Racial Differences in Beliefs about Genetic Screening among Patients at Inner-City Neighborhood Health Centers

Richard K. Zimmerman, MD, MPH; Melissa Tabbarah, PhD, MPH; Mary Patricia Nowalk, PhD, RD; Mahlon Raymund, PhD; Ilene K. Jewell, MS Hyg; Stephen A. Wilson, MD; and Edmund M. Ricci, PhD, MLitt Pittsburgh, Pennsylvania

Financial support: This project was funded by P01 HS 10864 INTRODUCTION from the Agency for Healthcare Research and Quality and Racial disparities have been observed in a variety 1 P60 MD000207-01 from the National Institutes of Health. of diseases, including cancer incidence and death rates, obesity prevalence and mellitus.'-3 Background: has the potential to identify per- Unfortunately, racial disparity also occurs in use of sons at high nsk for disease. Given the history of racial dispari- medical services, including screening for certain ties in screening, early detection and accessing treatment, cancers and immunizations." 45 The obvious question understanding racial differences in beliefs about is is why these disparities occur. Unequal access to essential to preventing disparties in some condifions. care is clearly one reason;6'7 differing cultural Methods: In 2004, a sample of older adult pafients from four beliefs, values and trust in the medical system are inner-city health centers was surveyed to assess beliefs other reasons.8"9 about genetic determinants of disease, genetic testing and Many diseases have a genetic basis and among religion. Logistic regression determined which beliefs were high-risk groups genetic screening, at least in part, associated with race. has the potential to identify who might benefit from Results: Of the 314 respondents, 50% were African Ameri- early counseling and screening. Genetic testing may cans. Most respondents thought that , cys- also help in treatment decisions by identifying which tic fibrosis and diabetes are primanly genetic. African Ameri- patients are more likely to respond to certain treat- cans were more likely than Caucasians to believe that ments or by identifying pathways for drug metabo- genetic testing will lead to racial (Odds ratio lism. However, participation in genetic screening is a (OR): 3.02,95% confidence interval (C:1} 1.5-6.0) and to think complex decision that involves knowledge about that all pregnant women should have genetic tests (OR=3.8, genetics, knowledge about genetic screening, ethical 95% Cl: 1.7-8.6). African Amer'cons were more likely to and religious values, and concerns about discrimina- believe that God's Word is the most important source for tion.'"'1 Some studies show racial differences in moral decisions (OR: 3.6, 95% Cl :1.5-8.7).1 beliefs about genetic testing and racial disparities in Conclusion: African Americans and Caucasians differ in the actual uptake of genetic testing.'2"'3 Understanding beliefs about genetic testing and the basis for moral deci- such differences is essential for a just distribution of sion-making. Acknowledging and understanding these dif- resources and to respect for differing values. ferences may lead to better medical care. The purposes of this paper were to identify racial differences in beliefs about the causes of diseases Key words: African Americans * genetics U ethics * beliefs whose etiology is environmental (e.g., exposure to * disparities * genetic testing influenza virus), genetic (e.g., sickle cell disease) or a © 2006. From the Department of Family Medicine and Clinical Epidemiology, combination (obesity), and to explore racial differ- University of Pittsburgh School of Medicine (Zimmerman, Tabbarah, Nowalk, ences in beliefs about genetic testing, ethical and reli- Raymund); the Department of Behavioral and Community Health Sciences, gious values and concerns about discrimination. Our Graduate School of Public Health (Jewell, Zimmerman, Ricci); and UPMC St. approach included both exploration and hypothesis Margaret Family Health Center (Wilson), Pittsburgh, PA. Send correspon- testing of racial differences in these items. The popu- dence and reprint requests for J NatI Med Assoc. 2006;98:370-377 to: Dr. Richard Kent Zimmerman, Department of Family Medicine and Clinical lation consisted of older adult patients attending four Epidemiology; University of Pittsburgh School of Medicine; 3518 Fifth Ave., inner-city health centers that serve the economically Pittsburgh, PA 15261; phone: (412) 383-2354; fax: (412) 383-2306; e-mail: disadvantaged, high proportions of minority patients [email protected]; web site: www.pitt.edu/-familymd/immunization/ and those with limited healthcare options.

370 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 98, NO. 3, MARCH 2006 RACIAL DIFFERENCES IN BELIEFS ABOUT GENETIC SCREENING METHODS seen at one of the health centers in the last year and who continued to participate in our studies.'4 A per- Sample and sonalized introductory letter and a letter from the In 2004, we surveyed by telephone patients from health centers endorsing the project and encourag- four inner-city health centers. These centers were ing participation were sent to each of the sampled included because they were known to serve large patients. A $10 honorarium was offered for complet- numbers of persons of color and of disadvantaged ing the survey. Of the panel, 248 participated, 14 persons and were willing to implement quality refused and 15 were ineligible-for a response rate improvement initiatives. Most ofthese patients were of 80% [248/(325-15)]. This panel was augmented part of a panel of 325 persons that was initially by a convenience sample that, following HIPAA selected from a random sample (of billing records) guidelines, was recruited by the sites using an intro- of patients who were 250 years old and had been ductory letter and recruitment sheet that was distrib-

Table 1. Patient characterisfics Overall Caucasians African Americans (n=314) (n=157) (n=157) Variable % % % P Value Age (%7) 50-64 52 52 52 65+ 48 48 48 1.00 Female (%) 72 63 80 <0.001 Marital Status (76) Married 30 41 20 Widowed 30 27 32 Never married 11 11 10 Separated/divorced 30 21 38 <0.001 Level of Education (%5) Some college education or more 40 48 33

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 98, NO. 3, MARCH 2006 371 RACIAL DIFFERENCES IN BELIEFS ABOUT GENETIC SCREENING uted by office staff during visits. Among these 104 characteristics, including race, health behaviors, new recruits, 83 interviews were completed, 0 attitudes and beliefs regarding genetic determinants refused and one was ineligible-for a response rate of disease, genetic testing and religious beliefs as of 81% (83/103). As such, the total sample for this they relate to genetic testing. Given the exploratory study was 331 patients. nature ofthe study and the desire to investigate ethi- cal concerns, we did not focus on a particular behav- Survey Questionnaire ioral theory. However, we have been influenced by The items in the questionnaire and the layout and previously used the Theory of Reasoned were designed by a multidisciplinary team using an Action-particularly the components related to iterative process after a review of literature about beliefs and attitudes about outcomes."5 The final ethical concerns about genetic testing. Items on the questionnaire included approximately 36 multiple- questionnaire assessed self-reported demographic choice and three-point Likert scale questions related

Table 2. Percent of respondents who attribute disease to , the environment, neither or both, by race African Overall* Caucasians Americans Disease (n=314) (n=157) (n=157) P Valuet Sickle Cell Anemia Genes 88 88 88 Environment 1 1 1 Both 4 4 5 Neither 6 7 5 0.859 Cystic Fibrosis Genes 75 80 70 Environment 4 2 8 Both 22 12 10 Neither 9 7 13 0.044 Cancer Genes 32 26 39 Environment 9 9 10 Both 46 58 34 Neither 12 8 17 <0.001 Obesity Genes 31 25 37 Environment 14 14 14 Both 43 52 35 Neither 11 9 13 0.023 Diabetes Genes 61 51 71 Environment 6 5 6 Both 26 36 17 Neither 7 7 6 <0.001 Alcoholism Genes 27 23 32 Environment 20 18 22 Both 40 48 33 Neither 12 11 13 0.079 The Flu Genes 3 3 3 Environment 69 64 74 Both 12 17 8 Neither 16 16 16 0.121 * May not add up to 100% due to rounding; t P value by Fisher's exact test

372 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 98, NO. 3, MARCH 2006 RACIAL DIFFERENCES IN BELIEFS ABOUT GENETIC SCREENING to this paper, depending on skip patterns. tests in the case of small cell counts). Logistic regres- From August to October 2004, telephone surveys sion analysis was performed to determine variables of this sample were performed by trained interview- significantly associated with race. In this multivariate ers using computer-assisted telephone interviewing model, we included as independent variables all vari- (CATI) permitting direct data entry during the inter- ables associated in bivariate analyses with the view."6 The CATI system managed the sample of dependent variable at the P<0.10Ilevel or if specified persons to be contacted-that is, it randomly a priori (i.e., age). Because attitude about genetic test- assigned people to be contacted to each interviewer ing specific to was highly corre- and recorded the outcome ofattempts to reach them. lated (r=0.58, P<0.001) with the attitude about genet- The CATI system also directed question sequence, ic testing specific to the handicapped, we only reduced unintentionally skipped questions and pro- included the former variable in our multivariate mod- vided automatic range checks. el. Although we tested for interactions between edu- cation group and each attitude in our model, no sig- Statistical Analysis nificant interactions were found. All statistical In order to specifically study racial differences analyses were performed using SAS 8.2 statistical between African Americans and Caucasians, we used software (SAS Inc., Cary, NC). Statistical signifi- race as an outcome variable, as has been done else- cance was set at P<0.05 and data were unweighted. where,1 and excluded the 17 questionnaires from par- This project was approved by the Institutional ticipants who reported that they were neither African- Review Board ofthe University ofPittsburgh. American nor Caucasian. Attitudes about genetic testing were dichotomized into "agree/neutral" or RESULTS "disagree." We chose these categories because only 1-5% ofparticipants gave "neutral" responses to spe- Demographics cific attitudinal items. Bivariate associations were Fifty percent of the respondents were African- examined using Chi-squared tests (or Fisher's exact American and 50% Caucasian. Distributions for sex,

Table 3. Attitudes* on genetic testing by race African Overall Caucasians Americans Attitudes on Genetic Testing (7o) (n=314) (n=157) (n=157) P Valuet Genetic testing to check for risk of getting a disease is a good idea 90 90 90 0.865 Employers should be able to see the results of genetic testing before hiring workers 29 26 30 0.358 Genetic testing will lead to racial discrimination 47 34 58 <0.001 Genetic testing will lead to discrimination against the handicapped 55 47 64 0.003 Research on genetics will bring cures for many diseases 94 93 95 0.637 Research on genetics is tampering with nature and unethical 25 17 31 0.003 All pregnant women should have tests to look for genetic problems in the baby 70 58 79 <0.001 Only pregnant women who want to should have tests to look for genetic problems in the baby 81 81 79 0.709 A pregnant woman whose baby has an abnormal genetic test should have an abortion 23 20 24 0.378 People should be able to use genetic testing to select the sex of their children 17 17 14 0.517 * Includes only patients who gave "agree" and "neutral" responses; t P value by Chi-squared test

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 98, NO. 3, MARCH 2006 373 RACIAL DIFFERENCES IN BELIEFS ABOUT GENETIC SCREENING marital status, level ofeducation, household income, found for four ofthese diseases: cystic fibrosis, can- self-rated health, likelihood of having a physical cer, obesity and diabetes (Table 2). examination within the last year, religion and reli- gious influence differed significantly between races Aftitudes about Genetic Testing (Table 1). Interestingly, a higher percentage of Most (>90%) respondents thought that genetic African Americans thought God's Word was the testing is a good idea and that research on genetics most important source for moral decisions than did would bring cures for many diseases (Table 3), while Caucasians (79% vs. 56%, P

Table 4. Demographics, health and attitudes about predictive genetic testing among African Americans compared with Caucasians African Americans vs. Caucasians Variable Odds Ratio 95% Confidence Interval P Value Age 50-64 years (ref., 65+ years) 1.78 0.57-2.43 0.657 Female (ref., male) 1.30 0.59-2.82 0.515 Some college education or more (ref.,

374 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 98, NO. 3, MARCH 2006 RACIAL DIFFERENCES IN BELIEFS ABOUT GENETIC SCREENING on genetic testing was tampering with nature and to certain diseases would provide a basis for block- thereby unethical, and more likely to agree that all ing access to societal benefits, such as health insur- pregnant women should have genetic tests. Although ance or employment.28 Such concerns are not African Americans were less likely to identify them- unfounded.28 For example, Murray and Herrnstein, selves as Christian/Catholic/Orthodox, African in The Bell Curve, suggest that African Americans Americans remained more likely to believe that are less intelligent by nature and thus, less worthy of God's Word was their most important source for government programs.29 Although the limitations moral decisions. and of their methodology have been widely discussed, their conclusions are additionally disturb- DISCUSSION ing because of the implication that intelligence is a As indicated in Table 4, lower perceived health major measure ofhuman worthiness and value. Lef- status, belief that genetic testing will lead to racial fel has rightly stated that, "Any type of discrimina- discrimination, belief that all pregnant women tion that is connected to one's genetic endowment should have genetic tests, and beliefthat God's Word represents a gross misuse of scientific research."30 is the most important source for moral decisions Indeed, the ethics of distributive justice indicate that were significantly associated with race when con- all should have equal access. A committee of the trolling for other factors. National Academy of Sciences found that, based on The perception of lower health status among the the principles of autonomy, privacy, confidentiality African-American respondents is not surprising for and equity, disclosure of genetic information and several reasons. First, racial disparities occur in genetic testing should not be mandated.28 However, many diseases, including cancer incidence and mor- the National Academy of Sciences notes that their tality, AIDS incidence, obesity prevalence, and dia- position is in conflict with some current practices in betes mellitus incidence and prevalence.'-3 Second, insurance, such as life insurance, for which com- unequal access to care due to lack of insurance or plaints about genetic discrimination have occurred.28 inability to pay, is clearly another reason.6'7 Third, The third area of concern about genetic testing minorities may participate in medical care less fre- among African-American respondents is racial dis- quently due to greater distrust of and less satisfac- crimination in employment. Approximately one- tion with the medical system. Published studies that third of respondents in our study thought employers have explored the role of trust in participation in should be able to see the results of genetic testing medical treatment and/or research have indicated before hiring workers. Carrier frequencies for mark- that African Americans have expressed far less trust ers ofincreased susceptibility to diseases from occu- in healthcare providers than Caucasians.17-21 pational chemical exposure have been documented The finding that this sample ofAfrican Ameri- to vary by race.31 On the positive side, such testing cans' fears that genetic testing would lead to racial could assist employers in reducing occupational discrimination is understandable given that African exposures among those at higher risk for disease, in Americans perceive racial discrimination in other decreasing liability risks, or in reducing health areas of medical care. For instance, discrimination insurance costs.32'33 However, employers might has been reported among those waiting for kidney refuse to hire or terminate persons determined to be transplantation and, in quality of healthcare, among at higher risk of certain diseases associated with hospitalized cardiac patients.21'22 Concern about dis- occupational exposures.32'33 Genetic testing also crimination is most associated with the Tuskegee could be used to determine those at higher genetic syphilis study, where it has been most widely publi- risk for nonoccupational diseases, thereby allowing cized but actually predates the Tuskegee inci- employers to determine who would result in higher dent.9'23'24 From this work and that of others, we insurance costs.34 Because ofgenetic differences, the believe that concerns about racial discrimination risk for a number-of diseases varies by race; there- resulting from genetic testing focus on three areas: fore, racial disparities could occur if genetic testing 1) racially based population control, 2) insurance, became part ofemployment decisions. and 3) employment. Historically, the move- Given the concerns raised by these respondents ment in the United States and Europe25'26 has given about racial discrimination, we were surprised that rise to fears of racial discrimination based on genet- more African Americans than Caucasians thought ics and racially based population control. A fear of that all pregnant women should have genetic testing. genocide9'24'27 is another concern expressed in the On the other hand, similar percentages of respon- medical and lay literature related to sickle cell dents of each race thought that only those pregnant screening programs and to the use of contraceptives women who wanted tests to look for genetic prob- in the African-American population.9'27 lems should have them. In another study ofyounger A second concern is that genetic predispositions women, African Americans report more acceptance

JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION VOL. 98, NO. 3, MARCH 2006 375 RACIAL DIFFERENCES IN BELIEFS ABOUT GENETIC SCREENING of having a child with Down's syndrome than other more difficult to reach than socioeconomically races and are much less likely to consider abortion advantaged groups. The survey response rate was for Down's syndrome in either the first (23% vs. 80%, although we cannot differentiate respondents 80% for whites) or second (11% vs. 76% for whites) and nonrespondents in part due to HIPAA privacy trimester.35 Furthermore, African Americans are issues preventing release ofnonrespondent data. Due more likely to report as very important avoidance of to the sampling process-that is, a random sample any risk of miscarriage than are women of other augmented by a convenience sample-the results races (i.e., whites, Latinas, Asians and Pacific cannot be generalized beyond this sample. Given that Islanders).3" Our divergent findings may be due to the majority of persons (70% ofAfrican Americans the age ofour sample (.50 years). We offer two pos- and 51% of Caucasians) had incomes <$20,000, sibilities to explain the apparent differences between interpretations should account for this fact. our findings and those in the literature. First, given Several suggestions could be made for future the age of our sample, prenatal genetic testing was studies. First, qualitative data may offer insight into unavailable during their child bearing years. Second- beliefs not ascertained from quantitative studies. ly, they may wish to be aware of sickle cell dis- Qualitative data would better inform the breadth of ease-given the publicity about it-and to prepare beliefs and concerns about genetic testing in differ- for potential problems found by testing. We found ent populations, including religious concerns from that African Americans aged .50 more frequently various faith traditions. Areas for study in relation to cited "God's Word" as an important source for moral genetic screening and engineering include beliefs decisions than did Caucasians. We cannot generalize regarding the sanctity of life (e.g., humans as bear- to younger African Americans outside our sample. ers of the image of God, abortion and ); Our findings that 76% ofpeople (83% ofblacks and consequences ofgenetic enhancement and germ line 69% of whites) feel religion influences their lives changes; potential for further discrimination, includ- "quite a lot" support prior studies that religion ing political tyranny; the abilities and limitations of affects decisions about health and healthcare servic- humans; the causes of suffering; the meaning of ill- es.36-40 For instance, a study of women with breast ness, death and the afterlife; safety (e.g., balance of cancer found that African-American women rely on nature); impact on parent-child relationships; and religiousness as a coping resource to a greater extent definitions of kinship. Second, future studies may than Caucasians.37 To exclude religion from discus- wish to incorporate theoretical models such as the sions about genetics may reflect cultural insensitivi- Precaution-Adoption Process to understand an indi- ty and run the risk of increasing racial disparity. A vidual's choices about genetic screening.42 Third, a review of ethical concerns about genetic interven- population-based study of larger numbers and more tions published in religious literature found the most diverse socioeconomic strata would lead to better frequently mentioned concerns were family generalizability and greater opportunities to com- values/parent-child relationships, political tyranny, pare both racial and socioeconomic differences at sanctity of life/abortion and reductionism/human the same time. dignity.4' Other concerns in the religious literature included racial discrimination, "playing God," con- CONCLUSION fidentiality, impact on biodiversity/ pool and Low-income African Americans are more likely possible military abuses.4' Therefore, ignoring or than whites to believe that genetic testing will lead dismissing the active role of religious beliefs with to racial discrimination and to believe that God's regard to health issues may be perceived as disre- Word is their most important source for moral deci- spectful or culturally insensitive. sions. Clinicians and those responsible for public Race and ethnicity are complex concepts, involv- policy regarding genetics and health should recog- ing aspects that are social constructions as well as nize the importance of such racial differences. Fail- those that are genetic. In our study, race was self- ure to address concerns about racial discrimination selected by the respondent using the race and ethnic- and beliefs about the importance of God's Word ity designation options required for research spon- could lead to further mistrust and/or avoidance of sored by the U.S. government. Our findings should the healthcare system in general and genetic testing be interpreted in this context. in particular, with the ultimate result of increased racial disparities. Strengths and Limitations Strengths of this study include the use of comput- REFERENCES er-assisted telephone interviewing and a large number 1. Ward E, Jemal A, Cokkinides V, et al. 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