Too Many Referrals of Low-risk Women for BRCA1/2 Genetic Services by Family Physicians

doi:10.1158/1055-9965.EPI-07-2879

Cancer Epidemiol Biomarkers Prev. Author manuscript; available in PMC 2009 November 3.

Published in final edited form as:

Cancer Epidemiol Biomarkers Prev. 2008 November; 17(11): 2980–2986.

doi: 10.1158/1055-9965.EPI-07-2879

PMCID: PMC2772063

NIHMSID: NIHMS67445

Too Many Referrals of Low-risk Women for BRCA1/2 Genetic Services by Family Physicians

Della Brown White,¹ Vence L. Bonham,¹ Jean Jenkins,² Nancy Stevens,³ and Colleen M. McBride¹

¹ Social & Behavioral Research Branch, National Human Genome Research Institute (NHGRI), National Institutes of Health (NIH) Bethesda MD

² Office of the Director, NHGRI, NIH

³ University of Washington School of Medicine, Seattle WA

Corresponding author: Della Brown White, Postdoctoral Fellow, Social and Behavioral Research Branch, NHGRI, NIH, 31 Center Drive, Bldg 31, Room B1B54G, Bethesda, MD 20892-2073, Phone: 301-443-2617; Fax: 301-480-3108; Email: whitede/at/mail.nih.gov

The publisher's final edited version of this article is available free at Cancer Epidemiol Biomarkers Prev

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Abstract

Increasing availability and public awareness of BRCA1/2 genetic testing will increase women’s self-referrals to genetic services. The objective of this study was to examine whether patient characteristics influence family physicians’ (FPs’) referral decisions when a patient requests BRCA1/2 genetic testing. FPs (n = 284) completed a web-based survey in 2006 to assess their attitudes and practices related to using genetics in their clinical practice. Using a 2×2×2 factorial design we tested the effects of a hypothetical patient’s race, level of worry and insurance status on FPs’ decisions to refer her for BRCA1/2 testing. The patient was not appropriate for referral based on USPSTF guidelines. No patient characteristics were associated with FPs’ referral decisions. Although referral was not indicated, only 8% did not refer to genetic services, 92% referred for genetic services, and 50% referred to genetic counseling. FPs regarded it unlikely that the patient carried a mutation. However, 65% of FPs believed if they refused to refer for genetic services it would harm their relationship with the patient. Despite scarce and costly genetic services FPs were likely to inappropriately refer a low-risk patient who requested BRCA1/2 testing. The implications of this inappropriate referral on women’s screening behavior, genetic services, and health care costs are unknown. Clinicians and patients could benefit from education about appropriate use of genetic services so that both are more comfortable with a decision against referral.

Keywords: BRCA1/2 genetic services, physician referral, family physicians, evidence-based medicine, practice guidelines

Introduction

The integration of genomics into clinical practice is forecast to have important benefits for health care delivery and health outcomes (1). BRCA 1 and BRCA 2 (BRCA1/2) testing for familial breast and ovarian cancer is an example of the kinds of testing that will be available clinically. Carriers of BRCA1/2 mutations are at substantially increased risk for breast and ovarian cancer. However, the distribution of BRCA1/2 mutations in the general population is very low, estimated at 1 in 300 to 500 (2). Additionally, hereditary breast cancers account for about 5 to 10% of all breast cancer cases, with BRCA1/2 mutations only contributing to a small fraction of these cases (3). One study reported that within an average general practitioner’s caseload of 1700 patients, only 140 patients would be estimated to have a family history of breast, colorectal or breast/ovarian cancer, and 10 of these patients would be considered appropriate for referral to genetic counseling based on well-defined risk criteria (4).

Direct-to-consumer marketing of BRCA1/2 testing and American women’s tendency to overestimate their risks of breast cancer (5) create consumer demand as women “self refer” to primary care clinicians and request genetic testing (6–9). Traditionally, genetic testing is provided in the context of appropriate genetic counseling or education; yet, clinical genetic services in the U.S. remain relatively scarce (10–12). The low prevalence of BRCA1/2 mutations means that in the majority of self-referral situations, primary care clinicians will be in the position of having to dissuade low-risk women from BRCA1/2 counseling and testing. This will put considerable pressure on clinicians to make appropriate referrals.

Inappropriate referral to BRCA1/2 testing also could have significant implications for health care costs and service delivery. Results of Myriad Genetics Laboratories’ direct-to-consumer marketing campaign for BRACAnalysis® lead to a 240% increase in the number of referrals to genetic services within managed care settings (6,7) creating delays in patient access to these services (6). At $3,000 per test in the U.S., BRCA testing and supportive genetic counseling is a significant expenditure of resources (13).

Moreover, the patient-clinician conversations required to clarify why a patient is or is not appropriate for genetic service referral may increase visit time in ways that do not directly benefit patient care. This may be particularly true in circumstances in which women present with heightened worry and misperceptions about the factors that contribute to their risk. Insurance status also may further complicate these conversations when women, with health care insurance believe that they have the right to services even if they are not appropriate.

Biases such as under-referral of minority women to BRCA1/2 services also could occur in ways that exacerbate existing racial/ethnic disparities in health delivery (14–17). Patient characteristics such as age, race and gender have been noted as reasons for patients not receiving clinically recommended services (16). However, evidence to date suggests that patient demands for clinical services (18,19), including cancer susceptibility testing (20,21) are likely to be granted even when deemed inappropriate by the physician (19,22). Reasons for these patterns of inappropriate referral have included physician concerns about patient satisfaction and fears of malpractice (23).

To this end, the US Preventive Services Task Force (USPSTF) published guidelines in late 2005 to assist clinicians in determining which patients are appropriate for referral to genetic counseling and testing for BRCA1/2 mutations (24). These guidelines recommend against routine referrals of low-risk women to BRCA1/2 genetic services. While clinicians have indicated favorable attitudes towards practice guidelines (25), concerns have been raised that guidelines can be too rigid and impractical to incorporate and interfere with physician autonomy, (26–28). Further, clinicians may have difficulty applying the USPSTF referral guidelines because they have low levels of confidence in their ability to calculate breast cancer risk and related counseling (4,29,30). Physicians also lack confidence in their ability to discuss mammography screening and to decide whether a patient should be referred for genetic counseling (4,30).

Family physicians (FPs) who provide the majority of primary care in the U.S. (31) will be fielding the majority of self-referral for BRCA1/2 testing. Thus, FPs’ adherence to USPSTF guidelines has significant implications for the impact of self referral on genetic services and breast cancer screening more generally. FPs’ competence in considering women’s concerns about breast cancer has broader implications for cancer control. For example, inappropriate referral could influence women’s adherence to screening guidelines if they misunderstand indications from their doctors that they are unlikely to have increased familial risk.

This report describes results of an experiment where via a web-based survey, FPs were presented with a hypothetical patient named “Terry” who requests genetic testing but is not appropriate for referral based on USPSTF guidelines. The experiment also tested whether varying “Terry’s” personal characteristics influenced FPs’ referral decisions for BRCA1/2 testing.

Materials and Methods

Study Design

A cross-sectional 2×2×2 factorial design was used. All FPs viewed a hypothetical patient named “Terry” who presents for her annual exam and requests genetic testing for breast cancer. The vignette describes “Terry’s” request as being prompted by her sister’s recent diagnosis of breast cancer at age 53 and provided a description of “Terry”, including her age, health status, family history of cancer, ethnicity (Not Ashkenazi Jewish) and results of the previous year’s mammography results. Physicians were randomized to see one of eight variations of the vignette based on the three experimental factors: (a) level of worry (high vs. not high), (b) insurance status (insured vs. not insured) and (c) race (black vs. white as indicated by the picture provided with the vignette - see Figure 1). In each vignette “Terry” was not appropriate for referral to BRCA1/2 genetic services based on the USPSTF guidelines (24); the estimated prevalence of BRCA1/2 mutations in women with the same health history as “Terry” is 2.8% and 2.9% for “Terry’s” sister (32).

Figure 1

Example of web page used to present the hypothetical scenarios to physicians. This experimental description of “Terry” is black race, insurance, high level of worry.

After reading the vignette, physicians were asked a series of questions that included their decision regarding whether or not to refer “Terry” to genetic services. For these questions, physicians were not allowed to scroll back to the page with the patient description. Participants who completed the follow-up survey were entered into a lottery to receive one of six iPods. The study procedures were approved by the Institutional Review Boards at the National Human Genome Research Institute and the American Academy of Family Physicians.

Sample

The sample for this report was drawn from a longitudinal survey of members of the American Academy of Family Physicians (AAFP) conducted to evaluate the AAFP’s Annual Clinical Focus on Genomics in January 2005. First, a random stratified sample of 10,000 AAFP members was drawn such that half of the sample had completed residency less than fifteen years ago; a total of 1035 FPs completed this web-based survey (10% response rate). Compared to the AAFP membership as a whole, FPs who completed the first survey were significantly more likely to be working in teaching hospitals compared to the AAFP membership as a whole (18% vs. 9%, respectively). At the end of this survey FPs who completed the survey were asked to provide personal identifiers that would enable them to be re-contacted for a similar survey a year hence.

A total of 694 of the 1035 FPs (67%) agreed to be re-contacted via e-mail to complete the follow-up survey. E-mails were sent to inform these FPs that they could log onto a web-site, review brief consent information and complete a follow-up survey between May 8, 2006 and June 2, 2006. Two email reminders went to each participant; one at seven days after the broadcast email, and the other at 14 days after the broadcast email. The final sample included the 284 physicians (27% response rate) who completed questions related to the referral of “Terry” to genetic services. This sample size enables us to detect effects of the experimental manipulation that are in the small to medium range of standardized effect sizes with 80% power at the p < .05 level of significance (33). Analyses were conducted in fall 2006.

Measures & Survey Items

Demographics and practice characteristics

Gender and time out of residency were obtained from AAFP membership records. Self-identified race and practice characteristics (including approach to work, teaching/training environment, urban setting or not, the proportion of non-white residents and residents living in poverty) were assessed in the initial web-based survey.

Referral decision

FPs were asked the following question: “How likely are you to refer “Terry” to the following services considering the circumstances described? (neither genetic testing or genetic counseling, both genetic testing and genetic counseling, genetic testing as she requests, genetic counseling, or other).”

Attitudes about the referral decision

FPs were asked two questions: (a) “How sure are you that your decision about this referral is the best clinical decision?” (b) “How sure are you that your decision about this referral is an optimal use of genetic services?” For each question FPs rated their responses on a scale of 1 (not at all sure) to 7 (extremely sure).

Factors important in referral decision

FPs were asked to rate the importance of patient characteristics (e.g., “Terry’s” race, age, sister’s age at diagnosis) in their referral decision on a scale of 1 (not at all important) to 7 (extremely important). FPs also were asked the extent to which they agreed or disagreed with the following: “If you refuse to refer “Terry” for genetic counseling or testing, it will harm your relationship with her.” FPs rated their agreement using a 5-point Likert scale (strongly disagree, disagree, neither agree nor disagree, agree, strongly agree). FPs’ opinions about “Terry’s” level of risk for breast cancer were assessed with the following two questions: (a) “What do you think is the likelihood that “Terry” has a genetic mutation that increases her risk for breast cancer?”; (b) “How would you rate “Terry’s” level of breast cancer risk?” FPs responded on a scale of 1 (very low) to 7 (very high).

Value of referral to genetic services

FPs were asked a series of questions to assess their opinions about the value of referring “Terry” to genetic counseling (e.g., “Terry” could get needed reassurance from your referral for genetic counseling even if she isn’t appropriate for testing”), and for genetic testing (e.g., “There’s no harm in referring “Terry” for genetic testing even if she isn’t really appropriate for testing”). FPs rated their responses using a 5-point Likert scale (strongly disagree, disagree, neither agree nor disagree, agree, strongly agree).

Statistical Analyses

Means and proportions were computed to describe the distribution of survey items. Contingency tables were used to examine the bivariate relationships among the three experimental factors (a) level of worry (high vs. not high), (b) insurance status (insured vs. not insured) and (c) race (black picture vs. white picture) and outcome variable of interest (i.e., FP’s referral decision). Multivariable polytomous logistic regression models were used to test the association of the three experimental dichotomous factors on FP’s referral decision. Throughout this report p<0.05 is used as the criterion for statistical significance.

Results

Sample characteristics

FPs who completed the follow-up survey were predominantly non-Hispanic White physicians (87%) and male (71%); most practiced in urban areas (65%), half were more than 15 years out of residency and one-third were currently working in a teaching or training environment. About half reported practicing in a clinic where more than 15% minority patients, and 43% practiced in a clinic where more than 10% of residents lived in poverty. FPs who completed the first and second surveys were demographically similar (e.g., male: 67%, 71%, respectively, preferred innovative practice: 61%, 66%, respectively, and practiced in a teaching environment: 30%, 35%, respectively).

Experiment outcomes

FPs’ referral decisions were not associated with “Terry’s” level of worry (p = 0.89) insurance status (p = 0.99) or race (p = 0.65). Although “Terry” was not appropriate for referral to BRCA1/2 genetic services, only 8% of FPs made a decision against referral (See Figure 2). Thus, 92% of FPs made a referral decision inconsistent with the USPSTF guideline. Half reported they would refer “Terry” for genetic counseling only, 23% said they would refer her to both genetic testing and counseling, 13% would refer “Terry” directly to genetic testing as requested and 6% of participants noted they would make a decision other than those presented such as asking to have “Terry’s” sister tested for BRCA1/2.

Figure 2

FPs’ decisions to refer “Terry” to genetic services.

Manipulation checks on the experimental factors showed that FPs accurately recalled the details of “Terry’s” age, race, and emotional status. Fifty nine percent of FPs accurately recalled that “Terry’s” age was below 50, 94% of FPs who saw a White “Terry” identified her race as White, and 70% who saw a Black “Terry” indicated that she was Black. FPs who saw the “High Worry Terry” rated her as significantly more nervous (p<0.001) and afraid (p<0.001), than those for whom “Terry” presented without mention of worry.

Explanations for non-guideline recommended referral decisions

To better understand factors that might underlie the referral decisions of the 260 FPs who indicated a decision inconsistent with referral guidelines, we explored FPs’ beliefs about the appropriateness of their referral decision (See Table 1). FPs perceived “Terry’s” risk for breast cancer to be moderate (mean = 4.2, SD = 1.1); but regarded her risk of having a genetic mutation as relatively low (mean = 2.8, SD = 1.4). FPs reported being relatively sure that their referral decision was the best clinical decision (mean = 4.8, SD = 1.4) and an optimal use of genetic services (mean = 4.5, SD = 1.5). FPs rated “Terry’s” level of emotional distress (mean = 5.5, SD = 1.2, scale 1–7) and her sister’s age at diagnosis (mean = 5.1, SD = 1.5, scale 1–7) as important factors in their referral decision. “Terry’s” race (mean = 3.2, SD = 1.7) and insurance status (mean = 3.4, SD = 1.9) were less important factors in their decision.

Table 1

Beliefs about the appropriateness of referral decision among physicians who reported non-guideline recommended referral decisions for “Terry” (n = 260)^*

We also explored FPs’ beliefs about the costs and benefits of their referral decisions (See Table 2). The majority of FPs agreed “Terry” would be likely to benefit from genetic counseling, could get needed reassurance from the referral to genetic counseling even if she was not appropriate for testing, and that there was no harm in referring “Terry” for genetic counseling even if she was not appropriate for testing. Reponses to the likelihood of benefit from referral to genetic counseling and benefit from referral to genetic testing were significantly associated (χ² = 7.45, df = 1, p = 0.01). Those who indicated “Terry” could benefit from testing were significantly more likely to say she would benefit from counseling as well, whereas the reverse was not the case. Most respondents (65%) believed that refusing “Terry’s” request might harm their relationship with her. FPs who decided to refer “Terry” were more likely to agree that refusal to refer “Terry” would harm the relationship than those who did not refer “Terry” on for genetic services.

Table 2

Beliefs about the costs and benefits of referral decisions among physicians who reported non-guideline recommended referral decisions for “Terry” (n = 260)^*

Discussion

USPSTF guidelines recommend against routine referrals of low-risk women for BRCA1/2 genetic services (24). The patient in this report did not meet the guidelines for referral. Yet, 92% of FPs chose to refer her to genetic services. No presenting characteristics (e.g., level of worry, insurance status, race) were associated with the referral decision.

Most FPs believed that the decision to refer was an optimal use of genetic services suggesting that they may underestimate the “costs” of referral. Indeed, although Myriad’s direct-to-consumer marketing campaign increased referrals to genetic services by 240%, the majority of physicians in the market area perceived that the campaign had no impact on clinical practice (6,7). Moreover, the majority of women referred by physicians reported having delays of over six months to access genetic services (6). Referral of low-risk women could create a bottleneck in getting services to high-risk women who stand to benefit most.

Our results also suggest that FPs made referral decisions, in part, to preserve their relationship with the patient. Similarly, previous research suggests that cancer susceptibility testing is more likely to be ordered when directly requested by patients (20,21). Moreover, direct-to-consumer advertising consistently has been associated with increased patient demand in the form of more requests for prescriptions (34) and other clinical services (22). The fact that these requests frequently are granted even when clinicians deem them to be clinically inappropriate suggests that physicians may need additional support in declining patient requests (19,22).

In the case of “Terry”, FPs may have struck the balance between “Terry’s” request for genetic services and their belief that “Terry” was unlikely to have a BRCA1/2 mutation by referring her to genetic counseling rather than genetic testing. For example the challenge of helping women discriminate genetic risk from other risk factors such as age may have seemed more suited to a genetic counseling session than the primary care visit.

Further, the FP’s instinct to refer “Terry” to genetic counseling may have been an appropriate response to their lack of confidence in their abilities to do genetic risk assessment or their concerns about the time it would take to adequately assess risk and provide related counseling. In this circumstance, referral to genetic counseling may have been viewed by the FP as the only feasible alternative. This dilemma suggests the need to provide providers and patients with educational tools and decision aids on the appropriateness of BRCA1/2 testing. For example, an interactive computer-based decision aid designed to educate women about breast cancer genetic services has been shown to be beneficial in increasing breast cancer and genetic testing knowledge and reducing intentions to test and risk perception among low-risk women (35). Additionally, hotlines also have been employed to this end. The National Cancer Institute’s Atlantic Region Cancer Information Service implemented an educational intervention using the 1-800-4-CANCER line (36). Results at six months indicated that average risk women reported decreased intentions to test and high risk women reported increased intentions to test. Hence, additional research is needed to evaluate these services in supporting physicians and patients to make decisions about BRCA1/2 testing.

Additionally, physicians need to gain greater familiarity and understanding of what risk factors deem women to be at high genetic risk for breast cancer. FPs reported the age of “Terry’s” sister at diagnosis as one of the most important factors in their decision to refer “Terry” to genetic services. “Terry’s” sister’s age was not consistent with USPSTF referral guidelines (i.e., < 50 yrs at age of diagnosis). Previous research also has noted the lack of physician knowledge about factors important in risk assessment and appropriate referrals for BRCA1/2 testing (8,9,29,37) and cancer susceptibility testing in general (20,21). Additionally, patients too could benefit from education on familial breast and ovarian cancer and related genetic testing to further enhance appropriate requests and referrals to genetic services. The services described above could be useful in raising such awareness.

Several limitations of the study must be considered in interpreting these results. Data are cross-sectional and the direction of the associations can not be established. The response rate to the initial survey was relatively low, although the initial and follow-up survey participants appeared to well represent the larger AAFP membership (38). However, this self-selected sample of FPs who participated was inclined toward innovation and thus may have included those who were most likely to be knowledgeable of and receptive to genetic innovations in clinical care. Thus these results may overestimate readiness to refer.

Additionally, the USPSTF guidelines for referral to BRCA1/2 genetic services were published less than one year prior to the follow-up survey (24). Over 90% of FPs in this sample reported having heard of USPSTF however we did not assess whether FPs were aware of the new guidelines specific for BRCA1/2 referral. Future studies should assess awareness of guidelines to help differentiate whether physicians are making referral decision despite knowing practice guidelines. Further, more research is needed to assess how the letter grades used to define USPSTF guidelines may influence clinician referral behaviors. Adherence to guidelines may be influenced by physicians’ perceptions about the validity of the data used to devise the guidelines. FPs’ responses also were based on a hypothetical scenario and may not accurately reflect how they actually would respond in a clinical setting. Prospective studies with real patients that incorporate medical chart reviews are needed to increase the validity of physician responses and more accurately assess referrals rates.

When considering whether genomic medicine has the potential to improve health care delivery and patient health outcomes, it will be important to understand how factors such as patient characteristics, direct-to-consumer advertising, physicians’ knowledge of genetics and adherence to guidelines might influence health care delivery and health disparities. Inappropriate referrals of patients at low risk for carrying genetic mutations to limited genetic professional services could hinder access to these services by high-risk patients and increase out-of-pocket costs to patients. This is especially true for the future of cancer prevention and control as we move towards the dissemination of genetic susceptibility testing not only for rare, hereditary cancers but also more common “sporadic” cancers which contribute to a greater public health burden (39–41). To maximize appropriate referral for genetic services, research should focus on the role of clinician-patient relationships in referrals, patient education and clinician training in genetic risk assessment and counseling skills.

Acknowledgments

This research was supported [in part] by the Intramural Research Program of the National Human Genome Research Institute, National Institutes of Health. The content is solely the responsibility of the authors and does not necessarily represent the official views of the NHGRI or NIH. We thank the American Academy of Family Physicians for partnering with us in this research. We express our gratitude to Cristopher Price and Amanda Parsad for their statistical expertise and the team lead by Donald Dorfman at Esprit Health for designing the website. We thank Dr. Alan Guttmacher and Dr. William Feero for their comments on an earlier version of this manuscript. We are very grateful to all of the physicians who participated in this study.

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