ORIGINAL RESEARCH Impact of the COVID-19 pandemic on the care of cancer patients in Spain M. Amador1*, X. Matias-Guiu2, G. Sancho-Pardo3, J. Contreras Martinez4, J. C. de la Torre-Montero5, A. Peñuelas Saiz6, P. Garrido7, R. García-Sanz8, Á. Rodríguez-Lescure9 & L. Paz-Ares10 1 Spanish Association Against Cancer (AECC), C. del Teniente Cnel. Noreña, Madrid; 2Pathology Department, Bellvitge University Hospital, Barcelona; 3Radiation Oncology Department, Santa Creu i Sant Pau Hospital, Barcelona; 4Radiation Oncology Department, Malaga Regional Hospital, Malaga; 5Comillas Pontifical University, San Juan de Dios Department of Health Sciences, Madrid; 6Oncology-Hematology-Radiotherapy of Vall d’Hebron University Hospital, Barcelona; 7Medical Oncology Department, Ramon y Cajal University Hospital, Madrid; 8Hematology Department, Salamanca University Hospital/Salamanca Biomedical Research Institute (HUS/ IBSAL/CIBERONC), Salamanca; 9Medical Oncology Department, Elche University General Hospital, Elche; 10Medical Oncology Department, 12 de Octubre University Hospital, Madrid, Spain Available online 30 April 2021 Background: Studies evaluating the effects of the COVID-19 pandemic on public healthcare systems are limited, particularly in cancer management. As no such studies have been carried out in Spain, our objective is to describe and quantify the impact of the COVID-19 pandemic on cancer patients in Spanish hospitals during the first wave of the pandemic. Materials and methods: This retrospective, multicenter, nationwide study collected information from hospital departments treating oncology patients. An electronic questionnaire comparing outcomes and management of oncohematological patients for the March-June 2019 and March-June 2020 periods was used. Results: Information from 78 departments (36 tertiary hospitals) was analyzed. Forty-four departments implemented adapted protocols during March 2020. Most of these (n ¼ 38/44; 86.4%) carried out COVID-19 triage, while 26 of 44 (59.1%) carried out onsite polymerase chain reaction tests for clinically suspected cases. A shift from in-person to telephone visits was observed in 43 of 44 (97.7%) departments. Comparing the March-June 2019 and March- June 2020 periods, the number of new patients decreased by 20.8% (from 160.2 to 126.4). Decreases were also seen in the mean number of total (2858.2 versus 1686.1) and cancer (465.5 versus 367.2) biopsies, as well as the mean number of bone marrow biopsies (30.5 versus 18.6). Concerning the number of patients visiting specific cancer care departments, a decrease from 2019 to 2020 was seen for mean number of chemotherapy treatments (712.7 versus 643.8) and radiation therapy (2169.9 versus 2139.9). Finally, a reduction from 2019 to 2020 of 12.9% (from 8.6 to 7.4) in the mean number of patients included in clinical trials was noted. Conclusions: This study provides the first comprehensive data concerning the impact of COVID-19 on cancer care in Spain. The pandemic caused a 20.8% decrease in newly diagnosed patients, which may impact future outcomes. Measures must be taken to ensure cancer management receives priority in times of healthcare emergencies. Key words: COVID-19, pandemic, cancer, care, Spain INTRODUCTION causing an atypical form of pneumonia.3,4 Since then, the Coronaviruses are one group of the most pathogenic agents etiological agent, named SARS-CoV-2, has spread worldwide, affecting the human respiratory system.1 Coronavirus out- with the World Health Organization declaring the current breaks were responsible for healthcare emergencies such as the outbreak a public health emergency on 30 January 2020.5 In severe acute respiratory syndrome (SARS)-CoV reported in Spain, the first case of COVID-19 was reported on 31 January 2003, and the Middle East respiratory syndrome (MERS)-CoV in 2020.6 Between 1 March and 30 June 2020, a total of 240 978 2012.2 In December 2019, a new coronavirus disease (COVID- individuals tested positive for COVID-19 in Spain and 27 134 19) emerging most likely from China has been responsible for deaths were reported.7 The disease exhibits a wide variety of clinical manifestations ranging from asymptomatic or mild forms to severe pneumonia with respiratory and systemic, *Correspondence to: Dr MariLuz Amador, Medical Director, Spanish Associa- tion Against Cancer (AECC), Teniente Coronel Noreña, 30, 28045, Madrid, multi-organ dysfunction (including acute respiratory distress Spain. Tel: þ34-91-319-41-38 syndrome, sepsis, and septic shock) requiring intensive care E-mail: mluz.amador@aecc.es (M. Amador). treatment.1,8 As a consequence of the COVID-19 pandemic, 2059-7029/© 2021 The Author(s). Published by Elsevier Ltd on behalf of routine clinical practices in Spain were modified extensively to European Society for Medical Oncology. This is an open access article under the deal with such a critical healthcare scenario.9 CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Volume 6 - Issue 3 - 2021 https://doi.org/10.1016/j.esmoop.2021.100157 1 ESMO Open M. Amador et al. Cancer is a major public health issue worldwide10 and the Board of the 12 de Octubre University Hospital in Madrid second most common cause of mortality, accounting for (20/410, 28 July 2020). approximately one in six deaths. By 2030 its incidence is expected to increase by w45%,10 making it the world’s Data collection and variables evaluated leading cause of death. As cancer morbidity and mortality The e-questionnaire was developed by physicians directly are directly related to the stage at diagnosis,11 earlier involved in the hospital care of cancer patients during the detection and treatment are therefore associated with first wave of the pandemic in Spain (March to June 2020). better prognosis and survival outcomes.12,13 Cancer pa- Data were retrospectively collected between 30 July and tients are a particularly at-risk population for developing 12 October 2020 from the mentioned departments. The severe COVID-19. This is particularly the case for patients questionnaire was composed of two main sections: (i) anti- receiving active treatment, those who have metastatic dis- COVID-19-specific measures taken in relation to patient care ease, and those who are affected by lung and hematological as measured by the implementation of specific action pro- malignancies.14-17 tocols and general measures taken in each department to Given the impact of COVID-19 on healthcare resources, adapt to the situation; and (ii) impact on cancer care, the redeployment of physicians (including oncologists) to measuring changes in the number of new patient referrals, COVID-19-specific tasks, and the possible reluctance of sick number of diagnostic procedures (such as solid tumors and people to seek medical assistance at healthcare facilities, bone marrow biopsies), number of treatments adminis- there is a heightened risk that the diagnosis and treatment tered, and finally participation in clinical trials. It should be of cancer patients during the pandemic will be delayed for noted that between March and June 2020, polymerase unacceptably long periods. To this end, multicenter studies chain reaction (PCR) tests were only carried out on clinically evaluating the effect of the pandemic on public healthcare suspected cases. The e-questionnaire used to record re- systems are limited, particularly in relation to cancer man- sponses to the different variables was sent to the heads of agement.18-21 As no such studies have been carried out in the participating departments’ participants. Spain, the objective of the present work was to evaluate and quantify the impact of the COVID-19 pandemic on the Data analysis hospital-based care of cancer patients during the first wave of the pandemic from March to June 2020 in Spain. The impact of the pandemic was established by assessing absolute and relative changes during the considered period MATERIALS AND METHODS (March to June) in 2019 (control) versus the same period in 2020. Categorical variables were expressed as absolute and Study design relative frequencies, whereas continuous variables as the This was a retrospective, multicenter, nationwide study in mean and range (minimum and maximum values). All which data were collected from participating hospitals descriptive analyses were carried out with the statistical across four key departments involved in the management of software package SAS 9.4 (SAS Institute, NC; 2013).22 oncohematological patients (hematology, medical oncology, radiation oncology, and pathology). Data were collected for RESULTS the March to June period of 2019 and compared with the Participating hospitals same period in 2020. Five national scientific societies in Spain [Spanish Society of Pathological Anatomy (SEAP-IAP); A total of 37 tertiary hospitals were invited to participate in Spanish Society of Oncological Nursing (SEEO); Spanish So- the study (Figure 1), with 36 of the 37 (97.3%) sites ciety of Hematology and Hemotherapy (SEHH); Spanish providing data from at least one of the four departments. Society of Medical Oncology (SEOM); and Spanish Society of Overall, the participation of the departments was: hema- Radiation Oncology (SEOR)] together with the Spanish As- tology, 12 hospitals (32%); medical oncology, 13 hospitals sociation Against Cancer (AECC) collaborated in the study. (35%); radiation oncology: 19 hospitals (51%); and pathol- An electronic (e-)questionnaire addressing a range of vari- ogy: 34 hospitals (92%). Information from a total of 78 ables was sent to departments as indicated above in 37 departments was available for analysis. The complete list of public general hospitals. The questionnaire for each hospitals providing data from each department and the department is shown in Supplementary Appendix, available names of participating researchers are shown in the at https://doi.org/10.1016/j.esmoop.2021.100157. All Supplementary Appendix, available at https://doi.org/10. participating sites were public general hospitals providing 1016/j.esmoop.2021.100157. tertiary level care, some of which were the only hospitals of this type in the concerned region. As Spain has fewer than a Specific anti-COVID-19 measurements hundred public general tertiary care hospitals, the overall Forty-four departments initiated specific action protocols obtained data are considered representative of the national against COVID-19; 24 (54.5%) of these did so in the first half situation. The number of participating hospitals per region of March 2020, and the remainder in the second half of that was chosen to be indicative of the COVID-19 incidence rate same month (Table 1). Of the 44 departments, 38 (86.4%) during the first wave, which was heterogeneous across the implemented COVID-19 infection and contact triage pro- country. This study was approved by the Ethics Review cedures during routine clinical practice, and 26 departments 2 https://doi.org/10.1016/j.esmoop.2021.100157 Volume 6 - Issue 3 - 2021 M. Amador et al. ESMO Open Figure 1. Distribution of participating hospitals in the autonomous regions of Spain and the number of COVID-19 cases treated by each. The value in white indicates the number of participating hospitals in each region. (59.1%) carried out onsite PCR tests for clinically suspected 62.1% (n ¼ 21.3, range: 0-159) were admitted to hospital, COVID-19 cases. A shift from in-person to telephone/ and 19.7% (mean 6.8, range: 0-30) of them died thereafter. internet consultations was observed in 43 (97.7%) of the 44 departments, while physical assistance was maintained in 95.5% of departments for those patients whose condition New and successive medical visits could not be evaluated by telephone. Most departments Compared with the March-June period in 2019, the mean (97.7%, n ¼ 43/44) followed national guidelines (SEHH number of new patient visits decreased by 20.8% (from guidelines for hematology; SEOM guidelines for medical 160.2, range: 151.4-173.1, to 126.4, range: 105.3-144.3) for oncology; SEOR guidelines for radiation oncology) for the the same period in 2020. For successive consultations modification of therapeutic strategies. Overall, between (including follow-up, treatment, and other kinds of visit), March and June 2020, out of a mean of 34.3 patients many were shifted from in-person to remote (telephone) (range: 0-215) per department, 77.5% (mean 26.6, range: 0- visits, with the mean number of telephone visits increasing 125) of patients who were clinically suspected of having three-fold compared with the same period in 2019. On the COVID-19 tested positive. Among symptomatic patients, other hand, the mean number of physical visits decreased Table 1. Specific anti-COVID-19 measurements Total (n [ 44) Hematology (n [ 12) Medical oncology (n [ 13) Radiation oncology (n [ 19) n (%) n (%) n (%) n (%) Specific action protocols Date of first implemented measures 1-15 March 24 (54.5) 9 (75.0) 8 (61.5) 7 (36.8) 16-30 March 20 (45.5) 3 (25.0) 5 (38.5) 12 (63.2) Separated circuits: non-contaminated/contaminated 38 (86.4) 12 (100.0) 13 (100.0) 13 (68.4) Onsite PCR 26 (59.1) 10 (83.3) 9 (69.2) 7 (36.8) Change from physical to telemedicine consultations 43 (97.7) 12 (100.0) 13 (100.0) 18 (94.7) Ongoing physical visits in cases where necessary 42 (95.5) 12 (100.0) 13 (100.0) 17 (89.5) Specific guidelines for the modification of therapeutic strategies From same department 35 (79.5) 10 (83.3) 10 (76.9) 15 (78.9) National guidelines 43 (97.7) 12 (100.0) 13 (100.0) 18 (94.7) International guidelines 34 (77.3) 8 (66.7) 10 (76.9) 16 (84.2) Other guidelines 12 (27.3) 4 (33.3) 4 (30.8) 4 (21.1) PCR, polymerase chain reaction. Volume 6 - Issue 3 - 2021 https://doi.org/10.1016/j.esmoop.2021.100157 3 ESMO Open M. Amador et al. Diagnostic procedures Table 2. COVID-19 impact on cancer care For solid tumors, the mean number of total cytologies and Percentage change Mean data for (March-June 2019 March-June 2019 biopsies decreased by 57.1% (1950.9 versus 843.7) and versus 2020) versus 2020 41.2% (2858.2 versus 1686.1), respectively, in the 2020 Medical consultationsa period compared with the 2019 period. Considering specific New visits 20.8 160.2 versus 126.4 cancer diagnoses, mean numbers were reduced by 30.2% Successive consultations (57.7 versus 40.0) for cytologies and 21.2% (465.5 versus Telephone 298.5 118.0 versus 467.3 Physical 22.3 1224.4 versus 952.0 367.2) for biopsies. Regarding diagnostic procedures carried Diagnosisb out on hematological patients in the 2020 period, a Cytologies 57.1 1950.9 versus 843.7 decrease of 31.4% (58.8 versus 39.9) was reported for bone Cytologies with cancer 30.2 57.7 versus 40.0 diagnosis marrow aspirates and 38.3% (30.5 versus 18.6) for bone Ratio cancer/cytologies 52.2 4.1 versus 6.3 marrow biopsies compared with 2019 figures. The reduction Biopsies 41.2 2858.2 versus 1686.1 in the mean number of flow cytometry tests in 2020 versus Biopsies with cancer 21.2 465.5 versus 367.2 diagnosis 2019 was 12.5% (220.7 versus 192.6) and 15.8% (626.0 Ratio cancer/biopsies 40.9 16.6 versus 23.4 versus 524.0) for additional genetic studies on blood can- Specific diagnostic cers (Table 2). proceduresc Bone marrow aspirates 31.4 58.8 versus 39.9 Bone marrow biopsies 38.3 30.5 versus 18.6 Treatment delivery Flow cytometry tests 12.5 220.7 versus 192.6 Neoplastic genetic 15.8 626.0 versus 524.0 We observed a decrease in 2020 of 14.3% in the mean studies number of patients visiting day hospitals (980.0 versus Treatments Patients treated in day 14.3 980.0 versus 837.9 837.9), with a decrease of 9.5% in the mean number of hospitals (ambulatory patients receiving chemotherapy (712.7 versus 643.8). The therapy)d use of granulocyte colony-stimulating factors increased by Treatments in day 7.7 1500.1 versus 1377.7 hospitalsd 27.0% in 2020 with respect to the same period in 2019 (64.0 Patients treated with 9.5 712.7 versus 643.8 versus 81.2). Interestingly, the use of immune checkpoint chemotherapyd inhibitors (ICIs) in 2020 increased by 11.0% compared with Patients treated with 27.0 64.0 versus 81.2 G-CSFd 2019 figures (121.4 versus 135.0). We also observed an in- Patients treated with 11.0 121.4 versus 135.0 crease of 2.1% in the use of tyrosine kinase inhibitors (189.3 immune checkpoints versus 191.6) in 2020 compared with 2019 data. The mean inhibitorse Patients treated with 2.1 189.3 versus 191.6 number of autologous hematopoietic stem cell transplants tyrosine kinase decreased by 7.5% (3.3 versus 2.9) in 2020 compared with inhibitorse the same period in 2019, while the mean number of allo- Hematopoietic stem cell transplantsf geneic transplants decreased by 27.2% (3.4 versus 2.4). Autologous 7.5 3.3 versus 2.9 Finally, the mean number of patients visiting radiation Allogenic 27.2 3.4 versus 2.4 oncology facilities and the mean number of treatments Radiation therapiesg Patients treated 5.3 146.4 versus 138.4 administered decreased by 5.3% (146.4 versus 138.4) and Treatments carried out 1.3 2169.9 versus 2139.9 1.3% (2169.9 versus 2139.9), respectively (Table 2). (sessions) Clinical research activitiesh Trials interrupted by the 0.1 e Clinical research pandemic Trial discontinuations 2.2 e The inclusion of patients in oncology-specific clinical trials due to the pandemic decreased by 12.9% during the 2020 period compared with Clinical trials recruitment 32.1 30.4 versus 40.1 the 2019 period (mean 7.4, range: 4.1-11.0, versus mean Screening visits 1.6 14.6 versus 13.9 Enrolled patients 12.9 8.6 versus 7.4 8.6, range: 8.0-9.9), whereas an increase of 32.1% in the G-CSF, granulocyte colony-stimulating factors. 2020 period compared with 2019 was observed in the a Data obtained from 37 departments (hematology, medical oncology, and radiation number of clinical trials in general (mean 40.1, range: 38.8- oncology) of 28 hospitals. b Pathology departments of 34 hospitals. 41.7, versus mean 30.4, range: 28.7-31.5), presumably due c Hematology departments of nine hospitals. to COVID-19 research (Table 2). d Seven hematology and nine medical oncology departments. e Medical oncology departments of eight hospitals. f Hematology departments of six hospitals that carry out transplants. DISCUSSION g The radiation oncology departments of 18 hospitals. h 29 departments (hematology, medical oncology, and radiation oncology) of 22 The COVID-19 pandemic has dramatically impacted most hospitals. public healthcare systems around the world. The Spanish public healthcare system guarantees universal health coverage and free access for all Spanish individuals and by 22.3% (from 1224.4, range: 1184.7-1282.6, to 952.0, eligible foreigners.23 During the first wave of the COVID-19 range: 758.6-1143.9) during the 2020 period compared pandemic (March to June 2020), the Spanish healthcare with 2019 (Table 2). system was forced to reorganize a large proportion of its 4 https://doi.org/10.1016/j.esmoop.2021.100157 Volume 6 - Issue 3 - 2021 M. Amador et al. ESMO Open resources toward the management of SARS-CoV-2-infected follow-up, review, and other visits that were not the first patients and to implement specific action protocols to visit to the specialist), with a three-fold increase in the avoid the infection of healthy healthcare professionals and number of telephone visits and a 22.3% decrease of in- patients admitted to or attending hospitals.24 The goal of person visits. Regarding treatments, we identified a the present study was to collect, for the first time in Spain, decrease of 9.5% in the mean number of chemotherapy accurate data on the impact of the first wave of the treatments and 1.3% in radiation treatments, together with pandemic on care provision and outcomes in oncology pa- a clear increase in the use of colony-stimulating factors tients from a representative sample of 36 hospitals.17,25,26 (increase of 27.0% when compared with the same period in Our study presents some major limitations, such as its 2019) and ICIs (11.0%). All of these results corroborate the retrospective nature and the exclusive hospital perspective effort made to adapt different treatment modalities and of cancer management as neither primary care nor schedules to the healthcare situation at the time. Differ- screening data were included (different sources for these ences between the decrease in systemic and radiation data exceeded our operational capacity). Additionally, not treatments might reflect the use of radiotherapy as an all contacted departments responded to the questionnaire, alternative to systemic and/or surgical treatment. In addi- which may limit the representation since data could be tion, data on other systemic treatments (chemotherapy, influenced by selection and measurement bias. ICIs, tyrosine kinase inhibitors) revealed similar efforts to Our results reveal that routine practice in hematology, adapt to the prevailing situation while maintaining and medical oncology, radiation oncology, and pathology de- adapting treatments for patients with already diagnosed partments in Spain was impacted early in the pandemic. solid tumors. That being said, the most concerning data for Specific action protocols were implemented during the us are those related to attention provided to newly diag- month of March 2020 in participating departments, nosed patients.18,20 including the development of clinical triage protocols and For patients visiting an oncology or hematology depart- onsite COVID-19 PCR testing for patients attending hospi- ment for the first time, a decrease of 20.8% in the mean tals. These measurements aimed to protect all patients from number of new visits, considered as a surrogate of newly infection. diagnosed cases, was identified. Similarly, for solid tumors, It is important to note that of all symptomatic patients, we observed a decrease (21.2%) in the mean number of 62.1% were admitted, 77.5% were confirmed by PCR, and cancer biopsies carried out during the studied period. The 19.7% died from COVID-19-related causes. It is also percentage differences between 2019 and 2020 with important to point out that PCR testing was not routinely respect to total cytologies and biopsies could indicate a available during the first wave of the pandemic in Spain certain prioritization to perform these diagnostic proced- unless there was solid clinical evidence of suspected infec- ures when a cancer was suspected. For hematological tu- tion. This could explain the high rate of positive results in mors, a decrease in the mean number of diagnostic tested patients. The 19.7% mortality rate for admitted procedures such as bone marrow aspirates (31.4%) and cancer patients was similar to that reported for the general biopsies (38.3%) was reported, which likely reflects a population who required hospital admission due to COVID- reduction in the number of consecutive explorations in 19 at that time.27 previously diagnosed patients (i.e. leukemia patients under We also observed a shift from physical visits to telephone therapeutic monitoring), as well as a reduction of new di- visits at most (97.7%) of the participating sites, particularly agnoses of diseases where bone marrow examination is for follow-up consultations. However, only a 14.3% decrease essential (myelodysplasia, leukemia, myeloma). In addition, was seen in the mean number of cancer patients being a reduction in the mean number of allogeneic (27.2%) and cared for in day hospitals. In solid tumors, the shift from autologous (7.5%) hematopoietic stem cell transplantations intravenous to oral agents due to the pandemic situation was also noted, probably reflecting a delay in the per- has been very limited (although no measurements on this forming of these procedures as a strategy of physicians to topic are available). For hematology malignancies, the avoid deep and long-term myelosuppression in these reduction in the number of day hospital treatments was patients. related to those therapies considered less relevant. How- In our opinion, these data concerning the decrease in ever, others considered as more critical were less affected new visits, cancer biopsies, and hematology diagnoses are (the number of therapies with ICIs increased). In-person the most concerning of this study, but also potentially the visits were also maintained for those cases where there most actionable. While acknowledging the study’s limita- was a need for patients to be physically examined. Given tions, our data provide a good idea of the quantitative the above, it can be concluded that departments and impact of COVID-19 on cancer care and assistance. In healthcare professionals assisting cancer patients reacted addition, our data are consistent with previously published early in the pandemic to protect their patients by imple- data from other countries,18,20,21 and individual institutions menting specific measurements such as clinical triage or in our country.28 A survey carried out by Cancer Research PCR and by adapting practices to the given UK showed that the pandemic impacted their testing (two circumstances.18,20,21 in five patients), cancer care (two in three patients), and We observed similar trends to changing and adapting treatment (one in three patients).18 Dinmohamed et al.20 care variables like successive visits to hospitals (including revealed a reduction in cancer diagnosis by 26% for all Volume 6 - Issue 3 - 2021 https://doi.org/10.1016/j.esmoop.2021.100157 5 ESMO Open M. Amador et al. cancer sites (excluding skin cancer) and 60% for skin cancer Conclusions (excluding basal cell carcinoma) in April 2020. Moreover, This study provides the first comprehensive dataset Jazieh et al.21 reported a reduction of services in more than describing the negative impact of the COVID-19 pandemic half of all centers (55%) and the missing of at least one cycle on cancer care in Spain. Oncology patients are particularly of therapy by >10% of cancer patients (46%). The situation vulnerable to this pandemic, presenting more frequent and meant that patients were exposed to harm due to the severe forms of disease, often requiring hospitalized care, interruption of cancer-specific care (36% of centers) and and with poorer evolution. In addition, we have docu- noncancer-related care (39%). mented a significant delay in cancer diagnosis and treat- Our data highlight that one in five patients with cancer ment that may potentially have consequences on was either not diagnosed or diagnosed late during the first outcomes: reduced survival time, less effective treatments, wave of the pandemic in Spain, where many (if not all) non- and increased morbidity and suffering. We have shared COVID-19 diagnosis-related procedures were stopped. This these results with Spain’s health authorities and suggest took place together with the collapse of Spain’s primary cancer diagnosis and management should be prioritized in healthcare system, which represents the most important critical times such as the current pandemic scenario. A entry to the health system for cancer patients. Moreover, united approach is needed to address the shortfall in new and although this hypothesis cannot be quantified, we diagnoses created by this situation. Indeed, the solution is consider that patients’ fear of being infected in hospitals likely to be complex and multidisciplinary (from evaluating and primary care clinics might also have contributed to the current structures and human resources to ensure that the decrease of new cancer diagnoses. This ‘gap’ generated most vulnerable cancer patients are vaccinated in a timely during the first wave has probably not been covered to the manner). At the time of writing, (February 2021), Spain was present time and might be even greater after the second experiencing a new wave of COVID-19, which in our and third waves of the pandemic. These data are important opinion, will increase delays in the diagnosis and treatment given their potential consequences, as it is well known that of cancer patients if no concerted actions are taken, with an early diagnosis and treatment are associated with better the impact no doubt to be felt heavily by patients and the prognosis and survival outcomes in cancer patients.16,17 public healthcare system alike. Delayed cancer treatment is related to increased mortality across surgical, systemic treatment, and radiotherapy in- ACKNOWLEDGEMENTS dications.29 In this way, the delay in cancer diagnosis during The authors express their gratitude to all the doctors/de- the COVID-19 pandemic will probably result in an increase partments of the hospitals involved in the project and to in the stage at which treatment is initiated for a large Meisys for advice on the writing of this paper. proportion of patients and may impact long-term survival, morbidity, and quality of life. Indeed, it has been estimated that delays in cancer diagnosis will be responsible for an FUNDING additional 10 000 deaths from breast and colorectal cancer This work was supported by funding from the AECC, a non- in the coming 10 years in the USA.30 In a national profit organization, whose medical department funded the population-based modeling study in the UK, the impact on study and the medical writing (no grant number). net survival at 1, 3, and 5 years after diagnosis was used to estimate the number of additional deaths that could be attributed to cancer compared with pre-pandemic data.31 DISCLOSURE The increased rate of mortality due to breast, colorectal, The authors have declared no conflicts of interest. esophageal, and lung cancer could result in 3291-3621 additional deaths within 5 years. Finally, the COVID-19 pandemic has also impacted clinical REFERENCES research. In our study, the inclusion of patients in cancer 1. Rothan HA, Byrareddy SN. 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Jazieh AR, Akbulut H, Curigliano G, et al. Impact of the COVID-19 36. Huang C, Huang L, Wang Y, et al. 6-month consequences of COVID-19 pandemic on cancer care: a global collaborative study. JCO Glob in patients discharged from hospital: a cohort study. Lancet. 2021;397: Oncol. 2020;6:1428-1438. 220-232. Volume 6 - Issue 3 - 2021 https://doi.org/10.1016/j.esmoop.2021.100157 7