Abstracts

Introduction

Social inequalities in the epidemiological profile of neoplasms differ depending on the primary location of the cancer and the analyzed indicator, whether incidence, mortality, or survival ¹1. Torre LA, Islami F, Siegel RL, Ward EM, Jemal A. Global cancer in women: burden and trends. Cancer Epidemiol Biomarkers Prev 2017; 26:444-57.^,22. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394-424.. Studies indicate a higher incidence of breast and thyroid cancers in women from higher socioeconomic strata ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.^,44. Liu Z, Zhang K, Du XL. Risks of developing breast and colorectal cancer in association with incomes and geographic locations in Texas: a retrospective cohort study. BMC Cancer 2016; 16:294.^,55. Altekruse S, Das A, Cho H, Petkov V, Yu M. Do US thyroid cancer incidence rates increase with socioeconomic status among people with health insurance? An observational study using SEER population-based data. BMJ Open 2015; 5:e009843.^,66. Swegal WC, Singer M, Peterson E, Feigelson HS, Kono SA, Snyder S, et al. Socioeconomic factors affect outcomes in well-differentiated thyroid cancer. Otolaryngol Head Neck Surg 2016; 154:440-5., whereas women from lower strata are at higher risk of cervical and stomach cancers ⁷7. Singh GK, Miller BA, Hankey BF, Edwards BK. Persistent area socioeconomic disparities in U.S. incidence of cervical cancer, mortality, stage, and survival, 1975-2000. Cancer 2004; 101:1051-7.^,88. Mihor A, Tomsic S, Zagar T, Lokar K, Zadnik V. Socioeconomic inequalities in cancer incidence in Europe: a comprehensive review of population-based epidemiological studies. Radiol Oncol 2020; 54:1-13..

In some European countries, colorectal cancer was prevalent in higher socioeconomic levels until the 1980s ⁹9. Kogevinas EM, Pearce N, Susser M, Boffetta P, editors. Social inequalities and cancer. Lyon: International Agency for Research on Cancer; 1997. (IARC Scientific Publications, 138)., but became even ¹⁰10. Savijärvi S, Seppä K, Malila N, Pitkäniemi J, Heikkinen S. Trends of colorectal cancer incidence by education and socioeconomic status in Finland. Acta Oncol (Madr) 2019; 58:1557-63. or higher in the highest social vulnerability strata after the 2000s ¹¹11. Lynge E, Martinsen JI, Larsen IK, Kjarheim K. Colon cancer trends in Norway and Denmark by socio-economic group: a cohort study. Scand J Public Health 2015; 43:890-8.. In the United States and Canada, in the 2000s, those of lower socioeconomic levels also had a higher incidence of cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12..

Lung cancer incidence and mortality tend to follow the previous social distribution of smoking prevalence ²2. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394-424.. Low- and middle-income countries currently have higher rates of lung cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.^,99. Kogevinas EM, Pearce N, Susser M, Boffetta P, editors. Social inequalities and cancer. Lyon: International Agency for Research on Cancer; 1997. (IARC Scientific Publications, 138). than those with high-income ⁹9. Kogevinas EM, Pearce N, Susser M, Boffetta P, editors. Social inequalities and cancer. Lyon: International Agency for Research on Cancer; 1997. (IARC Scientific Publications, 138).^,1212. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15..

Women of poorer socioeconomic conditions have higher incidence and mortality rates of cervical and stomach cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.^,1212. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15.^,1313. Vale DB, Sauvaget C, Murillo R, Muwonge R, Zeferino LC, Sankaranarayanan R. Correlação da mortalidade por câncer do colo do útero com fertilidade, acesso a cuidados de saúde e indicadores socioeconômicos. Rev Bras Ginecol Obstet 2019; 41:249-55.. However, countries show a different inequality pattern in death rates from breast cancer: some have higher rates in the highest socioeconomic levels ¹⁴14. Di Sibio A, Abriata G, Forman D, Sierra MS. Female breast cancer in Central and South America. Cancer Epidemiol 2016; 44 Suppl 1:S110-20.^,1515. Girianelli VR, Gamarra CJ, Azevedo e Silva G. Disparities in cervical and breast cancer mortality in Brazil. Rev Saúde Pública 2014; 48:459-67., and others have no differences between social strata ¹⁶16. Lundqvist A, Andersson E, Ahlberg I, Nilbert M, Gerdtham U. Socioeconomic inequalities in breast cancer incidence and mortality in Europe: a systematic review and meta-analysis. Eur J Public Health 2016; 26:804-13.^,1717. Menvielle G, Rey G, Jougla E, Luce D. Diverging trends in educational inequalities in cancer mortality between men and women in the 2000s in France. BMC Public Health 2013; 13:823..

Recently, incidence and mortality rates of colorectal cancer which were prevalent in higher social strata became even ¹⁸18. Santos-Sánchez V, Córdoba-Doña JA, Viciana F, Escolar-Pujolar A, Pozzi L, Ramis R. Geographical variations in cancer mortality and social inequalities in southern Spain (Andalusia). 2002-2013. PLoS One 2020; 15:e0233397. or higher in lower social strata ¹⁹19. Enewold L, Horner MJ, Shriver CD, Zhu K. Socioeconomic disparities in colorectal cancer mortality in the United States, 1990-2007. J Community Health 2014; 39:760-6.^,2020. Elstad JI, Torstensrud R, Lyngstad TH, Kravdal O. Trends in educational inequalities in mortality, seven types of cancers, Norway 1971-2002. Eur J Public Health 2012; 22:771-6..

Regarding survival, research on different types of cancer indicates that people in the lower-income social strata have a shorter survival time for most cancers ⁷7. Singh GK, Miller BA, Hankey BF, Edwards BK. Persistent area socioeconomic disparities in U.S. incidence of cervical cancer, mortality, stage, and survival, 1975-2000. Cancer 2004; 101:1051-7.^,2121. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018; 391:1023-75.^,2222. Arias-Ortiz NE, de Vries E. Health inequities and cancer survival in Manizales, Colombia: a population-based study. Colomb Med 2018; 49:63-72.^,2323. Gorey KM, Luginaah IN, Holowaty EJ, Fung KY, Hamm C. Breast cancer survival in Ontario and California, 1998-2006: socioeconomic inequity remains much greater in the United States. Ann Epidemiol 2009; 19:121-4.^,2424. Singh GK, Jemal A. Socioeconomic and racial/ethnic disparities in cancer mortality, incidence, and survival in the United States, 1950-2014: over six decades of changing patterns and widening inequalities. J Environ Public Health 2017; 2017:2819372..

The International Agency for Research on Cancer (IARC) of the World Health Organization (WHO) recognizes that producing evidence on the extent of social inequalities in cancer is essential to provide information on measures for reducing social inequities in access to health care and the diagnosis and treatment of the disease ²⁵25. Vaccarella S, Lortet-Tieulent J, Saracci R, Fidler MM, Conway DI, Vilahur N, et al. Reducing social inequalities in cancer: setting priorities for research. CA Cancer J Clin 2018; 68:324-6..

In Brazil, studies on social inequalities in cancer incidence and mortality are scarce ¹³13. Vale DB, Sauvaget C, Murillo R, Muwonge R, Zeferino LC, Sankaranarayanan R. Correlação da mortalidade por câncer do colo do útero com fertilidade, acesso a cuidados de saúde e indicadores socioeconômicos. Rev Bras Ginecol Obstet 2019; 41:249-55.^,1515. Girianelli VR, Gamarra CJ, Azevedo e Silva G. Disparities in cervical and breast cancer mortality in Brazil. Rev Saúde Pública 2014; 48:459-67.^,2626. Antunes JL, Borrell C, Pérez G, Boing AF, Wünsch-Filho V. Inequalities in mortality of men by oral and pharyngeal cancer in Barcelona, Spain and São Paulo, Brazil, 1995-2003. Int J Equity Health 2008; 7:14.^,2727. Boing AF, Antunes JLF. Condições socioeconômicas e câncer de cabeça e pescoço: uma revisão sistemática de literatura. Ciênc Saúde Colet 2011; 16:615-22.. Research is essential to expand knowledge of the pattern of social disparities in cancer in Brazil, which differ according to the location of neoplasms and changes in magnitude and direction over time. Our objective was to analyze the inequalities in incidence, mortality, and survival of the main types of cancer in women dwelling in Campinas, São Paulo State, from 2010 to 2014, according to the Social Vulnerability Index (SVI).

Methods

This is an ecological study on incidence, mortality, and survival of the most frequent neoplasms among women residing in the city of Campinas from 2010 to 2014, according to the area of residence stratified by the level of social vulnerability.

Campinas is a large city located 99km Northwest of São Paulo, capital of the state of São Paulo, with an estimated 1,213,792 inhabitants in 2020 and the 14th most populous city in the country, with an urbanization rate of 98.3%. In 2010, its Human Development Index (HDI) was 0.805, which is considered very high ²⁸28. Instituto Brasileiro de Geografia e Estatística. Cidades e estados. https://www.ibge.gov.br/cidades-e-estados/sp/campinas.html (accessed on 15/Dec/2020).
https://www.ibge.gov.br/cidades-e-estado... .

Information on cancer cases and deaths were obtained from the Population-Based Cancer Registry (RCBP) and from the Mortality Information System (SIM) of the Municipal Health Department of Campinas, codified by the International Classification of Diseases, 10th Revision (ICD-10). The studied types of cancer were: breast cancer (C50), colorectal cancer (C18_20), lung and bronchial cancer (C33_34), stomach cancer (C16), and cervical cancer (C53), which are the most prevalent among women in Brazil, and thyroid cancer (C73), which is the third most common type of cancer in Campinas.

Data on mortality from cervical cancer were corrected by proportional reallocation of deaths from cancer of the “uterus, part unspecified - NOS [not otherwise specified]” (coded as C55) for the categories of the cervix (C53) and the body of the uterus (C54) ²⁹29. Loos AH, Bray F, McCarron P, Weiderpass E, Hakama M, Parkin DM. Sheep and goats: separating cervix and corpus uteri from imprecisely coded uterine cancer deaths, for studies of geographical and temporal variations in mortality. Eur J Cancer 2004; 40:2794-803., considering the age group and area of residence of the cases.

The São Paulo Social Vulnerability Index 2010 (IPVS-2010), developed by the SEADE Foundation ³⁰30. Fundação Sistema Estadual de Análise de Dados. IPVS versão 2010: Índice Paulista de Vulnerabilidade Social. http://indices-ilp.al.sp.gov.br/view/pdf/ipvs/metodologia.pdf (accessed on 15/Aug/2020).
http://indices-ilp.al.sp.gov.br/view/pdf... , was used to stratify areas of residence according to social vulnerability. IPVS combines demographic and socioeconomic variables. The demographic variables are: % of households headed by individuals aged 10 to 29 years, % of households headed by women aged 10 to 29 years, mean age of the head of household, and % of households with children aged 0 to 5 years. The socioeconomic variables are: disposable household and per capita income, mean income of women heads of household, % of households with per capita income up to ½ a minimum wage, % of households with per capita income up to ¼ a minimum wage, and % of literate people who are the head of the household. The IPVS is calculated for each census tract and categorized into seven groups, from IPVS 1 to IPVS 7, in which 1 is very low social vulnerability and 6-7 is very high social vulnerability, 6 for urban areas and 7 for rural areas.

The social vulnerability strata in Campinas were based on the areas covered by the primary healthcare units (UBS), with available information on deaths and cancer cases in the municipality. To each UBS area was assigned a vulnerability score considering the proportion of census sectors classified at each level of the IPVS. The areas were ordered from the lowest to the highest score and grouped into three social vulnerability stratum (SVS), with SVS1 and SVS3 being the lowest and highest social vulnerability stratum, respectively. Each SVS corresponds to approximately one third of the population of the municipality. Figure 1 shows areas covered by the UBS, grouped according to social vulnerability strata.

The SVS population data from 2010 to 2014 were obtained from the population estimates of the areas covered by UBS, conducted by the Municipal Health Department of Campinas using data from the 2010 demographic census of the Brazilian Institute of Geography and Statistics (IBGE) ³¹31. Secretaria Municipal de Saúde de Campinas. População por faixa etária e sexo das áreas de abrangências dos CS e Distritos de Saúde, 2000 a 2018. http://tabnet.campinas.sp.gov.br/dh?populacao/pop3.def (accessed on 15/Aug/2020).
http://tabnet.campinas.sp.gov.br/dh?popu... .

The mean values of incidence and mortality rates per 100,000 women by type of cancer were calculated for each SVS from 2010 to 2014. Incidence and mortality rates were standardized by age using the direct method, considering as standard the world population of 1960, modified by Doll et al. in 1966 ³²32. Doll R, Payne P, Waterhouse J, editors. Cancer incidence in five continents: a technical report. New York: Springer-Verlag; 1966..

The incidence rate ratios (RR) and their respective 95% confidence intervals (95%CI) were estimated using Equation 1:

Where:

Where: CI is the confidence interval, SR is the standardized rate, and SE is the standard error of the standardized rate ³³33. Agência Internacional para Pesquisa sobre o Câncer; Assossiaçao Internacional de Registros de Câncer. Registro de câncer: princípios e métodos. Rio de Janeiro: Agência Internacional para Pesquisa sobre o Câncer; 1995. (Publicações Científicas da IARC, 95)..

To assess inequalities in cancer incidence and mortality in SVS, the concentration index was calculated using the covariance method, based on the standardized rates of incidence and mortality for each type of cancer analyzed and according to Equation 3, to compute the covariance between the health variable y and the fractional rank R:

Where: µ is the mean of y and R is the fractional rank of the i ^th person in the income distribution.

The concentration index is a synthetic measurement of socioeconomic inequalities which could be applied to analysis in several dimensions, inspired by the Gini index and the Lorenz curve, and adapted to a measurement of inequalities in health by O’Donnell et al. ³⁴34. O'Donnell O, van Doorslaer E, Wagstaff A, Lindelow M. Analyzing health equity using household survey data: a guide to techniques and their implementation. Washington DC: World Bank; 2008. and Schneider et al. ³⁵35. Schneider MC, Castillo-Salgado C, Bacallao J, Loyola E, Mujica OJ, Vidaurre M, et al. Métodos de mensuração das desigualdades em saúde. Rev Panam Salud Pública 2002; 12:398-414.. In this study, the concentration index offers a synthetic measurement of inequalities in cancer incidence and mortality, according to the social vulnerability strata of the area of residence of patients.

The concentration index ranges from -1 to +1, in which negative values indicate a greater cumulative risk of cancer incidence or mortality in groups of highest vulnerability and positive values indicate higher risk in groups of lowest social vulnerability. Values close to zero represent a low level of socioeconomic inequality, and values close to +1 or -1 indicate a higher level of inequality ³⁵35. Schneider MC, Castillo-Salgado C, Bacallao J, Loyola E, Mujica OJ, Vidaurre M, et al. Métodos de mensuração das desigualdades em saúde. Rev Panam Salud Pública 2002; 12:398-414.. A significance level of 5% was considered in the analyses performed.

The survival estimate of each type of cancer for each SVS was calculated by the complement of the mortality incidence RR, which has been used and validated as a 5-year survival rate proxy ³⁶36. Asadzadeh Vostakolaei F, Karim-Kos HE, Janssen-Heijnen MLG, Visser O, Verbeek ALM, Kiemeney LALM. The validity of the mortality to incidence ratio as a proxy for site-specific cancer survival. Eur J Public Health 2011; 21:573-7., according to Equation 4:

Where: SRM is the standardized mortality rate and SRI is the standardized incidence rate.

Statistical analyses were performed using the softwares Microsoft Excel 2016 (https://products.office.com/) and Stata 15.0 (https://www.stata.com). The map was built using the TabWin version 4.1.5 (http://siab.datasus.gov.br/DATASUS/index.php?area=060805&item=3).

The research was approved by the Research Ethics Committee of the School of Medical Sciences, State University in Campinas (opinion n. 09217719.9.0000.5404).

Results

Among the studied neoplasms, breast and colorectal cancer were the most prevalent in the three SVS. Thyroid cancer was the third most prevalent for women who live in areas of lowest and intermediate vulnerability whereas lung and cervical cancer were the third and fourth for women who live in areas of highest social vulnerability, with similar incidences (Table 1).

A comparison between the three strata shows that women of higher social vulnerability have higher mortality rates for cervical, stomach, and lung cancer and lower mortality rates for breast and colorectal cancer than women of lower vulnerability (Table 2).

The 5-year survival estimate was lower in SVS3 (highest vulnerability) than in SVS1 (lowest vulnerability) for all types of cancer analyzed, with the greatest difference observed for stomach cancer and the smallest difference for cervical cancer (Table 3).

The incidence RR between SVS3 and SVS1 show that women living in areas of highest social vulnerability have a lower risk of breast cancer (RR = 0.46), colorectal cancer (RR = 0.56), and thyroid cancer (RR = 0.32) and higher risk of cervical cancer (RR = 2.32). Lung and stomach cancers showed no significant differences (Table 4).

Women of lowest social vulnerability had a higher mortality risk for breast (RR = 0.69) and colorectal cancers (RR = 0.69) whereas women of highest social vulnerability had a higher mortality risk for cervical (RR = 2.35) and stomach cancers (RR = 1.43), with no differences in lung and thyroid neoplasms (Table 4).

The concentration indices for incidence and mortality rates confirm the inequalities verified with the RR between SVS3 and SVS1. The incidence concentration index was positive for breast, colorectal, and thyroid cancers, indicating a higher risk for women of lower social vulnerability strata, and negative for cervical cancer, indicating a higher risk for women of higher social vulnerability (Table 4). Stomach and lung cancers showed no significant inequality (Table 4). The mortality concentration index was positive for breast and colorectal cancers, although lower than the incidence index, and negative for cervical and stomach cancers, with no significant differences regarding thyroid and lung cancers (Table 4).

Discussion

Our results indicate that social disparities greatly differ according to the location of the cancer and the type of indicator analyzed. Overall, the lower SVS has higher incidences of breast, thyroid, and colorectal cancer and higher mortality rates from breast and colorectal cancers. However, inequalities were lower in mortality than in incidence. The high vulnerability stratum had a lower estimated survival for all types of cancer analyzed.

Most research shows that women of higher socioeconomic status have a higher incidence of breast cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.^,44. Liu Z, Zhang K, Du XL. Risks of developing breast and colorectal cancer in association with incomes and geographic locations in Texas: a retrospective cohort study. BMC Cancer 2016; 16:294.. Mackillop et al. ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12. found that women in the decile of highest socioeconomic status had a higher risk of breast cancer than those of the lowest socioeconomic level in the United States (RR = 1.35) and in the province of Ontario, Canada (RR = 1.10). A study conducted in Texas (United States) from 2008 to 2011 found a 69% higher incidence of breast cancer in women residing in areas of higher income ⁴4. Liu Z, Zhang K, Du XL. Risks of developing breast and colorectal cancer in association with incomes and geographic locations in Texas: a retrospective cohort study. BMC Cancer 2016; 16:294.. Our study identified greater inequalities than the mentioned surveys and found that the incidence of breast cancer in women of lowest social vulnerability was 2.18 times higher than in women of highest vulnerability.

According to our results, women from the highest social vulnerability stratum had a 32% lower risk of dying from breast cancer. Evidence from research carried out in Southern Spain and Costa Rica found that women from the lowest socioeconomic stratum had an 18% and a 35% lower risk of death from breast cancer in Spain ¹⁸18. Santos-Sánchez V, Córdoba-Doña JA, Viciana F, Escolar-Pujolar A, Pozzi L, Ramis R. Geographical variations in cancer mortality and social inequalities in southern Spain (Andalusia). 2002-2013. PLoS One 2020; 15:e0233397. and in Costa Rica, respectively ³⁷37. Fantin R, Santamaría-Ulloa C, Barboza-Solís C. Socioeconomic inequalities in cancer mortality: is Costa Rica an exception to the rule? Int J Cancer 2020; 147:1286-93.. Other studies found no social inequalities regarding breast cancer mortality rates, including those conducted by Menvielle et al. ¹⁷17. Menvielle G, Rey G, Jougla E, Luce D. Diverging trends in educational inequalities in cancer mortality between men and women in the 2000s in France. BMC Public Health 2013; 13:823. in France between 1999 and 2007, Gadeyne et al. ³⁸38. Gadeyne S, Deboosere P, Vandenheede H, Neels K. Does birth history account for educational differences in breast cancer mortality? A comparison of premenopausal and postmenopausal women in Belgium. Int J Cancer 2012; 131:2878-85. in Belgium from 1991 to 1995, and Power et al. ³⁹39. Power C, Hyppönen E, Smith GD. Socioeconomic position in childhood and early adult life and risk of mortality: a prospective study of the mothers of the 1958 British birth cohort. Am J Public Health 2005; 95:1396-402. in the United Kingdom. In South Korea, inequality went the opposite direction, with higher breast cancer mortality rates among women in the lowest socioeconomic segments ⁴⁰40. Kim CW, Lee SY, Moon OR. Inequalities in cancer incidence and mortality across income groups and policy implications in South Korea. Public Health 2008; 122:229-36..

Our results indicated that women of lower social vulnerability had an 8.7% higher 5-year survival rate. Similarly, in the United States, they had an 8.3% higher rate ⁴¹41. Feinglass J, Rydzewski N, Yang A. The socioeconomic gradient in all-cause mortality for women with breast cancer: findings from the 1998 to 2006 National Cancer Data Base with follow-up through 2011. Ann Epidemiol 2015; 25:549-55.. In Colombia, women with contributory and special health insurance had a 10% higher survival rate than women who had subsidized coverage or no health insurance ²²22. Arias-Ortiz NE, de Vries E. Health inequities and cancer survival in Manizales, Colombia: a population-based study. Colomb Med 2018; 49:63-72.. Gorey et al. ²³23. Gorey KM, Luginaah IN, Holowaty EJ, Fung KY, Hamm C. Breast cancer survival in Ontario and California, 1998-2006: socioeconomic inequity remains much greater in the United States. Ann Epidemiol 2009; 19:121-4. found that women from the lowest income stratum in California (United States) had lower survival rates (0.89; 95%CI: 0.81; 0.98), but the authors identified no statistically significant difference in survival in Ontario.

Our study found that women from the lowest social vulnerability stratum have higher mortality and incidence rates of breast cancer because of a greater exposure to risk factors, including reproductive factors and hormone replacement therapy ¹⁶16. Lundqvist A, Andersson E, Ahlberg I, Nilbert M, Gerdtham U. Socioeconomic inequalities in breast cancer incidence and mortality in Europe: a systematic review and meta-analysis. Eur J Public Health 2016; 26:804-13.^,3838. Gadeyne S, Deboosere P, Vandenheede H, Neels K. Does birth history account for educational differences in breast cancer mortality? A comparison of premenopausal and postmenopausal women in Belgium. Int J Cancer 2012; 131:2878-85.^,3939. Power C, Hyppönen E, Smith GD. Socioeconomic position in childhood and early adult life and risk of mortality: a prospective study of the mothers of the 1958 British birth cohort. Am J Public Health 2005; 95:1396-402.. The higher incidence could also be caused by a greater access to mammography, which detects small tumors in the early stages of the disease ⁴²42. Bray F, McCarron P, Parkin DM. The changing global patterns of female breast cancer incidence and mortality. Breast Cancer Res 2004; 6:229.^,4343. Welch HG, Prorok PC, O'Malley AJ, Kramer BS. Breast-cancer tumor size, overdiagnosis, and mammography screening effectiveness. N Engl J Med 2016; 375:1438-47.. Mortality rates showed lower inequality than incidence rates and women of higher social vulnerability had a lower 5-year survival rate, which could indicate that the socially-disadvantaged segment has difficulty in accessing diagnosis and treatment in the early stages of cancer ²2. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394-424.^,1515. Girianelli VR, Gamarra CJ, Azevedo e Silva G. Disparities in cervical and breast cancer mortality in Brazil. Rev Saúde Pública 2014; 48:459-67.^,2121. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018; 391:1023-75..

Our findings show a higher incidence and mortality from colorectal cancer in women residing in areas of lower social vulnerability. On the other hand, a study carried out in Canada and in the United States found that women in poorer socioeconomic conditions had a higher incidence of this type of cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.. Other studies carried out in Finland ¹⁰10. Savijärvi S, Seppä K, Malila N, Pitkäniemi J, Heikkinen S. Trends of colorectal cancer incidence by education and socioeconomic status in Finland. Acta Oncol (Madr) 2019; 58:1557-63. and California ⁴⁴44. Steinbrecher A, Fish K, Clarke CA, West DW, Gomez SL, Cheng I. Examining the association between socioeconomic status and invasive colorectal cancer incidence and mortality in California. Cancer Epidemiol Biomarkers Prev 2012; 21:1814-22. found no association between colorectal cancer incidence and socioeconomic status.

Regarding mortality, a survey carried out in California found that women of the lower socioeconomic level had higher rates of deaths from colorectal cancer ⁴⁴44. Steinbrecher A, Fish K, Clarke CA, West DW, Gomez SL, Cheng I. Examining the association between socioeconomic status and invasive colorectal cancer incidence and mortality in California. Cancer Epidemiol Biomarkers Prev 2012; 21:1814-22., whereas other studies conducted in Spain and Colombia found no differences between socioeconomic strata ¹²12. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15.^,1818. Santos-Sánchez V, Córdoba-Doña JA, Viciana F, Escolar-Pujolar A, Pozzi L, Ramis R. Geographical variations in cancer mortality and social inequalities in southern Spain (Andalusia). 2002-2013. PLoS One 2020; 15:e0233397.. Nevertheless, results of a research conducted in Costa Rica were similar to those of Campinas, in which the higher socioeconomic level had higher mortality rates ³⁷37. Fantin R, Santamaría-Ulloa C, Barboza-Solís C. Socioeconomic inequalities in cancer mortality: is Costa Rica an exception to the rule? Int J Cancer 2020; 147:1286-93..

Studies carried out in Finland, Denmark, and the United States show that rates of incidence and mortality from colorectal cancer were highest in the higher socioeconomic level until the 1980s and, from 2000 onward, in the higher social vulnerability level ¹⁰10. Savijärvi S, Seppä K, Malila N, Pitkäniemi J, Heikkinen S. Trends of colorectal cancer incidence by education and socioeconomic status in Finland. Acta Oncol (Madr) 2019; 58:1557-63.^,1111. Lynge E, Martinsen JI, Larsen IK, Kjarheim K. Colon cancer trends in Norway and Denmark by socio-economic group: a cohort study. Scand J Public Health 2015; 43:890-8.^,1919. Enewold L, Horner MJ, Shriver CD, Zhu K. Socioeconomic disparities in colorectal cancer mortality in the United States, 1990-2007. J Community Health 2014; 39:760-6.. Incidence and mortality from colorectal cancer increased partly because the countries’ economic growth affected the population’s dietary pattern, increased obesity, and physical inactivity ¹¹11. Lynge E, Martinsen JI, Larsen IK, Kjarheim K. Colon cancer trends in Norway and Denmark by socio-economic group: a cohort study. Scand J Public Health 2015; 43:890-8.^,4545. Guimarães RM, Rocha PGM, Muzi CD, Ramos RS. Increase income and mortality of colorectal cancer in Brazil, 2001-2009. Arq Gastroenterol 2013; 50:64-9.. The increased exposure to risk factors initially affects the entire population before the socioeconomic strata differ regarding risk identification and cancer prevention and control measures ⁴⁶46. Vaccarella S, Lortet-Tieulent J, Saracci R, Fidler MM, Conway DI, Vilahur N, et al. Reducing social inequalities in cancer: setting priorities for research. Lyon: International Agency for Research on Cancer; 2019. (IARC Scientific Publications, 168).. In the United States, mortality from colorectal cancer decreased 53% from 1975 to 2007 because of changes in risk factors, mainly diet and physical inactivity, increased screening coverage, and improved treatment. However, individuals with higher socioeconomic status had an even greater mortality decrease ¹⁹19. Enewold L, Horner MJ, Shriver CD, Zhu K. Socioeconomic disparities in colorectal cancer mortality in the United States, 1990-2007. J Community Health 2014; 39:760-6..

Women in the lower vulnerability stratum had a 6.42% higher rate of survival from colorectal cancer. Research carried out in Northern Portugal and in South Korea found no differences in survival according to schooling, income level, and occupation ⁴⁷47. Antunes L, Mendonça D, Bento MJ, Rachet B. No inequalities in survival from colorectal cancer by education and socioeconomic deprivation: a population-based study in the North Region of Portugal, 2000-2002. BMC Cancer 2016; 16:608.^,4848. Lee HE, Kim EA, Zaitsu M, Kawachi I. Occupational disparities in survival in Korean women with cancer: a nationwide registry linkage study. BMJ Open 2020; 10:e039259.. Women in the higher vulnerability stratum possibly have lower survival rates because of a late diagnosis, when tumors are in more advanced stages.

Similarly to studies of other countries ³⁹39. Power C, Hyppönen E, Smith GD. Socioeconomic position in childhood and early adult life and risk of mortality: a prospective study of the mothers of the 1958 British birth cohort. Am J Public Health 2005; 95:1396-402.^,4949. Lortet-Tieulent J, Franceschi S, Dal Maso L, Vaccarella S. Thyroid cancer "epidemic" also occurs in low- and middle-income countries. Int J Cancer 2019; 144:2082-7.^,5050. Hoebel J, Kroll LE, Fiebig J, Lampert T, Katalinic A, Barnes B, et al. Socioeconomic inequalities in total and site-specific cancer incidence in Germany: a population-based registry study. Front Oncol 2018; 8:402., our study found that women with lower social vulnerability have higher incidence rates of thyroid cancer. On the other hand, mortality rates from thyroid cancer were equal between SVS. Deaths from thyroid cancer are rare and we found no studies which analyzed inequalities in this cancer’s mortality. Our results showed that women from the lowest SVS had a higher 5-year survival rate, corroborating with studies conducted in the United States and in South Korea ⁶6. Swegal WC, Singer M, Peterson E, Feigelson HS, Kono SA, Snyder S, et al. Socioeconomic factors affect outcomes in well-differentiated thyroid cancer. Otolaryngol Head Neck Surg 2016; 154:440-5.^,4040. Kim CW, Lee SY, Moon OR. Inequalities in cancer incidence and mortality across income groups and policy implications in South Korea. Public Health 2008; 122:229-36.. We found that the highest social level has a three times higher cancer incidence than the lowest level, which suggests a cancer overdiagnosis in this part of the population ²2. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394-424.^,4949. Lortet-Tieulent J, Franceschi S, Dal Maso L, Vaccarella S. Thyroid cancer "epidemic" also occurs in low- and middle-income countries. Int J Cancer 2019; 144:2082-7.^,5151. Welch HG, Black WC. Overdiagnosis in cancer. J Natl Cancer Inst 2010; 102:605-13..

Women with higher social vulnerability had a higher incidence of cervical cancer, corroborating with the usual literature ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.^,77. Singh GK, Miller BA, Hankey BF, Edwards BK. Persistent area socioeconomic disparities in U.S. incidence of cervical cancer, mortality, stage, and survival, 1975-2000. Cancer 2004; 101:1051-7.^,88. Mihor A, Tomsic S, Zagar T, Lokar K, Zadnik V. Socioeconomic inequalities in cancer incidence in Europe: a comprehensive review of population-based epidemiological studies. Radiol Oncol 2020; 54:1-13.^,5050. Hoebel J, Kroll LE, Fiebig J, Lampert T, Katalinic A, Barnes B, et al. Socioeconomic inequalities in total and site-specific cancer incidence in Germany: a population-based registry study. Front Oncol 2018; 8:402.. In Germany, from 2010 to 2013, women from the lowest socioeconomic stratum had a 12% higher risk of having cervical cancer than women from the highest socioeconomic stratum ⁵⁰50. Hoebel J, Kroll LE, Fiebig J, Lampert T, Katalinic A, Barnes B, et al. Socioeconomic inequalities in total and site-specific cancer incidence in Germany: a population-based registry study. Front Oncol 2018; 8:402.. In Canada and the United States, women of higher socioeconomic status also had a lower incidence of cervical cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.. The same relation is observed for mortality. In our study, women of higher social vulnerability had 2.35 times higher mortality rates. A study carried out in Colombia between 1998 and 2007 found that women with lower schooling levels had over five times higher rates of mortality from cervical cancer than women with higher schooling levels (RR = 5.75) ¹²12. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15.. In South Korea, women of lowest socioeconomic status had over two times higher mortality rates than women of highest socioeconomic status ⁴⁰40. Kim CW, Lee SY, Moon OR. Inequalities in cancer incidence and mortality across income groups and policy implications in South Korea. Public Health 2008; 122:229-36..

Unlike other studies ²⁴24. Singh GK, Jemal A. Socioeconomic and racial/ethnic disparities in cancer mortality, incidence, and survival in the United States, 1950-2014: over six decades of changing patterns and widening inequalities. J Environ Public Health 2017; 2017:2819372.^,4848. Lee HE, Kim EA, Zaitsu M, Kawachi I. Occupational disparities in survival in Korean women with cancer: a nationwide registry linkage study. BMJ Open 2020; 10:e039259., we found that women of lower and higher social vulnerability had less than 1% difference in survival from cervical cancer. Women from the highest and the lowest socioeconomic strata had a 7% difference in survival in the United States between 1988 and 1994 ²⁴24. Singh GK, Jemal A. Socioeconomic and racial/ethnic disparities in cancer mortality, incidence, and survival in the United States, 1950-2014: over six decades of changing patterns and widening inequalities. J Environ Public Health 2017; 2017:2819372.. In South Korea, women of the working class with minimum qualifications had a 42% lower survival rate than more qualified workers ⁴⁸48. Lee HE, Kim EA, Zaitsu M, Kawachi I. Occupational disparities in survival in Korean women with cancer: a nationwide registry linkage study. BMJ Open 2020; 10:e039259.. The small difference in survival between women of higher and lower social vulnerability contrasts with the results of incidence and mortality, which are unfavorable for women of higher social vulnerability.

We found no evidence of inequality in the incidence of stomach cancer among women from the different analyzed strata. Mackillop et al. ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12. also found no difference among Canadian women. Studies in the United States and Germany, however, found that women from the lower socioeconomic segment had a higher incidence of stomach cancer ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12.^,5050. Hoebel J, Kroll LE, Fiebig J, Lampert T, Katalinic A, Barnes B, et al. Socioeconomic inequalities in total and site-specific cancer incidence in Germany: a population-based registry study. Front Oncol 2018; 8:402.. Regarding mortality, we found that women in the highest SVS in Campinas had a 43% higher risk of dying from stomach cancer than those of lowest vulnerability, corroborating with studies conducted in Spain and Colombia ¹²12. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15.^,1818. Santos-Sánchez V, Córdoba-Doña JA, Viciana F, Escolar-Pujolar A, Pozzi L, Ramis R. Geographical variations in cancer mortality and social inequalities in southern Spain (Andalusia). 2002-2013. PLoS One 2020; 15:e0233397.. Mortality was 26% higher in women from the lowest socioeconomic status in Spain ¹⁸18. Santos-Sánchez V, Córdoba-Doña JA, Viciana F, Escolar-Pujolar A, Pozzi L, Ramis R. Geographical variations in cancer mortality and social inequalities in southern Spain (Andalusia). 2002-2013. PLoS One 2020; 15:e0233397. and 98% higher in women who only attended elementary school than in those with higher education in Colombia ¹²12. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15.. According to a study conducted in Colombia ²²22. Arias-Ortiz NE, de Vries E. Health inequities and cancer survival in Manizales, Colombia: a population-based study. Colomb Med 2018; 49:63-72., the survival of women with subsidized coverage was 30% lower than of those who had better-coverage health insurance. This supports our findings that women with stomach cancer in the highest vulnerable stratum have lower survival rates. However, authors of a study conducted in South Korea found no difference in the survival of women with stomach cancer according to occupational groups ⁴⁸48. Lee HE, Kim EA, Zaitsu M, Kawachi I. Occupational disparities in survival in Korean women with cancer: a nationwide registry linkage study. BMJ Open 2020; 10:e039259..

Women of highest social vulnerability have higher mortality and lower survival rates from stomach cancer, which could indicate difficulties in accessing diagnosis and timely treatment.

Although we found no inequalities in the incidence and mortality from lung cancer, other authors found higher cancer rates in the lower socioeconomic levels in Canada and the United States ³3. Mackillop WJ, Zhang-Salomons J, Boyd CJ, Groome PA. Associations between community income and cancer incidence in Canada and the United States. Cancer 2000; 89:901-12., Spain ¹⁸18. Santos-Sánchez V, Córdoba-Doña JA, Viciana F, Escolar-Pujolar A, Pozzi L, Ramis R. Geographical variations in cancer mortality and social inequalities in southern Spain (Andalusia). 2002-2013. PLoS One 2020; 15:e0233397., and Colombia ¹²12. De Vries E, Arroyave I, Pardo C, Wiesner C, Murillo R, Forman D, et al. Trends in inequalities in premature cancer mortality by educational level in Colombia, 1998-2007. J Epidemiol Community Health 2015; 69:408-15.. On the other hand, a study carried out in Costa Rica found no differences in lung cancer mortality between socioeconomic strata ³⁷37. Fantin R, Santamaría-Ulloa C, Barboza-Solís C. Socioeconomic inequalities in cancer mortality: is Costa Rica an exception to the rule? Int J Cancer 2020; 147:1286-93.. Differences observed between countries are possibly caused by temporal changes in the distribution of smoking, a practice which used to be common in segments of higher socioeconomic status and is now prevalent in the poorer segments of the population ⁹9. Kogevinas EM, Pearce N, Susser M, Boffetta P, editors. Social inequalities and cancer. Lyon: International Agency for Research on Cancer; 1997. (IARC Scientific Publications, 138)..

This study found that women of highest social vulnerability had the lowest rate of survival from lung cancer. Similarly, in South Korea, workers with minimum qualifications had a 41% lower rate of survival from lung cancer than those most qualified ⁴⁸48. Lee HE, Kim EA, Zaitsu M, Kawachi I. Occupational disparities in survival in Korean women with cancer: a nationwide registry linkage study. BMJ Open 2020; 10:e039259.. On the other hand, a study carried out in Colombia found no difference in the survival of women with lung cancer according to schooling ²²22. Arias-Ortiz NE, de Vries E. Health inequities and cancer survival in Manizales, Colombia: a population-based study. Colomb Med 2018; 49:63-72..

Lung cancer is quite aggressive and leads to low survival rates in most countries ²¹21. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018; 391:1023-75. because of its late diagnosis, considering that the disease is usually silent and causes no symptoms in the early stages ⁵²52. Instituto Nacional de Câncer José Alencar Gomes da Silva. Estimativa 2018. Incidência de câncer no Brasil. Rio de Janeiro: Instituto Nacional de Câncer José Alencar Gomes da Silva; 2018.. Women living in areas of lower social vulnerability have higher 5-year survival rates, which could indicate access to better treatment ⁴⁰40. Kim CW, Lee SY, Moon OR. Inequalities in cancer incidence and mortality across income groups and policy implications in South Korea. Public Health 2008; 122:229-36..

Determinants of social inequalities in the occurrence and evolution of cancer cases influence the degree of exposure to risk factors related to socioeconomic conditions and lifestyle, environmental and occupational factors, access to screening and early-diagnosis programs, access to and quality of treatment, and even palliative care ⁹9. Kogevinas EM, Pearce N, Susser M, Boffetta P, editors. Social inequalities and cancer. Lyon: International Agency for Research on Cancer; 1997. (IARC Scientific Publications, 138).^,4646. Vaccarella S, Lortet-Tieulent J, Saracci R, Fidler MM, Conway DI, Vilahur N, et al. Reducing social inequalities in cancer: setting priorities for research. Lyon: International Agency for Research on Cancer; 2019. (IARC Scientific Publications, 168)..

The incidence of most types of cancer analyzed is associated with lifestyle and exposure to risk factors that can be modified, particularly smoking, alcohol abuse, obesity, physical inactivity, inadequate diet, among others ⁵³53. Toporcov TN, Wünsch Filho V. Epidemiological science and cancer control. Clinics 2018; 73 Suppl 1:e627s.^,5454. Danaei G, Vander Hoorn S, Lopez AD, Murray CJL, Ezzati M. Causes of cancer in the world: comparative risk assessment of nine behavioural and environmental risk factors. Lancet 2005; 366:1784-93.. Temporal changes have affected the distribution of such factors among the socioeconomic segments of the Brazilian population ⁵⁵55. Malta DC, Bernal RTI, Vieira Neto E, Curci KA, Pasinato MTM, Lisbôa RM, et al. Trends in risk and protective factors for noncommunicable diseases in the population with health insurance in Brazil from 2008 to 2015. Rev Bras Epidemiol 2018; 21 Suppl 1:e180020..

Women from the highest social vulnerability stratum had higher mortality from cervical and stomach cancers, lower inequality in the mortality than in the incidence of breast and colorectal cancer, and lower 5-year survival rates for the six types of cancer analyzed. This could indicate that these women have smaller access to screening, early diagnosis, and treatment programs, resulting in shorter survival time from delay in treatment ²¹21. Allemani C, Matsuda T, Di Carlo V, Harewood R, Matz M, Nikšić M, et al. Global surveillance of trends in cancer survival 2000-14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet 2018; 391:1023-75.^,5656. Woods LM, Rachet B, Coleman MP. Origins of socio-economic inequalities in cancer survival: a review. Ann Oncol 2006; 17:5-19..

Considering that those of highest social vulnerability have lower survival rates, the Brazilian Ministry of Health created a law that establishes a maximum of 60 days between cancer diagnosis and the beginning of treatment, seeking to reduce delays ⁵⁷57. Brasil. Lei nº 12.732, de 22 de novembro de 2012. Dispõe sobre o primeiro tratamento de paciente com neoplasia maligna comprovada e estabelece prazo para seu início. Diário Oficial da União 2012; 23 nov.. Since the Brazilian Unified National Health System (SUS) was implemented in Brazil in 1998, oncology policies have become more organized, including health promotion actions, screening programs for breast and cervical cancer, and access to early diagnosis and treatment ⁵⁸58. Migowski A, Atty ATM, Tomazelli JG, Dias MBK, Jardim BC. A atenção oncológica e os 30 anos do Sistema Único de Saúde. Rev Bras Cancerol 2018; 64:247-50.; however, achieving an equal provision of cancer care in Brazil remains a challenge ¹⁵15. Girianelli VR, Gamarra CJ, Azevedo e Silva G. Disparities in cervical and breast cancer mortality in Brazil. Rev Saúde Pública 2014; 48:459-67..

One of the limitations of our study is the use of survival estimates calculated from the complement of the ratio between mortality and incidence rates and not from the follow-up cohort of patients with cancer. However, we emphasize that this method is recommended as a proxy for 5-year survival rates, as long as the mortality information is of high quality and the incidence and survival rates are stable, and that it has been used in other articles ³⁵35. Schneider MC, Castillo-Salgado C, Bacallao J, Loyola E, Mujica OJ, Vidaurre M, et al. Métodos de mensuração das desigualdades em saúde. Rev Panam Salud Pública 2002; 12:398-414.^,5959. Parkin DM, Bray F. Evaluation of data quality in the cancer registry: principles and methods. Part II. Completeness. Eur J Cancer 2009; 45:756-64.^,6060. Reis RS, Scaff AJM. Cancer survival in Brazil: estimate through the mortality to incidence ratio. J Public Health Epidemiol 2018; 10:295-302.. Another limitation is that the social vulnerability indicator is ecologically and not individually based, defined according to the area of residence. On the other hand, we used good-quality information to analyze cancer mortality and incidence, seeking to fill a gap in the literature about social inequalities in the incidence, mortality, and survival of different types of cancer in Brazil.

Conclusions

Our results indicate large differences in social inequalities between incidence, mortality, and survival for each type of cancer studied. Women of higher social vulnerability possibly have the smallest differences between mortality and incidence for breast and colorectal cancers, the highest mortality from cervical and stomach cancers, and lower survival rates for all types of cancer because of barriers in accessing early diagnosis and timely treatment. The results also indicate that analyzing social inequalities in the incidence and mortality of neoplasms is essential to implement priority actions which promote health equality.

Acknowledgments

The authors thank Espaço da Escrita (State University in Campinas) for the language services provided.

References

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