ABSTRACT
OBJECTIVE
To analyze the impact of the different phases of the covid-19 pandemic on hospitalizations for oral (CaB) and oropharyngeal (CaOR) cancer in Brazil, carried out within the scope of the Brazilian Unified Health System (SUS).
METHODS
We obtained data regarding hospital admissions due to CaB and CaOR between January 2018 and August 2021 from the SUS Hospital Information System, analyzing hospital admissions as rates per 100,000 inhabitants. We divided the pandemic (January 2020 to August 2021) and pre-pandemic (January 2018 to December 2019) periods into four-month periods, comparing the pandemic period rates with analogous rates for the pre-pandemic period – for Brazil, by macro-region and by a group of procedures performed during hospitalization. We also analyzed the impact of the pandemic on the average cost of hospitalizations, expressing the results in percentage change.
RESULTS
Rates of hospitalization in the SUS due to CaB and CaOR decreased during the pandemic in Brazil. The most significant reduction occurred in the second four-month period of 2020 (18.42%), followed by decreases in the third four-month period of 2020 (17.76%) and the first and second four-month periods of 2021 (respectively, 14.64% and 17.07%), compared with 2019. The South and Southeast showed the most expressive and constant reductions between the different phases of the pandemic. Hospitalizations for clinical procedures suffered a more significant decrease than for surgical procedures. In Brazil, the average expenditure per hospitalization in the four-month pandemic periods was higher than in the reference periods.
CONCLUSION
After more than a year of the pandemic’s beginning in Brazil, the SUS hospital care network for CaB and CaOR had yet to be re-established. The repressed demand for hospitalizations for these diseases, which have fast evolution, will possibly result in delays in treatment, negatively impacting the survival of these patients. Future studies are needed to monitor this situation.
Mouth Neoplasms; Oropharyngeal Neoplasms; Hospital Care; Unified Health System; COVID-19; Pandemics
RESUMO
OBJETIVO
Analisar o impacto das diferentes fases da pandemia de covid-19 sobre as hospitalizações por câncer bucal (CaB) e de orofaringe (CaOR) no Brasil, realizadas no âmbito do Sistema Único de Saúde (SUS).
MÉTODOS
Os dados quanto às internações hospitalares por CaB e CaOR, entre janeiro de 2018 e agosto de 2021, foram obtidos no Sistema de Informações Hospitalares do SUS. As internações foram analisadas sob a forma de taxas por 100 mil habitantes. Os períodos de pandemia (janeiro de 2020 a agosto de 2021) e pré-pandemia (janeiro de 2018 a dezembro de 2019) foram divididos em quadrimestres; as taxas quadrimestrais do período pandêmico foram comparadas às taxas análogas do período pré-pandemia – para o Brasil, por macrorregião e por grupo de procedimentos realizados na internação. O impacto da pandemia sobre o valor médio das internações também foi analisado. Os resultados foram expressos em variação percentual.
RESULTADOS
As taxas de internação hospitalar no SUS por CaB e CaOR reduziram durante a pandemia no Brasil. Em comparação com os quadrimestres de 2019, a maior redução foi identificada no segundo quadrimestre de 2020 (18,42%), seguida das reduções do terceiro quadrimestre de 2020 (17,76%) e do primeiro e segundo quadrimestres de 2021 (respectivamente, 14,64% e 17,07%). Sul e Sudeste apresentaram as reduções mais expressivas e constantes entre as diferentes fases da pandemia. As internações para procedimentos clínicos sofreram maior redução do que para procedimentos cirúrgicos. No Brasil, o gasto médio por internação nos quadrimestres da pandemia foi maior do que nos quadrimestres de referência.
CONCLUSÃO
Após mais de um ano do início da pandemia no Brasil, a rede hospitalar de cuidado ao CaB e CaOR do SUS ainda não tinha se restabelecido. A demanda reprimida de hospitalizações por essas doenças, que são de rápida evolução, possivelmente resultará em atrasos para tratamento, com impacto negativo para a sobrevida desses pacientes; futuros estudos são necessários para monitorar essa situação.
Neoplasias Bucais; Neoplasias Orofaríngeas; Hospitalização; Sistema Único de Saúde; COVID-19; Pandemias
INTRODUCTION
Cancer currently occupies the second position among the diseases that cause the most deaths and years of life lost due to disability worldwide. According to the 2019 Global Burden of Disease Study, oral (CaB) and oropharyngeal (CaOR) cancers accounted for approximately 2.3% of new cases and 3.1% of deaths from all cancers in the world in 2019, which represents about 540,000 new cases and 313,000 deaths11. Kocarnik JM, Compton K, Dean FE, Fu W, Gaw BL, Harvey JD, et al. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: a systematic analysis for the global burden of disease study 2019. JAMA Oncol. 2022 Mar;8(3):420-44. https://doi.org/10.1001/jamaoncol.2021.6987
https://doi.org/10.1001/jamaoncol.2021.6...
. In Brazil, this subtype occupies the fifth position among the most frequent neoplasms in men22. Ministério da Saúde (BR). Instituto Nacional do Câncer José Alencar Gomes da Silva. Estimativa 2020: incidência de câncer no Brasil. Rio de Janeiro: INCA; 2019.. Its incidence in Brazil, for both sexes, was estimated at 5.6 cases per 100,000 inhabitants by the Global Cancer Observatory 2020 (Globocan); it is the second highest rate in Latin America, lower only than the rate in Cuba33. International Agency for Research on Cancer. Cancer today. Lyon: World Health Organization. 2022 [cited 2022 Jan 10]. Available from: https://gco.iarc.fr/today/online-analysis-map?v=2020&mode=population&mode_population=continents&population=9 00&populations=900&key=asr&sex=0&cancer=39&type=0&statistic=5&prevalence=0& population_group=0&ages_group%5B%5D=0&ages_group%5B%5D=17&nb_items=10&gr
https://gco.iarc.fr/today/online-analysi...
.
The treatment of CaB and CaOR involves surgery and/or radiotherapy associated, or not, with chemotherapy and depends on the hospital structure44. Pfister DG, Spencer S, Adkins D, Birkeland AC, Brizel DM, Busse PM, et al. Head and neck cancers: NCCN guidelines. Plymouth Meeting: NCCN; 2021 [cited 2022 Mar 9]. Available from: https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1437
https://www.nccn.org/guidelines/guidelin...
. Surgeries, which tend to be highly complex, require hospitalization, and radio and chemotherapy treatments, as well as clinical treatments for complications or intercurrences, may also require hospital care. Invasive or advanced-stage lesions often involve mutilating surgical approaches, such as glossectomy and maxillectomy, of which possible consequences are orofacial deformities and functional deficits. Due to treatment sequelae, these patients may depend on hospital care, including recurrent and long-period hospitalizations. More than half of patients with head and neck cancer – a group that includes oral and oropharyngeal cancers – start treatment with lesions in advanced stages55. Abrahão R, Perdomo S, Pinto LF, Carvalho FN, Dias FL, Podestá JR, et al. Predictors of survival after head and neck squamous cell carcinoma in South America: the interchange study. JCO Glob Oncol. 2020 Mar;6(6):486-99. https://doi.org/10.1200/GO.20.00014
https://doi.org/10.1200/GO.20.00014...
,66. Kowalski LP, Oliveira MM, Lopez RV. E Silva DRM, Ikeda MK, Curado MP. Survival trends of patients with oral and oropharyngeal cancer treated at a cancer center in São Paulo, Brazil. Clinics (São Paulo). 2020;75(4):1-8. https://doi.org/10.6061/clinics/2020/e1507
https://doi.org/10.6061/clinics/2020/e15...
and, consequently, are more dependent on highly complex care and the hospital environment. Oral and oropharyngeal cancers are considered health problems with high economic and social impact, and, in general, the more complex the treatment required, the more expensive it becomes77. Speight PM, Palmer S, Moles DR, Downer MC, Smith DH, Henriksson M, et al. The cost-effectiveness of screening for oral cancer in primary care. Health Technol Assess. 2006 Apr;10(14):1-144. https://doi.org/10.3310/hta10140
https://doi.org/10.3310/hta10140...
. From 2008 to 2016, the Brazilian Unified Health System (SUS) spent around 500 million reais on hospitalizations to treat this subtype of cancer88. Milani V, Zara AL, da Silva EN, Cardoso LB, Curado MP, Ribeiro-Rotta RF. Direct healthcare costs of lip, oral cavity and oropharyngeal cancer in Brazil. PLoS One. 2021 Feb;16(2):e0246475. https://doi.org/10.1371/journal.pone.0246475
https://doi.org/10.1371/journal.pone.024...
.
The covid-19 pandemic has affected health systems worldwide, and care provision to cancer patients has also reflected this health crisis. Reduction in the routine activities of cancer care services and the number of surgeries, postponement of elective treatments and diagnostic procedures, and suspension of screening services were some of the impacts reported in the literature99. Riera R, Bagattini AM, Pacheco RL, Pachito DV, Roitberg F, Ilbawi A. Delays and disruptions in cancer health care due to COVID-19 pandemic: systematic review. JCO Glob Oncol. 2021 Feb;7(7):311-23. https://doi.org/10.1200/GO.20.00639
https://doi.org/10.1200/GO.20.00639...
,1010. Amit M, Tam S, Bader T, Sorkin A, Benov A. Pausing cancer screening during the severe acute respiratory syndrome coronavirus 2pandemic: should we revisit the recommendations? Eur J Cancer. 2020 Jul;134:86-9. https://doi.org/10.1016/j.ejca.2020.04.016
https://doi.org/10.1016/j.ejca.2020.04.0...
. The fear of contamination by the new disease may also have kept symptomatic patients away from health services. Regarding CaB and CaOR, empirical evidence from the initial period of the pandemic indicated a reduction in the number of diagnostic procedures and hospitalizations in Brazil1111. Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on hospitalizations for oral and oropharyngeal cancer in Brazil. Community Dent Oral Epidemiol. 2021 Jun;49(3):211-5. https://doi.org/10.1111/cdoe.12632
https://doi.org/10.1111/cdoe.12632...
,1212. Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on oral biopsies in the Brazilian National Health System. Oral Dis. 2020 Aug;28(51):925-8. https://doi.org/10.1111/odi.13620
https://doi.org/10.1111/odi.13620...
, even in the face of the non-interruption of the operation of reference cancer services in the country. Timely diagnosis and treatment are critical factors for the survival of patients with CaB and CaOR55. Abrahão R, Perdomo S, Pinto LF, Carvalho FN, Dias FL, Podestá JR, et al. Predictors of survival after head and neck squamous cell carcinoma in South America: the interchange study. JCO Glob Oncol. 2020 Mar;6(6):486-99. https://doi.org/10.1200/GO.20.00014
https://doi.org/10.1200/GO.20.00014...
,1313. Schutte HW, Heutink F, Wellenstein DJ, Broek GB, Hoogen FJA, Marres HAM, et al. Impact of time to diagnosis and treatment in head and neck cancer: a systematic review. Otolaryngol – Head Neck Surg (United States). 2020;162(4):446-57. https://doi.org/10.1177/0194599820906387
https://doi.org/10.1177/0194599820906387...
,1414. Graboyes EM, Kompelli AR, Neskey DM, Brennan E, Nguyen S, Sterba KR, et al. Association of treatment delays with survival for patients with head and neck cancer: a systematic review. JAMA Otolaryngol Head Neck Surg. 2019 Feb;145(2):166-77. https://doi.org/10.1001/jamaoto.2018.2716
https://doi.org/10.1001/jamaoto.2018.271...
, and due to their potential to cause delays in the identification and treatment of these diseases, possible disruptions in the care network due to the pandemic need to be understood.
At the beginning of March 2022 – this study’s conduction period –, Brazil had more than 29 million confirmed cases and about 653,000 deaths by covid-191515. Ministério da Saúde (BR). Departamento de Informática do SUS. Painel Coronavírus. Brasília, DF. 2021 [cited 2022 Mar 9]. Available from: https://covid.saude.gov.br/
https://covid.saude.gov.br/...
. Since February 2020, when the first case of the disease was reported in the country, the pandemic has been characterized by different phases, with periods of resurgence and others of attenuation. Although national lockdown policies were not implemented, there was greater rigidity in local measures (municipal and state) of social distancing in periods of worsening pandemic1616. Moraes RF, Silva LL, Toscano CM. Covid-19 e medidas de distancimaneto social no Brasil: análise comparativa dos planos estaduais de flexibilização. Brasília, DF: IPEA; 2020. (Nota Técnica Dinte, n. 25).. During these periods, the Brazilian health system faced intense overload, which may have impacted the care for other diseases prevalent in the country. However, the impact of the breakdown of health services on care for other conditions, considering the different stages of the pandemic in Brazil, is not yet known. Surveillance of cancer care services is essential to maintain their effectiveness and to comprehend and mitigate the possible effects of the current health crisis in the care of this disease. Thus, this study aims to analyze the impact of covid-19 on hospitalizations for CaB and CaOR in the SUS, considering the different phases of the pandemic.
METHODS
This study analyzed hospitalizations for CaB and CaOR (ICD-10 C00-C10), recorded in the SUS Hospital Information System (SIH-SUS) between January 2018 and August 2021. This information system consolidates and makes available – publicly and anonymously – data on all hospital admissions in Brazil within the scope of the SUS. To ensure that the most recent periods of the study did not reflect possible delays in the consolidation of data by the SIH – as hospitalizations can be processed in the SIH with some delay concerning the period in which they occurred –, information from the period of interest was retrieved from the databases from the months following that period (until November 2021). The SIH databases, made available by month and by Federation Unit (UF), were unified using the TabWin, a tabulation tool the Brazilian Ministry of Health offers.
We compared the months of the pandemic period (2020 and 2021) with their analogs in the reference period (2018 and 2019) to analyze the effect of the pandemic on hospital admissions for CaB and CaOR – the comparison of the pandemic years with the average of the years 2018 and 2019 was performed as a validation analysis of the comparison with the year 2019. We analyzed the study period by month and four-month period, assessing monthly and four-monthly hospitalizations using rates – dividing the number of hospitalizations in the month or the four months in each UF and macro-region by the number of inhabitants and multiplying by 100,000. We collected the number of hospitalizations by the state of residence and month of hospitalization and obtained the number of inhabitants in each UF/macro-region using population projections from the Brazilian Institute of Geography and Statistics (IBGE). We presented the comparison between the rates as a percentage of variation, obtained by the equation: [(rate of the pandemic period under analysis/rate of the comparable period in the reference year) -1] *100.
Each hospital admission recorded in the SIH is linked to the primary procedure performed in that hospitalization. We extracted the number of procedures per group from the SIH using the Procedure Group selection to understand the impact of the pandemic on the types of procedures performed on patients hospitalized for CaB and CaOR. The SUS classifies the procedures performed in their health services into eight groups. Groups 3 (Clinical Procedures) and 4 (Surgical Procedures) are the main ones for hospitalizations in which the primary diagnosis is CaB and CaOR. We analyzed the four-monthly number of procedures for these two groups using rates – dividing the number of clinical and surgical procedures (separately) in the four months in each macro-region by the number of inhabitants and multiplying by 100,000. We compared the 2021 and 2020 rates with 2019 as a percentage of change. Finally, we calculated the average expenditure per hospitalization to analyze the impact of the pandemic on the amounts spent on hospitalizations. We divided the total amount spent on hospitalizations due to CaB and CaOR (which included hospital and professional services) per four-month period by the number of hospitalizations in the same period, in each macro-region – both metrics obtained from the SIH. Then, we compared the mean value per hospitalization between the four months of the pandemic with its analogs in the reference period.
We presented this study’s results by UF and macro-region of Brazil: North, Northeast, Southeast, South, and Midwest. For the presentation by UF, we created maps with cartographic bases obtained through the IBGE website. All analyses employed the Stata 14.0 software.
RESULTS
Hospitalization rates for CaB and CaOR in Brazil carried out by the SUS reduced in pandemic years compared with the reference years (2018 and 2019). For Brazil, the most significant reductions occurred in the second and third four-month periods of 2020 and the first and second ones of 2021, respectively, 18.42%, 17.76%, 14.64%, and 17.07% of reduction, considering the comparison with the rates of the analogous 2019 four-month periods. In these periods, a decrease occurred in the rates of the country’s five regions. The South presented the most expressive decreases (above 20%), while the Northeast region had the smallest reductions in the third four-month period of 2020 and the first and second four-month periods of 2021 – of less than 5%. Table 1 shows these results and the rates for each period.
Four-month period rate of hospital admissions for oral and oropharyngeal cancer (per 100,000 inhabitants) by macro-region, and for Brazil, considering the pre-pandemic (2018 and 2019) and the pandemic (2020 and 2021) periods, and percentage difference between the periods.
Figure 1 shows the monthly behavior of hospitalizations due to CaB and CaOR in Brazil, considering the period from January 2019 to August 2021. According to the Figure, the first significant drop in the rates of this indicator occurred in April 2020, i.e., at the end of the first four-month period of 2020. Since then, the indicators have remained below the level prior to that period. After this initial drop, September, October, and November 2020 showed slightly higher rates than the other months – however, still far from the pre-pandemic level. The hospitalization rates for the months of 2021 are lower than those for 2020. Despite the behavior suggestive of recovery in the last analyzed month of that year (August 2021), it is still far from the pre-pandemic level.
Monthly rate of hospital admissions (per 100,000 inhabitants) for oral and oropharyngeal cancer in Brazil, considering the pre-pandemic (2019) and pandemic (2020 and 2021) periods.
Figure 2 shows the variation in hospitalization rates by CaB and CaOR by UF, comparing the years 2021 and 2020 with 2019. The results indicate the predominance of a pattern of rate reduction. In addition, they indicated that UFs with the highest hospitalization rates in the pre-pandemic period continued showing the highest rates in the pandemic years. In other words, the magnitude of the rates decreased in the pandemic years, but the pre-pandemic spatial pattern of this indicator remained: the lowest rates continued in the UFs in the North and Northeast regions; the highest in those of the South and Southeast regions.
Annual rate of hospitalizations for oral and oropharyngeal cancer (per 100,000 inhabitants) by Federation Unit, considering the pre-pandemic (2019) and pandemic (2020 and 2021) periods.
The analysis of the groups of procedures performed on patients hospitalized for CaB and CaOR indicated that clinical procedures suffered a more significant reduction than surgical ones, comparing the 2021 and 2020 four-month periods with those of 2019. From the second four-month period of 2020 onward, the rates of both groups of procedures decreased in all periods. However, the decrease percentage was consistently more significant in rates for clinical procedures. Compared to the 2019 four-month periods, the most significant variation in the rates of clinical procedures occurred in the second four-month period of 2020 (-24.62%). In that same period, the variation in surgical procedures was -11.97% (Table 2). The clinical (Group 3) and surgical (Group 4) procedures together accounted for approximately 99.8% of all procedures performed on these patients in 2019, 2020, and 2021 (in 2019: Group 3 – 52.17% and Group 4 – 47.66%; in 2020: Group 3 – 49.81% and Group 4 – 49.97%; in 2021: Group 3 – 48.61% and Group 4 – 51.17%; data not shown).
Four-month period rate of clinical and surgical procedures (per 100,000 inhabitants) in hospital admissions for oral and oropharyngeal cancer, by macro-region, and for Brazil, considering the pre-pandemic (2019) and pandemic (2020 and 2021) periods, and the percentage difference between periods.
Figure 3 presents the variation in average expenditure per hospitalization, considering the pre-pandemic and pandemic periods. In Brazil, the average spending per hospitalization in the four months of the pandemic was higher than in the comparable four-month period of the reference year (2019). This pattern also occurred in the South, Southeast, and Northeast regions – the latter had the third four-month period of 2020 as an exception, whose average expenditure per hospitalization was lower than in the same period in 2019. The North and Midwest showed a different behavior, with some four-month periods of the pandemic period having an average cost per hospitalization higher than in the pre-pandemic period, but others with the opposite situation (Figure 3).
Average expenditure per hospitalization for oral and oropharyngeal cancer (in BRL), by four-month period, by macro-region, and for Brazil, considering the pre-pandemic (2019) and pandemic (2020 and 2021) periods.
In general, the analyses considering 2019 as a reference showed similar results to the validation analysis, which considered 2018 and 2019 average values as a reference.
DISCUSSION
This study showed that hospitalizations for CaB and CaOR carried out by the SUS decreased in all phases of the pandemic in Brazil. The first and most crucial reduction occurred in the second four-month period of 2020 when the pandemic began to intensify in the country, prompting local governments to institute social distancing measures to contain the so-called first wave. From then on – until the end of the study period – even though there were periods with a less expressive reduction than that experienced in the second four-month period of 2020, hospital admissions for CaB and CaOR carried out by the SUS no longer returned to their pre-pandemic level. Identifying a sustained reduction in these rates is one of the main results of this analysis. By investigating the impact of the pandemic on hospital admissions for CaB and CaOR within the public health system in Brazil, this investigation provided evidence of the magnitude and distribution of the problem and can contribute to mitigating it.
Since they are considered essential, the SUS’s hospital and cancer care services remained in operation during the pandemic in Brazil. However, maintaining these services did not prevent the health crisis triggered by covid-19 from affecting hospital capacity for this disease, as indicated by the results of this article and research carried out in the initial period of the pandemic1111. Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on hospitalizations for oral and oropharyngeal cancer in Brazil. Community Dent Oral Epidemiol. 2021 Jun;49(3):211-5. https://doi.org/10.1111/cdoe.12632
https://doi.org/10.1111/cdoe.12632...
,1717. Costa AM, Ribeiro AL, Ribeiro AG, Gini A, Cabasag C, Reis RM, et al. Impact of COVID-19 pandemic on cancer-related hospitalizations in Brazil. Cancer Contr. 2021;28:1-7. https://doi.org/10.1177/10732748211038736
https://doi.org/10.1177/1073274821103873...
. Possible reasons for this effect are diverse and may be related to the overload of the hospital structure due to the influx of cases of covid-19 requiring hospitalization, the concern to guarantee hospital beds for these cases, the lack of professionals, supplies, and/or equipment – depleted or reallocated for covid-19 assistance –, to the social consequences of the social distancing measures, and the economic crisis arising from the health crisis and the fear of the patients themselves of being infected by the new virus, thus choosing not to seek the healthcare services1818. Jazieh AR, Akbulut H, Curigliano G, Rogado A, Alsharm AA, Razis ED, et al. Impact of the COVID-19 Pandemic on cancer care: a global collaborative study. JCO Glob Oncol. 2020 Sep;6(6):1428-38. https://doi.org/10.1200/GO.20.00351
https://doi.org/10.1200/GO.20.00351...
,1919. Vanni G, Materazzo M, Pellicciaro M, Ingallinella S, Rho M, Santori F, et al. Breast cancer and COVID-19: the effect of fear on patients’ decision-making process. In Vivo. 2020 Jun;34(3 Suppl):1651-9. https://doi.org/10.21873/invivo.11957
https://doi.org/10.21873/invivo.11957...
, among others. Other countries, such as India, Spain, and the United Kingdom, also reported reductions in the capacity of the hospital system to treat cases of head and neck cancer due to the pandemic scenario2020. Gupta A, Arora V, Nair D, Agrawal N, Su YX, Holsinger FC, et al. Status and strategies for the management of head and neck cancer during COVID-19 pandemic: indian scenario. Head Neck. 2020 Jul;42(7):1460-5. https://doi.org/10.1002/hed.26227
https://doi.org/10.1002/hed.26227...
. In Spain, a study carried out in 44 hospital services indicated that 45.5% of them had to suspend oncological surgeries considered high priority in patients with head and neck cancer at some point during the pandemic2121. Mayo-Yáñez M, Palacios-García JM, Calvo-Henríquez C, Ayad T, Saydy N, León X, et al. COVID-19 pandemic and its impact on the management of head and neck cancer in the spanish healthcare system. Int Arch Otorhinolaryngol. 2021 Aug;25(4):e610-5. https://doi.org/10.1055/s-0041-1736425
https://doi.org/10.1055/s-0041-1736425...
. However, these results are not directly comparable to those of this study – despite the similarity of the theme, the outcomes under analysis are different.
The reduction in cancer hospitalizations may still indicate, in part, postponement of treatment due to medical decisions to balance risks, as cancer patients have worse outcomes when affected by covid-19 than the general population2323. Liang W, Guan W, Chen R, Wang W, Li J, Xu K, et al. Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China. Lancet Oncol. 2020 Mar;21(3):335-7. https://doi.org/10.1016/S1470-2045(20)30096-6
https://doi.org/10.1016/S1470-2045(20)30...
,2424. Wu Z, McGoogan JM. Characteristics of and important lessons from the Coronavirus Disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. JAMA. 2020 Apr;323(13):1239-42. Available from: https://jamanetwork.com/ https://doi.org/10.1001/jama.2020.2648
https://jamanetwork.com/...
. However, specifically for CaB and CaOR, this is not the recommended situation. A statistical modeling study estimated that, in the pandemic context, cases of CaB and CaOR would be among the types most favored by immediate treatment, compared with postponement2525. Hartman HE, Sun Y, Devasia TP, Chase EC, Jairath NK, Dess RT, et al. Integrated survival estimates for cancer treatment delay among adults with cancer during the COVID-19 pandemic. JAMA Oncol. 2020 Dec;6(12):1881-9. https://doi.org/10.1001/jamaoncol.2020.5403
https://doi.org/10.1001/jamaoncol.2020.5...
. In updated recommendations for the period of the covid-19 pandemic, the European Society for Medical Oncology indicates that mouth and oropharynx tumors at the T1 stage should already be a high/medium priority for primary surgery, and all other ones should be a high priority2626. European Society for Medical Oncology. Head and neck cancers in the COVID-19 era. Lugano: SMO; 2021 [cited 2022 Mar 7]. Available from: https://www.esmo.org/guidelines/cancer-patient-management-during-the-covid-19-pandemic/head-and-neck-cancers-in-the-covid-19-era
https://www.esmo.org/guidelines/cancer-p...
. Therefore, we believe that the reduction in hospitalizations found in this analysis is not essentially reflecting programmed delays in the treatment of neoplasms. The results may represent more serious situations, such as (1) barriers to accessing hospital treatment during the pandemic; and (2) impacts of the pandemic on the diagnosis of these diseases, with under-identifying cases that should be admitted to the hospital network for treatment. Decreased numbers of diagnostic procedures for oral cancer occurred in Brazil1212. Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on oral biopsies in the Brazilian National Health System. Oral Dis. 2020 Aug;28(51):925-8. https://doi.org/10.1111/odi.13620
https://doi.org/10.1111/odi.13620...
,2727. Gomes AP, Schuch LF, Tarquinio SB, Etges A, Vasconcelos AC. Reduced demand for oral diagnosis during COVID-19: a Brazilian center experience. Oral Dis. 2022 Apr;28(Suppl 1):5958-9. Epub. fev 2020;1-2: https://doi.org/10.1111/odi.13547
https://doi.org/10.1111/odi.13547...
,2828. Abrantes TC, Bezerra KT, Silva CN, Costa LC, Cabral MG, Agostini M, et al. Oral cancer diagnosis during the COVID-19 pandemic in an oral pathology laboratory in Rio de Janeiro, Brazil. Oral Dis. 2022 Apr;28(Suppl 1):997-8. E-pub:1-2, 2020. https://doi.org/10.1111/odi.13669
https://doi.org/10.1111/odi.13669...
. The reduction in hospitalizations due to underdiagnosis is a likely and worrying scenario, as cases not diagnosed during this period may arrive at hospital services with tumors at a more advanced stage, with a lower survival chance55. Abrahão R, Perdomo S, Pinto LF, Carvalho FN, Dias FL, Podestá JR, et al. Predictors of survival after head and neck squamous cell carcinoma in South America: the interchange study. JCO Glob Oncol. 2020 Mar;6(6):486-99. https://doi.org/10.1200/GO.20.00014
https://doi.org/10.1200/GO.20.00014...
,1313. Schutte HW, Heutink F, Wellenstein DJ, Broek GB, Hoogen FJA, Marres HAM, et al. Impact of time to diagnosis and treatment in head and neck cancer: a systematic review. Otolaryngol – Head Neck Surg (United States). 2020;162(4):446-57. https://doi.org/10.1177/0194599820906387
https://doi.org/10.1177/0194599820906387...
,1414. Graboyes EM, Kompelli AR, Neskey DM, Brennan E, Nguyen S, Sterba KR, et al. Association of treatment delays with survival for patients with head and neck cancer: a systematic review. JAMA Otolaryngol Head Neck Surg. 2019 Feb;145(2):166-77. https://doi.org/10.1001/jamaoto.2018.2716
https://doi.org/10.1001/jamaoto.2018.271...
,2929. Sud A, Torr B, Jones ME, Broggio J, Scott S, Loveday C, et al. Effect of delays in the 2-week-wait cancer referral pathway during the COVID-19 pandemic on cancer survival in the UK: a modelling study. Lancet Oncol. 2020 Aug;21(8):1035-44. https://doi.org/10.1016/S1470-2045(20)30392-2
https://doi.org/10.1016/S1470-2045(20)30...
.
This study analyzed the phases of the pandemic by four months and, considering the variation in the weekly number of deaths in the country since the notification of the first case (in February 2020)1515. Ministério da Saúde (BR). Departamento de Informática do SUS. Painel Coronavírus. Brasília, DF. 2021 [cited 2022 Mar 9]. Available from: https://covid.saude.gov.br/
https://covid.saude.gov.br/...
, assumed that the first four-month period of 2020 represented the initial period of the pandemic in Brazil; the second represented the first wave; the third, the first period of attenuation of social distancing measures; and finally, the two four-month periods of 2021 represented the second wave of the pandemic. The first and most crucial drop in hospital admissions for CaB and CaOR within the scope of the SUS occurred in the first wave phase, when the health system faced its first collapse, with the depletion of material and human resources and structural overload due to the intense spread of covid-19 across the country. This was also the phase in which local governments implemented the most restrictive social distancing measures1616. Moraes RF, Silva LL, Toscano CM. Covid-19 e medidas de distancimaneto social no Brasil: análise comparativa dos planos estaduais de flexibilização. Brasília, DF: IPEA; 2020. (Nota Técnica Dinte, n. 25).. The reductions identified in the first wave phase are, therefore, compatible with the disorderly character of that period. However, although there were slight recoveries compared with the first wave phase, none of the subsequent ones showed a return of rates to pre-pandemic levels. The maintenance of these reductions more than a year after the start of the pandemic suggests that the impact of this health crisis on hospital care for CaB and CaOR was not a momentary situation, resulting only from an initial adaptation of care to a new and atypical context. The impact of this sustained reduction in mortality/survival from these neoplasms in the short and medium term is still uncertain and needs to be monitored, mainly because these are subtypes of cancer that, in regular times, are already too lethal – the average five-year survival is 50%55. Abrahão R, Perdomo S, Pinto LF, Carvalho FN, Dias FL, Podestá JR, et al. Predictors of survival after head and neck squamous cell carcinoma in South America: the interchange study. JCO Glob Oncol. 2020 Mar;6(6):486-99. https://doi.org/10.1200/GO.20.00014
https://doi.org/10.1200/GO.20.00014...
.
This study also identified that the reduction in hospital admissions carried out by the SUS varied in magnitude in the different macro-regions of the country. The North and, above all, the Northeast were the regions that showed the smallest reductions in hospitalization rates. On the other hand, the South and Southeast regions showed more significant and constant reductions during the different phases of the pandemic. Brazil’s South and Southeast regions have the best indicators of access to health services3030. Stopa SR, Malta DC, Monteiro CN, Szwarcwald CL, Goldbaum M, Cesar CL. Acesso e uso de serviços de saúde pela população brasileira, Pesquisa Nacional de Saúde 2013. Rev Saúde Publica. 2017;51(1):1s-11s. https://doi.org/10.1590/S1518-8787.2017051000074
https://doi.org/10.1590/S1518-8787.20170...
, including higher rates of procedures for diagnosing oral cancer1212. Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on oral biopsies in the Brazilian National Health System. Oral Dis. 2020 Aug;28(51):925-8. https://doi.org/10.1111/odi.13620
https://doi.org/10.1111/odi.13620...
. Due to the more significant provision of health services in these regions, more malignant lesions are likely diagnosed and, proportionally, more in the initial stages. As cancer diagnosis was an area greatly affected by the pandemic in the country, regions that performed more of these procedures possibly showed more significant reductions in hospitalizations. Furthermore, cases in initial staging are less likely to have been prioritized for treatment by the health system in the context of a health crisis since, given the limited supply of hospital structure for treatment, more advanced and urgent cases are expectedly prioritized.
The South and Southeast regions showed a notable increase in the mean value per hospitalization for CaB and CaOR, starting from the first wave phase – for the other regions, this trend was not so clear. We hypothesize that the South and Southeast have a higher possibility of organizing the flow of care in periods of limited resources through selective screening, including telemedicine, monitoring cases, and prioritizing more serious situations – which require more costly interventions. However, the pattern of expenditures in these regions may also reflect a decrease in the diagnosis of lesions at an earlier stage, which requires less invasive and costly treatments. Finally, clinical procedures linked to hospitalizations decreased more than surgical procedures in all pandemic phases, starting from the first wave phase. Guidelines for managing CaB and CaOR during the pandemic did not advocate replacing surgery with other treatment modalities. We believe the present results indicate that clinical demands are more likely to correspond to an elective and postponable or manageable need in an outpatient setting than surgical demands.
This study has several limitations that must be considered when interpreting its results. The SIH covers hospitalizations carried out by the SUS and does not consider those occurring within the scope of the supplementary network (private hospitals and those with health insurance agreements). Therefore, this study does not present an overview of all hospitalizations due to CaB and CaOR that occurred in the country. Data from the 2019 National Health Survey indicate that approximately 71.5% of the Brazilian population does not have a health insurance plan3131. Szwarcwald CL, Stopa SR, Damacena GN, Almeida WD, Souza Júnior PR, Vieira ML, et al. Mudanças no padrão de utilização de serviços de saúde no Brasil entre 2013 e 2019. Cien Saúde Colet. 2021 Jun;26 suppl 1:2515-28. https://doi.org/10.1590/1413-81232021266.1.43482020
https://doi.org/10.1590/1413-81232021266...
, thus depending on the SUS for care/hospitalization needs. In addition, oral cancer is an outcome associated with socioeconomic conditions: individuals in more vulnerable situations – and who, consequently, depend more on public health services – are at increased risk of developing this disease3232. Conway DI, Petticrew M, Marlborough H, Berthiller J, Hashibe M, Macpherson LM. Socioeconomic inequalities and oral cancer risk: a systematic review and meta-analysis of case-control studies. Int J Cancer. 2008 Jun;122(12):2811-9. https://doi.org/10.1002/ijc.23430
https://doi.org/10.1002/ijc.23430...
. Therefore, despite analyzing only data linked to the SUS, this article includes a significant portion of the population affected by this disease. Considering the universal nature of the SUS and the impossibility of accurately equating the proportion of patients with CaB and CaOR using health insurance plans in the hospital environment, it is noteworthy that the rates presented were calculated using the total population as a denominator.
The hospitalization rates presented here may account for more than one hospital admission of the same patient for the same cause, as the SIH provides consolidated data; therefore, these duplications cannot be identified and excluded. However, this is not a critical limitation for this analysis, which aimed to measure reductions in the provision of hospital services possibly associated with the pandemic without considering aspects related to individual risks. Furthermore, we highlight that analyzing the data by macro-region and using the four months to represent the pandemic phases – with standardization of this division for all regions – disregards the heterogeneity in the space-time patterns of dissemination present in the course of the pandemic in Brazil. Future studies that consider local characteristics of the dynamics of the pandemic in the country may be necessary.
This study revealed that, after more than a year of the beginning of the pandemic in Brazil, the hospital care network for CaB and CaOR of the SUS had not yet been re-established. It also showed evidence that, during the pandemic, the hospital network prioritized more serious cases of CaB and CaOR. The hospitalizations reductions may reflect barriers to access to hospital treatment due to the pandemic’s overload and disruption of this sector. The repressed demand for hospitalizations for cases of CaB and CaOR, which are rapidly evolving diseases, will be (and already is) related to delays in starting treatment, with a negative impact on the survival of these patients – a situation that will worsen proportionally to the time this breakdown lasts. This study highlights the need for health management attention to the CaB and CaOR care network, as this, in addition to the immediate need to resume its care capacity, will probably need to expand it in the short term to mitigate the probable damage caused by the pandemic in the care of these diseases and prevent this disruption from increasing the mortality.
REFERENCES
-
1Kocarnik JM, Compton K, Dean FE, Fu W, Gaw BL, Harvey JD, et al. Cancer incidence, mortality, years of life lost, years lived with disability, and disability-adjusted life years for 29 cancer groups from 2010 to 2019: a systematic analysis for the global burden of disease study 2019. JAMA Oncol. 2022 Mar;8(3):420-44. https://doi.org/10.1001/jamaoncol.2021.6987
» https://doi.org/10.1001/jamaoncol.2021.6987 -
2Ministério da Saúde (BR). Instituto Nacional do Câncer José Alencar Gomes da Silva. Estimativa 2020: incidência de câncer no Brasil. Rio de Janeiro: INCA; 2019.
-
3International Agency for Research on Cancer. Cancer today. Lyon: World Health Organization. 2022 [cited 2022 Jan 10]. Available from: https://gco.iarc.fr/today/online-analysis-map?v=2020&mode=population&mode_population=continents&population=9 00&populations=900&key=asr&sex=0&cancer=39&type=0&statistic=5&prevalence=0& population_group=0&ages_group%5B%5D=0&ages_group%5B%5D=17&nb_items=10&gr
» https://gco.iarc.fr/today/online-analysis-map?v=2020&mode=population&mode_population=continents&population=9 00&populations=900&key=asr&sex=0&cancer=39&type=0&statistic=5&prevalence=0& population_group=0&ages_group%5B%5D=0&ages_group%5B%5D=17&nb_items=10&gr -
4Pfister DG, Spencer S, Adkins D, Birkeland AC, Brizel DM, Busse PM, et al. Head and neck cancers: NCCN guidelines. Plymouth Meeting: NCCN; 2021 [cited 2022 Mar 9]. Available from: https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1437
» https://www.nccn.org/guidelines/guidelines-detail?category=1&id=1437 -
5Abrahão R, Perdomo S, Pinto LF, Carvalho FN, Dias FL, Podestá JR, et al. Predictors of survival after head and neck squamous cell carcinoma in South America: the interchange study. JCO Glob Oncol. 2020 Mar;6(6):486-99. https://doi.org/10.1200/GO.20.00014
» https://doi.org/10.1200/GO.20.00014 -
6Kowalski LP, Oliveira MM, Lopez RV. E Silva DRM, Ikeda MK, Curado MP. Survival trends of patients with oral and oropharyngeal cancer treated at a cancer center in São Paulo, Brazil. Clinics (São Paulo). 2020;75(4):1-8. https://doi.org/10.6061/clinics/2020/e1507
» https://doi.org/10.6061/clinics/2020/e1507 -
7Speight PM, Palmer S, Moles DR, Downer MC, Smith DH, Henriksson M, et al. The cost-effectiveness of screening for oral cancer in primary care. Health Technol Assess. 2006 Apr;10(14):1-144. https://doi.org/10.3310/hta10140
» https://doi.org/10.3310/hta10140 -
8Milani V, Zara AL, da Silva EN, Cardoso LB, Curado MP, Ribeiro-Rotta RF. Direct healthcare costs of lip, oral cavity and oropharyngeal cancer in Brazil. PLoS One. 2021 Feb;16(2):e0246475. https://doi.org/10.1371/journal.pone.0246475
» https://doi.org/10.1371/journal.pone.0246475 -
9Riera R, Bagattini AM, Pacheco RL, Pachito DV, Roitberg F, Ilbawi A. Delays and disruptions in cancer health care due to COVID-19 pandemic: systematic review. JCO Glob Oncol. 2021 Feb;7(7):311-23. https://doi.org/10.1200/GO.20.00639
» https://doi.org/10.1200/GO.20.00639 -
10Amit M, Tam S, Bader T, Sorkin A, Benov A. Pausing cancer screening during the severe acute respiratory syndrome coronavirus 2pandemic: should we revisit the recommendations? Eur J Cancer. 2020 Jul;134:86-9. https://doi.org/10.1016/j.ejca.2020.04.016
» https://doi.org/10.1016/j.ejca.2020.04.016 -
11Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on hospitalizations for oral and oropharyngeal cancer in Brazil. Community Dent Oral Epidemiol. 2021 Jun;49(3):211-5. https://doi.org/10.1111/cdoe.12632
» https://doi.org/10.1111/cdoe.12632 -
12Cunha AR, Antunes JL, Martins MD, Petti S, Hugo FN. The impact of the COVID-19 pandemic on oral biopsies in the Brazilian National Health System. Oral Dis. 2020 Aug;28(51):925-8. https://doi.org/10.1111/odi.13620
» https://doi.org/10.1111/odi.13620 -
13Schutte HW, Heutink F, Wellenstein DJ, Broek GB, Hoogen FJA, Marres HAM, et al. Impact of time to diagnosis and treatment in head and neck cancer: a systematic review. Otolaryngol – Head Neck Surg (United States). 2020;162(4):446-57. https://doi.org/10.1177/0194599820906387
» https://doi.org/10.1177/0194599820906387 -
14Graboyes EM, Kompelli AR, Neskey DM, Brennan E, Nguyen S, Sterba KR, et al. Association of treatment delays with survival for patients with head and neck cancer: a systematic review. JAMA Otolaryngol Head Neck Surg. 2019 Feb;145(2):166-77. https://doi.org/10.1001/jamaoto.2018.2716
» https://doi.org/10.1001/jamaoto.2018.2716 -
15Ministério da Saúde (BR). Departamento de Informática do SUS. Painel Coronavírus. Brasília, DF. 2021 [cited 2022 Mar 9]. Available from: https://covid.saude.gov.br/
» https://covid.saude.gov.br/ -
16Moraes RF, Silva LL, Toscano CM. Covid-19 e medidas de distancimaneto social no Brasil: análise comparativa dos planos estaduais de flexibilização. Brasília, DF: IPEA; 2020. (Nota Técnica Dinte, n. 25).
-
17Costa AM, Ribeiro AL, Ribeiro AG, Gini A, Cabasag C, Reis RM, et al. Impact of COVID-19 pandemic on cancer-related hospitalizations in Brazil. Cancer Contr. 2021;28:1-7. https://doi.org/10.1177/10732748211038736
» https://doi.org/10.1177/10732748211038736 -
18Jazieh AR, Akbulut H, Curigliano G, Rogado A, Alsharm AA, Razis ED, et al. Impact of the COVID-19 Pandemic on cancer care: a global collaborative study. JCO Glob Oncol. 2020 Sep;6(6):1428-38. https://doi.org/10.1200/GO.20.00351
» https://doi.org/10.1200/GO.20.00351 -
19Vanni G, Materazzo M, Pellicciaro M, Ingallinella S, Rho M, Santori F, et al. Breast cancer and COVID-19: the effect of fear on patients’ decision-making process. In Vivo. 2020 Jun;34(3 Suppl):1651-9. https://doi.org/10.21873/invivo.11957
» https://doi.org/10.21873/invivo.11957 -
20Gupta A, Arora V, Nair D, Agrawal N, Su YX, Holsinger FC, et al. Status and strategies for the management of head and neck cancer during COVID-19 pandemic: indian scenario. Head Neck. 2020 Jul;42(7):1460-5. https://doi.org/10.1002/hed.26227
» https://doi.org/10.1002/hed.26227 -
21Mayo-Yáñez M, Palacios-García JM, Calvo-Henríquez C, Ayad T, Saydy N, León X, et al. COVID-19 pandemic and its impact on the management of head and neck cancer in the spanish healthcare system. Int Arch Otorhinolaryngol. 2021 Aug;25(4):e610-5. https://doi.org/10.1055/s-0041-1736425
» https://doi.org/10.1055/s-0041-1736425 -
22Shaw R, Schache AG, Ho MW, Winter SC, Glasbey J, Ganly I, et al. UK Head and neck cancer surgical capacity during the second wave of the COVID-19 pandemic: have we learned the lessons? COVIDSurg collaborative. Clin Otolaryngol. 2021 Jul;46(4):729-35. https://doi.org/10.1111/coa.13749
» https://doi.org/10.1111/coa.13749 -
23Liang W, Guan W, Chen R, Wang W, Li J, Xu K, et al. Cancer patients in SARS-CoV-2 infection: a nationwide analysis in China. Lancet Oncol. 2020 Mar;21(3):335-7. https://doi.org/10.1016/S1470-2045(20)30096-6
» https://doi.org/10.1016/S1470-2045(20)30096-6 -
24Wu Z, McGoogan JM. Characteristics of and important lessons from the Coronavirus Disease 2019 (COVID-19) outbreak in China: summary of a report of 72 314 cases from the Chinese Center for Disease Control and Prevention. JAMA. 2020 Apr;323(13):1239-42. Available from: https://jamanetwork.com/ https://doi.org/10.1001/jama.2020.2648
» https://jamanetwork.com/» https://doi.org/10.1001/jama.2020.2648 -
25Hartman HE, Sun Y, Devasia TP, Chase EC, Jairath NK, Dess RT, et al. Integrated survival estimates for cancer treatment delay among adults with cancer during the COVID-19 pandemic. JAMA Oncol. 2020 Dec;6(12):1881-9. https://doi.org/10.1001/jamaoncol.2020.5403
» https://doi.org/10.1001/jamaoncol.2020.5403 -
26European Society for Medical Oncology. Head and neck cancers in the COVID-19 era. Lugano: SMO; 2021 [cited 2022 Mar 7]. Available from: https://www.esmo.org/guidelines/cancer-patient-management-during-the-covid-19-pandemic/head-and-neck-cancers-in-the-covid-19-era
» https://www.esmo.org/guidelines/cancer-patient-management-during-the-covid-19-pandemic/head-and-neck-cancers-in-the-covid-19-era -
27Gomes AP, Schuch LF, Tarquinio SB, Etges A, Vasconcelos AC. Reduced demand for oral diagnosis during COVID-19: a Brazilian center experience. Oral Dis. 2022 Apr;28(Suppl 1):5958-9. Epub. fev 2020;1-2: https://doi.org/10.1111/odi.13547
» https://doi.org/10.1111/odi.13547 -
28Abrantes TC, Bezerra KT, Silva CN, Costa LC, Cabral MG, Agostini M, et al. Oral cancer diagnosis during the COVID-19 pandemic in an oral pathology laboratory in Rio de Janeiro, Brazil. Oral Dis. 2022 Apr;28(Suppl 1):997-8. E-pub:1-2, 2020. https://doi.org/10.1111/odi.13669
» https://doi.org/10.1111/odi.13669 -
29Sud A, Torr B, Jones ME, Broggio J, Scott S, Loveday C, et al. Effect of delays in the 2-week-wait cancer referral pathway during the COVID-19 pandemic on cancer survival in the UK: a modelling study. Lancet Oncol. 2020 Aug;21(8):1035-44. https://doi.org/10.1016/S1470-2045(20)30392-2
» https://doi.org/10.1016/S1470-2045(20)30392-2 -
30Stopa SR, Malta DC, Monteiro CN, Szwarcwald CL, Goldbaum M, Cesar CL. Acesso e uso de serviços de saúde pela população brasileira, Pesquisa Nacional de Saúde 2013. Rev Saúde Publica. 2017;51(1):1s-11s. https://doi.org/10.1590/S1518-8787.2017051000074
» https://doi.org/10.1590/S1518-8787.2017051000074 -
31Szwarcwald CL, Stopa SR, Damacena GN, Almeida WD, Souza Júnior PR, Vieira ML, et al. Mudanças no padrão de utilização de serviços de saúde no Brasil entre 2013 e 2019. Cien Saúde Colet. 2021 Jun;26 suppl 1:2515-28. https://doi.org/10.1590/1413-81232021266.1.43482020
» https://doi.org/10.1590/1413-81232021266.1.43482020 -
32Conway DI, Petticrew M, Marlborough H, Berthiller J, Hashibe M, Macpherson LM. Socioeconomic inequalities and oral cancer risk: a systematic review and meta-analysis of case-control studies. Int J Cancer. 2008 Jun;122(12):2811-9. https://doi.org/10.1002/ijc.23430
» https://doi.org/10.1002/ijc.23430
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Funding: Fundação de Apoio à Pesquisa do Estado de São Paulo (Fapesp – process 2021/07433-6). Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (Capes - Funding code 001).
Publication Dates
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Publication in this collection
26 May 2023 -
Date of issue
2023
History
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Received
17 Mar 2022 -
Accepted
03 Aug 2022