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Abstract

Background:

Breast self-examination (BSE) was previously recommended to help early-stage breast cancer detection to improve prognosis. However, BSE is not recommended in the United States anymore due to the findings that it fails to significantly decrease mortality while increasing biopsy cases, causing unnecessary harm. Nonetheless, international researchers have continued to investigate the benefits of BSE in medically underserved regions. These studies raise the possibility that BSE could be beneficial in rural America, where people face higher mortality from chronic diseases compared to the general population.

Objectives:

Determine if BSE has benefits for medically underserved populations to inform a potential reevaluation of breast cancer screening recommendations.

Design:

Systematic review.

Data Sources and Methods:

A systematic review was conducted using a set of terms to identify articles on breast cancer survival and BSE in rural and/or underserved populations within the past 10 years. The search yielded over 200 articles across 3 databases (PubMed, CINAHL, and SCOPUS), and they were further screened to include studies that show rural populations performing BSE, effects of BSE in breast cancer diagnosis and/or mortality of breast cancer patients, factors contributing to the efficacy of BSE, factors that affect women’s willingness to perform BSE, and effects of BSE on breast cancer awareness/behaviors to seek further screening.

Results:

The final synthesis from 12 articles suggests that BSE is associated with early breast cancer detection (4/12), increased accessibility to breast cancer screening (2/12), and positively influence women to seek further breast cancer screening in rural populations (3/12). It also identifies a potential need for improved education on breast cancer and screening, including BSE practices, to promote early breast cancer detection (3/12).

Conclusion:

The reevaluation of the current recommendations to determine if exceptions should be made to specific populations would be helpful in addressing late detection and poor prognosis in medically underserved populations.

Keywords

breast cancer breast self-examination rural health women’s health breast cancer screening

Introduction

Breast cancer is the most common non-skin cancer in women in the United States. About 264,000 cases of breast cancer are diagnosed each year and result in over 42,000 deaths annually, making breast cancer the fourth leading cause of death due to cancer.¹ Breast cancer that is localized, has spread regionally, or has spread distantly has a 5-year survival rate of 99%, 86%, and 30%, respectively.² With prognosis worsening when breast cancer is caught at later stages, early detection is crucial for improving patient outcomes.³

Before 1980, the American Cancer Society (ACS) recommended monthly breast self-examination (BSE) starting as early as high school years. In 1983, these guidelines were adjusted as a recommendation for women over 20 years old.⁴ Since 2003, the ACS and several other national organizations no longer recommend universal BSEs, stating that women should instead be informed about the benefits and risks of the screening tools as well as reporting any new symptoms to their healthcare provider.⁴

These recommendations from the ACS were made following a systematic review of randomized control trials in Cochrane Library and Medline.⁵ The study aimed to determine if regular BSE reduces breast cancer morbidity and mortality by comparing BSE with no intervention. The data showed no difference in mortality between the 2 groups and found that the experimental (BSE) group had almost double the amount of breast biopsies with 3406 biopsies compared to 1856 in the control (no intervention) group.⁵ Given these results and the robust sample size, the ACS decided that physicians should no longer recommend BSEs to all women over 20 years old as they had been previously.

While BSE is no longer recommended in the United States, other countries, particularly developing or underdeveloped countries, have continued to study the role of BSE in breast cancer patient outcomes. These studies suggest that BSE may be beneficial in medically underserved populations. This article works to answer the question of whether BSE is associated with benefits including increased breast cancer detection rates, increased breast cancer screening, and decreased mortality, making BSE applicable to rural and medically underserved populations.

Methods

To analyze important trends in performance of BSE by women in underdeveloped and developing countries, initial articles for review were collected via a parallel search of three databases: PubMed (n = 167), SCOPUS (n = 197), and CINAHL (n = 67). Polyglot Systematic Review Accelerator was used to translate the initial PubMed query into search terms for SCOPUS and CINAHL.⁶ The following search terms were used to identify specific studies published between 2010 and 2023.

PubMed search (accessed August 30, 2023)

(“Breast Self-Examination”[Mesh] OR “breast self exam*”[tiab] OR “breast self-exam*”[tiab] OR “self breast exam*”[tiab] OR “self-breast exam*”[tiab] OR “BSE”[tiab] OR ((“self exam*”[tiab] OR “self-exam*”[tiab]) AND breast*[tiab]) OR (“self”[tiab] AND “exam*”[tiab] AND “breast*”[tiab])) AND (“Rural Population”[Mesh] OR “Rural Health”[Mesh] OR “Rural Health Services”[Mesh] OR “Hospitals, Rural”[Mesh] OR “rural*”[tiab])

CINAHL search (accessed August 30, 2023)

((MH “Breast Self-Examination”) OR (TI “breast self exam*” OR AB “breast self exam*”) OR (TI “breast self-exam*” OR AB “breast self-exam*”) OR (TI “self breast exam*” OR AB “self breast exam*”) OR (TI “self-breast exam*” OR AB “self-breast exam*”) OR (TI BSE OR AB BSE) OR (((TI “self exam*” OR AB “self exam*”) OR (TI self-exam* OR AB self-exam*)) AND (TI breast* OR AB breast*)) OR ((TI self OR AB self) AND (MH “Breast Examination” OR (TI exam* OR AB exam*)) AND (TI breast* OR AB breast*))) AND ((MH “Rural Population”) OR (MH “Rural Health”) OR (MH “Rural Health Services”) OR (MH “Hospitals, Rural”) OR (MH “Rural Health Centers”) OR (MH “Rural Areas”) OR (TI rural* OR AB rural*))

SCOPUS search (accessed August 30, 2023)

(INDEXTERMS(“Breast Self-Examination”) OR TITLE-ABS(“breast self exam*”) OR TITLE-ABS(“breast self-exam*”) OR TITLE-ABS(“self breast exam*”) OR TITLE-ABS(“self-breast exam*”) OR TITLE-ABS(BSE) OR ((TITLE-ABS(“self exam*”) OR TITLE-ABS(self-exam*)) AND TITLE-ABS(breast*)) OR (TITLE-ABS(self) AND TITLE-ABS(exam*) AND TITLE-ABS(breast*))) AND (INDEXTERMS(“Rural Population”) OR INDEXTERMS(“Rural Health”) OR INDEXTERMS(“Rural Health Services”) OR INDEXTERMS(“Hospitals, Rural”) OR INDEXTERMS(“Rural Health Centers”) OR INDEXTERMS(“Rural Areas”) OR TITLE-ABS(rural*))

The eligibility criteria included studies on BSE that mention one or more of the following: rural or medically underserved populations, comparison of grade or stage at time of diagnosis for subjects who performed BSE versus subjects who did not perform BSE, factors affecting how well subjects perform BSE, comparison of breast cancer mortality between subjects who performed versus did not perform BSE, factors that make clinical breast examination (CBE) and/or mammography more difficult to obtain than BSE, and assessment of whether BSE could lead to further breast cancer detection methods such as CBE or mammography. Studies that were not original research publications (e.g., systematic reviews and posters), studies that were not about BSE, and studies that only looked at the reasons why women either perform or do not perform BSE (including studies that just looked at demographics) were excluded to screen out studies that did not include relevant data for the analysis.

After deduplicating the dataset (articles from the database searches) using Zotero, an initial screen of the titles and abstracts was conducted through Rayyan using the inclusion and exclusion criteria described above. Three screeners were assigned to each abstract, and to decrease bias, each screener was blinded from others’ decisions and worked independently.

Once the articles were screened based on their titles and abstracts, they were exported to Microsoft Excel. The articles were assessed in their entirety based on the inclusion and exclusion criteria described above. Studies that considered breast cancer with other types of cancer (e.g., breast cancer and cervical cancer) were excluded to avoid the potential confounding question of if the health benefits identified in these studies could be explained by screening of other cancer types, which would both be outside the scope of this project and make it difficult to determine if these benefits are actually associated with BSE practice. Two reviewers were assigned to independently screen each article. Each reviewer was required to provide their reasoning for including or excluding any given article. For the articles that met the inclusion criteria, data regarding study design, population (geographical region, sample size, characteristics of participants, etc.), intervention, and outcome (group means, frequencies, variables controlled for, significant differences, odds ratios, etc.) were extracted for the review. For articles that did not meet the inclusion criteria or met the exclusion criteria, those reasons were also outlined in the Excel sheet. If the two reviewers were in disagreement, a third reviewer was assigned to break the tie. The review was prepared using the PRISMA guidelines⁷ and the methodology described here is outlined in Figure 1 (Supplemental File 1).

Figure 1.

PRISMA flow diagram of the systematic review workflow and the number of articles at each stage of the review process (n).⁷

Results

Using the methods described above, 12 articles were identified to be included in the systematic review. The summary of key findings is shown in Table 1.

Table 1.

Key summary of articles included in the systematic review.

Authors (year)	Study design	Population	Country	Outcome
Parameshwari et al. (2013)⁸	Case Control Study	Arpookara Panchayat of Kottayam district of Kerala; 20 cases and 80 age-matched controls free from breast cancer selected from same Panchayat; Mean age 49.7 for cases and 49.6 for controls	India	There were significant differences in the number of cases vs. Controls reporting awareness of breast cancer symptoms and BSE: only 5 participants with breast cancer reported awareness while 42 (52.5%) of controls were aware
Foroozani et al. (2020)⁹	Retrospective Study	725 patients with newly diagnosed (<6months) breast cancer in Shiraz and Kermanshah	Iran	Knowledge of BSE was inversely associated with patients’ delay in diagnosis
Tesfaw et al. (2021)¹⁰	Cross-Sectional Study	Patients with histologically confirmed breast cancer who were treated between 1 September 2019 and 30 April 2020 at the two hospitals, median age 40	Ethiopia	Factors determining advanced-stage breast cancer included rural residents, painless breast lump/wound, traveling over 5km for care, no BSE, presenting more than 3 months after lesion was first noticed, and misdiagnosis at initial visit
Dianatinasab et al. (2016)¹¹	Cross-Sectional Study	505 newly diagnosed patients with breast cancer from southern Iran	Iran	Women with knowledge of BSE, higher literacy patients, women living in less rural areas, married women, and women with ductal tumors type of cancer were all diagnosed at earlier days compared to their respective counterparts. But feeling a lump as an initial symptom was associated with a delay in diagnosis
Dadzi and Adam (2019)¹²	Descriptive Cross-Sectional Study (Survey)	385 respondents infarming/fishing communities, ages 15-49	Ghana	Respondents reported multiple educational sources, including healthcare workers, friends, books, and other means. Women different on when it was most appropriate to perform exams preceding or following menstruation or at any point in the month
Sharp et al. (2019)¹³	Convenience-Based Sampling Approach	Women aged 25 and older with no personal history of breast cancer,100 from urban Kampala and 301 from rural villages in south central Uganda	Uganda	Participants reported cost and lack of education regarding where to receive breast exams as barriers
Das et al. (2019)¹⁴	Quasi-Experimental Study	502 rural women between 15-50 years	India	After intervention in the post-test, 96% of subjects had good skills in BSE, 4% had average skills and none had poor skills
Wu and Lee (2019)¹⁵	Cross-Sectional Study	944 women from two urban and one rural area, mean age was 47.1	Philippines	Descriptive statistics were computed for univariate analyses; while 60% of participants reported they knew BSEs needed to be performed monthly, only 25% actually performed them monthly. Filipino women with higher education were more likely to have a mammogram compared to those with no college education and no insurance. Highly educated women and women with insurance were more likely to ever have CBE, and cost remained the greatest factor in choosing CBE over a mammogram
Leung et al. (2014)¹⁶	Longitudinal Study	11,200 women aged 50-55	Australia	Significantly less women in rural areas received CBE compared to their urban counterparts and significantly less women in urban areas performed BSE compared to their rural counterparts and their area of residence is associated with this result
Karimian et al. (2022)¹⁷	Experimental	100 women between 20 to 60 years old with no training on BSE	Iran	There were no significant differences across face-to-face and video-based training methods (P = 0.08), but face-to-face training was more effective in improving negligence and/or forgetfulness in applying BSE and in correcting or modifying the previous knowledge around the issue
White and Camper (2016)¹⁸	Pilot Implementation Study	Women aged 18-78 years in rural Dominican Republic who were waiting to receive medical care at mobile medical clinics offered by U.S. volunteers in four barrios	Dominican Republic	With breast health and BSE education, knowledge of BSE improved from 37% to 54%. Also, there was an increase in health care follow-ups if women discovered a suspicious lump (88% to 100%)
Kohler et al. (2017)¹⁹	Cross-Sectional Study	262 women randomly chosen based on their geographic coordinate in Lilongwe district	Malawi	There was a significant correlation between breast cancer awareness and BSE (p<0.001), with the majority of participants (70%) performing BSE and reporting benefits

BSE: breast self-examination. CBE: clinical breast examination.

The articles that were included in the systematic review were analyzed to address the primary research question of if BSE is associated with benefits including increased breast cancer detection rates, increased breast cancer screening, and decreased mortality. From this analysis, findings were identified in four key areas.

Effects of BSE on breast cancer diagnosis and/or mortality of breast cancer patients

While BSE is no longer recommended in the United States as a breast cancer screening method, recent international studies raise the possibility that it may have benefits for rural populations. Indeed, poorer knowledge of breast cancer symptoms and BSE practice were inversely associated with breast cancer diagnosis in rural India.⁸ Similarly, a negative association between knowledge of BSE and breast cancer staging at the time of diagnosis was found in two separate rural Iranian cities.⁹ In addition, a cross-sectional study on patients from various oncology units in Ethiopia also showed an association between if the patient practiced BSE and breast cancer staging at the time of diagnosis, where a lack of BSE performance was associated with higher staging at the time of diagnosis. Moreover, this study also identified that rural residence and long distance from healthcare facilities were also positively associated with delayed breast cancer diagnosis.¹⁰ Consistent with above studies, a cross-sectional study in rural Iran found that patients from rural areas faced a delay in diagnosis compared to their city counterparts. Patients who had knowledge of BSEs were diagnosed significantly earlier than those who were unaware, but women who felt a lump as an initial symptom were diagnosed later, though the delay was non-significant.¹¹

Factors affecting competency in BSE performance

Several studies revealed that knowledge on how to perform BSE is an important factor when evaluating its utility.^12–14 A study conducted in rural Ghana in which most women did not practice BSE revealed that over half the women who were aware of but did not practice BSE admitted that it was because they did not know how to perform one properly.¹² Another study on women in rural Uganda reported that the greatest barrier to breast cancer screening was knowledge, with over 55% of the population stating they had never received education on breast cancer.¹³ The suggestion that many women may not be performing BSE due to a lack of knowledge on how to perform them well highlights an opportunity for healthcare workers to provide better education for their patients. Indeed, a study did assess the ability of an educational program in rural India to improve BSE skills by employing a pre- and post-test survey to assess knowledge about breast cancer and actual performance of BSE. The improvement in post-test knowledge and BSE performance were both significant.¹⁴

Factors that make BSE more convenient to perform than other screening methods

Lack of resources can influence women’s willingness and/or ability to receive mammograms for breast cancer screening.¹⁵ Women in rural Philippines were only receiving mammograms as diagnostic tests, not as a component of a routine screening. Despite receiving education on the significance of screening, 80% of women preferred to perform BSE or receive CBE rather than a mammogram because of financial concerns. Similarly in Australia, women living in rural areas were more likely to perform BSEs in place of receiving a CBE, which is not free.¹⁶ With the development of a program intended to offer free mammograms to women aged 55–69, women in rural areas were more inclined to receive a mammogram due to improved access. However, BSEs remained the exam of choice over CBEs due to cost.¹⁶

Effects of BSE on breast cancer awareness/behaviors to seek further screening

Understanding the reasoning for performing a BSE is necessary for women to conduct them regularly. A 2022 interventional comparison study found that video-based multimedia training effectively raised awareness about breast neoplasms and improved breast self-examination performance, facilitating earlier diagnosis and enhancing understanding of BSE’s role and breast cancer knowledge.¹⁷ Similarly, a pilot study conducted in the Dominican Republic aimed to gauge breast cancer knowledge among locals and evaluate responses to screening education.¹⁸ It revealed that after BSE education, all participants reported improved knowledge of examining their breasts for lumps and knowing whom to contact if a lump was detected. In 2017, Kohler et al. surveyed women in Malawi’s Lilongwe district to assess breast cancer knowledge and behaviors. Awareness of breast self-examination was positively correlated with breast cancer awareness.¹⁹ Additionally, women unaware of BSE and CBE had stronger fatalistic beliefs, potentially deterring early care-seeking.¹⁹ The three studies collectively highlight the role of BSE education in encouraging early medical attention and further screening.

Discussion

The primary screening tools available for breast cancer screening are mammograms and clinical physical breast examinations. Of these, mammograms are routinely difficult to access, have a high cost to perform, and have been shown to not lead to improved mortality outcomes.⁵ In areas that are medically underserved, with patient populations who do not have easy access to mammograms, therefore, detection and screening of breast cancer is highly reliant on physical clinical examinations which are not foolproof and can miss early breast cancer detection in these populations.²⁰ In the study by Foroozani et al., living in rural areas was associated with both delay of diagnosis and a higher risk of advanced stage at diagnosis, both of which may be due to limited access to screening and diagnostic services.⁹ While mammography is now the standard screening method for women, these technologies are not available to millions of women around the world.¹²

Articles that specifically studied under-resourced and rural areas were looked at to determine if BSE would be effective in specific regions within the United States. Many articles concluded that BSE is an effective form of breast cancer screening in target populations, provided everyone understands the limitations of BSE in screening and detection. According to the ACS, women living in the United States ages 45–54 should receive mammograms every year.²¹ After the age of 54, the recommendation is for women to receive a mammogram every 2 years.²¹ The current screening and detection recommendations do not consider the diverse circumstances of women living within rural America, however. One study’s results indicated that access to early detection and interventions is an important determinant of the prognosis of breast cancer at the time of diagnosis.¹⁹ This study also identified travel time and transportation as barriers to receiving a clinical breast exam for rural, Malawian patients.¹⁹ Women living in the rural United States are medically underserved due to similar barriers and others, including social stigma, low health literacy, and staffing shortages.²² By providing an alternative to standard screening procedures, education on BSE for women with extenuating circumstances in the United States that are unable to conveniently access routine breast cancer interventions may lower the mortality rate of breast cancer within the United States. Another study reported lack of access to breast cancer screening facilities, a lack of knowledge about the risks of breast cancer, and misconceptions of BSE in general as three factors that contribute to poorer breast cancer prognosis and outcomes.¹⁸ The study determined that the provision of health education had a positive effect on increasing knowledge and attitude about BSE and encouraged women to seek medical care before the breast cancer has advanced and become symptomatic, consequently leading to earlier detection and potentially better outcomes.¹⁸ With fewer physicians advising patients within the United States to perform BSE, the understanding of BSE and its purpose may be limited. Furthermore, for women who are not routinely receiving the recommended preventative measures such as mammography and CBE, BSE would be their only breast cancer screening option.

The systematic review suggests that there are several barriers to receiving any screening tests for breast cancer, primarily lack of knowledge^12–14 and lack of access in rural settings.¹⁶ Having access to screening is important for diagnosing cancer at an earlier stage.^9,10 Women living in urban areas were more likely to be educated on breast cancer, receive regular screenings, and receive earlier diagnoses, all of which led to better outcomes.^9,10,13,16 Indeed, as seen in Karimian et al., BSE training resulted in increased knowledge regarding breast cancer, improved performance of BSEs for screening, and earlier diagnoses of breast cancer.¹⁷ To equitize breast cancer screenings among all populations, future breast cancer screening recommendations should consider accessibility of the recommendation and proper patient education to ensure adherence.

This study addresses a major gap in healthcare research by considering the potential benefits of BSEs in medically underserved regions (Figure 2). The medically underserved represent a population where disparities in healthcare access and higher mortality rates exist. The study employs a systematic review methodology, utilizing a set of terms to search multiple databases for recent studies. This approach enhances the robustness of the analysis. The inclusion of the number of abstracts obtained from the search provides a tangible starting point for the subsequent analysis, offering a quantitative aspect to the study. The methods highlight the consideration of social determinants of health in the analysis and the need for qualitative and quantitative measures to understand the impact of BSEs on diverse populations.

Figure 2.

Summary diagram of the systematic review. 230 articles from PubMed, SCOPUS, and CINAHL were screened as described above. Twelve of the 230 articles were included in the review whose results suggest that breast self-examination (BSE) practice may provide benefits in rural and underserved communities as outlined in the figure.

Limitations

This study effectively emphasizes the need to reconsider recommendations regarding BSE based on specific populations and social determinants. However, it is crucial to acknowledge the study’s limitations to ensure a balanced interpretation of the results. Due to the limited number of recent articles published on the topic of BSE, the study did not extensively assess the articles for internal/external biases. Furthermore, while the current breast cancer screening recommendations were established in 2003, this work only looked at articles published in the past 10 years. The reason for this was to ensure that the studies being analyzed were performed after the seminal work in the Cochrane Reviews was published to assess new findings in the field. However, it is possible that important findings and insights from studies conducted in the intervening years and those that were conducted prior to the Cochrane Review articles were missed. These limitations could have introduced data bias to the study in the form of selection, confirmation, and publication biases. Future work with gray literature searches and inclusion of older studies on breast cancer screening may help mitigate this limitation. Additionally, the assumption that results from international studies can be applied to rural Americans may oversimplify the complexities of healthcare systems and cultural differences. The cultural differences between the United States and the countries in these studies have not been assessed and could pose challenges to applying results from international studies to underserved populations in the United States. Historical context for changing attitudes and research representing unique American populations may improve the overall validity of the conclusions. Given the field of breast cancer research has evolved rapidly in recent history, a broader temporal and narrower geographic scope might capture a more comprehensive understanding of how current recommendations for American women have developed over time. In keeping with the strengths and weaknesses of the research and methodology, future research should delve into the efficacy of applying information derived from settings outside of the United States to underserved populations in the United States. Programs improving knowledge of BSE could also be implemented to investigate further the need to provide customized approaches to breast cancer screening modalities in unique populations. The results of such efforts may illuminate methods of modifying healthcare recommendations to address current issues regarding late diagnosis and inaccessibility to breast cancer screenings.

Conclusion

The main goal of this systematic review was to determine if BSE could have benefits as a breast cancer screening tool in specific populations. The resulting work suggests that BSE is still an important tool for many communities worldwide and the reasons they have for continued use of the practice may potentially apply to rural or medically underserved areas. BSE raised awareness of breast cancer symptoms, it was found to be more convenient to perform than alternative screening methods in rural areas, and individuals who performed BSE presented earlier for treatment of breast cancer. These results suggest that communities without access to routine screening with more reliable tools like mammography could benefit from recommending the routine practice of BSE instead. Although it was outside the scope of this study, future research on this subject could also explore the relative efficacy of CBE as compared to BSE. Additionally, research could be done looking into the potential benefits of alternative screening recommendations for other populations with reduced access to medical care such as low-income regions or people living with disabilities. Overall, the findings from this study highlight the continued relevance of BSE globally, and warrant revisiting the current recommendations for breast cancer screening set out by the ACS. Further research focused specifically on underserved populations in the United States may help strengthen existing recommendations and address the challenges of breast cancer screening for these populations.

Supplemental Material

sj-docx-1-whe-10.1177_17455057241311400 – Supplemental material for Benefits of breast self-examinations for medically underserved populations: A systematic review

Supplemental material, sj-docx-1-whe-10.1177_17455057241311400 for Benefits of breast self-examinations for medically underserved populations: A systematic review by Caroline M Cassidy, Christopher I Choi, Benjamin Herdman, Taryn K Kilbane, Jessica F Lannen, James P McConnell, Michelle M Moufawad and Beth A Bailey in Women’s Health

Footnotes

Acknowledgements

We thank Rebecca Renirie for her help in training and generating the database search terms. This article was the culmination of a class project for which the student authors received a grade for the Central Michigan University College of Medicine, Medicine and Society course, taught by the final author.

Declarations

ORCID iD

Christopher I Choi

Supplemental material

Supplemental material for this article is available online.

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Supplementary Material

Please find the following supplemental material available below.

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