key: cord-0768269-blfixj99 authors: Tagliamento, Marco; Agostinetto, Elisa; Bruzzone, Marco; Ceppi, Marcello; Saini, Kamal S.; de Azambuja, Evandro; Punie, Kevin; Westphalen, C. Benedikt; Morgan, Gilberto; Pronzato, Paolo; Del Mastro, Lucia; Poggio, Francesca; Lambertini, Matteo title: Mortality in adult patients with solid or hematological malignancies and SARS-CoV-2 infection with a specific focus on lung and breast malignancies: a systematic review and meta-analysis date: 2021-05-27 journal: Crit Rev Oncol Hematol DOI: 10.1016/j.critrevonc.2021.103365 sha: 894911bcb925641f79da44fdd0ae0d8795c14497 doc_id: 768269 cord_uid: blfixj99 Background A systematic review and meta-analysis were performed to estimate the mortality in patients with cancer and SARS-CoV-2 infection. Methods A systematic search of PubMed, up to 31 January 2021, identified publications reporting the case-fatality rate (CFR) among adult patients with solid and/or hematological malignancies and SARS-CoV-2 infection. The CFR, defined as the rate of death among this population, was assessed with a random effect model; 95% confidence intervals (CI) were calculated. Results Among 135 selected studies (N = 33,879 patients), the CFR was 25.4% (95% CI 22.9%-28.2%). At a sensitivity analysis of studies with at least 100 patients, the CFR was 21.9% (95% CI 19.1%-25.1%). Among COVID-19 patients with lung (N = 1,135) and breast (N = 1,296) cancers, CFR were 32.4% (95% CI 26.5%-39.6%) and 14.2% (95% CI 9.3%-21.8%), respectively. Conclusions COVID-19 patients with lung cancer have a comparatively higher probability of mortality than those with breast cancer. Since the start of the coronavirus disease 2019 pandemic, the global cumulative number of cases has reached more than 108 million cases all over the world, with over 2.6 million cases of deaths, as of March 2, 2021 1 . Patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection and a diagnosis of cancer are at high risk of severe symptomatic disease and death 2 . Several efforts have been made to prevent SARS-CoV-2 infection among patients with cancer, as well as to ensure continuity of cancer care during the pandemic 3, 4 . Cancer has been shown to be an independent adverse prognostic effect on COVID-19-related mortality 5, 6 . However, its effect across different patient subgroups is uncertain, and wide variability seem to exist according to different tumor types. In particular, patients with lung cancers have been reported to have disproportionally higher mortality rates from COVID-19, while those with breast cancer showed relatively lower mortality rates [7] [8] [9] . Since the outbreak of the pandemic, several case-series and cohort studies describing the clinical outcomes and mortality of SARS-CoV-2 infection in patients with cancer have been published. However, the relatively small sample size of most reports, their retrospective design and the restriction to hospitalized patients represent important limitations to interpret the reported mortality rate, and the extent to which these can be extrapolated to the wider population of patients with cancer. A systematic-review and pooled analysis assessing the mortality rate of patients with SARS-CoV-2 infection and underlying cancer was published in 2020, but it included a relatively limited number of studies (n = 52) and did not provide mortality pooled data according to tumor types 6 . Moreover, to the best of our knowledge, no systematic review and meta-analyses have been published focusing specifically on lung and breast malignancies. To provide updated evidence on this important topic, we performed a systematic review and meta-analysis aiming to estimate the case-fatality rate (CFR) of patients with solid and/or hematological malignancies and SARS-CoV-2 infection. In addition, we also focused separately on J o u r n a l P r e -p r o o f patients with lung and breast cancer, in order to evaluate the CFR associated with these common tumors. A systematic search of PubMed library up to 31 January 2021 was performed by two authors (M.T. and F.P.); any disagreement was discussed among all authors and resolved. The search strategy on PubMed included different combinations of terms: (covid OR coronavirus OR sars) AND (cancer OR tumor OR tumour OR tumors OR tumours OR malignancy OR malignancies OR neoplasia OR neoplasm) AND (mortality OR death). Duplicated results were not included. Only the most recent and updated version of a same study was considered. The following inclusion criteria were considered: i) publications reporting the mortality rate in patients with cancer and SARS-CoV-2 infection and/or specifically the mortality rate among patients with lung or breast cancer; ii) any type of study (observational, randomized controlled trials or case series); iii) studies involving patients with solid and/or hematological malignancies; iv) studies involving adult patients; v) studies including at least 10 patients; vi) publications in English. A meta-analysis of selected studies was performed in order to assess the CRF among adult patients with solid and/or hematological malignancies and SARS-CoV-2 infection, defined as the cumulative rate of deaths among patients with history of malignancy and SARS-CoV-2-infection. Moreover, the mortality rates among patients with lung and breast cancer and SARS-CoV-2 infection were separately computed. A random effect model was used to assess the CFR, and 95% confidence intervals (CI) were calculated. The likelihood of publication bias was assessed by Egger's test. The Higgins I 2 index was used to assess the heterogeneity between studies. Sensitivity analyses were carried out after excluding studies with less than 100 patients. The systematic search of the literature returned 1,727 records. In total, 1,551 were excluded on the basis of the title and 34 based on the abstract not fulfilling the inclusion criteria, while 7 were duplicates. A total of 135 studies were selected, including 33,879 patients with solid and/or hematological malignancies and SARS-CoV-2 infection (Table 1) . Overall, the CFR was 25.4% (95% CI 22.9%-28.2%; Egger's test p=0.001) (Figure 1) . A sensitivity analysis of the 66 studies (N = 31,184) including at least 100 patients showed a CFR of 21.9% (95% CI 19.1%-25.1%) ( Figure S1 ). In total, 42 and 31 studies reported the mortality rate among COVID-19 patients with lung (N=1,135) and breast (N=1,296) cancers, respectively ( Table 1) . The CFR among patients with lung cancer and SARS-CoV2 infection was 32.4% (95% CI 26.5%-39.6%) when including all studies ( Figure 2 ) and 22.7% (95% CI 11.8%-43.8%) at the sensitivity analysis after excluding studies with less than 100 patients ( Figure S2 ). The CFR among patients with breast cancer and SARS-CoV2 infection was 14.2% (95% CI 9.3%-21.8%) when including all studies ( Figure 3 ) and 9.4% (95% CI 4.0%-22.4%) at the sensitivity analysis after excluding studies with less than 100 patients ( Figure S3 ). Over a year after the outbreak of the pandemic, this large meta-analysis reports the impact of COVID-19 in patients with solid and/or hematological malignancies. Overall, these patients were found to have a high probability of mortality (CFR = 25.4%); the absolute rate was particularly high among patients with lung cancer (32.4%), while it was lower in those with breast cancer (14.2%). These findings strongly highlight the need to dedicate special attention to patients with cancer during the ongoing pandemic. Overall, there is a growing evidence that patients with a history of cancer have a higher mortality rate due to COVID-19 as compared with the general population. Several international registries, such as The International Severe Acute Respiratory and Emerging Infections Consortium (ISARIC) 87 , the OnCOVID 145 , the Clinical impact of COVID-19 on patients with Cancer (CCC-19) 146 , the GCO-002 CACOVID-19 126 , reported a mortality rate of oncological patients with SARS-CoV-2 infection up to 40% 147 . The majority of these studies did not foresee a control group of patients with COVID-19 without cancer. Instead, a recent retrospective study, evaluating by a multivariate model the difference in mortality from COVID-19 between 312 patients with cancer and 4,833 patients without cancer in the U.S., found a higher death rate in the cancer group. Among patients with cancer, having an active or progressive disease was shown to increase the likelihood of mortality (p<0.001) 101 . Our findings confirm the high probability of mortality in patients with solid and/or hematological malignancies and SARS-CoV-2 infection. Since the COVID-19 outbreak, major efforts have been implemented to protect the most vulnerable patients from SARS-CoV-2 infection. Among them, the following measures have been suggested in cancer care: the rationalization of working practices, the adaptation of chemotherapy regimens as well as other systemic treatments, the deferral of procedures for diseases with favorable biology or not requiring urgent care, and additional measures related to specific subtypes of cancer [148] [149] [150] [151] [152] . Aggressive preventive measures include preferential access to COVID-19 vaccination, which should be administered as early as possible 153 . Furthermore, ensuring cancer care continuity during the COVID-19 pandemic should represent a priority, J o u r n a l P r e -p r o o f considering treatment interruptions or discontinuations only on a case-by-case basis, taking into account each patient and tumor characteristics 3, 4 . In our meta-analysis, patients with lung cancer had a comparatively higher CFR than the overall population, consistent with the data reported in the Thoracic Cancers International COVID-19 Collaboration (TERAVOLT) registry (not included in our separate analysis of the CFR in lung cancer, since patients with non-lung thoracic malignancies were included as well, like in the study by Lièvre et al.) 8, 126 , and with previous reports of patients in China [154] [155] [156] . Whether this high mortality rate may be reduced with special management of such patients in intensive care, is an open question 8 . On the contrary, a comparatively lower CFR was observed in patients with breast cancer, suggesting that breast cancer per se does not seem to be a major determinant of COVID-19 mortality. One potential explanation might be that patients with lung cancer tend to be older than those with breast cancer. Furthermore, co-existing (pulmonary) conditions might further raise the risk for an unfavorable outcome in patients with lung cancer diagnosed with COVID-19, as well as the different spectrum of anticancer treatments received compared to breast cancer. Conversely, the delays in cancer diagnosis and treatment due to the COVID-19 pandemic may have an impact on the outcome of this disease, considering that a significant proportion of the important gain in disease-specific overall survival observed in the last 20-30 years are attributable to early detection and improved treatments 157 . The long-term effect on cancer-specific survival outcomes due to the temporary suspension of routine screening during the peak of the pandemic will be only and fully revealed in the future 157 . Our meta-analysis has some limitations that should be acknowledged. It included heterogeneous cohorts, involving hospitalized and non-hospitalized patients, with both solid and/or hematological malignancies currently receiving or not active anticancer treatments (and different types) at the time of SARS-CoV-2 infection. Some studies only reported on in-hospital mortality, and sometimes exclusively on 30-day rate. Moreover, we evaluated the mortality rate considering death from any cause, instead of focusing specifically on death due to COVID-19 or due to cancer progression (this specific information was frequently unavailable in the studies J o u r n a l P r e -p r o o f included in the meta-analysis). As expected, the heterogeneity in the analyses was significant (p<0.001) probably due to the high number of evaluated studies characterized by different study design, population, sample size, and the geographical variability in the spread of the pandemic. Nevertheless, notably, more than 75% of CFR reported in the individual studies ranged between 0.10 and 0.39, so our pooled estimate (CFR = 0.254) reflects this trend. Our study has also several strengths. The present meta-analysis included a large number of studies (n=135) and patients (n=33,879). All studies published in the first year since the start of the pandemic were evaluated. The CFR computed among the overall population is consistent with a previous analysis 6 . In addition, we also separately focused on patients with lung and breast cancer, in order to evaluate the CFR associated with these two common malignancies. Our systematic review and meta-analysis showed that patients with solid and/or hematological malignancies and SARS-CoV-2 infection have a high probability of mortality, with a comparatively higher CFR in patients with lung cancer, and a comparatively lower CFR in patients with breast cancer. Based on these results, patients with underlying cancer deserve special attention with aggressive preventive measures that should also include early access to COVID-19 vaccination. Zhang L et al. Abbreviations. CFR: case-fatality rate; 95% CI: 95% confidence interval. Marcello Ceppi is a researcher at the Clinical Epidemiology Unit of the IRCCS Ospedale Policlinico San Martino in Genova (Italy). His area of expertise is the statistical analysis of epidemiological and clinical data in the field of oncology with particular reference to advanced statistical methods applied to cohort and case-control studies, clinical trials and meta-analysis. He was responsible for data analysis in several projects funded by Italian Association for Cancer Research (AIRC) and Italian Ministry of Health. Kamal S. Saini, MBBS, MD, MRCP (UK), DM, is the Executive Medical Director at Covance Inc., and also works as a locum consultant medical oncologist at the NHS (UK). He has over 16 years of experience in drug development, which includes enrolling patients into cancer trials, helping design and execute studies, medical monitoring and data analysis of global trials, interfacing with regulatory bodies, and working with biotech and pharmaceutical companies to refine drug development strategies. His main areas of interest are breast and lung cancers, optimization of oncology trial design, intersection of COVID-19 and cancer, and adopting a precision medicinebased approach to the treatment of patients with cancer. World Health Organization. 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Educate SARS-CoV-2 Transmission in Patients With Cancer at a Tertiary Care Hospital in Wuhan, China Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China Clinical characteristics of COVID-19-infected cancer patients: a retrospective case study in three hospitals within Wuhan, China The COVID-19 pandemic and impact on breast cancer diagnoses: what happened in England in the first half of 2020 Evandro de Azambuja is a medical oncologist form the Institut Jules Bordet He is a breast cancer specialist and the head of the Medical Support Team. He has been extensively involved in large phase III registration trials in breast cancer and had a special interest in cardiac toxicity cause by anticancer treatments His main areas of interest are breast cancer and hereditary cancer syndromes. He is deeply involved in clinical cancer research as principal investigator for several phase I-III trials with a focus on triple negative breast cancer. He is currently working on a PhD investigating plasma and tissue single-cell multiomics in early triple negative breast breast cancer. He is involved in the EORTC Breast Cancer Group, board member of the Belgian Society of Medical Oncology and Committee member of ESMO Young Oncologists Committee and ESMO Resilience Task Force Since 2017 he heads the "Molecular Diagnostics and Therapy Programme" and the "Molecular Tumour Board" at the University of Munich (Germany). Furthermore, he serves as the medical lead for early phase clinical trials in medical oncology. He has received research support from the German Research Foundation, the Universities of Hamburg and Munich and young investigator awards from the AACR and GRG/AGA. Dr Westphalen has authored and co-authored more than seventy research papers. Dr Westphalen joined ESMO in 2017 and was a participant in the "ESMO Leaders Generation Programme Gilberto Morgan is an American oncologist with a background in molecular biology currently practicing in Lund (Sweden) His clinical activity is dedicated to the care of different type of cancer, particularly focused on patients with breast cancer. He has been extensively involved as PI or co-PI in phase II/III clinical trials in advanced and early breast cancer She took the specialty in Medical Oncology in 1993 at the University of Naples. She is the director of the Breast Unit at the IRCCS Ospedale Policlinico San Martino in Genova (Italy), and professor of oncology at the University of Genova. She is PI of phase II and III trials in metastatic and early breast cancer patients, and PI of toxicity and supportive care studies. She is PI of many research projects on breast cancer. She is reviewer of research projects for Cancer Research UK and EORTC. She is member of the Scientific Committee of GIM (Gruppo Italiano Mammella), secretary of the breast cancer working group of Alliance Against Cancer, chairperson of the steering committee of the AIOM (Associazione Italiana Oncologia Medica) recommendations for fertility preservation in cancer patients and she is a member of the steering committee of the AIOM recommendations for the management of breast cancer patients Since the beginning of her career, she focused on the clinical management of early and advanced breast cancer, developing expertise and specific skills in breast cancer care. She is mainly involved as sub-investigator in several studies regarding breast cancer He is mainly focused on the care of breast cancer patients and is deeply involved in cancer research. Above all, he has a particular expertise in the management of breast cancer in young women, with a specific attention to the fertility and pregnancy-related issues that they have to face after diagnosis. He is member of the guideline group on fertility preservation in cancer patients for the European Society for Medical Oncology (ESMO), the European Society of