Abstract

This ecological study examined time series, from 2002 to 20121, of age-adjusted coefficients of cervical cancer mortality, in Brazil, in women aged 20 years or more, by race. The information sources were Brazil’s mortality information system (Sistema de Informação sobre Mortalidade - SIM) and the official bureau of statistics (Instituto Brasileiro de Geografia e Estatística - IBGE). Annual changes in age-adjusted mortality rates were calculated using the Prais-Winsten linear regression method. Black women die more and the rate is decreasing less. Racial inequality has increased over the years. In 2002, there were 0.08 more deaths per 100,000 women in the black population than among white women; in 2021, the number was one death. Health policymaking should consider racial differences in the implementation of strategies and goals.

Key words:
Cervical neoplasms; Ethnic origin and health; Racial factors; Mortality; Time series studies

Introduction

Cervical cancer ranks third in causes of female mortality worldwide. It occurs more frequently in disadvantaged populations as part of a complex of diseases connected with poverty, race and unfavorable living conditions¹1 Arbyn M, Castellsagué X, Sanjosé S, Bruni LM, Saraiya M, Bray F, Ferlay J. Worldwide burden of cervical cancer. Annals Oncol 2011; 22(12):2675-2686..

Incidence is reduced by early diagnosis of precursor lesions and vaccination against human papillomavirus (HPV)²2 Pimple S, Mishra G, Shastri S. Global strategies for cervical cancer prevention Current Opinion in Obstetr Gynecol 2016; 28(1):4-10.. Cervical cancer is a disease that can be screened for; the high number of related deaths - and its continuing to be a public health problem - is associated with its being diagnosed late, at an advanced stage.

Nearly all cases of cervical cancer are caused by chronic infection with high-risk, oncogenic subtypes of HPV. Accordingly, risk factors are those associated with an increased likelihood of HPV infection, including early sexual initiation, multiple sexual partners or a partner with multiple sexual partners, immunosuppression, a history of sexually transmitted infection, a history of HPV-related vulvar or vaginal dysplasia and lack of access to screening³3 Cohen PA, Jhingran A, Oaknin A, Denny L. Cervical cancer: unequal progress. Lancet 2019; 393(10167):169-182..

Although race is another prominent risk factor in the international scientific literature⁴4 Collins Y, Holcomb K, Chapman-Davis E, Khabele D, Farley JH. Gynecologic cancer disparities: A report from the Health Disparities Taskforce of the Society of Gynecologic Oncology. Gynecol Oncol 2014; 133(2):353-361., most studies in Brazil have limited themselves to examining aspects relating to poverty and fail to give proper emphasis to racial inequalities in health⁵5 Werneck J. Racismo institucional e saúde da população negra. Saude Soc 2016; 25(3):535-549.^,66 Araújo EM, Costa MCN, Noronha CV, Hogan VK, Vines AI, Araújo TM. Desigualdades em saúde e raça/cor da pele: revisão da literatura do Brasil e dos Estados Unidos (1996-2005). Saude Colet 2010; 7(40):116-121..

Introducing race data into national information systems enables indicators to be constructed to reveal racial inequalities, thus making it possible to assess health service performance in social inclusion⁷7 Braz RM, Oliveira PTR, Reis AT, Machado NMS. Avaliação da completude da variável raça/cor nos sistemas nacionais de informação em saúde para aferição da equidade étnico-racial em indicadores usados pelo Índice de Desempenho do Sistema Único de Saúde. Saude Debate 2013; 37(99):554-562.. However, data for constructing indicators by race are not always available in sufficient quality and quantity. Despite the limitations, calculating and disseminating indicators contributes to the debate and improving information systems to identify racial differences.

In that regard, this study examined time series of mortality from cervical cancer in Brazil from 2002 to 2021 by race.

Methods

This ecological time series study drew on data from Brazil’s mortality information system (Sistema de Informações sobre Mortalidade, SIM) and population information from the official bureau of statistics (Instituto Brasileiro de Geografia e Estatística, IBGE). These data were used to calculate cervical cancer mortality rates in Brazil, from 2002 to 2021, by race (Figure 1).

The study considered all deaths of women aged 20 or over, residing in Brazilian territory, the underlying cause of whose death was cervical cancer.

To counter classification bias (deaths from cervical cancer classified as “part unspecified”), the causes considered were those specified in the 10^th revision of the International Statistical Classification of Diseases and Related Health Problems (ICD10) as Malignant neoplasm of cervix uteri (C53), Malignant neoplasm of corpus uteri (C54) and Malignant neoplasm of uterus, part unspecified (C55). Also, deaths classified as C55 (Malignant neoplasm of uterus, part unspecified) were redistributed proportionally by year and age group. This was a four-step procedure: first, deaths classified as Malignant neoplasm of cervix uteri and of corpus uteri were added together; second, deaths from Malignant neoplasm of cervix uteri and of corpus uteri were each calculated as proportions of the total number of Malignant neoplasm of cervix uteri and of corpus uteri); third, deaths from Malignant neoplasm of the uterus, part unspecified, were redistributed as Malignant neoplasm of cervix uteri and of corpus uteri in the proportions calculated in the second step; and fourth, the value obtained in step three was added to the original deaths from Malignant neoplasm of cervix uteri and of corpus uteri, to give the corrected number of deaths⁸8 Silva GA, Girianelli VR, Gamarra CJ, Teixeira MTB. Cervical cancer mortality trends in Brazil, Evolução da mortalidade por câncer do colo do útero no Brasil, 1981-2006. Cad Saude Publica 2010; 26(12):2399-2407.^,99 Sousa AMV, Teixeira CCA, Medeiros SS, Nunes SJC, Salvador PTCO, Barros RMB, Lima FFS, Nascimento GGC, Santos J, Souza DLB, Bezerra APS, Meira KC. Mortalidade por câncer do colo do útero no estado do Rio Grande do Norte, no período de 1996 a 2010: tendência temporal e projeções até 2030. Epidemiol Serv Saude 2016; 25(2):311-322..

The mortality rate by race was calculated by dividing the number of deaths from cervical cancer in women aged 20 or over by the number of women aged 20 or over per 100,000 women. Rates were adjusted for age distribution using the standard global population¹⁰10 Doll R, Muir C, Waterhouse J. Cancer Incidence in Five Continents. Berlin, New York: Springer-Verlag, Heidelberg; 1970..

For standardization purposes, age groups by race were obtained by linear projection from 2000 and 2010 census data, given that the IBGE does not provide intercensal estimates from which to stratify the population simultaneously by race and age group.

Race for both population and mortality was obtained by self-reporting and classified, by the IBGE definitions, as white, brown, black, yellow, and indigenous⁷7 Braz RM, Oliveira PTR, Reis AT, Machado NMS. Avaliação da completude da variável raça/cor nos sistemas nacionais de informação em saúde para aferição da equidade étnico-racial em indicadores usados pelo Índice de Desempenho do Sistema Único de Saúde. Saude Debate 2013; 37(99):554-562.^,1111 Petruccelli JL, Saboia AL. Características étnico-raciais da população: classificação e identidades. Rio de Janeiro: IBGE, Ministério do Planejamento, Orçamento e Gestão; 2013.. Brown women were added to black women in both numerator (deaths) and denominator (population) to give the mortality coefficient for black women. The category “black” (the sum of black and brown women) represents, on the one hand, the population descended from Africans born in the diaspora and, on the other, the process of miscegenation as a dimension of Brazil¹¹11 Petruccelli JL, Saboia AL. Características étnico-raciais da população: classificação e identidades. Rio de Janeiro: IBGE, Ministério do Planejamento, Orçamento e Gestão; 2013..

The data from 2002 to 2021 were analyzed by estimating annual percentage changes (APCs) in cervical cancer mortality rates, by race, with their respective 95% confidence intervals, using a linear regression model with Prais-Winsten correction. Rates were considered rising when the APC was positive and falling when negative. In the study model, rate trends were considered non-significant when p>0.05.

This study was approved by the research ethics committee of the School of Medicine of the Universidade de São Paulo on 05 September 2018 (Research Protocol No. 162/18).

Results

From 2002 to 2021, 133,429 deaths from cervical cancer were recorded in Brazil. Of these, 63,102 (47.3%) occurred in white women, 10,741 (8.1%) in black women, 57,584 (43.2%) in brown women, 635 (0.48%) in yellow women, 632 (0.47%) in indigenous women. The black population (brown women plus black women) accounted for 68,325 (51.2%) of these deaths. Mortality among black and white women represented 98.50% of total records in the study period.

In 2002, the mortality rate in black women was 1.0% higher than in white women; in 2021, the difference was 17.8%, i.e., racial inequality had increased. In the population of indigenous women, fluctuating rates have resulted from the small numbers involved and this group’s minor participation in the general population. In 2002, mortality among indigenous people was 47.3% lower than among white people. In 2021, mortality among indigenous women was 123.5% higher than among white women (Table 1).

Table 2 shows descriptive statistics for the study object variable in Brazil, from 2002 to 2021, by race. Indigenous race returned the highest average rate (10.99), and white returned the lowest (6.5). The time series with the largest relative variation from the average was for the yellow race (53.90%) and the smallest for the black race (6.13%). Asymmetry coefficients were positive for all time series (except for black race), indicating below-average data concentration for the period (Table 2 and Figure 2).

Table 3 shows the trend in mortality from cervical cancer. For the female population in Brazil, the annual percentage varied negatively by 1.33% (95%CI -1.56 to -1.10), indicating a downward trend. The percentage variations in the white and yellow populations showed even stronger downturns of -1.74% (95%CI -2.24 to -1.23) and -7.17% (95%CI -9.31 to -4.97), respectively.

While mortality decreased significantly among white and yellow women during the study period, the annual percentage variation for black women was more minor (APC of 0.98% CI95% -1.93 to -0.02), indicating values close to stability although decreasing. The trend was upward among indigenous women, with a positive annual percentage variation of 4.74% (95%CI 2.39 to 7.16).

The trends found were thus heterogeneous: mortality rates decreased most in the white and yellow populations, and racial inequality increased concomitantly.

Discussion

As far as is known, this study is the first to examine relationships between race and age-standardized, corrected cervical cancer mortality on a Brazil-country basis.

Cervical cancer mortality trends from 2002 to 2021 were found to differ by race in Brazil and to display different temporal patterns. Racial inequality increased in the study period.

Relationship between race and health has been investigated in the United States since the 1980s. In Brazil, although 56.1% of the population is black, the field of black health has been established only since the 2000s, when the 3^rd World Conference Against Racism, Xenophobia, and Related Intolerance was held. A special secretariat for the promotion of racial equality policies (Secretaria Especial de Promoção de Políticas de Igualdade Racial, SEPPIR) was subsequently set up under the Presidency of the Republic¹²12 Berquó E. Demografia da desigualdade - Algumas considerações sobre os negros no Brasil. In: VI Encontro Nacional de Estudos Populacionais. São Paulo; 1988. p. 89-110..

The category “black” reflects an ethnic and racial identity and is present in denominations that combat racism. It makes it possible to understand the effects of the history, culture, and economic and political contexts that have deeply imprinted the meanings of Brazilian social realities and the effects of racial discrimination.

Some studies trace the panorama of mortality from cervical cancer in specific states or municipalities and highlight social inequality. In 2013, nine out of ten deaths from cervical cancer occurred in less-developed local regions, where the risk of death before age 75 was three times higher¹³13 Meira KC, Silva GA, Silva CMFP, Valente JG. Efeito idade-período-coorte na mortalidade por câncer do colo uterino. Rev Saude Publica 2013; 47(2):274-282.. In the city of Recife between 2000 and 2004, most deaths were among black women from 40 to 59 years old (that is, under 60 years old) without a steady partner, who were housewives, residing in neighborhoods without basic infrastructure and public hospital users¹⁴14 Mendonça VG, Lorenzato FRB, Mendonça JG, Menezes TCN, Guimarães MJB. Mortalidade por câncer do colo do útero: Características sociodemográficas das mulheres residentes na cidade de Recife, Pernambuco. Rev Bras Ginecol Obstet 2008; 30(5):248-255.. In Rio de Janeiro and São Paulo, mortality from cervical cancer decreased significantly, especially in women born after 1960¹³13 Meira KC, Silva GA, Silva CMFP, Valente JG. Efeito idade-período-coorte na mortalidade por câncer do colo uterino. Rev Saude Publica 2013; 47(2):274-282.. Rio Grande do Norte mortality coefficient did not vary considerably between 1996 and 2010. Nonetheless, coefficients increased in areas where socioeconomic conditions were worse¹⁰10 Doll R, Muir C, Waterhouse J. Cancer Incidence in Five Continents. Berlin, New York: Springer-Verlag, Heidelberg; 1970.. An increasing trend was also observed from 2000 to 2011 in Piauí¹⁵15 Madeiro A, Rufino AC, Brandão NS, Santos IS. Tendências da mortalidade por câncer do colo do útero no Piauí, 2000-2011. Cad Saude Colet 2016; 24(3):282-285..

While there is little research in Brazil to examine associations between race and cervical cancer, in the USA, there have been many studies whose results are to those in Brazil. However, only one such study has analyzed time series. Between 2000 and 2012, mortality rates for black women aged 65 in the USA were found to follow an increasing trend against a stable trend for white women¹⁶16 Yoo W, Kim S, Huh WK, Dilley S, Coughlin SS, Partridge EE, Chung Y, Dicks V, Lee JK, Bae S. Recent trends in racial and regional disparities in cervical cancer incidence and mortality in United States. PLoS One 2017; 12(2):e0172548.. As compared with white women, non-Hispanic black women faced an increased risk of cervical cancer mortality, while Hispanic women showed decreased risk¹⁷17 Markt SC, Tang T, Cronin AM, Katz IT, Howitt BE, Horowitz NS, Lee LJ, Wright AA. Insurance status and cancer treatment mediate the association between race/ethnicity and cervical cancer survival. PLoS One 2018; 13(2):e0193047.

18 Rauh-Hain JA, Melamed A, Schaps D, Bregar AJ, Spencer R, Schorge JO, Rice LW, Del Carmen MG. Racial and ethnic disparities over time in the treatment and mortality of women with gynecological malignancies. Gynecol Oncol 2018; 149(1):4-11.^-1919 Benjamin Zhan YL. Racial/Ethnic, Socioeconomic, and Geographic Disparities of Cervical Cancer Advanced-Stage Diagnosis in Texas. Womens Health Issues 2014; 24(5):519-527..

The differences in cervical cancer mortality, by race, found here, can be explained by the unequal distribution of social resources. Although this situation results from levels of poverty, it is catalysed by racial inequalities. The central interventions to control cervical cancer are oncotic cytology, timely diagnosis, and treatment; accordingly, the different mortality rates can be explained by difficulties in accessing services. Younger black women in Rio de Janeiro had less access, received less information, and rated worse the care they received²⁰20 Martins LFL, Almeida LMD, Szklo AS, Szklo M, Thuler LCS, Enes MDFG, Pinheiro RS, Coeli CM. Factors associated with the lack of access to cervical cancer screening test results in the Brazilian unified health system network in the municipality of Rio de Janeiro. Eur J Cancer Prev 2018; 27(4):339-346.. A similar situation was found in two cities in Rio Grande do Sul (Pelotas and São Leopoldo), where racial inequalities in access persisted even after controlling for age and socioeconomic factors²¹21 Bairros FS, Meneghel SN, Dias-da-Costa J, Bassani DG, Menezes AMB, Gigante DP, Olinto MTA. Desigualdades raciais no acesso à saúde da mulher no Sul do Brasil. Cad Saude Publica 2011; 27(12):2364-2372.. In Brazil, black women had significantly fewer Pap smears and breast exams and more late diagnoses with worse prognoses²²22 Martínez-Mesa J, Werutsky G, Campani RB, Wehrmeister FC, Barrios CH. Inequalities in Pap smear screening for cervical cancer in Brazil. Prev Med (Baltim) 2013; 57(4):366-371.

23 Renna Junior NL, Silva GA. Tendências temporais e fatores associados ao diagnóstico em estágio avançado de câncer do colo uterino: análise dos dados dos registros hospitalares de câncer no Brasil, 2000-2012. Epidemiol Serv Saude 2018; 27(2):e2017285.

24 Thuler LCS, Aguiar SS, Bergmann A. Determinantes do diagnóstico em estadio avançado do câncer do colo do útero no Brasil. Rev Bras Ginecol Obstet 2014; 36(6):237-243.^-2525 Amorim V, Barros M, Cesar C, Carandina L, Goldbaum M. Fatores associados a não realização do exame de Papanicolaou: um estudo de base populacional no Município de Campinas, São Paulo, Brasil. Cad Saude Publica 2006; 22(11):2329-2338.. A similar situation in access to medical procedures has been found in the USA. Even when clinically indicated, black women received less surgery for early-stage disease, less chemotherapy, and less radiotherapy¹⁸18 Rauh-Hain JA, Melamed A, Schaps D, Bregar AJ, Spencer R, Schorge JO, Rice LW, Del Carmen MG. Racial and ethnic disparities over time in the treatment and mortality of women with gynecological malignancies. Gynecol Oncol 2018; 149(1):4-11.^,2626 Benard VB, Watson M, Saraiya M, Harewood R, Townsend JS, Stroup AM, Weir HK, Allemani C. Cervical cancer survival in the United States by race and stage (2001-2009): Findings from the CONCORD-2 study. Cancer 2017; 123 (Supl. 24):5119-5137..

Macrostructural and political factors hinder the black population’s access to services. Vulnerability influences decision-making and assertion of rights. Relationships between individuals and how they position themselves in the world are dictated by social, cultural, and historical conditions, which shape the health and disease process and many other conditions. These determinants maintain and reproduce social forms in diverse domains, preventing people from demanding health services²⁷27 Theodoro ML. A formação do mercado de trabalho e a questão racial no Brasil. In: Theodoro ML, organizador. As políticas públicas e a desigualdade racial no Brasil: 120 anos após a abolição. Brasília: Ipea; 2008. p. 15-44.

28 Munanga K. História do Negro no Brasil: o negro na sociedade brasileira: resistência, participação e contribuição. Brasília: Fundação Cultural Palmares; 2004.^-2929 Theophilo RL, Rattner D, Pereira ÉL. The vulnerability of afro-brazilian women in perinatal care in the unified health system: Analysis of the active ombudsman survey. Cien Saude Colet 2018; 23(11):3505-3516.. Although slavery was abolished in Brazil more than a century ago, its relics and updated forms exist and are expressed in a socially disadvantaged black population. Most economic and health indicators reveal unfair differences by race³⁰30 Lopes F. Experiências desiguais ao nascer, viver, adoecer e morrer: tópicos em saúde da população negra no Brasil. In: Seminário saúde da população negra Estado de São Paulo 2004. São Paulo; 2005. p. 53-101.. The positions occupied by groups and individuals in social space, the way they relate to each other, and nature in the process of producing wealth are at the origin of diseases and their unequal distribution in the population.

The findings of this study should be interpreted in view of the limitations of using secondary data. Although the quality of the Mortality Information System (SIM) has improved, approximately 30% of deaths in the study period were found to have been classified as unspecified uterine cancer. The proportional redistribution described in the Methods section was designed to circumvent this limitation.

Surprisingly, completion of the race field in SIM records proved good quality. Race could be determined in 95.0% of deaths from cervical cancer (ICD C53 and deaths redistributed from ICD C55). This improved over time, with better quality data in recent years: notification rates were 90.7% in 2002 and 97.8% in 2021.

Another factor to be considered when interpreting the results is that, between the 2000 and 2010 Censuses, the percentage of self-declared black and brown respondents increased, while those self-declared white decreased¹¹11 Petruccelli JL, Saboia AL. Características étnico-raciais da população: classificação e identidades. Rio de Janeiro: IBGE, Ministério do Planejamento, Orçamento e Gestão; 2013.. The effect of this phenomenon on the mortality coefficient for the black population was to increase the denominator and thus reduce the coefficient. For the white population, the opposite occurred: the denominator decreased, increasing the coefficient. It is thus possible that the coefficients given here for black women are underestimated and those for white women, overestimated. Accordingly, racial inequality may be even more pronounced than in our results.

Importantly, the classification of race in the census and SIM data may not be uniform. Although both records self-declared race, the census offers greater accuracy because it is conducted by personnel specifically trained to obtain population information.

This study’s importance resides in its originality. It is the first study to examine relationships between race and age-standardised, corrected cervical cancer mortality on a Brazil-country basis. Furthermore, it underlines the challenge of overcoming inequalities in health service access to create a truly universal and equitable health system. Services need to organize care in such a manner as to grasp and address racial disparities. Interventions in the social determinants of health and related conditioning factors should reflect the endevour to achieve racial equality.

Lastly, the study findings point to the need for a policy and management decision-making structure that give priority to reducing the effects of institutional racism. As regards the policy to combat cervical cancer, black women should receive special attention when strategies are developed for Brazil’s national cervical and breast cancer control programme (Programa Nacional de Controle do Câncer do Colo do Útero e de Mama). Primary health care goals and activities, HPV vaccination coverage, screening, the referral and counter-referral system, and implementation of a service network for timely treatment should consider the specifics and needs of the black population.

References

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