Ethnic inequalities in coverage and use of women’s cancer screening in Peru

Objective This study aimed to assess ethnic inequalities in the coverage and utilization of cancer screening services among women in Peru. Methods Data from the 2017–2023 Demographic and Family Health Survey in Peru were analyzed to evaluate ethnic disparities in screening coverage for breast and cervical cancer, including clinical breast examination (CBE), Pap smear test (PST), and mammography. Measures such as the GINI coefficient and Slope Index of Inequality (SII) were used to quantify coverage and utilization disparities among ethnic groups. Results The study included 70,454 women aged 30–69. Among women aged 40–69, 48.31% underwent CBE, 84.06% received PST, and 41.69% underwent mammography. It was found inequalities in coverage for any cancer screening (GINI: 0.10), mammography (GINI: 0.21), CBE (GINI: 0.19), and PST (GINI: 0.06), in 25 Peruvian regions. These inequalities were more pronounced in regions with larger populations of Quechua, Aymara, and Afro-Peruvian women. In rural areas, Quechua or Aymara women (SII: -0.83, -0.95, and − 0.69, respectively) and Afro-Peruvian women (SII: -0.80, -0.92, and − 0.58, respectively) experienced heightened inequalities in the uptake of CBE, mammography, and PST, respectively. Like Quechua or Aymara women (SII: -0.50, SII: -0.52, and SII: -0.50, respectively) and Afro-Peruvian women (SII: -0.50, SII: -0.58, and SII: -0.44, respectively) with only a primary education. Conclusion Ethnic inequalities affect breast and cervical cancer screening coverage across regions in Peru. In Quechua, Aymara, and Afro-Peruvian women the uptake of mammography, CBE, and PST was less frequently than their white or mestizo counterparts. These inequalities are attributed to sociodemographic conditions such as lower education levels and residence in rural or non-capital areas. Supplementary Information The online version contains supplementary material available at 10.1186/s12905-024-03225-6.


Background
In 2022, breast cancer impacted over two million women globally, resulting in an age-standardized mortality rate of 12.7 deaths per 100,000 women [1].Similarly, cervical cancer affected 600,000 women, with an age-standardized mortality rate of 7.1 deaths per 100,000 women [2].However, Peru presents a hopeful trend, with 68% of women aged 25 to 65 having undergone cervical cancer screening, a vital practice for early detection and treatment [3].Notably, although 84% of Peruvian women undergo this screening, the mortality rate for cervical cancer remains high at 12.1% [2,4].Furthermore, despite breast cancer ranking as the second most diagnosed neoplasm in Latin America [2,5], only 16.9% of Peruvian women aged 40-59 had received a mammogram by 2018, and by 2022, the mortality rate for breast cancer stood at 9.4 [2,6].
Guidelines advocate for regular screenings for women aged 40 to 74, with mammograms recommended every one to two years [7].Women aged 30-49 should undergo at least one cervical cancer screening test [8], such as the Papanicolaou test (commonly known as the pap smear test).Detecting cancer early through this proactive approach significantly improves patient survival rates.However, screening programs in low-and middleincome countries encounter challenges in reaching the entire target population [9][10][11].Peru faces obstacles as approximately 50% of breast cancer cases are identified at an advanced stage [12].Responding to these challenges, Peru has revised its breast and cervical cancer screening programs since 2017 to address identified gaps [13].The age ranges for clinical breast examinations have been adjusted to 40 to 69 years, for pap smears 50 to 64 years, and for mammograms 50 to 69 years, with the aim of achieving 60% coverage within the target age group [14,15].Despite significant investment, disparities in cervical and breast cancer screening services persist in Peru [16,17].Contributing factors include inadequate resources, infrastructure limitations, sociodemographic conditions (such as age, income, education, and area of residence), as well as health and personal factors like awareness, language barriers, and cultural beliefs [18][19][20][21].These disparities disproportionately impact women with lower socioeconomic status, leading to increased mortality rates from breast and cervical cancer [22,23].While investigations in Latin America typically focus on sociodemographic factors, ethnicity is often overlooked in studies [24,25].In Peru, a multicultural nation where ethnic identification significantly impacts healthcare access [26,27], it is crucial to examine ethnic disparities in cancer care.Therefore, this study aims to assess ethnic inequities in the coverage and utilization of cancer screening services among women in Peru.

Study design
A cross-sectional study was conducted using data from the Demographic and Family Health Survey (DHS, or ENDES in Spanish) spanning from 2017 to 2023, with a focus on cancer screening coverage among women across 25 regions in Peru.The National Institute of Statistics and Informatics (or INEI acronym in Spanish) annually conducts the DHS survey nationwide.Peru, a populous country in Latin America with approximately 32 million inhabitants, harbors a significant female population, with a notable concentration, particularly among women, in the capital city of Lima [28].This research encompassed an analysis of general cancer screenings, clinical breast examinations, Papanicolaou smear tests, and mammography performance [14,15].

Cancer screening evaluations
The DHS survey includes specific inquiries designed to gather data concerning cancer screening among Peruvian women.These inquiries cover general cancer screening for women aged 30 to 69 (Have you ever undergone a general cancer screening?),clinical breast examinations for women aged 40 to 69 (Have you had a clinical breast exam performed by a physician or other healthcare professional?),Papanicolaou smear tests for women aged 50 to 64 (Have you had a Pap smear test performed by a physician or other healthcare professional?), and mammography for women aged 50 to 69 within the last 24 months (Have you had a mammogram performed by a physician or other healthcare professional?).

Sociodemographic conditions
It was explored how various sociodemographic factors influenced cancer screening coverage or evaluations among women.These characteristics included educational level (none, elementary school, high school, or university), wealth index (ranging from the lower to the first quintile), residency area (urban or rural) and place (capital or other regions), health insurance (with or without), and ethnic groups in Peru (white, mestizo, Quechua or Aymara, and Afro-Peruvian).

Statistical analysis
The analysis was performed using Stata v.17.0, which considered the complex sample of DHS by adjusting for survey design features with the "svy" command.Descriptive statistics, including frequencies and percentages, were calculated for each categorical variable.The Rao-Scott test was utilized to detect notable variations among women who received cancer screening evaluations.

Inequality analysis in coverage
The "lorenz" command was employed to assess distributional inequalities.It was examined ethnic and sociodemographic inequalities in cancer screening coverage among women in 25 Peruvian regions.The GINI coefficient is determined using a graph with two axes and an equidistant line, known as the "equity line, " with a GINI value of zero.To calculate the GINI coefficient, it is necessary to divide the area between the equity line and the Lorenz curve (which illustrates the distribution of cancer coverage in regions) by the total area under the equity line.A GINI coefficient of zero indicates perfect equity, whereas a value of one signifies absolute inequality [29].

Inequality analysis in evaluations
It was also used the "siilogit" command to look at differences between individuals using the Slope Index of Inequality (SII) based on ethnic group and a stratified analysis by sociodemographic conditions to assess differences in how well Peruvian women did on cancer screening evaluations.The SII enables us to include a wealth index as an equity stratifier and calculate inequality with values ranging from − 1 to + 1, where values between − 1 and 0 indicate higher disparity and values between 0 and + 1 represent lower inequality [30].

Sensitivity analysis
Additionally, it was created plots in R Studio v.4.2.2 to represent the geographic distribution of cancer screening coverage among women in 25 regions of Peru.Also, to assess the impact of the COVID-19 pandemic, it was created an annual variation plot showing changes in coverage, GINI index, and SII for cancer screening assessments from 2017 to 2023.

Ethical aspects
Given that the DHS data collection process involved participants' informed consent, no ethical committee evaluation was necessary.Moreover, data obtained from the INEI platform are anonymized and securely stored (http://iinei.inei.gov.pe/microdatos/).
Regarding cancer screening evaluations in target age groups based on sociodemographic variables.The study indicated substantial variations in the percentage of women who received examinations compared to those who did not (p < 0.001).Following wealth quintile and residence, education was the variable with the greatest variation in cancer screening evaluation performance (Table 1).
The study delved into inequality in cancer screening coverage across target age groups of Peruvians women evaluated in 25 regions (Appendix 2).Screening coverage for any cancer among women aged 30-69 revealed a GINI coefficient of 0.10 (95% CI: 0.08 to 0.11).For women aged 50 to 64, Pap test coverage exhibited a GINI coefficient of 0.06 (95% CI: 0.04 to 0.09), while clinical breast examination coverage for women aged 40 to 69 demonstrated a GINI coefficient of 0.19 (95% CI: 0.13 to 0.22).Moreover, mammography coverage among women aged 50 to 69 displayed a GINI coefficient of 0.21 (95% CI: 0.16 to 0.25), with higher inequality observed in regions with larger populations of Quechua, Aymara, and Afro-Peruvian women.But the inequality in coverage for different ethnic groups of women across the 25 regions is higher (Fig. 1).
In the analysis of annual variations in cancer screening coverage for certain age groups of women in the 25 regions (Fig. 4).Pap smear coverage was almost uniform, at approximately 70%.Overall cancer screening coverage in Peru was less than 50% and decreased during the COVID-19 pandemic period (2020-2021).The regions with more white and mestizo women had higher coverage than those with Quechua or Aymara, and Afro-Peruvian women.Also, mammogram coverage was more unequal for women 50-69 than pap smear coverage for women 50-64.Since 2017, inequality has declined, but during and after the pandemic period in Peru, it increased, especially in Quechua or Aymara, and Afro-Peruvian women (Fig. 5).

Discussion
It was found that the coverage for cervical cancer screening with pap testing in Peruvian women exceeded the national target of 60% in 2017 and 80% in 2023 for all women except for those Afro-Peruvians [3,14].This could be related to the high mortality rate for cervical cancer in Peru, an expression of barriers to accessing cancer care in some ethnic groups and [2,31].Notably, women without higher education, with lower incomes, and residing in rural areas or outside of the capital are at higher risk [32,33].The findings also show that nonwhite and mestizo women undergo cervical and breast Fig. 4 Annual variations in cancer screening coverage for women among ethnic groups.Note Peru was affected by the COVID-19 pandemic over the period represented in gray Fig. 5 Annual variations of inequality in cancer screening for women among ethnic groups.Note Peru was affected by the COVID-19 pandemic over the period represented in gray cancer screenings less frequently than other ethnic groups, highlighting inequalities in cancer screening utilization [34][35][36][37].Socioeconomic inequalities faced by Quechua or Aymara women further exacerbate these inequities, suggesting systemic gaps within the Peruvian healthcare system such as limited access to healthcare facilities, particularly for these women, that belonging to native Peruvian groups, who faced challenges such as language barriers, discrimination from healthcare professionals, and differing perspectives on health prevention [18,27,38].
Only one third of women aged 50 to 69 receive mammography screening, contributing to the high prevalence of advanced-stage breast cancer in Peruvian women.Socioeconomic inequity exacerbates challenges in breast cancer screening, diagnosis, and treatment [25,39], with inequalities particularly pronounced among women with lower education levels, lower income, and residing in rural areas where less than 20% of mammograms are performed.White or mestizo women show lower inequalities in all cancer screening evaluations considered in this study, compared to Quechua, Aymara, or Afro-Peruvian women.The inequality in mammography screening underscores the influence of cancer-related beliefs, stigma, and discomfort with screening among non-white or mestizo women [35,40,41].Clinical breast examination emerges as an alternate strategy with higher coverage among Peruvian women, highlighting the importance of boosting awareness through self-examination initiatives [42].
Despite previous research highlighting the exacerbating effects of poverty, lower education, and a lack of health insurance on cancer screening inequalities [43][44][45][46], this study finds that Quechua, Aymara, and Afro-Peruvian women continue to reside in areas marked by significant inequalities in screening services due to these factors.These adverse sociodemographic conditions contribute to increased inequity in cancer screening coverage across Peruvian regions, particularly in those with more women identified as Quechua, Aymara, and Afro-Peruvian [18,27,38].Additionally, this situation could be closer of Brazil context, where breast cancer mortality rates are increasing among Afro-American women [47].Thus, efforts to raise awareness about cancer screening must be evaluated, with a focus on implementing measures to overcome women's screening challenges and establishing systems to facilitate timely cancer diagnosis and treatment initiation [42,48].
Assessing inequalities in cancer screening among Peruvian women is important, and this study reveals higher breast and cervical cancer screening inequalities among Quechua, Aymara, and Afro-Peruvian women residing in rural and non-capital areas.This could be attributed to greater access to healthcare and cancer treatment facilities, specifically in urban areas like Lima, the capital city of Peru, which exhibits the highest rates of pap smear testing, clinical breast examination, and mammography coverage [19,20,49].However, the centralism in Peru and the limited availability of resources, staff, and infrastructure for cancer diagnosis in rural areas underscore the challenges of implementing more sensitive and specific screening tests for breast and cervical cancer [40,50,51].
Furthermore, women with higher education levels demonstrate lower ethnic inequalities in the utilization of mammography and pap smear tests, emphasizing the importance of educational interventions in enhancing cancer knowledge and raising awareness about participating in breast and cervical cancer prevention programs [52][53][54][55].Such programs should encompass not only screening tests but also immunization against the human papillomavirus to prevent cervical cancer malignant lesions [56,57].Additionally, efforts to enhance vaccination coverage and reinforce the regular practice of breast self-examination among women for improve early cancer detection [58,59].
In the period covered in this research on breast and cervical cancer screening inequalities, the COVID-19 pandemic emerged in Peru since 2020 [60,61].It was found that overall cancer screening coverage declined dramatically in this period (2020 and 2021), perhaps due to the confinement and limitations of cancer screening programs, affecting more Quechua, Aymara, and Afro-Peruvian women.The immunization measures for controlling COVID-19 in Peru, could also impact in a minor increase in cancer screening coverage since 2022 [62].Quechua, Aymara, and Afro-Peruvian women had a stable trend of higher mammography and pap test coverage inequality compared to white or mestizo Peruvian women, who exhibited lower inequality in 2022.While there was no consistent pattern of ethnic inequalities in utilization of breast and cervical cancer screening services, Quechua, Aymara, and Afro-Peruvian women exhibited a tendency towards greater inequality during and after the COVID-19 pandemic compared to other ethnic groups.
The inequality measures used in this research approximate the unequal coverage of cancer screening for women belonging to different ethnic groups in the 25 Peruvian regions.However, the GINI coefficient may yield higher inequality estimations for certain sociodemographic conditions due to improper registration of Quechua, Aymara, and Afro-Peruvian groups in certain regions [63].On the other hand, the common trend in inequalities in the use of these cancer screening assessments among Peruvian women estimated with the SII may be an expression of the unequal distribution of wealth across some specific groups that face adverse sociodemographic conditions [64].The higher poverty in Peru after COVID-19 pandemic could explains the increase in health inequalities [65].
The study's limitations in examining ethnic discrepancies in cancer screening coverage and utilization among Peruvian women were due to social desirability bias, where some women gave good responses without testing.Some women may not remember if these screenings were for cancer or may have had other breast and cervical cancer screening tests, such as DNA testing for human papillomavirus, visual inspections using acetic acid or Lugol's iodine on cervix samples, or magnetic resonance and ultrasound scans for breast cancer suspicion.This study did not examine whether certain women were checked for breast or cervical cancer based on family history, past diagnosis or treatment, or screening awareness.However, the DHS's Spanish-only questions and lack of a multicultural approach underrepresent specific ethnic groups.

Conclusion
In conclusion, it was identified ethnic inequalities in breast and cervical cancer screening coverage for women across Peruvians regions.Moreover, those women who faced adverse sociodemographic conditions like lower education levels and living in rural or non-capital places led to significant inequalities in the utilization of mammography and pap smear tests.These inequalities were higher among Quechua, Aymara, and Afro-Peruvian women compared to those identifying as white or mestizo.This is concerning, given the increase in these inequalities during and after the COVID-19 pandemic hit the Peruvian population.

Fig. 1 Fig. 2 Fig. 3
Fig. 1 Inequality in women's cancer screening coverage among different ethnic groups in the 25 Peruvians regions

Table 1
Sociodemographic characteristics of Peruvian women with cancer screening evaluations according to ethnic identifications

Variables Total of Peruvian women aged 30-69 (n = 70,454) Women aged 30-69 screened for cancer (n = 19,839) Women aged 40-69 with clinical breast exam (n = 13,852) Women aged 50-64 with PAP smear test (n = 12,211)
*Weighted estimation for complex sampleNote In the comparison between women according to the performance of cancer screening evaluation with Rao-Scott test, all p-values were less than 0.001