Breast cancer screening adherence rates and barriers of implementation in ethnic, cultural and religious minorities: A systematic review

Ferreira,Cristiana Sofia; Rodrigues,Joana; Moreira,Stefanie; Ribeiro,Filipa; Longatto‑Filho,Adhemar

doi:10.3892/mco.2021.2301

Breast cancer screening adherence rates and barriers of implementation in ethnic, cultural and religious minorities: A systematic review

Authors:
- Cristiana Sofia Ferreira
- Joana Rodrigues
- Stefanie Moreira
- Filipa Ribeiro
- Adhemar Longatto‑Filho
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Affiliations: School of Medicine, University of Minho, Braga, Minho 4710‑057, Portugal
Published online on: May 19, 2021 https://doi.org/10.3892/mco.2021.2301
Article Number: 139
Copyright: © Ferreira et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Breast cancer is the most common cancer affecting women worldwide. Adherence to breast cancer screening guidelines is frequently lower in racial, ethnic and cultural minority populations and is affected by potential inequities or barriers to screening that these minorities face. Therefore, the aim of the present study was to collect information from different minority groups worldwide, assess adherence to breast cancer screening and evaluate barriers or limitations causing non‑adherence, which should facilitate the development of effective interventions. A search was conducted through PubMed and Web of Science. Studies were considered as eligible if they met the following criteria: i) Female patients; ii) breast cancer screening program implemented in the country; iii) minority groups; iv) asymptomatic; v) report written in Portuguese or English; vi) study published from 2015 onwards. The Critical Appraisal Skills Programme checklist was used for qualitative studies and the Strengthening The Reporting of Observational Studies in Epidemiology checklist for cross‑sectional studies. From the 348 initial articles, 86 were removed due to duplication and 19 were selected, analyzed and summarized, accordingly. Of the 19 studies included, 5.3% were classified as high quality, 52.6% as moderate to high and 42.1% as moderate. A total of 15 studies were cross‑sectional and 4 were qualitative, collectively including 250,733 women. The rate of adherence to mammogram in different minorities was evaluated, obtaining a mean value of 49.7% in the last 2 years, and statistically significant barriers were selected and divided into sociodemographic; personal; ethnic, cultural and religious; and external factors. The characteristics of each population play a major role in the population's breast health practices. If the population, adherence rates, barriers and inequities are carefully studied, screening models may be customized and participation to breast cancer screening can be optimized, thereby reducing the high breast cancer‑associated mortality.

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1	World Health Organization: WHO\|Breast cancer. https://www.who.int/cancer/prevention/diagnosis-screening/breast-cancer/en/. Accessed March 22, 2020.
2	Morrell S, Taylor R, Roder D and Dobson A: Mammography screening and breast cancer mortality in Australia: An aggregate cohort study. J Med Screen. 19:26–34. 2012.PubMed/NCBI View Article : Google Scholar
3	Nelson HD, Fu R, Cantor A, Pappas M, Daeges M and Humphrey L: Effectiveness of breast cancer screening: Systematic review and meta-analysis to update the 2009 U.S. Preventive services task force recommendation. Ann Intern Med. 164:244–255. 2016.PubMed/NCBI View Article : Google Scholar
4	Roder D, Houssami N, Farshid G, Gill G, Luke C, Downey P, Beckmann K, Iosifidis P, Grieve L and Williamson L: Population screening and intensity of screening are associated with reduced breast cancer mortality: Evidence of efficacy of mammography screening in Australia. Breast Cancer Res Treat. 108:409–416. 2008.PubMed/NCBI View Article : Google Scholar
5	Morrell S, Taylor R, Roder D, Robson B, Gregory M and Craig K: Mammography service screening and breast cancer mortality in New Zealand: A National Cohort Study 1999-2011. Br J Cancer. 116:828–839. 2017.PubMed/NCBI View Article : Google Scholar
6	Niell BL, Freer PE, Weinfurtner RJ, Arleo EK and Drukteinis JS: Screening for breast cancer. Radiol Clin North Am. 55:1145–1162. 2017.PubMed/NCBI View Article : Google Scholar
7	Coleman C: Early detection and screening for breast cancer. Semin Oncol Nurs. 33:141–155. 2017.PubMed/NCBI View Article : Google Scholar
8	Moss SM, Nyström L, Jonsson H, Paci E, Lynge E, Njor S and Broeders M: Euroscreen Working Group. The impact of mammographic screening on breast cancer mortality in Europe: A review of trend studies. J Med Screen. 19 (Suppl 1):S26–S32. 2012.PubMed/NCBI View Article : Google Scholar
9	Van Schoor G, Moss SM, Otten JD, Donders R, Paap E, den Heeten GJ, Holland R, Broeders MJ and Verbeek AL: Increasingly strong reduction in breast cancer mortality due to screening. Br J Cancer. 104:910–914. 2011.PubMed/NCBI View Article : Google Scholar
10	Puliti D and Zappa M: Breast cancer screening: Are we seeing the benefit? BMC Med. 10(106)2012.PubMed/NCBI View Article : Google Scholar
11	Veitch D, Goossens R, Owen H, Veitch J, Molenbroek J and Bochner M: Evaluation of conventional training in Clinical Breast Examination (CBE). Work. 62:647–656. 2019.PubMed/NCBI View Article : Google Scholar
12	Greenwald ZR, Fregnani JH, Longatto-Filho A, Watanabe A, Mattos JSC, Vazquez FL and Franco EL: The performance of mobile screening units in a breast cancer screening program in Brazil. Cancer Causes Control. 29:233–241. 2018.PubMed/NCBI View Article : Google Scholar
13	Lopes LV, Miguel F, Freitas H, Tavares A, Pangui S, Castro C, Lacerda GF, Longatto-Filho A, Weiderpass E and Santos LL: Stage at presentation of breast cancer in Luanda, Angola-a retrospective study. BMC Health Serv Res. 15(471)2015.PubMed/NCBI View Article : Google Scholar
14	Talley CH, Yang L and Williams KP: Breast cancer screening paved with good intentions: Application of the information-motivation-behavioral skills model to racial/ethnic minority women. J Immigr Minor Health. 19:1362–1371. 2017.PubMed/NCBI View Article : Google Scholar
15	Mauad EC, Nicolau SM, Moreira LF, Haikel RL, Longatto-Filho A and Baracat EC: Adherence to cervical and breast cancer programs is crucial to improving screening performance. Rural Remote Health. 9(1241)2009.PubMed/NCBI
16	Mauad EC, Silvay TB, Haikel RL, Bauab S and Longatto-Filhoy A: Is community intervention in breast cancer screening in Brazil feasible? J Med Screen. 18(51)2011.PubMed/NCBI View Article : Google Scholar
17	Miller BC, Sarma EA, Sun Y, Messina CR and Moyer A: Psychosocial predictors of mammography history among Chinese American women without a recent mammogram. Ethn Health. 25:862–873. 2020.PubMed/NCBI View Article : Google Scholar
18	Adu PA, Ukah UV and Palmer SD: Association between recency of immigration and mammography uptake: Results from a Canadian National Survey. J Immigr Minor Heal. 19:228–235. 2017.PubMed/NCBI View Article : Google Scholar
19	De Andrade Souza CI, Araújo DS, Teles DA, Carvalho SG, Cavalcante KW, Rabelo WL, Alves CN and Fonseca AJ: Factors related to non-adherence to mammography in a city of the Brazilian Amazonian area: A population-based study. Rev Assoc Med Bras (1992). 63:35–42. 2017.PubMed/NCBI View Article : Google Scholar
20	Guo Y, Cheng TC and Lee HY: Factors associated with adherence to preventive breast cancer screenings among middle-aged African American women. Soc Work Public Health. 34:646–656. 2019.PubMed/NCBI View Article : Google Scholar
21	Vahabi M, Lofters A, Kim E, Wong JP, Ellison L, Graves E and Glazier RH: Breast cancer screening utilization among women from Muslim majority countries in Ontario, Canada. Prev Med. 105:176–183. 2017.PubMed/NCBI View Article : Google Scholar
22	Zorogastua K, Sriphanlop P, Reich A, Aly S, Cisse A and Jandorf L: Breast and cervical cancer screening among US and non US born African American Muslim Women in New York City. AIMS PUBLIC Health. 4:78–93. 2017.PubMed/NCBI View Article : Google Scholar
23	Farzaneh E, Heydari H, Shekarchi AA and Kamran A: Breast and cervical cancer-screening uptake among females in Ardabil, northwest Iran: A community-based study. Onco Targets Ther. 10:985–992. 2017.PubMed/NCBI View Article : Google Scholar
24	Pilkington L, Haigh MM, Durey A, Katzenellenbogen JM and Thompson SC: Perspectives of Aboriginal women on participation in mammographic screening: A step towards improving services. BMC Public Health. 17(697)2017.PubMed/NCBI View Article : Google Scholar
25	Lee EE, Nandy K, Szalacha L, Park H, Oh KM, Lee J and Menon U: Korean American women and mammogram uptake. J Immigr Minor Heal. 18:179–186. 2016.PubMed/NCBI View Article : Google Scholar
26	Freund A, Cohen M and Azaiza F: Factors associated with routine screening for the early detection of breast cancer in cultural-ethnic and faith-based communities. Ethn Health. 24:527–543. 2019.PubMed/NCBI View Article : Google Scholar
27	Hong HC, Ferrans CE, Park C, Lee H, Quinn L and Collins EG: Effects of Perceived Discrimination and Trust on Breast Cancer Screening among Korean American Women. Womens Health Issues. 28:188–196. 2018.PubMed/NCBI View Article : Google Scholar
28	Molina Y, Plascak JJ, Patrick DL, Bishop S, Coronado GD and Beresford SAA: Neighborhood predictors of mammography barriers among US-based latinas. J Racial Ethn Heal Disparities. 4:233–242. 2017.PubMed/NCBI View Article : Google Scholar
29	Shaw T, Ishak D, Lie D, Menon S, Courtney E, Li ST and Ngeow J: The influence of Malay cultural beliefs on breast cancer screening and genetic testing: A focus group study. Psychooncology. 27:2855–2861. 2018.PubMed/NCBI View Article : Google Scholar
30	Wildes KA, Nápoles-Springer A, Pérez-Stable E, Talavera G and Rios E: Physician gender differences in general and cancer-specific prevention attitudes and practices. J Cancer Educ. 24:85–93. 2009.PubMed/NCBI View Article : Google Scholar
31	Lee HY, Lee MH, Jang YJ and Lee DK: Breast cancer screening disparity among Korean American immigrant women in midwest. Asian Pac J Cancer Prev. 18:2663–2667. 2017.PubMed/NCBI View Article : Google Scholar
32	Cohen EL, Wilson BR, Vanderpool RC and Collins T: Identifying sociocultural barriers to mammography adherence among Appalachian Kentucky Women. Health Commun. 31:72–82. 2016.PubMed/NCBI View Article : Google Scholar
33	O'Hara J, McPhee C, Dodson S, Cooper A, Wildey C, Hawkins M, Fulton A, Pridmore V, Cuevas V, Scanlon M, et al: Barriers to breast cancer screening among diverse cultural groups in Melbourne, Australia. Int J Environ Res Public Health. 15(1677)2018.PubMed/NCBI View Article : Google Scholar
34	Ma J, Jemal A, Fedewa SA, Islami F, Lichtenfeld JL, Wender RC, Cullen KJ and Brawley OW: The American Cancer Society 2035 challenge goal on cancer mortality reduction. CA Cancer J Clin. 69:351–362. 2019.PubMed/NCBI View Article : Google Scholar
35	Brouwers MC, De Vito C, Bahirathan L, Carol A, Carroll JC, Cotterchio M, Dobbins M, Lent B, Levitt C, Lewis N, et al: What implementation interventions increase cancer screening rates? a systematic review. Implement Sci. 6(111)2011.PubMed/NCBI View Article : Google Scholar
36	Yeoh KG, Chew L and Wang SC: Cancer screening in Singapore, with particular reference to breast, cervical and colorectal cancer screening. J Med Screen. 13 (Suppl 1):S14–S19. 2006.PubMed/NCBI
37	Australian Institute of Health and Welfare: Breast Screen Australia Monitoring Report 2006-2007 and 2007-2008. Canberra, 2010. AIHW, Canberra, Cancer series no. 55. Cat. no. CAN 51, 2010.
38	Israel Cancer Association. The Israel Cancer Association-Colorectal Cancer. http://en.cancer.org.il/template_e/default.aspx?PageId=7747. Accessed March 25, 2020.
39	Azevedo e Silva G, Bustamante-Teixeira MT, Aquino EML, Tomazelli JG and dos-Santos-Silva I: Acesso à detecção precoce do câncer de mama no sistema Único de saúde: Uma análise a partir dos dados do sistema de informações em saúde. Cad Saude Publica. 30:1537–1550. 2014.PubMed/NCBI View Article : Google Scholar : (In Portuguese).
40	Moser K, Patnick J and Beral V: Inequalities in reported use of breast and cervical screening in Great Britain: Analysis of cross sectional survey data. BMJ. 338(b2025)2009.PubMed/NCBI View Article : Google Scholar
41	Nuche-Berenguer B and Sakellariou D: Socioeconomic determinants of cancer screening utilisation in Latin America: A systematic review. PLoS One. 14(e0225667)2019.PubMed/NCBI View Article : Google Scholar
42	Davis TC, Arnold C, Berkel HJ, Nandy I, Jackson RH and Glass J: Knowledge and attitude on screening mammography among low-literate, low- income women. Cancer. 78:1912–1920. 1996.PubMed/NCBI View Article : Google Scholar
43	Davis TC, Williams MV, Marin E, Parker RM and Glass J: Health Literacy and Cancer Communication. CA Cancer J Clin. 52:134–149. 2002.PubMed/NCBI View Article : Google Scholar
44	Consedine NS, Magai C, Krivoshekova YS, Ryzewicz L and Neugut AI: Fear, anxiety, worry, and breast cancer screening behavior: A critical review. Cancer Epidemiol Biomarkers Prev. 13:501–510. 2004.PubMed/NCBI
45	Azami-Aghdash S, Ghojazadeh M, Sheyklo SG, Daemi A, Kolahdouzan K, Mohseni M and Moosavi A: Breast cancer screening barriers from the womans perspective: A meta-synthesis. Asian Pacific J Cancer Prev. 16:3463–3471. 2015.PubMed/NCBI View Article : Google Scholar
46	Katapodi MC, Pierce PF and Facione NC: Distrust, predisposition to use health services and breast cancer screening: Results from a multicultural community-based survey. Int J Nurs Stud. 47:975–983. 2010.PubMed/NCBI View Article : Google Scholar
47	Mouslim MC, Johnson RM and Dean LT: Healthcare system distrust and the breast cancer continuum of care. Breast Cancer Res Treat. 180:33–44. 2020.PubMed/NCBI View Article : Google Scholar
48	Keemers-Gels ME, Groenendijk RP, van den Heuvel JH, Boetes C, Peer PG and Wobbes TH: Pain experienced by women attending breast cancer screening. Breast Cancer Res Treat. 60:235–240. 2000.PubMed/NCBI View Article : Google Scholar
49	Elewonibi B and BeLue R: The influence of socio-cultural factors on breast cancer screening behaviors in Lagos, Nigeria. Ethn Heal. 24:544–559. 2019.PubMed/NCBI View Article : Google Scholar
50	O'Reilly D, Kinnear H, Rosato M, Mairs A and Hall C: Uptake of breast screening is influenced by current religion and religion of upbringing. J Relig Health. 52:1168–1176. 2013.PubMed/NCBI View Article : Google Scholar
51	Fox SA, Pitkin K, Paul C, Carson S and Duan N: Breast cancer screening adherence: Does church attendance matter? Health Educ Behav. 25:742–758. 1998.PubMed/NCBI View Article : Google Scholar
52	McEwan J, Underwood C and Corbex M: Injustice! that is the cause: A qualitative study of the social, economic, and structural determinants of late diagnosis and treatment of breast cancer in Egypt. Cancer Nurs. 37:468–475. 2014.PubMed/NCBI View Article : Google Scholar
53	Lee SY: Cultural factors associated with breast and cervical cancer screening in Korean American Women in the US: An integrative literature review. Asian Nurs Res (Korean Soc Nurs Sci). 9:81–90. 2015.PubMed/NCBI View Article : Google Scholar
54	Kawar LN: Barriers to breast cancer screening participation among Jordanian and Palestinian American women. Eur J Oncol Nurs. 17:88–94. 2013.PubMed/NCBI View Article : Google Scholar
55	Glazier RH, Klein-Geltink J, Kopp A and Sibley LM: Capitation and enhanced fee-for-service models for primary care reform: A population-based evaluation. CMAJ. 180:E72–E81. 2009.PubMed/NCBI View Article : Google Scholar
56	Todd L, Harvey E and Hoffman-Goetz L: Predicting breast and colon cancer screening among English-as-a-second- language older Chinese immigrant women to Canada. J Cancer Educ. 26:161–169. 2011.PubMed/NCBI View Article : Google Scholar
57	Alexandraki I and Mooradian AD: Barriers related to mammography use for breast cancer screening among minority women. J Natl Med Assoc. 102:206–218. 2010.PubMed/NCBI View Article : Google Scholar
58	Gierisch JM, O'Neill SC, Rimer BK, DeFrank JT, Bowling JM and Skinner CS: Factors associated with annual-interval mammography for women in their 40s. Cancer Epidemiol. 33:72–78. 2009.PubMed/NCBI View Article : Google Scholar
59	Baron RC, Melillo S, Rimer BK, Coates RJ, Kerner J, Habarta N, Chattopadhyay S, Sabatino SA, Elder R and Leeks KJ: Task Force on Community Preventive Services. Intervention to increase recommendation and delivery of screening for breast, cervical, and colorectal cancers by healthcare providers. A systematic review of provider reminders. Am J Prev Med. 38:110–117. 2010.PubMed/NCBI View Article : Google Scholar
60	Lurie N, Margolis KL, McGovern PG, Mink PJ and Slater JS: Why do patients of female physicians have higher rates of breast and cervical cancer screening? J Gen Intern Med. 12:34–43. 1997.PubMed/NCBI View Article : Google Scholar
61	Perez LG, Elder JP, Haughton J, Martinez ME and Arredondo EM: Socio-demographic moderators of associations between psychological factors and Latinas' breast cancer screening behaviors. J Immigrant and Minority Health. 20:823–830. 2018.PubMed/NCBI View Article : Google Scholar
62	Smalls BL, Aroh A, McQuerry K, Adegboyega A, Schoenberg N and Hatcher J: Social support and breast cancer screening in rural Appalachia. Psychooncology. 27:2281–2288. 2018.PubMed/NCBI View Article : Google Scholar
63	Valdovinos C, Penedo FJ, Isasi CR, Jung M, Kaplan RC, Giacinto RE, Gonzalez P, Malcarne VL, Perreira K, Salgado H, et al: Cancer Causes Control 27:27-37, 2016.