This study found that mortality from all types of cancer and the five most common types in Brazil decreased in 2020, the first year of the COVID-19 pandemic, compared to the previous year. However, in 2022, mortality from all cancers was higher than in the reference year, as well as the mortality from colorectal, female breast, and prostate cancer. During the pandemic, mortality from COVID-19 in cancer patients (i.e., cancer as a contributing cause), a direct impact of the pandemic on this population, was higher, respectively, in 2021 and 2020, and the highest rates followed the waves of the pandemic in the country. The findings showed that this mortality was negatively associated with the number of hospital beds in the public health system (SUS) per inhabitant, considering the 133 RGI in Brazil, suggesting a protective role of the availability of hospital care concerning deaths due to COVID-19 in cancer patients.
For 2020, the present study's findings seem to align with the competing cause hypothesis, as the reduction in the death rate from all cancers in 2020 appears to have been partly compensated by the death rate from COVID-19 in cancer patients from that same year. This explanation supports that many individuals with cancer, at a higher risk of death from this disease, may have died from COVID-19, as this population had a higher risk of death from COVID-19 than the general population[21–23]. However, this rationale needs additional reflection: the contributing cause of death is likely underreported in the mortality information system, especially considering the first pandemic year, in which the unprepared health services – responsible for completing the causes of death – were under massive pressure and overload in the fight against COVID-19.
A study in Brazil identified that mortality from ill-defined causes increased in 2020 compared to the period between 2015 and 2019[20]. In the present study, death rates from cancer as the underlying cause were adjusted for ill-defined causes, according to redistribution techniques established in the literature[27], but there are no statistical procedures to correct the underreporting of deaths due to COVID-19 that had cancer as a contributing cause. Thus, the present study suggests that mortality from COVID-19 in cancer patients (1) is probably much higher than recorded, and (2) was not just a competing cause but an additional cause of death in this population since the first year of the pandemic. In other words, mortality from COVID-19 not only took the lives of patients who would die from cancer but added preventable deaths to the mortality burden of this population, especially at the peaks of the pandemic. The results from 2021 contribute to these rationales, as both mortality from cancer as the underlying cause of death and mortality from COVID-19 in cancer patients increased in 2021 compared to 2020.
Compared to 2019, mortality from all types of cancer increased nearly 3.0% in 2022 countrywide, reaching 5.6% in the South region. A study that monitored 40 years of cancer mortality in Brazil reported an increasing trend for all cancers between 2003 and 2017, however, with an average annual percentage variation for the period of 0.2%[29], a much lower increase than observed in 2022. Unlike 2020 and 2021, the 2022 findings align with the hypothesis raised at the beginning of the pandemic – mainly from statistical modeling studies – that cancer mortality would increase due to disruptions in the provision of cancer care[12–15]. As cancer mortality is not an outcome that occurs immediately, analyses with longer follow-ups are necessary. However, the findings from 2022 justify the fear that this worrying movement has already begun.
Results by type of cancer reveal that the mortality from colorectal, female breast, and prostate cancer, despite having reduced in the first year of the pandemic, began to increase from 2021 onwards, with even more significant percentages of increase in 2022. The growth reached 8.5% for colorectal cancer. According to Maruthappu et al.[30], who use the survival analysis of Quaresma, Coleman, and Rachet[31] as a basis for the classification, these are cancers considered treatable, as their five-year survival rate is greater than 50%. Still considering the hypothesis that cancer mortality would increase as a result of delays in diagnosis and treatment of cases, it is reasonable to expect that this impact would be more evident in treatable cancers, i.e., those that would benefit more from timely diagnosis and treatment.
Observational studies have reported changes in the diagnosis and treatment of these cancers during the pandemic in Brazil. The number of mammograms performed by the SUS in 2020 decreased by more than 40%, reaching a 67% reduction in Rondônia, a state in the North of the country[32]. We highlight that this region, which in 2019 already had the worst mammography coverage by the SUS in Brazil[33], showed the most significant increase in mortality from female breast cancer in 2022. Also, the situation remained unfavorable in 2021: 15% fewer exams than in 2019 in Brazil[34]. Analysis that compared new cases of colorectal and anal cancer in the outpatient clinics of a reference center for cancer treatment in São Paulo, reported a decrease in newly diagnosed patients referred and an increase in locally advanced disease from March to July 2020 compared to the same period in 2019. The authors argue that the difficulty of having colonoscopies and the patient's fear of going to hospital during the pandemic may explain the decrease[35]. Concerning prostate cancer, a study that analyzed the number of therapeutic procedures for this type of cancer (radical prostatectomy plus radiotherapy) in Brazil, carried out by the SUS during the pandemic, indicated that there was a 22% reduction between August 2020 and March 2021, compared to the same period in previous years[36]. The present study suggests that the increase in mortality from colorectal, female breast, and prostate cancer (i.e., treatable cancers) identified in 2022 may be due to the disruptive effect of the pandemic on the cancer care network – and warns that this consequence may last for a few years.
TBL neoplasms were those with the lowest variation in mortality in 2022 compared to the pre-pandemic year. The literature considers this type of cancer non-treatable, as its five-year survival rate is less than 10%[30]. Given that the pandemic impacted the provision of care for TBL cancer, with a relevant reduction in the number of surgeries in the SUS[9], one explanation could be that the disruption of health services less impacts mortality due to neoplasms that are more lethal – and less responsive to the acting of health services. However, the 9.35% increase in mortality from this type of cancer in the Midwest region in 2022 draws attention. A study that analyzed mortality from TBL neoplasms in the Midwest states from 2000 to 2015 found an increasing trend in only two of its four states for the female population, which presented an average annual percentage change (APC) of approximately 1.6%, and in only one state for the male population, with an APC of 0.6%[37]. Therefore, the result of the present study is atypical and deserves more careful investigation. The reductions found in deaths from stomach cancer seem compatible with recent trends for this type of cancer in Brazil[29], with the reduction peaking in 2020 and 2021, following the logic of a competitive cause. It is noteworthy that this type of cancer is not considered a non-treatable neoplasm, but its low five-year survival rate (18.8%[31]) also indicates a non-favorable prognosis.
The North and Northeast had the lowest mortality from COVID-19 in cancer patients in the three pandemic years. There is a substantial chance of underreporting in these regions, as these regions (1) were severely affected by the pandemic, in which the first spikes in mortality due to COVID-19 occurred in the country[38, 39]; and (2) have the most room for improvements concerning the quality of records in SIM[40]. For Brazil and each region separately (results not shown), these rates were higher in the periods corresponding to the peaks of deaths from COVID-19 in the country. These are expected results, as these deaths are a direct consequence of the pandemic and followed its dynamics of resurgence and slowdown. Studies with the American population have identified similar results[24, 25]. The rate of COVID-19 in cancer patients, which is not irrelevant, makes it clear that relying only on the underlying cause of death may lead to underestimating the impact of the pandemic on patients with cancer.
The density of SUS hospital beds was negatively associated with mortality from COVID-19 in cancer patients in the Northeast, South, and the whole country, in an analysis adjusted for the HDI of the analysis units – the 133 RGI in Brazil. These regions correspond to an intermediate geographical stratification between states and cities, which always includes large urban centers. The RGI likely covers the entire path through the health system that a resident of these goes through, with larger cities acting as a reference for smaller nearby cities, which do not have hospitals or health services of greater technological complexity[41]. If a cancer patient with COVID-19 lives in a small town without a hospital and needs hospital attention, they are likely to be referred for hospital treatment in a more structured city close to their local residence. This characteristic makes RGI an opportune territorial division to study the determinants of mortality from COVID-19 in cancer patients, identifying which factors are associated with more favorable regional outcomes. The availability of beds may be crucial in protecting this vulnerable population from preventable deaths, as cancer patients were more likely to develop severe cases of COVID-19[21–23] and, consequently, to depend more on the hospital network. The present results align with this rationale; however, additional investigations that analyze the flow of bed occupancy and/or ICU beds in different regions can contribute to this understanding and support decisions on allocating health resources in possible future crises. Also, the significant results for SUS beds, even with adjustment for HDI, point to the crucial role of the public health system for the cancer population during this outbreak.
The decrease in death rates from cancer as the underlying cause that the present study found in the first year of the pandemic is compatible with the findings of other studies in Brazil[19] and other countries[16–18]. However, this study observed lower decreases than those reported for Brazil[19]. Differences in the definition of the reference rate for comparison and, mainly, the characteristics of the present study could explain these discrepancies. As far as we know, this study is the first to analyze cancer mortality using the final version of the SIM from 2020 and 2021, as well as extending the analysis to the year 2022, and to use data from the 2022 Census of Brazil to calculate the mortality rates. The final versions of the annual mortality databases contain more recorded deaths than preliminary versions, and the 2022 Census reported a smaller population than estimates based on previous censuses. These differences could justify the discrepancies in the results.
The main limitation of this study concerns the registration of deaths. As already mentioned, the quality of recording the underlying cause of death decreased during the pandemic, with an increase in the percentage of deaths with an ill-defined underlying cause compared to previous years[20], which may be an expected consequence of a collapsing health system. To minimize this limitation, the methodology of this study included the redistribution of ill-defined deaths, considering variations by sex, age group, month, and RGI for the analysis of the underlying cause of death; however, no statistical correction replaces qualified registration.
This study suggests an increase in mortality from cancer, especially treatable cancers – colorectal, breast, and prostate –, in 2022 as an impact of the COVID-19 pandemic in Brazil due to the burden that the new disease imposed on health services, especially at the hospital level, and the replacement of health priorities during the health crisis. With cancer diagnoses and treatments delayed due to the overload of hospital care, the patients likely arrived in cancer care services with more advanced diseases and lower chance of survival. As it is a chronic disease whose cure may require years of treatment, which causes sequelae and has the potential for recurrence – factors in part related to access to timely diagnosis and treatment – the deleterious impact of COVID-19 on cancer care may continue to have an impact on mortality from this disease years after the pandemic's control. The literature reports that cancer care disruptions during the COVID-19 pandemic could lead to significant life loss but also argues that this damage could be mitigated by increasing diagnostic and treatment capacity in the short term to address the service backlog[14]. The results of the present study highlight the need to understand what consequences the pandemic may have brought on health services, which can be worked on to prevent the increase in mortality in the coming years. Surveillance in health in the coming years is critical, as well as monitoring the production of cancer diagnosis and treatment services and the delay in the onset of treatment.
Also, concerning the cancer patients, COVID-19 not only took the lives of patients who would die of cancer – it was not one cause of death that replaced another; it likely added preventable deaths to the mortality burden of this population. The availability of SUS hospital beds may have acted as a protective factor against this additional mortality source for the cancer population in Brazil. This evidence can join the accumulated knowledge about the COVID-19 pandemic to assist in equitable strategies to mitigate the COVID-19 impact on the cancer patients and to contribute to decision-making in health crisis.