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Figure.  Participating North American Cancer Centers in the COVID-19 and Cancer Consortium (CCC19)
Participating North American Cancer Centers in the COVID-19 and Cancer Consortium (CCC19)

Map shows the 126 cancer centers in the CCC19 that were included in this review as of June 1, 2021. The markers (spiked circles with 19s, representing the stylized logo of the CCC19) represent the cities in which participating cancer centers were located. The lines from markers to numbers (preceded by x) indicate the number of partner sites in the overlapping geographic location (eg, x2 indicates 2 partner sites).

Table 1.  Major Registries
Major Registries
Table 2.  Risk Factors Associated With Severe Disease and Mortality in Patients With COVID-19 From Different Registries
Risk Factors Associated With Severe Disease and Mortality in Patients With COVID-19 From Different Registries
1.
Desai  A, Gupta  R, Advani  S,  et al.  Mortality in hospitalized patients with cancer and coronavirus disease 2019: a systematic review and meta-analysis of cohort studies.   Cancer. 2021;127(9):1459-1468. doi:10.1002/cncr.33386 PubMedGoogle ScholarCrossref
2.
Jee  J, Foote  MB, Lumish  M,  et al.  Chemotherapy and COVID-19 outcomes in patients with cancer.   J Clin Oncol. 2020;38(30):3538-3546. doi:10.1200/JCO.20.01307 PubMedGoogle ScholarCrossref
3.
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;21(7):904-913. doi:10.1016/S1470-2045(20)30310-7 PubMedGoogle ScholarCrossref
4.
Bakouny  Z, Hawley  JE, Choueiri  TK,  et al.  COVID-19 and cancer: current challenges and perspectives.   Cancer Cell. 2020;38(5):629-646. doi:10.1016/j.ccell.2020.09.018 PubMedGoogle ScholarCrossref
5.
Wang  Q, Berger  NA, Xu  R.  Analyses of risk, racial disparity, and outcomes among US patients with cancer and COVID-19 infection.   JAMA Oncol. 2021;7(2):220-227. doi:10.1001/jamaoncol.2020.6178 PubMedGoogle ScholarCrossref
6.
Desai  A, Khaki  AR, Kuderer  NM.  Use of real-world electronic health records to estimate risk, risk factors, and disparities for COVID-19 in patients with cancer.   JAMA Oncol. 2021;7(2):227-229. doi:10.1001/jamaoncol.2020.5461 PubMedGoogle ScholarCrossref
7.
The RECOVERY Collaborative Group.  Dexamethasone in hospitalized patients with Covid-19.   N Engl J Med. 2021;384:693-704. doi:10.1056/NEJMoa2021436Google Scholar
8.
Angus  DC, Derde  L, Al-Beidh  F,  et al; Writing Committee for the REMAP-CAP Investigators.  Effect of hydrocortisone on mortality and organ support in patients with severe COVID-19: the REMAP-CAP COVID-19 corticosteroid domain randomized clinical trial.   JAMA. 2020;324(13):1317-1329. doi:10.1001/jama.2020.17022 PubMedGoogle Scholar
9.
Dequin  PF, Heming  N, Meziani  F,  et al; CAPE COVID Trial Group and the CRICS-TriGGERSep Network.  Effect of hydrocortisone on 21-day mortality or respiratory support among critically ill patients with COVID-19: a randomized clinical trial.   JAMA. 2020;324(13):1298-1306. doi:10.1001/jama.2020.16761 PubMedGoogle ScholarCrossref
10.
Tomazini  BM, Maia  IS, Bueno  FR,  et al; Em Nome dos Investigadores da Coalizao COVID-19 Brasil III.  COVID-19–associated ARDS treated with dexamethasone (CoDEX): study design and rationale for a randomized trial.   Rev Bras Ter Intensiva. 2020;32(3):354-362. doi:10.5935/0103-507X.20200063 PubMedGoogle ScholarCrossref
11.
Liu  J, Zhang  S, Dong  X,  et al.  Corticosteroid treatment in severe COVID-19 patients with acute respiratory distress syndrome.   J Clin Invest. 2020;130(12):6417-6428. doi:10.1172/JCI140617 PubMedGoogle ScholarCrossref
12.
Ramiro  S, Mostard  RLM, Magro-Checa  C,  et al.  Historically controlled comparison of glucocorticoids with or without tocilizumab versus supportive care only in patients with COVID-19-associated cytokine storm syndrome: results of the CHIC study.   Ann Rheum Dis. 2020;79(9):1143-1151. doi:10.1136/annrheumdis-2020-218479 PubMedGoogle ScholarCrossref
13.
American Cancer Society. COVID-19 vaccines in people with cancer. American Cancer Society. Updated July 13, 2021. Accessed February 4, 2021. https://www.cancer.org/treatment/treatments-and-side-effects/physical-side-effects/low-blood-counts/infections/covid-19-vaccines-in-people-with-cancer.html
14.
Kuderer  NM, Hill  JA, Carpenter  PA, Lyman  GH. Challenges and opportunities for COVID-19 vaccines in patients with cancer. Cancer Invest. 2021;39(3):205-213. doi:10.1080/07357907.2021.1885596
15.
Lyman  GH, Kuderer  NM.  Randomized controlled trials versus real-world data in the COVID-19 era: a false narrative.   Cancer Invest. 2020;38(10):537-542. doi:10.1080/07357907.2020.1841922 PubMedGoogle ScholarCrossref
16.
Desai  A, Warner  J, Kuderer  N,  et al.  Crowdsourcing a crisis response for COVID-19 in oncology.   Nat Cancer. 2020;1(5):1-4. doi:10.1038/s43018-020-0065-z PubMedGoogle ScholarCrossref
17.
@ADesaiMD. COVID19nCancer is important! Data out of China indicates higher risk. Lets collaborate to survey data, provide update on the effective risk mitigation strategies @NIH designated cancer centers for #oncologists #cancer patients @GlopesMd @marklewismd @ASCO @ASH_hematology #SoMe. https://twitter.com/ADesaiMD/status/1238605058775732224. Posted March 13, 2020. Accessed February 7, 2021.
18.
COVID-19 and Cancer Consortium. What information is collected in the CCC19 survey? COVID-19 and Cancer Consortium; 2020. Accessed June 2021. https://ccc19.org/faqs
19.
Kuderer  NM, Choueiri  TK, Shah  DP,  et al; COVID-19 and Cancer Consortium.  Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study.   Lancet. 2020;395(10241):1907-1918. doi:10.1016/S0140-6736(20)31187-9 PubMedGoogle ScholarCrossref
20.
Warner  JL, Rubinstein S, Grivas P, et al. Clinical impact of COVID-19 on patients with cancer: data from the COVID-19 and Cancer Consortium (CCC19). J Clin Oncol. 2020;38(18 suppl):LBA110. Accessed December 10, 2020. doi:10.1016/S0140-6736(20)31187-9
21.
Kuderer  NM, Wulff-Burchfield  E, Rubinstein  SM, Grivas  P, Warner  JL.  Cancer and COVID-19—authors’ reply.   Lancet. 2020;396(10257):1067-1068. doi:10.1016/S0140-6736(20)32065-1 PubMedGoogle ScholarCrossref
22.
Rivera  DR, Peters  S, Panagiotou  OA,  et al; COVID-19 and Cancer Consortium.  Utilization of COVID-19 treatments and clinical outcomes among patients with cancer: a COVID-19 and Cancer Consortium (CCC19) cohort study.   Cancer Discov. 2020;10(10):1514-1527. doi:10.1158/2159-8290.CD-20-0941 PubMedGoogle ScholarCrossref
23.
Rosovsky R, Li A, Desai A, et al; COVID-19 and Cancer Consortium (CCC19). Venous thrombotic complications in cancer patients with SARS-CoV-2 infection: report from the COVID-19 and Cancer Consortium (CCC19) registry analysis. Res Pract Thromb Haemost. 2020;4(suppl 1):PB/CO07.
24.
Li  A, Kuderer NM, Warner JL, et al. Incidence of and risk factors for venous thromboembolism among hospitalized patients with cancer and COVID-19: report from the COVID-19 and Cancer Consortium (CCC19) registry. Abstract presented at: virtual annual meeting and exposition of the American Society of Hematology; December 5, 2020. Accessed December 28, 2020. https://ash.confex.com/ash/2020/webprogram/Paper138834.html
25.
Li A, Kuderer NM, Hsu CY, et al. The COVID-TE risk assessment model for venous thromboembolism in hospitalized patients with cancer and COVID-19. J Thromb Haemost. Published online July 14, 2021. doi:10.1111/jth.15463
26.
Grivas P, Khaki AR, Wise-Draper TM, et al. Association of clinical factors and recent anticancer therapy with COVID-19 severity among patients with cancer: a report from the COVID-19 and Cancer Consortium. Ann Oncol. 2021;32(6):P787-P800. doi:10.1016/j.annonc.2021.02.024
27.
Thompson  MA, Henderson  JP, Shah  PK,  et al; COVID-19 and Cancer Consortium.  Association of convalescent plasma therapy with survival in patients with hematologic cancers and COVID-19.   JAMA Oncol. 2021. Published online June 17, 2021. doi:10.1001/jamaoncol.2021.1799PubMedGoogle Scholar
28.
COVID-19 and Cancer Consortium. Publications. COVID-19 and Cancer Consortium; 2021 Accessed August 3, 2021. https://ccc19.org/publications
29.
Pinato  DJ, Lee  AJX, 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(7):1841. doi:10.3390/cancers12071841 PubMedGoogle ScholarCrossref
30.
Pinato  DJ, Zambelli  A, Aguilar-Company  J,  et al.  Clinical portrait of the SARS-CoV-2 epidemic in European cancer patients.   Cancer Discov. 2020;10(10):1465-1474. doi:10.1158/2159-8290.CD-20-0773 PubMedGoogle ScholarCrossref
31.
NIHR Imperial Biomedical Research Centre. OnCovid: natural history and outcomes of cancer patients during the COVID19 epidemic. National Institute for Health Research; 2021. Accessed August 3, 2021. https://imperialbrc.nihr.ac.uk/research/covid-19/covid-19-ongoing-studies/oncovid
32.
Palmieri  C, Turtle  L, Docherty  A,  et al.  Prospective data of first 1,797 hospitalised patients with cancer and COVID-19 derived from the COVID-19 Clinical Information Network and International Severe Acute Respiratory and Emerging Infections Consortium, WHO Coronavirus Clinical Characterisation Consortium.   Ann Oncol. 2020;31(suppl 4):S992. doi:10.1016/j.annonc.2020.08.1735 Google ScholarCrossref
33.
Pinato  DJ, Scotti  L, Gennari  A,  et al; OnCovid Study Group.  Determinants of enhanced vulnerability to coronavirus disease 2019 in UK patients with cancer: a European study.   Eur J Cancer. 2021;150:190-202. doi:10.1016/j.ejca.2021.03.035 PubMedGoogle ScholarCrossref
34.
Dettorre  GM, Dolly  S, Loizidou  A,  et al; OnCovid Study Group.  Systemic pro-inflammatory response identifies patients with cancer with adverse outcomes from SARS-CoV-2 infection: the OnCovid inflammatory score.   J Immunother Cancer. 2021;9(3):e002277. doi:10.1136/jitc-2020-002277 PubMedGoogle Scholar
35.
Lee  LY, Cazier  JB, Angelis  V,  et al; UK Coronavirus Monitoring Project Team.  COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study.   Lancet. 2020;395(10241):1919-1926. doi:10.1016/S0140-6736(20)31173-9 PubMedGoogle ScholarCrossref
36.
Garassino  MC, Whisenant  JG, Huang  LC,  et al; TERAVOLT Investigators.  COVID-19 in patients with thoracic malignancies (TERAVOLT): first results of an international, registry-based, cohort study.   Lancet Oncol. 2020;21(7):914-922. doi:10.1016/S1470-2045(20)30314-4 PubMedGoogle ScholarCrossref
37.
Horn L, Whisenant JG, 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(18 suppl):LBA111. doi:10.1200/JCO.2020.38.18_suppl.LBA111
38.
Baena Espinar  J, Torri  V, Whisenant  J,  et al.  Defining COVID-19 outcomes in thoracic cancer patients: TERAVOLT (Thoracic Cancers International COVID 19 Collaboration).   Ann Oncol. 2020;31(suppl 4):S1204-S1205. doi:10.1016/j.annonc.2020.08.2316 Google ScholarCrossref
39.
American Society of Clinical Oncology. ASCO COVID-19 Registry data dashboard. American Society of Clinical Oncology; 2021. Accessed June 2, 2021. https://www.asco.org/asco-coronavirus-information/coronavirus-registry/covid-19-registry-data-dashboard
40.
American Society of Clinical Oncology. ASCO COVID-19 Registry data dashboard. American Society of Clinical Oncology. November 3, 2020. Accessed December 5, 2020. https://www.asco.org/asco-coronavirus-information/coronavirus-registry/covid-19-registry-data-dashboard
41.
Mileham KF, Brunooge SS, Aggarwal C, et al. Mortality risk for patients undergoing cancer treatment who acquire SARS-CoV-2: ASCO registry. J Clin Oncol. 2021;39(15 suppl):6509. doi:10.1200/JCO.2021.39.15_suppl.6509
42.
ASH Research Collaborative. COVID-19 Registry data summaries. ASH Research Collaborative. Updated July 18, 2021. Accessed June 2, 2021. https://www.ashresearchcollaborative.org/s/covid-19-registry/data-summaries
43.
ASH Research Collaborative. COVID 19 Registry data summaries. ASH Research Collaborative. Updated July 18, 2021. Accessed December 10, 2020. https://www.ashresearchcollaborative.org/s/covid-19-registry-data-summaries
44.
Wood  WA, Neuberg  DS, Thompson  JC,  et al.  Outcomes of patients with hematologic malignancies and COVID-19: a report from the ASH Research Collaborative Data Hub.   Blood Adv. 2020;4(23):5966-5975. doi:10.1182/bloodadvances.2020003170 PubMedGoogle ScholarCrossref
45.
Wood W, Neuberg DS, Thompson JC, et al. Outcomes of patients with hematologic malignancies and COVID-19 infection: a report from the ASH Research Collaborative Data Hub. Abstract presented at: virtual annual meeting and exposition of the American Society of Hematology; December 5, 2020. Accessed January 31, 2021. https://ash.confex.com/ash/2020/webprogram/Paper141327.html
46.
Bernabe-Ramirez  C, Velazquez  AI, Olazagasti  C,  et al.  The HOLA COVID-19 study: an international effort to determine how COVID-19 has impacted oncology practices in Latin America.   Cancer Cell. 2020;38(5):605-608. doi:10.1016/j.ccell.2020.10.013 PubMedGoogle ScholarCrossref
47.
Coronavirus (COVID-19) Outcomes Registries in Immunocompromised Individuals Australia (CORIA): a multisite registry and optional biorepository in people with COVID-19 and selected conditions affecting immune function. ClinicalTrials.gov identifier: NCT04354818. Updated July 28, 2020. Accessed December 5, 2020. https://clinicaltrials.gov/ct2/show/NCT04354818
48.
ESMO. ESMO-CoCARE registry. European Society for Medical Oncology; 2020. Accessed December 5, 2020. https://www.esmo.org/covid-19-and-cancer/collaborating-on-registries-studies-and-surveys/esmo-cocare-registry
49.
European Society for Medical Oncology. ESMO Congress 2021. European Society for Medical Oncology; 2020. Accessed August 3, 2021. https://www.esmo.org/meetings/esmo-congress-2021
50.
de Joode  K, Dumoulin  DW, Tol  J,  et al; DOCC Investigators.  Dutch Oncology COVID-19 Consortium: outcome of COVID-19 in patients with cancer in a nationwide cohort study.   Eur J Cancer. 2020;141:171-184. doi:10.1016/j.ejca.2020.09.027 PubMedGoogle ScholarCrossref
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National Cancer Institute. NCI COVID-19 in Cancer Patients Study (NCCAPS). National Cancer Institute. Updated November 9, 2020. Accessed December 5, 2020. https://www.cancer.gov/research/key-initiatives/covid-19/coronavirus-research-initiatives/nccaps
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Ahlstrom J. Myeloma Crowd introduces largest COVID-19 multiple myeloma patient study. Myeloma Crowd by HealthTree, Crowd Care Foundation. April 16, 2020. Accessed August 3, 2021. https://www.myelomacrowd.org/the-myeloma-crowd-introduces-the-largest-covid-19-multiple-myeloma-study/
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Myeloma Crowd by HealthTree. Improving myeloma patient outcomes and accelerating a cure. Myeloma Crowd by HealthTree, Crowd Care Foundation; 2021. Accessed August 3, 2021. https://www.myelomacrowd.org/healthtree/
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Multiple Myeloma Research Foundation. MMRF partners with Dana Farber Cancer Institute on COVID-19 IMPACT research study (antibody-based COVID-19 testing). Multiple Myeloma Research Foundation. July 28, 2021. Accessed August 3, 2021. https://themmrf.org/2021/07/28/mmrf-partners-with-dana-farber-cancer-institute-on-covid-19-impact-research-study-antibody-based-covid-19-testing
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Chari  A, Samur  MK, Martinez-Lopez  J,  et al.  Clinical features associated with COVID-19 outcome in multiple myeloma: first results from the International Myeloma Society data set.   Blood. 2020;136(26):3033-3040. doi:10.1182/blood.2020008150 PubMedGoogle ScholarCrossref
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Sharma  A, Bhatt  NS, St Martin  A,  et al.  Clinical characteristics and outcomes of COVID-19 in haematopoietic stem-cell transplantation recipients: an observational cohort study.   Lancet Haematol. 2021;8(3):e185-e193. doi:10.1016/S2352-3026(20)30429-4 PubMedGoogle ScholarCrossref
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Frigault  MJ, Nikiforow  S, Mansour  MK,  et al.  Tocilizumab not associated with increased infection risk after CAR T-cell therapy: implications for COVID-19?   Blood. 2020;136(1):137-139. doi:10.1182/blood.2020006216 PubMedGoogle ScholarCrossref
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Kim  E, Rubinstein  SM, Nead  KT, Wojcieszynski  AP, Gabriel  PE, Warner  JL.  The evolving use of electronic health records (EHR) for research.   Semin Radiat Oncol. 2019;29(4):354-361. doi:10.1016/j.semradonc.2019.05.010 PubMedGoogle ScholarCrossref
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Shyr  Y, Berry  LD, Hsu  CY.  Scientific rigor in the age of COVID-19.   JAMA Oncol. 2021;7(2):171-172. doi:10.1001/jamaoncol.2020.6639 PubMedGoogle ScholarCrossref
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    Review
    September 2, 2021

    COVID-19 and Cancer: A Review of the Registry-Based Pandemic Response

    Author Affiliations
    • 1Division of Medical Oncology, Department of Medicine, Mayo Clinic, Rochester, Minnesota
    • 2Division of Hematology, Department of Medicine, Mayo Clinic, Rochester, Minnesota
    • 3Department of Medicine, University of Connecticut, Farmington
    • 4Division of Hematology, Department of Medicine, Medical Oncology and Palliative Care, University of Wisconsin, Madison
    • 5Department of Medicine, University of Chicago, Chicago, Illinois
    • 6Division of Hematology/Oncology, St. Michael’s Hospital, University of Toronto, Toronto, Ontario, Canada
    • 7Advanced Cancer Research Group, Seattle, Washington
    • 8Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, Washington
    • 9Division of Clinical Research, Fred Hutchinson Cancer Research Center, Seattle, Washington
    • 10Division of Oncology, Department of Medicine, University of Washington, Seattle
    • 11Vanderbilt-Ingram Cancer Center, Vanderbilt University Medical Center, Nashville, Tennessee
    • 12Department of Surgery and Cancer, Imperial College London, London, United Kingdom
    • 13Division of Oncology, Department of Translational Medicine, Piemonte Orientale University, Novara, Italy
    • 14Oncology Department, Centre Hospitalier Universitaire Vaudois, Lausanne, Switzerland
    • 15Division of Hematology, Department of Medicine, University of North Carolina at Chapel Hill
    • 16Aurora Cancer Care, Advocate Aurora Health, Milwaukee, Wisconsin
    JAMA Oncol. 2021;7(12):1882-1890. doi:10.1001/jamaoncol.2021.4083
    Abstract

    Importance  The COVID-19 pandemic has had consequences for patients with cancer worldwide and has been associated with delays in diagnosis, interruption of treatment and follow-up care, and increases in overall infection rates and premature mortality.

    Observations  Despite the challenges experienced during the pandemic, the global oncology community has responded with an unprecedented level of investigation, collaboration, and technological innovation through the rapid development of COVID-19 registries that have allowed an increased understanding of the natural history, risk factors, and outcomes of patients with cancer who are diagnosed with COVID-19. This review describes 14 major registries comprising more than 28 500 patients with cancer and COVID-19; these ongoing registry efforts have provided an improved understanding of the impact and outcomes of COVID-19 among patients with cancer.

    Conclusions and Relevance  An initiative is needed to promote active collaboration between different registries to improve the quality and consistency of information. Well-designed prospective and randomized clinical trials are needed to collect high-level evidence to guide long-term epidemiologic, behavioral, and clinical decision-making for this and future pandemics.

    Introduction

    Despite increasing vaccine availability, the COVID-19 pandemic continues to pose a substantial threat worldwide. Patients with cancer are a distinctly vulnerable population1; they are often immunocompromised and are at an increased risk of experiencing COVID-19–associated complications.2-6 Potential treatments for COVID-19 have been intensively studied. For example, the performance of the Randomised Evaluation of COVID-19 Therapy (RECOVERY) clinical trial7 in the United Kingdom (UK) and the pace of vaccine development and deployment have been impressive. Despite these successes, patients with cancer have largely been excluded from these studies. The RECOVERY study and 4 other prospective clinical trials8-12 of corticosteroid therapy either did not include cancer as a comorbidity or were not adequately powered to determine efficacy or safety in the subset of patients with cancer. Most of the clinical trials of COVID-19 vaccines did not include patients who were actively receiving anticancer treatment or had a recent history of cancer.13,14 Thus, well-designed registries and retrospective cohort studies remain important tools for increasing our collective understanding of the natural history and outcomes of COVID-19 among patients with cancer.15

    Despite the many challenges that the pandemic has created, the global biomedical community has responded with an unprecedented level of investigation, collaboration, and technological innovation. One example from the field of oncology has been the rapid development of COVID-19 registries, with major efforts coming from crowdsourcing models that aim to understand the natural history, risk factors, and outcomes among patients with cancer who are diagnosed with COVID-19.16 The present study reviewed and described 14 major registries comprising more than 28 500 patients with cancer and COVID-19 (eTable in the Supplement). The inclusion criteria and the number of patients accrued for each registry are summarized in Table 1. Individual registries were approved by their respective institutional review boards.

    COVID-19 and Cancer Consortium (CCC19)

    The CCC19 is a grassroots crowdsourcing initiative that originated on Twitter.17 To our knowledge, the CCC19 registry was the first among many COVID-19 registries developed for patients with cancer. The CCC19 registry contained more than 10 000 cases as of June 1, 2021, which were sourced across 128 participating sites in North America18 (Figure). Apart from understanding the association of COVID-19 with cancer outcomes, the CCC19 also aims to study factors associated with short-term and long-term outcomes of COVID-19 and cancer treatment modifications made in response to a diagnosis of COVID-19.

    Among patients older than 18 years with active or previous cancer and confirmed SARS-CoV-2 infection, an initial analysis of 928 patients revealed that 43% had active (ie, measurable) cancer and 39% were receiving active treatment.19,20 Death within 30 days was documented in 13% of patients. An update to this original report that included extended follow-up data found that 30-day all-cause mortality had increased to 17% for all patients and to 20% when patients without complete 30-day follow-up were censored.21 Another report from the CCC1922 examined the potential role of COVID-19 treatments among more than 2000 patients with cancer and found no statistically significant 30-day all-cause mortality benefit associated with hydroxychloroquine or high-dose corticosteroid therapy alone or in combination. Potential benefit was found with remdesivir therapy; however, the report concluded that the benefits observed in a retrospective cohort study and the type of treatment chosen for COVID-19 reflected factors associated with clinical decision-making as well as disparities in access to the drugs, highlighting the difficulty in providing definitive statements about drug benefits based on data from retrospective studies, even in the era of COVID-19.20,22

    Furthermore, data from this registry yielded a venous thromboembolism incidence of 10% among patients with cancer who were admitted to the intensive care unit for illness associated with COVID-19.23-25 Venous thromboembolism was more frequently observed among those who had recently received any anticancer therapy vs no recent anticancer therapy (5.2% vs 2.2%, respectively) and those with active disease progression vs no disease progression (7.1% vs 2.0%).23 An update of these data24,25 revealed that those with active disease who had recently received anticancer therapy continued to be at a particularly increased risk of venous thromboembolism and pulmonary embolism. This cohort study also suggested that patients who received anticoagulant or antiplatelet therapy before admission may have had a lower risk of developing venous thromboembolism or pulmonary embolism.24 These findings have led to the development of a risk assessment model for venous thromboembolism to assist with real-time evidence-based decisions for hospitalized patients with cancer and COVID-19.25

    The CCC19 subsequently published an analysis of 4966 patients with COVID-19 and cancer.26 In a multivariable logistic regression analysis, older age, male sex, obesity, comorbidities, non-Hispanic Black race/ethnicity, Hispanic ethnicity, worse Eastern Cooperative Oncology Group (ECOG) performance status, hematologic cancer, recent receipt of cytotoxic chemotherapy, low or high lymphocyte count, high absolute neutrophil count, thrombocytopenia, and elevated creatinine, troponin, lactate dehydrogenase, and C-reactive protein levels were all associated with more severe COVID-19 illness and worse outcomes. This analysis also found that certain anticancer therapies (eg, rituximab, cyclophosphamide, doxorubicin hydrochloride [hydroxydaunorubicin], vincristine sulfate [Oncovin], and prednisone [R-CHOP] therapy) were associated with particularly high 30-day mortality (>40%). This finding is being further investigated in an expanded cohort of patients with hematologic cancer.

    One study27 evaluated the association of convalescent plasma therapy with 30-day mortality among adults with hematologic cancer who were hospitalized with COVID-19, finding that treatment with convalescent plasma was associated with improved 30-day mortality (hazard ratio [HR], 0.52; 95% CI, 0.29-0.92), which suggested a potential survival benefit with convalescent plasma therapy in this subgroup. This survival benefit was also observed among patients in the intensive care unit (HR, 0.40; 95% CI, 0.20-0.80) and patients requiring mechanical ventilation (HR, 0.32; 95% CI, 0.14-0.72).

    The CCC19 is currently conducting additional studies that focus on older patients with cancer, minority and underrepresented racial and ethnic groups with cancer, patients with prostate cancer, and patients with co-occurring infections, sarcoma, and bleeding complications (list of ongoing studies available on CCC19 website28).

    OnCovid

    OnCovid is an ongoing observational study29-31 sponsored by Imperial College London that was initiated in March 2020 with the aim of documenting characteristics and outcomes of SARS-CoV-2 infection among patients with cancer. OnCovid is a pantumor registry with purposefully broad inclusion criteria (ie, patient age ≥18 years, confirmed diagnosis of any type of cancer, and diagnosis of SARS-CoV-2 infection confirmed by nasopharyngeal swab testing). The OnCovid study is the first, to our knowledge, to investigate the progression of the SARS-Cov-2 pandemic in Europe, documenting a case fatality rate of 29% in its first report of 204 patients recruited in the UK, Italy, and Spain.29 In a follow-up report of 890 European patients, the OnCovid researchers reported an overall case fatality rate of 33.6%, finding that older age, male sex, and comorbidity burden were associated with complicated COVID-19 symptoms and a higher risk of death.30 No detrimental consequences were observed among those recently exposed to systemic anticancer therapies, and the receipt of anti–COVID-19 therapies was associated with improvements in mortality. Mortality among patients with cancer who were admitted with COVID-19 was concentrated outside of oncology department inpatient areas and was characterized by highly complex symptomatic needs, highlighting challenges in the delivery of high-quality palliative care to these patients.32 The OnCovid researchers found substantial geographic heterogeneity in COVID-19 outcomes in Europe,33 helping to clarify the role of the systemic proinflammatory response in adverse outcomes associated with COVID-19 among patients with cancer and validating that hypoalbuminemia and lymphopenia, when combined in the OnCovid Inflammation Score, were independently associated with worse outcomes in this patient population.34

    UK Coronavirus Cancer Monitoring Project (UK CCMP)

    The National Health Service in the UK initiated the UK CCMP35 on March 18, 2020. This project aims to collect pertinent information from patients with cancer and COVID-19 and provide real-time daily updates to individual cancer centers for the facilitation of informed decision-making. In a preliminary analysis of 800 patients with COVID-19 and cancer, a mortality rate of 28% was reported, which was largely associated with older age, male sex, and a higher number of comorbidities. The UK CCMP analysis did not find any significant association between cancer treatment within 4 weeks and mortality among those with cancer and COVID-19.35

    Thoracic Cancers International COVID-19 Collaboration (TERAVOLT)

    The TERAVOLT36 is one of the first global registries aimed at understanding COVID-19 among patients with thoracic cancers, including small cell lung cancer, non–small cell lung cancer, mesothelioma, carcinoid or neuroendocrine tumors of thoracic origin, and thymic epithelial tumors. Garassino et al36 presented initial data from the TERAVOLT registry at the 2020 annual meeting of the American Association for Cancer Research; these data were collected from 200 patients who were primarily from European centers. Of those, 151 patients (76%) had non–small cell lung cancer, 148 patients (74%) were receiving active treatment for cancer, 152 patients (76%) required hospitalization, and 66 patients (33%) with thoracic cancer died. Previous or current smoking, older age (>65 years), treatment with chemotherapy alone, and the presence of comorbidities were independent factors significantly associated with an increased risk of death.36 Updated data from 400 patients were subsequently reported at the 2020 annual meeting of the American Society of Clinical Oncology (ASCO), revealing a 35.5% mortality rate.37 In addition, in September 2020, results from a study including a global population of 1012 patients38 were presented at the 2020 virtual conference of the European Society for Medical Oncology, confirming a mortality rate of 32% among 326 patients with thoracic cancer and COVID-19. An ECOG performance status of 2 or higher, older age (>65 years), smoking history, stage IV disease, receipt of more than 10 mg of steroid medication per day, treatment with chemotherapy alone, and no treatment were all found to be significantly associated with worse outcomes.38 It is notable that no specific information was available regarding the reasons for steroid use (ie, whether steroid medications were initiated for the treatment of certain comorbid conditions, such as chronic obstructive pulmonary disease or autoimmune disorders, or to reduce the severity of illness). Therefore, given the unmeasured and potential unknown sociodemographic confounders, randomized clinical trials remain the criterion standard to provide definitive answers regarding the efficacy of COVID-19 therapies, such as corticosteroid medications.

    American Society of Clinical Oncology

    The ASCO registry aims to capture longitudinal data regarding the consequences of COVID-19 for patient care and outcomes during and after the acute phase of COVID-19 among patients who are receiving active cancer treatment or who are disease-free within 12 months of surgical resection. A regularly updated data dashboard39 summarizes demographic, cancer, and COVID-19 information of cases in the registry.40 As of June 1, 2021, the registry contained data on 3747 patients that were submitted from 60 practices; more than 60% of these patients were receiving drug-based therapy at the time of their COVID-19 diagnosis. The registry is collecting robust follow-up information for up to 2 years after COVID-19 diagnosis, including information on disruptions in cancer treatment, long-haul symptoms of COVID-19, and vaccination status. Initial results were presented at the ASCO 2021 annual meeting,41 and further analysis is ongoing. This registry provides financial support to sites for the costs associated with inputting data in the registry.

    American Society of Hematology Research Collaborative (ASH RC)

    The ASH RC COVID-19 registry is a global public reference tool that captures data on individuals who have been diagnosed with a hematologic condition (past or present), received a positive test result for COVID-19, and/or experienced a post–COVID-19 hematologic complication. A regularly updated data dashboard42 summarizes demographic, cancer, comorbidity, and COVID-19 information of cases in the registry. As of June 1, 2021, the registry contained data on 1095 patients with hematologic conditions, including 1013 patients with hematologic cancer. The nearly real-time observational summaries for the ASH RC COVID-19 registry are available on its public-facing data dashboard.43 A unique feature of the ASH RC COVID-19 registry is its inclusion of patients younger than 5 years to older than 90 years. More than 50% of patients in the registry are non-White and reside in countries across the globe. The most common comorbidities documented were hypertension and diabetes. The highest mortality was found among those older than 70 years.

    Initial results from the first 250 patients from 74 sites who were included in the ASH RC COVID-19 registry were published in December 2020.44 Diverse hematologic cancers were well represented. The overall mortality rate was 28% (95% CI, 23%-34%), with the greatest risk observed among those with older age, underlying hematologic cancer with a physician-estimated survival prognosis of less than 12 months, and relapsed/refractory disease. In some cases, death occurred after a decision to forgo admission to the intensive care unit in favor of a palliative approach. The use of COVID-19–directed therapies throughout the entire cohort was common. Updated results on 656 patients from the ASH RC COVID 19 registry were presented at the 2020 ASH annual meeting.45 A continued high risk of death (20% overall mortality rate) among patients with hematologic cancer and COVID-19 was observed, with a 33% mortality rate among those who were hospitalized with COVID-19.

    Hematology Oncology in Latin America (HOLA)

    The HOLA COVID-19 study,46 initiated on August 4, 2020, is an international collaboration composed of Latinx oncology professionals and specialists from countries in Latin America, the Caribbean, and the US. It is the largest effort focusing on the South American continent. Approximately 704 specialists responded to a survey over a 4-week period as part of a cross-sectional study to understand the pandemic’s consequences for cancer care in Latin American countries.

    COVID-19 Outcomes Registries in Immunocompromised Individuals Australia (CORIA)

    The CORIA47 is an observational cohort study of immunosuppressed populations, including patients with cancer and transplant recipients who have received positive test results for COVID-19. A total of 30 institutions across Australia are part of the CORIA registry, and the study plans to enroll approximately 1000 patients.

    European Society for Medical Oncology COVID-19 Care (ESMOCoCARE)

    The ESMOCoCARE registry48 is an international collaborative project comprising cancer centers and organizations from across Europe and around the world, focusing mainly on Europe and Asia. The registry covers the heterogeneity of European, Asian, and African countries. A partnership between ESMOCoCARE and the CCC19 has been established, and the CCC19 has shared its common data dictionary with the aim of performing a final pooled analysis. This worldwide collaboration should enable the inclusion of larger samples to address important issues related to granular questions about COVID-19 and cancer care. Given the complexity of general data protection regulations for registries in the European Union, which remained in effect during the COVID-19 pandemic, the first results from a group of more than 1500 patients were delayed and will be presented during the ESMO annual meeting in September 2021.49

    Dutch Oncology COVID-19 Consortium (DOCC)

    The DOCC, a national registry in the Netherlands, analyzed data from 351 patients with COVID-19 and cancer in its first analysis.50 The main cancer diagnoses among patients with COVID-19 were non–small cell lung cancer, breast cancer, and chronic lymphocytic leukemia. An overall mortality rate of 32.5% (114 of 351 patients) was reported, and the mortality rate was highest among patients with hematologic and lung cancers. Other independent risk factors associated with fatal outcomes included male sex, older age (>65 years), comorbidities, and active cancer.

    NCI COVID-19 in Cancer Patients Study (N-CCaPS)

    The N-CCaPS is a prospective observational cancer study with a planned accrual goal of 2000 patients with active cancer requiring therapy who have been recently diagnosed with COVID-19.51 This study is being conducted through the National Cancer Institute (NCI) Experimental Clinical Trials Network, the NCI National Clinical Trials Network, and the NCI Community Oncology Research Program. Notably, the collection of blood samples at baseline and throughout treatment will allow for extensive correlative laboratory analyses, including genome-wide association studies, characterization of cytokine changes, serologic testing to assess short-term and long-term immunity associated with SARS-CoV-2 infection, and COVID-19 vaccination status and coagulation parameters.

    Myeloma Crowd Research Initiative (MCRI)

    Registries containing patients with specific types of cancer include the MCRI COVID-19 study (also called the COVID-19 Myeloma Patient Study),52 which is part of the HealthTree platform.53 This registry is an innovative patient-focused tool designed to collect data on patients diagnosed with COVID-19 who have multiple myeloma or precursor conditions. This study is being led by myeloma researchers in the US in collaboration with the nonprofit organization, Myeloma Crowd.52 The Multiple Myeloma Research Foundation and the International Myeloma Society have also initiated similar registries for patients with multiple myeloma.54

    The International Myeloma Society published its first results from a data set comprising 650 patients with myeloma, 96% of whom had multiple myeloma and 54% of whom were receiving first-line therapy for treatment of the disease.55 High but variable mortality rates ranging from 27% to 57% (mean, 33%) were documented among patients based on the location of the medical facility at the time of hospitalization. A multivariable logistic regression analysis revealed that age, high-risk disease, kidney involvement, and suboptimal multiple myeloma control were independently associated with adverse outcomes among patients with concurrent COVID-19.

    Center for International Blood and Marrow Transplant Research (CIBMTR)

    The CIBMTR56 is an international joint initiative comprising 234 participating centers (188 in the US and 46 outside of the US). The goal of this initiative is to collect data to evaluate the consequences of COVID-19 for outcomes among patients with autologous and allogeneic hematopoietic stem cell transplants. As of June 7, 2021, data on 3224 patients with confirmed COVID-19 were available. Results from an analysis of 318 patients from the CIBMTR registry revealed that an age of 50 years or older (HR, 2.53; 95% CI, 1.16-5.52), male sex (HR, 3.53; 95% CI, 1.44-8.67), and COVID-19 diagnosis within 1 year of transplant (HR, 2.67; 95% CI, 1.33-5.36) were associated with a higher risk of death among recipients of allogeneic hematopoietic stem cell transplants.56 Among these transplant recipients, the presence of lymphoma was associated with a higher risk of death compared with plasma cell disorder or myeloma (HR, 2.41; 95% CI,1.08-5.38). Frigault et al57 published data suggesting that early and limited receipt of tocilizumab therapy (an interleukin-6 receptor inhibitor) may not be associated with increases in the overall risk of infection among patients who are substantially immunocompromised.

    Other Efforts

    Similar to the efforts described above, the American College of Surgeons is collecting data on adult patients, including those with cancer, those planning to undergo surgery, and those diagnosed with COVID-19.58 The Alliance for Clinical Trials in Oncology is also developing a data repository based on NCI policies,59 but these data are available for alliance member sites only. An international cancer control partnership established a joint initiative between the International Agency for Research on Cancer, the Global Initiative for Cancer Registry Development, and the International Association of Cancer Registries, inviting cancer registries across the globe to respond to an online survey assessing the impact of the pandemic for the cancer care system.59 The results of the survey had not yet been published at the time of the present review.

    Discussion

    The results from registry efforts have allowed us to understand several consequences of COVID-19 for patients with cancer. First, the 30-day all-cause mortality rate among patients with cancer and COVID-19 was high, with estimates ranging from 13% to 57%. Second, overall factors that were consistently associated with mortality across the registries included age, sex, and number of comorbidities (Table 2). Third, cancer-specific factors that were consistently identified across registries as being associated with high mortality were thoracic cancer, hematologic cancer, low ECOG performance status, and active and progressive cancer (Table 2). Fourth, registries with large samples revealed additional vulnerabilities in this large patient population that were associated with higher mortality, including race, ethnicity, and certain laboratory parameters (eg, hypoalbuminemia and lymphopenia). Fifth, identification of the benefits of convalescent plasma and remdesivir therapies for the treatment of COVID-19 has been suggested among patients with cancer, especially those with hematologic cancer. These results may provide context and hypotheses for researchers to design prospective studies and/or randomized clinical trials for this vulnerable subgroup.

    Limitations

    This study has limitations. By design, registries are observational and subject to chance, bias, and confounding. Most of these registries collect data abstracted from electronic health records, which may be limited in scope and coverage.60 Data on the severity of comorbidities, socioeconomic factors, insurance access and coverage, social factors associated with health, and COVID-19–associated health information that are managed outside of the reporting institution may be missing. In addition, long-term outcome data may be lacking in some registries. Given the heterogeneity and wide range of variables being collected by various registries using nonhomogeneous and sometimes inconsistent measures, assessing the true associations between specific clinical elements remains a challenge.

    Another major inherent limitation of registry-based studies is the potential for selection bias; all registries, with the exception of the CIBMTR, which has federally mandated reporting, could best be considered to contain data from convenience samples. For example, some registry cohorts may have a selection bias toward hospitalized patients, which could overestimate mortality. Although most registries have taken steps to prevent internally duplicated data entry, the possibility of duplicated data remains, particularly across registries. A heterogeneous patient population with missing or inconsistently available cancer-associated and noncancer-associated confounding factors still limits the findings of many studies. A potential solution for sample size limitations is the performance of a carefully conducted meta-analysis and the potential merging of data from different cancer registries to create a meta-cohort (subject to multivariate adjustments). However, data harmonization among disparate variables collected is a considerable challenge. None of the registries has been able to collect comprehensive data on social factors associated with health, which may play an important part in the observed disparities among patients with COVID-19.5

    Conclusions and Moving Forward

    Most registries are still in the process of collecting and analyzing data; hence, the available results are best considered preliminary. Consistent collection and reporting of clinical parameters along with common data elements and standardized definitions will be instrumental in attaining an improved understanding. Furthermore, well-designed randomized clinical trials are necessary to achieve evidence-based conclusions with a higher degree of reliability.61 Therefore, an initiative is needed to promote active collaboration between different registries to improve the quality and consistency of information.

    The COVID-19 pandemic has allowed us to identify potential approaches to better handle any future health crisis. Although a robust global response to the COVID-19 pandemic occurred, we found that because of the variation in inclusion criteria among most registries (which were sometimes limited by disease groups or location), there could be a potential for overlap of information, producing data duplication or redundancy in these scientific efforts. Moving forward, concerted standardized efforts, in which individual registries come together to develop a common mechanism for consistent data collection and reporting, may provide faster, more accurate, and more robust results for clinical implementation. In addition, given the background of the current pandemic, there is a need to identify factors associated with adverse outcomes among minority populations and actively address them to prevent similar occurrences in any future pandemic.

    Data from the registry efforts help to address 1 piece of a puzzle that will need to be simultaneously solved through well-designed clinical trials to develop high-level evidence.14 The COVID-19 pandemic response has highlighted opportunities to collaborate with colleagues across disciplines and geographic boundaries and strengthen the health care system to continue delivering the highest quality of care to patients.

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    Article Information

    Accepted for Publication: July 1, 2021.

    Published Online: September 2, 2021. doi:10.1001/jamaoncol.2021.4083

    Corresponding Author: Michael A. Thompson, MD, PhD, Aurora Cancer Care Center, Advocate Aurora Health, 2900 W Oklahoma Ave, Milwaukee, WI 53215 (michael.thompson2@aah.org).

    Author Contributions: Dr Thompson had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Drs Desai and Mohammed were co–senior authors.

    Concept and design: Desai, Mohammed, Duma, Lyman, Mishra, Rini, Peters, Warner, Wood, Thompson.

    Acquisition, analysis, or interpretation of data: Desai, Mohammed, Garassino, Hicks, Kuderer, Lyman, Pinato, Peters, Whisenant, Thompson.

    Drafting of the manuscript: Desai, Mohammed, Duma, Kuderer, Lyman, Pinato, Rini, Peters, Wood, Thompson.

    Critical revision of the manuscript for important intellectual content: All authors.

    Statistical analysis: Peters.

    Obtained funding: Warner.

    Administrative, technical, or material support: Mishra, Pinato, Rini, Peters, Thompson.

    Supervision: Desai, Garassino, Kuderer, Warner, Wood, Thompson.

    Conflict of Interest Disclosures: Dr Duma reported serving as a consultant and/or advisor for AstraZeneca, Boehringer Ingelheim, Bristol Myers Squibb, Inivata, NeoGenomics Laboratories, and Pfizer outside the submitted work. Dr Garassino reported receiving personal fees from AstraZeneca, Bristol Myers Squibb, Janssen Pharmaceuticals, Merck & Co, Mirati Therapeutics, Pfizer, Roche, and Takeda Pharmaceutical outside the submitted work. Dr Hicks reported receiving grants from Gilead Sciences outside the submitted work. Dr Kuderer reported receiving personal fees from Amgen, BeyondSpring, Bristol Myers Squibb, Celldex Therapeutics, Invitae, Janssen Pharmaceuticals, Sandoz, Spectrum Pharmaceuticals, and Total Health Pharmaceuticals; personal fees (directed to her husband) from G1 Therapeutics, Jazz Pharmaceuticals, Partner Therapeutics, and Seattle Genetics; and grants (directed to her husband) from Samsung outside the submitted work. Dr Lyman reported receiving grants (directed to the Fred Hutchinson Cancer Research Center) from Amgen and serving as a consultant for BeyondSpring, Bristol Myers Squibb, G1 Therapeutics, Jazz Pharmaceuticals, Merck & Co, Partner Therapeutics, Sandoz, and Seattle Genetics outside the submitted work. Dr Mishra reported receiving grants (directed to the Vanderbilt-Ingram Cancer Center) from the National Cancer Institute and remuneration for authorship of articles from National Geographic during the conduct of the study. Dr Pinato reported receiving grants from Bristol Myers Squibb and Merck Sharp & Dohme and personal fees from AstraZeneca, Bayer, Bristol Myers Squibb, Da Volterra, Eisai, H3 Biomedicine, MiNA Therapeutics, Roche, and ViiV Healthcare outside the submitted work. Dr Peters reported receiving grants (via institutional financial support for clinical trials in which she was an investigator) from Amgen, AstraZeneca, Biodesix, Boehringer Ingelheim, Bristol Myers Squibb, Clovis Oncology, GlaxoSmithKline, Illumina, Eli Lilly and Company, Merck Sharp & Dohme, Merck Serono, Mirati Therapeutics, Novartis, Pfizer, Phosplatin Therapeutics, and Roche/Genentech; serving as a consultant and/or advisor for AbbVie, Amgen, AstraZeneca, Bayer, BeiGene, Biocartis, Boehringer Ingelheim, Bristol Myers Squibb, Clovis Oncology, Daiichi Sankyo, Debiopharm Group, ecancer.org, Eli Lilly and Company, Elsevier, Foundation Medicine, Illumina, Imedex, IQVIA, Incyte, Janssen Pharmaceuticals, Medscape, Merck Sharp & Dohme, Merck Serono, Merrimack, Novartis, Oncology Education, PharmaMar, Phosplatin Therapeutics, Pfizer, Physicians’ Education Resource, Prime Pharma, Regeneron Pharmaceuticals, RMEI Medical Education, Roche/Genentech, RTP Pharma, Sanofi, Seattle Genetics, and Takeda Pharmaceutical; and receiving honoraria (via fees to her institution) for lectures at organized public events from AstraZeneca, Boehringer Ingelheim, Bristol Myers Squibb, ecancer.org, Eli Lilly and Company, Illumina, Imedex, Medscape, Merck Sharp & Dohme, Novartis, Pfizer, Physicians’ Education Resource, Prime Pharma, Roche/Genentech, RTP Pharma, Sanofi, and Takeda Pharmaceutical outside the submitted work. Dr Warner reported receiving grants from the National Cancer Institute during the conduct of the study; personal fees from Roche and Westat, nonfinancial support from IBM Watson Health, and ownership of HemOnc.org outside the submitted work. Dr Wood reported receiving grants from Pfizer outside the submitted work. Dr Thompson reported receiving personal fees from Adaptive Biotechnologies, Bristol Myers Squibb, Elsevier ClinicalPath, Epizyme, Illumina, Takeda Pharmaceutical, and UpToDate; nonfinancial support from Syapse; and serving on the advisory board of Doximity outside the submitted work. No other disclosures were reported.

    Funding/Support: This work was supported by grant P30 CA068485 from the Vanderbilt-Ingram Cancer Center (Drs Mishra, Warner, and Rini), grant PS3416 from the Wellcome Trust Strategic Fund (Dr Pinato), funding from the National Institute for Health Research (NIHR) Imperial Biomedical Research Centre (Dr Pinato), and infrastructure support from the Cancer Research UK Imperial Centre. The views expressed are those of the authors and not necessarily those of the NIHR or the UK Department of Health and Social Care.

    Role of the Funder/Sponsor: The funding organizations had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

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