Factors related to mammography adherence among women in Brazil: A scoping review

Abstract Aim To explore and synthesize the literature on factors related to mammography screening adherence among women in Brazil. Design A scoping review. Methods We searched 11 databases for studies published between 2006–January 2020. All identified articles were screened, and data were extracted from eligible studies. We used the UK Government Social Research Service weight of evidence appraisal tool to appraise the quality of the included study. Results From a total of 1,384 identified articles, 22 were retained. All included studies used quantitative, non‐experimental methods and all but two studies used cross‐sectional data. Quality of evidence varied across studies. We identified 41 factors that were investigated across the set of studies. Demographic and socio‐economic factors were the most commonly investigated, with older age, urban residence, living in the southeast of Brazil, higher level of education, higher income and private health insurance most consistently associated with mammography adherence.


| INTRODUC TI ON
Worldwide, breast cancer is the most common malignant neoplasm among women, accounting for almost one in four cases of cancer and the greatest number of cancer-related deaths in less developed countries (Bray et al., 2018). The incidence of breast cancer is rising in low-and middle-income countries, as is the mortality rate, such that 62% of breast cancer deaths worldwide now occur in developing countries (Torre et al., 2017). The burden of breast cancer in Brazil, the largest country in South America, is similarly high. Breast cancer is the most prevalent cancer in Brazilian women, with prevalence rates ranging from 38.74/100,000 in the Northeast region-74.30/100,000 in the Southeast region of the country (Brazil, 2016). Moreover, breast cancer mortality is much higher in Brazil than in most high-income countries, with mortality rising from 10.83/100,000 in 2002 (Carioli et al., 2018)-14.5/100,000 in 2018 (International Agency for Research on Cancer, 2020). This contrasts with most European and North American countries where mortality has declined, largely attributed to treatment advances as well as early cancer detection via mammography screening (Wild et al., 2020).
Mammography screening is considered the gold standard for the early detection of breast cancer because smaller lesions can be identified and treatment initiated earlier in the disease trajectory, thereby improving treatment effectiveness (Silva & Hortale, 2012).
The Brazilian Ministry of Health established guidelines in 2004, which were updated in 2015 by the Brazilian National Institute of Cancer (Brazil, 2015), to now recommend that all women aged 50-69 years undergo mammography screening every 2 years. Women aged 40-49 years are advised to undergo mammography screening only if they are deemed to be at high risk for breast cancer or if their annual clinical breast examination is abnormal. Specific legislation to ensure access to mammography was enacted in 2008. Despite the recommendation and legislation, Brazilian data indicate that overall, many women are not undergoing mammography screening, particularly those aged 50-60 years. Furthermore, Brazilian research suggests that many women are diagnosed at an advanced stage, resulting in reduced likelihood of cure as well as more costly treatments (Lee et al., 2012).
Women's non-adherence to mammography screening has been the focus of research worldwide, particularly in western countries.
Factors found to be associated with mammography non-adherence include lower educational attainment, lower individual and community socio-economic status, non-White ethnicity and increased presence of co-morbid disease (Hubbard et al., 2016). Recent reviews also suggest that prior breast and cervical cancer screening behaviour predicts mammography use, as does access to a physician, a physician recommendation, care by an obstetrician/gynaecologist and having health insurance and a regular source of health care (Madadi, 2014;Sarma, 2015).
Social factors, such as a lack of social support and cultural norms of privacy and modesty, may also influence women's screening behaviour (Sarma, 2015). Though this research provides insight, findings might have limited applicability to the unique Brazilian context. Various Brazilian studies have investigated mammography adherence ; however, there has been no knowledge synthesis that identifies the factors related to adherence across studies. An overall understanding of the factors that influence Brazilian women's use of mammography is foundational to identifying gaps in the literature, so as to inform future research endeavours as well as the development of effective health services that can create the conditions that promote adherence. Accordingly, the purpose of this scoping review was to identify the factors related to mammography screening adherence among women in Brazil.

| Design
A scoping review was deemed appropriate because this type of review is used to address an exploratory question with the aim of mapping the key concepts, types of evidence and gaps in research related to a defined area (Colquhoun et al., 2014). We employed the methodological framework outlined by Arksey and O'Malley (2005) and enhanced by Levac and colleagues (2010), which included the stages of: (a) identifying the research question; (b) identifying relevant studies; (c) study selection; (d) charting the data; and (e) collating, summarizing and reporting the results. We did not conduct the optional stage of consultation with stakeholders (Arksey & O'Malley, 2005;Colquhoun et al., 2014;Levac et al., 2010 (Brazil, 2015). All searches were run consecutively on the same day.

| Study selection
Studies included in this review (a) were published in English, Spanish or Portuguese; (b) were published in a peer review journal; (c) had a study sample that included women in Brazil; (d) investigated factors related to mammography screening; (e) measured mammography screening adherence among individuals or groups; (f) included the outcome of mammography screening as self-reported or collected via a health service database; and (g) used a comparative research design. We excluded studies that were published in the grey literature in the form of reports, book chapters, conference papers or theses.
Two independent reviewers (CM and AM) performed the initial title and abstract screening of the articles and the articles that did not meet the inclusion criteria were excluded. The full text of the remaining articles were retrieved and screened according to the inclusion criteria. Where there was ambiguity, FH and SD assessed the article to determine the final set of studies to be included in this review. We also reviewed the reference lists of relevant manuscripts, but no additional publications were included.

| Charting the data: data extraction
We adapted the EPPI-Centre systematic reviews instrument (Newman & Elbourne, 2004) to extract data from the included studies based on the purpose of our review. Using our data extraction template, we retrieved the following information from each study: author, publication year, language, study design, setting and sample, mammography adherence (%), factors related to mammography adherence and non-significant factors examined.

| Collating and summarizing: data analysis and quality assessment
We divided the selected studies into three groups according to the outcome used in the included studies: (a) adherence to mammography within 2 years (as per national recommendations); (b) never versus ever had mammography; or (c) adherence to mammography at other time points. We then identified all the factors evaluated in the studies and grouped these factors into the following: demographic, socio-economic, health service use, medical and health history and previous cancer screening. For each study, we identified which factors were found to be significantly related to mammography adherence and whether these findings were obtained through bivariate or multivariate analysis.
Although study quality was not a criterion for inclusion in our review, we used the UK Government Social Research Service (GSRS) weight of evidence appraisal tool (Gough, 2007) to appraise the quality of the included studies. The GSRS appraisal tool assesses the trustworthiness of the findings, the appropriateness of the design and analysis and the relevance of the focus of the study for addressing the questions of the review. Each of the three sections was scored separately and then summed to yield assessments of low-, medium-or high-quality evidence. Two reviewers (CM and AM) independently assessed each article. English-language articles were also assessed by FH and VSD. When there were differences in scores, the reviewers discussed the rationale for their scores and came to agreement.

| Ethics
Ethical approval was not required for this study.

| Identification and selection of studies
We identified a total of 1,384 articles from our initial search of the 11 databases. We then excluded 92 duplicates and 1,288 articles that did not meet the inclusion criteria during the title and abstract screening. We reviewed the full text of 143 articles to determine whether they met the inclusion criteria. At the end of the identification and selection process, a final sample of 22 studies met all inclusion criteria and were retained for data extraction (Figure 1).

| Characteristics of studies
The publication dates of the 22 studies included in this scoping review ranged from 2006-2019, with 50% of the studies published after 2014. All 22 studies used quantitative, non-experimental methods, wherein 2 were longitudinal (Caleffi et al., 2010;Marchi & Gurgel, 2010) and the remainder were cross-sectional. All studies assessed the relationship of various factors to mammography adherence. Data were collected from pre-existing Brazilian National Health surveys (9 studies), women in a health unit/centre (7 studies), women via a home interview (5 studies) and women via telephone (1 study). Eleven studies assessed adherence to mammography within 2 years (as per national recommendations), two of which divided their sample into 2 age groups and conducted separate analyses and one of which divided their sample into two different years.
Six studies assessed never versus ever had mammography, one of which divided their sample into two different years, while another into 2 different regions of Brazil and conducted separate analyses.
The five studies that assessed other frequencies of mammography included one study that analysed the data from two different age groups separately. Thus, among the 22 studies, there were 27 separate investigations.
Study characteristics, including the weight of evidence scores, are summarized in Table 1. Of the 27 investigations, their weight of evidence scores was distributed as follows: 4 high; 17 medium; and 6 low. Demographic and socio-economic factors were the most commonly investigated and within these categories, age, race, marital status, education, income and health insurance were the most frequently assessed. Older age was related to mammography adherence in all but five of the 18 investigations that included age (6 bivariate, 12 multivariate analyses). The study by Buranello et al., (2018) was the only study to find declining rates of adherence among older participants after controlling for other factors. Race was not found to be related to mammography adherence, except in three of the 13 investigations (3 bivariate, 10 multivariate). Only six of the 14 investigations that examined the association between marital status and mammography adherence found significant results, with higher rates of adherence among women living with partners (4 bivariate, 10 multivariate). Higher education was found to be associated with adherence in 13 of the 18 investigations that included education (4 bivariate, 14 multivariate); the other five investigations yielded non-significant results.

| Demographic and socio-economic factors
Similarly, higher income (18 investigations) and health insurance (16 investigations) were consistently associated with adherence.
The exceptions were the three and two studies, for income and health insurance, respectively, that found non-significant results.
Though less commonly assessed, when urban/rural household location (8 investigations) and region (6 investigations) were included in multivariate analysis, urban residence and living in the southeast of Brazil were significantly related to higher levels of mammography adherence.

| Health service use factors
A previous medical appointment was significantly related to mammography adherence in all seven investigations where this factor was included, despite variation in time frame ranging from 15 days (Novaes et al., 2006)-12 months (Lima-Costa & Matos, 2007Marchi & Gurgel, 2010;Oliveira et al., 2011;Souza et al., 2017).

| Medical and health history
Eighteen medical and health history factors were examined.
Self-reported health was the most commonly investigated, with a positive perception of health found to be associated with   mammography adherence in three of the six investigations (Lima-Costa & Matos, 2007;Novaes et al., 2006;Rodrigues et al., 2015).

TA B L E 2 Summary of factors associated with mammography adherence
Thirteen of the other medical and health history factors were assessed in only one or two investigations. Of those that were investigated more than twice, mixed results were found for menopause (3 investigations), personal history of cancer (4 investigations), family history of cancer (3 investigations) and tobacco use (3 investigations). No association was found for difficulties in performing daily activities, chronic disease, benign breast lumps, personal history of breast cancer, knowing someone with a history of breast cancer, current use of HRT or body mass index, although each of these was assessed in only 1 or 2 investigations.

| Previous cancer screening
Seven factors related to cancer screening were investigated.
Although each factor was only included in one or two investigations, all were significant when included, with the exception of breast selfexamination in one investigation (Caleffi et al., 2010).

| D ISCUSS I ON
To our knowledge, this is the first knowledge synthesis of the published literature to identify factors related to mammography adherence among women in Brazil. We located 22 studies, representing 27 separate investigations, wherein adherence was measured by: (a) whether women followed national recommendations (11 studies); (b) ever had a mammogram (6 studies); or (c) had a mammogram within another time frames (5 studies). Only two studies were longitudinal, with the remainder using a cross-sectional design with its risk of recall bias.
Demographic and socio-economic factors were the most commonly investigated, with older age, urban residence, living in the southeast of Brazil, higher level of education, higher income and private health insurance most consistently associated with mammography adherence. The association with previous health service use, medical and health history and previous cancer screening practices was investigated less often and with mixed results. One exception was the consistently positive relationship found between a recent previous medical appointment and mammography adherence in seven investigations.
Mammography adherence ranged widely across investigations, but the study samples varied from high risk samples (Buranello et al., 2018) to nationally representative samples (e.g. Viacava et al., 2019). However, the wide range in mammography adherence rates across studies also raises questions about differential access to mammography screening. There are large regional variations in health and health services in Brazil, including access to primary and speciality care (Albuquerque et al., 2017). Brazil (Shin et al., 2018). The relationships between socio-economic status and mammography update may be due to differences in access to information or perceived need, as well as economic barriers. For example, a study by Donnelly and colleagues (2015) of breast cancer screening in Qatar found that higher education and higher income were not only the strongest predictors of mammogram screening, but were also strongly associated with greater awareness of the national screening guidelines. Similarly, a recent study by de Oliveira et al., (2018) of women living in a rural area of Brazil found that both income and education levels were associated with knowledge and attitudes to breast cancer screening. Thus, even though women in Brazil have access to publicly funded healthcare services including mammography screening, there may still be barriers related to socio-economic status.
Other barriers related to socio-economic status may include access to transportation or the opportunity to leave work for a medical appointment (Shin et al., 2018). For example, a study of barriers to the use of breast cancer screening services in Nigeria found that 66.5% of the women reported transportation difficulties (Okoronkwo et al., 2015).
Brazilian researchers have also commented on the relationship between income and women's ability to manage their own time (Melo et al., 2016). Finally, it should be noted that although several studies showed significant results for race in bivariate analyses, the relationships generally became non-significant in multivariate analyses (e.g. Buranello et al., 2018;Oliveira et al., 2011;Theme Filha et al., 2016), indicating that the socio-economic conditions associated with race are the primary contributor to non-adherence. This reinforces the importance of multivariate analysis, controlling for other important factors.
Another reason for the importance of socio-economic status may be that there is competition for limited screening resources when most women are dependent on publicly provided health services (Vieira, 2015). This may help explain the importance of private insurance as a predictor of mammogram uptake in Brazil. Also, as discussed above, health services do vary by region of Brazil and several studies using multivariate analyses have shown that region is predictive of mammography uptake, even after controlling for the individual's socio-economic status. Until 2000, the Standardized World Income Inequality Database showed that Brazil ranked as one of the most unequal countries in the world (Solt, 2016). Although there have been improvements, Brazil still shows marked regional differences and inequalities in income and other social conditions (Melo et al., 2016).
The findings of our scoping review suggest that further research is required to tease apart the ways socio-economic factors influence adherence to mammography screening guidelines, including studies that move beyond investigations at the individual level to investigate the mechanisms by which structural barriers influence mammography uptake. For example, in addition to assessing the overall availability of health services, it is also important to account for the perceived quality of services. Studies have shown that there is a need to strengthen the primary healthcare centres in Brazil, not just in terms of the physical condition of the facilities, but also with respect to the quality of care.
For example, Fausto and colleagues (2017)  Future research should also consider factors that were not investigated in the studies in this review but may be influential. For example, the success of cancer screening programmes is at least partially dependent on individual and public health education to raise awareness about cancer and the benefits of early detection (Sivaram et al., 2018).  (Padela et al., 2015;Sousa, 2014).

| Quality of evidence
The quality of evidence varied across studies. Most of the 27 investigations were rated as medium quality, with only six being rated as low quality. Most studies drew on data from national or regional health surveys that were designed for a broader purpose. All but two of the investigations used cross-sectional designs with the potential for recall bias. Eight of the investigations were also weakened by the sole use of bivariate analysis and none reported effect sizes.
Although a lack of detail in many studies created challenges for assessing the quality of the evidence, our assessment suggests that the set of studies included in this review provide an adequate but preliminary evidence base for informing policy and practice. There is a need for more primary studies with stronger designs, more reliable outcome measures and more sophisticated analytic techniques.

| Strengths and limitations
The major strength of this scoping review was the breadth of our

| Implications for nursing and health policy
Even though mammography screening is a publicly funded healthcare service in Brazil, our results suggest that there may still be barriers related to socio-economic status, such as a lack of transportation or the opportunity to leave work for a medical appointment. Public health services should consider strategies to make mammography screening more accessible, such as a more convenient location and scheduling of mammography clinics. Diverse messaging may also be useful in reaching various subpopulations. However, the wide range in mammography adherence rates across regions of the country also raises larger policy questions about structural factors and differential access to mammography screening.

| CON CLUS ION
This review synthesized the literature on factors related to mammography adherence among women in Brazil. We identified several predictors of adherence/non-adherence: age, urban/rural household location, region of the country, income, health insurance and having a recent medical appointment. Our results reinforce the findings of studies in other countries regarding the importance of socioeconomic factors at the individual level for mammography uptake (Akinyemiju, 2012), but also suggest a need to examine structural factors that may have an impact on access to screening. Moving forward, it will also be important to move beyond prediction to understanding, for example, using structural equation modelling and qualitative research methods.

ACK N OWLED G EM ENT
We thank Altamira Mendonça and Angelita Henrique for assisting with the selection of articles for this study. We also acknowledge that C. B. Moreira and V. S. Dahinten share first authorship of this manuscript.

CO N FLI C T O F I NTE R E S T
No conflict of interest has been declared by the authors.

AUTH O R S CO NTR I B UTI O N S
Study design: CBM, VSD, AFH, AFCF. Data collection: CBM.

E TH I C A L A PPROVA L
This scoping review drew on published studies only, and did not involve human participants; therefore, it did not require ethical review.

DATA AVA I L A B I L I T Y S TAT E M E N T
All data generated or analysed during this study are included in this published article (and its supplementary information File S1).