Abstract
Context
Breast and cervical cancer are major public health issues, with high morbidity and mortality rates globally. In 2020, there were an estimated 2.3 million new breast cancer cases and 604,000 new cervical cancer cases worldwide. In Brazil, significant numbers of new cases were projected annually during the 2020–2022 period. Screening for these cancers through mammography and Cytopathologicals is recommended by the World Health Organization.
Objective
To describe the prevalence of self-reported mammography and cytopathological exams according to sociodemographic characteristics before and during the COVID-19 pandemic.
Methods
Panel study with data from the Risk and Protection Factor Surveillance for Chronic Diseases by Telephone Survey (VIGITEL), from 2012 to 2022. The outcomes were mammography in the last two years and cytopathological exams in the last three years. The proportions and 95% confidence intervals were described for the pre-pandemic period (2012–2020) and the pandemic period (2021–2022).
Results
The groups with the largest decreases in the prevalence of mammography were those aged 45–54 years, married, with 12 or more years of education, living in the South region, and Indigenous people. For the cytopathological exam, the groups with the largest declines were those aged 25–34 years, white skin, and residents of the South region.
Conclusion
There was a decrease in the prevalence of both exams, especially among educated women, white women, and those living in the South region.
Keywords: Mammography, Cervical cancer, Breast cancer, COVID-19 Pandemic, Cytopathological test
Introduction
Breast and cervical cancers continue to pose significant health challenges for women [1]. Globally, breast cancer was the second most common type of cancer, with approximately 2.3 million new cases (11.6% of all diagnoses) and 670,000 deaths (6.9% of all cancer deaths), making it the leading cause of cancer death among women in 157 of the 185 countries assessed [1]. Cervical cancer was the eighth most frequent, with 661,000 new cases and 348,000 deaths, being the most common neoplasm among women in 25 countries, mainly in Sub-Saharan Africa, with 94% of deaths occurring in low- and middle-income countries [1]. In Brazil, breast cancer is the most prevalent among women, with an estimated 73,610 new cases per year for 2023–2025, corresponding to an age-standardized incidence rate of 41.89 cases per 100,000 women [2–4]. Cervical cancer ranks third, with an estimated 17,010 new cases annually, resulting in a crude incidence rate of 15.38 cases per 100,000 women [2–4].
For screening and early detection of abnormalities, the World Health Organization (WHO) recommends that mammography be performed every two years for all women aged 50 to 69 years, and that the Cytopathological test be performed annually for all women aged 25 to 64 years who have already initiated sexual activity. After two consecutive normal exams, it can be performed every three years [5]. It is important to highlight that the increase in mortality from these neoplasms is associated with the late diagnosis of cases [5].
However, despite the impact of these cancers in Brazil and around the world, during the COVID-19 pandemic, various health organizations, such as the National Cancer Institute (INCA) and international oncology medical societies, issued recommendations to postpone the screening and treatment of various diseases due to the severity of the pandemic scenario in the country [6]. Thus, health authorities in the states suspended these types of health services in order to prioritize COVID-19-related demands [6, 7], and the functioning of all non-essential health services was affected, including breast and cervical cancer screening.
Regarding sociodemographic characteristics, studies have found that, in the pre-pandemic period, women with lower education and family income, residing in the Northeast region, with black or indigenous skin color, were less likely to undergo preventive exams [8–10]. During the pandemic period, studies showed that inequities in access to and utilization of healthcare services for mammography and cytopathologic exams increased, a situation that may have been worsened by the COVID-19 pandemic. Education level, skin color, marital status, income, and region of residence were the main factors that differentiated women in terms of those who underwent these exams more frequently and those who underwent them less frequently [11, 12].
From this perspective, it can be observed that many areas of healthcare were affected due to the COVID-19 pandemic, including mammography and cytopathologic exams [12]. Previous studies have already shown a decrease in the prevalence of screening exams during the pandemic; however, to date, no studies have been identified that describe the characteristics of the women most affected during the COVID-19 pandemic [12, 14]. Identifying these characteristics is necessary to determine whether inequalities still persist, pinpoint which groups of women have experienced the greatest declines, and guide policymakers in reorganizing healthcare services and directing care, as well as creating an interventionist policy aimed at reversing this situation, with a focus on the most affected groups.
The aim of this study is to describe the prevalence of self-reported mammography and cytopathological exams according to sociodemographic characteristics before and during the COVID-19 pandemic.
Methods
This is a population-based panel study using data from the Risk and Protection Factor Surveillance for Chronic Diseases by Telephone Survey (VIGITEL) from 2012 to 2022, comparing the periods of 2012 to 2020 with 2021 to 2022.
VIGITEL is a telephone survey that is part of the Non-Communicable Diseases Risk Factor Surveillance System (NCD) of the Ministry of Health. It has been conducted annually since 2006, with the objective of monitoring the frequency and distribution of these risk factors in the adult population (aged ≥ 18 years) living in all 26 state capitals and the Federal District of Brazil, in households with at least one landline telephone.
The year 2020 was considered pre-pandemic because the COVID-19 pandemic began in March 2020. Therefore, the telephone interviews conducted by VIGITEL in 2020 were carried out by a specialized company between January and April, due to difficulties imposed by the pandemic on data collection. In the years considered, VIGITEL established a minimum sample size of approximately 1,500 individuals in 2014, 1,600 individuals in 2012, 2,000 individuals in 2013, 2015, 2016, 2017, 2018, 2019, and 2020. However, in 2020, due to the difficulties imposed by the COVID-19 pandemic on data collection (see "Clarification Note on VIGITEL 2020 Methodology"), a minimum sample size of 1,000 individuals was established in each city. This sample size allows for the estimation, with a 95% confidence level and a maximum margin of error of three percentage points, of the frequency of any risk or protective factor in the adult population.
Another particularity of VIGITEL 2021 is that data collection took place during an unusual period for the survey, from September 2021 to February 2022, enabling data collection during the COVID-19 pandemic. These samples allowed for the estimation, with a 95% confidence level and a maximum margin of error of four percentage points, of the frequency of any risk or protective factor in the adult population (aged ≥ 18 years).
Further details about the sampling process and data collection can be found in the published VIGITEL results, which are publicly available at: https://www.gov.br/saude/pt-br/composicao/vigilancia-em-saude-svs/inqueritos-de-saude/vigitel.
The participants of these surveys were selected through probabilistic sampling established in two phases:
The first phase involved a systematic random selection of at least 5,000 telephone lines per city, based on the registry provided by the National Telecommunications Agency (Anatel). These lines were then randomly selected again and divided into replicas of 200 lines each.
The second phase (carried out after identification) consisted of randomly selecting one adult (aged ≥ 18 years) resident in the selected household, from among the eligible lines for the system that had answered one of the six attempts made at different times.
The outcomes of this study were the percentage of women (> 45 years) who had a mammogram in the last two years and the percentage of women (25 to 64 years) who had a cytopathological exam (Pap smear) in the last three years.
For the first outcome (mammography), the following questions were asked:
“Have you ever had a mammogram, breast X-ray?” with response options: “no” and “yes.”
“How long ago did you have a mammogram?” with response options: “less than 1 year,” “between 1 and 2 years,” “between 2 and 3 years,” “between 3 and 5 years,” and “5 years or more.” For this analysis, the response options “less than 1 year” and “between 1 and 2 years” were grouped together.
For the second outcome (Cytopathological), the following questions were asked:
“Have you ever had a Cytopathological, preventive cervical cancer test?” with response options: “no” and “yes.”
“How long ago did you have a Cytopathological?” with response options: “less than 1 year,” “between 1 and 2 years,” “between 2 and 3 years,” and “in the last 2 years.”
For this analysis, the response options “less than 1 year,” “between 1 and 2 years,” and “between 2 and 3 years” were grouped together.
The independent variables were: Age group: (45–54; 55–64; 65 years or more older for mammography); (24–34; 35–44; 45–54; 55–64 years for cytopathological exam); Skin color/race: (White; Black/Brown; Yellow; Indigenous); Marital status: (Single; Married; Common-law marriage; Widowed; Divorced/Separated); Education level: (0–8 years; 9–11 years; 12 years or more); Region: (North; Northeast; Midwest; Southeast; South);
For statistical analysis, the estimates were weighted to represent the population of each capital, assigning final weights to each individual using the “pesorake” command. This approach aligned the sociodemographic composition of the adult population with a telephone line in the VIGITEL sample to the estimated composition of the total adult population in the same capital.
The Stata software version 16.1 was used to perform this analysis, considering the sampling design of the survey. The proportions of the outcome and their respective 95% confidence intervals (CI) were described according to the following periods: pre-pandemic (2012–2020) and during the pandemic (2021–2022). The absolute difference in outcomes was calculated based on independent variables between the years 2012–2020 (pre-pandemic) and 2021–2022 (during the pandemic) to identify potential effects of the COVID-19 pandemic on the change in outcome prevalence. To assess the differences in proportions between the years 2012–2020 and 2021–2022, a chi-square test was performed. The significance level adopted was 5% for two-tailed tests.
This study was conducted in accordance with the ethical principles outlined in the Declaration of Helsinki. The protocol was approved by National Research Ethics Commission for Human Beings of the Ministry of Health (CAAE: 65,610,017.1.0000.0008). All study participants provided verbal consent to participate in the study; therefore, the signing of the Informed Consent Form (ICF) was replaced by verbal consent, as per the Vigitel survey protocol.
Results
Information from 109,696 women regarding mammography in the last two years and from 183,156 women regarding the cytopathological exam in the last three years was analyzed.
Table 1 describes the sample characteristics for the concatenated years 2012–2020 and 2021–2022. Regarding age group, 25% of the sample was between 25 and 34 years old in both periods. In terms of skin color/race, 51.2% and 56.0% were Black/Brown, 38.7% and 45.2% were single, 37.1% and 38.6% had 9 to 11 years of schooling, and 45.2% and 44.6% resided in the Southeast region during the periods of 2012–2020 and 2021–2022, respectively (Table 1).
Table 1.
Characteristics of the sample of women from the Risk and Protection Factors Surveillance for Chronic Diseases by Telephone Survey (VIGITEL), 2012 to 2022
| Variable | 2012–2020 (%) | 2021–2022 (%) |
|---|---|---|
| Age group | ||
| 18–24 years | 14.8 | 13.3 |
| 25–34 years | 25.2 | 25.0 |
| 35–44 years | 19.3 | 18.6 |
| 45–54 years | 17.4 | 18.1 |
| 55–64 years | 12.4 | 13.5 |
| 60 years or more | 10.9 | 11.6 |
| Skin color/race | ||
| White | 45.6 | 42.1 |
| Black/brown | 51.2 | 56.0 |
| Yellow | 2.0 | 1.2 |
| Indigenous | 1.3 | 0.7 |
| Marital status | ||
| Single | 38.7 | 45.2 |
| Married | 35.8 | 31.0 |
| Common-law marriage | 10.3 | 9.5 |
| Widows | 8.1 | 7.6 |
| Separated/Divorced | 7.1 | 6.7 |
| Education level | ||
| 0–8 years | 32.4 | 26.2 |
| 9–11 years | 37.1 | 38.6 |
| 12 years or more | 30.5 | 35.1 |
| Region | ||
| North | 9.8 | 10.1 |
| Northeast | 25.5 | 25.6 |
| Midwest | 11.4 | 11.7 |
| Southeat | 45.2 | 44.6 |
| South | 8.1 | 8.0 |
Confidence Interval (CI 95%)
Overall, the prevalence of mammography in the last two years was 77.9% (95% CI 77.6;78.1) during the period of 2012–2020 and 72.8% (95% CI 71.8;73.9) during the period of 2021–2022, indicating a decrease of −5.1 percentage points (p.p.).
The groups with the largest declines in the prevalence of mammography in the last two years (for the periods of 2012–2020 and 2021–2022, respectively) were women aged 45 to 54 years: 78.3% (95% CI 77.8;78.3) vs 70.7% (95% CI 68.3;73.1), a decrease of −7.6 p.p., married women: 82.0% (95% CI 81.7;82.4) vs 74.9% (95% CI 73.3;76.5), a decrease of −7.2 p.p., women with 12 or more years of education: 88.5% (95% CI 88.2;88.9) vs 78.7% (95% CI 77.0;80.4), a decrease of −9.8 p.p., women residing in the South region: 81.7% (95% CI 81.0;82.3) vs 72.0% (95% CI 68.8;75.1), a decrease of −9.7 p.p., indigenous women: 73.1% (95% CI 70.7;75.5) vs 50.7% (95% CI 39.6;61.9), a decrease of −22.4 p.p. It is observed that the largest decreases occurred in the group of indigenous women and in the group of women with higher education (Table 2).
Table 2.
Prevalence of self-reported mammography in the last two years, Risk Factors and Protection Surveillance for Chronic Diseases by Telephone Survey (VIGITEL), 2012 to 2022
| Variable | 2012–2020 % (IC95%) | 2021–2022 % (IC95%) | Diference in p.p | p value |
|---|---|---|---|---|
| Total | 77,9 (77,6;78,1) | 72,8 (71,8;73,9) | −5,1 | < 0,001 |
| Age group | ||||
| 45–54 years | 78,3 (77,8;78,3) | 70,7 (68,3;73,1) | −7,6 | < 0,001 |
| 55–64 years | 78,6 (78,2;78,9) | 75,4 (74,0;76,9) | −2,6 | 0,06 |
| 65 years or more | 74,2 (73,7;74,8) | 68,2 (66,2;70,3) | −6,0 | < 0,001 |
| Skin color/race | ||||
| White | 80,4 (80,0;80,7) | 73,1 (71,4;74,8) | −7,3 | < 0,001 |
| Black/brown | 76,8 (76,4;77,2) | 73,3 (71,9;74,8) | −3,5 | 0,07 |
| Yellow | 77,9 (75,8;80,0) | 69,7 (56,9;82,4) | −8,2 | < 0,001 |
| Indigenous | 73,1 (70,7;75,5) | 50,7 (39,6;61,9) | −22,4 | < 0,001 |
| Marital status | ||||
| Single | 70,2 (70,2;71,4) | 68,7 (66,5;70,1) | −1,5 | 0,29 |
| Married | 82,0 (81,7;82,4) | 74,9 (73,3;76,5) | −7,1 | < 0,001 |
| Common-law marriage | 78,7 (77,6;79,6) | 74,0 (70,1;79,6) | −4,7 | 0,01 |
| Widows | 71,9 (71,2;72,6) | 70,7 (67,7;73,7) | −1,2 | 0,54 |
| Separated/Divorced | 76,6 (75,9; 77,3) | 74,5 (71,6;77,5) | −2,1 | 0,27 |
| Education Level | ||||
| 0–8 years | 72,1 (71,6; 72,5) | 68,7 (66,7;70,6) | −3,4 | 0,10 |
| 9–11 years | 80,2 (79,8;80,6) | 74,2 (72,4;76,0) | −6,0 | < 0,001 |
| 12 years or more | 88,5 (88,2;88,9) | 78,7 (77,0;80,4) | −9,8 | < 0,001 |
| Region | ||||
| North | 73,1 (72,5;73,7) | 66,8 (64,5;69,2) | −6,3 | < 0,001 |
| Northeast | 77,3 (76,8;77,7) | 71,7 (69,9;73,5) | −5,6 | < 0,001 |
| Midwest | 77,7 (77,1;78,3) | 68,7 (65,9;71,5) | −9,0 | < 0,001 |
| Southeat | 78,3 (77,6;78,9) | 75,5 (72,9;78,2) | −2,8 | 0,14 |
| South | 81,7 (81,0;82,3) | 72,0 (68,8;75,1) | −9,7 | < 0,001 |
Confidence Interval (CI 95%)
Overall, the prevalence of the cytopathological exam decreased from 81.7% (95% CI 81.6;81.9) during the period of 2012–2020 to 77.2% (95% CI 76.3;78.0) during the period of 2021–2022, indicating a decrease of −4.5 percentage points (p.p.).
The largest decreases occurred in the following groups, women from the South region: 87.4% (95% CI 86.9;87.9) vs 78.6% (95% CI 75.8;81.4), a decrease of −8.8 p.p., women with 9–11 years of education: 81.1% (95% CI 80.3;81.4) vs 76.5% (95% CI 75.1;77.9), a decrease of −4.6 p.p., women with 12 or more years of education: 85.7% (95% CI 85.4;85.9) vs 79.3% (95% CI 78.1;80.5), a decrease of −6.4 p.p., women aged 25 to 34 years: 76.0% (95% CI 75.6;76.5) vs 69.9% (95% CI 67.5;72.3), a decrease of −6.1 p.p. and white women: 84.8% (95% CI 84.6;85.1) vs 79.1% (95% CI 77.8;80.5), a decrease of −5.7 p.p. (Table 3).
Table 3.
Prevalence of self-reported Papanicolaou test in the last three years, Risk and Protection Factors Surveillance for Chronic Diseases by Telephone Survey (VIGITEL), 2012 to 2022
| Variable | 2012–2020 % (IC95%) | 2021–2022 % (IC95%) | Diference in p.p | p value |
|---|---|---|---|---|
| Total | 81,7 (81,6;81,9) | 77,2 (76,3;78,0) | −4,5 | 0,01 |
| Age group | ||||
| 25–34 years | 76,0 (75,6;76,5) | 69,9 (67,5;72,3) | −6,1 | < 0,001 |
| 35–44 years | 84,4 (84,1;84,8) | 78,1 (76,4;79,8) | −6,3 | < 0,001 |
| 45–54 years | 85,5 (85,2;85,8) | 82,7 (81,3;84,2) | −2,8 | 0,53 |
| 55–64 years | 83,0 (82,6;83,3) | 81,6 (80,3;82,9) | 1,4 | 0,42 |
| Skin color/race | ||||
| White | 84,8 (84,6;85,1) | 79,1 (77,8;80,5) | −5,7 | < 0,001 |
| Black/brown | 80,2 (80,0;80,6) | 75,7 (74,5; 76,8) | −4,5 | 0,01 |
| Yellow | 78,9 (77,5;80,4) | 80,1 (71,2;89,0) | 1,2 | 0,50 |
| Indigenous | 75,7 (73,9;77,6) | 85,4 (77,6;93,1) | 9,7 | < 0,001 |
| Marital status | ||||
| Single | 73,1 (72,7;73,5) | 68,5 (66,9;70,0) | −4,6 | 0,02 |
| Married | 88,0 (87,8;88,3) | 84,7 (83,5;85,9) | −3,3 | 0,03 |
| Common-law marriage | 84,3 (83,8;84,8) | 83,7 (81,5;85,9) | −0,6 | 0,71 |
| Widows | 80,0 (79,2;80,7) | 75,5 (71,9;79,1) | −4,5 | 0,02 |
| Separated/Divorced | 84,1 (83,6;85,7) | 84,0 (81,7;86,4) | −0,1 | 0,96 |
| Education level | ||||
| 0–8 years | 78,2 (77,8;78,6) | 74,7 (72,8;76,7) | −3,5 | < 0,001 |
| 9–11 years | 81,1 (80,3;81,4) | 76,5 (75,1;77,9) | −4,6 | 0,02 |
| 12 years or more | 85,7 (85,4;85,9) | 79,3 (78,1;80,5) | −6,4 | < 0,001 |
| Region | ||||
| North | 81,1 (80,7;81,4) | 76,8 (75,3;78,4) | −4,3 | 0,02 |
| Northeast | 75,3 (74,9;75,6) | 70,5 (68,9;72,0) | −4,8 | 0,01 |
| Midwest | 78,9 (78,4;79,4) | 77,1 (74,8;79,4) | −1,8 | 0,34 |
| Southeat | 85,4 (84,9;85,8) | 81,0 (78,9;83,2) | −4,4 | 0,01 |
| South | 87,4 (86,9;87,9) | 78,6 (75,8;81,4) | −8,8 | < 0,001 |
Confidence Interval (CI 95%)
Discussion
The results of this study demonstrated a decrease in the performance of mammography and cytopathological exams in the period of 2021–2022 compared to the period of 2012–2020. Regarding mammography, the groups with the largest decreases were women aged 45 to 59 years, married women, those with higher education, and women residing in the South region. As for the cytopathological exam, the groups with the largest decreases were women aged 25 to 34 years, those with higher education, white women, and those residing in the South region.
In our study, the greatest decrease in the prevalence of mammography was observed among women aged 45 to 54 years, which may be explained by the lack of encouragement for mammography between the ages of 45 and 50, since the current Brazilian guidelines for breast cancer screening emphasize the importance of screening above this age group (50 to 69 years) [15].
However, another group that showed a significant decrease in the prevalence of this exam was women aged 65 years or older. Among the factors that may have influenced this result are the fear of COVID-19 contamination, especially among elderly women, difficulty in accessing care through the SUS (Unified Health System) due to the system's overload caused by the pandemic, and the fear of detecting any abnormalities in the exam [7].
To explain the decrease in the prevalence of the cytopathological exam among women aged 25 to 34 years, several hypotheses have been raised. Studies point to the main reasons for non-adherence to the exam as shame associated with body exposure to the healthcare professional, fear of the exam results, difficulty in scheduling appointments, lack of proper infrastructure and work processes, and the absence of gynecological complaints [16, 17].
Supporting this hypothesis, other studies show that the main factors contributing to the decrease in cytopathological exams were women with a diagnosis of precursor lesions opting to wait for the pandemic to ease before starting treatment, the impact of the overload of outpatient services in addressing COVID-19-related demands, the suspension of elective procedures, and the consequent reduction in cervical cancer screening [7, 18].
The literature shows that married women constitute a group with high adherence to mammography [11]; however, during the years that the pandemic lasted, this scenario changed. Among the reasons raised to explain the decrease in mammography prevalence among married women is the fact that the exam requires traveling to imaging clinics, which often have waiting lists in enclosed spaces and require proximity to the radiologist, with no possibility of social distancing during the procedure. In this sense, women who underwent the exam would be putting themselves at risk of contracting COVID-19 [19].
Furthermore, married women seemed to be more conscious about the risk of contracting the novel coronavirus during the pandemic, showing greater concern in following safety measures, as they feared both contracting and transmitting the virus to their family members [20].
There was a decrease in the prevalence of mammography and cytopathological exams among more educated women. This group has greater access to healthcare services [21] and, therefore, may have adhered more strictly to the WHO recommendations for COVID-19 prevention and control, following isolation and social distancing measures, which resulted in a reduction in the number of exams conducted [22].
There was a decrease in the prevalence of both exams in all regions of Brazil, with a notable reduction in the South region, where technical reports had already described a 30% to 45% decrease in mammography procedures during the pandemic [23]. In Brazil, the measures to combat the new coronavirus varied by state. In Rio Grande do Sul (RS), the Controlled Distancing System was implemented to prevent and combat the COVID-19 pandemic, prioritizing the opening of only essential healthcare services during the years 2020 and 2021 [24].
Another theory considers the fact that the South region was the second most affected by COVID-19, both in absolute and relative numbers, when compared to other regions of the country [25]. Specifically, the state of Rio Grande do Sul (RS) reported 2,292,823 cases and 38,683 deaths by February 2022, the final date of the VIGITEL 2021 interviews, while the state of Paraná reported 2,320,412 cases and 42,077 deaths, and the state of Santa Catarina recorded 1,717,775 cases and 21,488 deaths during the same period [26]. The dissemination of these absolute numbers through news portals and newspapers may have generated a greater sense of fear among women in the South region, contributing to the decrease in the prevalence of these exams [6].
Another hypothesis that may be linked to the decline in the prevalence of mammography is the technical note issued by Nacional Cancer Institute in 2020, advising people not to seek health services for cancer screening and to reschedule their exams for when the containment measures were eased [6].
Regarding race/skin color, Indigenous women experienced the greatest declines in mammography rates. This situation can be explained by the significant geographical limitations in accessing treatment centers for nearly all Indigenous communities, coupled with a reduced presence of health promotion programs during the COVID-19 pandemic [27]. These are historically known and entrenched social inequities/inequalities that were exacerbated by the pandemic [28].
There was a decline in the performance of the Cytopathological among white women. It is observed that, although white women have better access to quality healthcare services and are more aware of the importance of prevention through Cytopathologicals, the pandemic served as both a personal and public incentive to deprioritize this exam [22]. However, it is worth highlighting that Indigenous woman underwent the Cytopathological more during the pandemic compared to the pre-pandemic period. This is because the test is more readily available at basic health units compared to mammography, and this result can be explained by the implementation of a public policy by the Special Secretariat for Indigenous Health (SESAI), aimed at promoting prevention and screening for cervical cancer during the pandemic [29].
In addition to understanding the pandemic-related reductions, it is important to highlight international and national efforts to strengthen cervical cancer screening and early treatment. In 2020, the WHO launched the Global Strategy to Accelerate the Elimination of Cervical Cancer, with the “90–70–90” targets: vaccinate 90% of girls against HPV by age 15, screen 70% of women with a high-performance test at ages 35 and 45, and ensure that 90% of diagnosed women receive appropriate treatment [30].
Implementing these actions in Brazil is crucial to strengthen organized screening and reduce inequalities in access to prevention and early treatment, especially following interruptions in healthcare services during the pandemic. An important advancement occurred in August 2025 with the introduction of the DNA-HPV molecular test in the SUS, initially in 12 states [31]. This method allows early detection of 14 high-risk HPV genotypes, including in asymptomatic women, increasing the effectiveness of screening and aligning the country with international targets for cervical cancer elimination [31].
To restore coverage, the SUS could implement active follow-up of unscreened women, electronic monitoring, educational campaigns, and flexible access through extended hours, mobile units, and appointment systems. Prioritizing vulnerable groups and strengthening integration between primary care and specialized services can help reduce inequalities and efficiently guide public health interventions.
This study has limitations and strengths. First, there is a regional bias that may interfere with the prevalence of the exams. A limitation already acknowledged by the authors is the geographical restriction of the study to the capitals, which present distinct population characteristics compared to other regions. These cities have greater access to healthcare resources and broader screening coverage, even before the pandemic. Second, there is a selection bias, as the sample only includes individuals from Brazilian capitals and the Federal District who have landline phones; however, this bias was minimized by using post-stratification weighting. Third, a recall bias may have occurred in the self-reported questions about mammography and cytopathological examinations. The small sample size during the COVID-19 pandemic years could also be a limitation. However, it is important to highlight that this study leverages data from a telephone survey with rigorous methodology, being cost-effective, quick, and reliable. Through this study, it is possible to monitor health inequities both before and during the COVID-19 pandemic for comparative purposes.
Finally, among the women evaluated in this analysis, there was a decrease in the coverage of preventive exams post-pandemic. This reduction was led by women from the Southern region and women with higher levels of education. However, one peculiarity was observed: the group of Indigenous women had the greatest decrease in mammography rates but an increase in the performance of the Cytopathological test during this period. Based on these findings, it was generally observed that the inequities were reduced, not due to an improvement in the groups with poorer prevalence rates, but because the decline in prevalence was more pronounced in the groups with better prevalence rates during the pre-pandemic period.
Acknowledgements
YPV is a social demand scholar from the Coordination for the Improvement of Higher Education Personnel (CAPES), process number 88887.605391/2021-00.SCD. PMV is a Junior Postdoctoral fellow from CNPq, and SCD is a research productivity fellow from CNPq.
Abbreviations
- VIGITEL
Risk and Protection Factor Surveillance for Chronic Diseases by Telephone Survey
- NCD
Non-Communicable Diseases Risk Factor Surveillance System
- SUS
Unified Health System
- NCI
National Cancer Institute
- SESAI
Special Secretariat for Indigenous Health
- CAAE
Research Ethics Committee Registration Code
- WHO
World Health Organization
- CI
Confidence Interval
- p.p.
Percentage Points
Authors’ contributions
Vieira YP contributed to the analysis, interpretation of data, writing, and critical revision of the manuscript. Reis RCZ, Versola HA, Fantoura MRC, and Coluci VO contributed to the interpretation of data, writing, and critical revision of the manuscript. Volz PM contributed to the interpretation of data, writing, and critical revision of the manuscript. Dumith SC contributed to the guidance, analysis, and interpretation of data, and the critical revision of the manuscript. All authors approved the final version of the manuscript and are responsible for all its aspects, including ensuring its accuracy and integrity.
Funding
This study has no funding.
Data availability
The datasets analysed during the current study are available in the VIGITEL repositor in https://svs.aids.gov.br/download/Vigitel/.
Declarations
Ethics approval and consent to participate
This study was conducted in accordance with the ethical principles outlined in the Declaration of Helsinki. VIGITEL was approved by the National Research Ethics Commission for Human Beings of the Ministry of Health (CAAE: 65610017.1.0000.0008). Informed consent for participation was obtained verbally via telephone from all participants, in accordance with the Vigitel survey protocol.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Pan American Health Organization (PAHO). Global cancer burden increases amid growing need for services. PAHO/WHO; 2024. Available from: https://www.paho.org/en/news/1-2-2024-global-cancer-burden-growing-amidst-mounting-need-services. Cited 2025 Aug 24.
- 2.National Cancer Institute (INCA). Estimate 2023: Cancer incidence in Brazil. Rio de Janeiro: INCA; 2022. Available from: https://www.gov.br/inca/pt-br/assuntos/cancer/numeros/estimativa.
- 3.National Cancer Institute (INCA). Data and numbers on cervical cancer – Annual report 2023. Rio de Janeiro: INCA; 2023. Available from: https://www.inca.gov.br/sites/ufu.sti.inca.local/files/media/document/dados_e_numeros_colo_22marco2023.pdf.
- 4.Santos MO, Lima FCS, Martins LFL, Oliveira JFP, Almeida LM, Cancela MC. Estimate of cancer incidence in Brazil, 2023–2025. Rev Bras Cancerol. 2023;69(1):e213700. Available from: https://rbc.inca.gov.br/index.php/revista/article/view/3700.
- 5.American Society of Clinical Oncology. COVID-19 guidance for practices translated to seven languages. Alexandria: ASCO; 2020. 2020. Available from: https://www.asco.org/practice-policy/policy-issues-statements/asco-in-action/covid-19-guidance-practices-translated-seven. Cited 2023 May 23.
- 6.National Cancer Institute José Alencar Gomes da Silva. Technical Note – DIDEPRE/CONPREV/INCA – 30/3/2020 Early Detection of Cancer During the Covid-19 Pandemic. 2020.
- 7.Ribeiro CM, Correa F de M, Migowski A. Short-term effects of the COVID-19 pandemic on cancer screening procedures, diagnostic investigation, and treatment in Brazil: a descriptive study, 2019–2020. Epidemiol e Serviços Saúde . 2022;31(1). Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S223796222022000100303&tlng=pt. [DOI] [PMC free article] [PubMed]
- 8.Moreira CB, Dahinten VS, Howard AF, Fernandes AFC, Schirmer J. Factors related to mammography adherence among women in Brazil: A scoping review. Nurs Open. 2021;8(5):2035–49. Available from: https://onlinelibrary.wiley.com/doi/10.1002/nop2.706. [DOI] [PMC free article] [PubMed]
- 9.Vieira RA da C, Formenton A, Bertolini SR. Breast cancer screening in Brazil. Barriers related to the health system. Rev Assoc Med Bras . 2017 May;63(5):466–74. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0104-42302017000500466&lng=en&tlng=en. [DOI] [PubMed]
- 10.Mottram R, Knerr WL, Gallacher D, Fraser H, Al-Khudairy L, Ayorinde A, et al. Factors associated with attendance at screening for breast cancer: a systematic review and meta-analysis. BMJ Open. 2021;11(11):e046660. Available from: https://bmjopen.bmj.com/lookup/doi/10.1136/bmjopen-2020-046660. [DOI] [PMC free article] [PubMed]
- 11.Saes-Silva E, Vieira YP, Viero V dos SF, Rocha JQS, Saes M de O. Trend of inequalities in the performance of mammography in Brazilian capitals in the last ten years. Cien Saude Colet. 2023;28(2):397–404. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232023000200397&tlng=pt. [DOI] [PubMed]
- 12.Cairns A, Jones VM, Cronin K, Yocobozzi M, Howard C, Lesko N, et al. Impact of the COVID-19 Pandemic on Breast Cancer Screening and Operative Treatment. Am Surg . 2022;88(6):1051–3. Available from: http://journals.sagepub.com/doi/10.1177/00031348221087920. [DOI] [PMC free article] [PubMed]
- 13.Masson H. Cervical pap smears and pandemics: The effect of COVID-19 on screening uptake & opportunities to improve. Women’s Heal . 2021;17:174550652110170. Available from: http://journals.sagepub.com/doi/10.1177/17455065211017070. [DOI] [PMC free article] [PubMed]
- 14.Solla Negrao EM, Cabello C, Conz L, Mauad EC, Zeferino LC, Vale DB. The impact of the COVID-19 pandemic on breast cancer screening and diagnosis in a Brazilian metropolitan area. J Med Screen. 2022;096914132211220. Available from: http://journals.sagepub.com/doi/10.1177/09691413221122055. [DOI] [PMC free article] [PubMed]
- 15.National Cancer Institute José Alencar Gomes da Silva. Guidelines for Early Detection of Breast Cancer in Brazil. 2015.
- 16.Jorge RJB, Diógenes MAR, Mendonça FA da C, Sampaio LRL, Jorge Júnior R. Papanicolaou Test: Feelings Reported by Nursing Professionals When Undergoing This Test. Cien Saude Colet. 2011;16(5):2443–51. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232011000500013&lng=pt&tlng=pt. [DOI] [PubMed]
- 17.Barcelos MRB, Lima R de CD, Tomasi E, Nunes BP, Duro SMS, Facchini LA. Quality of cervical cancer screening in Brazil: external assessment of the PMAQ. Rev Saude Publica. 2017;51. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0034-89102017000100261&lng=en&tlng=en. [DOI] [PMC free article] [PubMed]
- 18.Andrade MS, Almeida MMG de, Araújo TM de, Santos KOB. Factors Associated with Non-Adherence to Papanicolau Testing Among Women Attended by the Family Health Strategy in Feira de Santana, Bahia, 2010. Epidemiol e Serviços Saúde. 2014;23(1):111–20. Available from: http://scielo.iec.pa.gov.br/scielo.php?script=sci_arttext&pid=S1679-49742014000100011&lng=en&nrm=iso&tlng=en.
- 19.Lindemann IL, Simonetti AB, Amaral CP do, Riffel RT, Simon TT, Stobbe JC, et al. Perception of the fear of being contaminated by the new Coronavirus. J Bras Psiquiatr. 2021;70(1):3–11. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0047-20852021000100003&tlng=pt.
- 20.Acrani GO, Simonetti AB, Amaral CP do, Simon TT, Stobbe JC, Lindemann IL. Implementation of preventive measures against SARS-CoV-2/Covid-19: a cross-sectional study in Passo Fundo, RS. Cad Saúde Coletiva. 2022. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1414-462X2022005024205&tlng=pt.
- 21.Pinheiro RS, Viacava F, Travassos C, Brito A dos S. Gender, morbidity, access and utilization of health services in Brazil. Cien Saude Colet. 2002;7(4):687–707. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232002000400007&lng=pt&tlng=pt.
- 22.Bezerra ACV, Silva CEM da, Soares FRG, Silva JAM da. Factors Associated with Population Behavior During Social Isolation in the COVID-19 Pandemic. Cien Saude Colet. 2020;25(suppl 1):2411–21. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232020006702411&tlng=pt. [DOI] [PubMed]
- 23.Secretary of Health of the State of Rio Grande do Sul. Technical Note No. 64 – Breast Cancer: Mammograms during the COVID-19 Pandemic in Rio Grande do Sul, 2020–2022. Porto Alegre: Secretary of Health of the State of Rio Grande do Sul; 2021 [cited 2024 Oct 12]. https://www.estado.rs.gov.br/upload/arquivos//nota-tecnica-n-64-marilyn-25-10-22-final-1.pdf
- 24.Rio Grande do Sul. Decree No. 55856 of April 27, 2021. Establishes the Controlled Distancing System for the purposes of prevention and confrontation of the epidemic caused by the novel Coronavirus (COVID-19) within the State of Rio Grande do Sul, reiterating the declaration of a state of emergency, 2021. Available from: https://leisestaduais.com.br/rs/decreto-n-55240-2020-rio-grande-do-sul-institui-o-sistema-de-distanciamento-controlado-para-fins-de-prevencao-e-de-enfrentamento-a-epidemia-causada-pelo-novo-coronavirus-covid-19-no-ambito-do-estado-do-rio-grande-do-sul-rei.
- 25.Secretary of health of Rio Grande do Sul. Coronavirus Dashboard . 2021. Available from: https://ti.saude.rs.gov.br/covid19/. Cited 2023 May 23.
- 26.Brazil. Coronavirus Panel. Brasília: Ministry of Health; 2023 [cited 2023 May 23]. https://covid.saude.gov.br/
- 27.Ribeiro AA, Rossi LA. Covid-19 pandemic and the motivations for demanding health service in indigenous villages. Rev Bras Enferm. 2020;73(suppl 2). Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0034-71672020001400405&tlng=en. [DOI] [PubMed]
- 28.Minayo MC de S, Freire NP. Pandemic exacerbates health inequalities. Cien Saude Colet. 2020;25(9):3555–6. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1413-81232020000903555&tlng=pt. [DOI] [PubMed]
- 29.Brasil. National Health Foundation. National Policy for the Health Care of Indigenous Peoples. 2nd edition. Brasília: Ministry of Health, National Health Foundation; 2002. p. 40.
- 30.WORLD HEALTH ORGANIZATION. Global strategy to accelerate the elimination of cervical cancer as a public health problem. Genebra: WHO; 2020. Available from: https://www.who.int/publications/i/item/9789240014107. Cited 2025 Aug 24.
- 31.Brazil. Ministry of Health (BR). Ministry of Health offers 100% national innovative technology to detect cervical cancer in the SUS. Brasília: Ministry of Health; 2025. Available from: https://www.gov.br/saude/pt-br/assuntos/noticias/2025/agosto/ministerio-da-saude-oferta-tecnologia-inovadora-100-nacional-para-detectar-cancer-do-colo-do-utero-no-sus. Cited 2025 Aug 24.
- 32.Vieira YP, Viero V dos SF, Vargas BL, Nunes GO, Machado KP, Neves RG, et al. Trends and inequalities in self-reported cervical cancer screening in Brazilian capitals from 2011 to 2020. Cad Saude Publica. 2022;38(9). Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0102-311X2022000905011&tlng=pt. [DOI] [PubMed]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets analysed during the current study are available in the VIGITEL repositor in https://svs.aids.gov.br/download/Vigitel/.