Familial Cancer (2014) 13:311–324 DOI 10.1007/s10689-013-9695-y
ORIGINAL ARTICLE
Attitudes and knowledge of medical practitioners to hereditary cancer clinics and cancer genetic testing Ian Teng • Allan Spigelman
Published online: 4 December 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract Genetic testing for susceptibility for common cancers is widely available. Thus, doctors have a role in identifying and referring patients who would benefit from a consultation with a specialist in genetics. This study aims to assess doctors’ referral rates, knowledge and attitudes towards cancer genetic testing, broken down by specialty (gastrointestinal, breast/ovarian, other specialties and General Practitioners-GPs). A 4-page questionnaire was mailed out to the GPs of all patients seen in 2012 in the Hereditary Cancer Clinic of St. Vincent’s Hospital Sydney (n = 128) and all the specialists in St. Vincent’s Hospital Sydney that might refer to the HCC (n = 33). 50 questionnaires were returned (31 %). Most doctors had referred a patient for cancer genetic testing (90 %). The average proportion of patients referred was 1 in 68.5 patients with breast/ovarian specialists referring the most, followed by gastrointestinal specialists and GPs. There was suboptimal knowledge of cancer genetic testing amongst doctors. Breast/ovarian specialists were most knowledgeable, followed by gastrointestinal specialists, other specialists and GPs. There were indications of inappropriate referral amongst doctors. Most (77.6 %) doctors were willing to receive further information on cancer genetics. Nearly all (94 %) doctors believe that it is their duty to inform an
I. Teng University of New South Wales, Unit 3, 39-41 Houston Road, Kingsford, NSW 2032, Australia e-mail: [email protected]; [email protected] A. Spigelman (&) St. Vincent’s Hospital Sydney, UNSW St. Vincent’s Clinical School, Level 5, De Lacy Building, Victoria Street, Darlinghurst, NSW 2010, Australia e-mail: [email protected]
individual at high risk for hereditary cancer that cancer genetic counselling and testing is available. The majority of doctors have positive attitudes towards cancer genetic testing. Defective knowledge scores, however, indicate that doctors need further training or tools to enable them to refer patients appropriately for cancer genetic testing. Keywords Cancer genetics Genetic testing Evaluation
Introduction The Centre of Disease Control and Prevention (2013) reported that genetic tests have been developed for more than 2200 diseases and 2000 of those are available for use clinically. Inherited forms of cancer (hereditary cancer), such as breast, ovarian and colon cancer are included within these 2000 diseases. This development of cancer genetic testing has major implications for patient management; allowing medical practitioners to identify asymptomatic individuals who have inherited an increased susceptibility to cancer, whilst increasing surveillance of these individuals for early cancer detection and possibly providing prophylactic treatment to improve the patients’ outcome. With the increase in availability as well as increased patients’ awareness of cancer genetic testing, it is expected that demand for medical practitioners to provide these services to their patients will increase. Hence, medical practitioners may have to deal with the complex medical, social and ethical questions related to genetic testing [1]. They will also have to be able to appropriately refer patients for cancer genetic counselling and/or testing. These provide the rationale for an exploration of the
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attitudes and knowledge of medical practitioners towards cancer genetic testing. A number of studies, mostly surveys, have attempted to do that. From these studies, several patterns are apparent. Medical practitioners generally approve of cancer genetic testings and believe they have a role to play in genomic medicine [2]. However, this positive attitude is tempered by medical practitioners’ fears of the negative consequences of cancer genetic testing which include the psychological impact on patient and family, discrimination in jobs and insurance, and confidentiality issues [1, 3–5]. It is also obvious that a barrier against referring patients for cancer genetic testing is medical practitioners’ lack of knowledge on cancer genetic testing [2, 6]. Furthermore, many medical practitioners do not refer a patient for cancer genetic testing because they believe that a patient’s cancer genetic testing results cannot be used effectively to improve the patient’s management. Reported reasons for this include doubt about the clinical utility and viability of cancer genetic testing, perceived lack of approved guidelines for patient management after a cancer genetic testing and perceived lack of evidence-based strategies for the detection and prevention of hereditary cancer [1, 5]. Moreover, adherence of medical practitioners to guidelines regarding cancer genetic testing is poor, leading to over-referral of average-risk patients and underreferral of high-risk patients [7, 8]. However, there are no Australian studies regarding this topic, with most of the studies being conducted in USA. Besides that, most of the studies are ten or more years old. Thus, in light of recent advances and new information regarding cancer genetic testing, screening and prevention [9, 10], there is a need to evaluate the knowledge and attitudes of Australian medical practitioners towards cancer genetic testing. Hence, the purpose of this study is to evaluate and compare, in general practitioners and specialists, the attitudes to and knowledge of cancer genetic testing, and patient referral rates for cancer genetic testing. To this effect, questionnaires that aim to assess knowledge, attitudes and referral rates of cancer genetic testing were mailed out to a subset of general practitioners and specialists in St. Vincent’s Hospital (Sydney).
Materials and methods
I. Teng, A. Spigelman
It was also approved by the St Vincent’s Hospital Research Governance Office for site approval at the Hereditary Cancer Clinic; approval number LNRSSA/13/SVH/135. Study population The study population consisted of both general practitioners (GPs) and specialists (n = 161). The GPs to whom surveys were sent consisted of the GPs of all patients seen in 2012 in the Hereditary Cancer Clinic (HCC) of St. Vincent’s Hospital Sydney (n = 128). The HCC provides cancer specific genetic counselling, risk assessment and gene testing. Referrals are mostly received from doctors and specialists at St Vincent’s Public Hospital, St Vincent’s Clinic and St Vincent’s Private Hospital. Patients are also referred from outside the hospital system by GPs and other specialists in the surrounding suburbs, as well as self-referring. The specialists surveyed consists of the specialists in St. Vincent’s Hospital Sydney that might refer to the HCC (n = 33). The specialties involved include oncology, obstetrics-gynaecology (ob-gyn) and internal medicine. Survey instrument The survey instrument was a 4-page self-administered questionnaire (Appendix 1), developed using questions from previous surveys testing the knowledge and attitudes of health practitioners towards cancer genetic testing. The questions in this questionnaire are aimed at eliciting referral rates, knowledge and attitudes towards cancer genetic testing. Response categories for questions were either yes/no, multiple choice, Likert scales, and short answer. Procedure The questionnaire was mailed out on the 26th of July 2013 along with a cover letter explaining the aims of the study and reassuring the respondents that their responses would be anonymous. Two weeks later, a follow up letter was mailed, reminding doctors to complete and return the questionnaire. The letter also gave the option of requesting another questionnaire if the original one was misplaced/ discarded. Two weeks after that, a similar follow-up letter was mailed. Doctors’ consent to participate was inferred by completion and return of the questionnaire.
Ethics approval Analysis This study was considered as Low and Negligible Risk Research and was reviewed and validated by the St Vincent’s Hospital Human Research Ethics Committee. The approval number was LNR/13/SVH/125.
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The aim of the analysis is to extract both quantitative and qualitative information regarding referral rates, knowledge and attitudes of doctors towards cancer genetic testing.
Attitudes and knowledge of medical practitioners
Descriptive analyses (means and standard deviations or frequency tables) were performed on the answers to all the questions, and these were stratified by specialties. Statistical methods such as Independent samples Kruskal-Willis test, correlation tests (i.e. Chi-square test, Phi & Cramer’s V), and regression analyses were then used to find out whether different specialties responded differently, and what the relationships between the answers to different questions and referral rates were. The statistical software IBM SPSS Statistics Version 21 was used for this. For referral rates, doctors were asked whether they referred (yes or no). The percentages of doctors who refer were then calculated. From the patients’ files, the actual GP and specialist referral rate was calculated and then compared with this study’s self-reported referral rate. The questionnaire also asked doctors to state the proportion of patients they refer (i.e. 1 in x patients). These proportions were then converted to numerical data for entry into SPSS by dividing 1 by x. For example, doctors who referred 1 in 10 of their patients, were given a value of 0.1 (1 divided by 10). Doctors who do not refer are given a value of 0.0. For questions that assess doctors’ knowledge, several options were listed and doctors were asked to choose the correct answer. ‘‘Appendix 2’’ shows the correct answers to the 5 knowledge questions (Questions 6, 8, 9, 10, and 12). To assess whether doctors refer appropriately, two questions were formulated, question 6 and 12. Question 6 asks doctors who refer, ‘‘How important is each of the factors below in your decision making on whether to refer someone for cancer genetic testing?’’ The answer was in Likert scales (1–5). Doctors that selected 1–3 were categorized as labelling that factor ‘‘not important’’ and those that selected 4 or 5 were categorized as ‘‘important’’. Then, depending on whether said factor is indeed important to consider before referral (refer to ‘‘Appendix 2’’), doctors’ responses were labelled as correct (1) or incorrect (0). Question 12 was, ‘‘Can a person with no cancer and no proven gene mutation in his/her family be referred to a Hereditary Cancer Clinic for cancer genetic testing; if yes, please describe the circumstances under which this might be so.’’ The correct answer is ‘‘Yes’’, and the respondent must have indicated that the patient was eligible for Ashkenazi testing or mentioned ethnicity of patient. Question 7 assessed the reason some doctors do not refer. For doctors who stated they did not refer patients for cancer genetic testing (n = 5), they were given a list of reasons and asked to rate how important said reasons are in preventing them from referring. They were asked to rate from 1 to 5, 5 being the most important hindrance. The mean of each response were then calculated. The higher the mean, the more important the reason is.
313 Table 1 Number of doctors who have referred a patient for cancer genetic testing Ever referred? No Clinical specialty
Total
Total
Yes
Breast/ovarian
0
4
4
Gastrointestinal
0
10
10
GP Other
4 1
28 3
32 4
45
50
5
Results Overall, 31 % of doctors surveyed (50 out of 161) returned the questionnaire. The response rates differed between specialties, with 25 % (32/128) of GPs, and 54.5 % (18/33) of specialists returning the questionnaire. Of the specialists, 66.6 % (10/15) of those in gastrointestinal, 44.4 % (4/9) of those in breast/ovarian and 44.4 % (4/9) of those in other specialties returned the questionnaire. The specialties included in the ‘‘other’’ group are medical oncology, radiation oncology, general surgery and head and neck surgery. GPs had practiced for the longest time period (23.6 ± 10.2 years); doctors in the field of breast/ovarian practiced for 22.5 ± 5 years; and those who specialized in gastrointestinal practiced for 18.6 ± 9.9 years. Those in other specialties have an average of 16.8 ± 4.7 years in practice. Referral rates Of the 50 respondents, 45 (90 %) indicated that they have referred a patient for cancer genetic testing. All breast/ ovarian specialists and gastrointestinal specialists have referred. For GPs, 87.5 % (28 out of 32) have referred patients for cancer genetic testing; for others, 75 % (3 out of 4) have referred. Out of the 5 that have never referred, 4 were GPs and 1 was from ‘‘other’’ specialty (head and neck surgeon). From the patients’ files from which the mailing list of GPs was obtained, only 18 out of 144 (12.5 %) patients were referred by their GPs, and 113 out of 144 patients (78.5 %) were referred by their specialists (Table 1). In terms of proportion of patients referred, doctors referred an average of 1 in 68.5 patients. GPs referred 1 in 790 patients; gastrointestinal specialists referred 1 in 34 patients; breast/ovarian specialists referred 1 in 15 patients; and those in other specialties referred 1 in 33 patients. Oneway ANOVA as well as independent samples Kruskal– Wallis test showed that there were significant differences between the groups (p \ 0.001). Breast/ovarian specialists
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Table 2 Responses of doctors to question 6 Question/Factor
Percentage of doctors who were correct, % (n = 44)
Percentage of doctors who were correct out of each specialty, % Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
GP (n = 27)
Other (n = 3)
Number of family members of patient with cancer
90.9
100.0
90.0
88.9
100.0
Age of onset of cancer in family member(s) of patient
90.9
100.0
100.0
85.2
100.0
Presence of a known mutation in a family member of patient
95.5
100.0
100.0
92.6
100.0
Age of onset of cancer in patient
79.5
75.0
90.0
77.8
66.7
Patients’ request
65.9
75.0
80.0
55.6
100.0
Features of patients’ disease (e.g. triple negative breast cancer or multiple colorectal polyps) Impact on further treatment
65.9
50.0
60.0
70.4
66.7
56.8
50.0
50.0
55.6
100.0
Impact on future surveillance
77.3
75.0
80.0
77.8
66.7
Average
77.8375
78.125
81.25
75.4875
87.5125
referred the most (p \ 0.06), followed by gastrointestinal specialists (p \ 0.05) and GPs came in last (p \ 0.05). However, other specialties had no significant differences with any of the three groups above. When asked when the last time the doctors referred a patient was, most (29/67.4 %) indicated ‘‘last 6 months’’. Stratified by specialties, all breast/ovarian specialists have referred in the last 6 months. Only GPs said that they referred in the last 24 months.
cancer (13), and to reassure an anxious and insisting patient (7). 5 doctors gave characteristics of the cancer/tumour as the reason. There was a significant correlation between answering ‘‘No’’ and referral rates (p \ 0.01). From regression, those that answered ‘‘no’’ tended to refer less patients for cancer genetic testing (p \ 0.05) (Table 3).
Knowledge of referral guidelines
When asked to estimate the cost of the first family member (proband) to undergo cancer genetic testing, more than half (56.3 %) of doctors selected the correct answer. However, out of this 27, one selected this by guessing (‘‘no clue’’ was written beside the question). Those in other specialties were most accurate, with 75 % (3/4) selecting the correct option. 60 % (6/10) of gastrointestinal specialists, 60 % (18/30) of GPs, and none of the breast/ovarian specialists were correct. Phi and Cramer’s V showed significant correlation (p \ 0.05) between estimated cost and clinical specialty. No significant relationship was found between estimated cost of cancer genetic testing and referral rate, from correlation tests and regression. No significant relationship found between being correct and referral rate.
To assess whether doctors refer appropriately, two questions were formulated. The first asks doctors who refer, ‘‘How important is each of the factors below in your decision making on whether to refer someone for cancer genetic testing?’’ Table 2 shows the responses of doctors to this question. There was also an option for doctors to write down other factors that influence their decision-making in whether to refer a patient for cancer genetic testing. One wrote gender & ethnicity of relative. The second question was, ‘‘Can a person with no cancer and no proven gene mutation in his/her family be referred to a Hereditary Cancer Clinic for cancer genetic testing; if yes, please describe the circumstances under which this might be so.’’ Only 6 % (3/50) of doctors responded correctly. All three were breast/ovarian specialists. None of the doctors in the gastrointestinal, ‘‘other’’ or GP category were correct. 29 (58 %) of doctors replied ‘‘Yes’’ but gave the incorrect reason. For those that selected ‘‘Yes’’, the two most common reasons were if the patient had a strong family history of
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Knowledge of the cost of cancer genetic testing
Knowledge of the time taken for cancer genetic testing Table 4 shows the responses of doctors, stratified by profession when asked about the estimated turnaround time for routine cancer genetic testing. Only 22.9 % (11) of doctors answered correctly, with 30.0 % of gastrointestinal specialists’ answering correctly,
Attitudes and knowledge of medical practitioners
315
Table 3 Responses to question 8 Estimated cost for proband to undergo cancer genetic testing, $
Frequency (percentage) (n = 48)
Clinical specialty Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
\1000
12 (25.0 %)
2
4
6
1000–1999
27 (56.3 %)
0
6
18
3
2000-2999 [3000
5 (10.4 %) 4 (8.3 %)
0 2
0 0
4 2
1 0
GP (n = 27)
Other (n = 3)
Table 4 Responses of doctors to question 9
Table 5 Responses of doctors to question 10
Frequency (percentage) (n = 48)
Frequency (percentage) (n = 48)
GP (n = 30)
Other (n = 4) 0
Clinical specialty Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
\1
0 (0 %)
0
0
0
1–2
2 (4.2 %)
0
0
1
1
2–4
20 (41.7 %)
2
5
12
1
4–8
11 (22.9 %)
1
3
6
1
[8
15 (31.3 %)
1
2
11
1
Turnaround time for proband to undergo urgent cancer genetic testing, weeks
Frequency (percentage) (n = 48)
0
Clinical specialty Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
GP (n = 27)
Other (n = 3)
\1
2 (4.2 %)
1
0
1
0
1–2
15 (31.3 %)
1
4
9
1
2–4 4–8
15 (31.3 %) 10 (20.8 %)
2 0
3 2
8 7
2 1
[8
6 (12.5 %)
0
1
5
0
followed by breast/ovarian (25.0 %) and other specialists (25.0 %), and GPs (20.0 %). Table 5 shows the responses of doctors, stratified by profession when asked about the estimated turnaround time for urgent cancer genetic testing. For urgent cancer genetic testing, only 31.3 % (15) estimated correctly. The most accurate specialty was gastrointestinal (40.0 %) followed by GPs (30.0 %), and breast/ovarian and other specialties, both at 25.0 %. Desire for further information Most (77.6 %–38/49) of doctors expressed a desire for further information regarding cancer genetic testing. Most gastrointestinal specialists (90 %) and GPs (84 %) wanted more information. On the other hand, only a few of the breast/ ovarian specialists (33.3 %) and ‘‘other’’ specialists (25 %) wanted further information. Independent samples Kruskal– Wallis test showed that the differences between groups were
significant (p \ 0.05). Further analysis by regression showed that the desire for further information is highest in gastrointestinal specialists (p \ 0.05), followed by GPs (p \ 0.05). Breast/ovarian specialists and ‘‘other’’ specialists had significantly lower (p \ 0.05) desire for further information, but no significant differences between them. Reason for not referring Table 6 shows the responses of doctors to Question 7. 4 of the 5 doctors who answered this question were GPs and the last was from ‘‘other’’ specialty, specifically a head and neck surgeon. Doctors were given an option to state other reasons for not referring patients for cancer genetic testing. One GP stated that there is no treatment available whilst another GP said that no patient has requested cancer genetic testing. The head and neck surgeon said that cancer genetic testing had limited utility for most patients.
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Table 6 Responses of doctors to question 7 Reason for not referring
Mean (n = 5)
Mean by specialty GP (n = 4)
Other (n = 1)
Cancer genetic testing is not helpful
2.400
2.75
1
Cancer genetic testing may cause psychological distress to the patient
2.200
2.5
1
Patient confidentiality/privacy will be at risk
1.400
1.5
1
Cancer genetic testing is too costly
2.200
2.5
1
Cancer genetic testing takes too long
1.800
2.0
1
Patients with a positive test result may face discrimination at work or when seeking insurance
2.600
2.5
3
A positive result in cancer genetic testing may negatively affect relationship with patient’s family and relatives
3.000
3.0
3
Perceived roles When asked, ‘‘Do you think it is your duty of care to inform an individual at high risk for hereditary cancer that cancer genetic counselling and testing is available?’’ most (n = 47, 94.0 %) doctors replied affirmatively. All three of those who said no were GPs. Question 13 asked doctors to select the actions that they carry out in their practice. The results are tabulated in Table 7.
Discussion
(2003–2013) or a more likely explanation, given that the cohort of doctors surveyed came from the HCC files, is that the sample is biased. There was wide discrepancy between the self-reported GP referral rate (87.5 %) and the actual referral rate calculated from patient files (12.5 %). Similarly, for specialists, there was significant difference between the selfreported referral rate (94.4 %) and the actual referral rate (78.5 %). These may mean that the doctors referred to other hereditary clinics, or they overestimated the number of patients that they referred, or that they refer but happened not to refer in 2012. It may also mean that the doctors who did not respond to this survey were those that tended not to refer patients for cancer genetic testing.
Referral rates Knowledge Of 50 doctors, 45 (90 %) indicated they have referred. This differs greatly from other studies, all of which have less than 50 % referral rates [11–13]. In terms of absolute numbers, doctors in this study referred an average of 1 in 68.5 patients which is more than the 2 patients a year out of 30 patients daily found in another study [5]. These may indicate a true difference in referral rates in the past decade
Overall, doctors had a suboptimal knowledge of cancer genetic testing. For example, one doctor incorrectly stated that gender is important in deciding whether to refer a patient for cancer genetic testing. Furthermore, some doctors were honest enough to write down on the questionnaire that they had ‘‘no clue’’ to some of the questions. This
Table 7 Responses of doctors to question 13 Actions
Take a family history
Frequency and percentage of doctors who carry the action out Overall (n = 50)
Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
GP (n = 32)
Other (n = 4)
50 (100 %)
4
10
32
4
Identify families where cancer genetic testing is indicated
38 (76 %)
3
9
24
2
Counsel and give information to families where cancer genetic testing is indicated
30 (60 %)
2
5
21
2
Obtain informed consent for cancer genetic testing from patient before the genetic testing
10 (20 %)
1
0
9
0
Discuss management options for a patient with positive cancer genetic testing result
25 (50 %)
3
5
15
2
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Attitudes and knowledge of medical practitioners
finding of suboptimal knowledge is similar to many other studies done in Europe and in USA [2, 3, 6, 14]. When analysed by specialty, breast/ovarian specialists seemed to be most knowledgeable about cancer genetic testing, followed by gastrointestinal specialists and ‘‘other’’ specialists, and lastly GPs. This finding is similar to those reported in other studies. These state that oncologists were most knowledgeable, followed by obstetric-gynaecologists, other specialists and lastly GPs [2, 14–17]. More than half (58 %) of doctors said they would refer a patient with no cancer and no proven gene mutation in his/ her family for cancer genetic testing but gave the incorrect reason. This may indicate that many doctors refer patients who do not need cancer genetic testing to hereditary cancer clinics, leading to over-referral. This correlates with a recent study that addressed adherence to guidelines on cancer genetic testing for BRCA1/2. Trivers et.al. [7] found that 29 % of 1878 responding doctors incorrectly referred average-risk women for cancer genetic testing. No statistically significant correlation could be found between doctors’ knowledge and their referral rates. This is probably due to the small sample size in this study. Desire for further information Breast/ovarian specialists and ‘‘other’’ specialists have the least desire for further information on cancer genetic testing. This may make it difficult for educational efforts aimed at improving their knowledge on cancer genetic testing to be successful. GPs had the worst knowledge scores, but nearly all (84 %) wanted further information on cancer genetic testing. These may show that GPs realize that their knowledge of cancer genetics may be insufficient and are willing to correct this by receiving further information on cancer genetic testing. Reasons for not referring ‘‘A positive result in cancer genetic testing may negatively affect relationship with patient’s family and relatives’’ was found to be the most important reason for not referring patients for cancer genetic testing, followed closely by ‘‘concerns on discrimination at work or in insurance’’. Interestingly, ‘‘patient confidentiality/privacy will be at risk’’ was given the least importance. This contrasts with the widespread emphasis placed on patient privacy and confidentiality. An example can be seen in the informed consent form for cancer genetic testing. There is a section labelled ‘‘Sharing the result’’ where the patient can decide whether to consent to his/her cancer genetic testing result being given to relevant family members and health professionals (‘‘Appendix 3’’).
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One GP stated that ‘‘there is no treatment’’ whilst a head and neck surgeon said that cancer genetic testing had limited utility for most patients. This may mean that some GPs have the false impression that there are no evidence based treatment/management protocols for patients with a proven gene mutation. This is concerning as there are many evidence-based interventions to decrease cancer risk in these patients [10]. Another GP said that no patient has requested cancer genetic testing, which might indicate a passive approach to the taking of a personal and family history and discussion about the merits of referral. Perceived roles Nearly all (94 %) the responding doctors believe that it is their duty to inform an individual at high risk for hereditary cancer that cancer genetic counselling and testing is available, reflecting a positive attitude towards cancer genetic testing. However, there remain a proportion of GPs that believe otherwise, and ways of correcting this belief need to be considered. Responding doctors appeared to show acceptance of their role in genetics. There was general agreement that their role include taking a family history, and identifying families where cancer genetic testing is indicated. More than half of doctors (60 %) said they would counsel and give information to families where cancer genetic testing is indicated, and half stated they would discuss management options for patients with a positive cancer genetic testing result. This receptiveness to cancer genetic testing has also been found in previous research [2–5, 11, 18, 19]. Limitations There are several limitations to this study. Firstly, the specialists are all from St. Vincent’s Hospital Sydney and the GPs are drawn from patients’ files in the St. Vincent’s Hospital Hereditary Cancer Clinic. This may not be representative of the general doctor population. Secondly, the overall response rate (31 %) was lower than we would have liked, especially for GPs (only 25 %). However, this was comparable to other studies in this field (for example, 35 % for Acheson et.al [12]., 28 % for Cremers et.al [15]., and 32.5 % for Mehnert et.al. [20]). Furthermore, the sample of doctors who do not refer is very small, consisting of only four doctors, none of whom are breast/ovarian or gastrointestinal specialists. This makes it difficult to draw conclusions about doctors who do not refer. Besides, there are widely unequal numbers in each specialty. All these lead to difficulties in finding relationships between knowledge and attitudes of doctors towards cancer genetic testing and their referral rates or their specialties. However, it should be
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noted that this study was meant as a pilot qualitative study which aims to find out what lessons can be learnt regarding doctors’ knowledge and attitude towards cancer genetic testing, so that future more comprehensive quantitative studies can be designed to further investigate this topic.
Conclusion Genetic factors play an important role in the development of various types of cancers and therefore doctors may come into contact with individuals and families who may benefit from a referral to hereditary cancer clinics. Encouragingly, doctors in this survey reported high referral rates to genetics services. However, there are indications that they
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may be referring inappropriately. This suggests a need for educating doctors on cancer genetic testing, especially cancer genetics referral guidelines. Fortunately, high proportions of those who completed the questionnaire were interested in receiving further information on cancer genetic testing. Further research into the effectiveness of different types of training and guidelines in leading to appropriate cancer genetic referrals is now required. Acknowledgments We thank Cassandra Shearer, Robert Kent, Louise Lynagh and Manisha Chauhan for their help in designing and carrying out this survey. We also thank Jason Chen for assistance in statistical analyses.
Appendix 1
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Appendix 2: The correct answers to the knowledge questions (Question 6, 8, 9, 10, 12)
Question no.
Question
Correct answer
6
How important are each of the factors below in your decision making on whether to refer someone for cancer genetic testing? Please rate from 1 (least important) to 5 (most important) by circling the appropriate number.
1–3 = Not important 4 & 5 = Important
Number of family members of patient with cancer
Important
Age of onset of cancer in family member(s) of patient
Important
Presence of a known mutation in a family member of patient
Important
Age of onset of cancer in patient
Important
Patients’ request
Not important
Features of patients’ disease (e.g. triple negative breast cancer or multiple colorectal polyps)
Important
Impact on further treatment
Important
Impact on future surveillance $1000–1999
Important
8
Please estimate the current cost for the first family member (the proband) to undergo cancer genetic testing?
9
Please estimate the current turnaround time for the first family member (the proband) to undergo routine cancer genetic testing? Please estimate the current turnaround time for the first family member (the proband) to undergo urgent cancer genetic testing?
4–8 weeks
Can a person with no cancer and no proven gene mutation in his/ her family be referred to a Hereditary Cancer Clinic for cancer genetic testing; if yes, please describe the circumstances under which this might be so
Yes and in the reason section, the respondent indicated that the patient was eligible for Ashkenazi testing or stated ethnicity
10
12
1–2 weeks
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Appendix 3
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a vignette-based study. Cancer 117 (23):5334–5343. doi:10.1002/ cncr.26166 McCarthy AM, Bristol M, Fredricks T, Wilkins L, Roelfsema I, Liao K, Shea JA, Groeneveld P, Domchek SM, Armstrong K (2013) Are physician recommendations for BRCA1/2 testing in patients with breast cancer appropriate? A population-based study. Cancer. doi:10.1002/cncr.28268 Cheah PY (2009) Recent advances in colorectal cancer genetics and diagnostics. Crit Rev Oncol Hematol 69(1):45–55. doi:10. 1016/j.critrevonc.2008.08.001 National Cancer Institute (2009) BRCA1 and BRCA2: cancer risk and genetic testing. National Cancer Institute Culver JO, Hull JL, Dunne DF, Burke W (2001) Oncologists’ opinions on genetic testing for breast and ovarian cancer. Genet Med 3(2):120–125 Acheson LS, Stange KC, Zyzanski S (2005) Clinical genetics issues encountered by family physicians. Genet Med 7(7):501–508 Wideroff L, Freedman AN, Olson L, Klabunde CN, Davis W, Srinath KP, Croyle RT, Ballard-Barbash R (2003) Physician use of genetic testing for cancer susceptibility: results of a national survey. Cancer Epidemiol Biomarkers Prev 12(4):295–303 Wideroff L, Vadaparampil ST, Greene MH, Taplin S, Olson L, Freedman AN (2013) Hereditary breast/ovarian and colorectal cancer genetics knowledge in a national sample of US physicians. J Med Genet 42(10):749 Cremers R, van Asperen C, Kil P, Vasen H, Wiersma T, van Oort I, Kiemeney L (2012) Urologists’ and GPs’ knowledge of
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324 hereditary prostate cancer is suboptimal for prostate cancer counseling: a nation-wide survey in The Netherlands. Fam Cancer 11 (2):195–200. doi:10.1007/s10689-011-9500-8 16. Baars MJ, Henneman L, Ten Kate LP (2005) Deficiency of knowledge of genetics and genetic tests among general practitioners, gynecologists, and pediatricians: a global problem. Genet Med 7(9):605–610 17. Doksum T, Bernhardt BA, Holtzman NA (2003) Does knowledge about the genetics of breast cancer differ between nongeneticist physicians who do or do not discuss or order BRCA testing? Genet Med 5(2):99–105
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ORIGINAL ARTICLE
Attitudes and knowledge of medical practitioners to hereditary cancer clinics and cancer genetic testing Ian Teng • Allan Spigelman
Published online: 4 December 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract Genetic testing for susceptibility for common cancers is widely available. Thus, doctors have a role in identifying and referring patients who would benefit from a consultation with a specialist in genetics. This study aims to assess doctors’ referral rates, knowledge and attitudes towards cancer genetic testing, broken down by specialty (gastrointestinal, breast/ovarian, other specialties and General Practitioners-GPs). A 4-page questionnaire was mailed out to the GPs of all patients seen in 2012 in the Hereditary Cancer Clinic of St. Vincent’s Hospital Sydney (n = 128) and all the specialists in St. Vincent’s Hospital Sydney that might refer to the HCC (n = 33). 50 questionnaires were returned (31 %). Most doctors had referred a patient for cancer genetic testing (90 %). The average proportion of patients referred was 1 in 68.5 patients with breast/ovarian specialists referring the most, followed by gastrointestinal specialists and GPs. There was suboptimal knowledge of cancer genetic testing amongst doctors. Breast/ovarian specialists were most knowledgeable, followed by gastrointestinal specialists, other specialists and GPs. There were indications of inappropriate referral amongst doctors. Most (77.6 %) doctors were willing to receive further information on cancer genetics. Nearly all (94 %) doctors believe that it is their duty to inform an
I. Teng University of New South Wales, Unit 3, 39-41 Houston Road, Kingsford, NSW 2032, Australia e-mail: [email protected]; [email protected] A. Spigelman (&) St. Vincent’s Hospital Sydney, UNSW St. Vincent’s Clinical School, Level 5, De Lacy Building, Victoria Street, Darlinghurst, NSW 2010, Australia e-mail: [email protected]
individual at high risk for hereditary cancer that cancer genetic counselling and testing is available. The majority of doctors have positive attitudes towards cancer genetic testing. Defective knowledge scores, however, indicate that doctors need further training or tools to enable them to refer patients appropriately for cancer genetic testing. Keywords Cancer genetics Genetic testing Evaluation
Introduction The Centre of Disease Control and Prevention (2013) reported that genetic tests have been developed for more than 2200 diseases and 2000 of those are available for use clinically. Inherited forms of cancer (hereditary cancer), such as breast, ovarian and colon cancer are included within these 2000 diseases. This development of cancer genetic testing has major implications for patient management; allowing medical practitioners to identify asymptomatic individuals who have inherited an increased susceptibility to cancer, whilst increasing surveillance of these individuals for early cancer detection and possibly providing prophylactic treatment to improve the patients’ outcome. With the increase in availability as well as increased patients’ awareness of cancer genetic testing, it is expected that demand for medical practitioners to provide these services to their patients will increase. Hence, medical practitioners may have to deal with the complex medical, social and ethical questions related to genetic testing [1]. They will also have to be able to appropriately refer patients for cancer genetic counselling and/or testing. These provide the rationale for an exploration of the
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attitudes and knowledge of medical practitioners towards cancer genetic testing. A number of studies, mostly surveys, have attempted to do that. From these studies, several patterns are apparent. Medical practitioners generally approve of cancer genetic testings and believe they have a role to play in genomic medicine [2]. However, this positive attitude is tempered by medical practitioners’ fears of the negative consequences of cancer genetic testing which include the psychological impact on patient and family, discrimination in jobs and insurance, and confidentiality issues [1, 3–5]. It is also obvious that a barrier against referring patients for cancer genetic testing is medical practitioners’ lack of knowledge on cancer genetic testing [2, 6]. Furthermore, many medical practitioners do not refer a patient for cancer genetic testing because they believe that a patient’s cancer genetic testing results cannot be used effectively to improve the patient’s management. Reported reasons for this include doubt about the clinical utility and viability of cancer genetic testing, perceived lack of approved guidelines for patient management after a cancer genetic testing and perceived lack of evidence-based strategies for the detection and prevention of hereditary cancer [1, 5]. Moreover, adherence of medical practitioners to guidelines regarding cancer genetic testing is poor, leading to over-referral of average-risk patients and underreferral of high-risk patients [7, 8]. However, there are no Australian studies regarding this topic, with most of the studies being conducted in USA. Besides that, most of the studies are ten or more years old. Thus, in light of recent advances and new information regarding cancer genetic testing, screening and prevention [9, 10], there is a need to evaluate the knowledge and attitudes of Australian medical practitioners towards cancer genetic testing. Hence, the purpose of this study is to evaluate and compare, in general practitioners and specialists, the attitudes to and knowledge of cancer genetic testing, and patient referral rates for cancer genetic testing. To this effect, questionnaires that aim to assess knowledge, attitudes and referral rates of cancer genetic testing were mailed out to a subset of general practitioners and specialists in St. Vincent’s Hospital (Sydney).
Materials and methods
I. Teng, A. Spigelman
It was also approved by the St Vincent’s Hospital Research Governance Office for site approval at the Hereditary Cancer Clinic; approval number LNRSSA/13/SVH/135. Study population The study population consisted of both general practitioners (GPs) and specialists (n = 161). The GPs to whom surveys were sent consisted of the GPs of all patients seen in 2012 in the Hereditary Cancer Clinic (HCC) of St. Vincent’s Hospital Sydney (n = 128). The HCC provides cancer specific genetic counselling, risk assessment and gene testing. Referrals are mostly received from doctors and specialists at St Vincent’s Public Hospital, St Vincent’s Clinic and St Vincent’s Private Hospital. Patients are also referred from outside the hospital system by GPs and other specialists in the surrounding suburbs, as well as self-referring. The specialists surveyed consists of the specialists in St. Vincent’s Hospital Sydney that might refer to the HCC (n = 33). The specialties involved include oncology, obstetrics-gynaecology (ob-gyn) and internal medicine. Survey instrument The survey instrument was a 4-page self-administered questionnaire (Appendix 1), developed using questions from previous surveys testing the knowledge and attitudes of health practitioners towards cancer genetic testing. The questions in this questionnaire are aimed at eliciting referral rates, knowledge and attitudes towards cancer genetic testing. Response categories for questions were either yes/no, multiple choice, Likert scales, and short answer. Procedure The questionnaire was mailed out on the 26th of July 2013 along with a cover letter explaining the aims of the study and reassuring the respondents that their responses would be anonymous. Two weeks later, a follow up letter was mailed, reminding doctors to complete and return the questionnaire. The letter also gave the option of requesting another questionnaire if the original one was misplaced/ discarded. Two weeks after that, a similar follow-up letter was mailed. Doctors’ consent to participate was inferred by completion and return of the questionnaire.
Ethics approval Analysis This study was considered as Low and Negligible Risk Research and was reviewed and validated by the St Vincent’s Hospital Human Research Ethics Committee. The approval number was LNR/13/SVH/125.
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The aim of the analysis is to extract both quantitative and qualitative information regarding referral rates, knowledge and attitudes of doctors towards cancer genetic testing.
Attitudes and knowledge of medical practitioners
Descriptive analyses (means and standard deviations or frequency tables) were performed on the answers to all the questions, and these were stratified by specialties. Statistical methods such as Independent samples Kruskal-Willis test, correlation tests (i.e. Chi-square test, Phi & Cramer’s V), and regression analyses were then used to find out whether different specialties responded differently, and what the relationships between the answers to different questions and referral rates were. The statistical software IBM SPSS Statistics Version 21 was used for this. For referral rates, doctors were asked whether they referred (yes or no). The percentages of doctors who refer were then calculated. From the patients’ files, the actual GP and specialist referral rate was calculated and then compared with this study’s self-reported referral rate. The questionnaire also asked doctors to state the proportion of patients they refer (i.e. 1 in x patients). These proportions were then converted to numerical data for entry into SPSS by dividing 1 by x. For example, doctors who referred 1 in 10 of their patients, were given a value of 0.1 (1 divided by 10). Doctors who do not refer are given a value of 0.0. For questions that assess doctors’ knowledge, several options were listed and doctors were asked to choose the correct answer. ‘‘Appendix 2’’ shows the correct answers to the 5 knowledge questions (Questions 6, 8, 9, 10, and 12). To assess whether doctors refer appropriately, two questions were formulated, question 6 and 12. Question 6 asks doctors who refer, ‘‘How important is each of the factors below in your decision making on whether to refer someone for cancer genetic testing?’’ The answer was in Likert scales (1–5). Doctors that selected 1–3 were categorized as labelling that factor ‘‘not important’’ and those that selected 4 or 5 were categorized as ‘‘important’’. Then, depending on whether said factor is indeed important to consider before referral (refer to ‘‘Appendix 2’’), doctors’ responses were labelled as correct (1) or incorrect (0). Question 12 was, ‘‘Can a person with no cancer and no proven gene mutation in his/her family be referred to a Hereditary Cancer Clinic for cancer genetic testing; if yes, please describe the circumstances under which this might be so.’’ The correct answer is ‘‘Yes’’, and the respondent must have indicated that the patient was eligible for Ashkenazi testing or mentioned ethnicity of patient. Question 7 assessed the reason some doctors do not refer. For doctors who stated they did not refer patients for cancer genetic testing (n = 5), they were given a list of reasons and asked to rate how important said reasons are in preventing them from referring. They were asked to rate from 1 to 5, 5 being the most important hindrance. The mean of each response were then calculated. The higher the mean, the more important the reason is.
313 Table 1 Number of doctors who have referred a patient for cancer genetic testing Ever referred? No Clinical specialty
Total
Total
Yes
Breast/ovarian
0
4
4
Gastrointestinal
0
10
10
GP Other
4 1
28 3
32 4
45
50
5
Results Overall, 31 % of doctors surveyed (50 out of 161) returned the questionnaire. The response rates differed between specialties, with 25 % (32/128) of GPs, and 54.5 % (18/33) of specialists returning the questionnaire. Of the specialists, 66.6 % (10/15) of those in gastrointestinal, 44.4 % (4/9) of those in breast/ovarian and 44.4 % (4/9) of those in other specialties returned the questionnaire. The specialties included in the ‘‘other’’ group are medical oncology, radiation oncology, general surgery and head and neck surgery. GPs had practiced for the longest time period (23.6 ± 10.2 years); doctors in the field of breast/ovarian practiced for 22.5 ± 5 years; and those who specialized in gastrointestinal practiced for 18.6 ± 9.9 years. Those in other specialties have an average of 16.8 ± 4.7 years in practice. Referral rates Of the 50 respondents, 45 (90 %) indicated that they have referred a patient for cancer genetic testing. All breast/ ovarian specialists and gastrointestinal specialists have referred. For GPs, 87.5 % (28 out of 32) have referred patients for cancer genetic testing; for others, 75 % (3 out of 4) have referred. Out of the 5 that have never referred, 4 were GPs and 1 was from ‘‘other’’ specialty (head and neck surgeon). From the patients’ files from which the mailing list of GPs was obtained, only 18 out of 144 (12.5 %) patients were referred by their GPs, and 113 out of 144 patients (78.5 %) were referred by their specialists (Table 1). In terms of proportion of patients referred, doctors referred an average of 1 in 68.5 patients. GPs referred 1 in 790 patients; gastrointestinal specialists referred 1 in 34 patients; breast/ovarian specialists referred 1 in 15 patients; and those in other specialties referred 1 in 33 patients. Oneway ANOVA as well as independent samples Kruskal– Wallis test showed that there were significant differences between the groups (p \ 0.001). Breast/ovarian specialists
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Table 2 Responses of doctors to question 6 Question/Factor
Percentage of doctors who were correct, % (n = 44)
Percentage of doctors who were correct out of each specialty, % Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
GP (n = 27)
Other (n = 3)
Number of family members of patient with cancer
90.9
100.0
90.0
88.9
100.0
Age of onset of cancer in family member(s) of patient
90.9
100.0
100.0
85.2
100.0
Presence of a known mutation in a family member of patient
95.5
100.0
100.0
92.6
100.0
Age of onset of cancer in patient
79.5
75.0
90.0
77.8
66.7
Patients’ request
65.9
75.0
80.0
55.6
100.0
Features of patients’ disease (e.g. triple negative breast cancer or multiple colorectal polyps) Impact on further treatment
65.9
50.0
60.0
70.4
66.7
56.8
50.0
50.0
55.6
100.0
Impact on future surveillance
77.3
75.0
80.0
77.8
66.7
Average
77.8375
78.125
81.25
75.4875
87.5125
referred the most (p \ 0.06), followed by gastrointestinal specialists (p \ 0.05) and GPs came in last (p \ 0.05). However, other specialties had no significant differences with any of the three groups above. When asked when the last time the doctors referred a patient was, most (29/67.4 %) indicated ‘‘last 6 months’’. Stratified by specialties, all breast/ovarian specialists have referred in the last 6 months. Only GPs said that they referred in the last 24 months.
cancer (13), and to reassure an anxious and insisting patient (7). 5 doctors gave characteristics of the cancer/tumour as the reason. There was a significant correlation between answering ‘‘No’’ and referral rates (p \ 0.01). From regression, those that answered ‘‘no’’ tended to refer less patients for cancer genetic testing (p \ 0.05) (Table 3).
Knowledge of referral guidelines
When asked to estimate the cost of the first family member (proband) to undergo cancer genetic testing, more than half (56.3 %) of doctors selected the correct answer. However, out of this 27, one selected this by guessing (‘‘no clue’’ was written beside the question). Those in other specialties were most accurate, with 75 % (3/4) selecting the correct option. 60 % (6/10) of gastrointestinal specialists, 60 % (18/30) of GPs, and none of the breast/ovarian specialists were correct. Phi and Cramer’s V showed significant correlation (p \ 0.05) between estimated cost and clinical specialty. No significant relationship was found between estimated cost of cancer genetic testing and referral rate, from correlation tests and regression. No significant relationship found between being correct and referral rate.
To assess whether doctors refer appropriately, two questions were formulated. The first asks doctors who refer, ‘‘How important is each of the factors below in your decision making on whether to refer someone for cancer genetic testing?’’ Table 2 shows the responses of doctors to this question. There was also an option for doctors to write down other factors that influence their decision-making in whether to refer a patient for cancer genetic testing. One wrote gender & ethnicity of relative. The second question was, ‘‘Can a person with no cancer and no proven gene mutation in his/her family be referred to a Hereditary Cancer Clinic for cancer genetic testing; if yes, please describe the circumstances under which this might be so.’’ Only 6 % (3/50) of doctors responded correctly. All three were breast/ovarian specialists. None of the doctors in the gastrointestinal, ‘‘other’’ or GP category were correct. 29 (58 %) of doctors replied ‘‘Yes’’ but gave the incorrect reason. For those that selected ‘‘Yes’’, the two most common reasons were if the patient had a strong family history of
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Knowledge of the cost of cancer genetic testing
Knowledge of the time taken for cancer genetic testing Table 4 shows the responses of doctors, stratified by profession when asked about the estimated turnaround time for routine cancer genetic testing. Only 22.9 % (11) of doctors answered correctly, with 30.0 % of gastrointestinal specialists’ answering correctly,
Attitudes and knowledge of medical practitioners
315
Table 3 Responses to question 8 Estimated cost for proband to undergo cancer genetic testing, $
Frequency (percentage) (n = 48)
Clinical specialty Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
\1000
12 (25.0 %)
2
4
6
1000–1999
27 (56.3 %)
0
6
18
3
2000-2999 [3000
5 (10.4 %) 4 (8.3 %)
0 2
0 0
4 2
1 0
GP (n = 27)
Other (n = 3)
Table 4 Responses of doctors to question 9
Table 5 Responses of doctors to question 10
Frequency (percentage) (n = 48)
Frequency (percentage) (n = 48)
GP (n = 30)
Other (n = 4) 0
Clinical specialty Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
\1
0 (0 %)
0
0
0
1–2
2 (4.2 %)
0
0
1
1
2–4
20 (41.7 %)
2
5
12
1
4–8
11 (22.9 %)
1
3
6
1
[8
15 (31.3 %)
1
2
11
1
Turnaround time for proband to undergo urgent cancer genetic testing, weeks
Frequency (percentage) (n = 48)
0
Clinical specialty Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
GP (n = 27)
Other (n = 3)
\1
2 (4.2 %)
1
0
1
0
1–2
15 (31.3 %)
1
4
9
1
2–4 4–8
15 (31.3 %) 10 (20.8 %)
2 0
3 2
8 7
2 1
[8
6 (12.5 %)
0
1
5
0
followed by breast/ovarian (25.0 %) and other specialists (25.0 %), and GPs (20.0 %). Table 5 shows the responses of doctors, stratified by profession when asked about the estimated turnaround time for urgent cancer genetic testing. For urgent cancer genetic testing, only 31.3 % (15) estimated correctly. The most accurate specialty was gastrointestinal (40.0 %) followed by GPs (30.0 %), and breast/ovarian and other specialties, both at 25.0 %. Desire for further information Most (77.6 %–38/49) of doctors expressed a desire for further information regarding cancer genetic testing. Most gastrointestinal specialists (90 %) and GPs (84 %) wanted more information. On the other hand, only a few of the breast/ ovarian specialists (33.3 %) and ‘‘other’’ specialists (25 %) wanted further information. Independent samples Kruskal– Wallis test showed that the differences between groups were
significant (p \ 0.05). Further analysis by regression showed that the desire for further information is highest in gastrointestinal specialists (p \ 0.05), followed by GPs (p \ 0.05). Breast/ovarian specialists and ‘‘other’’ specialists had significantly lower (p \ 0.05) desire for further information, but no significant differences between them. Reason for not referring Table 6 shows the responses of doctors to Question 7. 4 of the 5 doctors who answered this question were GPs and the last was from ‘‘other’’ specialty, specifically a head and neck surgeon. Doctors were given an option to state other reasons for not referring patients for cancer genetic testing. One GP stated that there is no treatment available whilst another GP said that no patient has requested cancer genetic testing. The head and neck surgeon said that cancer genetic testing had limited utility for most patients.
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Table 6 Responses of doctors to question 7 Reason for not referring
Mean (n = 5)
Mean by specialty GP (n = 4)
Other (n = 1)
Cancer genetic testing is not helpful
2.400
2.75
1
Cancer genetic testing may cause psychological distress to the patient
2.200
2.5
1
Patient confidentiality/privacy will be at risk
1.400
1.5
1
Cancer genetic testing is too costly
2.200
2.5
1
Cancer genetic testing takes too long
1.800
2.0
1
Patients with a positive test result may face discrimination at work or when seeking insurance
2.600
2.5
3
A positive result in cancer genetic testing may negatively affect relationship with patient’s family and relatives
3.000
3.0
3
Perceived roles When asked, ‘‘Do you think it is your duty of care to inform an individual at high risk for hereditary cancer that cancer genetic counselling and testing is available?’’ most (n = 47, 94.0 %) doctors replied affirmatively. All three of those who said no were GPs. Question 13 asked doctors to select the actions that they carry out in their practice. The results are tabulated in Table 7.
Discussion
(2003–2013) or a more likely explanation, given that the cohort of doctors surveyed came from the HCC files, is that the sample is biased. There was wide discrepancy between the self-reported GP referral rate (87.5 %) and the actual referral rate calculated from patient files (12.5 %). Similarly, for specialists, there was significant difference between the selfreported referral rate (94.4 %) and the actual referral rate (78.5 %). These may mean that the doctors referred to other hereditary clinics, or they overestimated the number of patients that they referred, or that they refer but happened not to refer in 2012. It may also mean that the doctors who did not respond to this survey were those that tended not to refer patients for cancer genetic testing.
Referral rates Knowledge Of 50 doctors, 45 (90 %) indicated they have referred. This differs greatly from other studies, all of which have less than 50 % referral rates [11–13]. In terms of absolute numbers, doctors in this study referred an average of 1 in 68.5 patients which is more than the 2 patients a year out of 30 patients daily found in another study [5]. These may indicate a true difference in referral rates in the past decade
Overall, doctors had a suboptimal knowledge of cancer genetic testing. For example, one doctor incorrectly stated that gender is important in deciding whether to refer a patient for cancer genetic testing. Furthermore, some doctors were honest enough to write down on the questionnaire that they had ‘‘no clue’’ to some of the questions. This
Table 7 Responses of doctors to question 13 Actions
Take a family history
Frequency and percentage of doctors who carry the action out Overall (n = 50)
Breast/ovarian (n = 4)
Gastrointestinal (n = 10)
GP (n = 32)
Other (n = 4)
50 (100 %)
4
10
32
4
Identify families where cancer genetic testing is indicated
38 (76 %)
3
9
24
2
Counsel and give information to families where cancer genetic testing is indicated
30 (60 %)
2
5
21
2
Obtain informed consent for cancer genetic testing from patient before the genetic testing
10 (20 %)
1
0
9
0
Discuss management options for a patient with positive cancer genetic testing result
25 (50 %)
3
5
15
2
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Attitudes and knowledge of medical practitioners
finding of suboptimal knowledge is similar to many other studies done in Europe and in USA [2, 3, 6, 14]. When analysed by specialty, breast/ovarian specialists seemed to be most knowledgeable about cancer genetic testing, followed by gastrointestinal specialists and ‘‘other’’ specialists, and lastly GPs. This finding is similar to those reported in other studies. These state that oncologists were most knowledgeable, followed by obstetric-gynaecologists, other specialists and lastly GPs [2, 14–17]. More than half (58 %) of doctors said they would refer a patient with no cancer and no proven gene mutation in his/ her family for cancer genetic testing but gave the incorrect reason. This may indicate that many doctors refer patients who do not need cancer genetic testing to hereditary cancer clinics, leading to over-referral. This correlates with a recent study that addressed adherence to guidelines on cancer genetic testing for BRCA1/2. Trivers et.al. [7] found that 29 % of 1878 responding doctors incorrectly referred average-risk women for cancer genetic testing. No statistically significant correlation could be found between doctors’ knowledge and their referral rates. This is probably due to the small sample size in this study. Desire for further information Breast/ovarian specialists and ‘‘other’’ specialists have the least desire for further information on cancer genetic testing. This may make it difficult for educational efforts aimed at improving their knowledge on cancer genetic testing to be successful. GPs had the worst knowledge scores, but nearly all (84 %) wanted further information on cancer genetic testing. These may show that GPs realize that their knowledge of cancer genetics may be insufficient and are willing to correct this by receiving further information on cancer genetic testing. Reasons for not referring ‘‘A positive result in cancer genetic testing may negatively affect relationship with patient’s family and relatives’’ was found to be the most important reason for not referring patients for cancer genetic testing, followed closely by ‘‘concerns on discrimination at work or in insurance’’. Interestingly, ‘‘patient confidentiality/privacy will be at risk’’ was given the least importance. This contrasts with the widespread emphasis placed on patient privacy and confidentiality. An example can be seen in the informed consent form for cancer genetic testing. There is a section labelled ‘‘Sharing the result’’ where the patient can decide whether to consent to his/her cancer genetic testing result being given to relevant family members and health professionals (‘‘Appendix 3’’).
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One GP stated that ‘‘there is no treatment’’ whilst a head and neck surgeon said that cancer genetic testing had limited utility for most patients. This may mean that some GPs have the false impression that there are no evidence based treatment/management protocols for patients with a proven gene mutation. This is concerning as there are many evidence-based interventions to decrease cancer risk in these patients [10]. Another GP said that no patient has requested cancer genetic testing, which might indicate a passive approach to the taking of a personal and family history and discussion about the merits of referral. Perceived roles Nearly all (94 %) the responding doctors believe that it is their duty to inform an individual at high risk for hereditary cancer that cancer genetic counselling and testing is available, reflecting a positive attitude towards cancer genetic testing. However, there remain a proportion of GPs that believe otherwise, and ways of correcting this belief need to be considered. Responding doctors appeared to show acceptance of their role in genetics. There was general agreement that their role include taking a family history, and identifying families where cancer genetic testing is indicated. More than half of doctors (60 %) said they would counsel and give information to families where cancer genetic testing is indicated, and half stated they would discuss management options for patients with a positive cancer genetic testing result. This receptiveness to cancer genetic testing has also been found in previous research [2–5, 11, 18, 19]. Limitations There are several limitations to this study. Firstly, the specialists are all from St. Vincent’s Hospital Sydney and the GPs are drawn from patients’ files in the St. Vincent’s Hospital Hereditary Cancer Clinic. This may not be representative of the general doctor population. Secondly, the overall response rate (31 %) was lower than we would have liked, especially for GPs (only 25 %). However, this was comparable to other studies in this field (for example, 35 % for Acheson et.al [12]., 28 % for Cremers et.al [15]., and 32.5 % for Mehnert et.al. [20]). Furthermore, the sample of doctors who do not refer is very small, consisting of only four doctors, none of whom are breast/ovarian or gastrointestinal specialists. This makes it difficult to draw conclusions about doctors who do not refer. Besides, there are widely unequal numbers in each specialty. All these lead to difficulties in finding relationships between knowledge and attitudes of doctors towards cancer genetic testing and their referral rates or their specialties. However, it should be
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noted that this study was meant as a pilot qualitative study which aims to find out what lessons can be learnt regarding doctors’ knowledge and attitude towards cancer genetic testing, so that future more comprehensive quantitative studies can be designed to further investigate this topic.
Conclusion Genetic factors play an important role in the development of various types of cancers and therefore doctors may come into contact with individuals and families who may benefit from a referral to hereditary cancer clinics. Encouragingly, doctors in this survey reported high referral rates to genetics services. However, there are indications that they
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may be referring inappropriately. This suggests a need for educating doctors on cancer genetic testing, especially cancer genetics referral guidelines. Fortunately, high proportions of those who completed the questionnaire were interested in receiving further information on cancer genetic testing. Further research into the effectiveness of different types of training and guidelines in leading to appropriate cancer genetic referrals is now required. Acknowledgments We thank Cassandra Shearer, Robert Kent, Louise Lynagh and Manisha Chauhan for their help in designing and carrying out this survey. We also thank Jason Chen for assistance in statistical analyses.
Appendix 1
Attitudes and knowledge of medical practitioners
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Appendix 2: The correct answers to the knowledge questions (Question 6, 8, 9, 10, 12)
Question no.
Question
Correct answer
6
How important are each of the factors below in your decision making on whether to refer someone for cancer genetic testing? Please rate from 1 (least important) to 5 (most important) by circling the appropriate number.
1–3 = Not important 4 & 5 = Important
Number of family members of patient with cancer
Important
Age of onset of cancer in family member(s) of patient
Important
Presence of a known mutation in a family member of patient
Important
Age of onset of cancer in patient
Important
Patients’ request
Not important
Features of patients’ disease (e.g. triple negative breast cancer or multiple colorectal polyps)
Important
Impact on further treatment
Important
Impact on future surveillance $1000–1999
Important
8
Please estimate the current cost for the first family member (the proband) to undergo cancer genetic testing?
9
Please estimate the current turnaround time for the first family member (the proband) to undergo routine cancer genetic testing? Please estimate the current turnaround time for the first family member (the proband) to undergo urgent cancer genetic testing?
4–8 weeks
Can a person with no cancer and no proven gene mutation in his/ her family be referred to a Hereditary Cancer Clinic for cancer genetic testing; if yes, please describe the circumstances under which this might be so
Yes and in the reason section, the respondent indicated that the patient was eligible for Ashkenazi testing or stated ethnicity
10
12
1–2 weeks
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Appendix 3
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Attitudes and knowledge of medical practitioners
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