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

Alvina G Lai, Laura Pasea, Amitava Banerjee, Geoff Hall, Spiros Denaxas, Wai Hoong Chang, Michail Katsoulis, Bryan Williams, Deenan Pillay, Mahdad Noursadeghi, David Linch, Derralynn Hughes, Martin D Forster, Clare Turnbull, Natalie K Fitzpatrick, Kathryn Boyd, Graham R Foster, Tariq Enver, Vahe Nafilyan, Ben Humberstone, Richard D Neal, Matt Cooper, Monica Jones, Kathy Pritchard-Jones, Richard Sullivan, Charlie Davie, Mark Lawler, Harry Hemingway, Alvina G Lai, Laura Pasea, Amitava Banerjee, Geoff Hall, Spiros Denaxas, Wai Hoong Chang, Michail Katsoulis, Bryan Williams, Deenan Pillay, Mahdad Noursadeghi, David Linch, Derralynn Hughes, Martin D Forster, Clare Turnbull, Natalie K Fitzpatrick, Kathryn Boyd, Graham R Foster, Tariq Enver, Vahe Nafilyan, Ben Humberstone, Richard D Neal, Matt Cooper, Monica Jones, Kathy Pritchard-Jones, Richard Sullivan, Charlie Davie, Mark Lawler, Harry Hemingway

Abstract

Objectives: To estimate the impact of the COVID-19 pandemic on cancer care services and overall (direct and indirect) excess deaths in people with cancer.

Methods: We employed near real-time weekly data on cancer care to determine the adverse effect of the pandemic on cancer services. We also used these data, together with national death registrations until June 2020 to model deaths, in excess of background (pre-COVID-19) mortality, in people with cancer. Background mortality risks for 24 cancers with and without COVID-19-relevant comorbidities were obtained from population-based primary care cohort (Clinical Practice Research Datalink) on 3 862 012 adults in England.

Results: Declines in urgent referrals (median=-70.4%) and chemotherapy attendances (median=-41.5%) to a nadir (lowest point) in the pandemic were observed. By 31 May, these declines have only partially recovered; urgent referrals (median=-44.5%) and chemotherapy attendances (median=-31.2%). There were short-term excess death registrations for cancer (without COVID-19), with peak relative risk (RR) of 1.17 at week ending on 3 April. The peak RR for all-cause deaths was 2.1 from week ending on 17 April. Based on these findings and recent literature, we modelled 40% and 80% of cancer patients being affected by the pandemic in the long-term. At 40% affected, we estimated 1-year total (direct and indirect) excess deaths in people with cancer as between 7165 and 17 910, using RRs of 1.2 and 1.5, respectively, where 78% of excess deaths occured in patients with ≥1 comorbidity.

Conclusions: Dramatic reductions were detected in the demand for, and supply of, cancer services which have not fully recovered with lockdown easing. These may contribute, over a 1-year time horizon, to substantial excess mortality among people with cancer and multimorbidity. It is urgent to understand how the recovery of general practitioner, oncology and other hospital services might best mitigate these long-term excess mortality risks.

Keywords: COVID-19; health informatics; oncology.

Conflict of interest statement

Competing interests: ML has received honoraria from Pfizer, EMD Serono and Roche for presentations unrelated to this research, and an unrestricted educational grant from Pfizer for research unrelated to the research presented in this paper. AB has received research funding from AstraZeneca. MF has received research funding from AstraZeneca, Boehringer Ingelheim, Merck and MSD and honoraria from Achilles, AstraZeneca, Bayer, Boehringer Ingelheim, Bristol-Meyers Squibb, Celgene, Guardant Health, Merck, MSD, Nanobiotix, Novartis, Pharmamar, Roche and Takeda for advisory roles or presentations unrelated to this research. GF receives funding from companies that manufacture drugs for hepatitis C virus (AbbVie, Gilead, MSD) and is a consultant for GSK, Arbutus and Shionogi in areas unrelated to this research.

© Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY. Published by BMJ.

Figures

Figure 1
Figure 1
Weekly hospital data (January 2019–June 2020) on changes in urgent referrals and chemotherapy clinic attendance from eight hospitals in the UK mapped to phases of the pandemic. Weekly changes from January 2020 to June 2020 were mapped to phases of the pandemic. Weekly values were plotted as percentage increase or decrease relative to the 2019 average. The data for Northern Ireland include five health and social care trusts (HSCs) that cover all health service provisions in Northern Ireland: Belfast HSC, Northern HSC, South Eastern HSC, Southern HSC and Western HSC. Vertical dotted lines indicate the Christmas bank holiday.
Figure 2
Figure 2
Office for National Statistics data on weekly registrations of deaths in the England and Wales from 3 January 2020 to 15 May 2020. (A) Upper panel indicates the number of weekly deaths. (B) Lower panel indicates weekly changes in relative risk estimates calculated by comparing the current weekly deaths to 5-year weekly averages. Dates indicate week ending on a particular date.
Figure 3
Figure 3
Estimated total (direct and indirect) excess deaths by cancer site over a 1-year period. (A) 1-year mortality for incident and prevalent cancers. The whiskers are 95% CIs. (B) Total excess deaths were scaled up to the population of England aged 30+ consisting of 35 million individuals using England mortality estimates for both incident and prevalent cancers combined. We estimated direct excess deaths at a 10% infection rate. We estimated total (direct and indirect) excess deaths for 40% (10% infected, 30% affected) and 80% (10% infected, 70% affected) of the population.
Figure 4
Figure 4
Total (direct and indirect) excess deaths for both incident and prevalent cancers by cancer site and number of comorbidities over a 1-year period. Stacked bar chart indicates the proportion of individuals with 0, 1, 2 and 3+ comorbidities by cancer site. We estimated total excess deaths for 40% (10% infected, 30% affected) of the population. Total excess deaths were scaled up to the population of England aged 30+ consisting of 35 million individuals using England mortality estimates for both incident and prevalent cancers combined.

References

    1. Banerjee A, Pasea L, Harris S, et al. . Estimating excess 1-year mortality associated with the COVID-19 pandemic according to underlying conditions and age: a population-based cohort study. Lancet 2020;395:1715–25. 10.1016/S0140-6736(20)30854-0
    1. Kuderer NM, Choueiri TK, Shah DP, et al. . Clinical impact of COVID-19 on patients with cancer (CCC19): a cohort study. The Lancet 2020;395:1907–18. 10.1016/S0140-6736(20)31187-9
    1. Williamson E, Walker AJ, Bhaskaran KJ, et al. . OpenSAFELY: factors associated with COVID-19-related Hospital death in the linked electronic health records of 17 million adult NHS patients. MedRxiv 2020.
    1. Rosenbaum L. The Untold Toll - The Pandemic's Effects on Patients without Covid-19. N Engl J Med 2020;382:2368–71. 10.1056/NEJMms2009984
    1. Vrdoljak E, Sullivan R, Lawler M. Cancer and coronavirus disease 2019; how do we manage cancer optimally through a public health crisis? Eur J Cancer 2020;132:98–9. 10.1016/j.ejca.2020.04.001
    1. Thomson DJ, Palma D, Guckenberger M, et al. . Practice recommendations for risk-adapted head and neck cancer radiation therapy during the COVID-19 pandemic: an ASTRO-ESTRO consensus statement. Int J Radiat Oncol Biol Phys 2020;107:618–27. 10.1016/j.ijrobp.2020.04.016
    1. NHS England Provider-based cancer waiting times for April 2019. Available: [Accessed 17 Jun 2020].
    1. Burki TK. Cancer guidelines during the COVID-19 pandemic. Lancet Oncol 2020;21:629–30. 10.1016/S1470-2045(20)30217-5
    1. British Society of Gastroenterology Endoscopy activity and COVID-19: BSG and JAG guidance. Available: [Accessed 19 Apr 2020].
    1. National Institute for Health and Care Excellence COVID-19 rapid guideline: delivery of systemic anticancer treatments. Available: [Accessed 19 Apr 2020].
    1. American Cancer Society Survey: COVID-19 affecting patients’ access to cancer care. Available: [Accessed 19 Apr 2020].
    1. American College of Surgeons COVID-19 guidelines for triage of breast cancer patients. Available: [Accessed 19 Apr 2020].
    1. American Society for Radiation Oncology COVID-19 coding guidance. Available: [Accessed 19 Apr 2020].
    1. 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
    1. 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
    1. Lee LY, Cazier J-B, Angelis V, et al. . COVID-19 mortality in patients with cancer on chemotherapy or other anticancer treatments: a prospective cohort study. Lancet 2020;395:1919–26. 10.1016/S0140-6736(20)31173-9
    1. Public Health England Guidance on shielding and protecting people defined on medical grounds as extremely vulnerable from COVID-19. Available: [Accessed 19 Apr 2020].
    1. Public Health England Guidance on social distancing for everyone in the UK. Available: [Accessed 19 Apr 2020].
    1. Hanna TP, Evans GA, Booth CM. Cancer, COVID-19 and the precautionary principle: prioritizing treatment during a global pandemic. Nat Rev Clin Oncol 2020:1–3.
    1. Renzi C, Kaushal A, Emery J, et al. . Comorbid chronic diseases and cancer diagnosis: disease-specific effects and underlying mechanisms. Nat Rev Clin Oncol 2019;16:746–61. 10.1038/s41571-019-0249-6
    1. Health Data Research UK DATA-CAN - The Health Data Research Hub for Cancer. Available: [Accessed 20 Apr 2020].
    1. George J, Mathur R, Shah AD, et al. . Ethnicity and the first diagnosis of a wide range of cardiovascular diseases: associations in a linked electronic health record cohort of 1 million patients. PLoS One 2017;12:e0178945–17. 10.1371/journal.pone.0178945
    1. Bhaskaran K, Forbes HJ, Douglas I, et al. . Representativeness and optimal use of body mass index (BMI) in the UK clinical practice research Datalink (CPRD). BMJ Open 2013;3:e003389. 10.1136/bmjopen-2013-003389
    1. Mathur R, Bhaskaran K, Chaturvedi N, et al. . Completeness and usability of ethnicity data in UK-based primary care and hospital databases. J Public Health 2014;36:684–92. 10.1093/pubmed/fdt116
    1. Herrett E, Thomas SL, Schoonen WM, et al. . Validation and validity of diagnoses in the general practice research database: a systematic review. Br J Clin Pharmacol 2010;69:4–14. 10.1111/j.1365-2125.2009.03537.x
    1. Denaxas S, Gonzalez-Izquierdo A, Direk K, et al. . UK phenomics platform for developing and validating electronic health record phenotypes: CALIBER. J Am Med Inform Assoc 2019;26:1545–59. 10.1093/jamia/ocz105
    1. Denaxas SC, George J, Herrett E, et al. . Data resource profile: cardiovascular disease research using linked bespoke studies and electronic health records (CALIBER). Int J Epidemiol 2012;41:1625–38. 10.1093/ije/dys188
    1. Kuan V, Denaxas S, Gonzalez-Izquierdo A, et al. . A chronological map of 308 physical and mental health conditions from 4 million individuals in the English National health service. Lancet Digit Health 2019;1:e63–77. 10.1016/S2589-7500(19)30012-3
    1. Shah AD, Langenberg C, Rapsomaniki E, et al. . Type 2 diabetes and incidence of cardiovascular diseases: a cohort study in 1·9 million people. Lancet Diabetes Endocrinol 2015;3:105–13. 10.1016/S2213-8587(14)70219-0
    1. Rapsomaniki E, Timmis A, George J, et al. . Blood pressure and incidence of twelve cardiovascular diseases: lifetime risks, healthy life-years lost, and age-specific associations in 1·25 million people. Lancet 2014;383:1899–911. 10.1016/S0140-6736(14)60685-1
    1. Pikoula M, Quint JK, Nissen F, et al. . Identifying clinically important COPD sub-types using data-driven approaches in primary care population based electronic health records. BMC Med Inform Decis Mak 2019;19:86. 10.1186/s12911-019-0805-0
    1. Pujades-Rodriguez M, Duyx B, Thomas SL, et al. . Rheumatoid arthritis and incidence of twelve initial presentations of cardiovascular disease: a population record-linkage cohort study in England. PLoS One 2016;11:e0151245. 10.1371/journal.pone.0151245
    1. Dai M, Liu D, Liu M, et al. . Patients with cancer appear more vulnerable to SARS-COV-2: a multi-center study during the COVID-19 outbreak. Cancer Discov 2020:CD-20-0422 10.1158/-20-0422
    1. Office for National Statistics Coronavirus (COVID-19) infection survey. Available: [Accessed 3 Sep 2020].
    1. GOV UK Sero-surveillance of COVID-19. Available: [Accessed 3 Sep 2020].
    1. Valenti L, Bergna A, Pelusi S, et al. . SARS-CoV-2 seroprevalence trends in healthy blood donors during the COVID-19 Milan outbreak. medRxiv 2020.
    1. Salje H, Tran Kiem C, Lefrancq N, et al. . Estimating the burden of SARS-CoV-2 in France. Science 2020;369:208–11. 10.1126/science.abc3517
    1. Understanding Society COVID-19 survey. Available: [Accessed 17 Jun 2020].
    1. Office for National Statistics Estimates of the population for the UK, England and Wales, Scotland and Northern Ireland. Available: [Accessed 23 Apr 2020].
    1. NHS England NHS warning to seek help for cancer symptoms as half of public report concerns with getting checked. Available:
    1. Margulis AV, Fortuny J, Kaye JA, et al. . Validation of cancer cases using primary care, cancer registry, and hospitalization data in the United Kingdom. Epidemiology 2018;29:308–13. 10.1097/EDE.0000000000000786
    1. Banerjee A, Chen S, Pasea L, et al. . Excess deaths in people with cardiovascular diseases during the COVID-19 pandemic. medRxiv 2020.
    1. Kroenke CH, Kubzansky LD, Schernhammer ES, et al. . Social networks, social support, and survival after breast cancer diagnosis. J Clin Oncol 2006;24:1105–11. 10.1200/JCO.2005.04.2846
    1. Elovainio M, Hakulinen C, Pulkki-Råback L, et al. . Contribution of risk factors to excess mortality in isolated and Lonely individuals: an analysis of data from the UK Biobank cohort study. Lancet Public Health 2017;2:e260–6. 10.1016/S2468-2667(17)30075-0
    1. Maruthappu M, Watkins J, Noor AM, et al. . Economic downturns, universal health coverage, and cancer mortality in high-income and middle-income countries, 1990-2010: a longitudinal analysis. Lancet 2016;388:684–95. 10.1016/S0140-6736(16)00577-8
    1. Longer-Run economic consequences of pandemics. Available: [Accessed 1 May 2020].

Source: PubMed

3
Prenumerera