Estimated impact of the COVID-19 pandemic on cancer services and excess 1-year mortality in people with cancer and multimorbidity: near real-time data on cancer care, cancer deaths and a population-based cohort study
Open accessPublished version of a preprint
Abstract
Background: Cancer and multiple non-cancer conditions are considered by the Centers for Disease Control and Prevention (CDC) as high risk conditions in the COVID-19 emergency. Professional societies have recommended changes in cancer service provision to minimize COVID-19 risks to cancer patients and health care workers. However, we do not know the extent to which cancer patients, in whom multi-morbidity is common, may be at higher overall risk of mortality as a net result of multiple factors including COVID-19 infection, changes in health services, and socioeconomic factors. Methods: We report multi-center, weekly cancer diagnostic referrals and chemotherapy treatments until April 2020 in England and Northern Ireland. We analyzed population-based health records from 3,862,012 adults in England to estimate 1-year mortality in 24 cancer sites and 15 non-cancer comorbidity clusters (40 conditions) recognized by CDC as high-risk. We estimated overall (direct and indirect) effects of COVID-19 emergency on mortality under different Relative Impact of the Emergency (RIE) and different Proportions of the population Affected by the Emergency (PAE). We applied the same model to the US, using Surveillance, Epidemiology, and End Results (SEER) program data. Results: Weekly data until April 2020 demonstrate significant falls in admissions for chemotherapy (45-66% reduction) and urgent referrals for early cancer diagnosis (70-89% reduction), compared to pre-emergency levels. Under conservative assumptions of the emergency affecting only people with newly diagnosed cancer (incident cases) at COVID-19 PAE of 40%, and an RIE of 1.5, the model estimated 6,270 excess deaths at 1 year in England and 33,890 excess deaths in the US. In England, the proportion of patients with incident cancer with ≥1 comorbidity was 65.2%. The number of comorbidities was strongly associated with cancer mortality risk. Across a range of model assumptions, and across incident and prevalent cancer cases, 78% of excess deaths occur in cancer patients with ≥1 comorbidity. Conclusion: We provide the first estimates of potential excess mortality among people with cancer and multimorbidity due to the COVID-19 emergency and demonstrate dramatic changes in cancer services. To better inform prioritization of cancer care and guide policy change, there is an urgent need for weekly data on cause-specific excess mortality, cancer diagnosis and treatment provision and better intelligence on the use of effective treatments for comorbidities.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the UK, cancer deaths increased about 10% at the height of the April 2020 lockdown; however, more recent fluctuations in cancer mortality remain unclear.
“In the UK, cancer deaths increased about 10% at the height of the April 2020 lockdown; however, more recent fluctuations in cancer mortality remain unclear (Lai et al., 2020).”
From Direct and indirect mortality impacts of the COVID-19 pandemic in the United States, March 1, 2020 to January 1, 2022 (2023) · cites this paper as Lai et al., 2020
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Factors associated with COVID-19-related death using OpenSAFELY
Williamson, E. J., Walker, A. J., Bhaskaran, K., Bacon, S., Bates, C., Morton, C. E., Curtis, H. J., Mehrkar, A., Evans, D., Inglesby, P., et al. (2020) · Nature · doi:10.1038/s41586-020-2521-4 · Cited by 6,674 · see citing works
Collaborative, T. O., Williamson, E., Walker, A. J., Bhaskaran, K., Bacon, S., Bates, C., Morton, C. E., Curtis, H. J., Mehrkar, A., Evans, D., et al. (2020) · doi:10.1101/2020.05.06.20092999 · Cited by 6,674 · see citing works
Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China
Liang, W., Guan, W., Chen, R., Wang, W., Li, J., Xu, K., Li, C., Ai, Q., Lu, W., Liang, H., et al. (2020) · The Lancet Oncology · doi:10.1016/s1470-2045(20)30096-6 · Cited by 4,384 · see citing works
Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study
Kuderer, N. M., Choueiri, T. K., Shah, D. P., Shyr, Y., Rubinstein, S. M., Rivera, D. R., Shete, S., Hsu, C.-Y., Desai, A., de Lima Lopes, G., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)31187-9 · Cited by 1,726 · see citing works
Rapsomaniki, E., Timmis, A., George, J., Pujades-Rodriguez, M., Shah, A. D., Denaxas, S., White, I. R., Caulfield, M. J., Deanfield, J. E., Smeeth, L., et al. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60685-1 · Cited by 1,643 · see citing works
Self-citationDai, M., Liu, D., Liu, M., Zhou, F., Li, G., Chen, Z., Zhang, Z., You, H., Wu, M., Zheng, Q., et al. (2020) · Cancer Discovery · doi:10.1158/2159-8290.cd-20-0422 · Cited by 1,589 · see citing works
Type 2 diabetes and incidence of cardiovascular diseases: a cohort study in 1.9 million people
Shah, A. D., Langenberg, C., Rapsomaniki, E., Denaxas, S., Pujades-Rodriguez, M., Gale, C. P., Deanfield, J., Smeeth, L., Timmis, A., & Hemingway, H. (2015) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(14)70219-0 · Cited by 1,225 · see citing works
Self-citationValidation and validity of diagnoses in the General Practice Research Database: a systematic review
Herrett, E., Thomas, S. L., Schoonen, W. M., Smeeth, L., & Hall, A. J. (2010) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2009.03537.x · Cited by 1,109 · see citing works
Lee, L. Y., Cazier, J.-B., Angelis, V., Arnold, R., Bisht, V., Campton, N. A., Chackathayil, J., Cheng, V. W., Curley, H. M., Fittall, M. W., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)31173-9 · Cited by 1,103 · see citing works
Self-citationSARS-CoV-2 Transmission in Patients With Cancer at a Tertiary Care Hospital in Wuhan, China
Yu, J., Ouyang, W., Chua, M. L. K., & Xie, C. (2020) · JAMA Oncology · doi:10.1001/jamaoncol.2020.0980 · Cited by 1,062 · see citing works
Estimating the burden of SARS-CoV-2 in France
Salje, H., Tran Kiem, C., Lefrancq, N., Courtejoie, N., Bosetti, P., Paireau, J., Andronico, A., Hozé, N., Richet, J., Dubost, C.-L., et al. (2020) · Science · doi:10.1126/science.abc3517 · Cited by 1,038 · see citing works
Social networks, social support, and survival after breast cancer diagnosis
Kroenke, C. H., Kubzansky, L. D., Schernhammer, E. S., Holmes, M. D., & Kawachi, I. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2005.04.2846 · Cited by 792 · see citing works
The untold toll—the pandemic's effects on patients without covid-19
Rosenbaum, L. (2020) · New England Journal of Medicine · doi:10.1056/nejmms2009984 · Cited by 698 · see citing works
Collateral damage: the impact on outcomes from cancer surgery of the COVID-19 pandemic
Sud, A., Jones, M. E., Broggio, J., Loveday, C., Torr, B., Garrett, A., Nicol, D. L., Jhanji, S., Boyce, S., Gronthoud, F. A., et al. (2020) · Annals of Oncology · doi:10.1016/j.annonc.2020.05.009 · Cited by 553 · see citing works
Self-citationBanerjee, A., Pasea, L., Harris, S., Gonzalez-Izquierdo, A., Torralbo, A., Shallcross, L., Noursadeghi, M., Pillay, D., Sebire, N., Holmes, C., et al. (2020) · The Lancet · doi:10.1016/s0140-6736(20)30854-0 · Cited by 518 · see citing works
Self-citationCompleteness and usability of ethnicity data in UK-based primary care and hospital databases
Mathur, R., Bhaskaran, K., Chaturvedi, N., Leon, D. A., van Staa, T. P., Grundy, E. M. D., & Smeeth, L. L. (2013) · Journal of Public Health · doi:10.1093/pubmed/fdt116 · Cited by 464 · see citing works
Elovainio, M., Hakulinen, C., Pulkki-Råback, L., Virtanen, M., Josefsson, K., Jokela, M., Vahtera, J., & Kivimäki, M. (2017) · The Lancet Public Health · doi:10.1016/s2468-2667(17)30075-0 · Cited by 411 · see citing works
Cancer, COVID-19 and the precautionary principle: prioritizing treatment during a global pandemic
Hanna, T. P., Evans, G. A., & Booth, C. M. (2020) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-020-0362-6 · Cited by 402 · see citing works
Longer-run Economic Consequences of Pandemics
Jordà, Ò., Singh, S. P., & Taylor, A. M. (2020) · National Bureau of Economic Research · doi:10.3386/w26934 · Cited by 361 · see citing works
Cancer guidelines during the COVID-19 pandemic
Burki, T. K. (2020) · The Lancet Oncology · doi:10.1016/s1470-2045(20)30217-5 · Cited by 330 · see citing works
Kuan, V., Denaxas, S., Gonzalez-Izquierdo, A., Direk, K., Bhatti, O., Husain, S., Sutaria, S., Hingorani, M., Nitsch, D., Parisinos, C. A., et al. (2019) · The Lancet Digital Health · doi:10.1016/s2589-7500(19)30012-3 · Cited by 305 · see citing works
Self-citationDenaxas, S., George, J., Herrett, E. L., Shah, A. D., Kalra, D., Hingorani, A. D., Mika Kivimaki, B., Timmis, A., Smeeth, L. L., & Hemingway, H. (2012) · International Journal of Epidemiology · doi:10.1093/ije/dys188 · Cited by 228 · see citing works
Self-citationUK phenomics platform for developing and validating electronic health record phenotypes: CALIBER
Denaxas, S., González-Izquierdo, A., Direk, K., Fitzpatrick, N. K., Fatemifar, G., Banerjee, A., Dobson, R., Howe, L. J., Kuan, V., Lumbers, R. T., et al. (2019) · Journal of the American Medical Informatics Association · doi:10.1093/jamia/ocz105 · Cited by 227 · see citing works
Self-citationThomson, D. J., Palma, D. A., Gückenberger, M., et al. (2020) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2020.04.016 · Cited by 209 · see citing works
Maruthappu, M., Watkins, J. A., Noor, A. M., Williams, C., Ali, R., Sullivan, R. J., Zeltner, T. B., & Atun, R. A. (2016) · The Lancet · doi:10.1016/s0140-6736(16)00577-8 · Cited by 201 · see citing works
Self-citationAmerican Society for Radiation Oncology
Pritchard, J. (2015) · doi:10.4135/9781483345758.n37 · Cited by 189 · see citing works
Comorbid chronic diseases and cancer diagnosis: disease-specific effects and underlying mechanisms
Renzi, C., Kaushal, A., Emery, J. D., Hamilton, W. T., Neal, R. D., Rachet, B., Rubin, G. P., Singh, H., Walter, F. M., de Wit, N. J., et al. (2019) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-019-0249-6 · Cited by 184 · see citing works
Self-citationExcess deaths in people with cardiovascular diseases during the COVID-19 pandemic
Banerjee, A., Chen, S., Pasea, L., Lai, A. G., Katsoulis, M., Denaxas, S., Nafilyan, V., Williams, B., Wong, W. K., Bakhai, A., et al. (2020) · European Journal of Preventive Cardiology · doi:10.1093/eurjpc/zwaa155 · Cited by 164 · see citing works
Self-citationBhaskaran, K., Forbes, H. J., Douglas, I., Leon, D. A., & Smeeth, L. L. (2013) · BMJ Open · doi:10.1136/bmjopen-2013-003389 · Cited by 156 · see citing works
George, J., Mathur, R., Shah, A. D., Pujades‐Rodríguez, M., Denaxas, S., Smeeth, L. L., Timmis, A., & Hemingway, H. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178945 · Cited by 97 · see citing works
Self-citationSARS-CoV-2 seroprevalence trends in healthy blood donors during the COVID-19 outbreak in Milan.
Valenti, L. V. C., Bergna, A., Pelusi, S., Facciotti, F., Lai, A., Tarkowski, M., Lombardi, A., Berzuini, A., Caprioli, F., Santoro, L., et al. (2021) · Blood transfusion · doi:10.2450/2021.0324-20 · Cited by 94 · see citing works
Self-citationPikoula, M., Quint, J. K., Nissen, F., Hemingway, H., Smeeth, L. L., & Denaxas, S. (2019) · BMC Medical Informatics and Decision Making · doi:10.1186/s12911-019-0805-0 · Cited by 88 · see citing works
Self-citationSARS-CoV-2 seroprevalence trends in healthy blood donors during the COVID-19 Milan outbreak
Valenti, L., Bergna, A., Pelusi, S., Facciotti, F., Lai, A., Tarkowski, M., Berzuini, A., Caprioli, F., Santoro, L., Baselli, G., et al. (2020) · doi:10.1101/2020.05.11.20098442 · Cited by 88 · see citing works
Self-citationMargulis, A. V., Fortuny, J., Kaye, J. A., Calingaert, B., Reynolds, M., Plana, E., McQuay, L. J., Atsma, W. J., Franks, B., de Vogel, S., et al. (2017) · Epidemiology · doi:10.1097/ede.0000000000000786 · Cited by 64 · see citing works
Pujades‐Rodríguez, M., Duyx, B., Thomas, S. L., Stogiannis, D., Rahman, A., Smeeth, L. L., & Hemingway, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151245 · Cited by 63 · see citing works
Self-citationThomson, D. J., Palma, D. A., Gückenberger, M., et al. (2020) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2020.04.019 · Cited by 52 · see citing works
Vrdoljak, E., Sullivan, R., & Lawler, M. (2020) · European Journal of Cancer · doi:10.1016/j.ejca.2020.04.001 · Cited by 44 · see citing works
Self-citationMargulis, A. V., Fortuny, J., Kaye, J. A., et al. (2018) · Epidemiology · doi:10.1097/ede.0000000000000856 · Cited by 13 · see citing works
Flagged first, then by citations
Research works printed but not linked: 2
- [10]National Institute for Health and Care Excellence COVID-19 rapid guideline: delivery of systemic anticancer treatments. Available: https://www.nice.org.uk/guidance/ng161/chapter/6-Prioritising-systemic-anticancer-treatments [Accessed 19 Apr 2020]. 33497155
- [15]Sud A, Jones ME, Broggio J, et al Collateral damage: the impact on outcomes from cancer surgery of the COVID-19 pandemic. Ann Oncol 2020; 31: 1065– 74. 10.1016/j.annonc.2020.05.009 32442581 PMC7237184 · DOI
Cited by
Sorted by citations
Challenges in creating herd immunity to SARS-CoV-2 infection by mass vaccination
Anderson, R. M., Vegvari, C., Truscott, J., & Collyer, B. S. (2020) · The Lancet · doi:10.1016/s0140-6736(20)32318-7 · Cited by 529 · see citing works
Excess mortality: the gold standard in measuring the impact of COVID-19 worldwide?
Beaney, T., Clarke, J. M., Jain, V., Golestaneh, A. K., Lyons, G., Salman, D., & Majeed, A. (2020) · Journal of the Royal Society of Medicine · doi:10.1177/0141076820956802 · Cited by 370 · see citing works
Lee, W.-E., Woo Park, S., Weinberger, D. M., Olson, D., Simonsen, L., Grenfell, B. T., & Viboud, C. (2023) · eLife · doi:10.7554/elife.77562 · Cited by 90 · see citing works
Cumulative burden of psychiatric disorders and self-harm across 26 adult cancers
Chang, W. H., & Lai, A. G. (2022) · Nature Medicine · doi:10.1038/s41591-022-01740-3 · Cited by 81 · see citing works
Self-citationMcCloskey, C., Ortega, M. T., Nair, S., Garcia, M. J., & Manevy, F. (2023) · PharmacoEconomics - Open · doi:10.1007/s41669-022-00361-3 · Cited by 66 · see citing works
“4%, respectively, which might have resulted in increased mortality rates in patients with cancer and multimorbidity [121].”
BackgroundSharma, J., Mahajan, A., Bakhshi, S., Patil, V., Verma, N., Radhakrishnan, V., Singh, A., Kayal, S., Seth, R., Pushpam, D., et al. (2022) · Cancer · doi:10.1002/cncr.33945 · Cited by 30 · see citing works
Rine, S., Lara, S. T., Bikomeye, J. C., Beltrán-Ponce, S., Kibudde, S., Niyonzima, N., Lawal, O. O., Mulamira, P., & Beyer, K. M. (2023) · Journal of Global Health · doi:10.7189/jogh.13.06048 · Cited by 16 · see citing works
- Authors
- Lai, A. G., Pasea, L., Banerjee, A., Hall, G., Denaxas, S., Chang, W. H., Katsoulis, M., Williams, B., Pillay, D., Noursadeghi, M., Linch, D., Hughes, D., Forster, M. D., Turnbull, C., Fitzpatrick, N. K., Boyd, K., Foster, G. R., Enver, T., Nafilyan, V., Humberstone, B., Neal, R. D., Cooper, M., Jones, M., Pritchard-Jones, K., Sullivan, R., Davie, C., Lawler, M., & Hemingway, H.
- Affiliations
- Health Data Research UK (GB)
- Barts Health NHS Trust (GB)
- University of Leeds (GB)
- The Alan Turing Institute (GB)
- University College London (GB)
- University College London Hospitals NHS Foundation Trust (GB)
- UCL Biomedical Research Centre (GB)
- Royal Free London NHS Foundation Trust (GB)
- Institute of Cancer Research (GB)
- Northern Ireland Cancer Network, Northern Ireland, UK
- Queen Mary University of London (GB)
- Office for National Statistics, London, UK
- Office for National Statistics (GB)
- DATA-CAN, Health Data Research UK hub for cancer hosted by UCLPartners, London, UK
- King's College London (GB)
- Queen's University Belfast (GB)
- Corresponding author
- Lai, Alvina G
- ORCID
- Lai, Alvina G
- Pasea, Laura
- Banerjee, Amitava
- Hall, Geoff
- Denaxas, Spiros
- Chang, Wai Hoong
- Katsoulis, Michail
- Williams, Bryan
- Pillay, Deenan
- Noursadeghi, Mahdad
- Linch, David
- Hughes, Derralynn
- Forster, Martin D
- Turnbull, Clare
- Fitzpatrick, Natalie K
- Foster, Graham R
- Enver, Tariq
- Nafilyan, Vahe
- Humberstone, Ben
- Neal, Richard D
- Jones, Monica
- Sullivan, Richard
- Lawler, Mark
- Hemingway, Harry
- Venue
- BMJ Open
- Publisher
- BMJ
- Published
- 2020-11
- Volume
- 10
- Issue
- 11
- Pages
- e043828
- ISSN
- 2044-6055 (ISSN-L)
- PMC
- PMC7674020
- OpenAlex
- W3098511379
- Cited by
- 447
- References
- 38
- Citations by year
- 2026: 16 · 2025: 22 · 2024: 32 · 2023: 70 · 2022: 126 · 2021: 117 · 2020: 60
- FWCI
- 33.68
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- BMJ Open (publishedVersion, cc-by)
- medRxiv (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- LSHTM Research Online (London School of Hygiene and Tropical Medicine) (acceptedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- UCL Discovery (University College London) (submittedVersion)
- Research Portal (King's College London) (submittedVersion, other-oa)
- HighWire Press Open Archive (submittedVersion)
- Research Portal (Queen's University Belfast) (submittedVersion, cc-by)
- Greater South Information System
- Funders
- Health Data Research UK - DATA-CAN (MC_PC_19006)
- Wellcome Trust (204841/Z/16/Z)
- National Institute for Health Research University College London Hospitals Biomedical Research Centre (BRC714/HI/RW/101440)
- National Institute for Health Research Great Ormond Street Hospital Biomedical Research Centre (19RX02)
- Topics
- Health Sciences › Medicine › Oncology › COVID-19 and healthcare impacts
- Health Sciences › Medicine › Oncology › Global Cancer Incidence and Screening
- Physical Sciences › Mathematics › Modeling and Simulation › COVID-19 epidemiological studies
- Keywords
- COVID-19 pandemic, cancer care, excess mortality, multimorbidity, urgent cancer referral, cancer mortality, indirect mortality, healthcare disruption, general practitioner services
- MeSH terms
- Multimorbidity, COVID-19, SARS-CoV-2, Adult, Cause of Death, England, Female, Follow-Up Studies, Humans, Male, Middle Aged, Neoplasms, Population Surveillance, Time Factors, Models, Statistical, Survival Rate, Pandemics
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
