Research Article
J Fam Med. 2015;2(2): 1024.
Primary Care Physicians’ Experience and Confidence with Genetic Testing and Perceived Barriers to Genomic Medicine
Chambers CV¹*, Axell-House DB², Mills G¹,Bittner-Fagan H³, Rosenthal MP³, Johnson M4 and Stello B4
¹Department of Family and Community Medicine, Thomas Jefferson University, USA
²Sidney Kimmel Medical College at Thomas Jefferson University, USA
³Department of Family and Community Medicine, Christiana Care Health System, USA
4Department of Family Medicine, Lehigh Valley Hospital and Health Network, Allentown, Pennsylvania, USA
*Corresponding author: Chambers CV, Department of Family and Community Medicine, Thomas Jefferson University, USA
Received: March 03, 2015; Accepted: March 31, 2015; Published: April 01, 2015
Abstract
Purpose: Genetic testing is progressing towards use of patients’ genomes for personalized medicine. Primary care physicians (PCPs) may use genetic tests to screen and assess risk. However, PCPs’ current preparedness for the expanding integration of genetics into practice is uncharacterized. We examined primary care physicians’ perceptions of and experience with genetic testing.
Methods: An anonymous survey was mailed to PCPs across three regional health networks querying opinions of, experience with, confidence in, and perceived barriers to genetic testing.
Results: The survey response rate was 37.8%. Respondents believed learning about new genetic advances was important to clinical practice (67.0%). A minority (19.0%) had ordered genetic testing in six months, with cancer risk testing the most frequently ordered. Respondents were not confident in the skills required for using genetic testing in practice. Few respondents felt that they had time to counsel about genetic risk (9.5%) or that most patients could comprehend the concept of risk (27.0%).
Conclusions: Primary care physicians had a high opinion of using genetic testing in medicine, but reported little experience or confidence incorporating genetic testing into practice. A majority perceived time constraints and patient comprehension as barriers. These data demonstrate a need for genetics educational resources for physicians and patients.
Keywords: Genetics; Primary care; Family medicine; Personalized medicine; Genomics
Abbreviations
PCP: Primary Care Physician; DTC: Direct to Consumer
Introduction
From the completion of the Human Genome Project in 2003 to the recently mandated withdrawal of the genome screening products of 23 and Me™ (Mountain View, California) there has been exponential development in health-related genomic information [1]. A glimpse of the potential benefit of genomic information in healthcare has been realized in targeted chemotherapy [2], tailored warfarin therapy [3], diagnosis of Mendelian disease [4], and expanded newborn screening [5]. These successes have heralded the development of “personalized medicine,” which incorporates a patient’s unique genomic make-up into individualization of disease prevention and treatment
Genomic science is developing rapidly, but much of basic science research remains too ambiguous to translate to clinical medicine. At the benchtop, DNA sequencing is still too inaccurate to use on a large scale, and once a DNA sequence is completed, the significance of each discovered variant is still largely unknown [6]. Despite these barriers, the public’s interest in genetics fueled the development of companies like 23 and Me™, a company that provided Direct-to-Consumer (DTC) genetic tests. In November, 2014, the FDA suspended the company’s health-related genetic reporting services due to lack of validation of the genetic tests and their uses [7], but the possibility of new companies arising remains.
Primary Care Physicians (PCPs) play a unique role in medical genetics in that they will likely be the first providers to assess patient need for genetic testing [8]. PCPs are also the most likely physicians to be presented with DTC test results given their longterm relationships with patients [9-10]. PCPs have been anticipating the clinical impact of genetic tests in their practice since before the completion of the Human Genome Project [11]. Since then, many PCPs overall continue to note that they lack confidence, knowledge, and experience with genetic tests despite their anticipation [12-14]. These PCPs identified a need for increased education for themselves to reliably interpret test results [15-20], access to genetic counselors for referral [21], and increased education for the public to prevent anxiety and misinterpretations of results [22-23]. Further, they identified that ethical controversy exists over incidental findings, informed consent, and the ever-changing nature of genetic knowledge [24-27].
In 15 years of study into this area, primary care providers have reported that they perceive themselves deficient in assimilating the skills that they feel are necessary to participate in genomics medicine. The purpose of our study was to determine whether PCPs have improved in experience, confidence, and ability to order genetic testing since the recent surge of clinically relevant tests and wellpublicized rise and fall of affordable DTC genetic tests.
Methods
Survey population and recruitment
Three regional networks of PCPs in the Delaware Valley participated in the study: 1) Jeff Care, an organization of PCPs affiliated with Thomas Jefferson University; 2) the Lehigh Valley Health Network, including its Practice-Based Research Network; and 3) the Christiana Care Health System and the Delaware Academy of Family Physicians.
Physicians were invited to participate in January, 2013. A postcard with the investigators’ signatures and respective health system logos was mailed to every provider within the three networks to request his or her participation. Two weeks later, a packet was mailed containing a cover letter describing the project in detail, a link to an online version of the survey, a printed copy of the survey, a stamped and addressed return envelope, and a $5 gift card as remuneration for their time. The providers were informed that their surveys would remain anonymous. Consequently, non-responders were not identifiable and no follow-up emails or letters were sent.
Survey design
Investigators created a novel survey through an iterative process consisting of 20 questions, 5 of which had multiple sub-questions for a total of 50 answerable units. Thirty-four questions used a Likert scale, five were dichotomous (yes/no), six had multiple choices, three were “check-all-that-apply,” and two were free text. All “checkall- that-apply” questions also included an “other” option with an accompanying free text box for description. The survey allowed participants to skip questions.
The survey consisted of five informal sections: 1) Demographic and practice information; 2) Opinions regarding genetic testing; 3) Experience with genetic testing; 4) Confidence in tasks in evaluating and managing genetic disease; and 5) Perceived barriers to implementing genomic medicine.
Funding and approval
The study was funded through an internal grant through the Dean’s Office of Sidney Kimmel Medical College. The study was reviewed and approved by the Institutional Review Boards representing each of the participating health networks.
Data analysis
Survey data were entered into Excel for analysis. Personal characteristics were described as frequencies and percentages. The personal characteristics included age, gender (male, female), practice type (academic/private, rural/suburban/urban), specialty (family medicine, internal medicine, other), affiliation (Jeff Care, LVHN, CCHS/DAFP), and Electronic Medical Record (EMR) use.
Data were evaluated by descriptive statistics and comparisons of categorical responses from different groups were made using 2x2 contingency tables and Fisher’s two-tailed exact test. Descriptive statistics include non-responder rates.
Results
Survey response
A total of 833 postcards/surveys were sent to PCPs within the three networks. Of these, 315 surveys were returned resulting in an overall response rate of 37.8%. Less than a quarter (23.2%) of responders wrote free text box answers, which were mostly used to further describe their practices and did not contribute to the results.
Demographics
Slightly more than half of the respondents were male (54.1%) or between the ages of 45 and 64 (53.5%). Regarding specialty, 65.8% were family medicine physicians, 22.6% were internal medicine physicians, with 11.6% reporting other specialties including pediatrics, emergency medicine, geriatrics, and palliative care. Additional respondent demographic characteristics are listed in Table 1.
n
%
Gender
Male
166
54.1
Female
141
45.9
Age
25-34
48
15.6
35-44
78
25.3
45-54
86
27.9
55-64
79
25.6
65-74
11
3.6
= 75
6
1.9
Clinical Role
Family Medicine Physician
204
65.8
Internal Medicine Physician
70
22.6
Other
36
11.6
Practice Setting
Rural
20
10.0
Suburban
108
54.0
Urban
66
35.0
Multiple
22
11.0
Practice Type
Academic
92
29.2
Private
106
33.7
Both
12
3.8
No option chosen
105
33.3
Healthcare Affiliate
JeffCare
68
22.3
CCHS/DAFP
129
42.3
LVHN
108
35.4
Use EMR
275
89.0
Table 1: Demographics of the Respondents.
Opinions of genetic testing
Participants were asked their opinions regarding genetic testing. Approximately two-thirds of respondents agreed that learning about new advances in genetic testing was important to their practice (67.0%). Slightly less agreed that the genetic risk contributes a clinically meaningful portion of overall disease risk (64.8%). Very few agreed to the statement that physicians should consider genetic testing with all patients (15.9%).
Experience with genetic testing
A minority of respondents had ordered genetic testing (19.0%); the most frequent tests ordered were cancer risk testing (n=29), preconception/prenatal testing (n=11), and pharmacogenomic testing (n=9). A minority of respondents had consulted with a genetics counselor (18.4%) in the past six months, with the most frequent consultations for cancer risk testing (n=49) and prenatal testing (n=11).
The majority of respondents had initiated a discussion about genetic testing less than monthly (80.6%). Similarly, 88.6% of respondent’s reported being asked about genetic testing by patients less than monthly.
Confidence in genetics and genetic testing
Participants were asked how confident they were in their ability to perform seven tasks in evaluating and managing diseases with a genetic basis (Table 2). Physicians were most confident in “ability to take a thorough family history” (67.3%) and least confident in “ability to order genetic testing for hereditary cancers” (23.8%).
Confidence
None
Low
Some
High
Very High
Take a thorough family history
10.2%
21.3%
46.0%
17.8%
3.5%
Counsel patients about risk reduction strategies based on the results of genetic testing
12.4%
27.0%
32.1%
19.4%
7.6%
Assess risk of hereditary disease
11.1%
30.2%
42.2%
11.7%
2.5%
Build a family medical history pedigree chart
13.7%
28.9%
33.7%
17.8%
4.1%
Counsel patients about whether or not to have genetic counseling
10.5%
36.2%
39.4%
11.1%
1.3%
Discuss risks, benefits, limits to genetic testing for hereditary cancers
19.4%
38.1%
32.4%
7.9%
0.6%
Order genetic testing for hereditary cancers
23.2%
45.4%
23.8%
4.8%
1.3%
Table 2: Primary care physicians’ confidence in ability to perform evaluation and management tasks for diseases with a genetic basis.
Physicians aged 25-44 were more confident than physicians aged 45-54 in their ability to take a thorough family history (73.8% vs. 60.5%, p<0.05), build a family medical history pedigree chart (62.7% vs. 48.8%, p<0.05), and discuss risks, benefits, and limits to genetic testing for hereditary cancers (46.8% vs. 32.6%, p<0.05).
Physicians who had higher confidence ordered more genetic testing and were more likely to consult with a genetic counselor (Table 3). Physicians who had higher confidence more often agreed that genetic testing is important to their practice (all tasks, p<0.0001) and that genetics contributes a meaningful portion to disease (all tasks, p<0.05, except “order genetic testing for hereditary cancers” p=0.289).
Ordered Genetic Testing in 6 mo
Consulted with genetic counselor in 6 mo
Yes
p-value
Yes
p-value
Take a thorough family history
0.0469
0.1251
Confident (n=211)
22.3%
20.8%
Not Confident (n=103)
12.6%
13.6%
Build a family medical history pedigree chart
0.1127
0.0125
Confident (n=174)
22.4%
23.6%
Not Confident (n=140)
15.0%
12.1%
Assess risk of hereditary disease
0.0013
0.5587
Confident (n=177)
25.4%
19.8%
Not Confident (n=137)
10.9%
16.8%
Order genetic testing for hereditary cancers
0.0001
0.0167
Confident (n=93)
35.5%
26.9%
Not Confident (n=221)
12.2%
14.9%
Discuss risks, benefits, limits to genetic testing for hereditary cancers
0.0082
0.0379
Confident (n=128)
26.6%
24.2%
Not Confident (n=186)
14.0%
14.5%
Counsel patients about whether or not to have genetic counseling
0.0016
0.0005
Confident (n=162)
25.9%
25.9%
Not Confident (n=152)
11.8%
10.5%
Counsel patients about risk reduction strategies based on the results of genetic testing
0.0054
0.0047
Confident (n=185)
24.3%
23.8%
Not Confident (n=129)
11.6%
10.9%
Table 3: Confidence of PCPs based on experience. Percentage of respondents who had “some,” “high” or “very high” confidence in ability to perform tasks for geneticbased disease if they had or had not ordered genetic testing or consulted a genetic counselor in the past 6 months.
Confidence did not vary significantly across practice type (academic/private) or setting (rural/suburban/urban).
Confidence in counseling on common genetic diseases in the primary care setting
Physicians were surveyed on how confident they were in counseling patients in the outpatient setting about genetic issues relevant to primary care (Table 4). The vast majority of physicians were confident in counseling about newborn screening (93.2%). Physicians were least confident in counseling about Familial Adenomatous Polyposis (26.6%).
Some
High
Very High
Total
Newborn Genetic screening
24.7%
57.1%
11.4%
93.2%
Hereditary non-polyposis colorectal cancer
38.2%
22.0%
0.6%
60.8%
MEN syndromes
36.6%
16.5%
3.6%
56.6%
Long QT syndrome
32.6%
16.8%
3.2%
52.6%
Hemochromatosis
30.0%
14.5%
3.9%
48.4%
Pharmacogenomics
37.1%
9.4%
1.3%
47.7%
Hereditary breast and ovarian cancer syndrome
34.9%
10.4%
0.7%
45.9%
Factor V Leiden
27.9%
9.4%
1.6%
39.0%
Prenatal genetic screening
24.1%
6.2%
1.0%
31.3%
Huntington Disease
23.6%
6.5%
0.3%
30.4%
Familial adenomatous polyposis
21.4%
4.9%
0.3%
26.6%
Table 4: Percentage of respondents who had “some,” “high” or “very high” confidence in counseling about a specific genetic disease or screening panel.
Barriers to incorporating genetic/genomic testing into practice
Respondents were asked about barriers to incorporating genetic/ genomic testing into their practice in two different ways.
First, they were asked how much they agreed with statements about potential barriers to the routine incorporation of genetic testing into their clinical practice (Table 5). Very few respondents believed they had enough time to counsel patients about genetic risk (9.5%) or that patients could understand the concept of risk (27.0%). Very few physicians felt that they had adequate resources in their practices to help patients understand genetic risk (4.8%); somewhat more respondents felt that their hospital or network had such resources (29.8%).
Agree
Strongly Agree
Total
I have enough time to counsel patients about genetic risk
9.2%
0.3%
9.5%
Most patients can understand the concept of genetic risk
25.7%
1.3%
27.0%
In my practice, I have adequate resources to help patients understand genetic risk
4.8%
0.0%
4.8%
My hospital or network has adequate resources to help patients understand genetic risk
24.4%
5.4%
29.8%
Table 5: Primary care physicians’ evaluation of barriers to incorporating genetic risk assessment in primary care. Percentage of physicians agreeing with the following stand-alone statements.
The second item was a clinical scenario with a patient wishing to discuss Direct-to-Consumer (DTC) genetic test results. Respondents rated how important various barriers were to discussing the test results (Table 6). The most important barrier was a personal sense of inadequate knowledge (83.7%). The potential barrier that was identified as least important was lack of reimbursement (49.8%).
Somewhat Important
Very Important
Total
Inadequate Knowledge (self)
29.2%
54.5%
83.7%
Lack of Time
32.5%
41.7%
74.2%
Potential ethical dilemmas
33.7%
35.6%
69.3%
Lack of current relevance to medical decisions
34.1%
32.5%
66.6%
Lack of Reimbursement
25.2%
24.6%
49.8%
Table 6: Laboratory values at hospital admission.
Discussion
A majority of primary care physicians in our study had a favorable opinion of genetic testing, but little collective experience ordering genetic tests, consulting genetic counselors, or initiating discussions of genetic testing with patients. Other studies of primary care physicians report a similarly positive opinion of genetic testing. However, the rate of ordering genetic testing or consulting with a genetic counselor in our study is less than half the rate in other studies [15, 28-29], a finding that may be attributable to the specialty mix of our population. Although our study found no significant difference between the specialties in percentage who had ordered genetic testing, previous research has demonstrated that family medicine physicians order fewer genetic tests than internal medicine physicians, opting instead to refer for testing [29-30].
The most frequently cited reason for ordering both genetic testing and genetics consultation was for the assessment of cancer risk. This is consistent with prior surveys indicating that breast and ovarian cancer risk assessment are the most common reasons PCPs order genetic testing [15, 28]. Most PCPs have familiarity with the increased risk of breast and ovarian cancer in a patient with first-degree relatives affected and has developed confidence in recommending genetic testing for appropriate patients [12-14]. Although primary care physicians are also aware of the genetic basis of many other hereditary disorders, they demonstrate low levels of knowledge and confidence in recognizing clinical scenarios where the testing is indicated [31- 34]. Electronic medical systems may offer help with the integration of this new technology into practice. Our respondents reported a high rate of EMR use, reflecting national trends. Electronic medical records could potentially be programmed to incorporate genomic information and detailed family pedigrees into decision support systems for ordering genetic testing [35]. However, genetic and family pedigree information would have to be collected in a standardized fashion before such a system could be debuted successfully. Without such a system, if PCPs feel uncomfortable with cancer genetics, it may be best to refer to genetic counselors for optimal evaluation for the ordering and interpreting of genetic tests.
Our finding that physicians who felt confident in these tasks were more likely to have ordered genetic testing or consulted with a genetic counselor in the past six months is consistent with previous studies [15,17,28]. Physician confidence in these tasks also correlated with the beliefs that genetic testing is important and that genetic risk contributes to disease risk, reinforcing previous findings [18].
Younger physicians in our study (aged 25-44 years) reported more confidence than physicians aged 45-54 on a few genetic testing tasks. In previous studies, the effect of age or year of graduation on confidence levels has varied from no difference [15,19] to increased confidence in physicians 50 years and older [17,18]. While younger physicians score higher when tested for knowledge about genetics [36-37], they perceive that their ability to apply that knowledge is low, resulting in lower confidence, at least at the beginning of the learning curve. Despite the issue of low confidence, PCPs have previously adapted successfully to integration of new technologies. It seems likely that with increased education and consultation with genetics experts, PCPs will learn how to incorporate genetic testing and interpretation into their practices.
Physicians in our study reported having the highest confidence in counseling about newborn screening among all the genetic testing options. This is in contrast to recent research in which only 16.5% of Canadian family medicine physicians and 62.6% of Canadian pediatricians report feeling confident in their ability to explain newborn screening results to parents [38]. These disparities may reflect differences in physician training and clinical experience in Canada versus the United States.
Most PCPs identified lack of time and patient comprehension as impediments to counseling about genetic risk. When presented with a DTC testing scenario, PCPs added inadequate knowledge (self), lack of relevance, and potential ethical dilemmas to the list of barriers. Lack of time is the most commonly cited barrier to discussing genetic tests and results by PCPs; lack of knowledge, lack of clinical relevance, and moral/ethical concerns are also frequently mentioned [17-18, 39]. One recent survey of the public found that patients generally have good recall of genetic testing results and do not have a deterministic view of genetics. However, these findings were disproportionately more prevalent in patients with higher levels of education and higher socioeconomic status [40] and may not be generalizable. Other studies have concluded that there is public misinterpretation of the role of genes in disease, how genetic disease is transmitted, and what a positive genetic test means [9, 41-42].
The physicians in our study did not feel that their practices had resources to improve patient comprehension, and only three out of ten agreed that their hospitals or networks had such resources. Genetics counselors could potentially fill this niche, but there is great variability in PCPs’ ability to make referrals to professionals with this skill set. Much of this variability can be attributed to practice setting. A recent study found that while 82.3% of PCPs based in academic medical centers reported that had access to genetics specialists for their patients, only 47.1% of community-based PCPs did [43].
Less than half of PCPs thought that lack of reimbursement was a barrier to discussion about DTC genetic test results. A previous study also found that PCPs were concerned about the costs associated with DTC genetic tests, but their concern was for the financial burden on their patients, not their own reimbursement [17]. Primary care physicians frequently provide counseling and management services that are not reimbursed [44], but they may be underestimating the amount of time it could take to explain results associated with indeterminate future risk.
Limitations of this study include potential response bias, since we were unable to determine how respondents might have differed from non-respondents. Participation may have been influenced by interest or knowledge about genetics. Additionally, confidence was selfreported and no objective measurement of respondents’ capabilities was performed. The use of Likert scales can result in central tendency bias; however, this was only reflected in some of our Likert scale responses. We feel that the responses that did reflect this bias yielded the most important results. Physician responses to clinical scenarios may not mirror behavior in an actual patient encounter. Although our sample included more diversity than other studies on physician readiness for the incorporation of genetics into clinical practice in terms of practice type (academic and non-academic) and setting (urban, suburban and rural), respondents came from one regional area of the United States.
Conclusions
Lack of experience, confidence, and resources continue to hinder primary care physicians’ optimal use of genetic testing. After more than a decade of studies of genetic tests and the PCP population, minimal progress has been made in experience and confidence. Establishing undergraduate, graduate, and continuing medical education must be a priority in order to improve and support clinician knowledge. Further research in this subject must evaluate which learning opportunities physicians would prefer. Examining the effects of age, specialty, and practice type on objective knowledge and confidence would aid in development of the right educational tools. Resources at the practice and hospital/network level including, for example, on-site genetics counseling, point of service apps on handheld devices, or EMR-based decision support, could then be tailored to primary care physicians’ needs for managing the inevitable integration of genomic medicine into clinical practice.
Acknowledgment
Work supported by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health under grant number U54-GM104941 (PI: Binder-Macleod).
References
- Green ED, Guyer MS; National Human Genome Research Institute. Charting a course for genomic medicine from base pairs to bedside. Nature. 2011; 470: 204-213.
- Chin L, Andersen JN, Futreal PA. Cancer genomics: from discovery science to personalized medicine. Nat Med. 2011; 17: 297-303.
- International Warfarin Pharmacogenetics Consortium, Klein TE, Altman RB, Eriksson N, Gage BF, Kimmel SE, Lee MT . Estimation of the warfarin dose with clinical and pharmacogenetic data. N Engl J Med. 2009; 360: 753-764.
- Bamshad MJ, Ng SB, Bigham AW, Tabor HK, Emond MJ, Nickerson DA, et al. Exome sequencing as a tool for Mendelian disease gene discovery. Nat Rev Genet. 2011; 12: 745-755.
- Hiraki S, Green NS. Newborn screening for treatable genetic conditions: past, present and future. Obstet Gynecol Clin North Am. 2010; 37: 11-21.
- Katsanis SH, Katsanis N. Molecular genetic testing and the future of clinical genomics. Nat Rev Genet. 2013; 14: 415-426.
- Annas GJ, Elias S. 23andMe and the FDA. N Engl J Med. 2014; 370: 2248-2249.
- Burke W. Genetic testing in primary care. Annu Rev Genomics Hum Genet. 2004; 5: 1-14.
- Leighton JW, Valverde K, Bernhardt BA. The general public's understanding and perception of direct-to-consumer genetic test results. Public Health Genomics. 2012; 15: 11-21.
- Gollust SE, Gordon ES, Zayac C, Griffin G, Christman MF, Pyeritz RE, et al. Motivations and perceptions of early adopters of personalized genomics: perspectives from research participants. Public Health Genomics. 2012; 15: 22-30.
- Fetters MD, Doukas DJ, Phan KL. Family physicians' perspectives on genetics and the human genome project. Clin Genet. 1999; 56: 28-34.
- Escher M, Sappino AP. Primary care physicians' knowledge and attitudes towards genetic testing for breast-ovarian cancer predisposition. Ann Oncol. 2000; 11: 1131-1135.
- Friedman L, Cooper HP, Webb JA, Weinberg AD, Plon SE. Primary care physicians' attitudes and practices regarding cancer genetics: a comparison of 2001 with 1996 survey results. J Cancer Educ. 2003; 18: 91-94.
- Lubin IM, McGovern MM, Gibson Z, Gross SJ, Lyon E, Pagon RA, et al. Clinician perspectives about molecular genetic testing for heritable conditions and development of a clinician-friendly laboratory report. J Mol Diagn. 2009; 11: 162-171.
- Bernhardt BA, Zayac C, Gordon ES, Wawak L, Pyeritz RE, Gollust SE. Incorporating direct-to-consumer genomic information into patient care: attitudes and experiences of primary care physicians. Per Med. 2012; 9: 683-692.
- Goldsmith L, Jackson L, O'Connor A, Skirton H. Direct-to-consumer genomic testing from the perspective of the health professional: a systematic review of the literature. J Community Genet. 2013; 4: 169-180.
- Selkirk CG, Weissman SM, Anderson A, Hulick PJ. Physicians' preparedness for integration of genomic and pharmacogenetic testing into practice within a major healthcare system. Genet Test Mol Biomarkers. 2013; 17: 219-225.
- Powell KP, Cogswell WA, Christianson CA, Dave G, Verma A, Eubanks S, et al. Primary care physicians' awareness, experience and opinions of direct-to-consumer genetic testing. J Genet Couns. 2012; 21: 113-126.
- Mainous AG, Johnson SP, Chirina S, Baker R. Academic family physicians' perception of genetic testing and integration into practice: a CERA study. Fam Med. 2013; 45: 257-262.
- Passamani E. Educational challenges in implementing genomic medicine. Clin Pharmacol Ther. 2013; 94: 192-195.
- Haga SB, Burke W, Agans R. Primary-care physicians' access to genetic specialists: an impediment to the routine use of genomic medicine? Genet Med. 2013; 15: 513-514.
- Mardis ER. The $1,000 genome, the $100,000 analysis? Genome Med. 2010; 2: 84.
- James KM, Cowl CT, Tilburt JC, Sinicrope PS, Robinson ME, Frimannsdottir KR, et al. Impact of direct-to-consumer predictive genomic testing on risk perception and worry among patients receiving routine care in a preventive health clinic. Mayo Clin Proc. Mayo Foundation for Medical Education and Research; 2011 Oct; 86: 933–940.
- Green RC, Berg JS, Grody WW, Kalia SS, Korf BR, Martin CL, et al. ACMG recommendations for reporting of incidental findings in clinical exome and genome sequencing. Genet Med. 2013; 15: 565-574.
- Wolf SM, Annas GJ, Elias S. Point-counterpoint. Patient autonomy and incidental findings in clinical genomics. Science. 2013; 340: 1049–1050.
- Ross LF, Rothstein M a, Clayton EW. Mandatory extended searches in all genome sequencing: “incidental findings,” patient autonomy, and shared decision making. JAMA. 2013; 310: 367–368.
- Christenhusz GM, Devriendt K, Dierickx K. To tell or not to tell? A systematic review of ethical reflections on incidental findings arising in genetics contexts. Eur J Hum Genet. 2013; 21: 248-255.
- Klitzman R, Chung W, Marder K, Shanmugham A, Chin LJ, Stark M, et al. Attitudes and practices among internists concerning genetic testing. J Genet Couns. 2013; 22: 90-100.
- Ronquillo JG, Li C, Lester WT. Genetic testing behavior and reporting patterns in electronic medical records for physicians trained in a primary care specialty or subspecialty. J Am Med Inform Assoc. 2012; 19: 570-574.
- Shields AE, Burke W, Levy DE. Differential use of available genetic tests among primary care physicians in the United States: results of a national survey. Genet Med. 2008; 10: 404-414.
- Marzuillo C, De Vito C, Boccia S, D'Addario M, D'Andrea E, Santini P, et al. Knowledge, attitudes and behavior of physicians regarding predictive genetic tests for breast and colorectal cancer. Prev Med. 2013; 57: 477-482.
- Wideroff L, Vadaparampil ST, Greene MH, Taplin S, Olson L, Freedman AN. Hereditary breast/ovarian and colorectal cancer genetics knowledge in a national sample of US physicians. J Med Genet. 2005; 42: 749-755.
- Bellcross CA, Kolor K, Goddard KA, Coates RJ, Reyes M, Khoury MJ. Awareness and utilization of BRCA1/2 testing among U.S. primary care physicians. Am J Prev Med. 2011; 40: 61-66.
- Burke W, Culver J, Pinsky L, Hall S, Reynolds SE, Yasui Y, et al. Genetic assessment of breast cancer risk in primary care practice. Am J Med Genet A. 2009; 149A: 349-356.
- Marsolo K, Spooner SA. Clinical genomics in the world of the electronic health record. Genet Med. 2013; 15: 786-791.
- Houwink EJ, van Luijk SJ, Henneman L, van der Vleuten C, Jan Dinant G, Cornel MC. Genetic educational needs and the role of genetics in primary care: a focus group study with multiple perspectives. BMC Fam Pract. 2011; 12: 5.
- Baars MJH, Henneman L, ten Kate LP. Deficiency of knowledge of genetics and genetic tests among general practitioners, gynecologists, and pediatricians: A global problem. Genet Med. The American College of Medical Genetics. 2005; 7: 605–610.
- Hayeems RZ, Miller FA, Carroll JC, Little J, Allanson J, Bytautas JP, et al. Primary care role in expanded newborn screening: After the heel prick test. Can Fam Physician. 2013; 59: 861-868.
- Scheuner MT, Sieverding P, Shekelle PG. Delivery of genomic medicine for common chronic adult diseases: a systematic review. JAMA. 2008; 299: 1320-1334.
- Kaphingst K a, McBride CM, Wade C, Alford SH, Reid R, Larson E, et al. Patients’ understanding of and responses to multiplex genetic susceptibility test results. Genet Med. 2012;14: 681–687.
- Haga SB, Barry WT, Mills R, Ginsburg GS, Svetkey L, Sullivan J, et al. Public knowledge of and attitudes toward genetics and genetic testing. Genet Test Mol Biomarkers. 2013; 17: 327-335.
- Condit CM, Shen L. Public understanding of risks from gene-environment interaction in common diseases: implications for public communications. Public Health Genomics. 2011; 14: 115-124.
- Haga SB, O'Daniel JM, Tindall GM, Mills R, Lipkus IM, Agans R. Survey of genetic counselors and clinical geneticists' use and attitudes toward pharmacogenetic testing. Clin Genet. 2012; 82: 115-120.
- Yarnall KS, Pollak KI, Østbye T, Krause KM, Michener JL. Primary care: is there enough time for prevention? Am J Public Health. 2003; 93: 635-641.
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