Artigos

INTRODUCTION

Cervical cancer (CC) is the fourth most frequent worldwide, with nearly 570,000 cases per year (3.2% of all cancers), corresponding to an estimated risk of 15.1 cases per 100,000 women1,2.
In 2018, the mean age at diagnosis and mortality of CC was 53 and 59 years, respectively. The incidence of CC varies widely, and can be up to twice as high in underdeveloped countries compared to developed countries3,4.
In Latin America and the Caribbean, CC is the leading cause of death in women, with a mortality rate three times higher compared to those in North America5. In 2020, more than half a million women worldwide were diagnosed with CC and approximately 342,000 of these women died as a result of CC, most of them living in poor countries. The estimates for the year 2030 are for an increase in deaths in the Americas, and that 89% of the deaths will occur in Latin America and the Caribbean6.
The main risk factor for CC is infection with the Human Papillomavirus (HPV), a virus that affects skin and mucous membranes and can be detected early by cytological screening through the Pap smear, also known as the preventive exam or oncotic colpocytology. Developed by George Papanicolau in 1930, this is the most common method of cervical cancer screening, as it is one of the most effective and widely used screening tests to detect cervical disease7. Its widespread use of cytological screening stems from its ease, cost-effectiveness, and ability to identify premalignant disease8.
This test is aimed at sexually active women; however, virgins, menopausal women, hysterectomized women, pregnant women, and those who are not sexually active can also undergo it8. It is estimated that up to 80% of deaths from cervical cancer could be avoided by performing the Pap smear regularly, along with adequate patient follow-up for treatment4.
The World Health Organization (WHO) along with the Human Reproduction Programme (HRP) have recently released guidance to assist countries to make fairer and more equitable progress in CC screening and treatment. The recommendations include targets such as achieving 90% coverage of HPV vaccination in girls up to 15 years of age; 70% coverage of Pap smear screening and 90% treatment of precancerous lesions9.
However, public health policies on CC screening guidelines are instituted according to the needs of each country, and these are based on the best available evidence to determine who should be screened and when to start screening10.
In Brazil, screening should be performed from the age of 25 on all women who have started sexual activity, every three years, if the first two annual exams do not show changes, and continue until the age of 64. If there is a change in one of the first two tests, such as HPV infection, the test must be repeated annually10. In the United States, guidelines suggest that screening for CC begin at age 21, preferably between ages 30 to 65, and be repeated every 3 years. In Great Britain, all women aged 25 to 49 years must have the screening, repeated every three years, and those aged 50 to 64 years, repeated every five years. In Canada, the recommendation is that women aged between 25 and 69 be tested every 3 years. In Australia, the age of initiation of screening is lower than in other countries; this country's health department suggests that women between the ages of 18 and 70 should have a Pap smear every 2 years11.
In developed countries, mortality from cervical cancer has decreased dramatically, mainly due to the introduction of the Pap smear. Subramaniam et al. (2011)12 report that 50% of invasive cervical malignancies are diagnosed in patients who have never been screened13. Studies show that, among racial minorities, there is an increase in CC mortality due to disparities in screening, which ranges from basic health information to difficulty in accessing the service14,15. Studies show that black women and those with lower socioeconomic conditions seek less health services to perform the Pap smear16.
Thus, identifying whether the issue of race/skin color per se directly influences access to women's health services with studies of greater scientific evidence is necessary, as it can elucidate racial inequity with fatal consequences. The findings of this research may allow the planning of specific actions and interventions aimed at populations at greater risk, seeking to reduce existing inequities and, consequently, the number of cases and deaths from CC.
Therefore, the objective of this study was to identify in the scientific literature the prevalence of performing the Pap smear among black women and compare it with other ethnic-racial groups.


METHOD

Protocol and registration

For the beginning of this systematic review, a protocol was prepared and registered in the International Prospective Register of Systematic Reviews (PROSPERO) under number CRD42021251764. The Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) statement was used as a writing guide for this review17. In this study, the research question was: “Is there a difference in the prevalence of access to the Pap smear between black women when compared to women of other races and ethnicities?”




Inclusion/exclusion criteria

The inclusion and exclusion criteria of the articles obtained during the searches in the databases were elaborated from the PICO18 strategy. The following studies were included: cross-sectional studies with female participants of all races and/or ethnic groups, without restriction of nationality and age, and which sought access to the Pap smear. Studies with males and children, studies that did not include race or ethnicity, studies did not report the prevalence of access to Pap smear, and those with other methodological designs were excluded.

Search and evaluation methods of studies

The search was performed in PubMed, Web of Science, Lilacs, Scopus, Cinahl databases, in addition to Google Scholar and Open Grey. The searches were carried out without restriction of language or publication date. For the construction of the search strategies, there was the support and consultation of a librarian with experience in the area. MeSH terms and keywords were used: “ethnic groups”, “race factors”, “pap smear test”, “prevalence”, “pap smear”, “Transversal studies” (Box 1).
The results obtained in the databases were exported to the Mendeley Desktop® reference manager version 1.19.4 for the elimination of duplicates. Then, the resulting articles were transferred to the Rayyan QCRI® software for blind reading of the articles. The searches were carried out on April 11, 2021.





Selection of studies

The first stage in the selection of studies consisted of reading titles and abstracts. Those who fulfilled the eligibility criteria were selected for the second stage (full textual reading). In all stages, blind reading was performed by two independent researchers (named MAPS and HKSM). Consensus meetings were held for conflict resolution in both stages; there was no need to consult the third reviewer (IRB). From this analysis, the studies to be included in this systematic review were obtained.


Data extraction

The data extracted from each study included in this review were: authors, year of publication, study location, sample size, age group of the study population, mean age or prevalent age group, race/ethnicity of participants, prevalence of access, measures of association and data collection method.
The search in the databases resulted in 2,906 studies, and of these, 611 were duplicates, totaling 2,295 articles selected for reading the title and abstract. At the end of this stage, 246 studies were selected for full textual reading, and of these, 29 articles met the eligibility criteria and were included in the review (Figure 1).

Risk of bias assessment

To assess methodological quality and risk of bias, the cross-sectional critical assessment tool was used for use in the Joanna Briggs Institute systematic review. The tool consists of eight questions that assess the methodological quality of the study and determine to what extent the study addresses the possibility of bias in its design, conduct and analysis19.
The questions were independently classified by the authors as “Yes”, “No”, “Unclear” or “Not/Applicable”. The classification of risk-of-bias results were evaluated as: (1) low risk, if the studies achieved more than 70% of a "yes" score; (2) moderate risk, if the "yes" score is between 50% and 69%; and (3) high risk of bias, if the bias score, if the “yes” score is less than 49%20. After the classification, carried out individually by MAPS and HKSM, a consensus meeting was held between them to resolve conflicts.

Meta-analysis

The Review Manager software (RevMan; version 5.3.5 – available at: (http://community.cochrane.org/tools/review-production-tools/revman-5/revman-5-download) was used for statistical analysis of the results and construction of the meta-analysis graphs, for which the random effects model was adopted and the Odds Ratio (OR) as a measure of association for dichotomous data, with a confidence interval (CI) of 95%.
Inconsistencies between the results of the studies were quantified using the I2 statistic, which illustrates the percentage of variability in the effect estimates that exceeds the effect of chance: I2 = [(Q - df) / Q] x 100%, where Q is the Cochran's homogeneity test statistic and df is its degrees of freedom. The heterogeneity between the studies was evaluated by visually examining the meta-analysis graphs to verify overlapping confidence intervals, using the Cochran's test for homogeneity with a significance level of 5% and considering the I2 statistic23. A value of I2 less than 50% corresponds to low heterogeneity; 50% or greater, significant heterogeneity and 75% or greater, substantial heterogeneity21.
The results of this meta-analysis were presented through Forest Plot and Funnel Plots, together with the description of their respective analyses.


RESULTS

The data obtained in each methodological stage of this systematic review will be discussed in a descriptive way.
Regarding the method of data collection in the primary studies, 12 studies had their data collected through telephone surveys, 6 studies through household surveys, 3 from medical records, 3 from databases, and 5 through self-administered questionnaires.
The included studies (Table 1) were developed in North and South America, two from Brazil22-23, one from Canada24 and the others from the United States of America (USA). American studies showed greater diversity of ethnic-racial groups among the population studied, however, African-Americans, blacks, whites and Hispanics were the most frequent categories.
Most articles from the USA showed similar prevalence among African Americans and other ethnicities. Brazilian studies show lower screening rates in the black population.
As for the year of publication, the studies included were published between the years 1996 and 2020. The sample showed great variability in size, ranging from 4423 to 169,488 women25.
As for age, in some studies the participants had a minimum age of 18 years14,24-37. In the others, the age group over 20 years was evaluated, most of them between 21 and 65 years22,23,38-43,49.
Two studies specifically evaluated women over 40 years of age44,45, another study evaluated women aged 50 years or older46 and one evaluated women over 65 years of age50. One study did not detail the age of the participants47.
Among the ethnic-racial groups included in this systematic review, the following are mentioned: white, black, brown, Indian, African-American, American, Hispanic, Latino, Asian, Philippine, Korean, Chinese and Caucasian. There was a difference in the prevalence of access between the ethnic-racial groups studied and included in this study.
Franklin30 divided the study into two groups: the 18 to 20-year-old group, which showed white women with the lowest prevalence (19.95%), and the group of women older than 65 years, also with white women with the lowest prevalence in access to the exam (10.64%). In general, among the studies included in this review, the prevalence of access by black women ranged from 4.66%46 to 90.60%36, and among white women it ranged from 14%42 to 89.47%25. Only Barbosa24 brought prevalence data for brown women (75.9%).
Only one study presented prevalence data for Native Americans (2.35%). For Asian women, the prevalence of access ranged from 2.56%46 to 76,333. Among African Americans, the lowest prevalence was 4.66%46, while the highest was reported by Ganesan48 (93%). Among Hispanics it ranged from 21.8%34 to 92.3%36; among Native Americans or Alaska Natives it ranged from 18.23%49 to 81.8%33.
As for association measures, nine studies did not provide data by ethnic-racial groups14,24,25,28,30,39,41,45,49. The highest chances of undergoing Pap smear were among white women (OR=2.49; 95%CI 1.12-4.54) when compared to black women29, and among Hispanic women (OR= 2.08; 95%CI 1.96-2.21) when compared to blacks and non-Hispanic whites51.


Risk of bias assessment

After applying the analysis tool for risk of bias, most studies had a low risk of bias, with only one study classified as having a moderate risk of bias (Bollen et al., 2000)47. Therefore, the articles adequately answered the research question and presented good methodological quality, allowing their results to be used in this study. The result of the analysis for the risk of bias is shown in Figure 2.

Meta-analysis

Of the 29 studies included in this systematic review, only 22 were used in the meta-analysis. Seven articles were excluded22,24-25,34,39-40,43 because, based on the data they presented, it was not possible to identify the number of black women or other ethnic-racial groups among the participants in the sample.
For this study, comparisons were performed that resulted in two meta-analyses. In the first meta-analysis (Figure 3), 19 studies were included and resulted in a sample of 101,654 black women and 604,648 white women. The proportion of Pap smear among black women was 70.8% and among white women it was 82.2%. The summary measure revealed that black women are less likely to undergo the Pap smear when compared to white women (OR: 0.61; 95% CI 0.43-0.86).
In comparing access to Pap smear for black women with other ethnic-racial groups (except white), 20 studies were included and resulted in a sample of 82,445 black women and 102,355 women from other ethnic-racial groups. Note that, for this analysis, there was no significant difference (Figure 5). The summary measure of this analysis (OR=1.39; 95%CI 0.82-2.35) shows that the chance of having a Pap smear between black women and women from other ethnic-racial groups does not have a significant difference.
Both meta-analyses showed high heterogeneity (I2 = 100%) and the Funnel plots (Figure 4 and Figure 6) show that some studies have varied data accuracy and are outside the area covered by the graph.
In an attempt to resolve the high heterogeneity in the first two comparisons, other analyses were performed that grouped studies with similar sample size, data extraction technique, and similar age of participants, however, heterogeneity remained high, and therefore these analyses were not reported in this article.
DISCUSSION

The present study estimated the prevalence of access to the Pap smear by ethnic-racial groups, through a systematic review of cross-sectional studies. The meta-analysis showed that black women are less likely to undergo the Pap smear when compared to white women, however, without significant differences when compared to other ethnic-racial groups.
The lower prevalence of access to Pap smear among black women may reflect higher CC incidence and mortality data among the black population. The overall cervical cancer mortality rate among African-American women is 10.1 deaths per 100,000 women, more than double that for white women. In addition, it is reported that, for black women, follow-up is different and inadequate after screening by Pap smear50.
As for the samples of the included studies, the studies were heterogeneous, however, population-based studies were included that generated representative samples to estimate the prevalence of Pap smear coverage in adult women.
Regarding the locations where the included studies were carried out, most studies were carried out in the USA, while two were carried out in Brazil and one was carried out in Canada. American studies brought greater diversity of ethnic-racial groups among the population studied, and among these, the group of African Americans, blacks, whites and Hispanics gained prominence.
In the United States, with the arrival of cytological screening by the Pap smear, introduced in 1950, invasive cervical cancer showed a reduction in the incidence rate. In 1973, the incidence was 14.2 new cases per 100,000 women, reducing to 7.8 per 100,000 in 199421. Due to the ease of diagnosis in early stages using the Pap smear, there was a significant reduction in CC morbidity and mortality in countries that implemented screening and treatment programs, as in the USA, which allowed a greater range of screening between races and ethnicities.
However, the United States and Brazil have similar histories in relation to the construction and implementation of structural racism37. In this study, racism is evidenced by the lower access to the Pap smear among African-American and black women when compared to white women and women from other ethnic-racial groups22,23,32,36,37,40,44,48.
In Brazil, the mark of centuries of enslavement of the black population still persists. Structural racism reflects on the occupation of different social spaces by white and black people, with unequal distribution of wealth, power and access to goods and services. This structure results in worse social, living and health conditions for the black Brazilian population. The Brazilian studies evaluated in this review corroborate this statement. In the two Brazilian studies evaluated, the lowest prevalence of access to Pap smear occurred for black women, with 33.33%23 and 77.4%22.
According to Ferreira56, the racial problem in Brazil is linked to nature and culture, characterizing a public health and management problem, especially for black women who suffer most from discrimination and social inequality. To reduce disparities in the health service, Brazil created the National Policy for the Comprehensive Health of the Black Population, established by the Ministry of Health, with the aim of helping to combat inequalities in the Unified Health System (SUS) and promoting health of the black population, considering that the country suffers from health inequities, a result of unfair socioeconomic and cultural processes caused by slavery and that feed racism to the present day and corroborates the morbidity and mortality of the black population16.
Although there are public policies to minimize racial disparities, in Brazil there is still the occurrence of discrimination and distinction of people in health services because of their color, culture or origin58. Ferreira56 reports in his study that 23.3% of the black population, when seeking care in the SUS, perceive this discrimination. This discrimination occurs from the restriction of these people's access to services, to the care provided by professionals.
In the United States, in March 2010, the Affordable Care Act (ACA) also known as “Obamacare” was enacted. This initiative aimed to democratize access to health care for more than 20 million vulnerable Americans, 2.8 million of whom are black. Although it was an initiative to reduce inequalities, this isolated action is not enough to solve the historical racial disparity57.
The report published in 2017 by the Center on Poverty (CPI) and Inequality at Stanford University showed for the United States the existence of racial inequality in ten areas evaluated (employment, poverty, use of social security, housing, education, incarceration, health, income, wealth and mobility), and concluded that the differences between whites and non-whites are substantial and the reduction of these inequalities has been occurring very slowly and even failing to occur. Studies show that in health and life expectancy, the difference between blacks and whites is considerable. Among blacks and indigenous people, a much worse performance is observed when compared to whites in most health indicators37.
In Brazil, racism is also reflected in the absence of knowledge production in Health Sciences focused on the specifics of the black population. For Werneck55, the health of black women is not considered a relevant topic in Health Sciences, a statement that is noticeable mainly in the inexpressive scientific production in this area, with a scarcity of studies that address the theme and in the curricular matrices of undergraduate and graduate courses in health. In the present review, only two Brazilian studies were identified that could be included.
Regarding the age group of women included in the studies, most had a sample in the younger age groups, and only two articles brought data for women over 65 years old28,48. According to Oliveira56, women over 59 years of age tend not to adhere to preventive and gynecological exams. This observation may be associated with the end of childbearing age and the beginning of menopause, leading to the abandonment of the routine of performing the Pap smear, which makes this age group more vulnerable to the development of cervical cancer. However, this fact can be justified because most countries do not include this population in screening programs.
Another point that may be linked to not performing the exam would be the lack of knowledge about the importance of screening. According to Gurgel et al57, some women only seek to undergo the examination when they have a gynecological complaint and not for the purpose of prevention. Therefore, it is not enough just to offer the cytopathological examination, it is necessary to sensitize women about its performance, since some do not have the knowledge about the importance of screening.
One study evaluated the national cervical cancer screening program in 12 countries that offered Pap smear through the public health system. It was observed that access to the exam is unequal in these countries, and data indicate that only 51% of the target population has been screened in recent years. In four of the 12 countries studied (Bolivia, Costa Rica, Ecuador and Panama), coverage was less than 35%, even in countries that have established screening programs51.
Carvalho58 reports that the strategies used in prevention programs come up against the lack of information, resulting in late diagnoses and increased mortality. It is necessary to create more effective strategies aimed at health education, especially for populations with lower levels of education and income, worse social indicators, as well as less access to health services, such as the black population57.
The diversity of nomenclatures used in the description of ethnic-racial groups in primary studies limited the performance of other meta-analyses. Another limitation of this study is that it is a systematic review of cross-sectional studies, which used information contained in the participants' memory, and therefore, information bias may occur. The inclusion of only articles of this nature can lead to generalized conclusions since the confounding factors are not always adjusted properly, as they are analyzed at the same time. The lack of identification of confounding factors and the strategies to deal with these factors, mainly in studies carried out in the 1990s and early 2000s, were seen from the assessment of the risk of bias. Despite the limitations, the present review was carried out with rigorous methodology by independent authors and brings together important results to guide health policies.
The high heterogeneity found in the two meta-analyses carried out with all eligible studies and comparing black and white women; and black women and other ethnicities (except white), can be explained by an overestimated measure of association, based on studies with varying sample sizes and studies that included women with access to private services.
Considering this and as a strategy to try to minimize the high heterogeneity obtained, we carried out two other meta-analyses, combining studies with participants with similar sociodemographic characteristics. Therefore, results were obtained with high heterogeneity and high publication bias, and we consider it important to analyze the results with caution.
It should be noted that the findings found in this review can serve as a basis for discussion of the topic, support future studies in order to minimize gaps on the subject and contribute to the formulation and management of public policies appropriate to the needs expressed in social and health indicators of black women. Studies that identify associations between race and the health of the black population are fundamental as thematic fields of research, in order to observe their repercussions, impact and ways of coping.

FINAL CONSIDERATIONS

The data presented in this study showed that race or skin color and ethnicity influence access to the Pap smear. This study showed that black women are less likely to undergo the Pap smear when compared to white women. Race is still an important factor to explain the inequalities of access, coupled with the lack of knowledge about the need to perform the exam and the lack of guidance for its execution; these factors represent a risk for non-adherence to the preventive program. Thus, there is a need to expand screening, develop preventive and effective strategies with a view to these vulnerable groups, in line with the reality of each country. We emphasize here the importance of health education actions, and that these start in primary health care, as an alternative to reduce deaths and burdens on health services.
Therefore, the main contribution of this study to the field of Women's Health and Public Health is to provide a discussion about racial inequities in the health of individuals and to encourage the development of new studies that provide a basis on racism and how it can affect the social and health determinants and conditions. The information contained in this review reinforces the importance of studies aimed at the black population and the need for more research that addresses access to health services for this population, aiming to reduce this gap in science.




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