Barriers to Breast Cancer-Screening Adherence in Vulnerable Populations

Simple Summary Breast cancer is the most prevalent cancer in the world. Early diagnosis can prevent cancer growth and therefore saving lives. Breast cancer screening through periodic mammography has been effective in decreasing mortality. However, adherence to screening does not meet the desired expectations in all population groups. The objective of this review is to identify the barriers that affect adherence to breast cancer–screening programs in an ethnically diverse group of women in order to propose public health measures to increase adherence. Although the dissemination of breast cancer–screening programs is still lacking in most of the vulnerable populations, we observed important favorable changes in those cases in which the population undergoes health education sessions, they are informed about cancer-screening programs or they seek medical attention. Therefore, implementing awareness campaigns focused on these populations should be promoted, as well as working on healthcare professional cultural competence to improve breast cancer–screening adherence worldwide. Abstract Breast cancer screening through periodic mammography has been effective in decreasing mortality and reducing the impact of this disease. However, adherence to screening does not meet the desired expectations from all populations. The main objective of this review is to explore the barriers that affect adherence to breast cancer–screening programs in vulnerable populations according to race and/or ethnicity in order to propose measures to reduce the lack of adherence. We conducted a search of publications in the PubMed Central and Scopus databases. The eligible criteria for the articles were as follows: original quantitative studies appearing in SJR- and/or JCR-indexed journals from 2016 to 2021 in English or Spanish. Most of them present common barriers, such as race/ethnicity (47%), low socioeconomic (35.3%) and educational levels (29.4%), no family history of cancer and being single (29.4%), medical mistrust and a health information gap (23.5%), lack of private health insurance (17.6%) and not having annual health checks (17.6%). The target populations with the lowest adherence were Black, Asian, Hispanic and foreign women. Implementing awareness campaigns focused on these populations should be promoted, as well as working on diversity, cultural acceptance and respect with healthcare workers, in order to improve breast cancer–screening adherence worldwide.


Introduction
Breast cancer is the most prevalent type of cancer worldwide, with 2.2 million cases reported in 2020, making it the leading cause of death among women. Specifically, 685,000 deaths were recorded in 2020 because of this disease, according to the latest data by the World Health Organization (WHO). It is estimated that one in every 12 women will have breast cancer during her lifetime [1], with the highest incidence being in those of 45-65 years old, when hormonal changes occur in the pre-and post menopause period [2]. Although the average survival rate for this cancer at 5 years is 89.2% overall, the stage at which it is diagnosed has a great influence, varying from 98% to 24% survival depending on whether it is diagnosed at stage I or stage IV, respectively [3]. According to these considerations, and assuming the impact that breast cancer has in women's lives, we can affirm that it is a public health problem worldwide. However, breast cancer mortality in high-income countries is decreasing thanks to research and improved treatments, together with the increased implementation of screening and early-diagnosis programs.
In Europe, a breast cancer-screening program consists of performing a mammography every 2 years on the asymptomatic women aged between 50 and 69 years old. Mammography is the most widely available test to diagnose breast cancer in asymptomatic and localized stages. In Spain, it has been shown that this screening modality reduced breast cancer mortality by 9% to 15% [4]. However, despite the proven effectiveness of this intervention, low levels of health literacy and inadequate knowledge about cancer screening, reported among women belonging to vulnerable populations, represent a serious concern. In fact, it is very common for these population groups to do not know what a cancer screening consists of, where accessing it or the possible consequences [5][6][7]. As a result, there are disparities in 5-year survival data of 90% in high-income countries versus 40-66% survival in low-income countries. The highest percentage of age-standardized deaths from breast cancer is in countries from Africa, where up to 50% of deaths from breast cancer occur in women aged under 50 years old [1].
In the United States (US), lack of medical insurance [5][6][7][8][9][10] appears as the main barrier to adherence or follow-up to cancer-screening programs for this disease in women belonging to certain population groups. Medical insurance financially protects the affected women from the multiple expenses that may arise from participation in this program or, even more, from the diagnosis of a suspected breast neoplasia. Some studies show a great lack of information in low-income populations, who admit to not having responded to the offer for cancer screening because they do not know what it consists of and are unaware of the disease risk factors, signs or symptoms [5][6][7][8][9][10]. Advani et al. insist on the need to improve the means of disseminating information to women, especially to those belonging to vulnerable groups [11]. The need for health education, particularly in vulnerable populations, promoting positive attitudes and behavioral changes among women would be effective in achieving better results in cancer-screening programs [10]. Other obstacles that appear in most of the studies are psychological barriers, mobility difficulties, language and cultural barriers, lack of time and/or the prioritization of other health issues [5][6][7][8][9][10][11][12].
The discomfort suffered by women in relation to being treated or examined by a male doctor is reported as a barrier in some studies [6,7,11,13]. Some of these women also reported that they would feel more comfortable being attended by female doctors, as well as an overall lack of confidence in the health system, based on personal experience and negative experiences reported in the media or through their own experiences [7]. In addition, feeling discriminated on the basis of their race and/or ethnicity also increases distrust in health systems. In an interview-based survey, Miller et al. [6] reported that Asian or Black women had been treated worse than white women in the United States (US).
On the other hand, a good doctor-patient relationship (DPR) is considered a positive factor for adherence, as it generates trust, comfort, and compliance with follow-up, which facilitate communication and participation in cancer-screening and early-detection programs [6,7].
The quality of the articles was checked by selecting articles published in journals indexed in the Journal Citation Report (JCR) and/or Scimago Journal & Country Rank (SJR), including the impact factor of the year of publication. The articles were also evaluated Scheme 1. Flowchart of the article-selection process.
The quality of the articles was checked by selecting articles published in journals indexed in the Journal Citation Report (JCR) and/or Scimago Journal & Country Rank (SJR), including the impact factor of the year of publication. The articles were also evaluated using the critical-reading program Critical Appraisal Skills Programme España (CASPe). The questions included in this program analyze the internal validity of the study in terms of methodological adequacy and accuracy. The three main questions that this questionnaire aims to answer are as follows: (i) are the results valid, (ii) what are the results, and (iii) are they applicable in your setting? In total, 17 original publications were included in our research.

Race and/or Ethnicity
A common factor related to a lower level of adherence to breast cancer screening is determined by the race and/or ethnicity of the women participating. There are multiple studies that have analyzed this barrier [15,18,19,21,24], which are reported in the 47% of the total articles researched (Table 1), which correlate race/ethnicity and country of birth as an impediment to the correct coverage of this screening program. The articles compare adherence in non-Hispanic white women with that in women of other ethnicities/races, as represented in Figure 1.

Race and/or Ethnicity
A common factor related to a lower level of adherence to breast cancer screening is determined by the race and/or ethnicity of the women participating. There are multiple studies that have analyzed this barrier [15,18,19,21,24], which are reported in the 47% of the total articles researched (Table 1), which correlate race/ethnicity and country of birth as an impediment to the correct coverage of this screening program. The articles compare adherence in non-Hispanic white women with that in women of other ethnicities/races, as represented in Figure 1. Black race/ethnicity is the one mentioned in the highest number of articles as a barrier to adherence (n = 6), followed by Hispanic (n = 5), Asian (n = 3) and foreign status (n = 2). Black race/ethnicity is the one mentioned in the highest number of articles as a barrier to adherence (n = 6), followed by Hispanic (n = 5), Asian (n = 3) and foreign status (n = 2). If we focus on the data of non-Hispanic white women compared with Black women, the latter show a lower frequency of screening mammography [19], a higher probability of reporting barriers (odds ratio-OR: 1.30) [18] and higher rates of late diagnosis (OR: 1.56) [20]. In addition, the rate of discrimination was five times higher in Black and Hispanic women (11.2% and 11.3%) than in white women (2.2%) [21].

Socioeconomic Level, Lack of Resources and Lack of Private Health Insurance
Low income and a lack of socioeconomic resources [16,18,19,23,24,27] appear as common barriers to adherence in six of the researched studies, which underlines the weight of this factor for adherence to a breast cancer-screening program. Figure 2 shows the main variables related to socioeconomic level that influence adherence to a breast cancer-screening program. If we focus on the data of non-Hispanic white women compared with Black women, the latter show a lower frequency of screening mammography [19], a higher probability of reporting barriers (odds ratio-OR: 1.30) [18] and higher rates of late diagnosis (OR: 1.56) [20]. In addition, the rate of discrimination was five times higher in Black and Hispanic women (11.2% and 11.3%) than in white women (2.2%) [21].

Socioeconomic Level, Lack of Resources and Lack of Private Health Insurance
Low income and a lack of socioeconomic resources [16,18,19,23,24,27] appear as common barriers to adherence in six of the researched studies, which underlines the weight of this factor for adherence to a breast cancer-screening program. Figure 2 shows the main variables related to socioeconomic level that influence adherence to a breast cancerscreening program. Low income is the variable that is present in most of the studies analyzed, and it is closely related to the lack of private health insurance and to unemployment ( Figure 2). Participants with a higher income level showed a 7.1% higher participation rate (relative risk-RR: 1.71, p < 0.001) [27]. Furthermore, when comparing low-income women with those of moderate (OR: 0.69) or high income (OR: 0.85), the latter two are less likely to report barriers to participation in this screening [18]. Another barrier reported by women was the transportation difficulties they experience to reach their corresponding health service facility, where women who have this as a barrier are 26.4% less likely to attend the screening [21].
Another factor common among several of the articles analyzed [21,25,30] is the lack of private health insurance. Having medical insurance (p = 0.0025) is related to greater adherence to mammography [25], a probability three times higher [21] than those women who do not have it, and it is also a factor that favors women's reporting fewer barriers to adherence to a screening program when they are asked about it [24].

Family and Individual Factors
Having a family or personal history of cancer and being married or of older age become protective factors for adherence in women. Having a high level of education; having good local language speaking ability; and knowing about the program are all associated with higher levels of adherence, as shown in Table 3. Low income is the variable that is present in most of the studies analyzed, and it is closely related to the lack of private health insurance and to unemployment ( Figure 2). Participants with a higher income level showed a 7.1% higher participation rate (relative risk-RR: 1.71, p < 0.001) [27]. Furthermore, when comparing low-income women with those of moderate (OR: 0.69) or high income (OR: 0.85), the latter two are less likely to report barriers to participation in this screening [18]. Another barrier reported by women was the transportation difficulties they experience to reach their corresponding health service facility, where women who have this as a barrier are 26.4% less likely to attend the screening [21].
Another factor common among several of the articles analyzed [21,25,30] is the lack of private health insurance. Having medical insurance (p = 0.0025) is related to greater adherence to mammography [25], a probability three times higher [21] than those women who do not have it, and it is also a factor that favors women's reporting fewer barriers to adherence to a screening program when they are asked about it [24].

Family and Individual Factors
Having a family or personal history of cancer and being married or of older age become protective factors for adherence in women. Having a high level of education; having good local language speaking ability; and knowing about the program are all associated with higher levels of adherence, as shown in Table 3.  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been related knowledge and awareness of this health problem and with early detection of f lapses [25,30,31]. Being married or in a couple has also been related to higher ad to these programs [17,25,26,30]. An et al. [26] observed that being married is rel higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.0 et al. [17] concluded that the odds of never having undergone mammography we in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been as with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22, are risk factors for adherence to the screening program. In contrast, high educatio and knowledge of the screening are strongly associated with higher participatio al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or a degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did th had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good speaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about brea screening between women and their confidence and involvement in healthcare s  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been knowledge and awareness of this health problem and with early dete lapses [25,30,31]. Being married or in a couple has also been related to to these programs [17,25,26,30]. An et al. [26] observed that being mar higher level of awareness of breast cancer-screening programs (OR: 29. et al. [17] concluded that the odds of never having undergone mammog in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has als with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level are risk factors for adherence to the screening program. In contrast, high and knowledge of the screening are strongly associated with higher pa al. [31] highlight that women with a school diploma (OR: 13.203, p < degree (OR: 6.750, p < 0.01) showed higher levels of mammography use had heard of the screening program (OR: 36.250, p < 0.01). Finally, havin speaking ability [25] is a determinant factor for better adherence (p = 0. Table 4 shows the main factors related to the levels of information a screening between women and their confidence and involvement in he  Having a personal and/or family history of cancer knowledge and awareness of this health problem and with e lapses [25,30,31]. Being married or in a couple has also been to these programs [17,25,26,30]. An et al. [26] observed that b higher level of awareness of breast cancer-screening program et al. [17] concluded that the odds of never having undergone in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older a with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educatio are risk factors for adherence to the screening program. In con and knowledge of the screening are strongly associated with al. [31] highlight that women with a school diploma (OR: 13 degree (OR: 6.750, p < 0.01) showed higher levels of mammog had heard of the screening program (OR: 36.250, p < 0.01). Fin speaking ability [25] is a determinant factor for better adheren Table 4 shows the main factors related to the levels of info screening between women and their confidence and involvem  Having a personal and/or family history of knowledge and awareness of this health problem a lapses [25,30,31]. Being married or in a couple has a to these programs [17,25,26,30]. An et al. [26] observ higher level of awareness of breast cancer-screening et al. [17] concluded that the odds of never having un in unmarried women (OR: 1.74, 95% CI [1.08-2.82] with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low are risk factors for adherence to the screening progra and knowledge of the screening are strongly associa al. [31] highlight that women with a school diplom degree (OR: 6.750, p < 0.01) showed higher levels of m had heard of the screening program (OR: 36.250, p < speaking ability [25] is a determinant factor for bette Table 4 shows the main factors related to the lev screening between women and their confidence and  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been related knowledge and awareness of this health problem and with early detection of f lapses [25,30,31]. Being married or in a couple has also been related to higher ad to these programs [17,25,26,30]. An et al. [26] observed that being married is rel higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.0 et al. [17] concluded that the odds of never having undergone mammography we in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been as with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22, are risk factors for adherence to the screening program. In contrast, high educatio and knowledge of the screening are strongly associated with higher participatio al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or a degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did th had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good speaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about brea screening between women and their confidence and involvement in healthcare s  Having a personal and/or family history of cancer has been knowledge and awareness of this health problem and with early dete lapses [25,30,31]. Being married or in a couple has also been related to to these programs [17,25,26,30]. An et al. [26] observed that being mar higher level of awareness of breast cancer-screening programs (OR: 29. et al. [17] concluded that the odds of never having undergone mammog in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has als with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level are risk factors for adherence to the screening program. In contrast, high and knowledge of the screening are strongly associated with higher pa al. [31] highlight that women with a school diploma (OR: 13.203, p < degree (OR: 6.750, p < 0.01) showed higher levels of mammography use had heard of the screening program (OR: 36.250, p < 0.01). Finally, havin speaking ability [25] is a determinant factor for better adherence (p = 0. Table 4 shows the main factors related to the levels of information a screening between women and their confidence and involvement in he  Having a personal and/or family history of knowledge and awareness of this health problem a lapses [25,30,31]. Being married or in a couple has a to these programs [17,25,26,30]. An et al. [26] observ higher level of awareness of breast cancer-screening et al. [17] concluded that the odds of never having un in unmarried women (OR: 1.74, 95% CI [1.08-2.82] with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low are risk factors for adherence to the screening progra and knowledge of the screening are strongly associa al. [31] highlight that women with a school diplom degree (OR: 6.750, p < 0.01) showed higher levels of m had heard of the screening program (OR: 36.250, p < speaking ability [25] is a determinant factor for bette Table 4 shows the main factors related to the lev screening between women and their confidence and  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of cancer has been related knowledge and awareness of this health problem and with early detection of f lapses [25,30,31]. Being married or in a couple has also been related to higher ad to these programs [17,25,26,30]. An et al. [26] observed that being married is rel higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.0 et al. [17] concluded that the odds of never having undergone mammography we in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been as with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22, are risk factors for adherence to the screening program. In contrast, high educatio and knowledge of the screening are strongly associated with higher participatio al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or a degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did th had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good speaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about brea screening between women and their confidence and involvement in healthcare s  Having a personal and/or family history of cancer has been knowledge and awareness of this health problem and with early dete lapses [25,30,31]. Being married or in a couple has also been related to to these programs [17,25,26,30]. An et al. [26] observed that being mar higher level of awareness of breast cancer-screening programs (OR: 29. et al. [17] concluded that the odds of never having undergone mammog in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has als with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level are risk factors for adherence to the screening program. In contrast, high and knowledge of the screening are strongly associated with higher pa al. [31] highlight that women with a school diploma (OR: 13.203, p < degree (OR: 6.750, p < 0.01) showed higher levels of mammography use had heard of the screening program (OR: 36.250, p < 0.01). Finally, havin speaking ability [25] is a determinant factor for better adherence (p = 0. Table 4 shows the main factors related to the levels of information a screening between women and their confidence and involvement in he  Having a personal and/or family history of cancer has been knowledge and awareness of this health problem and with early dete lapses [25,30,31]. Being married or in a couple has also been related to to these programs [17,25,26,30]. An et al. [26] observed that being mar higher level of awareness of breast cancer-screening programs (OR: 29. et al. [17] concluded that the odds of never having undergone mammog in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has als with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level are risk factors for adherence to the screening program. In contrast, high and knowledge of the screening are strongly associated with higher pa al. [31] highlight that women with a school diploma (OR: 13.203, p < degree (OR: 6.750, p < 0.01) showed higher levels of mammography use had heard of the screening program (OR: 36.250, p < 0.01). Finally, havin speaking ability [25] is a determinant factor for better adherence (p = 0. Table 4 shows the main factors related to the levels of information a screening between women and their confidence and involvement in he  Having a personal and/or family history of cancer has been knowledge and awareness of this health problem and with early dete lapses [25,30,31]. Being married or in a couple has also been related to to these programs [17,25,26,30]. An et al. [26] observed that being mar higher level of awareness of breast cancer-screening programs (OR: 29. et al. [17] concluded that the odds of never having undergone mammog in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has als with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level are risk factors for adherence to the screening program. In contrast, high and knowledge of the screening are strongly associated with higher pa al. [31] highlight that women with a school diploma (OR: 13.203, p < degree (OR: 6.750, p < 0.01) showed higher levels of mammography use had heard of the screening program (OR: 36.250, p < 0.01). Finally, havin speaking ability [25] is a determinant factor for better adherence (p = 0. Table 4 shows the main factors related to the levels of information a screening between women and their confidence and involvement in he  Having a personal and/or family history of cancer has been related knowledge and awareness of this health problem and with early detection of lapses [25,30,31]. Being married or in a couple has also been related to higher to these programs [17,25,26,30]. An et al. [26] observed that being married is r higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0 et al. [17] concluded that the odds of never having undergone mammography w in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,2 are risk factors for adherence to the screening program. In contrast, high educat and knowledge of the screening are strongly associated with higher participat al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a goo speaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about bre screening between women and their confidence and involvement in healthcare Table 4. Adherence to breast cancer-screening program according to information, conf involvement in health.

= Higher adherence.
Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.

Health Information Gap and Medical Mistrust
A study including 159 ethnically diverse women showed that after educational sessions, a decrease of 5% (p = 0.04) in the lack of knowledge about breast screening was observed [22] (Table 3). Moreover, there was an improvement in the ability to identify the correct starting age for screening after the session (14.8% presession vs. 37.7% postsession) and the frequency of screening (39.3% vs. 90.2). Another practice that seems to be associated with greater participation in screening programs is having an annual health checkup [25,26,28] (Table 4). According to An et al. [26], women are 16 times more likely to participate in the screening program if they undergo this health control (OR: 16.148, p < 0.05). Orji et al. conclude that women who had received an annual health checkup were more likely to participate in breast cancer-screening programs (OR: 5.86, p < 0.05) compared with those who did not receive it [28]. Table 4. Adherence to breast cancer-screening program according to information, confidence and involvement in health.

Authors/Year/Country RHC 1 EBCS 2 MM 3 A 4 AHC 5
Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of knowledge and awareness of this health problem an lapses [25,30,31]. Being married or in a couple has a to these programs [17,25,26,30]. An et al. [26] observ higher level of awareness of breast cancer-screening et al. [17] concluded that the odds of never having un in unmarried women (OR: 1.74, 95% CI [1.08-2.82]) with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low are risk factors for adherence to the screening progra and knowledge of the screening are strongly associa al. [31] highlight that women with a school diplom degree (OR: 6.750, p < 0.01) showed higher levels of m had heard of the screening program (OR: 36.250, p < 0 speaking ability [25] is a determinant factor for bette Table 4 shows the main factors related to the leve screening between women and their confidence and  Having a personal and/or family history of cancer ha knowledge and awareness of this health problem and with ea lapses [25,30,31]. Being married or in a couple has also been re to these programs [17,25,26,30]. An et al. [26] observed that bei higher level of awareness of breast cancer-screening programs ( et al. [17] concluded that the odds of never having undergone m in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low education are risk factors for adherence to the screening program. In contr and knowledge of the screening are strongly associated with h al. [31] highlight that women with a school diploma (OR: 13.2 degree (OR: 6.750, p < 0.01) showed higher levels of mammogra had heard of the screening program (OR: 36.250, p < 0.01). Finall speaking ability [25] is a determinant factor for better adherenc Table 4 shows the main factors related to the levels of inform screening between women and their confidence and involveme  Having a personal and/or family history of knowledge and awareness of this health problem an lapses [25,30,31]. Being married or in a couple has a to these programs [17,25,26,30]. An et al. [26] observ higher level of awareness of breast cancer-screening et al. [17] concluded that the odds of never having un in unmarried women (OR: 1.74, 95% CI [1.08-2.82]) with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low are risk factors for adherence to the screening progra and knowledge of the screening are strongly associa al. [31] highlight that women with a school diplom degree (OR: 6.750, p < 0.01) showed higher levels of m had heard of the screening program (OR: 36.250, p < 0 speaking ability [25] is a determinant factor for bette Table 4 shows the main factors related to the leve screening between women and their confidence and  Having a personal and/or family history of cancer has been related to better knowledge and awareness of this health problem and with early detection of future relapses [25,30,31]. Being married or in a couple has also been related to higher adherence to these programs [17,25,26,30]. An et al. [26] observed that being married is related to a higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). Shon et al. [17] concluded that the odds of never having undergone mammography were higher in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associated with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27,31] are risk factors for adherence to the screening program. In contrast, high educational level and knowledge of the screening are strongly associated with higher participation. Lee et al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or academic degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those who had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Englishspeaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast cancer screening between women and their confidence and involvement in healthcare systems.  Having a personal and/or family history of knowledge and awareness of this health problem an lapses [25,30,31]. Being married or in a couple has a to these programs [17,25,26,30]. An et al. [26] observ higher level of awareness of breast cancer-screening et al. [17] concluded that the odds of never having un in unmarried women (OR: 1.74, 95% CI [1.08-2.82]) with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low are risk factors for adherence to the screening progra and knowledge of the screening are strongly associa al. [31] highlight that women with a school diplom degree (OR: 6.750, p < 0.01) showed higher levels of m had heard of the screening program (OR: 36.250, p < 0 speaking ability [25] is a determinant factor for bette Table 4 shows the main factors related to the leve screening between women and their confidence and  Having a personal and/or family history of cancer ha knowledge and awareness of this health problem and with ea lapses [25,30,31]. Being married or in a couple has also been re to these programs [17,25,26,30]. An et al. [26] observed that bei higher level of awareness of breast cancer-screening programs ( et al. [17] concluded that the odds of never having undergone m in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low education are risk factors for adherence to the screening program. In contr and knowledge of the screening are strongly associated with h al. [31] highlight that women with a school diploma (OR: 13.2 degree (OR: 6.750, p < 0.01) showed higher levels of mammogra had heard of the screening program (OR: 36.250, p < 0.01). Finall speaking ability [25] is a determinant factor for better adherenc Table 4 shows the main factors related to the levels of inform screening between women and their confidence and involveme Having a personal and/or family history of cancer has been related to b knowledge and awareness of this health problem and with early detection of futur lapses [25,30,31]. Being married or in a couple has also been related to higher adher to these programs [17,25,26,30]. An et al. [26] observed that being married is related higher level of awareness of breast cancer-screening programs (OR: 29.152, p < 0.01). S et al. [17] concluded that the odds of never having undergone mammography were hig in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also been associ with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15,19,22,25,27 are risk factors for adherence to the screening program. In contrast, high educational l and knowledge of the screening are strongly associated with higher participation. Le al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.01) or acade degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as did those had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a good Eng speaking ability [25] is a determinant factor for better adherence (p = 0.0021). Table 4 shows the main factors related to the levels of information about breast ca screening between women and their confidence and involvement in healthcare syste  Having a personal and/or family history of cancer has been rel knowledge and awareness of this health problem and with early detectio lapses [25,30,31]. Being married or in a couple has also been related to hig to these programs [17,25,26,30]. An et al. [26] observed that being married higher level of awareness of breast cancer-screening programs (OR: 29.152, et al. [17] concluded that the odds of never having undergone mammograp in unmarried women (OR: 1.74, 95% CI [1.08-2.82]). Older age has also b with higher participation rates [31].

Health Information Gap and Medical Mistrust
However, the lack of health education and low educational level [15 are risk factors for adherence to the screening program. In contrast, high ed and knowledge of the screening are strongly associated with higher partic al. [31] highlight that women with a school diploma (OR: 13.203, p < 0.0 degree (OR: 6.750, p < 0.01) showed higher levels of mammography use, as had heard of the screening program (OR: 36.250, p < 0.01). Finally, having a speaking ability [25] is a determinant factor for better adherence (p = 0.0021 Table 4 shows the main factors related to the levels of information abou screening between women and their confidence and involvement in health It is demonstrated that a good doctor-patient relationship helps to increase levels of adherence [30] (OR: 1.485), which encourages healthcare providers to recommend patients participate in screening programs (p = 0.0027) [25]. In a study carried out in migrant women living in the US, longer length of stay (p < 0.001) and acculturation (p = 0.002) have been related to higher levels of adherence [29]. They also showed that higher levels of medical distrust were associated with lower participation in screening [29], although this factor was found to be not significantly associated with greater participation in another study [24]. However, acculturation also seems to be a protective factor according to the study by An et al. [26].

Discussion
As Krieger demonstrates, the exacerbation of inequities during the COVID-19 pandemic owing to structural racism in the US [32]; these results agree with the existing cultural barriers due to racism and injustices in healthcare systems across the world today. Johnson-Agbakwu et al. showed the inequities in mortality between white and Black populations [33] and how these have been exacerbated by the recent COVID-19 pandemic, seeking to propose measures to resolve this situation. Also in Italy, a study on the epidemiological characteristics of COVID-19 cases in non-Italian nationals confirmed that compared with Italians, undocumented foreigners have a greater risk of severe clinical outcomes [34]. Along the same lines, Ponce-Blandón et al. analyzed the complex reality faced by migrants who cross the Strait of Gibraltar for a better life [35], identifying various cultural barriers encountered by health professionals who were unable to provide culturally appropriate help when they were caring for people of different races/ethnicities: factors such as language, religious beliefs, cultural habits and prejudices, among others [36]. These factors could be the reason for lower participation in and a greater lack of knowledge of population-based health and early-detection programs. Molina-Barceló et al. [37] identified the profile of women who participated to a lesser extent in breast cancer screening in Spain: young, migrant and/or of nonwhite race and/or ethnicity.
The results on low incomes are consistent with other research that has studied barriers to accessing health services in general, not only in relation to adherence to screening programs. Zhou et al. [38] and Shahar et al. [39] studied Chinese and Malaysian populations and demonstrated a direct relationship between health variables and economic resources, which are interrelated, creating the so-called Hortwiz circle [40]: poverty-unhealthy-low income-poverty, suggesting that public health strategies should be directed at vulnerable populations. Lund et al. [41] found a significant relationship between poverty levels and mental illnesses owing to social exclusion, stress and barriers to accessing healthcare, demonstrating the influence of a lack of economic resources on physical, mental and social health across the world. Some studies show that a large population in the US are still without health insurance and that this population tends to be those with fewer resources [42]. Despite having private health insurance, the barriers to accessing basic health programs continue to be greater among those with fewer resources [43]. According to Serral et al. [44], the Spanish women who had higher participation rates in breast cancer screening were those (i) between 60 and 69 years, (ii) with high incomes, (iii) with private health insurance and (iv) born in a country with a Human Development Index (HDI) score over 0.8, which supports the results obtained in our study.
We have also demonstrated the importance of educating the population and informing women about breast cancer-screening programs. In fact, other studies have highlighted the importance of implementing health education programs in schools, with the aim of training children to understand health information from an early age [45]. Other studies have also shown the multiple positive effects of the implementation of annual health checkups and strongly recommend them to improve lifestyle habits [46]. Although population screening programs are intended to promote health equity, it cannot be denied that there are still inequities, with a tendency to lower participation in those social groups who are vulnerable, determined by all the barriers discussed above. For example, the participation rates in cancer screenings by age in the US, where 88% of the articles in our research come from, do not meet the required standards [47]. Therefore, boosting adherence in these vulnerable populations is a necessary global action.
Given the main barriers encountered in this study, some measures are proposed that aim to improve screening coverage in vulnerable populations. The implementation of awareness programs for migrant and/or nonwhite women could be useful to raise their awareness of the importance of breast cancer screening. To be accessible to them, the campaigns could be implemented in places related to their everyday lives, such as schools, the media and/or supermarkets. An example of this was conducted by Alkhasawneh et al. [48], who implemented a breast cancer education program for Arab women to increase knowledge of the subject and participation in screenings, and the results were clearly positive. Serral et al. [44] invited us to inform the population, focusing on women from the most vulnerable groups, of the benefits and risks of participating in a breast cancer-screening program, so that women can make informed decisions.
Moreover, work should be conducted on the implementation of annual health checkups, with the intention of recruiting women who are susceptible to neglecting screening. In this regard, we should work with health professionals because they are the key actors to enrolling patients who meet the requirements-informing and reminding patients of the importance of participating in screening programs. In addition, efforts should be aimed to avoid the health information gap and mistrust in healthcare systems in order to overcome the inequities that exacerbate the lack of adherence. Ponce-Blandón et al. [35] identified some difficulties to managing cultural differences from healthcare workers' perspectives and proposed measures to educate these professionals on the values of diversity and respect. It is crucial to guarantee medical trust in healthcare professionals and in healthcare systems in order to improve doctor-patient relationships, increasing satisfaction and the adherence to screening, with a particular focus on the diversity and cultural integration of all people.
Most of the studies were descriptive observational studies (95%), which gives a low level of evidence to the results; only two experimental studies were included (5%). However, given that the objective of this research was not to evaluate a health intervention but rather to analyze the factors and barriers that influence the lack of adherence to breast cancerscreening programs, we expected to find more descriptive studies than other types. Another limitation was that most of the publications analyzed were carried out in the US (88%); only two of the 17 were conducted outside of the US, one in Asia and one in Australia. For this reason, we encourage European and African researchers, as well as professionals across the world, to focus their research on this vital topic to gain health equity, which is included as an objective in the 2030 Agenda for Sustainable Development (Goal 3: ensure healthy lives and promote well-being for all at all ages).

Conclusions
Multiple barriers have been found to affect adherence to breast cancer-screening programs. The target populations with the lowest adherence in our study were Black, Asian, Hispanic and foreign women. Those with barriers are detailed in Scheme 2. A lack of knowledge of these screening programs and medical mistrust in healthcare systems owing to cultural differences also exacerbate this health issue. In general, the adoption and dissemination of breast cancer-screening programs is still deficient in a large part of vulnerable populations, where the influential barriers are associated with race and/or ethnicity (47% of the cases) and low socioeconomic level (35.3%). However, we observed important favorable changes in those cases in which the population undergoes health educational sessions, is informed about the screening or is recommended by health professionals to attend. Therefore, we propose interventions to avoid these social disparities and avoid the low levels of adherence in vulnerable populations, which are described in Scheme 2. We should mention that more in-depth studies on this health problem will be very useful to continue improving participation in and relieving the difficulties hindering women's adherence to these early-detection programs.
rather to analyze the factors and barriers that influence the lack of adherence to breast cancer-screening programs, we expected to find more descriptive studies than other types. Another limitation was that most of the publications analyzed were carried out in the US (88%); only two of the 17 were conducted outside of the US, one in Asia and one in Australia. For this reason, we encourage European and African researchers, as well as professionals across the world, to focus their research on this vital topic to gain health equity, which is included as an objective in the 2030 Agenda for Sustainable Development (Goal 3: ensure healthy lives and promote well-being for all at all ages).

Conclusions
Multiple barriers have been found to affect adherence to breast cancer-screening programs. The target populations with the lowest adherence in our study were Black, Asian, Hispanic and foreign women. Those with barriers are detailed in Scheme 2. A lack of knowledge of these screening programs and medical mistrust in healthcare systems owing to cultural differences also exacerbate this health issue. In general, the adoption and dissemination of breast cancer-screening programs is still deficient in a large part of vulnerable populations, where the influential barriers are associated with race and/or ethnicity (47% of the cases) and low socioeconomic level (35.3%). However, we observed important favorable changes in those cases in which the population undergoes health educational sessions, is informed about the screening or is recommended by health professionals to attend. Therefore, we propose interventions to avoid these social disparities and avoid the low levels of adherence in vulnerable populations, which are described in Scheme 2. We should mention that more in-depth studies on this health problem will be very useful to continue improving participation in and relieving the difficulties hindering women's adherence to these early-detection programs.