BRCA testing of breast cancer patients: medical specialists' referral patterns, knowledge and attitudes to genetic testing

BRCA testing of breast cancer patients: medical specialists’referral patterns, knowledge and attitudes to genetic testing

E. VAN RIEL, phd, genetic counsellor, Department of Medical Genetics, University Medical Centre Utrecht,Utrecht, C.C. WÁRLÁM-RODENHUIS, md, radiation oncologist, Department of Radiation Oncology, Univer-sity Medical Centre Utrecht, Utrecht, S. VERHOEF, phd, md, clinical geneticist, Family Cancer Clinic, theNetherlands Cancer Institute/Antoni van Leeuwenhoek Hospital, Amsterdam, E.J.TH. RUTGERS, phd, md, pro-fessor of surgical oncology, Division of Surgical Oncology, the Netherlands Cancer Institute/Antoni vanLeeuwenhoek Hospital, Amsterdam, & M.G.E.M. AUSEMS, phd, md, clinical geneticist, Department of MedicalGenetics, University Medical Centre Utrecht, Utrecht, the Netherlandsecc_1065 369..376

VAN RIEL E., WÁRLÁM-RODENHUIS C.C., VERHOEF S., RUTGERS E.J.TH. & AUSEMS M.G.E.M. (2010)European Journal of Cancer Care 19, 369–376BRCA testing of breast cancer patients: medical specialists’ referral patterns, knowledge and attitudes togenetic testing

This study explores knowledge about hereditary breast cancer, attitudes about BRCA testing and referralpattern to a family cancer clinic among medical specialists. A total of 92 questionnaires were completed bysurgeons (38), medical oncologists (29), radiation oncologists (13) and radiologists (12). The response rate was51%. A substantial (11–56%) proportion of medical specialists do not refer patients who meet current criteriafor BRCA testing. Although questions on inheritance were less well answered, overall knowledge was good.They had a positive attitude, but were concerned about the distress DNA testing might cause to familymembers. The majority (75%) stated that the best time for referral is after adjuvant therapy or during follow-up,but another important determinant was the patient’s wish or need (12%). Further studies are needed to gaininsight into the actual referral process, while ongoing training of medical specialists about genetic aspects ofbreast cancer is also necessary.

Keywords: attitude, breast cancer, genetic counselling, BRCA testing, referral and consultation.

INTRODUCTION

Worldwide, about 1 million women are diagnosed withbreast cancer every year (Parkin et al. 2005; Oldenburget al. 2007) and autosomal dominant susceptibility genesare involved in 5–10% of all breast cancers (Peto et al.1999). With the discovery of the BRCA1 and BRCA2genes, it became possible to test breast cancer patients and

their relatives for a genetic predisposition for breastcancer. This implies that eligible patients should be rec-ognized and referred, either on their own initiative or theirphysicians’. However, many women know little about thegenetic aspects of breast cancer (Miesfeldt et al. 2001;Velicer & Taplin 2001; Mouchawar et al. 2003). Althoughthey do not know much about hereditary breast cancer,most women have a positive attitude towards geneticcounselling and DNA testing (MacDonald et al. 2005).

Breast cancer patients and women with a positivefamily history have a strong need for information on thissubject (Cohn et al. 2003; MacDonald et al. 2005). Womenwho have been diagnosed with breast cancer at a youngage search actively for information about genetic factors,

Correspondence address: E. van Riel, Department of Medical Genetics,University Medical Centre Utrecht, PO Box 85090, 3508 AB Utrecht, theNetherlands (e-mail: [email protected]).

Accepted 21 September 2008DOI: 10.1111/j.1365-2354.2008.01065.x

European Journal of Cancer Care, 2010, 19, 369–376

Original article

© 2009 The AuthorsJournal compilation © 2009 Blackwell Publishing Ltd

especially if they have daughters (Cohn et al. 2003; Mac-Donald et al. 2005). A fair proportion of breast cancerpatients initiate a referral to a family cancer clinic. Thesewomen are often well educated (Rimer et al. 1996; Piet-erse et al. 2006). A larger proportion of women depend ontheir general practitioner (GP) or medical specialist forreferral for genetic counselling and BRCA testing. Tofacilitate accurate referrals, doctors must be trained toselect patients who meet the referral selection criteria.

Studies of GPs show that they have insufficient knowl-edge to select high-risk patients eligible for referral to afamily cancer clinic (Watson et al. 1999, 2001). However,in general, GPs do have a positive attitude towards genetictesting (Escher & Sappino 2000; Pichert et al. 2003). If ahigh-risk patient asks for referral, most GPs will refer herto a family cancer clinic (Pichert et al. 2003).

Apart from seeing their GPs, breast cancer patients areregularly seen by different medical specialists for treat-ment and follow-up. Little is known about the knowledgeand attitude to genetic counselling and DNA testingamong medical specialists. The few studies publishedseem to agree with the data on GPs, in that medicalspecialists in general have a positive attitude towardsgenetic counselling and testing, but also lack sufficientknowledge about hereditary breast cancer (Escher &Sappino 2000; Ardern-Jones et al. 2005).

In this study, we aimed to explore the knowledge andattitude to breast cancer genetic counselling and BRCAtesting among medical specialists from 28 hospitals and toassess the criteria they use to select patients for referral forgenetic counselling.

METHODS

Study design

Questionnaires were sent by mail to all members of thebreast cancer working groups of the ComprehensiveCancer Centres from the Middle Netherlands and Amster-dam regions. Before sending the questionnaires, a briefintroductory talk about the research project was given at ameeting for both groups. Five weeks after sending thequestionnaire, a reminder was sent to stimulate the par-ticipation rate.

Participants

The medical specialists (surgeons, medical oncologists,radiation oncologists, radiologists) were working in hospi-tals (n = 28) of the Middle Netherlands and Amsterdamregions.

Questionnaires

The forms included questions on social demographic char-acteristics, general questions on daily clinical practice andquestions on selection criteria for referral, knowledgeand attitudes to genetic counselling and BRCA testing.The level of knowledge on hereditary breast cancer wasassessed with items used by Pieterse et al. (2005) (adaptedfrom Claes et al. 2004). The total knowledge scores werecalculated by assigning one point for every correct answer(range 0–7). A mean correct knowledge score for the totalgroup and for each medical discipline was calculated asthe mean number of correct answers on the knowledgeitems. In addition, the percentage of correct answers foreach item was analysed, both for the total group and foreach medical discipline.

Statistical analysis

Data analysis was performed using spss 12.0.1. Descrip-tive statistics were used to describe the total study popu-lation. Differences between the medical disciplines weretested by means of a one-way anova or a non-parametricKruskal–Wallis test with significance levels of 0.05.

For questions on knowledge and attitudes, the answerwas left out of the analysis if no answer or both answerswere given. Written comments on questions and/oranswers were not analysed, unless they were written inthe category ‘Other, namely . . .’. Open-ended questionswere scored manually and grouped into differentcategories.

RESULTS

Characteristics of the participants

Of the medical specialists (182) approached, 92 returnedthe questionnaire (response rate 51%). Participants inthis study represented different medical specialties fromdifferent kinds of hospitals. Table 1 gives the socio-demographic characteristics of the participants.

Questions during consultations

The majority of participants (67%) received questions onthe heredity of breast cancer at least once a week: 96% ofparticipants said that such questions were asked by thepatient, 57% also mentioned the spouse and 53% familymembers. Sometimes, GPs contact medical specialists(12%) with questions on hereditary breast cancer.

If a patient did not ask about the heredity of breastcancer, 78% of the participants said they would bring up

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the subject if the family history was positive for breastcancer, whereas 6% would not mention it unless specifi-cally asked. Seventy-two per cent of the participants gaveexamples of frequently asked questions: 40% of suchquestions concerned the patient herself, 55% were relatedto family members, especially daughters, and 5% wereother questions.

Referral for genetic counselling and BRCA testing

Twelve per cent of the participants never referred a patientto a family cancer clinic. The majority of the participants(62%) said that they referred someone between once amonth and once every 3 months. Fifty-one per cent of theparticipants said that they would not refer a breast cancerpatient who had a relative with ovarian cancer. Similarly,other relevant criteria for referral were not always fol-lowed (Table 2). Criteria for referral used differed betweenmedical specialties, and especially radiologists referredless often.

Relevance of BRCA testing and task conception

Ninety-nine per cent of the participants considered itworthwhile to investigate whether a patient might have ahereditary form of breast cancer. Eighty-seven per centregarded referral for genetic counselling and BRCA testingas within their responsibility. Nine per cent saw otherspecialties as more appropriate for a referral to a familycancer clinic, with a role for the GP (8%). Task conceptiondiffers between medical specialty. Radiologists less oftenregarded referral for genetic counselling and BRCA testingto lie within their responsibility and more often saw a rolefor other specialties and the GP.

Knowledge

The participants in our study scored well on know-ledge questions. However, specific questions about the

heredity of breast cancer were less well answered(Table 3).

When the number of correct answers was calculated(range 0–7), the average score of the total group was 6.1,without any significant differences between medical spe-cialties (Table 4).

Table 1. Socio-demographic characteristics of the 92 participants

Gender Male 70%Female 30%

Age (years) Mean 49Median 47Range 34–65

Medical specialty Surgeon 41%Medical oncologist 32%Radiation oncologist 14%Radiologist 13%

Hospital Community hospital 71%University medical centre 19%Specialized oncology hospital 11%

Table 2. Criteria for referring a breast cancer patient for geneticcounselling and BRCA testing used in daily clinical practice

Criteria

Participants whosaid they wouldrefer a patient (%)

A patient with breast cancer <40 years 78A patient with pre-menopausal breast

cancer0

A patient with bilateral breast cancer,irrespective of age

46

A breast cancer patient with a first-degree relative with breast cancer, ifone of them <50 years of age

59

A patient with several first- and second-degree relatives with breast cancer

89

A patient with breast cancer and ovariancancer

85

A breast cancer patient with a relativewith ovarian cancer

49

A male breast cancer patient 44Other 7

Table 3. Participants’ knowledge about hereditary breast cancer

Participantswho gavecorrectanswer (%)

Early detection and treatment of breastcancer lead to longer survival than latedetection and treatment. (True)

94

All women who carry an altered gene(mutation) for breast cancer will developbreast cancer in the long term. (False)

88

A woman who has a sister with an alteredgene (mutation) for breast cancer has a50% chance (1 in 2) of also carrying themutation. (True)

78

A woman who does not have an alteredgene (mutation) for breast cancer cannevertheless develop breast cancer. (True)

100

Physical examination is only necessary ifyou have complaints; that is soon enoughto prevent breast cancer. (False)

100

If a father has an altered gene (mutation) forbreast cancer, then his children have a50% chance (1 in 2) of also having thismutation. (True)

72

In a family in which breast cancer hasfrequently occurred, if no altered gene(mutation) for breast cancer is found, thenregular breast surveillance is no longernecessary. (False)

100

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Attitude

Medical specialists had a positive attitude towards geneticcounselling and BRCA testing. A large majority held theopinion that genetic counselling and BRCA testing addedto the optimal treatment of breast cancer patients.Genetic counselling and BRCA testing were also consid-ered useful if no mutation was found and to add to aconsistent screening policy. A major point of concern wasthe distress such testing might cause family members(Table 5). Attitudes were not significantly differentbetween the medical specialties.

Most appropriate time for genetic testing

The majority of the participants (75%) felt that the besttime for genetic counselling and BRCA testing was afteradjuvant treatment (25%) and during follow-up (50%).However, a small percentage (10%) thought that the mostappropriate time was directly after diagnosis. Other timeswere also considered to be optimal (19%) (Table 6). The

main determinant for other time points was the patient’swish or need (12% of participants). There were no differ-ences between the different medical specialties.

Consequences of genetic counselling and BRCA testing

Seventy-eight per cent of participants mentioned conse-quences of genetic counselling and BRCA testing, whichcan be divided into: distress (17%), consequences forfamily members (12%), consequences for treatment (8%),changes in follow-up (24%), prophylactic surgery (28%)and other consequences (11%).

DISCUSSION

This study was designed to explore the referral process forgenetic counselling and BRCA testing by medical special-ists (surgeons, medical oncologists, radiation oncologistsand radiologists) from different hospitals who treat breastcancer patients. We studied criteria for referral usedduring consultations and several factors that may influ-ence the actual referral process, like knowledge and atti-tude. The results show that the participants have a goodknowledge of hereditary breast cancer and a positive atti-tude towards genetic counselling and BRCA testing.However, a substantial proportion (11–56% depending onthe chosen criteria) of the participants said they did notrefer patients who fulfil current criteria for referral to afamily cancer clinic.

Daily clinical practice

From our study, it is clear that medical specialistsinvolved in treating breast cancer patients receive manyquestions from patients about the heredity of breastcancer during consultations (67% at least once a week).This agrees with other studies, which show that patients(Cohn et al. 2003; MacDonald et al. 2005) and womenwith a positive family history for breast cancer (Mac-Donald et al. 2005) have a strong need to know more

Table 4. Average knowledge scores (range 0–7) for the differentmedical specialties

Average score (range 0–7) 95% CI

Surgeon 6.4 6.14–6.66Medical oncologist 6.1 5.73–6.47Radiation oncologist 5.8 5.01–6.59Radiologist 5.8 5.04–6.56

Total 6.1

Table 5. Participants’ attitudes towards genetic counselling andBRCA testing

Participantsagreed withstatement (%)

Genetic counselling and DNA testing add to anoptimal treatment for breast cancer patients

87

Genetic counselling and DNA testing candecrease worries about family members

84

Genetic counselling and DNA testing are onlyof value when a mutation has been found

4

Genetic counselling and DNA testing decreaseworries of breast cancer patients about familymembers

71

Genetic counselling adds to a consistentscreening policy for breast cancer for womenwith a positive family history for breastcancer

91

If there is a weak suspicion of hereditary breastcancer, a patient can be referred to a familycancer clinic

67

Genetic counselling and DNA testing causedistress in the family of a breast cancerpatient

68

Table 6. Best time for genetic testing in breast cancer patients

Participantsagreed (%)

Standarddeviation

Directly after diagnosis 10 0.30After surgery 2 0.15After adjuvant treatment 25 0.44During follow-up 50 0.50Other 19 0.39

Total percentage is more than 100% because participants couldgive more than one answer.

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about the genetics of breast cancer. We show that ques-tions about heredity are also asked by spouses, familymembers and GPs of breast cancer patients.

Nearly all clinicians (98%) attach value to determiningwhether a patient has a genetic predisposition for breastcancer and discuss hereditary breast cancer if the familyhistory gives reason to do so (78%). This is in agreementwith a study by Escher and Sappino (2000). Although themajority of the medical specialists in our study (87%)considered referral for genetic counselling and BRCAtesting to lie within their responsibility, some (12%) neverreferred a patient to a family cancer clinic. This might bepartly explained by the type of discipline (e.g. radiologistssaid they mentioned the indication for referral to the phy-sician who ordered the mammography, e.g. surgeon, GP)or the organization of the referral process (e.g. one medicalspecialist from a department being responsible for allreferrals).

Criteria for referral

Our findings suggest that a substantial proportion ofbreast cancer patients who meet the criteria for referral arenot being referred to a family cancer clinic. With ourstudy, we could not identify the reason for this. Becausealmost all participants attach value to investigatingwhether a patient has a genetic predisposition for breastcancer and, in general, have positive attitude towardsgenetic counselling and BRCA testing, it is unlikely thatattitude explains the low score for referrals. Other factors,e.g. insufficient knowledge, may contribute to the lack ofreferrals, as shown earlier for GPs (Watson et al. 1999,2001). For example, 51% of the participants would notrefer a breast cancer patient who has a relative withovarian cancer. It is possible that medical specialists arenot aware of the relationship between breast cancer andovarian cancer, although 85% said that they would referpatients with both breast cancer and ovarian cancer.

Patients too are not always well informed about theincidence of ovarian cancer in their family (Sijmons et al.2000) and they fail to report cases of ovarian cancer fromtheir paternal side (Quillin et al. 2006). These studiesemphasize the importance of drawing an adequate pedi-gree, both for the maternal and paternal sides of the family(Van Asperen et al., 2001). The missed referrals of patientswith a positive family history for both breast cancer andovarian cancer are particularly important because of thehigh detection rate of mutations in these families (Syrjä-koski et al. 2000; Wárlám-Rodenhuis et al. 2005).

A recent study by Carroll et al. (2008) showed thathigher levels of referral of GPs and medical specialists

were associated with more confidence in their knowledgeof criteria for referral. Better awareness of practical aspectsof referral for genetic counselling increased referral rate(Carroll et al. 2008). Also, confidence of medical special-ists and GPs in their own competencies in genetics, likeobtaining a family history and making a risk assessment,is shown to increase the number of referrals (Carroll et al.2008), thereby underscoring the importance of updatingcourses in genetics for doctors. To elucidate more aboutthe missed referrals, prospective studies among breastcancer patients can elucidate more about the reasons whya patient who fulfils criteria for referral is not actuallyreferred for genetic counselling.

Knowledge

We showed that the medical specialists had a high averagescore on the knowledge questions. They scored better onidentical knowledge questions compared with otherstudies among patients (Pieterse et al. 2005). For example,88% of the participants correctly answered the question‘All women who carry an altered gene (mutation) forbreast cancer will develop breast cancer in the long term’,while 40–73% of the patients gave the correct answer(Wonderlick & Fine 1997; Miesfeldt et al. 2001; Velicer &Taplin 2001).

Remarkably, questions on the heredity of breast cancerwere less well answered by the participants than the otherquestions, as described earlier for primary care physicians(Pichert et al. 2003). This lower score is of particularimportance when looking at the examples of frequentlyasked questions. Fifty-five per cent of the examples men-tioned represented questions about risks for familymembers, which might not have been answered correctlyif the medical specialist had insufficient knowledge aboutthe inheritance of breast cancer. The lower score forquestions on inheritance might be due to the limitedtime allotted for students to study genetics during theirmedical training in the Netherlands (Baars et al. 2005).

Attitude

The referral pattern may also be influenced by the physi-cians’ attitude towards genetic counselling and BRCAtesting. About 87% of the medical specialists reportedthat genetic counselling and BRCA testing add to anoptimal treatment for breast cancer patients. Only 4% ofthe participants in our study agree with the statement thatgenetic counselling and DNA testing are only of valuewhen a mutation has been found. If no mutation wasfound, a personal risk estimation can be made, with advice



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to screen high-risk women based on a detailed pedigreeand medical information of relatives. This contributes to aconsistent screening policy for high-risk women, whichwas shown to be highly appreciated by the medical spe-cialists in this study. The opportunity for medical inter-vention was also appreciated as has been reported byothers (Mehnert et al. 2003). Other benefits were alsomentioned by the participants in our study, such asimproved diagnostics and a screening policy for familymembers at risk.

Many participants in this study (68%) were under theimpression that genetic counselling can lead to distressin the patient’s family members, but 71% also agreedthat genetic counselling can decrease the patient’sworries about family members. This contradiction wasalso found in a study among gynaecologists (Mehnertet al. 2003) and patients (Velicer & Taplin 2001; Claeset al. 2004). The most frequently mentioned consequenceof BRCA testing (28%) in our study was the opportunityfor mutation carriers with breast cancer and healthyfamily members who carry the mutation to elect to haveprophylactic surgery.

Optimal time for BRCA testing

Seventy-five per cent of the participants indicated that theoptimal time for BRCA testing was after adjuvant treat-ment and during follow-up. This seems appropriate whenwe take into account that patients are more anxiousshortly after diagnosis compared with a year after diagno-sis (Burgess et al. 2005). Ten per cent of the participantsstated the optimal time for genetic testing to be directlyafter diagnosis. It is possible that if DNA testing couldprovide results more rapidly, this would influence thereported percentages. Participants frequently mentionedthat rapid test results were desirable for deciding about thesurgical treatment of breast cancer patients. In the case ofa BRCA mutation, a mastectomy could be the first choiceinstead of a lumpectomy. Patients have a more positiveattitude towards genetic testing directly after diagnosis ifthey have the benefits of prophylactic surgery (Weitzelet al. 2003; Schwartz et al. 2005). The patient mightchoose for a simultaneous contralateral prophylactic mas-tectomy and possibly for a direct reconstruction.

Although there are assumed to be negative psychologi-cal effects from genetic counselling and testing directlyafter a diagnosis of breast cancer, Schlich-Bakker et al.(2006, 2007a) showed that breast cancer patients who wereapproached for genetic counselling and BRCA testing atthe beginning of adjuvant radiotherapy were no more dis-tressed in the short term and long term than patients who

were not offered genetic counselling and testing. Themajority of these patients agreed to the timing (6–7 weeksafter surgery) or would have preferred an earlier approachfor genetic counselling (Schlich-Bakker et al. 2007b). Ourresults suggest that medical specialists prefer to referbreast cancer patients at least 6 months after diagnosis(e.g. after adjuvant treatment and during follow-up). Thisseems not to correspond with the wish of the patient.

Interestingly, 19% of the participants in this studychose the answer ‘other’ when asked what would be theoptimal time for genetic testing and then mentioned thepatient’s wish or need as the main determinant (12% ofparticipants). From our findings, we could not concludehow medical specialists actually determine whether apatient has a wish or need for genetic testing. Frojd andVon Essen (2006) showed that doctors working withinoncology care often underestimate how much informationpatients wish for and overestimate how much worrypatients experience, suggesting that the patients’ wish forinformation is not always met. Cancer patients whoseneeds are largely met show better psychological adjust-ment, lower levels of distress and are more satisfied withthe consultation (Butow et al. 1995). This has also beenshown in cancer genetic counselling: the better coun-selees consider their major needs to be fulfilled, the morepersonal control they perceive and the less anxious theyfeel (Pieterse et al. 2005).

Additional research is needed to gain insight into thecurrent preferences of the doctor and the patient regardingoptimal time for BRCA testing, and to assess the roles andinitiative of both the patient and the physician in breastcancer genetic counselling.

Limitations

Although a large number of participants completed thequestionnaire, the results of this study cannot be general-ized to all the medical specialists who treat breast cancerpatients. Specialists who are a member of a breast cancerworking group may have a greater interest in all topicsinvolved in the treatment of breast cancer, including agenetic predisposition for breast cancer. Also, a detailedstratified analysis on specialty was not possible due to thesmall numbers per specialty. However, this study didcover medical specialists in all the hospitals from two ofthe nine regions for the Comprehensive Cancer Centres inthe Netherlands.

Another confounding factor was that our results werenot a true representation of daily practice, but only areflection of what participants say or think they do inpractice.

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CONCLUSIONS

Medical specialists who treat breast cancer patients havegood knowledge and a positive attitude towards geneticcounselling and BRCA testing. However, our resultssuggest that the currently used criteria for referral are notbeing followed for a significant proportion of the patientsand we would stress the importance of continuing educa-tion of medical specialists.

The majority of the medical specialists felt that theoptimal timing of genetic testing was after adjuvant treat-ment or during follow-up, and that the patient’s wish orneed played an important role in determining the besttime. More research is needed to elucidate how referralsfor breast cancer genetic counselling are being made indaily clinical practice.

ACKNOWLEDGEMENTS

The authors would like to thank all the participants whofilled in the questionnaire. We would also like to thankMs I Leenen (Comprehensive Cancer Centre Middle Neth-erlands) and Ms S. Dijkhuis (Comprehensive CancerCentre Amsterdam) for practical support and Ms J Seniorfor critically reading the manuscript.

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BRCA testing of breast cancer patients: medical specialists' referral patterns, knowledge and attitudes to genetic testing