Dr. Hughes is assistant professor of psychiatry in the Department of Psychiatry and director of the Community and Minority Cancer Prevention and Control Initiative at the University of Pennsylvania in Philadelphia.
Acknowledgments: This work was supported by Department of Defense Grant #DAMD17-00-1-0262.
What role does culture play in cancer genetics research? Genetic counseling and testing for BRCA1 and BRCA2 mutations is increasingly being integrated into the clinical management of individuals who have a family history of cancer that is suggestive of inherited breast-ovarian cancer. While several studies have been conducted to understand the psychological, clinical, and familial impact of genetic testing, relatively little attention has been given to the role of cultural influences on the process of providing genetic counseling and testing services. Cultural factors such as beliefs and values and ethnic background are likely to play an important role in genetic risk profiles, decisions about participation in genetic risk assessment and testing, and responses to genetic risk information. This article reviews emerging literature on the role of cultural factors in cancer genetics research.
A substantial amount of research has been conducted to understand the clinical, psychological, and familial impact of genetic testing for inherited breast cancer risk. For example, women who are found to carry a cancer predisposing BRCA1 or BRCA2 (BRCA1/2) mutation have an estimated 55% to 85% increased risk of developing breast cancer and a 15% to 60% increased risk of developing ovarian cancer.1-3 Men who have a risk conferring the BRCA1/2 mutation are also at increased risk for developing prostate cancer.1 Several studies have also shown that rates of communicating BRCA1/2 test results to family members are high4-6. However, genetic testing may have an adverse effect on family and personal relationships.
In a recent study, approximately one third of BRCA1/2 mutation carriers reported that their family or personal relationships had been affected by genetic testing, and of these, 50% reported that these relationships were more emotionally strained after genetic testing.7 Data on the psychological impact of genetic counseling and testing continue to emerge, and recent studies have demonstrated that receiving BRCA1/2 test results may generate specific emotional reactions, such as anxiety or sadness, rather than have an adverse effect on overall psychological functioning.8-14 Compared to women who did not carry a deleterious BRCA1/2 mutation, BRCA1/2 mutation carriers reported significantly greater levels of genetic testing-specific distress in a recent study.15
While there is an abundance of data on the clinical, psychological, and familial impact of genetic counseling and testing for inherited breast cancer risk, culture is increasingly being recognized as an important factor in cancer genetics research. Culture is defined as a framework of beliefs and values that shape behavior and influence the way in which information about illness is interpreted and used to make healthcare decisions.16 Recent reviews have recommended increased consideration of cultural characteristics in cancer prevention and control research,16,17 and several studies have explored how cultural factors influence outcomes within cancer genetics studies (ie, genetic testing decisions, responses to genetic risk information).
While there is an increasing emphasis on distinguishing the contributions of underlying beliefs and values that are derived from one’s cultural worldview (racial or ethnic differences in cancer prevention and control behaviors)18 data are limited on the influence of specific cultural beliefs and values on genetic counseling and testing outcomes. For this reason, this review focuses on empirical research that has addressed how cultural factors such as ethnic background influence (A) the prevalence of genetic risk factors; (B) interest in genetic testing; and (C) responses to education and counseling about hereditary breast cancer and genetic testing. A review of how ethnic background has influenced these outcomes is informative for identifying areas that should be addressed in future cancer genetics research.
Research is now being conducted to identify susceptibility genes that confer an increased risk of developing other forms of cancer (eg, prostate cancer susceptibility genes)19,20 and investigators are now exploring interest in genetic testing21-24 for these forms of hereditary cancer.
This review is designed to identify underlying themes and issues related to cultural influences in cancer genetics research. Because increased attention is being directed towards reducing or eliminating racial and ethnic disparities in cancer morbidity and mortality,25,26 articles that address ethnic group differences among African-American and White women are the focus of this article.
Ethnic Differences in Cancer Risk
A substantial amount of research has demonstrated that ethnic background is an important factor in breast cancer risk and survival. For example, while breast cancer incidence rates are greater among White women than among women from other racial and ethnic groups (ie, African American, Hispanic, Asian), African-American women are at increased risk for developing early onset disease, have higher rates of advanced-stage breast cancer, and show reduced rates of breast cancer survival.27-30
Recent work suggests that ethnic differences in breast cancer risk may also be due to variations in genetic risk factors.31 For example, although BRCA1/2 mutations account for only about 5% to 10% of all breast cancer cases,32,33 the prevalence of three founder BRCA1/2 mutations (185delAG, 5382insC in BRCA1 and 617delT in BRCA2) is about 2.5% among women of Ashkenazi Jewish background.1,34 Specific BRCA1/2 mutations have also been identified among other ethnic groups, including Icelanders (999del5 in BRCA2), Norwegians (1136insA in BRCA1), and African Americans (M1775R, 1832del5, and 5296del4 in BRCA1).31 Furthermore, data from recent epidemiological studies suggest that the prevalence of deleterious BRCA1/2 mutations ranges between 12% to 21% among clinic-based samples of African-American women who have a personal and family history of breast and/or ovarian cancer.35 While our understanding of BRCA1/2 mutations among African Americans is increasing, efforts to further understand the penetrance of BRCA1/2 mutations among this population may be limited because of reduced participation in cancer genetics research.
Interest in Genetic Risk Assessment and Testing
Several studies have shown that women in the general population and those who have a family history of breast cancer report a high level of interest in genetic testing for inherited breast cancer risk.36-38 However, these studies were conducted before predictive testing was available, and findings from these studies were based on data collected from samples of women who had a low or moderate risk of having a BRCA1/2 gene alteration. However, one of the first studies to report actual rates of test acceptance found that only 43% of high-risk individuals identified from a hereditary breast cancer registry received BRCA1/2 test results.14 While this study suggested that rates of genetic test acceptance may be lower than anticipated among high-risk individuals, a recent study found that 82% of high-risk probands (ie, the first index case affected with breast and/or ovarian cancer to have genetic testing) ascertained from breast cancer clinics utilized genetic testing and received BRCA1/2 test results.39 However, a limitation of these studies is that the findings are based on samples that were ethnically homogenous. A study by Schwartz and colleagues39 found that rates of genetic test acceptance did not differ among African-American and White women; however, African-American women made up only 5% of the study sample.
Previous research has shown that African-American women are significantly less likely to participate in an education session about hereditary breast cancer and genetic testing compared to White women.40 Even though African-American women reported significantly greater expectations about the positive outcomes of genetic testing than White women,41 only 49% of African-American women participated in a pretest education session about hereditary breast cancer and genetic testing compared to 68% of white women.40
While greater levels of cancer-specific distress may be a barrier to participating in education and counseling programs designed to provide information about hereditary cancer and genetic testing among African-American women,40 it is possible that reduced participation in education programs that were conducted before actual testing was available may underestimate interest in testing among African Americans at high risk for having a BRCA1/2 gene alteration.
A recent study found that 82% of African Americans at high risk for having a BRCA1/2 gene alteration reported that they would definitely have genetic testing.42 However, our preliminary findings suggest that rates of participation in genetic risk assessment and testing may be lower among high-risk African-American women. Only about 60% of African-American women who had a family history of breast and/or ovarian cancer that was suggestive of inherited breast cancer susceptibility participated in genetic risk assessment and received BRCA1/2 test results.43 The small number of studies that have focused on genetic counseling and testing specifically among African Americans is a significant limitation in our ability to understand the psychological and behavioral impact of genetic counseling and testing for inherited breast cancer risk among this population. However, we can anticipate these potential effects based on data from studies that have evaluated responses to breast cancer risk counseling and education.
Responses to Risk Education and Counseling
Previous research has shown that African-American women may have different needs and preferences for information about inherited cancer risk. For example, when compared to White women, African-American women were less knowledgeable about breast cancer genetics (ie, transmission of inherited cancer susceptibility).41,44 Although there were no differences among African-American and White women in terms of overall perceptions of the limitations and risks of testing in one study,4 more recent work has demonstrated that African-American women have greater concerns about the limitations and risks of genetic testing.44 However, African-American women were significantly more concerned about their ability to handle the emotional impact of genetic testing results compared to White women in both studies.41,44
Only a few studies have evaluated ethnic differences in the impact of education about hereditary breast cancer and genetic testing. For example, African-American women who participated in an education program about hereditary breast cancer and genetic testing reported significantly greater genetic testing intentions and were more likely to provide a blood sample for storage and possible future testing following an education and counseling intervention about hereditary breast cancer compared to African-American women who received an education-only intervention.40
Although this study was conducted before predictive testing for BRCA1/2 mutations was available and participants were women who had a low-to-moderate risk of having a BRCA1/2 gene alteration, the effects of the education and counseling intervention were only observed among African-American women. There were no differences in genetic testing intentions or provision of a blood sample among white women who received the education and counseling intervention compared to white women who received the education-only intervention.40 However, printed educational materials that were designed to provide information about hereditary breast cancer, BRCA1/2 genes in the Ashkenazi Jewish population, and information about the benefits, limitations, and risks of genetic testing, led to greater perceptions of the limitations and risks of genetic testing, increased levels of knowledge about breast cancer genetics, and decreased genetic testing intentions among Ashkenazi Jewish women at low risk for having a BRCA1/2 gene alteration.45
While the specific mechanisms that contribute to differences in responses to education about hereditary breast cancer and genetic testing among African-American women and Ashkenazi Jewish women are unclear, it is possible that education and counseling provide in-person increased motivations to have genetic testing among African-Americans because they had a high level of trust in the nurse educator who delivered the intervention.40 The education and counseling sessions for the majority of the African-American participants were completed by an African American nurse educator.46 Emphasis on interpersonal relationships is a key component of African-American culture, and it is possible that women were able to identify more strongly with the African-American nurse during the education session. This process may have contributed to increased genetic testing motivations.
Previous research has shown that ethnic identity or the level of affiliation with one’s ethnic or racial group is associated with responses to breast cancer risk education and counseling. Improvements in risk comprehension and reductions in cancer-related distress were associated with higher levels of African-American ethnic identity among women who participated in a breast cancer risk education program that was delivered in a group format.47 The process of identifying with women who are of the same ethnic background may be one mechanism through which African-American women comprehend cancer risk information. However, it is also likely that the specific beliefs and values related to interpersonal relationships, temporal orientation, and religion and spirituality that are highly endorsed within one’s cultural worldview also have a direct influence on responses to risk information and counseling provided within genetic counseling and testing settings.48
Cultural Considerations in Genetic Counseling for BRCA1/2 Mutations
In most clinical research settings, predictive genetic testing for BRCA1/2 mutations is offered to individuals who have a minimum 10% to 20% prior probability of having a deleterious BRCA1/2 mutation.49 It is standard practice to provide pretest education about hereditary breast cancer, the probability of having a BRCA1/2 gene alteration, and information about the benefits, limitations, and risk of genetic testing in order to facilitate informed decision-making about genetic testing.49,50 Post-test counseling is also provided to improve adjustment to BRCA1/2 test results and enhance informed decisions about cancer prevention, surveillance, and treatment.49,50
While provision of risk information is one of the key aspects of genetic assessment and counseling, temporal orientation may influence the salience of risk information. Temporal orientation is described as the level of cognitive involvement within past, present, and future dimensions, and greater levels of future temporal orientation have been associated with improved psychological functioning following traumatic events.51 It is possible that cancer risk estimates may be more meaningful among individuals with a future temporal orientation because they increase perceptions of control. However, among individuals with a present or past temporal orientation, estimates of genetic probability and disease risk may be less meaningful because there is little focus on the immediate situation.48
Previous research conducted among African Americans and Whites affected with hypertension has shown that individuals who had a present temporal orientation reported lower perceptions of the efficacy of disease prevention and control, as well as lower perceptions of susceptibility to the consequences of uncontrolled hypertension.52 In this study, as well as in studies conducted among individuals from the general population, African Americans were significantly more likely than Whites to have a present temporal orientation.52,53
Previous studies have shown that greater levels of spiritual faith were associated with lower rates of test acceptance in a prior study by Schwartz and colleagues.39 However, religious and spiritual beliefs may play a significant role in coping with genetic risk information among African-American women. Spirituality and religion are critical aspects of African-American culture,46 and previous research has shown that African-American women affected with breast cancer were more likely than white women to use religious coping strategies and resources to adjust to their breast cancer diagnosis and treatment.54 Religious coping strategies may also be used by African-American women to cope with genetic risk information. However, the psychological impact of genetic testing for BRCA1/2 mutations among African-American women and the effectiveness of religious coping strategies has not been evaluated among high-risk African-American women who have received BRCA1/2 test results.
Genetic counseling and testing for BRCA1/2 mutations is increasingly being integrated into the clinical management of individuals who have a family history of disease that is suggestive of inherited cancer susceptibility. A substantial amount of research has been conducted to understand the clinical, psychological, and familial impact of genetic testing for BRCA1/2 mutations. While few studies have addressed these outcomes among ethnically diverse populations, our knowledge about the prevalence of BRCA1/2 genes among these populations is increasing. For example, recent studies have shown that the prevalence of BRCA1/2 susceptibility genes is 12% to 21% among African-American hereditary breast cancer families. This finding provides support for the need for future studies designed to clarify the penetrance of BRCA1/2 mutations among this population. However, this review has demonstrated that reduced participation of African Americans in cancer genetics research is consistent. This is likely to be a significant limitation of future cancer genetics research, and increased culturally sensitive community outreach efforts may be needed to educate lay audiences about the availability of genetic counseling and testing or to recruit African Americans into cancer genetics research protocols.
This review has also demonstrated that ethnic background influences responses to information about hereditary breast cancer and genetic testing. However, the mechanisms that contribute to ethnic differences in responses to education about hereditary breast cancer are not clear. Additional research is needed to evaluate the influence of specific cultural beliefs and values on psychological and behavioral responses to genetic counseling and testing. PP
1. Struewing JP, Hartge P, Wacholder S, et al. The risk of cancer associated with specific mutations of BRCA1 and BRCA2 among Ashkenazi Jews. N Engl J Med. 1997;336:1401-1408.
2. Ford D, Easton DF, Stratton M, et al. Genetic heterogeneity and penetrance analysis of the BRCA1 and BRCA2 genes in breast cancer families. The Breast Cancer Linkage Consortium. Am J Hum Genet. 1998;62:676-689.
3. Easton DF, Ford D, Bishop DT. Breast and ovarian cancer incidence in BRCA1mutation carriers. Am J Hum Genet. 1995;56:265-271.
4. Hughes C, Lerman C, Schwartz M, et al. All in the family: evaluation of the process and content of sisters communication about BRCA1 and BRCA2 genetic test results. Am J Med Genet. 2002;107:143-150.
5. Lerman C, Peshkin BN, Hughes C, Isaacs C. Family disclosure in genetic testing for cancer susceptibility: determinants and consequences. J Health Care Law Policy. 1998;1:353-372.
6. Hughes C, Lynch H, Durham C, et al. Communication of BRCA1/2 test results in hereditary breast cancer families. Cancer Res. 1999;8:51-59.
7. Metcalfe KA, Liede A, Hoodfar E, et al. An evaluation of needs of female BRCA1 and BRCA2 carriers undergoing genetic counseling. J Med Genet. 2000;37:866-874.
8. Schwartz MD, Peshkin BN, Hughes C, Main D, Isaacs C, Lerman C. Impact of BRCA1/BRCA2 mutation testing on psychological distress in a clinic-based sample. J Clin Oncol. 2002;20:514-520.
9. Appleton S, Fry A, Rees G, Rush R, Cull A. Psychosocial effects of living with an increased risk of breast cancer: an exploratory study using telephone focus groups. Psychooncology. 2000;9:511-521.
10. Coyne JC, Benazon NR, Gaba CG, et al. Distress and psychiatric morbidity among women from high-risk breast and ovarian cancer families. J Consult Clin Psychol. 2000;68:864-874.
11. Croyle RT, Smith KR, Botkin JR, Baty B, Nash J. Psychological responses to BRCA1 mutation testing: preliminary findings. Health Psychol. 1997;16:63-72.
12. Cull A, Anderson ED, Campbell S, Mackay J, Smyth E, Steel M. The impact of genetic counseling about breast cancer risk on women’s risk perceptions and levels of distress. Br J Cancer. 1999;79:501-508.
13. Dorval M, Patenaude AF, Schneider KA, et al. Anticipated versus actual emotional reactions to disclosure of results of genetic tests for cancer susceptibility: findings from p53 and BRCA1 testing programs. J Clin Oncol. 2000;18:2135-2142.
14. Lerman C, Narod S, Schulman K, et al. BRCA1 testing in families with hereditary breast-ovarian cancer. A prospective study of patient decision making and outcomes. JAMA. 1996;275:1885-1892.
15. Cella D, Hughes C, Peterman A, et al. A brief assessment of concerns associated with genetic testing for cancer: the Multidimensional Impact of Cancer Risk Assessment (MICRA). Health Psychology. In press.
16. Meyerowitz BE, Richardson J, Hudson S, Leedham B. Ethnicity and cancer outcomes: behavioral and psychosocial considerations. Psychol Bull. 1998;123:47-70.
17. Johnson KRS. Ethnocultural influences in cancer. J Clin Psychol Med Settings. 1998;5:357-364.
18. Resnicow K, Baranowski T, Ahluwalia JS, Braithwaite RL. Cultural sensitivity in public health: defined and demystified. Ethn Dis. 1999;9:10-21.
19. Rebbeck TR, Walker AH, Zeigler-Johnson C, et al. Association of HPC2/ELAC2 genotypes and prostate cancer. Am J Hum Genet. 2000;67:1014-1019.
20. Tavtigian SV, Simard J, Teng DH, et al. A candidate prostate cancer susceptibility gene at chromosome 17p. Nat Genet. 2001;27:172-180.
21. Doukas DJ, Fetters MD, Coyne JC, McCullough LB. How men view genetic testing for prostate cancer risk: findings from focus groups. Clin Genet. 2000;58:169-176.
22. Myers RE, Hyslop T, Jennings-Dozier K, et al. Intention to be tested for prostate cancer risk among African-American men. Cancer Epidemiol Biomarkers Prev. 2000;9:1323-1328.
23. Miesfeldt S, Jones SM, Cohn W, et al. Men’s attitudes regarding genetic testing for hereditary prostate cancer risk. Urology. 2000;55:46-50.
24. Bratt O, Bamber JE, Emanuelsson M, et al. Risk perception, screening practice and interest in genetic testing among unaffected men in families with hereditary prostate cancer. Eur J Cancer. 2000;36:235-241.
25. National Cancer Institute. The NCI Strategic Plan to Reduce Health Disparities. Bethesda, Md: National Institutes of Health; 1999.
26. Committee on Cancer Research among Minorities and the Medically Underserved, Institute of Medicine. The Unequal Burden of Cancer: An Assessment of NIH Research and Progress for Ethnic Minorities and the Medically Underserved. Washington, DC: National Academy Press; 1999.
27. Ries LA, Wingo PA, Miller DS, et al. The annual report to the nation on the status of cancer, 1973-1997, with a special section on colorectal cancer. Cancer. 2000;88:2398-2424.
28. Yood MU, Johnson CC, Blount A, et al. Race and differences in breast cancer survival in a managed care population. J Natl Cancer Inst. 1999;91:1487-1491.
29. Cancer Facts and Figures: 2001. Atlanta, Ga: National Cancer Society; 2001.
30. Wojcik BE, Spinks MK, Optenberg SA. Breast carcinoma survival analysis for African American and white women in an equal-access health care system. Cancer. 1998;82:1310-1318.
31. Neuhausen SL. Ethnic differences in cancer risk resulting from genetic variation. Cancer. 1999;86(suppl 11):1755-1762.
32. Miki Y, Swensen J, Shattuck-Eidens D, et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science. 1994;266:66-71.
33. Wooster R, Bignell G, Lancaster J, et al. Identification of the breast cancer susceptibility gene BRCA2. Nature. 1995;378:789-792.
34. Roa BB, Boyd AA, Volcik K, Richards CS. Ashkenazi Jewish population frequencies for common mutations in BRCA1 and BRCA2. Nat Genet. 1996;14:185-187.
35. Gao Q, Tomlinson G, Das S, et al. Prevalence of BRCA1 and BRCA2 mutations among clinic-based African American families with breast cancer. Hum Genet. 2000;107:186-191.
36. Chaliki H, Loader S, Levenkron JC, Logan-Young W, Hall WJ, Rowley PT. Women’s receptivity to testing for a genetic susceptibility to breast cancer. Am J Pub Health. 1995;85:1133-1135.
37. Lerman C, Daly M, Masny A, Balshem A. Attitudes about genetic testing for breast-ovarian cancer susceptibility. J Clin Oncol. 1994;12:843-850.
38. Tambor ES, Rimer BK, Strigo TS. Genetic testing for breast cancer susceptibility: awareness and interest among women in the general population. Am J Med Genet. 1997;68:43-49.
39. Schwartz M, Hughes C, Roth J, et al. Spiritual faith and genetic testing decisions among high-risk breast cancer probands. Cancer Epidemiol Biomarkers Prev. 2000;9:381-385.
40. Lerman C, Hughes C, Benkendorf JL, et al. Racial differences in testing motivation and psychological distress following pretest education for BRCA1 gene testing. Cancer Epidemiol Biomarkers Prev. 1999;8:361-367.
41. Hughes C, Gomez-Caminero A, Benkendorf J, et al. Ethnic differences in knowledge and attitudes about BRCA1 testing in women at increased risk. Patient Educ Couns. 1997;32:51-62.
42. Kinney AY, Croyle RT, Dudley WN, Bailey CA, Pelias MK, Neuhausen SL. Knowledge, attitudes, and interest in breast-ovarian cancer gene testing: a survey of a large African-American kindred with a BRCA1 mutation. Prev Med. 2001;33:543-551.
43. Hughes C, Fasaye GA, LaSalle VH, Finch C. Sociocultural influences on participation in genetic risk assessment and testing among African American women. 2002. Paper presented at: the 6th International Symposium on Predictive Oncology and Intervention Strategies; February 2002; Paris, France.
44. Donovan KA, Tucker DC. Knowledge about genetic risk for breast cancer and perceptions of genetic testing in a sociodemographically diverse sample. J Behav Med. 2000;23:15-36.
45. Schwartz MD, Benkendorf J, Lerman C, Isaacs C, Ryan-Robertson A, Johnson L. Impact of educational print materials on knowledge, attitudes, and interest in BRCA1/BRCA2: testing among Ashkenazi Jewish women. Cancer. 2001;92:932-940.
46. Jackson AP, Sears SJ. Implications of an Afrocentric worldview in reducing stress for African American women. J Counsel Devel. 1992;71:184-190.
47. Bowen DJ, Christensen CL, Powers D, Graves DR, Anderson CAM. Effects of counseling and ethnic identity on perceived risk and cancer worry in African American women. J Clin Psychol Med Settings. 1998;5:365-379.
48. Telfair J, Nash KB. African American culture. In: NL Fisher, ed. Cultural and Ethnic Diversity: A Guide for Genetics Professionals. Baltimore, Md: Johns Hopkins University Press; 1996:3659.
49. American Society of Clinical Oncology. Statement of the American Society of Clinical Oncology: genetic testing for breast cancer susceptibility. J Clin Oncol. 1996;14:1730-1736.
50. Peshkin BN, DeMarco TA, Brogan BM, Lerman C, Isaacs C. BRCA1/2 testing: complex themes in result interpretation. J Clin Oncol. 2001;19:2555-2565.
51. Holman EA, Silver RC. Getting “stuck” in the past: temporal orientation and coping with trauma. J Pers Soc Psychol. 1998;74:1146-1163.
52. Brown CM, Segal R. Ethnic differences in temporal orientation and its implications for hypertension management. J Health Soc Behav. 1996;37:350-361.
53. Jones JM. Cultural differences in temporal orientation: instrumental and expressive behaviors in time. In: McGrath JE, ed. The Social Psychology of Time: New Perspectives. Newbury Park, Calif: Sage Publications; 1988:21-37.
54. Bourjolly JN. Differences in religiousness among black and white women with breast cancer. Soc Work Health Care. 1998;28:21-39.