Critical components of genomic medicine practice for non‐genetics healthcare professionals: Genetic counselors' perspectives and implications for medical education

Genetic services are increasingly provided by non‐genetics healthcare professionals (NGHPs) with minimal formal training in genetics/genomics. Research demonstrates gaps in knowledge and clinical practices in genetics/genomics among NGHPs, but there is a lack of consensus on the specific knowledge needed by NGHPs to effectively provide genetic services. As clinical genetics professionals, genetic counselors (GCs) have insight into the critical components of genetics/genomics knowledge and practices needed by NGHPs. This study explored GCs' beliefs regarding whether NGHPs should provide genetic services and identified GCs' perceptions of the components of knowledge and clinical practice in genetics/genomics that are most critical for NGHPs providing genetic services. Two hundred and forty GCs completed an online quantitative survey with 17 participating in a follow‐up qualitative interview. Descriptive statistics and cross‐comparisons were generated for survey data. Interview data were analyzed using an inductive qualitative method for cross‐case analysis. Most GCs disagreed with NGHPs providing genetic services, but beliefs varied widely, ranging from disagreement due to perceived gaps in knowledge or clinical skills to acceptance of NGHPs providing genetic services due to limited access to genetics professionals. Across survey and interview data, GCs endorsed the interpretation of genetic test results, understanding implications of results, collaboration with genetics professionals, knowledge of the risks and benefits to testing, and recognizing indications for genetic testing as critical components of knowledge and clinical practice for NGHPs. Several recommendations for improving the provision of genetic services were provided by respondents including educating NGHPs to provide genetic services through case‐based continuing medical education and increasing collaboration between NGHPs and genetics professionals. As GCs are healthcare providers with experience and vested interests in educating NGHPs, their perspectives can help inform the creation of continuing medical education to ensure patients' access to high‐quality genomic medicine care from providers of varying backgrounds.


| INTRODUC TI ON
In recent decades, public interest in genetics and the integration of genetics/genomics into healthcare has progressively increased.
Since the completion of the Human Genome Project in 2003, the availability of genetic testing has skyrocketed with an estimated 75,000 genetic tests on the market as of 2018, and an additional 10 new tests entering the market each day (Phillips et al., 2018). Along with increases in the availability of genetic testing, genetic testing expenditures have also risen rapidly with the highest levels of spending centering on prenatal testing, hereditary cancer testing, and multigene panels (Phillips et al., 2018). As the demand for and utilization of genetic services has increased, questions have been raised about which healthcare professionals are best-suited to meet this demand.
Historically, genetics professionals including medical geneticists and genetic counselors (GCs) have provided the majority of genetic services, which may include ordering genetic tests, interpreting test results, providing genetic counseling, and related services (Campion et al., 2019). However, recent research has revealed critical shortages in the genetics professional workforce, resulting in increased wait times for patients and increased caseloads for genetics professionals (Maiese et al., 2019;United States Government Accountability Office, 2020). A growing subset of GCs have nondirect patient care or mixed positions, contributing to a shortage of GCs engaged in direct patient care that is not expected to reach equilibrium until between 2024 and 2030 (Hoskovec et al., 2018;National Society of Genetic Counselors, 2021b). As a result of this increased demand for genetics services and simultaneous stagnation of available genetics professionals in direct patient care positions, a majority of genetic test requests are now placed by non-genetics healthcare professionals (NGHPs) including obstetricians/gynecologists, oncologists, and others (Bajguz et al., 2021); however, it is unclear from existing data the proportion of genetic tests that are ordered without any GC involvement.
While the provision of genetic services by NGHPs may allow greater access to care for patients and their families, barriers exist in this genetic service delivery model including inadequate knowledge, challenges with collecting detailed or updated family histories, lack of confidence in assessing and referring patients for genetic conditions, and lack of resources and guidelines (Hamilton et al., 2017;Mikat-Stevens et al., 2015;White et al., 2020). Gaps in genetics/genomics knowledge and a lack of comfort have persisted in recent years in populations of both primary care physicians and non-genetics specialists (Chow-White et al., 2017;Dekanek et al., 2020;Gates et al., 2022;Hamilton et al., 2017;Kathrens-Gallardo et al., 2021). Additionally, several studies have evaluated clinical practices in genetics/genomics among these providers.
Studies found that half of surveyed primary care physicians had ordered a genetic test in the past year and over 75% had referred to genetics professionals, with even higher rates of test ordering for certain medical specialists such as neurologists (Domínguez-Carral et al., 2017;Salm et al., 2014;Truong et al., 2021). When NGHPs do order testing and counsel patients themselves, key limitations have been noted including a lack of construction of a comprehensive three-generation pedigree, discussion of the implications of test results for family members, benefits and limitations of risk management options, and the meaning of different potential variant results . Furthermore, primary care physicians often do not adhere to clinical guidelines for facilitating informed consent for genetic testing and inconsistently recognize clinical scenarios where genetic testing or referrals are warranted (Hamilton et al., 2017;Truong et al., 2021).
Unfortunately, gaps in genetics/genomics knowledge can lead to medical errors such as ordering the incorrect test, misinterpreting test results, incorrectly assuming a variant completely explains a family history of cancer, or providing inadequate information about genetic test results (Farmer et al., 2019(Farmer et al., , 2021. Errors like these can lead to adverse events with negative medical, ethical, and financial implications for patients and their relatives such as incorrect medical management recommendations or misuse of healthcare resources (Brierley et al., 2012). In addition, the psychosocial and emotional effects of these adverse events may negatively shift patient attitudes toward medical providers overall (Bensend et al., 2014).

K E Y W O R D S
clinical practice, education, genetic counselors, genetics services, genomic medicine, nongenetics healthcare professionals

What is known about this topic
Despite documented concerns about knowledge and clinical practices in genetics/genomics, non-genetics healthcare professionals (NGHPs) routinely provide genetic services. Core competencies in genetics/genomics for NGHPs have been suggested and published by several groups.  (Arcila et al., 2022;Korf et al., 2014;Tognetto et al., 2019). Additionally, educational modules and certificate programs have been developed by professional organizations and other stakeholders such as the American College of Medical Genetics and Genomics, American Society of Clinical Oncology, Nurse Practitioners in Women's Health, International Society of Nurses in Genetics, and the Jackson Laboratory, among others. So far these have shown promise in increasing NGHPs' knowledge, skills, comfort, and clinical practices related to genetics/genomics (Talwar et al., 2017).

What this paper adds to the topic
Despite this progress, GCs' opinions about NGHPs providing genetic services differ. Many acknowledge that accessibility and prior patient-provider relationship are potential benefits, but half of GC participants in a 2014 study perceived minimal or no benefit to NGHPs providing genetic services to their patients (Bensend et al., 2014). GCs are experts in genetics/genomics and often serve as healthcare professional educators, making them valuable stakeholders in both the provision of genetic services by NGHPs and the efforts to educate them (Dragojlovic et al., 2020;National Society of Genetic Counselors, 2021b). Therefore, it is important to understand what GCs perceive as the most critical aspects of genetics/genomics education for NGHPs to help increase patient access to high-quality genetic services from providers of varying backgrounds. The purpose of this study was to (1) understand GCs' perspectives on the provision of genetic services by NGHPs and (2) assess the knowledge and clinical practices in genetics/genomics that GCs believe are critical for NGHPs in the provision of genetic services.

| Participants and procedures
We performed a mixed-methods study to assess GCs' perspectives on the provision of genetic services by NGHPs and to identify the components of knowledge and clinical practice in genetics/genomics most critical for these providers. To do so, we utilized an online quantitative survey of practicing GCs and follow-up qualitative interviews to provide additional, deeper context to the preliminary survey.
We recruited a sample of GCs through email invitation using the National Society of Genetic Counselors (NSGC) and American Board of Genetic Counselors research listservs, representing a group of more than 5000 GCs in the United States and Canada. We supplemented recruitment through targeted social media posts and snowball sampling. Gift card incentives were offered to survey and interview participants.
In January of 2021, participants who volunteered for recontact were invited to complete a follow-up interview by audio-only online conferencing. Of the GCs who fully completed the initial quantitative survey, 103 participants indicated that they were interested in completing a follow-up interview. In multiple waves, eligible participants were randomly selected and invited via email to complete a follow-up interview. Recruitment continued until 17 interviews were completed. After completing 17 interviews, we recognized clear and common themes that provided sufficient additional context to the survey results. Considering time constraints and the rich data provided by the 17 participants, we did not conduct additional interviews. Interview responses were recorded and transcribed using the online transcription service Otter.ai (2021). Transcripts were manually reviewed by author T.C. and audited for transcription errors.
This study was approved by the Institutional Review Board at the University of North Carolina at Greensboro (Study #21-0120).
Participants provided consent for survey and/or interview responses to be shared in aggregate or using anonymized participant codes.

| Instrumentation
The quantitative survey was developed by the research team which included a GC who has conducted similar research before (T.B.) and a GC with prior experience in survey development (R.M.). The survey tool contained 10 items to elicit demographic information including gender identity, race, years in practice, work setting, and specialty.
Participants were asked a novel Likert-style question regarding their beliefs about whether NGHPs should provide genetic services.
Participants were then presented with a list of 16 genetics/genomics knowledge components and asked to select exactly five that they believe are most critical for NGHPs. These knowledge components were based on a previously published list of genetics/genomics competencies for NGHPs (Tognetto et al., 2019). Finally, participants were presented with a list of 12 components of clinical practice in genomics and were asked to select exactly five components that they believe are most critical for NGHPs. The list of clinical practices were based on a previously published list of clinical practices in genomics . The final survey was piloted with two GCs unassociated with the project before implementation. The full list of components of knowledge and clinical practice in genetics/genomics are available in the article's Supplementary Material (Table S1); the components as written in this text are presented in an abbreviated form.
The qualitative interview protocol was developed following completion of the online survey to allow for preliminary results to drive the research questions explored in the interviews. The interview protocol contained four major sections: demographic questions, GCs' beliefs about whether NGHPs should provide genetic services and the components of genetic services that NGHPs should provide to their patients, GCs' perceptions of the knowledge of NGHPs and the components of knowledge they perceive as most critical for NGHPs, and GCs' perceptions of the clinical practice in genetics/genomics of NGHPs and the components of clinical practice they perceive as most critical for NGHPs. Finally, the interviews concluded with two broad questions allowing for participants to express additional perspectives on the provision of genetic services by NGHPs.
Throughout the study, NGHPs were defined as healthcare professionals without formal training or expertise in genetics/genomics which may include primary care physicians, non-genetics specialists, mid-level providers, such as nurse practitioners, and others. Genetic services were defined as a set of clinical practices in genetics/genomics that includes family history risk assessment, ordering genetic testing, interpreting genetic testing results, the provision of genetic counseling, and other related services.

| Data analysis
Descriptive statistics including means and percentages were calculated for responses to the quantitative survey items. Crosscomparisons utilizing demographic data were calculated for participants' primary specialty and work setting using Chi-square analysis. Cross-comparisons based on participant specialty were limited to participants in cancer, prenatal, and pediatric specialties due to an insufficient number of participants in other specialties. Crosscomparisons utilizing the participants' years practicing as a GC were calculated using Spearman's rank-order correlation.
Qualitative analysis of the interview transcripts was conducted based on the Consensual Qualitative Research framework developed by Clara Hill and colleagues, an inductive qualitative analysis method (Hill, 2012). The primary data analysis team, consisting of authors T.C. and T.B., independently read each interview transcript and constructed domains from the interview data. For each case, excerpts of the transcript were coded into the appropriate corresponding domain and were distilled into a core idea summarizing the transcript excerpt. After grouping responses into domains, the primary data analysis team further classified excerpts into categories and subcategories as appropriate. After the coding of transcript excerpts was completed for all cases, the primary analysis team conducted cross analysis to identify commonalities across cases. At multiple points throughout the data analysis process, author R.M. served as a data auditor and reviewed the domains and categorization of each interview transcript. Any disagreements on the coding or categorization of transcript excerpts were discussed until a consensus was reached.

| Survey participant characteristics
A total of 240 GC participated in the online quantitative survey and answered at least one question, with 207 participants answering all questions. Demographic information is summarized in Table 1.
Most participants were female (91.8%), White (91.9%), and non-Hispanic (97.6%). The number of years practicing as a GC ranged from less than 1 year to 42 years, with a median of 5 years and mean of 8.2 years. The demographics of the study population are consistent with the 2021 NSGC Professional Status Survey and participants from all major specialties, work settings, and NSGC geographic regions are represented (National Society of Genetic Counselors, 2021a, 2021b).

| Beliefs about whether NGHPs should provide genetic services
Genetic counselors were asked to indicate the extent to which they agree with the following statement: "Non-genetics healthcare professionals should provide genetic services, including the ordering and interpreting of genetic tests." The majority of the 240 participants disagreed with the statement (38.3% somewhat and 15% strongly disagreed), 11.25% neither agreed nor disagreed, and 32.5% somewhat and 2.93% strongly agreed, respectively. There was a statistically significant difference in responses to the prompt based on participants' number of years practicing as a GC. As years practicing as a GC increased, participants' agreement with the prompt increased modestly (Spearman's correlation coefficient = 0.256; p < 0.001). No other significant relationships between demographic variables and responses to the prompt were identified.

| Critical components of genetics/genomics knowledge for NGHPs
Participants were asked to select exactly 5 of the 16 knowledge components that they believe are most critical in the provision of genetic services by NGHPs ( Table 2). A majority of participants selected 'interpretation of results' (85.3%), 'benefits and risks of genetic information' (65.3%), and 'indications for genetic testing' (60%) as the most critical components of genetics/genomics knowledge for NGHPs. Conversely, <10% of participants selected 'genomic approaches to treatment' (8%), 'multifactorial influences on complex disease' (5.8%), 'direct-to-consumer testing, results, and risks' (5.3%), and 'genomic variant interpretation' (3.6%) as components of knowledge that were most critical for NGHPs.

| Critical components of clinical practice in genetics/genomics for NGHPs
Participants were asked to select exactly 5 of the 12 components of clinical practice in genetics/genomics that they believe are most critical in the provision of genetic services by NGHPs. A majority of participants selected 'discuss risks, benefits, and limitations of testing' (81.1%), 'discuss implications of results for patients' (79.1%), 'refer patients to genetics experts' (70.4%), 'explain possible genetic results' (68.4%), and 'apply guidelines to manage patients with genetic conditions' (53.9%) as the most critical components of clinical practice for NGHPs (Table 3). Conversely, <20% of participants selected 'provide support to coping patient' (16%), 'discuss insurance issues (e.g., Genetic Information Non-Discrimination Act [GINA])' (14.6%), 'educate about emotions patient may experience' (12.1%), and 'refer to support groups' (2.9%) as components of clinical practice that were most critical for NGHPs.

| Interview participant characteristics
Seventeen GCs participated in the open-ended interview. Interviews ranged in length from 20 to 39 min, with a median length of 26 min.
The number of years practicing as a GC ranged from less than 1 year to 14 years, with a median of 4 years. Participants worked in a variety of specialties and settings ( quencing. Participants believed NGHPs should not regularly provide comprehensive testing due to the breadth of information generated by such testing, the potential for secondary findings, and the benefit of an assessment by a medical geneticist.

Genetic counselors also provided examples of other components
of genetic services they believe that NGHPs should not provide.
These include the interpretation of genetic testing results (n = 8), risk assessment (n = 2), providing genetic counseling (n = 2), and cascade testing for a known familial genetic variant (n = 2).

| Domain 2: Critical components of knowledge and clinical practice in genetics/genomics for NGHPs
Analysis of interview transcripts yielded multiple critical components of knowledge and clinical practices in genetics/genomics for NGHPs that were able to be grouped into six main categories. All Cancer 4 Pediatrics 4 Research 2 Neurology 2

Work setting
Hospital/Medical facility-Academic medical center 8 Hospital/Medical facility-Private (nonprofit or for profit) 5 Hospital/Medical facility-Public 3 University 1 Private company-Telegenetics 1 Note: Participants could report multiple specialties or work settings. Therefore, the total for each variable exceeds 17.

TA B L E 5
Types of genetic tests that genetic counselors believe non-genetics healthcare professionals have the skillset to order.

Routine screening 5
Single phenotype test a 5

Chromosomal microarray 4
Karyotype 4 Fragile X testing 3 Prenatal screening 3 a Single phenotype tests endorsed by participants include panels for epilepsy, arrhythmias, and hereditary cancer predisposition.

| Domain 3: Recommendations for improving the provision of genetic services
Although the first two domains described could be directly linked to the research questions, an additional domain related to improving the provision of genetic services emerged from the interview data. they've gone to a thousand websites or watched webinars, and they don't really take much from that.
Additionally, a majority of participants recognized the importance of collaborations between genetics providers and NGHPs (n = 10).  for NGHPs, but this study represents a novel step forward by having GCs rank components by how critical they believe them to be for NGHPs (Arcila et al., 2022;Korf et al., 2014;Tognetto et al., 2019).

| DISCUSS ION
Non-genetics healthcare professionals, particularly primary care physicians, have expressed a lack of confidence in these skills including identifying individuals with genetic conditions, knowing when to refer for genetic counseling, discussing benefits and risks to testing, and evaluating the clinical usefulness of a genetic test Hamilton et al., 2017). In addition to self-reported confidence by NGHPs, gaps in the genetics/genomics knowledge and clinical practices of NGHPs have been observed (Dekanek et al., 2020;Hamilton et al., 2017;Vadaparampil et al., 2015). These gaps in knowledge or clinical practice of NGHPs can result in adverse medical, psychological, and financial events for patients and their families due to inaccurate ordering, misinterpretation of results, or inadequate genetic counseling (Bensend et al., 2014;Brierley et al., 2012;Farmer et al., 2019Farmer et al., , 2021. Although limited, there have been some data published on differential outcomes between genetic services provided by NGHPs or genetic professionals, showing that NGHPs may miss opportunities for genetic testing or referrals or that pretest counseling discussions with GCs are more comprehensive and result in better patient recall of discussed information Truong et al., 2021). In contrast, a recent oncologist-led genetic test mainstreaming study found no differences in patient satisfaction, test uptake, and psychosocial measures including decisional conflict, showing that NGHP-led genetic services have the potential to increase access to genetic services without adverse patient outcomes (Yoon et al., 2022).  Wilkes et al., 2017). Genetics/genomics education initiatives for NGHPs like these have been developed by multiple stakeholder groups and professional organizations described above. Initiatives like these have been shown to increase confidence, impact clinical practices such as referral rate, and increase knowledge (East et al., 2022;Houwink et al., 2014;Reed et al., 2016). As experts in genetics/genomics with a vested interest in and the skills to educate NGHPs, GCs may serve in key roles in increasing the knowledge base of NGHPs in genetics/genomics. Future studies can continue to investigate the outcomes of continuing medical education in genetics/ genomics for NGHPs and the involvement of GCs in this education.

| Study limitations
Although demographics of the study participants are similar to national workforce data, participants in this study overwhelmingly identify as white and female. We found no difference in responses to survey questions based on practice setting or specialty; however, there were relatively more participants from academic medical centers and the pediatric specialty and fewer participants from commercial laboratories and the cancer specialty compared to national workforce data. Compared to the demographic characteristics of the survey sample, there was a lack of representation of participants working in industry roles and relative overrepresentation of participants in the prenatal specialty among interview participants.

| Practice implications
In both the survey and interview data, GCs consistently expressed that particular components of knowledge and clinical practice are critical for NGHPs when providing genetic services, including interpretation of results, understanding implications of results, cooperation with genetic professionals, and risk assessment. As GCs often interact with NGHPs in daily practice or provide informal education, the perspectives expressed here may help in highlighting components of knowledge and practice that significant proportions of GCs believe to be most important to allow for targeted education of NGHPs.
Additionally, GCs in this study emphasized the importance of serving as a resource to NGHPs seeking to provide genetic services to their patients, with some calling for an adjustment of attitudes of genetics professionals who believe they are the only providers that should provide genetic services. GCs in interviews consistently expressed that a lack of access to genetics professionals necessitates the involvement of NGHPs in providing genetics services to ensure access to care. Due to the limited access to genetics professionals for many patients, many clinics and healthcare systems have adjusted service delivery models to include GCs working in tandem with NGHPs, NGHPs providing certain components of genetic services for routine indications, or GCs providing a consultative service for other healthcare professionals (Harding et al., 2019;Stoll et al., 2018), echoing ideas expressed by GCs participating in this study. In the future, adjustments to traditional genetic service delivery models to increase the involvement of NGHPs may be necessary. Further research is needed to elicit GCs' perspectives on these adjustments and to evaluate the outcomes of modifying service delivery models in improving access to effective and timely genetic testing and counseling services.

| CON CLUS IONS
This study investigated GCs' perspectives on the provision of genetic services by NGHPs and identified components of knowledge and clinical practice in genetics/genomics that GCs believe are critical for NGHPs. Participants expressed a range of opinions about whether they believe NGHPs should provide genetic services that included disagreement due to perceived gaps in knowledge or lack of clinical skills and acceptance of NGHPs providing genetic services due to limited access to genetics professionals. GCs endorsed interpretation of results, understanding implications of results, cooperation with genetic professionals, knowledge of the risks and benefits to testing, and risk assessment as critical components of knowledge and clinical practice in genetics/genomics for NGHPs. Alongside previously published core competencies in genetics/genomics and frameworks for genetics/genomics education for NGHPs, our data highlight the components of knowledge and clinical practice that GCs believe to be the most critical for NGHPs who provide genetic services. Critically, these data have the potential to influence physician education initiatives by targeting training toward the knowledge and skills that GCs perceive as the most crucial components. As demand for genetic services continues to increase, GCs' perspectives can help shape the development of baseline and continuing education in genetics/genomics for NGHPs to ensure access to high-quality genomic medicine care for patients.

AUTH O R CO NTR I B UTI O N S
All authors contributed to the research concept and design for the study. Tanner Coleman performed data analysis for survey data.
Tanner Coleman, Tracy Bensend, and Rachel Mills analyzed and interpreted the interview data. All authors assisted with manuscript composition and provided final approval to the submitted manuscript. Tanner Coleman confirms that they had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. All of the authors gave final approval of this version to be published and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

ACK N OWLED G M ENTS
The research presented in this manuscript was completed while the first author was a trainee in the Genetic Counseling Program at the University of North Carolina at Greensboro. We are grateful for this institutional support and to the following individuals for their con-

CO N FLI C T O F I NTER E S T S TATEM ENT
Authors Tanner Coleman, Tracy Bensend, Rachel Mills, Lori A.
Orlando, and Lauren Doyle declare that they have no conflict of interest.

DATA AVA I L A B I L I T Y S TAT E M E N T
The data that support the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.

CO M PLI A N CE WITH E TH I C A L S TA N DA R DS: H U M A N S TU D I E S A N D I N FO R M E D CO N S E NT
This study was approved and conducted according to the ethical standards of the Institutional Review Board at the University of North Carolina at Greensboro (Study #21-0120). All applicable international, national, and/or institutional guidelines were followed.
A waiver of signed consent was obtained for the online survey, and verbal consent was provided by interview participants. Prior to beginning the online survey and interview, participants were presented with informed consent documents. Implied informed consent was obtained for individuals who voluntarily completed the online survey and submitted their responses.

A N I M A L S TU D I E S
No nonhuman animal studies were carried out by the authors for this article.