Advertisement
Original Research| Volume 139, P43-50, November 2020

Mortality in patients with cancer and coronavirus disease 2019: A systematic review and pooled analysis of 52 studies

Published:September 02, 2020DOI:https://doi.org/10.1016/j.ejca.2020.08.011
Mortality in patients with cancer and coronavirus disease 2019: A systematic review and pooled analysis of 52 studies
Previous ArticlePhase I trials and therapeutic intent in the age of precision oncology: What is a patient's chance of response?
Next ArticleImmunological features of coronavirus disease 2019 in patients with cancer

      Highlights

      • •
        Patients with both cancer and coronavirus disease 2019 (COVID-19) have a higher mortality than reported in the overall COVID-19-positive population.
      • •
        We aim to provide precise mortality estimates among patients with cancer and COVID-19.
      • •
        Pooled case mortality rate was 25.6% (95% CI: 22.0%–29.5%; I2 = 48.9%).
      • •
        Aggressive measures must be taken to reduce risk of infection in patients with cancer.

      Abstract

      Background

      Patients with coronavirus disease 2019 (COVID-19) who have underlying malignancy have a higher mortality rate compared with those without cancer, although the magnitude of such excess risk is not clearly defined. We performed a systematic review and pooled analysis to provide precise estimates of the mortality rate among patients with both cancer and COVID-19.

      Methods

      A systematic literature search involving peer-reviewed publications, preprints and conference proceedings up to July 16, 2020, was performed. The primary end-point was the case fatality rate (CFR), defined as the rate of death among patients with cancer and COVID-19. The CFR was assessed with a random effects model, which was used to derive a pooled CFR and its 95% confidence interval (CI).

      Results

      Fifty-two studies, involving a total of 18,650 patients with both COVID-19 and cancer, were selected for the pooled analysis. A total of 4243 deaths were recorded in this population. The probability of death was 25.6% (95% CI: 22.0%–29.5%; I2 = 48.9%) in this patient population.

      Conclusions

      Patients with cancer who develop COVID-19 have high probability of mortality. Appropriate and aggressive preventive measures must be taken to reduce the risk of COVID-19 in patients with cancer and to optimally manage those who do contract the infection.

      Keywords

      Abbreviations:

      AACR (American Association of Cancer Research), ASCO (American Society of Clinical Oncology), COVID-19 (coronavirus disease 2019), CCC-19 (COVID-19 and Cancer Consortium), ESMO (European Society for Medical Oncology), SARS-CoV-2 (severe acute respiratory syndrome coronavirus 2), TERAVOLT (Thoracic cancERs international coVid 19 cOLlaboraTion)

      1. Introduction

      The coronavirus disease 2019 (COVID-19) pandemic, caused by the beta-coronavirus severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), has spread globally and resulted in more than 635,000 deaths as of July 24, 2020 [

      COVID-19 dashboard. https://coronavirus.jhu.edu/map.html. [Accessed 24 July 2020].

      ]. Among patients with COVID-19, those with cancer have worse outcomes compared with those without underlying malignancy, but mortality rates differ significantly among studies, ranging from 3.7% to 61.5% [
      • Kalinsky K.
      • Accordino M.K.
      • Hosi K.
      • et al.
      Characteristics and outcomes of patients with breast cancer diagnosed with SARS-Cov-2 infection at an academic center in New York City.
      Breast Cancer Res Treat. 2020; 182: 239-242https://doi.org/10.1007/s10549-020-05667-6
      ,
      • He W.
      • Chen L.
      • Chen L.
      • et al.
      COVID-19 in persons with haematological cancers.
      Leukemia. 2020; 34: 1637-1645https://doi.org/10.1038/s41375-020-0836-7
      ].
      Even larger studies have significantly different mortality rates – for example, a prospective observational cohort study from the UK reported a mortality rate of 35.4% (617 deaths among 1743 patients with COVID-19 and cancer) [
      • Docherty A.B.
      • Harrison E.M.
      • Green C.A.
      • et al.
      Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study.
      BMJ. 2020; 369 (Published 2020 May 22): m1985https://doi.org/10.1136/bmj.m1985
      ], while the most recent update from the COVID-19 and Cancer Consortium (CCC-19) showed a death rate of 15.8% (433 deaths in a cohort of 2749 patients with both diseases) [

      Peters, S. Keynote address. Flexibility to sustain solidity: addressing new vulnerabilities in cancer at the time of COVID-19. AACR virtual meeting: COVID-19 and cancer. https://www.aacr.org/meeting/aacr-virtual-meeting-covid-19-and-cancer/program/. [Accessed 23 July 2020].

      ].
      Many of the studies reporting outcomes of patients with both cancer and COVID-19 to date have included relatively small numbers of such patients. Data related to this subpopulation are rapidly increasing but are mostly fragmented. The aim of this systematic review and pooled analysis is to provide a more robust estimate of the mortality rate among SARS-CoV-2–infected patients with underlying cancer.

      2. Methods

      2.1 Literature search

      A systematic literature review of PubMed, Google Scholar, MedRxiv and conference proceedings from the American Association of Cancer Research (AACR), American Society of Clinical Oncology, European Society for Medical Oncology 2020 up to July 16, 2020, was performed by two coauthors (KSS and MT), and disagreement was resolved by consensus with all authors. Multiple combinations of search terms were used: (COVID OR coronavirus OR SARS-CoV-2) AND (cancer OR tumour OR tumour OR malignancy OR malignancies OR neoplasia) AND (mortality OR death). The included study references were cross searched for additional studies. The duplicated reports were removed. The CCC-19 data were updated to reflect the keynote address at the AACR Virtual Meeting: COVID-19 and Cancer by Dr Solange Peters on July 21, 2020.

      2.2 Study selection

      Inclusion criteria were as follows: (i) studies reporting mortality rate in patients with cancer and COVID-19; (ii) any type of study (including retrospective studies, randomised controlled trials, prospective cohort studies and case series); (iii) studies involving adults; (iv) studies published in English, Spanish or French language.
      Exclusion criteria were as follows: (i) studies with less than 10 patients with both cancer and COVID-19; (ii) studies reported in languages other than the aforementioned ones.

      2.3 Data extraction

      Data were independently extracted by two authors (KSS and MT). Extracted data consisted of first author's name, type of publication (i.e. peer reviewed, preprint or conference proceeding), reported number of patients with cancer and COVID-19, the number of deaths among the study population, study time period, institution or country involved and type of cancer.

      2.4 Statistical analysis

      Primary end-point was the case fatality rate (CFR), defined as the rate of death among patients with cancer and COVID-19. The CFR was assessed with a random effects model, which was used to derive a pooled CFR and its 95% confidence interval (CI). Heterogeneity was assessed with the I2 test (substantial heterogeneity whenever I2 ≥ 50%). A sensitivity analysis was performed excluding reports including less than 100 patients.

      3. Results

      After the systematic literature search, 682 references (including 216 preprints) were retrieved, of which 598 were excluded on the basis of their titles and 32 on the basis of their abstract or full text due to various reasons (inclusion of paediatric patients, duplicated results, cohorts with less than 10 patients, studies not reporting number of deaths, studies not involving patients). In total, 52 studies were included in this pooled analysis with a total of 18,650 patients with cancer and reporting 4243 deaths (Table 1).
      Table 1Mortality data from 52 studies on patients with cancer and COVID-19.
      S No.First authorType of studyTotal patients with cancer and COVID-19Deaths in patients with cancer and COVID-19Time periodInstitution or countryType of cancer
      1Burn et al. [
      • Burn E.
      • Tebe C.
      • Fernandez-Bertolin S.
      • et al.
      The natural history of symptomatic COVID-19 in Catalonia, Spain: a multi-state model including 109,367 outpatient diagnoses, 18,019 hospitalisations, and 5,585 COVID-19 deaths among 5,627,520 people.
      medRxiv. 2020; (preprint)https://doi.org/10.1101/2020.07.13.20152454
      ]      		Preprint665613171 Mar to 6 May 2020Catalonia, SpainAny
      2Peters [

      Peters, S. Keynote address. Flexibility to sustain solidity: addressing new vulnerabilities in cancer at the time of COVID-19. AACR virtual meeting: COVID-19 and cancer. https://www.aacr.org/meeting/aacr-virtual-meeting-covid-19-and-cancer/program/. [Accessed 23 July 2020].

      ]      		Conference proceedings274943317 Mar to 26 June 2020COVID-19 and Cancer Consortium (CCC-19), USA, Canada, SpainAny
      3Docherty et al. [
      • Docherty A.B.
      • Harrison E.M.
      • Green C.A.
      • et al.
      Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study.
      BMJ. 2020; 369 (Published 2020 May 22): m1985https://doi.org/10.1136/bmj.m1985
      ]      		Peer reviewed17436176 Feb to 19 Apr 2020UKAny
      4Fratino et al. [
      • Fratino L.
      • Procopio G.
      • Di Maio M.
      • Cinieri S.
      • Leo S.
      • Beretta G.
      Coronavirus: older persons with cancer in Italy in the COVID-19 pandemic.
      Front Oncol. 2020; 10 (Published 2020 Apr 30): 648https://doi.org/10.3389/fonc.2020.00648
      ]      		Peer reviewed909150Upto 30 Mar 2020ItalyAny
      5Lee et al. [
      • Lee L.Y.W.
      • Cazier J.B.
      • Starkey T.
      • et al.
      COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study.
      Lancet. 2020; 395: 1919-1926https://doi.org/10.1016/S0140-6736(20)31173-9
      ]      		Peer reviewed80022618 Mar to 26 Apr 2020UK Coronavirus Cancer Monitoring Project (UKCCMP)Any
      6Montopoli et al. [
      • Montopoli M.
      • Zumerle S.
      • Vettor R.
      • et al.
      Androgen-deprivation therapies for prostate cancer and risk of infection by SARS-CoV-2: a population-based study (N = 4532).
      Ann Oncol. 2020; ([published online ahead of print, 2020 May 6]) (S0923-7534(20)39797-0)https://doi.org/10.1016/j.annonc.2020.04.479
      ]      		Peer reviewed43075Upto 1 Apr 202068 hospitals, Veneto, ItalyAny (but population restricted to men only)
      7Robilotti et al. [
      • Robilotti E.V.
      • Babady N.E.
      • Mead P.A.
      • et al.
      Determinants of COVID-19 disease severity in patients with cancer.
      Nat Med. 2020; ([published online ahead of print, 2020 Jun 24])https://doi.org/10.1038/s41591-020-0979-0
      ]      		Peer reviewed4235110 Mar to 7 Apr 2020New York, USAAny
      8Horn et al. [
      • Horn L.
      • Whisenant J.G.
      • Torri V.
      • et al.
      Thoracic Cancers International COVID-19 Collaboration (TERAVOLT): impact of type of cancer therapy and COVID therapy on survival.
      J Clin Oncol. 2020; 38 (LBA111-LBA111)
      ]      		Conference proceedings40014126 Mar to 12 Apr 2020TERAVOLT Registry (8 countries)Thoracic cancers only
      9Miyashita et al. [
      • Miyashita H.
      • Mikami T.
      • Chopra N.
      • et al.
      Do patients with cancer have a poorer prognosis of COVID-19? An experience in New York City.
      Ann Oncol. 2020; ([published online ahead of print, 2020 Apr 21]) (S0923-7534(20)39303-0)https://doi.org/10.1016/j.annonc.2020.04.006
      ]      		Peer reviewed334371 Mar to 6 Apr 2020Mt Sinai Health System, New York, USAAny
      10Graselli et al. [
      • Grasselli G.
      • Greco M.
      • Zanella A.
      • et al.
      Risk factors associated with mortality among patients with COVID-19 in intensive care units in Lombardy, Italy.
      JAMA Intern Med. 2020; ([published online ahead of print, 2020 Jul 15])https://doi.org/10.1001/jamainternmed.2020.3539
      ]      		Peer reviewed331202Upto 22 Apr 2020Lombardy, ItalyAny
      11Wang et al. [
      • Wang J.
      • Song Q.
      • Chen Y.
      • et al.
      Systematic investigations of COVID-19 in 283 cancer patients.
      medRxiv. 2020; https://doi.org/10.1101/2020.04.28.20083246
      ]      		Preprint2835017 Dec 2019 to 18 Mar 2020Hubei, ChinaAny
      12COVIDSurg Collaborative [
      COVIDSurg Collaborative
      Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study.
      Lancet. 2020; 396 ([published correction appears in Lancet. 2020 Jun 9]): 27-38https://doi.org/10.1016/S0140-6736(20)31182-X
      ]      		Peer reviewed239661 Jan to 31 Mar 202024 countriesAny (COVID-19 was diagnosed based on lab, clinical or radiological features)
      13Tian et al. [
      • Tian J.
      • Yuan X.
      • Xiao J.
      • et al.
      Clinical characteristics and risk factors associated with COVID-19 disease severity in patients with cancer in Wuhan, China: a multicentre, retrospective, cohort study.
      Lancet Oncol. 2020; 21: 893-903https://doi.org/10.1016/S1470-2045(20)30309-0
      ]      		Peer reviewed2324613 Jan to 18 Mar 20209 hospitals in Wuhan, ChinaAny
      14Mehta et al. [
      • Mehta V.
      • Goel S.
      • Kabarriti R.
      • et al.
      Case fatality rate of cancer patients with COVID-19 in a New York hospital system.
      Cancer Discov. 2020; ([published online ahead of print, 2020 May 1])https://doi.org/10.1158/2159-8290.CD-20-0516
      ]      		Peer reviewed2186118 Mar to 8 Apr 2020New York, USAAny
      15Yang et al. [
      • Yang K.
      • Sheng Y.
      • Huang C.
      • et al.
      Clinical characteristics, outcomes, and risk factors for mortality in patients with cancer and COVID-19 in Hubei, China: a multicentre, retrospective, cohort study.
      Lancet Oncol. 2020; ([published online ahead of print, 2020 May 29]) (S1470-2045(20)30310-30317)https://doi.org/10.1016/S1470-2045(20)30310-7
      ]      		Peer reviewed2053013 Jan to 18 Mar 20209 hospitals from Hubei, ChinaAny
      16Pinato et al. [
      • Pinato D.J.
      • Lee A.J.X.
      • Biello F.
      • et al.
      Presenting features and early mortality from SARS-CoV-2 infection in cancer patients during the initial stage of the COVID-19 pandemic in Europe.
      Cancers (Basel). 2020; 12 (Published 2020 Jul 8): E1841https://doi.org/10.3390/cancers12071841
      ]      		Peer reviewed20459Upto 6 Mar 20208 hospitals in the UK, Italy and SpainAny
      17Scarfò et al. [
      • Scarfò L.
      • Chatzikonstantinou T.
      • Rigolin G.M.
      • et al.
      COVID-19 severity and mortality in patients with chronic lymphocytic leukemia: a joint study by ERIC, the European Research Initiative on CLL, and CLL Campus.
      Leukemia. 2020; ([published online ahead of print, 2020 Jul 9])https://doi.org/10.1038/s41375-020-0959-x
      ]      		Peer reviewed1905528 Mar to 22 May 2020EuropeChronic lymphocytic leukaemia only
      18de Melo et al. [

      de Melo AC, Thuler LCS, da Silva JL, et al. Cancer inpatient with COVID-19: a report from the Brazilian National Cancer Institute. https://www.medrxiv.org/content/10.1101/2020.06.27.20141499v2. [Accessed 23 July, 2020].

      ]      		Preprint1816030 Apr to 26 May 2020Brazilian National Cancer InstituteAny
      19Martinez-Lopez et al. [
      • Martinez-Lopez J.
      • Mateos M.V.
      • Encinas C.
      • et al.
      Multiple myeloma and SARS-CoV-2 infection: clinical characteristics and prognostic factors of inpatient mortality.
      medRxiv. 2020; https://doi.org/10.1101/2020.06.29.20142455
      ]      		Preprint167561 Mar to 30 Apr 202073 hospitals in SpainMultiple myeloma only
      20Russel et al. [
      • Russell B.
      • Moss C.
      • Papa S.
      • et al.
      Factors affecting COVID-19 outcomes in cancer patients − a first report from Guys Cancer Centre in London.
      medRxiv. 2020; (Preprint)https://doi.org/10.1101/2020.05.12.20094219
      ]      		Preprint1563429 Feb to 12 May 2020Guys Hospital, London, UKAny
      21Basse et al. [
      • Basse C.
      • Diakite S.
      • Servois V.
      • et al.
      Characteristics and outcome of SARS-CoV-2 infection in cancer patients.
      medRxiv. 2020; https://doi.org/10.1101/2020.05.14.20101576
      ]      		Preprint1412613 Mar to 25 Apr 2020Institute Curie Hospital, Paris, FranceAny
      22Barlesi et al. [
      • Barlesi F.
      • Foulon S.
      • Bayle A.
      • et al.
      Abstract CT403 - outcome of cancer patients infected with COVID-19, including toxicity of cancer treatments.
      in: AACR virtual meeting. 2020
      https://www.abstractsonline.com/pp8/#!/9045/presentation/10935
      Date accessed: July 23, 2020
      ]      		Conference proceedings1372014 Mar to 15 Apr 2020Gustave Roussy Cancer Campus, Villejuif, FranceAny
      23Angelis et al. [
      • Angelis V.
      • Tippu Z.
      • Joshi K.
      • et al.
      Defining the true impact of coronavirus disease 2019 in the at-risk population of patients with cancer.
      Eur J Cancer. 2020; 136 ([published online ahead of print, 2020 Jul 7]): 99-106https://doi.org/10.1016/j.ejca.2020.06.027
      ]      		Peer reviewed113291 Mar to 30 Apr 2020Royal Marsden, London, UKAny
      24Gupta et al. [
      • Gupta S.
      • Hayek S.S.
      • Wang W.
      • et al.
      Factors associated with death in critically ill patients with coronavirus disease 2019 in the US.
      JAMA Intern Med. 2020; ([published online ahead of print, 2020 Jul 15])https://doi.org/10.1001/jamainternmed.2020.3596
      ]      		Peer reviewed112604 Mar to 4 Apr 202065 hospitals, USAAny
      25Zhang et al. [
      • Zhang H.
      • Wang L.
      • Chen Y.
      • et al.
      Outcomes of novel coronavirus disease 2019 (COVID-19) infection in 107 patients with cancer from Wuhan, China.
      Cancer. 2020; ([published online ahead of print, 2020 Jun 23])https://doi.org/10.1002/cncr.33042
      ]      		Peer reviewed107235 Jan to 18 Mar 20205 hospitals from Wuhan, ChinaAny
      26Deng et al. [
      • Deng G.
      • Yin M.
      • Chen X.
      • Zeng F.
      Clinical determinants for fatality of 44,672 patients with COVID-19.
      Crit Care. 2020; 24 (Published 2020 Apr 28): 179https://doi.org/10.1186/s13054-020-02902-w
      ]      		Peer reviewed1076Upto 11 Feb 2020ChinaAny
      27Dai et al. [
      • Dai M.
      • Liu D.
      • Liu M.
      • et al.
      Patients with cancer Appear more vulnerable to SARS-CoV-2: a multicenter study during the COVID-19 outbreak.
      Cancer Discov. 2020; 10: 783-791https://doi.org/10.1158/2159-8290.CD-20-0422
      ]      		Peer reviewed105121 Jan to 24 Feb 202014 hospitals from Hubei, ChinaAny
      28Luo et al. [
      • Luo J.
      • Rizvi H.
      • Preeshagul I.R.
      • et al.
      COVID-19 in patients with lung cancer.
      Ann Oncol. 2020; ([published online ahead of print, 2020 Jun 16]) (S0923-7534(20)39894-X)https://doi.org/10.1016/j.annonc.2020.06.007
      ]      		Peer reviewed1022512 Mar to 6 May 2020New York, USALung cancer only
      29Hultcrantz et al. [
      • Hultcrantze M.
      • Richter J.
      • Rosenbaum C.A.
      • et al.
      COVID-19 infections and outcomes in patients with multiple myeloma in New York City: a cohort study from five academic centers.
      Blood Cancer Discov. July 30 2020; https://doi.org/10.1158/2643-3230.BCD-20-0102
      ]      		Preprint1001810 Mar to 30 Apr 2020New York, USAMultiple myeloma only
      30Cook et al. [
      • Cook G.
      • John Ashcroft A.
      • Pratt G.
      • et al.
      Real-world assessment of the clinical impact of symptomatic infection with severe acute respiratory syndrome coronavirus (COVID-19 disease) in patients with multiple myeloma receiving systemic anti-cancer therapy.
      Br J Haematol. 2020; ([published online ahead of print, 2020 May 21])https://doi.org/10.1111/bjh.16874
      ]      		Peer reviewed7541Upto 18 May 2020UKMultiple myeloma only
      31Booth et al. [
      • Booth S.
      • Willan J.
      • Wong H.
      • et al.
      Regional outcomes of severe acute respiratory syndrome coronavirus 2 infection in hospitalised patients with haematological malignancy.
      Eur J Haematol. 2020; ([published online ahead of print, 2020 Jun 16])https://doi.org/10.1111/ejh.13469
      ]      		Peer reviewed66341 Mar to 6 May 2020England, UKHaematological malignancies only
      32Yarza et al. [
      • Yarza R.
      • Bover M.
      • Paredes D.
      • et al.
      SARS-CoV-2 infection in cancer patients undergoing active treatment: analysis of clinical features and predictive factors for severe respiratory failure and death.
      Eur J Cancer. 2020; ([published online ahead of print, 2020 Jun 6]) (S0959-8049(20)30313-0)https://doi.org/10.1016/j.ejca.2020.06.001
      ]      		Peer reviewed63169 Mar to 19 Apr 2020Hospital Universitario 12 de Octubre, Madrid, SpainAny
      33Assaad et al. [
      • Assaad S.
      • Avrillon V.
      • Fournier M.L.
      • et al.
      High mortality rate in cancer patients with symptoms of COVID-19 with or without detectable SARS-COV-2 on RT-PCR.
      Eur J Cancer. 2020; ([published online ahead of print, 2020 Jun 7]) (S0959-8049(20)30314-2)https://doi.org/10.1016/j.ejca.2020.05.028
      ]      		Peer reviewed5581 Mar to 25 Apr 2020Centre Léon Bérard, Paris, FranceAny
      34Wang et al. [
      • Wang B.
      • Van Oekelen O.
      • Mouhieddine T.H.
      • et al.
      A tertiary center experience of multiple myeloma patients with COVID-19: lessons learned and the path forward.
      J Hematol Oncol. 2020; 13 (Published 2020 Jul 14): 94https://doi.org/10.1186/s13045-020-00934-x
      ]      		Peer reviewed58141 Mar to 30 Apr 2020New York, USAMultiple myeloma only
      35Gonzalez-Cao et al. [
      • Gonzalez-Cao M.
      • Antonazas-Basa M.
      • Puertolas T.
      • et al.
      Cancer immunotherapy does not increase the risk of death by COVID-19 in melanoma patients.
      medRxiv. 2020; https://doi.org/10.1101/2020.05.19.20106971
      ]      		Preprint50131 Apr to 17 May 2020SpainMelanoma only
      36Suleyman et al. [
      • Suleyman G.
      • Fadel R.A.
      • Malette K.M.
      • et al.
      Clinical characteristics and morbidity associated with coronavirus disease 2019 in a series of patients in metropolitan detroit.
      JAMA Netw Open. 2020; 3 (Published 2020 Jun 1)e2012270https://doi.org/10.1001/jamanetworkopen.2020.12270
      ]      		Peer reviewed49199 Mar to 27 Mar 2020Henry Ford Health System, Detroit, Michigan, USAAny
      37Rogado et al. [
      • Rogado J.
      • Obispo B.
      • Pangua C.
      • et al.
      Covid-19 transmission, outcome and associated risk factors in cancer patients at the first month of the pandemic in a Spanish hospital in Madrid.
      Clin Transl Oncol. 2020; ([published online ahead of print, 2020 May 25]): 1-5https://doi.org/10.1007/s12094-020-02381-z
      ]      		Peer reviewed45191 Feb to 7 Apr 2020Hospital Universitario Infanta Leonor of Madrid, SpainAny
      38Aries et al. [
      • Aries J.A.
      • Davies J.K.
      • Auer R.L.
      • et al.
      Clinical outcome of coronavirus disease 2019 in haemato-oncology patients.
      Br J Haematol. 2020; ([published online ahead of print, 2020 May 18])https://doi.org/10.1111/bjh.16852
      ]      		Peer reviewed351411 Mar to 11 May 2020Barts Cancer Centre, UKHaematological malignancies only
      39Martín-Moro et al. [
      • Martín-Moro F.
      • Marquet J.
      • Piris M.
      • et al.
      Survival study of hospitalised patients with concurrent COVID-19 and haematological malignancies.
      Br J Haematol. 2020; 190: e16-e20https://doi.org/10.1111/bjh.16801
      ]      		Peer reviewed34119 Mar to 17 Apr 2020Ramón y Cajal University Hospital, Madrid SpainHaematological malignancies only
      40Zhang et al. [
      • Zhang L.
      • Zhu F.
      • Xie L.
      • et al.
      Clinical characteristics of COVID-19-infected cancer patients: a retrospective case study in three hospitals within Wuhan, China.
      Ann Oncol. 2020; 31: 894-901https://doi.org/10.1016/j.annonc.2020.03.296
      ]      		Peer reviewed28813 Jan to 26 Feb 20203 hospitals in Wuhan, ChinaAny
      41Kalinsky et al. [
      • Kalinsky K.
      • Accordino M.K.
      • Hosi K.
      • et al.
      Characteristics and outcomes of patients with breast cancer diagnosed with SARS-Cov-2 infection at an academic center in New York City.
      Breast Cancer Res Treat. 2020; 182: 239-242https://doi.org/10.1007/s10549-020-05667-6
      ]      		Peer reviewed27110 Mar to 29 Apr 2020Columbia University Irving Medical Center, USABreast cancer only
      42Joharatnam-Hogan et al. [
      • Joharatnam-Hogan N.
      • Hochhauser D.
      • Shiu K.K.
      • et al.
      Outcomes of the 2019 Novel Coronavirus in patients with or without a history of cancer - a multi-centre North London experience.
      medRxiv. 2020; https://doi.org/10.1101/2020.04.16.20061127
      ]      		Preprint26612 Mar to 7 Apr 2020London, UKAny
      43Stroppa et al. [
      • Stroppa E.M.
      • Toscani I.
      • Citterio C.
      • et al.
      Coronavirus disease-2019 in cancer patients. A report of the first 25 cancer patients in a western country (Italy).
      Future Oncol. 2020; 16: 1425-1432https://doi.org/10.2217/fon-2020-0369
      ]      		Peer reviewed25921 Feb to 18 Mar 2020Piacenza's general hospital, ItalyAny
      44Ciceri et al. [
      • Ciceri F.
      • Castagna A.
      • Rovere-Querini P.
      • et al.
      Early predictors of clinical outcomes of COVID-19 outbreak in Milan, Italy.
      Clin Immunol. 2020; 217 ([published online ahead of print, 2020 Jun 12]): 108509https://doi.org/10.1016/j.clim.2020.108509
      ]      		Peer reviewed221125 Feb to 24 Mar 2020San Raffaele Hospital, Lombardy, ItalyAny
      45Bogani et al. [
      • Bogani G.
      • Ditto A.
      • Bosio S.
      • Brusadelli C.
      • Raspagliesi F.
      Cancer patients affected by COVID-19: experience from Milan, Lombardy.
      Gynecol Oncol. 2020; ([published online ahead of print, 2020 Jun 10]) (S0090-8258(20)31976-4)https://doi.org/10.1016/j.ygyno.2020.06.161
      ]      		Peer reviewed193Feb and Mar 2020Lombardy, ItalyAny
      46Guan et al. [
      • Guan W.J.
      • Liang W.H.
      • Zhao Y.
      • et al.
      Comorbidity and its impact on 1590 patients with COVID-19 in China: a nationwide analysis.
      Eur Respir J. 2020; 55 (Published 2020 May 14): 2000547https://doi.org/10.1183/13993003.00547-2020
      ]      		Peer reviewed18311 Dec 2019 to 31 Jan 2020Wuhan, ChinaAny
      47Tagliamento et al. [
      • Tagliamento M.
      • Lambertini M.
      • Genova C.
      • et al.
      Call for ensuring cancer care continuity during COVID-19 pandemic.
      ESMO Open. 2020; 5e000783https://doi.org/10.1136/esmoopen-2020-000783
      ]      		Peer reviewed17410 Mar to 6 Apr 2020ItalySolid cancers
      48Wang L et al. [
      • Wang L.
      • He W.
      • Yu X.
      • et al.
      Coronavirus disease 2019 in elderly patients: characteristics and prognostic factors based on 4-week follow-up.
      J Infect. 2020; 80: 639-645https://doi.org/10.1016/j.jinf.2020.03.019
      ]      		Peer reviewed1531 Jan to 6 Feb 2020Wuhan, ChinaAny
      49He et al. [
      • He W.
      • Chen L.
      • Chen L.
      • et al.
      COVID-19 in persons with haematological cancers.
      Leukemia. 2020; 34: 1637-1645https://doi.org/10.1038/s41375-020-0836-7
      ]      		Peer reviewed13823 Jan to 14 Feb 2020Union Hospital and Wuhan Central Hospital, ChinaHaematological malignancies only
      50Lattenist et al. [
      • Lattenist R.
      • Yildiz H.
      • De Greef J.
      • Bailly S.
      • Yombi J.C.
      COVID-19 in adult patients with hematological disease: analysis of clinical characteristics and outcomes.
      Indian J Hematol Blood Transfus. 2020; ([published online ahead of print, 2020 Jul 7]): 1-5https://doi.org/10.1007/s12288-020-01318-4
      ]      		Peer reviewed13613 Mar to 15 May 2020Universite´ catholique de Louvain, Brussels, BelgiumHaematological malignancies only
      51Yu et al. [
      • Yu J.
      • Ouyang W.
      • Chua M.L.K.
      • Xie C.
      SARS-CoV-2 transmission in patients with cancer at a tertiary care hospital in Wuhan, China.
      JAMA Oncol. 2020; 6 ([published online ahead of print, 2020 Mar 25]): 1108-1110https://doi.org/10.1001/jamaoncol.2020.0980
      ]      		Peer reviewed12330 Dec 2019 to 17 Feb 2020Wuhan, ChinaAny
      52Wu et al. [
      • Wu Q.
      • Chu Q.
      • Zhang H.
      • et al.
      Clinical outcomes of coronavirus disease 2019 (COVID-19) in cancer patients with prior exposure to immune checkpoint inhibitors.
      Cancer Commun (Lond). 2020; ([published online ahead of print, 2020 Jul 15])https://doi.org/10.1002/cac2.12077
      ]      		Peer reviewed1149 Jan to 20 Mar 2020Hubei, ChinaAny, with prior exposure to immune checkpoint inhibitors
      COVID-19, coronavirus disease 2019; TERAVOLT, Thoracic cancERs international coVid 19 cOLlaboraTion.
      Pooled case mortality rate among patients with cancer and COVID-19 was 25.6% (95% CI: 22.0%–29.5%; I2 = 48.9%) (Fig. 1). A sensitivity analysis excluding reports with less than 100 patients showed an I2 = 49.7% for studies with ≥100 patients.
      Fig. 1
      Fig. 1Forest plot of 52 studies reporting outcomes in patients with both cancer and COVID-19. COVID-19, coronavirus disease 2019.

      4. Discussion

      The COVID-19 pandemic has had a major impact on patients with cancer [
      • Saini K.S.
      • de Las Heras B.
      • de Castro J.
      • et al.
      Effect of the COVID-19 pandemic on cancer treatment and research.
      Lancet Haematol. 2020; 7: e432-e435https://doi.org/10.1016/S2352-3026(20)30123-X
      ], including a sharp reduction in cancer screening and the postponement of ongoing or planned therapy during the initial months of the pandemic, which could result in excess deaths from cancer in the future [
      • Lai A.G.
      • Pasea L.
      • Banerjee A.
      • et al.
      Estimating excess mortality in people with cancer and multimorbidity in the COVID-19 emergency.
      medRxiv. 2020; (Preprint)https://doi.org/10.1101/2020.05.27.20083287
      ,
      • Sharpless N.E.
      COVID-19 and cancer.
      Science. 2020; 368: 1290https://doi.org/10.1126/science.abd3377
      ].
      To restart standard cancer treatment protocols, it is important to quantify the risk of mortality among patients with both cancer and COVID-19, and data generated by large registries such as CCC-19 and Thoracic cancERs international coVid 19 cOLlaboraTion could be valuable in this regard [
      • Kuderer N.M.
      • Choueiri T.K.
      • Shah D.P.
      • et al.
      Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study.
      Lancet. 2020; 395: 1907-1918https://doi.org/10.1016/S0140-6736(20)31187-9
      ,
      • Garassino M.C.
      • Whisenant J.G.
      • Huang L.C.
      • et al.
      COVID-19 in patients with thoracic malignancies (TERAVOLT): first results of an international, registry-based, cohort study.
      Lancet Oncol. 2020; 21: 914-922https://doi.org/10.1016/S1470-2045(20)30314-4
      ]. Meta-analyses are also a useful tool to aggregate smaller data sets and estimate mortality risks in this vulnerable population.
      The results of our pooled analysis clearly show that the mortality is high among patients with cancer and COVID-19 and should be considered as an independent risk factor, in addition to older age, male sex, black race, current smoker, other comorbidities and so on. As more data become available, it is becoming increasingly clear that within the population of patients with both cancer and COVID-19, there are subsets with greater risk, such as patients with haematological malignancies or lung cancer, which need deeper analysis.

      5. Conclusions

      Patients with cancer who develop COVID-19 have high probability of mortality. Appropriate and aggressive preventive measures must be taken to reduce the risk of infection with SARS-CoV-2 in patients with cancer and to optimally manage those who do contract the infection.

      Author statements

      Conflict of interest statement

      K.S.S. reports receiving consulting fees from the European Commission outside the submitted work. M.T. reports receiving travel grants from Roche, Bristol-Myers Squibb, AstraZeneca and Takeda and receiving honoraria as a medical writer from Novartis and Amgen outside the submitted work. M.L. reports acting as a consultant for Roche and Novartis and receiving speaker honoraria from Roche, Takeda, Lilly, Novartis, Pfizer and Theramex outside the submitted work. G.C. reports receiving personal fees for consulting, advisory role and speakers’ bureau from Roche/Genentech, Novartis, Pfizer, Lilly, Foundation Medicine, Samsung and Daichii-Sankyo; receiving honoraria from Ellipses Pharma; fees for travel and accommodation from Roche/Genentech and Pfizer outside the submitted work. E.d.A. reports receiving honoraria and advisory board fees from Roche/GNE, Novartis and Seattle Genetics; receiving travel grants from Roche/GNE, GSK and Novartis and receiving research grant to institution from Roche/GNE, AstraZeneca, GSK, Novartis and Servier outside the submitted work. The other authors do not report any conflicts of interest.

      Role of funding source

      None.

      Ethical approval and consent to participate

      Not applicable.

      Authors' contributions

      K.S.S. and E.d.A. conceptualised the manuscript; all authors provided significant inputs; K.S.S. and M.T. collected the data, and R.M.N. performed the analysis. All authors wrote, reviewed, edited and approved this final manuscript.

      References

      1. COVID-19 dashboard. https://coronavirus.jhu.edu/map.html. [Accessed 24 July 2020].

        View in Article
        • Kalinsky K.
        • Accordino M.K.
        • Hosi K.
        • et al.
        Characteristics and outcomes of patients with breast cancer diagnosed with SARS-Cov-2 infection at an academic center in New York City.
        Breast Cancer Res Treat. 2020; 182: 239-242https://doi.org/10.1007/s10549-020-05667-6
        View in Article
        • He W.
        • Chen L.
        • Chen L.
        • et al.
        COVID-19 in persons with haematological cancers.
        Leukemia. 2020; 34: 1637-1645https://doi.org/10.1038/s41375-020-0836-7
        View in Article
        • Docherty A.B.
        • Harrison E.M.
        • Green C.A.
        • et al.
        Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study.
        BMJ. 2020; 369 (Published 2020 May 22): m1985https://doi.org/10.1136/bmj.m1985
        View in Article

      5. Peters, S. Keynote address. Flexibility to sustain solidity: addressing new vulnerabilities in cancer at the time of COVID-19. AACR virtual meeting: COVID-19 and cancer. https://www.aacr.org/meeting/aacr-virtual-meeting-covid-19-and-cancer/program/. [Accessed 23 July 2020].

        View in Article
        • Saini K.S.
        • de Las Heras B.
        • de Castro J.
        • et al.
        Effect of the COVID-19 pandemic on cancer treatment and research.
        Lancet Haematol. 2020; 7: e432-e435https://doi.org/10.1016/S2352-3026(20)30123-X
        View in Article
        • Lai A.G.
        • Pasea L.
        • Banerjee A.
        • et al.
        Estimating excess mortality in people with cancer and multimorbidity in the COVID-19 emergency.
        medRxiv. 2020; (Preprint)https://doi.org/10.1101/2020.05.27.20083287
        View in Article
        • Sharpless N.E.
        COVID-19 and cancer.
        Science. 2020; 368: 1290https://doi.org/10.1126/science.abd3377
        View in Article
        • Kuderer N.M.
        • Choueiri T.K.
        • Shah D.P.
        • et al.
        Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study.
        Lancet. 2020; 395: 1907-1918https://doi.org/10.1016/S0140-6736(20)31187-9
        View in Article
        • Garassino M.C.
        • Whisenant J.G.
        • Huang L.C.
        • et al.
        COVID-19 in patients with thoracic malignancies (TERAVOLT): first results of an international, registry-based, cohort study.
        Lancet Oncol. 2020; 21: 914-922https://doi.org/10.1016/S1470-2045(20)30314-4
        View in Article
        • Burn E.
        • Tebe C.
        • Fernandez-Bertolin S.
        • et al.
        The natural history of symptomatic COVID-19 in Catalonia, Spain: a multi-state model including 109,367 outpatient diagnoses, 18,019 hospitalisations, and 5,585 COVID-19 deaths among 5,627,520 people.
        medRxiv. 2020; (preprint)https://doi.org/10.1101/2020.07.13.20152454
        View in Article
        • Fratino L.
        • Procopio G.
        • Di Maio M.
        • Cinieri S.
        • Leo S.
        • Beretta G.
        Coronavirus: older persons with cancer in Italy in the COVID-19 pandemic.
        Front Oncol. 2020; 10 (Published 2020 Apr 30): 648https://doi.org/10.3389/fonc.2020.00648
        View in Article
        • Lee L.Y.W.
        • Cazier J.B.
        • Starkey T.
        • et al.
        COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study.
        Lancet. 2020; 395: 1919-1926https://doi.org/10.1016/S0140-6736(20)31173-9
        View in Article
        • Montopoli M.
        • Zumerle S.
        • Vettor R.
        • et al.
        Androgen-deprivation therapies for prostate cancer and risk of infection by SARS-CoV-2: a population-based study (N = 4532).
        Ann Oncol. 2020; ([published online ahead of print, 2020 May 6]) (S0923-7534(20)39797-0)https://doi.org/10.1016/j.annonc.2020.04.479
        View in Article
        • Robilotti E.V.
        • Babady N.E.
        • Mead P.A.
        • et al.
        Determinants of COVID-19 disease severity in patients with cancer.
        Nat Med. 2020; ([published online ahead of print, 2020 Jun 24])https://doi.org/10.1038/s41591-020-0979-0
        View in Article
        • Horn L.
        • Whisenant J.G.
        • Torri V.
        • et al.
        Thoracic Cancers International COVID-19 Collaboration (TERAVOLT): impact of type of cancer therapy and COVID therapy on survival.
        J Clin Oncol. 2020; 38 (LBA111-LBA111)
        View in Article
        • Miyashita H.
        • Mikami T.
        • Chopra N.
        • et al.
        Do patients with cancer have a poorer prognosis of COVID-19? An experience in New York City.
        Ann Oncol. 2020; ([published online ahead of print, 2020 Apr 21]) (S0923-7534(20)39303-0)https://doi.org/10.1016/j.annonc.2020.04.006
        View in Article
        • Grasselli G.
        • Greco M.
        • Zanella A.
        • et al.
        Risk factors associated with mortality among patients with COVID-19 in intensive care units in Lombardy, Italy.
        JAMA Intern Med. 2020; ([published online ahead of print, 2020 Jul 15])https://doi.org/10.1001/jamainternmed.2020.3539
        View in Article
        • Wang J.
        • Song Q.
        • Chen Y.
        • et al.
        Systematic investigations of COVID-19 in 283 cancer patients.
        medRxiv. 2020; https://doi.org/10.1101/2020.04.28.20083246
        View in Article
        • COVIDSurg Collaborative
        Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study.
        Lancet. 2020; 396 ([published correction appears in Lancet. 2020 Jun 9]): 27-38https://doi.org/10.1016/S0140-6736(20)31182-X
        View in Article
        • Tian J.
        • Yuan X.
        • Xiao J.
        • et al.
        Clinical characteristics and risk factors associated with COVID-19 disease severity in patients with cancer in Wuhan, China: a multicentre, retrospective, cohort study.
        Lancet Oncol. 2020; 21: 893-903https://doi.org/10.1016/S1470-2045(20)30309-0
        View in Article
        • Mehta V.
        • Goel S.
        • Kabarriti R.
        • et al.
        Case fatality rate of cancer patients with COVID-19 in a New York hospital system.
        Cancer Discov. 2020; ([published online ahead of print, 2020 May 1])https://doi.org/10.1158/2159-8290.CD-20-0516
        View in Article
        • Yang K.
        • Sheng Y.
        • Huang C.
        • et al.
        Clinical characteristics, outcomes, and risk factors for mortality in patients with cancer and COVID-19 in Hubei, China: a multicentre, retrospective, cohort study.
        Lancet Oncol. 2020; ([published online ahead of print, 2020 May 29]) (S1470-2045(20)30310-30317)https://doi.org/10.1016/S1470-2045(20)30310-7
        View in Article
        • Pinato D.J.
        • Lee A.J.X.
        • Biello F.
        • et al.
        Presenting features and early mortality from SARS-CoV-2 infection in cancer patients during the initial stage of the COVID-19 pandemic in Europe.
        Cancers (Basel). 2020; 12 (Published 2020 Jul 8): E1841https://doi.org/10.3390/cancers12071841
        View in Article
        • Scarfò L.
        • Chatzikonstantinou T.
        • Rigolin G.M.
        • et al.
        COVID-19 severity and mortality in patients with chronic lymphocytic leukemia: a joint study by ERIC, the European Research Initiative on CLL, and CLL Campus.
        Leukemia. 2020; ([published online ahead of print, 2020 Jul 9])https://doi.org/10.1038/s41375-020-0959-x
        View in Article

      26. de Melo AC, Thuler LCS, da Silva JL, et al. Cancer inpatient with COVID-19: a report from the Brazilian National Cancer Institute. https://www.medrxiv.org/content/10.1101/2020.06.27.20141499v2. [Accessed 23 July, 2020].

        View in Article
        • Martinez-Lopez J.
        • Mateos M.V.
        • Encinas C.
        • et al.
        Multiple myeloma and SARS-CoV-2 infection: clinical characteristics and prognostic factors of inpatient mortality.
        medRxiv. 2020; https://doi.org/10.1101/2020.06.29.20142455
        View in Article
        • Russell B.
        • Moss C.
        • Papa S.
        • et al.
        Factors affecting COVID-19 outcomes in cancer patients − a first report from Guys Cancer Centre in London.
        medRxiv. 2020; (Preprint)https://doi.org/10.1101/2020.05.12.20094219
        View in Article
        • Basse C.
        • Diakite S.
        • Servois V.
        • et al.
        Characteristics and outcome of SARS-CoV-2 infection in cancer patients.
        medRxiv. 2020; https://doi.org/10.1101/2020.05.14.20101576
        View in Article
        • Barlesi F.
        • Foulon S.
        • Bayle A.
        • et al.
        Abstract CT403 - outcome of cancer patients infected with COVID-19, including toxicity of cancer treatments.
        in: AACR virtual meeting. 2020
        https://www.abstractsonline.com/pp8/#!/9045/presentation/10935
        Date accessed: July 23, 2020
        View in Article
        • Angelis V.
        • Tippu Z.
        • Joshi K.
        • et al.
        Defining the true impact of coronavirus disease 2019 in the at-risk population of patients with cancer.
        Eur J Cancer. 2020; 136 ([published online ahead of print, 2020 Jul 7]): 99-106https://doi.org/10.1016/j.ejca.2020.06.027
        View in Article
        • Gupta S.
        • Hayek S.S.
        • Wang W.
        • et al.
        Factors associated with death in critically ill patients with coronavirus disease 2019 in the US.
        JAMA Intern Med. 2020; ([published online ahead of print, 2020 Jul 15])https://doi.org/10.1001/jamainternmed.2020.3596
        View in Article
        • Zhang H.
        • Wang L.
        • Chen Y.
        • et al.
        Outcomes of novel coronavirus disease 2019 (COVID-19) infection in 107 patients with cancer from Wuhan, China.
        Cancer. 2020; ([published online ahead of print, 2020 Jun 23])https://doi.org/10.1002/cncr.33042
        View in Article
        • Deng G.
        • Yin M.
        • Chen X.
        • Zeng F.
        Clinical determinants for fatality of 44,672 patients with COVID-19.
        Crit Care. 2020; 24 (Published 2020 Apr 28): 179https://doi.org/10.1186/s13054-020-02902-w
        View in Article
        • Dai M.
        • Liu D.
        • Liu M.
        • et al.
        Patients with cancer Appear more vulnerable to SARS-CoV-2: a multicenter study during the COVID-19 outbreak.
        Cancer Discov. 2020; 10: 783-791https://doi.org/10.1158/2159-8290.CD-20-0422
        View in Article
        • Luo J.
        • Rizvi H.
        • Preeshagul I.R.
        • et al.
        COVID-19 in patients with lung cancer.
        Ann Oncol. 2020; ([published online ahead of print, 2020 Jun 16]) (S0923-7534(20)39894-X)https://doi.org/10.1016/j.annonc.2020.06.007
        View in Article
        • Hultcrantze M.
        • Richter J.
        • Rosenbaum C.A.
        • et al.
        COVID-19 infections and outcomes in patients with multiple myeloma in New York City: a cohort study from five academic centers.
        Blood Cancer Discov. July 30 2020; https://doi.org/10.1158/2643-3230.BCD-20-0102
        View in Article
        • Cook G.
        • John Ashcroft A.
        • Pratt G.
        • et al.
        Real-world assessment of the clinical impact of symptomatic infection with severe acute respiratory syndrome coronavirus (COVID-19 disease) in patients with multiple myeloma receiving systemic anti-cancer therapy.
        Br J Haematol. 2020; ([published online ahead of print, 2020 May 21])https://doi.org/10.1111/bjh.16874
        View in Article
        • Booth S.
        • Willan J.
        • Wong H.
        • et al.
        Regional outcomes of severe acute respiratory syndrome coronavirus 2 infection in hospitalised patients with haematological malignancy.
        Eur J Haematol. 2020; ([published online ahead of print, 2020 Jun 16])https://doi.org/10.1111/ejh.13469
        View in Article
        • Yarza R.
        • Bover M.
        • Paredes D.
        • et al.
        SARS-CoV-2 infection in cancer patients undergoing active treatment: analysis of clinical features and predictive factors for severe respiratory failure and death.
        Eur J Cancer. 2020; ([published online ahead of print, 2020 Jun 6]) (S0959-8049(20)30313-0)https://doi.org/10.1016/j.ejca.2020.06.001
        View in Article
        • Assaad S.
        • Avrillon V.
        • Fournier M.L.
        • et al.
        High mortality rate in cancer patients with symptoms of COVID-19 with or without detectable SARS-COV-2 on RT-PCR.
        Eur J Cancer. 2020; ([published online ahead of print, 2020 Jun 7]) (S0959-8049(20)30314-2)https://doi.org/10.1016/j.ejca.2020.05.028
        View in Article
        • Wang B.
        • Van Oekelen O.
        • Mouhieddine T.H.
        • et al.
        A tertiary center experience of multiple myeloma patients with COVID-19: lessons learned and the path forward.
        J Hematol Oncol. 2020; 13 (Published 2020 Jul 14): 94https://doi.org/10.1186/s13045-020-00934-x
        View in Article
        • Gonzalez-Cao M.
        • Antonazas-Basa M.
        • Puertolas T.
        • et al.
        Cancer immunotherapy does not increase the risk of death by COVID-19 in melanoma patients.
        medRxiv. 2020; https://doi.org/10.1101/2020.05.19.20106971
        View in Article
        • Suleyman G.
        • Fadel R.A.
        • Malette K.M.
        • et al.
        Clinical characteristics and morbidity associated with coronavirus disease 2019 in a series of patients in metropolitan detroit.
        JAMA Netw Open. 2020; 3 (Published 2020 Jun 1)e2012270https://doi.org/10.1001/jamanetworkopen.2020.12270
        View in Article
        • Rogado J.
        • Obispo B.
        • Pangua C.
        • et al.
        Covid-19 transmission, outcome and associated risk factors in cancer patients at the first month of the pandemic in a Spanish hospital in Madrid.
        Clin Transl Oncol. 2020; ([published online ahead of print, 2020 May 25]): 1-5https://doi.org/10.1007/s12094-020-02381-z
        View in Article
        • Aries J.A.
        • Davies J.K.
        • Auer R.L.
        • et al.
        Clinical outcome of coronavirus disease 2019 in haemato-oncology patients.
        Br J Haematol. 2020; ([published online ahead of print, 2020 May 18])https://doi.org/10.1111/bjh.16852
        View in Article
        • Martín-Moro F.
        • Marquet J.
        • Piris M.
        • et al.
        Survival study of hospitalised patients with concurrent COVID-19 and haematological malignancies.
        Br J Haematol. 2020; 190: e16-e20https://doi.org/10.1111/bjh.16801
        View in Article
        • Zhang L.
        • Zhu F.
        • Xie L.
        • et al.
        Clinical characteristics of COVID-19-infected cancer patients: a retrospective case study in three hospitals within Wuhan, China.
        Ann Oncol. 2020; 31: 894-901https://doi.org/10.1016/j.annonc.2020.03.296
        View in Article
        • Joharatnam-Hogan N.
        • Hochhauser D.
        • Shiu K.K.
        • et al.
        Outcomes of the 2019 Novel Coronavirus in patients with or without a history of cancer - a multi-centre North London experience.
        medRxiv. 2020; https://doi.org/10.1101/2020.04.16.20061127
        View in Article
        • Stroppa E.M.
        • Toscani I.
        • Citterio C.
        • et al.
        Coronavirus disease-2019 in cancer patients. A report of the first 25 cancer patients in a western country (Italy).
        Future Oncol. 2020; 16: 1425-1432https://doi.org/10.2217/fon-2020-0369
        View in Article
        • Ciceri F.
        • Castagna A.
        • Rovere-Querini P.
        • et al.
        Early predictors of clinical outcomes of COVID-19 outbreak in Milan, Italy.
        Clin Immunol. 2020; 217 ([published online ahead of print, 2020 Jun 12]): 108509https://doi.org/10.1016/j.clim.2020.108509
        View in Article
        • Bogani G.
        • Ditto A.
        • Bosio S.
        • Brusadelli C.
        • Raspagliesi F.
        Cancer patients affected by COVID-19: experience from Milan, Lombardy.
        Gynecol Oncol. 2020; ([published online ahead of print, 2020 Jun 10]) (S0090-8258(20)31976-4)https://doi.org/10.1016/j.ygyno.2020.06.161
        View in Article
        • Guan W.J.
        • Liang W.H.
        • Zhao Y.
        • et al.
        Comorbidity and its impact on 1590 patients with COVID-19 in China: a nationwide analysis.
        Eur Respir J. 2020; 55 (Published 2020 May 14): 2000547https://doi.org/10.1183/13993003.00547-2020
        View in Article
        • Tagliamento M.
        • Lambertini M.
        • Genova C.
        • et al.
        Call for ensuring cancer care continuity during COVID-19 pandemic.
        ESMO Open. 2020; 5e000783https://doi.org/10.1136/esmoopen-2020-000783
        View in Article
        • Wang L.
        • He W.
        • Yu X.
        • et al.
        Coronavirus disease 2019 in elderly patients: characteristics and prognostic factors based on 4-week follow-up.
        J Infect. 2020; 80: 639-645https://doi.org/10.1016/j.jinf.2020.03.019
        View in Article
        • Lattenist R.
        • Yildiz H.
        • De Greef J.
        • Bailly S.
        • Yombi J.C.
        COVID-19 in adult patients with hematological disease: analysis of clinical characteristics and outcomes.
        Indian J Hematol Blood Transfus. 2020; ([published online ahead of print, 2020 Jul 7]): 1-5https://doi.org/10.1007/s12288-020-01318-4
        View in Article
        • Yu J.
        • Ouyang W.
        • Chua M.L.K.
        • Xie C.
        SARS-CoV-2 transmission in patients with cancer at a tertiary care hospital in Wuhan, China.
        JAMA Oncol. 2020; 6 ([published online ahead of print, 2020 Mar 25]): 1108-1110https://doi.org/10.1001/jamaoncol.2020.0980
        View in Article
        • Wu Q.
        • Chu Q.
        • Zhang H.
        • et al.
        Clinical outcomes of coronavirus disease 2019 (COVID-19) in cancer patients with prior exposure to immune checkpoint inhibitors.
        Cancer Commun (Lond). 2020; ([published online ahead of print, 2020 Jul 15])https://doi.org/10.1002/cac2.12077
        View in Article

      Article info

      Publication history

      Published online: September 02, 2020
      Accepted: August 17, 2020
      Received: July 24, 2020

      Identification

      DOI: https://doi.org/10.1016/j.ejca.2020.08.011

      Copyright

      © 2020 Elsevier Ltd. All rights reserved.

      ScienceDirect

      Access this article on ScienceDirect

      The content on this site is intended for healthcare professionals.


      We use cookies to help provide and enhance our service and tailor content. To update your cookie settings, please visit the Cookie Preference Center for this site.
      Copyright © 2023 Elsevier Inc. except certain content provided by third parties.


      RELX