“For All My Family's Sake,I Should Go and Find Out”: An Australian Report on Genetic Counseling and Testing Uptake in Individuals at High Risk of Breast and/or Ovarian Cancer

Abstract

Context: Despite proven benefits, the uptake of genetic counseling and testing by at-risk family members of BRCA1 and BRCA2 mutation carriers remains low. Aims: This study aimed to examine at-risk individuals' reported reasons for and against familial cancer clinic (FCC) attendance and genetic testing. Methods: Thirty-nine telephone interviews were conducted with relatives of high-risk mutation carriers, 23% (n = 9) of whom had not previously attended an FCC. Interview responses were analyzed using the frameworks of Miles and Huberman. Results: The reasons most commonly reported for FCC attendance were for clarification of risk status and to gain access to testing. While disinterest in testing was one reason for FCC nonattendance, several individuals were unaware of their risk (n = 3) or their eligibility to attend an FCC (n = 2), despite being notified of their risk status through their participation in a large-scale research project. Individuals' reasons for undergoing testing were in line with that reported elsewhere; however, concerns about discrimination and insurance were not reported in nontestees. Conclusions: Current guidelines regarding notifying individuals discovered to be at increased risk in a research, rather than clinical setting, take a largely nondirective approach. However, this study demonstrates that individuals who receive a single letter notifying them of their risk may not understand/value the information they receive.

Introduction

Research has shown that although the majority of individuals identified as carriers of a breast and/or ovarian cancer-related mutation report an intention to notify their relatives of their increased risk of developing cancer (Barsevick et al., 2008), the rate of uptake of genetic counseling by at-risk relatives is low. Reported uptake rates range from 36% in one U.S. study (O'Neill et al., 2006) to figures as low as 23% in a sample of close relatives of Australian mutation carriers (Suthers et al., 2006). Reasons for these low figures are understudied, especially in the Australian healthcare context.

Previous international research has demonstrated that the following factors (among others) may contribute to nonattendance for genetic counseling in high-risk individuals: currently receiving cancer treatment (Vadaparampil et al., 2009), identifying with a non-Caucasian heritage (Simon and Petrucelli, 2009), and being from a lower socioeconomic background (Holloway et al., 2008). Other factors may include a desire to avoid worries/anxiety about cancer, the absence of biological children in the immediate family, and more practical concerns, such as the cost and time commitments involved (Geer et al., 2001). However, although the available literature provides some insights into at-risk individuals' reasons for and against genetic counseling attendance, data collected directly from high-risk individuals who do not attend clinics is sparse.

Also, international differences in patient attitudes to genetic counseling do exist and justify the examination of attitudes in countries such as Australia, and the comparison of these attitudes between countries (Meiser et al., 2007). There is limited research documenting reasons why Australians at high risk may not attend an familial cancer clinic (FCC), although one recent study found that unlike in other studies overseas, men from high-risk breast/ovarian cancer families who did not attend an FCC did not have higher levels of cancer-specific worry, and nor did they have fewer biological children, than those who had attended a clinic (Lobb et al., 2009).

Many previous studies have investigated individuals' attitudes toward genetic testing for hereditary breast and/or ovarian cancer risk. Studies have documented the following motives for undergoing genetic testing: to manage future cancer risk, to learn about one's children's risk, to inform screening decisions, to inform decisions about prophylactic surgery, to provide relief from uncertainty, and to guide important life decisions such as marriage and childbearing (Pasacreta, 2003). Reasons reported for nonuptake of testing range from concerns about health and life insurance implications, to fear of discrimination, lack of knowledge about testing benefits, concerns about the emotional impact of testing, and the cost (Pasacreta, 2003; Ropka et al., 2006; Kieran et al., 2007; Simon and Petrucelli, 2009).

The reasons cited against genetic testing also vary considerably by country, suggesting that genetic testing barriers are influenced by country-specific medico-legal factors and insurance legislation (Meiser et al., 2000; Peters et al., 2005; Lynch et al., 2006). It seems likely that concerns about cost, insurance implications, and privacy issues are not as prevalent in high-risk Australians, possibly because testing is typically offered free of charge and always in the context of genetic counseling at an accredited clinic (Wakefield et al., 2007). However, despite this, the genetic testing uptake of at-risk relatives of mutation carriers is still low in Australia, with one study reporting that only 44% of first-degree relatives who were informed that they may be at risk through their participation in a research study chose to attend an FCC and learn their genetic testing result (Keogh et al., 2004).

Given this, this study aimed to qualitatively examine the reasons for and against FCC attendance reported by a sample of Australians at increased risk of developing breast and/or ovarian cancer due to the presence of a pathogenic mutation identified in their family. A secondary aim of the study was to describe their reasons for and against undergoing genetic testing. In instances where individuals had decided to undergo genetic counseling and/or testing, they were also asked about their family members' decisions, and their beliefs about why any of their family members had/had not undergone counseling/testing were elicited.

Materials and Methods

Sample

The sample comprised 39 participants who were recruited through the Kathleen Cunningham Foundation Consortium for Research into Familial Aspects of Breast Cancer (kConFab). kConFab is a research co-operative that recruits families with four or more cases of breast or ovarian cancer on one side of the family and two or more living affected relatives with breast or ovarian cancer and four or more living first- or second-degree unaffected female relatives of affected cases [more details can be found in Mann et al. (2006) and at www.kconfab.org].

Only individuals from families originally recruited to kConFab through the Hereditary Cancer Clinic at Prince of Wales Hospital, Sydney, Australia, were invited to participate; however, not all of the notified relatives of the mutation carrier had chosen to attend the clinic themselves. According to the kConFab protocol, participants can nominate to be notified by letter if a family-specific mutation is identified in their family. Participants are not provided with a personal genetic test result by the research team; those who wish to know their own genetic status are directed to an FCC for genetic counseling before predictive genetic testing.

Recruitment of participants through kConFab, rather than through an FCC directly, allowed the unique opportunity to collect data on the views of individuals who have never presented at an FCC, despite their family history. This important group is difficult to engage in research and is hence underrepresented in the majority of reports describing attitudes toward genetic counseling and testing in high-risk individuals (Goelen et al., 1999). The eligibility criteria for participation in this study were as follows: being from a family with an identified BRCA1 and/or BRCA2 mutation; being 18 years of age or older; and having sufficient English skills to enable participation in a telephone interview.

Ethics approval for the study was obtained and a study package mailed to 161 individuals. Those who opted in to the study participated in a 30-40-min semi-structured telephone interview. The first section of the interview probed participants' reported reasons for and against genetic counseling attendance and genetic testing uptake. In the second part of the interview, the communication preferences regarding genetic testing in were explored, the results of which will be reported separately. Four interview schedules were prepared so as to be appropriate for participants who (1) had previously attended an FCC and received a positive genetic test result; (2) had previously attended an FCC and received a negative result; (3) were aware of a familial gene mutation but had either not attended a clinic or had attended one and subsequently opted not to have testing; and (4) reported being unaware of a familial gene mutation, despite having received a letter from kConFab notifying them of their potentially increased risk.

Data analysis

Interview responses were recorded and transcribed, and the conceptual framework of Miles and Huberman (1994) was used to guide analysis. Data collection and analysis took place concurrently, and newly emerging themes were discussed by the team to create new lines of questioning for subsequent interviews. Emergent themes were cross-tabulated by sample characteristics using QSR NVivo8, and counts of participants who endorsed particular beliefs were used to address potential researcher bias. Given this study's unique access to the difficult to reach cohort of high-risk individuals who have not attended an FCC, a more in-depth, secondary thematic analysis of the responses of clinic nonattendees was conducted. The responses of this group were given greater weight in the analysis than the responses of relatives who discussed their beliefs regarding possible reasons for nonattendance in their relatives.

Results

Sample characteristics

Fifty-three participants opted into the study; of these, 50 were interviewed. Of the 50 interviews, 39 were purposively selected for analysis to achieve a good spread of participant characteristics and to allow the determination of the broadest possible range of beliefs. Interviews with participants from groups that were underrepresented (e.g., men and those who had not attended an FCC) were preferentially selected over other groups for analysis. Purposive sampling is recommended in qualitative research to capture views from as many different perspectives as possible. In contrast, quantitative research aims to sample all eligible cases to achieve generalizable and representative results (Patton, 1990; Denzin and Lincoln, 1994). No statistically significant differences in age, sex, and education levels were observed when comparing the characteristics of the participants whose interviews were included in the analyses (n = 39), compared to those who were either not interviewed (n = 122) or whose interviews were not included in the analysis (n = 11).

Table 1 summarizes the characteristics of the sample, whose mean age was 58 years (range: 30-84 years). Twenty-eight participants were women (71%), 22 held post-school qualifications (56%), and 38 identified as Caucasian (97%). Thirty had previously attended an FCC (77%). All participants who had attended a clinic had undergone genetic testing.

Table 1.

Socio-Demographic, Family History, and Medical Characteristics of Sample

Demographic (n = 39)	Mean	Range
Age	58 (SD 12.11)	30-84

	n	%
Sex
Male	11	29
Female	28	71
Educational level
No post-school qualifications	17	44
Post-school qualifications	22	56
Marital status
Married or living as married	24	62
Divorced or separated	8	21
Widowed or never married	7	18
Previous cancer diagnosis
Breast cancer	8	21
Ovarian cancer	1	3
Prostate cancer	0	0
Other type of cancer (except nonmelanoma skin cancer)	4	10
Family cancer clinic attendance
Yes	30	77
No	9	23
Genetic testing result as disclosed through familial cancer clinic
Disclosed	30	77
Positive result	15	50
Negative result	13	43
Still awaiting result	2	7
Not disclosed	9	23

Reported reasons for and against family cancer clinic attendance

Half of those participants who had attended a clinic (hereafter denoted as “FCC attendee”; n = 15) reported gaining access to genetic testing as their primary reason clinic attendance. In addition, women identified having a strong family history as a reason for attending a clinic (n = 13), whereas no men identified this as a reason.

“A whole heap of my family went because we had lost other cousins to breast cancer.”—Female, 58 years old, FCC attendee.

“My grandmother had had ovarian cancer many years ago and with that knowledge we decided it would be a good idea to get it done.”—Female, 69 years old, FCC attendee.

Participants (n = 10) also reported requests from relatives as the main reason for their attendance.

“Because my aunt cracked the whip…She cracked the whip and we all did as we were told.”—Female, 62 years old, FCC attendee.

Some participants (n = 8) identified prevention and risk management as reasons for attending the clinic.

“So I could make an informed decision as to what to do from then on.”—Female, 65 years old, FCC attendee.

Participants who had not attended a clinic (n = 9) described several reasons for nonattendance, which included having decided a priori not to pursue genetic testing and as a result having chosen not to attend a clinic (n = 2) and not having had the time to attend (n = 2).

“I had a letter from … kConFab, yes, advising me that a gene had been located … I was given an option of going further in finding out more about it, which I have accepted, but so far I haven't done the next step … there wasn't any urgency … it's a little bit awkward for me to get a day off.”—Female, 84 years old, FCC nonattendee.

The remaining five participants were either unaware of the presence of a mutation within the family (n = 3) or were unaware that they were eligible to attend an FCC (n = 2). In each of the three participants who were unaware of the mutation, participants reported that they would be willing to attend an FCC if they were notified that a mutation had been identified. However, two participants placed little importance on the services that may be available in this situation. In one case, the participant reported that she would attend an FCC “just for curiosity … I don't know if I'd believe it all, but I'd be open to it” (female, 69 years old, FCC nonattendee). The lack of importance accorded to FCC attendance appeared to arise from her belief that her own and her sister's cancer were caused by external, not genetic, factors.

“I just feel, you know, we create a lot of our own issues and we can even change our DNA … I know why I got cancer … I was very careless with chemicals. I used to be spraying the garden, trying to have the best roses and it would drift over me.”—Female, 69 years old, FCC nonattendee.

Given this belief, this participant did not value genetic counseling (or testing), and when asked whether she would communicate with her daughter about the possibility of attending an FCC, she indicated there was no need because

“I tell my daughter; just because that was my experience in life she doesn't need to get it … I believe that the body has the power to heal itself.”—Female, 69 years old, FCC nonattendee.

The third participant who was unaware of a mutation admitted, “No, I've actually never heard of it [an FCC]” (female, 54 years old, FCC nonattendee), despite having had breast and ovarian cancer herself (and losing her mother and two younger sisters to breast cancer). When the services provided by FCCs were described to her, she expressed a keen desire to attend, explaining, “I'm always a bit petrified that it could get handed down to my daughter and like my granddaughter” and requested the contact details of her local clinic from the interviewer.

In each of these three cases, participants' understanding about the purpose of KConFab itself and the reason for their inclusion in the study appeared limited. All three described joining the study at the request of a relative, without understanding the potential relevance for their own health.

“I've got a cousin on my dad's side that's a doctor and she's going on that path. … I don't know how they got my name but I guess I was one of the rellies.”—Female, 69 years old, FCC nonattendee.

One participant reported not attending an FCC due to concerns about increasing anxiety.

“There's times when I think I'd like to go then I think I don't know if I'd really like to know or not. … I don't know if it would make me more paranoid.”—Male, 39 years old, FCC nonattendee.

Reported reasons for and against genetic testing

A summary of reported reasons for undergoing testing is provided in Table 2. The most commonly reported reason was for the benefit of children or other family members (n = 26). A large number of participants also discussed research as a primary reason for testing (n = 17).

“I was probably upset that I may have it and then I thought that for all my family's sake I should go and find out.”—Male, 63 years old, FCC attendee.

“Maybe it mightn't help us but it might help somebody one day.”—Female, 53 years old, FCC attendee.

Table 2.

Reported Reasons for Genetic Testing

Reason for genetic testing ^a	n	%
Certainty of personal genetic risk	24	62
Determining whether children are at risk	17	44
To assist with research	17	44
Asked to by relative	12	31
Personal risk reduction and increased surveillance	10	26
To help family members	8	21
Explanation of family history	5	13
Advised by doctor	3	8

More than one response permitted.

Having been asked to have genetic testing by a family member was another commonly reported reason to pursue testing (n = 12).

“My cousin who died who was the one who turned out that she was BRCA1 [carrier] and wanted us to get tested, she kind of made us promise we'd do it ourselves before she died.”—Female, 46 years old, FCC attendee.

Seven of the nine participants who had not had testing reported that they would undertake testing if it was more easily accessible/available to them.

“KConFab sent out a recommendation to go and get tested, which I haven't done … I'm keen to have the gene test but just haven't managed to coordinate it yet.”—Male, 40 years old, FCC nonattendee.

Of the two participants who decided against testing, one was unsure whether they would like to know their mutation status, whereas the other reported that knowledge of her status would not alter her health-related behaviors.

“It wasn't necessarily going to change anything if the gene was there or not in terms of my lifestyle, you know, I exercise, am healthy, you know, I don't smoke. I do all those things anyway so if I knew it wasn't going to change my life.”—Female, 30 years old, FCC nonattendee.

Participants who underwent testing also described their perceptions of the reasons why some of their family members declined, which are summarized in Table 3. Avoidance of anxiety was the most commonly perceived reason (n = 8). However, this was not commonly reported as a reason in actual nontestees (n = 2 out of 9).

Table 3.

Reasons Why Family Members Were Perceived to Have Refused Genetic Testing

Reasons why family members refused testing ^a	n	%
Anxiety or fear	8	21
Implications for family members	4	10
Lack of time	4	10
Would not affect their health-related behavior	4	10
Young age	3	8
Belief that they know mutation status without testing	3	8
Insurance	3	8
Concern about family members' reactions	2	5
Do not believe in genetic testing or its relevance to them	2	5
Prefer not to know	2	5
Beliefs about invincibility	1	3

More than 1 response or no response was permitted.

Discussion

The reasons most commonly reported for attending an FCC in this Australian sample were to obtain clarification of risk status and to gain access to genetic testing. In fact, many participants had decided to undertake genetic testing before making an appointment at a clinic. In line with this, two of the nonclinic attendees in our sample reported that they did not want to undergo testing and therefore had chosen not to attend genetic counseling, implying a lack of knowledge about the nongenetic testing services that can be provided by clinics.

While disinterest in testing was one reported reason for clinic nonattendance, several individuals reported that they were unaware of the presence of a mutation within their family, or that they were unaware that they were eligible to attend an FCC, despite having received a letter explicitly explaining that they were both at increased risk and eligible for testing. This is concerning and raises important questions about to how best to inform individuals about their risk when identified in a research setting. Similar findings have been described elsewhere, with a substantial proportion of men from high-risk breast/ovarian cancer families, for example, being reported to be unaware of the relevance of genetic testing in their situation, despite being specifically notified by letter (Lobb et al., 2009).

It is possible that individuals who receive a letter of this nature may not understand or comprehend the information it contains. Our data are reminiscent of those reported by Vadaparampil et al. (2009), who examined the recall of high-risk women who had been sent a genetic counseling referral letter by their surgeon after a breast cancer diagnosis. They reported that 20% of women did not recall receiving the letter at all, and of those who did recall receiving it, half thought the letter was sent to all patients and many were confused/overwhelmed by its contents.

It is possible that the letter received by the individuals in our study is ineffective in communicating the importance/benefits of FCC attendance in some high-risk cases. Current government and clinical guidelines regarding notifying individuals discovered to be at increased risk of cancer in the context of a research study take a largely nondirective approach (e.g., see www.privacy.gov.au/law/act/genetic). In many protocols, one notification letter is deemed sufficient in terms of adequately informing individuals of their risk status when this becomes known. Further follow-up of these individuals is discouraged due to concerns about being perceived as pressure to undergo genetic counseling/testing. However, this study demonstrates that individuals who receive a letter notifying them of their risk status may not understand/value the information they receive. If they did fully understand the letter, several of our participants may have availed themselves of these services.

The letter distributed to individuals identified as being at increased risk in this study might be improved by highlighting the range of nontesting services offered by FCCs (e.g., risk management advice and emotional support). This study also highlights the importance of considering other nonwritten alternatives for notification to supplement that already distributed. Subsequent to completion of our data collection, kConFab instituted a new methodology for monitoring the receipt of mutation notification letters. The current protocol involves asking letter recipients to acknowledge receipt of the letter by returning an “acknowledgement slip.” Those who do not return the slip are then telephoned up to three times to verify receipt of the letter. The impact of this protocol is being monitored and will be reported in future publications.

Consistent with other research on individuals' reasons for undergoing genetic testing for a range of hereditary conditions, participants in this study most often underwent testing to clarify their own or their children's risk of developing cancer. Not surprisingly, the male participants in our study did not appear as concerned about their own cancer risk as that of their children and female relatives when opting to have testing, possibly due to their perceived and actual lower personal risk of cancer than in women. Also, as reported elsewhere (Daly et al., 2001; Skirton et al., 2006), many participants reported altruistic motivations for testing.

With regard to barriers to genetic testing, there were significant discrepancies between reported and perceived reasons to not undertake genetic testing. Many participants who had undergone testing themselves believed that some of their family members declined testing due to a desire to minimize anxiety. However, the nine untested participants reported that not knowing about their risk status or the availability of genetic testing, and a lack of opportunity to attend a clinic, were the primary barriers, rather than fear of the emotional impact of a positive result. In fact, when asked whether they would undergo genetic testing if they were able, all but 2 of the 9 untested participants reported that they would. Therefore, increasing at-risk individuals understanding of their risk status and their access to testing services may yield the best outcomes in terms of testing uptake in the future. It may be that some previously described potential barriers to testing are over-stated in the Australian context, given that none of our nontestees reported concerns about the possible discrimination or adverse insurance and financial implications, although this may be reflective of a more global trend toward less concern about these issues (Kausmeyer et al., 2006).

Limitations

A key limitation of this, and similar studies, is the reliance on self-reports of beliefs and intentions. It is possible that participant responses were influenced by a desire to appear altruistic during their interview. For example, a large proportion of respondents (n = 17, 44%) cited “assisting with research” as a reason for undergoing genetic testing. Similarly, it is possible that the individuals who indicated that they would be interested in undergoing genetic counseling/testing during their interviews would not follow through with their stated intentions. Human behavior/cognition is complex and researchers may need to become more innovative in their development of research techniques that are able to effectively investigate how best to inform at-risk individuals of their options.

The response rate for the study was low, although it was consistent with other studies that have utilized a similar opt-in recruitment approach (Junghans et al., 2005). Other factors that may have contributed to the response rate may have included a reduced sense of relevance experienced by participants regarding the study, caused by the time delay between agreeing to participate in kConFab and receiving an invitation for this study. Also, relatively few nonclinic attendees and males were included in the study. It is therefore unlikely that the full range of nonclinic attendee's and men's views were captured. The study would have been strengthened if >9 clinic nonattendees and 11 men had been interviewed. Finally, the education level of participants in this study was high relative to the larger kConFab cohort and the general population (Australian Bureau of Statistics, 2008). Nonetheless, the study has unique strengths because participants were ascertained through a large research co-operative, rather than through FCCs directly. Thus, it is one of few studies that include data collected directly from at-risk individuals who have never approached an FCC.

Conclusions

This study demonstrated that this sample of Australians at risk of developing breast and/or ovarian cancer have a largely positive attitude toward genetic counseling and testing. Contrary to expectations, the key barrier to clinic attendance and genetic testing uptake was not having a negative attitude toward counseling/testing. Instead, it appeared the primary barrier to clinic attendance and testing uptake was a lack of understanding of their risk status and a lack of knowledge about their eligibility for genetic testing. This study demonstrates that careful consideration about the mode, format, and content of the information given to at-risk individuals is a crucial first step in allowing them to make an informed decision about whether they would like to avail themselves of genetics services. These data may guide the development of future genetic counseling strategies to assist nongenetics health professionals alerting their patients to their risk status.

Footnotes

Acknowledgments

We wish to thank Heather Thorne, Eveline Niedermayr, all the kConFab research nurses and staff, the heads and staff of the Family Cancer Clinics, and the Clinical Follow Up Study (funded by NHMRC grants 145684, 288704, and 454508) for their contributions to this resource, and the many families who contribute to kConFab. We would like to thank the participants in this study for sharing their experiences and Ursula Sansom-Daly for her efforts in data collection. Claire Wakefield is supported by a Postdoctoral Training Fellowship from the National Health and Medical Research Council of Australia (ID 510421). Bettina Meiser is supported by a Career Development Award from The National Health and Medical Research Council of Australia (ID 350989).

Disclosure Statement

The authors have no conflicts of interest to declare.

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