barriers to and motivations for physician referral of patients to cancer genetics clinics

ORIGINAL RESEARCH

Barriers to and Motivations for Physician Referralof Patients to Cancer Genetics Clinics

Carrie F. Prochniak & Lisa J. Martin & Erin M. Miller &

Sara C. Knapke

Received: 15 November 2010 /Accepted: 29 July 2011 /Published online: 13 August 2011# National Society of Genetic Counselors, Inc. 2011

Abstract Although it is well known that under-referral ofcolon cancer patients to cancer genetics clinics is a chronicproblem, no study has yet examined why physicians may beordering testing independently rather than referring patients tocancer genetics clinics. The current study explored variableswhich may impact a physician’s preference for orderingtesting independently or referring patients to outside cancergenetics experts. An online questionnaire, distributed to themembership of the American College of Gastroenterologyand the American Society of Colorectal Surgeons, yieldedresponses from 298 physicians. Motivations to refer to cancergenetics clinics rather than order testing independentlyincluded fear of genetic discrimination and a belief thatpatients benefit from genetic counseling about the risks,benefits and consequences of testing. These results suggestthat in order to increase referrals, genetic counselors must

educate physicians about the unique benefits patients receivefrom participating in genetic counseling.

Keywords Genetic counseling . Hereditary colorectalcancer . Genetic testing . Referral . Risk assessment

Introduction

Hereditary colorectal cancer accounts for as much as 5–10%ofall colorectal cancer cases (American Cancer Society 2008). Itis essential to identify individuals who are at risk forcolorectal cancer in order to provide appropriate medicalmanagement, including surveillance and surgical optionswhich have the potential to extend one’s lifespan by up to15 years (Järvinen et al. 2000). Despite the relatively highprevalence of hereditary colorectal cancer syndromes and theproven medical management options available, fewer patientsare being referred to cancer genetics clinics than expected(Singh et al. 2010). To address this deficiency, numerouseducational efforts regarding hereditary cancer syndrome riskassessment and management have been directed to specialtycare providers (e.g., gastroenterologists, colorectal surgeons)via publications in journals, online medical education, andpresentations at national meetings (Ellis 2008; Hendricks etal. 2006; Terdiman 2005; Wong et al. 2008). Despiteevidence showing the short-term success of educationalprograms in raising physician awareness and increasing theirability to recognize hereditary colorectal cancer syndromes,this pattern of under-referral to outside cancer geneticsexperts persists; these results suggest other barriers may playa role in referral decisions (Jenab-Wolcott et al. 2011).

Numerous barriers to referral to outside cancer geneticsexperts have been noted in the literature, including: lack ofknowledge regarding who should be referred; doubts about

C. F. Prochniak (*)Department of Women’s Health/Oncology, Aurora Health Care,945 N. 12th Street,Milwaukee, WI 53233, USAe-mail: [email protected]

L. J. MartinDivisions of Biostatistics and Epidemiology and Human Genetics,Department of Pediatrics,Cincinnati Children’s Hospital Medical Center,University of Cincinnati School of Medicine,Cincinnati, OH, USA

E. M. MillerThe Heart Institute,Cincinnati Children’s Hospital Medical Center,Cincinnati, OH, USA

S. C. KnapkeDivision of Human Genetics,Cincinnati Children’s Hospital Medical Center,Cincinnati, OH, USA

J Genet Counsel (2012) 21:305–325DOI 10.1007/s10897-011-9401-x

the clinical utility of genetic testing; and concerns regardinginsurance coverage of services, patient confidentiality, andgenetic discrimination (Freedman et al. 2003; Grover et al.2004; Huizenga et al. 2010; Mukherjee et al. 2010; Singh etal. 2010). However, in many of these studies, genetictesting is not separated from genetic counseling. This lackof distinction makes it difficult to identify the effects ofthese barriers on providers’ decisions not to pursue genetictesting, to coordinate testing independently, or to refer tooutside cancer genetics experts (Bellcross et al. 2011).

When a patient’s medical and family history are suggestiveof a hereditary cancer syndrome, the physician must initiallydecide if the patient wishes to pursue genetic testing. Thephysician then has the option to coordinate testing indepen-dently or to refer to outside cancer genetics experts. Batra andcolleagues (2002) used a pedigree consistent with a familyhistory of Lynch syndrome and a questionnaire to assessphysician practice patterns, including their opinion of theutility of genetic counseling. They found only half of theirsample of gastroenterologists would refer to a geneticcounselor to facilitate genetic testing, while the remaindervariously would provide their own counseling and testing,refer to a counselor only in the case of abnormal results, ornot provide counseling at all. These researchers also foundthat physicians who did not recommend genetic testing foran appropriate scenario-based patient viewed genetic tests asnot beneficial or believed they were not standard of care.Physicians who did not refer this high risk scenario patient togenetic counseling viewed genetic counseling as not bene-ficial and as too costly. These physicians were also morelikely to report they would provide their own geneticcounseling to the patient over referring to a geneticcounselor. It is important to note, however, that Batra etal.’s survey was administered in 1998, before the elaborationof the clinical utility of genetic testing and the effectivenessof medical management for Lynch syndrome.

Purpose of the Present Study

The primary objectives of this study were to: 1) provide acurrent assessment of gastroenterologists and colorectalsurgeons’ utilization of genetic testing and outside cancergenetics experts for hereditary colorectal cancer, 2) character-ize the risk assessment abilities of gastroenterologists andcolorectal surgeons, and 3) determine the influence of barriersand motivations experienced by physicians when decidingwhether to refer patients to outside cancer genetics experts orcoordinate genetic testing independently. For the purpose ofthis study, outside cancer genetics experts refers to clinicalmedical geneticists or genetic counselors with expertise incancer genetics and excludes other providers with clinicalexperience in genetics but who are not certified in medicalgenetics or genetic counseling. Independent coordination of

genetic testing refers to gastroenterologists or colorectalsurgeons who coordinate testing in their own offices.

Methods

Participants and Procedures

Participants included gastroenterologists and colorectal sur-geons who were recruited through emails directed to the entiremembership of both the American College of Gastroenterol-ogy in October 2009 and to the American Society ofColorectal Surgeons in February 2010. The survey wasavailable between October 2009 and May 2010. As themembership of these groups is not mutually exclusive,members of both groups were asked to disregard their secondinvitation if they had already completed the survey. Recruit-ment emails directed participants to an online questionnaire;participants had the option to complete the questionnaireanonymously. Participation in this survey was voluntary, andall participants provided informed consent. As an incentive forparticipation, respondents were given the opportunity torequest a packet of resources to be sent after they completedthe survey, including literature regarding the process ofgenetic testing and counseling as well as how to locate agenetic counselor. The study was approved by the IRBs ofboth Cincinnati Children’s Hospital Medical Center and theUniversity of Cincinnati.

Instrumentation

The authors designed a questionnaire to assess participants’use of genetic testing for hereditary colorectal cancer andreferral to outside cancer genetics experts (see Appendix).Items included a series of possible barriers to or motiva-tions for using genetic testing or outside cancer geneticsexperts in their practice. Questions were modeled uponthose used in prior studies (Batra et al. 2002; Freedman etal. 2003; Koil et al. 2003; McCann et al. 2007). Content ofquestions included physician practice patterns regardinggenetic testing for colorectal cancer, barriers and motiva-tions to genetic testing, physicians’ perceptions of their rolein genetic testing and confidence in this role, and use ofscenarios from Batra et al.’s study that addressed riskassessment abilities and referral patterns.

The authors minimally expanded upon these questionsderived from previously utilized questionnaires, furtherexpanded on questions addressing physician practice patternsand included additional barriers and motivations hypothesizedbased on the authors’ clinical experience. Additionally, theyconstructed three case scenarios regarding the management ofvarious individuals with a family history of colorectal cancer.These case scenarios were designed to fit the criteria for high,

306 Prochniak et al.

moderate and general population risk as delineated by theAGA (American Gastroenterological Association (2001)).The questionnaire also collected general demographicinformation such as medical specialty, degree, number ofpatients seen, and the year of graduation.

Data Analysis

To characterize how gastroenterologists and colorectal sur-geons utilize genetic testing and outside cancer geneticsexperts (objective 1), descriptive statistics (frequencies) forreported events were calculated. Frequencies for the twogroups of physicians were compared using chi-square tests.

To characterize the risk assessment ability of gastroenterol-ogists and colorectal surgeons (objective 2), their responses toanswers to three scenarios of risk were evaluated. For eachscenario, a single answer was designated as correct. Withrespect to risk assessment ability, respondents were classified ascorrect (if all three risk assessments were correct) or incorrect(if at least one risk assessment was incorrect). Individuals whodid not answer all three questions were defined as missing data.We then examined whether there were differences in theproportion correct based on physician type, history of orderingtumor or genetic testing, and history of referral to outsidecancer genetics experts, using chi-square tests.

To determine the influence of barriers and motivations onreferral preference (objective 3), we examined the Likert-typescales assessing endorsement of various motivations andbarriers. While these scales included four choices, for allquestions there were two predominant answers selected foreach question. Therefore, we created dichotomous variables.Participants who were designated as endorsing a motivationrated that motivation as either “very influential” or “somewhatinfluential,” while participants who were designated asendorsing a barrier selected either “strongly agree” or“somewhat agree.” Then chi-square analysis or Fisher’s exacttest was used to determine the significance of the motivationor barrier in relation to the physician’s preference regardingutilization of genetic counseling services. To determine if yearof graduation was associated with whether high risk patientswould be referred to an outside cancer genetics expert orwould receive the appropriate colorectal screening, we usedlogistic regression.

Throughout the analysis, respondents who selectedunsure or neutral were designated as missing data.

Results

Participant Demographics and Referral Recommendations

A total of 196 individuals completed the online survey inresponse to the American College of Gastroenterology

mailing. A total of 102 individuals completed the onlinesurvey in response to the American Society of ColorectalSurgeons. Based on the memberships for these groups,conservative estimated response rates were 4% and 6.5%,respectively.

The study sample consisted of 185 gastroenterologists(62.0%) and 105 colorectal surgeons (35.2%); the remainingeight individuals selected other specialties. Physicians hadbetween no and 10,000 patient visits per year (median = 2000visits per year). They graduated between 1958 and 2003(median = 1988). From logistic regression analysis, asreported year of graduation decreased, physicians were morelikely to recommend that the high risk scenario patient bereferred to an outside cancer genetics expert (χ2=6.42; p=.01)and to recommend the patient receive the appropriateintensity of colorectal screening (χ2=8.02; p=.0046). How-ever, there was no statistically significant relationshipbetween year of graduation and likelihood of orderinggenetic testing for the high risk scenario patient.

Only 18.9% of participants reported having receivedformal training in genetics, such as clinical rotations(during medical school, residency or fellowship), or courses(through undergraduate education, medical school, orcontinuing medical education). Physicians who reportedformal training in genetics were significantly less likely torefer the high risk scenario patient to outside cancergenetics experts (χ2=4.65; p=.03; 53.2% vs. 69.7%).

Utilization of Genetic Testing Services

The vast majority (82.7%) of providers had referred at leastone patient to outside cancer genetics experts or hadpreviously ordered either tumor or germline genetic testing(see Table 1). There was no statistically significantdifference in rates of referral or ordering between gastro-enterologists and colorectal surgeons. However, colorectalsurgeons were significantly more likely than gastroenterol-ogists to order germline genetic testing (χ2=8.84; p=.003;48.9% vs. 30.0%) and to refer to outside cancer geneticsexperts (χ2=11.5; p=.0007; 80.4% vs. 60.2%) for the high-risk scenario patient.

Risk Assessment Ability

When presented with clinical scenarios, the majority ofphysicians were able to correctly identify the high riskpatient (Fig. 1). Physicians were less able to discriminatepatients into moderate and general population risk catego-ries, thus the number of physicians who were able toperform an accurate risk assessment for all three patientswas low. There were no statistically significant differencesbetween the risk assessment abilities of gastroenterologistsand colorectal surgeons.

Barriers to and Motivations for Referral to Cancer Genetics 307

Physicians who were able to correctly classify all threescenarios into their correct risk category were not morelikely than those who were incorrect to have ever orderedtumor or genetic testing (89.7% vs. 91.7%, respectively), orto have previously referred to outside cancer geneticsexperts (84.6% vs. 82.3%, respectively).

Perceived Barriers and Motivations and Referral Preference

When asked whether they prefer to coordinate genetic testingindependently or to refer to outside genetics experts, 41.6% ofphysicians indicated they preferred to order testing indepen-dently instead of through referral. There was no statisticallysignificant difference between the referral preferences ofgastroenterologists (40.4%) and colorectal surgeons (44.9%).

The proportion of physicians who endorsed specificbarriers to and motivations for referral to outside cancergenetics experts, as well as the influence of these barriers andmotivations on referral preference is summarized in Table 2.Physicians who preferred to refer to outside cancer geneticsexperts versus those who preferred coordinating testingindependently were more likely to believe that patients areat risk for genetic discrimination (χ2=7.05; p=.008; 69.1%vs. 51.6%) and more likely to believe that patients undergoinggenetic testing benefit from genetic counseling by genetics

specialists regarding the risks, benefits and consequences ofthe test (χ2=3.90; p=.048; 77.0% vs. 65.3%). Physicianswho were able to correctly classify all three scenarios on thesurvey (n=70) into their correct risk category versus thosewho were not able to do so were also more likely to prefer toutilize outside cancer genetics experts (χ2=7.12; p=.008;71.4% vs. 52.7%).

Perceived Role of Physician in Genetics Consultation

Physicians who preferred to coordinate testing independentlywere more likely than those who preferred to refer for testingto feel that their role in the genetics evaluation processincluded ordering tumor testing (Fisher’s exact p=.026;95.2% vs. 83.8%); ordering germline genetic testing (Fish-er’s exact p=<.0001; 98.8% vs. 61.0%); interpreting genetictest results (χ2=44.96; p=<.0001; 91.7% vs. 40.7%); andproviding emotional support (χ2=6.67; p=.010; 90.8% vs.74.1%). These physicians were also more likely to feelconfident performing these roles (ordering tumor testing:χ2=11.93; p=.0006; 93.9% vs. 77.3%; ordering germlinetesting: χ2=30.04; p=<.0001; 95.0% vs. 65.0%; interpret-ing genetic test results: χ2=31.70; p=<.0001; 89.9% vs.55.9%), with the exception of providing emotional follow-up support (χ2=.83; p=.36; 83.8% vs. 79.1%; Fig. 2).

Discussion

The current study explored variables which may impact aphysician’s preference to order testing independently or referto outside cancer genetics experts for diagnosis of hereditarycolorectal cancer. Physicians who perceived their role includesordering tumor testing, ordering germline testing, andinterpreting genetic test results and those who felt confidentdoing so were more likely to report they would order theirown testing than those who preferred to refer patients fortesting. Physicians who preferred to refer to outside cancergenetics experts over ordering testing independently weremore likely to value the counseling provided by outsidegenetics experts regarding the risks, benefits and consequen-ces of the test. Thus, future strategies for increasing referral tooutside cancer genetics experts may be improved by focusing

0

10

20

30

40

50

60

70

80

90

100

High risk Moderate Risk Average risk All scenarioscorrect

Scenario

% c

orr

ect

GI

CRS

Fig. 1 Percentages of gastroenterologists (GI) and colorectal surgeons(CRS) that were able to correctly identify a scenario patient as high,moderate or general population risk

n %

Referred a patient to cancer genetic counseling 220 82.7

Ordered genetic testing for Lynch syndrome (MLH1, MSH2, MSH6, PMS2) 210 79.2

Ordered Microsatellite Instability (MSI) tumor testing 188 71.2

Ordered genetic testing for Familial Adenomatous Polyposis (FAP; APC) 191 72.1

Ordered Immunohistochemistry (IHC) tumor testing 134 51.1

Ordered genetic testing for MYH autosomal recessive polyposis (MAP; MYH) 93 35.6

Table 1 Physicians’ utilizationof genetic testing and outsidegenetics experts

N for entire table is approximate,and varies between 261 and 266for each particular question.Thus, n and % reported in theright column may not be consis-tent throughout table


on the unique, evidence-based benefits that genetic counselingprovides to patients over and above the services receivedwhen a physician orders tests independently.

Risk Assessment

Publications in journals directed toward gastroenterologistsand colorectal surgeons have focused on providing educa-tion regarding hereditary cancer syndrome risk assessment

and management (Hendricks et al. 2006; Terdiman 2005).Although these educational interventions have been suc-cessful in aiding providers in identifying patients at highestrisk, educational efforts have had a lesser impact onimproving providers’ ability to discriminate betweenpatients at moderate and general population risk. Data froma 1998 survey of gastroenterologists found that 79% wereable to correctly identify a scenario patient as having Lynchsyndrome (Batra et al. 2002). Additionally, in a survey

0

10

20

30

40

50

60

70

80

90

100

EmotionalSupport

Order tumortesting

Ordergermlinetesting

Interprettest results

% e

nd

ors

ing

item

EmotionalSupport

Ordertumortesting

Ordergermlinetesting

Interprettest results

OrderRefer

∗ ∗ ∗∗ ∗ ∗ ∗Role in genetics evaluation Confidence performing role

Fig. 2 Graph on the left: Comparison of perceived roles in geneticsevaluation between those who prefer to refer to outside cancergenetics experts vs. those who prefer to order testing independently.Graph on the right: Comparison of self-confidence in performing said

role between those who prefer to refer to outside cancer geneticsexperts vs. those who prefer to order testing independently. * Denotessignificant results (p<.05)

Table 2 Comparison of barriers and motivations endorsed by independent versus referring physicians

Participantsthat endorseditem

Participants whoprefer to ordertesting independentlythat endorsed item

Participants whoprefer to refer togenetics servicesthat endorsed item

n % n % n % p

Barriers

Genetic tests for inherited cancer susceptibility are not usually covered byinsurance

138 70.4 61 66.3 77 74.0 0.24

Patients with confirmed inherited colorectal cancer susceptibilitysyndromes are at risk for genetic discrimination

135 61.4 50 51.6 85 69.1 0.008a

Clear guidelines or strategies are not available for managing patientswith a confirmed inherited colorectal cancer susceptibility syndrome

86 37.8 41 41.4 45 33.3 0.21

Motivations

Recommendations and guidelines from professional organizations andgovernment agencies influence whether to refer to cancer genetics services

174 72.8 68 68.9 106 75.7 0.23

Patients undergoing genetic testing benefit from genetic counseling bygenetics specialists about the risks, benefits and consequences of the test

171 72.2 64 65.3 107 77.0 0.048a

The individual patient’s or family’s request for genetics services influenceswhether to refer to cancer genetics services

151 62.9 69 69.0 82 58.6 0.099

Genetic testing is useful in making decisions about surgery and medicalmanagement

139 58.7 61 61.0 78 56.9 0.53

Able to perform an accurate risk assessment 70 29.5 20 20.2 50 36.2 0.008a

Participants were asked to endorse specific barriers and motivations for referral regardless of their reported referral preference. Perceived barriersand motivations were then compared for physicians who preferred to order genetic testing themselves versus those who would refer patients togenetics services. a denotes significant differences as function of independent testing vs. referral for testing (p<.05). Total number of participantswho responded to each item varied between 212 and 237


conducted in 2007, 45% of primary care physicians whohad ordered BRCA testing in the prior year selected at leastone low risk scenario as an indication for BRCA testing(Bellcross et al. 2011). In the present study over 90% ofproviders were able to identify a similar high risk patient,but a majority (70%) was unable to stratify patients intohigh, moderate and low risk categories.

As genetics researchers continue to discover low andmoderate genetic risk factors for cancer and for othercommon diseases, their findings could significantly influ-ence referral patterns to genetic counseling. As educationalefforts thus far have focused on highly penetrant hereditarycancer susceptibility syndromes, future educational effortsneed to expand to include low and moderate risk factors,with an emphasis on which factors necessitate a referral tooutside cancer genetics experts.

Lack of knowledge regarding risk assessment has longbeen cited as a major barrier to referral; as such, educationalinterventions have been created in an attempt to improvephysicians’ ability to perform risk assessment, with thesecondary goal of increasing referrals to genetic counseling(Batra et al. 2002; Freedman et al. 2003). Results of thepresent study suggest education may have a limitedinfluence on utilization of genetic testing or referral tooutside cancer genetics experts. Namely, there was norelationship between participants’ ability to correctlyclassify all three scenarios into their correct risk categoryand prior use of tumor or genetic testing or outside cancergenetics experts. In other words, there may be physiciansordering testing who struggle with determining whichpatients are appropriate candidates for that testing.

On the other hand, physicians who were able to correctlyclassify all three scenarios were significantly more likely toreport a preference to refer to outside cancer geneticsexperts rather than coordinate testing independently. Thus,it may be that while educational efforts have not amelio-rated physicians’ struggle with accurate risk assessment,educational efforts have sufficiently emphasized the com-plexity surrounding genetic testing to sway physicians toprefer to have a genetics expert coordinate testing ratherthan be personally responsible for this testing.

Referral Patterns

While genetic testing includes the simple act of facilitatingtesting, genetic counseling includes providing a discussion ofthe risks, benefits and consequences of genetic testing,interpreting test results in the context of the family, andproviding emotional support to patients during the testingprocess (Peters and Biesecker 1997). However, many studiesof referral of patients by physicians to genetic counselingand genetic testing rarely separated the two differentprocesses. Therefore, it is difficult to compare rates of

utilization of outside cancer genetics experts, leading to alack of information regarding providers’ confidence inperforming the process of genetic counseling independently,without referral to outside cancer genetics experts.

In a study conducted from 1999 to 2000, physiciansreported general confusion about who should have genetictesting, what genetic testing meant for patients’ risk ofdeveloping cancer, and how to manage patients withpositive test results (Freedman et al. 2003). This confusionled over 90% of these physicians to believe geneticcounseling was a mandatory step in the process of genetictesting. However, in the current study, the majority ofphysicians reported feeling confident in their ability toorder and interpret genetic testing, suggesting they do notbelieve that genetic counseling prior to testing is mandatory.Only 72% believed that patients benefited from geneticcounseling by genetics experts during the testing process.These data suggest gastroenterologists and colorectalsurgeons have gained confidence in their ability to facilitategenetic testing independently (despite the low accuracy oftheir risk assessment abilities). Perhaps this increase inconfidence is related to increased education directedtowards these providers.

If physicians choose to perform genetic testing withoutthe aid of outside cancer genetics experts, it is essential thatthey be able to provide patients with accurate information.However, of the physicians in this study that coordinatedtheir own testing, 44% believed testing is not covered byinsurance, and 37% believed patients are at risk for geneticdiscrimination. In order to ensure optimal care for patientswhose genetic testing is coordinated by physicians, in-creased education is needed to correct these misconcep-tions. This education is especially timely given the passageof the Genetic Information Non-Discrimination Act, whichmany physicians may not realize extends protection formany patients and families. These common misconceptionsabout risk of genetic discrimination and insurance coverageof clinical genetic testing are likely to result in decreasedpursuit of genetic testing. However, as physicians whobelieved that patients are at risk for genetic discriminationwere significantly more likely to refer to outside cancergenetics experts, these misconceptions regarding geneticdiscrimination may actually be driving referrals to outsidecancer genetics experts.

Barriers and Motivations to Referral

A significant motivation for ordering genetic testingpreviously reported in the literature is patient requests forgenetics services (cf. Wideroff et al. 2003). Additionally,Brandt and colleagues (2008) found 73% of primary carephysicians and specialists based patient eligibility forreferral to outside cancer genetics experts on patient


request, and 54% of physicians did not refer eligiblepatients due to patient disinterest. However, it is not clearwhether patients specifically requested a referral to anoutside genetics expert or instead only expressed interest ingenetic testing, leaving it up to the physicians in their studyto decide whether they coordinated this testing themselvesor referred the patient to an outside cancer genetics expert.

The present findings suggest that having patients request agenetics evaluation does not make a physician more likely torefer to outside cancer genetics experts over ordering testingindependently. It may be that physicians who feel comfortabledoing so coordinate testing independently if patients do notspecifically ask for involvement of a genetics expert, and thusreferral to outside cancer genetics experts is only increasedwhen patients specifically ask for this referral. As direct toconsumer advertising increases, it will be important forgenetic counselors to provide information directly to consum-ers about the benefits of genetic counseling in order to ensurethat this important route of referral is maintained.

Another route of referral may result from recommenda-tions of professional organizations and guidelines thataddress when to refer to outside cancer genetics experts.In the present study, 74% of participants indicated theserecommendations and guidelines influenced their decisionsregarding whether to refer to outside cancer geneticsexperts. Several guidelines address the need for counselingand genetic testing for individuals at risk for hereditarycolorectal cancer, including: American Cancer SocietyColorectal Cancer Advisory Group, U.S. Multi-society TaskForce, and American College of Radiology Colon CancerCommittee (2008); American Society of Clinical Oncology(2005); Evaluation of Genomic Applications in Practice andPrevention (EGAPP) Working Group (2009). However,only the guideline produced by the American Society forGastrointestinal Endoscopy specifies that “expert counsel-ing” should be provided (American Society for Gastroin-testinal Endoscopy 2006). Additionally, the updated 2011National Comprehensive Cancer Network (NCCN) guide-lines regarding genetic/familial high-risk assessment forbreast and ovarian cancer were modified to approvesurgeons, oncologists, oncologist nurses and other qualifiedhealth care professionals for involvement in BRCA testing.

These types of guidelines “demote” genetic counselors/medical geneticists from being the only providers sanc-tioned to perform genetic testing by NCCN to stating that“genetic counseling is highly recommended” (NCCN 2011,p. BR/OV-1). As such, they are in direct contrast to the U.S.Preventive Services Task Force’s (USPSTF) 2005 guidelinerecommending “that women whose family history isassociated with an increased risk for deleterious mutationsin BRCA1 or BRCA2 genes be referred for geneticcounseling and evaluation for BRCA testing” (emphasisadded; U.S. Preventive Services Task Force 2005, p. 355).

The lack of emphasis on referral to outside cancer geneticsexperts in the existing guidelines may explain the presentfinding that although physicians endorsed guidelines as asignificant influence on their practice decisions, these guide-lines did not result in preference for referral to outside cancergenetics experts over coordinating testing independently.Thus, in order to increase referrals from colorectal special-ists, genetic counselors may consider lobbying for adaptationof the above guidelines to explicitly include referral tooutside cancer genetics experts. Future studies should alsoexamine whether the specific USPSTF guidelines issuedregarding breast cancer referrals have in fact increasedreferrals from specialist providers (Bellcross et al. 2011).

Perceived Benefit of Genetic Counseling

Genetic counseling addresses complex psychosocial issueswith participants including determinants of decision makingsuch as risk perception, personal experiences with cancer, andpersonal health beliefs, as well as communication within thefamily, adjustment to genetic conditions, and legal issues suchas genetic discrimination (Peters and Biesecker 1997). Up to40% of individuals going through genetic testing needprofessional psychosocial support (Bleiker et al. 2003).

Despite educational publications regarding the complexi-ties and importance of psychosocial support provided bygenetic counseling, many physicians believe they are able toprovide the same services as trained genetic counselors (Batraet al. 2002). Providers who participated in the current studyindicated that if they were going to order genetic testinginstead of referring to genetics professionals, it was their roleto provide emotional follow-up support. However, thesephysicians were no more confident in these skills than thosephysicians who deferred this role to genetics providers.

Beyond raising concern that physicians who order testingwithout consultation with genetics professionals are not ableto meet the psychosocial needs of their patients, these datasuggest genetic counselors may be uniquely positioned toaddress the emotional needs of patients beyond the ability of anon-genetics physician. Moreover, since the results show thatphysicians are more likely to refer when they understand thebenefit of genetic counseling, a possible means of increasingreferral to genetics clinics would be to emphasize the value ofgenetics professionals’ unique ability to address psychosocialneeds of patients and how this may in turn lead to properinformed consent, increased psychological well-being, andappropriate health behaviors. It is also important that geneticcounselors emphasize their willingness and availability toprovide genetic counseling at any point in the testing process,including post-testing, in order to increase referrals fromphysicians who feel confident coordinating the testing processindependently but do not feel confident addressing psychoso-cial concerns after test results are received.


To prevent genetic counselors’ role from being usurped byphysicians who order testing independently, future studiesmust demonstrate the worth of psychosocially focused geneticcounseling provided by trained genetic counselors over thebasic medical genetic risk assessment often performed by non-genetics medical providers (Peters and Biesecker 1997).Grave errors in medical recommendations by non-geneticsmedical providers have been reported (Brierley et al. 2010).An incidental finding of Collins’ and colleagues (Collins etal. 2000) study of patient satisfaction was that patients whohad a genetic counselor or medical geneticist participating intheir session with a gastroenterologists were more likely tohave a greater increase in knowledge regarding familialcolorectal cancer as compared to patients whose sessions didnot include a genetics professional, which the authorshypothesized would lead to an increased ability to provideinformed consent. However, this was not a controlled trial, andno psychosocial or health behavior outcomes were measured.

Therefore, further controlled studies comparing thegenetic counseling provided by non-genetics medicalproviders and genetic counselors must be conducted. Thesestudies must not only focus on knowledge and riskperception, but psychosocial outcomes such as anxietyand cancer-related worry. The Jane Engelberg MemorialFund project of Dawn Allain and Kate Shane entitled “Thevalue of genetic counselors in genetic testing for hereditarybreast-ovarian cancer” aims to demonstrate the value ofgenetic counseling by comparing outcomes of patients whohad genetic testing for BRCA1/2 through their non-geneticshealthcare provider versus those patients who were testedby genetic counselors (NSGC 2011). This study will beinstrumental in providing evidence of the benefit and valueof genetic counseling in the genetic testing process.

Study Limitations

A major limitation of this study was the low response rate foreach group. This limitation has been identified and com-mented on in other studies as due to increasing paperwork anddecreasing available time for physicians (Lowstuter et al.2008). The high rates of physicians that report previouslyordering tumor or genetic testing or referring to outsidecancer genetics experts is likely a result of ascertainmentbias, with a high response rate from physicians who areinterested in genetics. With this in mind, we expect thatuncertainty when performing risk assessment and barriers toand motivations for referral would be magnified in apopulation of physicians not as interested in genetics.

Additionally, although the questionnaire was modeledfrom previously published questionnaires, the specificquestions and scenarios used in this study were notindependently validated. This may limit direct comparisonswith other scenario-based research into physician testingand referral patterns. Many of the items elicited hypothet-ical behaviors. Research is needed to determine the extentto which physicians’ reports of what they are likely to dowould match their actual behavior in such situations.

Finally, due to the exploratory nature of this study, wedid not correct our type I error rate for multiple testing.Given the number of comparisons performed, using thisliberal alpha level (p=0.05) is likely to result in an inflatedtype I error rate. Thus, some of the statistically significantresults reported may be due to chance and these resultsshould be interpreted with caution. As such, future studiesare required to replicate our findings. Nonetheless, thisstudy provides important initial insight into barriers andmotivations for using cancer genetic counseling services.

Conclusion

In order to assure that the 5–10% of patients who havehereditary colorectal cancer susceptibility syndromes areprovided with appropriate care, increased effort is needed tofind a way to effectively provide genetic counseling andgenetic testing services to these patients. As the frequencywith which genetic testing is ordered in the offices ofgastroenterologists and colorectal surgeons increases, physi-cians will become more comfortable performing risk assess-ment and coordinating testing. Additionally, increased directto consumer advertising about the value of genetic testing mayimpact patient requests for genetic testing and the frequencywith which genetic testing is ordered by physicians. Forgenetic counselors to continue to reach patients at risk forhereditary colorectal cancer, research will need to be provethat cancer genetic counselors are better equipped thanspecialist physicians to meet the psychosocial and educationalneeds of patients, which in turn leads to better patient well-being and medical compliance with surveillance procedures.

Acknowledgements The authors would like to thank Dr. Jim Cranleyof Digestive Health Network and Dr. J. Michael Guenther of CranleySurgical Associates for providing guidance in developing the question-naire, and Dr. Janice Rafferty of the University of Cincinnati Division ofColon and Rectal Surgery for sponsoring the study with the AmericanSociety of Colorectal Surgery. Thanks also to the staff andmembers of theAmerican College of Gastroenterology and American Society ofColorectal Surgery for agreeing to participate in this project.


Appendix: Questionnaire


References

American Cancer Society. (2008). Colorectal cancer facts & figures2008–2010. Atlanta: American Cancer Society.

American Cancer Society Colorectal Cancer Advisory Group, U.S.Multi-society Task Force, & American College of RadiologyColon Cancer Committee. (2008). Screening and surveillance forthe early detection of colorectal cancer and adenomatous polyps,2008: A joint guideline from the American Cancer Society, theUS Multi-Society Task Force on Colorectal Cancer, and theAmerican College of Radiology. CA: A Cancer Journal forClinicians, 58, 130–160.

American Gastroenterological Association. (2001). American Gastro-enterological Association medical position statement: Hereditarycolorectal cancer and genetic testing. Gastroenterology, 121,195–197.

American Society for Gastrointestinal Endoscopy. (2006). ASGEguideline: Colorectal cancer screening and surveillance. Gastro-intestinal Endoscopy, 63(4), 546–557.

American Society of Clinical Oncology. (2005). Colorectal cancersurveillance: 2005 update of an American Society of ClinicalOncology guideline. Journal of Clinical Oncology, 23(33), 8512–8519.

Batra, S., Valdimarsdottir, H., McGovern, M., Itzkowitz, S., & Brown,K. (2002). Awareness of genetic testing for cancer predisposition

among specialists in gastroenterology. American Journal ofGastroenterology, 97(3), 729–733.

Bellcross, C., Kotor, K., Goddard, K. A. B., Coates, R. J., Reyes, M.,& Khoury, M. J. (2011). Awareness and utilization of BRCA1/2testing among U.S. primary care physicians. American Journal ofPreventive Medicine, 40(1), 61–66.

Bleiker, E. M. A., Hahn, D. E. E., & Aaronson, N. K. (2003).Psychosocial issues in cancer genetics: Current status and futuredirections. Acta Oncologica, 42(4), 276–286.

Brandt, R., Ali, Z., Sabel, A., McHugh T., & Gilman, P. (2008).Cancer genetics evaluation: Barriers to and improvements forreferral. Genetic Testing, 12(1), 9–12.

Brierley, K. L., Campfield, D., Ducane, W., Dohany, L., Donenberg, T.,Shannon, K., et al. (2010). Errors in delivery of cancer geneticsservices: Implications for practice. Connecticut Medicine, 74(7),413–423.

Collins, V., Halliday, J., Warren, R., & Williamson, R. (2000).Assessment of education and counselling offered by a familialcolorectal cancer clinic. Clinical Genetics, 57(1), 48–55.

Ellis, C. N. (2008). Inherited colorectal cancer syndromes. retrievedApril 18 2011, from American Society of Colon & RectalSurgeons Web Site: http://www.fascrs.org/physicians/education/core_subjects/2008/inherited_colorectal_cancer_syndromes/

Evaluation of Genomic Applications in Practice and Prevention(EGAPP) Working Group. (2009). Recommendations from theEGAPP working group: Genetic testing strategies in newly


http://www.fascrs.org/physicians/education/core_subjects/2008/inherited_colorectal_cancer_syndromes/

http://www.fascrs.org/physicians/education/core_subjects/2008/inherited_colorectal_cancer_syndromes/

diagnosed individuals with colorectal cancer aimed at reducingmorbidity and mortiality from Lynch syndrome in relatives.Genetics in Medicine, 11(1), 35–41.

Freedman, A. N., Wideroff, L., Olson, L., Davis, W., Klabunde, C.,Srinath, K. P., et al. (2003). US physicians’ attitudes towardgenetic testing for cancer susceptibility. American Journal ofMedical Genetics, 120A, 63–71.

Grover, S., Stoffel, E. M., Bussone, L., Tschoegl, E., & Syngal, S.(2004). Physician assessment of family cancer history andreferral for genetic evalution in colorectal cancer patients.Clinical Gastroenterology and Hepatology, 2, 813–819.

Hendricks, Y. M. C., de Jong, A. E., Morreau, H., Tops, C., Vasen, H.F. A., Wijnen, J. T., et al. (2006). Diagnostic approach andmanagement of Lynch syndrome (Hereditary NonpolyposisColorectal Carcinoma): A guide for clinicians. CA: A CancerJournal for Clinicians, 56(4), 213–225.

Huizenga, C. R., Lowstuter, K., Banks, K. C., Lagos, V. I., Vandergon,V. O., & Weitzel, J. N. (2010). Evolving perspectives on geneticdiscrimination in health insurance among health care providers.Familial Cancer, 9, 253–260.

Järvinen, H. J., Aarnio, M., Mustonen, H., Aktan-Collan, K.,Aaltonen, L. A., Peltomäki, P., et al. (2000). Controlled 15-yeartrial on screening for colorectal cancer in families with hereditarynonpolyposis colorectal cancer. Gastroenterology, 118, 829–834.

Jenab-Wolcott, J., Tan, K., Heitjan, D. F., Giantonio, B. J., Garin, M.,Powers, J., et al. (2011). Evaluation of physician knowledge andreferral practices for colorectal cancer (CRC) genetic riskassessment: The experience at the Hospital of University ofPennsylvania (HUP) [Abstract]. Journal of Clinical Oncology, 29(suppl 4; abstr 379)

Koil, C. E., Everett, J. N., Hoechstetter, L., Ricer, R. E., & Huelsman,K. M. (2003). Differences in physician referral practices andattitudes regarding hereditary breast cancer by clinical practicelocation. Genetics in Medicine, 5(5), 364–369.

Lowstuter, K. J., Sand, S., Blazer, K. R., MacDonald, D. J., Banks, K.C., Lee, C. A., et al. (2008). Influence of genetic discrimination

perceptions and knowledge on cancer genetics referral practiceamong clinicians. Genetics in Medicine, 10(9), 691–698.

McCann, S., MacAuley, D., Barnett, Y., Bunting, B., Bradley, A.,Jeffers, L., et al. (2007). Cancer genetics: Consultants’ percep-tions of their roles, confidence and satisfaction with knowledge.Journal of Evaluation in Clinical Practice, 13, 276–286.

Mukherjee, A., McGarrity, T. J., Ruggerio, F., Koltun, W., McKenna, K.,Portiz, L., et al. (2010). The revised Bethesda guidelines: Extent ofutilization in a university hospital medical center with a cancergenetics program. Hereditary Cancer in Clinical Practice, 8(9).

National Comprehensive Cancer Network (NCCN). (2011). NCCNclinical practice guidelines in onocology: Genetic/familial high-risk assessment: Breast and ovarian

National Society of Genetic Counselors (NSGC). (2011). JEMF awardrecipients. Retrieved April 19, 2011, from http://www.nsgc.org/MemberCenter/GrantsAwards/JEMFAwardRecipients/tabid/256/Default.aspx

Peters, J. A., & Biesecker, B. (1997). Genetic counseling andhereditary cancer. Cancer, 80(3), 577–586.

Singh, H., Schiesser, R., Anand, G., Richardson, P. A., & El-Serag, H.B. (2010). Underdiagnosis of Lynch syndrome involves morethan family history criteria. Clinical Gastroenterology andHepatology, 8, 523–529.

Terdiman, J. P. (2005). Colorectal cancer at a young age. Gastroen-terology, 128, 1067–1076.

U.S. Preventive Services Task Force. (2005). Genetic risk assessmentand BRCA mutation testing for breast and ovarian cancersusceptibility: Recommendation statement. Annals of InternalMedicine, 143(5), 335–361.

Wideroff, L., Freedman, A. N., Olson, L., Klabunde, C., Davis, W.,Srinath, K. P., et al. (2003). Physician use of genetic testing forcancer susceptibility: Results of a national survey. CancerEpidemiology, Biomarkers & Prevention, 12, 295–303.

Wong, C., Gibbs, P., Johns, J., Jones, I., Faragher, I., Lynch, E., et al.(2008). Value of database linkage: Are patients at risk of familialcolorectal cancer being referred for genetic counseling andtesting? Internal Medicine Journal, 38, 328–333.


http://www.nsgc.org/MemberCenter/GrantsAwards/JEMFAwardRecipients/tabid/256/Default.aspx



barriers to and motivations for physician referral of patients to cancer genetics clinics

Documents