluation.
      Xiong et al. 2021
      • Xiong Q.
      • Xu M.
      • Li J.
      • et al.
      Clinical sequelae of COVID-19 survivors in Wuhan, China: a single-centre longitudinal study.
      Tenforde et al. 2020
      • Tenforde M.W.
      • Kim S.S.
      • Lindsell C.J.
      • et al.
      Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network- united states.
      Goertz et al. 2020
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      Stavem et al. 2020
      • Stavem K.
      • Ghanima W.
      • Olsen M.K.
      • Gilboe H.M.
      • Einvik G.
      Persistent symptoms 1.5–6 months after COVID-19 in non-hospitalised subjects: a population-based cohort study.
      Petersen et al. 2020
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Logue et al. 2021
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      Jacobson et al. 2021
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      Carvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      Jacobs et al. 2020
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      Wang et al. 2020
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      Nehme et al. 2020
      • Nehme M.
      • Braillard O.
      • Alcoba G.
      • et al.
      COVID-19 symptoms: longitudinal evolution and persistence in outpatient settings.
      Galván-Tejada et al. 2020
      • Galván-Tejada C.E.
      • Herrera-García C.F.
      • Godina-González S.
      • et al.
      Persistence of COVID-19 symptoms after recovery in mexican population.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Iqbal et al 2021
      • Iqbal A.
      • Iqbal K.
      • Ali S.A.
      • et al.
      The COVID-19 sequelae: a cross-sectional evaluation of post-recovery symptoms and the need for rehabilitation of COVID-19 survivors.
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      Carvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      Carfi et al 2020
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      Mandal et al. 2020
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      Halpin et al. 2021
      • Halpin S.J.
      • McIvor C.
      • Whyatt G.
      • et al.
      Postdischarge symptoms and rehabilitation needs in survivors of COVID-19 infection: a cross-sectional evaluation.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Sudre et al. 2021
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of long COVID.
      Kamal et al. 2020
      • Kamal M.
      • Abo Omirah M.
      • Hussein A.
      • Saeed H
      Assessment and characterisation of post-COVID-19 manifestations.
      Chopra et al. 2021
      • Chopra V.
      • Flanders S.A.
      • O'Malley M.
      • Malani A.N.
      • Prescott H.C
      Sixty-day outcomes among patients hospitalized with COVID-19.
      Moreno-Pérez et al. 2021
      • Moreno-Pérez O.
      • Merino E.
      • Leon-Ramirez J.M.
      • et al.
      Post-acute COVID-19 syndrome. incidence and risk factors: a mediterranean cohort study.
      Carvalho et al. 2020
      • Carvalho-Schneider C.
      • Laurent E.
      • Lemaignen A.
      • Beaufils E.
      • Bourbao-Tournois C.
      • Laribi S.
      • et al.
      Follow-up of adults with noncritical COVID-19 two months after symptom onset.
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      Goertz et al. 2020
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      Stavem et al. 2020
      • Stavem K.
      • Ghanima W.
      • Olsen M.K.
      • Gilboe H.M.
      • Einvik G.
      Persistent symptoms 1.5–6 months after COVID-19 in non-hospitalised subjects: a population-based cohort study.
      Petersen et al. 2020
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Logue et al. 2021
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      Jacobson et al. 2021
      • Jacobson K.B.
      • Rao M.
      • Bonilla H.
      • et al.
      Patients with uncomplicated COVID-19 have long-term persistent symptoms and functional impairment similar to patients with severe COVID-19: a cautionary tale during a global pandemic.
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      Sykes et al. 2021
      • Sykes D.L.
      • Holdsworth L.
      • Jawad N.
      • Gunasekera P.
      • Morice A.H.
      • Crooks M.G.
      Post-COVID-19 symptom burden: what is long-COVID and how should we manage it?.
      Venturelli et al. 2021
      • Venturelli S.
      • Benatti S.V.
      • Casati M.
      • et al.
      Surviving COVID-19 in Bergamo province: a post-acute outpatient re-evaluation.
      Suárez-Robles et al. 2020
      • Suárez-Robles M.
      • del Rosario Iguaran-Bermúdez M.
      • García-Klepizg J.L.
      • Lorenzo-Villalba N.
      • Méndez-Bailón M.
      Ninety days post-hospitalization evaluation of residual COVID-19 symptoms through a phone call check list.
      COMEBAC Study Group et al. 2021
      • L Morin
      • Savale L.
      • et al.
      Writing Committee for the COMEBAC Study Group
      Four-month clinical status of a cohort of patients after hospitalization for COVID-19.
      FatigueCarfi et al 2020
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      Jacobs et al. 2020
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      Wang et al. 2020
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      Xiong et al. 2021
      • Xiong Q.
      • Xu M.
      • Li J.
      • et al.
      Clinical sequelae of COVID-19 survivors in Wuhan, China: a single-centre longitudinal study.
      Nehme et al. 2020
      • Nehme M.
      • Braillard O.
      • Alcoba G.
      • et al.
      COVID-19 symptoms: longitudinal evolution and persistence in outpatient settings.
      Tenforde et al. 2020
      • Tenforde M.W.
      • Kim S.S.
      • Lindsell C.J.
      • et al.
      Symptom duration and risk factors for delayed return to usual health among outpatients with COVID-19 in a multistate health care systems network- united states.
      Goertz et al. 2020
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      Petersen et al. 2020
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Logue et al. 2021
      • Logue J.K.
      • Franko N.M.
      • McCulloch D.J.
      • et al.
      Sequelae in adults at 6 months after COVID-19 infection.
      Iqbal et al 2021
      • Iqbal A.
      • Iqbal K.
      • Ali S.A.
      • et al.
      The COVID-19 sequelae: a cross-sectional evaluation of post-recovery symptoms and the need for rehabilitation of COVID-19 survivors.
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      Jacobs et al. 2020
      • Jacobs L.G.
      • Gourna Paleoudis E.
      • Lesky-Di Bari D.
      • et al.
      Persistence of symptoms and quality of life at 35 days after hospitalization for COVID-19 infection.
      Wang et al. 2020
      • Wang X.
      • Xu H.
      • Jiang H.
      • et al.
      Clinical features and outcomes of discharged coronavirus disease 2019 patients: a prospective cohort study.
      Nehme et al. 2020
      • Nehme M.
      • Braillard O.
      • Alcoba G.
      • et al.
      COVID-19 symptoms: longitudinal evolution and persistence in outpatient settings.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Peluso et al. 2021

      Peluso M.J., Kelly J.D., Lu S. et al. Rapid implementation of a cohort for the study of post-acute sequelae of SARS-CoV-2 infection/COVID-19. medRxiv. 2021 Mar 12;2021.03.11.21252311.

      Carfi et al 2020
      • Carfì A.
      • Bernabei R.
      • Landi F.
      Persistent symptoms in patients after acute COVID-19.
      Mandal et al. 2020
      • Mandal S.
      • Barnett J.
      • Brill S.E.
      • et al.
      Long-COVID’: a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19.
      Townsend et al. 2020
      • Townsend L.
      • Dyer A.H.
      • Jones K.
      • et al.
      Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection.
      Halpin et al. 2021
      • Halpin S.J.
      • McIvor C.
      • Whyatt G.
      • et al.
      Postdischarge symptoms and rehabilitation needs in survivors of COVID-19 infection: a cross-sectional evaluation.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Sudre et al. 2021
      • Sudre C.H.
      • Murray B.
      • Varsavsky T.
      • et al.
      Attributes and predictors of long COVID.
      Kamal et al. 2020
      • Kamal M.
      • Abo Omirah M.
      • Hussein A.
      • Saeed H
      Assessment and characterisation of post-COVID-19 manifestations.
      Moreno-Pérez et al. 2021
      • Moreno-Pérez O.
      • Merino E.
      • Leon-Ramirez J.M.
      • et al.
      Post-acute COVID-19 syndrome. incidence and risk factors: a mediterranean cohort study.
      Zhou et al. 2021
      • Zhou M.
      • Cai J.
      • Sun W.
      • et al.
      Does Post-COVID-19 symptoms exist? A longitudinal study of COVID-19 sequelae in Wenzhou, China.
      Arnold et al. 2020
      • Arnold D.T.
      • Hamilton F.W.
      • Milne A.
      • et al.
      Patient outcomes after hospitalisation with COVID-19 and implications for follow-up: results from a prospective UK cohort.
      Garrigues et al. 2020
      • Garrigues E.
      • Janvier P.
      • Kherabi Y.
      • et al.
      Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19.
      Xiong et al. 2021
      • Xiong Q.
      • Xu M.
      • Li J.
      • et al.
      Clinical sequelae of COVID-19 survivors in Wuhan, China: a single-centre longitudinal study.
      Huang et al. 2021
      • Huang C.
      • Huang L.
      • Wang Y.
      • et al.
      6-month consequences of COVID-19 in patients discharged from hospital: a cohort study.
      Goertz et al. 2020
      • Goërtz Y.M.J.
      • Van Herck M.
      • Delbressine J.M.
      • et al.
      Persistent symptoms 3 months after a SARS-CoV-2 infection: the post-COVID-19 syndrome?.
      Petersen et al. 2020
      • Petersen M.S.
      • Kristiansen M.F.
      • Hanusson K.D.
      • et al.
      Long COVID in the Faroe Islands - a longitudinal study among non-hospitalized patients.
      Cirulli et al. 2020
      • Cirulli E.T.
      • Barrett K.M.S.
      • Riffle S.
      • et al.
      Long-term COVID-19 symptoms in a large unselected population.
      Logue et al. 2021
      • Logue J.K.
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