Introduction

Primary care has a critical role in medical genetics, as the field has reached a defining point. While significant progress has been made in expanding and improving access to and knowledge of genetic services through rapid advances in both clinical practice and technological innovation, serious gaps remain in the delivery of genetic services to medically underserved populations. These gaps are created by disparities in the distribution of medical genetic workforce and limited health insurance reimbursement for genetic testing and counseling (Chou et al. 2009; Senier et al. 2015; Cooksey et al. 2005; Cooksey et al. 2006; Maiese et al. 2019). To bridge these gaps, integrating genetic services into primary care has been singled out as a priority. Primary care often serves as the only access point to medical care for many patients, especially in rural areas where there are shortages of medical professionals.

In the US, the shortage of genetic services workforce has been well documented (Cooksey et al. 2005; Cooksey et al. 2006). At the present, more than 600 genetic counseling positions remain unfilled (Henson et al. 2016; Stein 2016). Medical genetics residency positions face similar vacancies, and an increasing number of clinicians trained in genetics are leaving medical service positions to fill a growing number of job openings in biotechnology (Cichon and Feldman 2014). A national survey found that 68% of participating organizations had many vacancies in the area of geneticists and genetic counselors (Maiese et al. 2019).

Moreover, advances in next-generation sequencing have improved how we identify genetic etiologies while simultaneously increasing the demand for professionals qualified at interpreting these findings. As the technology matures, direct marketing of gene panels to consumers and physicians has resulted in more testing (Cornel and van El 2017). The cumulative effects of these trends are lengthy wait times for appointments, increased potential for misinterpretation of genetic test results, and overworked providers (Kaye et al. 2019). An American College of Medical Genetics (ACMG) survey showed that these trends have severely impacted families needing services: 46% of families of children with special healthcare needs experienced difficulty accessing services, and 42% of families had to wait over a month on average to see a genetic service provider (Kaye et al. 2019; Maiese et al. 2019).

Engaging, leveraging, and preparing the non-genetics healthcare workforce to deliver genetics-related services are needed to reduce disparities and meet the increasing demands for services. Primary care providers (PCPs), especially those practicing in rural areas, serve as points of entry and provide a pathway for patients and families to access appropriate care. In the absence of genetic specialists, PCPs often play a crucial role in caring for children and adults with genetic disorders (Andermann and Blancquaert 2010). Integrating genetic services delivery into primary care may potentially improve access to necessary services. In other words, optimal delivery of genetic services in many cases may rely heavily on the efforts of PCPs. To that end, strategies to support and better equip PCPs in delivering genetics-related care need to be identified, assessed, and implemented. The objectives of this scoping review are to (1) assess potential barriers to the integration of medical genetics and primary care, and (2) develop strategies to support the integration and mitigate barriers identified.

Methods

Some evidence has emerged in recent years to explore the topic surrounding integration of medical genetics into primary care. We conducted a scoping review to lend some clarity to this complex question as well as to refine and inform subsequent inquiries (Mays et al. 2001; Pham et al. 2014). The approach for this scoping review is based on Arksey and O’Malley’s framework: (1) identifying a research question; (2) searching relevant literature; (3) selecting articles; (4) charting the data; and (5) summarizing and reporting results (Arksey 2005).

Identifying a research question

This study was guided by the question, “What are barriers to the integration of genetic services and primary care?” For the purpose of this study, the scoping review is defined as a research synthesis that aims to map the literature on a particular topic or research area as well as identify key concepts; gaps in the research; and types and sources of evidence to inform practice, policymaking, and research (Daudt et al. 2013).

Literature search

To capture all relevant literature, the search strategies focused on broad topics, including interface of genetics and primary care, role of medical geneticists, and patient-centered care. We used a systematic approach centered on the aforementioned topics to search Ovid MEDLINE without any restrictions on the article publication dates up to February 2020.

For the initial searches, we used the following search terms: healthcare delivery, primary care, child health services, medical homes, underserved populations, vulnerable populations, genetics, genetic counseling, access to genetic services, infrastructure, financial, legal, and barriers. Based on initial search results and review, we included additional search terms to identify potential strategies, such as genetic risk assessment, patient-centered care, telegenetics, telemedicine, learning communities, disease management model, and patient satisfaction. We combined productive search terms with other productive search terms to conduct a Boolean search in order to yield results that were more specific to the overall review topic. These initial search results were limited to those in English language, involved human subjects only, and did not contain primary DNA sequencing data and/or analyses. Upon article retrieval, we reviewed the bibliographies of the articles in an attempt to identify additional titles. Since literature related specifically to PCPs, genetic services, and underserved populations is notably sparse, we further included and analyzed references from gray literature, using Google and Yahoo search engines. Snowballing method was applied whenever appropriate.

Citation management

References from the MEDLINE search and gray literature were extracted and exported into a bibliographic software, EndNote [v.X9, Clarivate, Philadelphia, PA], for management and analysis. Duplicate citations were removed, and all remaining titles and abstracts were screened for relevance

Article selection and exclusion criteria

We excluded references based on the following criteria: (1) published more than 15 years ago, (2) little relevant information or duplicate content that was more fully described in other titles, (3) peripherally related to the intersection of primary care and genetic services, and (4) focus on different aspects of genetics-oriented research with no primary care tie-in. We preemptively addressed any issues of double counting by reviewing all included systematic reviews and their bibliographies. We did not include references already included in the previously published systematic reviews. Figure 1 presents a flow chart of reference inclusion and exclusion.

Fig. 1
figure 1

Summary of literature searches and article selection

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Data characterization and synthesis

Upon screening the titles and abstracts, relevant citations were included for full-text review. Two reviewers read all of the articles and then assigned each to one of three categories for analysis: (1) barriers to integrating primary care and genetic services, (2) current landscape of genetic service delivery, or (3) primary care support and integration strategies. We constructed evidence tables to organize and summarize the articles. Articles in category one were summarized in Table 1 and those in categories two and three are collated in Table 2.

Table 1 Evidence on barriers to integration
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Table 2 Strategies to facilitate delivery of genetic services via integration with primary care
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Results

The literature search yielded 1340 unique titles. These titles were scanned for relevance based on titles and abstracts, where 414 titles were selected for further analysis (Fig. 1). The final set retained 42 articles, with 13 titles describing barriers encountered in the integration of genetic services and primary care (Table 1) and 29 related to primary care support and genetics integration strategies (Table 2).

Of the 42 articles analyzed, we identified 12 cross-sectional studies, seven reviews (systematic and basic literature), five randomized controlled trials, three implementation studies, and two pre-post analyses. We also found relevant information in one quantitative retrospective study, five qualitative studies, one mixed-methods study, two commentaries, a meeting report, a case report, a program evaluation, and an article detailing model development and evaluation.

Barriers for PCPs

Barriers to providing genetic services that were cited by PCPs include insufficient time to provide these services, a lack of access to genetic referrals and resources, and those related to limited knowledge in genetics (e.g., lack of clinical guidelines/care pathways, training, and confidence in genetics) (Carroll et al. 2009; McCahon et al. 2009; Najafzadeh et al. 2013; Wakefield et al. 2018). In the sole systematic review identifying barriers in our search, Mikat-Stevens and colleagues found that barriers most frequently mentioned by PCPs include a lack of knowledge about genetics and genetic risk assessment, concern for patient anxiety, a lack of access to geneticists, and insufficient time to address these challenges (Mikat-Stevens et al. 2015). In addition to reporting limited knowledge and difficulties accessing resources, expertise, and training, PCPs in rural areas expressed concerns about cost, distance, and poor patient engagement (Harding et al. 2019).

These barriers impact practice, further impeding care delivery to patients in need of genetic services. Some studies showed that most clinicians in primary care do not provide genomics-based care largely due to lack of knowledge (Lopes-Junior et al. 2017), or unavailability of clinical guidelines (Najafzadeh et al. 2013). Most PCPs would neither order genetic testing nor refer their patients to a genetics specialist as the first step in their evaluation (McCahon et al. 2009; Tarini et al. 2015). Kne and colleagues showed that there is even a lack of knowledge about how to utilize genetic counselors’ services appropriately (Kne et al. 2017). Even in cases where PCPs have received some genetic education, the knowledge and confidence gaps remain. In a sample of recently trained PCPs who had formal genetics education and positive views of the utility of genetic testing, the respondents felt unprepared to work with patients at risk for genetic conditions and were not confident about interpreting test results. Moreover, they were concerned about insurance discrimination and lacked trust in companies that offer genetic tests (Hauser et al. 2018).

Primary care and medical genetics integration

Mitigating barriers to integrating genetics into primary care, we identified a set of strategies for implementation. These strategies center on innovative service delivery approaches that go beyond face-to-face encounters with patients as well as educational outreach and support for PCPs.

As the use of telemedicine has become more integrated into care delivery to remote areas, its application in genetics has become more widely accepted. Moreover, results from a number of studies included in this review state that patients are generally just as satisfied, if not more, with telegenetics services as they are with traditional face-to-face consultations (Buchanan et al. 2015; Hilgart et al. 2012; Otten et al. 2016a; b). In addition, digital platforms and other electronic resources, such as web meetings, can be leveraged to deliver education or “refreshers” to PCPs as well as access to specialists, thereby empowering them to provide better care in their own communities (Hilgart et al. 2012). Nevertheless, barriers to access exist despite this level of satisfaction not just in the US but also beyond: one research team found that telegenetics technology uptake was significantly low throughout several European countries, which the team discovered was due primarily to a lack of financial resources, professional support, and/or knowledge, similar to their US counterpart (Otten et al. 2016a; b).

One of the ways to ameliorate the knowledge gap in genetics among PCPs is provide education and tools across a range of topics via various delivery modes and media. In a survey of PCPs, participants identified contact information for local genetic clinics, summaries of genetic disorders, referrals and testing criteria as useful information for their practice. While most preferred in-person learning, over half wanted contact with genetic counselors to answer questions and web-based education (Carroll et al. 2019). Evaluation of an interactive web-based curriculum focusing on communication; basics of genetic testing; risk assessment; ethical, legal, and social implication (ELSI) discussions; and practice behaviors demonstrated better shared decision-making and increases in ELSI discussions with patients (Wilkes et al. 2017). In addition, many innovations, such as standardized history forms and questionnaires, have been developed and disseminated to make gathering information on family history and hereditary risk factors easier for PCPs.

Patient-centered medical homes (PCMHs), which are characterized by team-based care coordinated by primary care to manage complex or chronic diseases, had originated as a care delivery model in pediatrics. PCMHs have been cited as being advantageous in many ways, including providing better access to, quality and continuity of, and patient satisfaction with medical care (Agency for Healthcare Research and Quality 2019; David et al. 2015). PCMHs have also been shown to be practical for underserved populations (Balachandra et al. 2009; Mead et al. 2014). Adapted specifically to enhance access to and quality of genetic services, Kubendran and colleagues developed and tested a collaborative services delivery model derived from the PCMH concept that consisted of a pediatrician, medical geneticist, and genetic counselor (Kubendran et al. 2016). This model also relies on the availability of telegenetics and involvement of families. To reduce long wait for referrals to geneticists, the proposed model refers patients who have genetic indications of a syndromic etiology directly to a geneticist via telegenetics, with all others delegated to primary care via an in-person pediatric or genetic counseling clinic before following up with the geneticist. This type of clinic provides a model of collaborative care that exemplifies a medical home neighbor and the integration of genetics into primary care (Kubendran et al. 2016). As partners in a PCMH, providing tools, education, and resources empower families to assume a primary role in care coordination, which results in higher satisfaction and improvement in healthcare outcomes (Ufer et al. 2018; Williams et al. 2018).

Discussion

Findings of this review show that, despite some progress, challenges remain in the integration of primary care and genetic services. Nevertheless, several articles have identified specific barriers that are amenable to interventions.

Recommendations

Since PCPs in medically underserved areas already take on the role of bridging the gap between primary care and genomic medicine, we must make it easier for these providers to access specialists and increase their genetics expertise to help their communities. Most PCPs have limited experience with clinically operationalizing the ever-growing body of actionable genetic information and are insufficiently prepared to incorporate this information into their current practices. The scoping review findings suggest the following strategies to bridge the gap in clinical knowledge and enhance access to genetic services: telegenetics, partnership trios that expands upon the PCMH concept, and learning communities (Fig. 2).

Fig. 2
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Strategies creating new pathways to genetic services via integration of medical genetics and primary care

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Telemedicine/telegenetics

In general, telemedicine can be an impactful mechanism for extending the reach of limited healthcare personnel and has been integrated into other clinical settings (Ekeland et al. 2010; Fortney et al. 2013; Terry et al. 2019). Using telemedicine can increase access to specialty services for underserved rural and urban populations. Tele-consultations can circumvent prohibitive travel and associated costs for patients. For patients with genetic disorders, these visits may have to occur on a regular basis for many years, so tele-consultations may maintain the status quo. Furthermore, for referring community providers, telemedicine technology opens up new possibilities for continuing education and training as well as interactions with specialists on a case-by-case basis (Beste et al. 2017). It may also be used for educating families and the larger healthcare community.

A systematic review of telemedicine in genetics services reported high levels of patient satisfaction and receptiveness (Hilgart et al. 2012). However, the use of telegenetics as a service delivery model remains low in the US, estimated at 26% in the most recent report (Beste et al. 2017). The lower uptake may be attributed to limited capacity due to various requirements, such as credentialing and reimbursement for these services. Low adoption rates have been observed in other parts of the world, such as Europe, in addition to the US (Otten et al. 2016a; Otten et al. 2016b). Allocation of financial resources to support telegenetics training, equipment, and technical assistance must be prioritized to increase uptake. Organizational support, leadership buy-in, and a culture oriented towards embracing innovations and change are additional facilitators for telemedicine uptake in genetics. However, the use of telemedicine has dramatically increased with the ongoing novel coronavirus (COVID-19) pandemic. While containing the spread of COVID-19 has been challenging, this situation has allowed clinicians to demonstrate the utility of telemedicine technologies. Particular to the US, the growing number of virtual “office” visits presents an opportunity to expand telemedicine and bring specialty care services, such as genomic medicine, to patients in underserved areas who otherwise would lack such access (Rockwell and Gilroy 2020).

Partnership trio

Since the introduction of the PCMH, the model has continued to be adapted and refined. As an adaptation of this and similar models, a partnership trio among non-genetics providers, clinical genetics providers, and parents/families would be especially effective. Developing a protocol and providing a mechanism to connect PCPs and genetic providers via genetic counselors or telegenetics would enhance access to genetic services, which is precisely what the partnership trio entails. When piloting their collaborative model, Kubendran and colleagues demonstrated high patient satisfaction and shortened wait time to receive appropriate genetic care (Kubendran et al. 2016). The widespread paucity of pertinent resources has compelled parents and families who have children with special healthcare needs to formalize support groups to share knowledge, provide peer support, facilitate connection to services, and advocate for policy change (Genetic Alliance 2019; Beste et al. 2017). Linking clinical and family partners and their efforts as a trio can significantly improve access to genetic services.

Learning communities

Enhanced training, evidence-based guidelines, and clinical tools support effective delivery of or facilitate access to genomic medicine by PCPs (Hauser et al. 2018). Access to information and expertise in genetics provides a critical resource for PCPs. Learning communities may represent a mechanism by which to facilitate information exchange and knowledge sharing among genetic and non-genetic providers. Within communities of clinicians, using a listserv to host questions and responses has been an effective way to share information. List-servs may also allow clinicians to have certain questions answered in real time. Moreover, little is known about the education needs of those providing wrap-around and social services, such as home visitors and early interventionists, as well as family support networks, and it would be beneficial to include those in the learning communities. These groups may also offer perspectives that would highly complement the clinical care delivery, thereby enhancing the overall education of all in the community.

Another strategy is using Project ECHO™ (Extension for Community Healthcare Outcomes), an interactive and evidence-based approach that provides medical education for managing complex and traditionally specialist-managed health conditions through tele-mentoring and co-management of patients with PCPs (University of New Mexico 2019). It is a model that is particularly well suited to serve patients in underserved areas. ECHO connects specialists located in academic centers (i.e., hubs) and community primary care sites (i.e., spokes) through the use of technology to improve communication and learning (Katzman et al. 2016). The ECHO model has demonstrated success in managing chronic conditions and now operates more than 90 hubs covering more than 45 diseases and health conditions in 16 countries (Arora et al. 2011a; b; Kaye et al. 2019). Arora and colleagues demonstrated that the quality of hepatitis C care provided by Project ECHO-trained PCPs was equal to that of care provided by university-based specialists (Arora et al. 2011a; b). Following a similar path, the ECHO model may create a dynamic, all-directional learning community between PCPs and specialists in genetics by enhancing PCPs’ knowledge, skillset, confidence, and practice in their local communities (Katzman et al. 2016).

This scoping review is comprehensive and rigorous, identifying both gray literature and articles from MEDLINE, including reference lists from articles extracted from the search. However, this review may not have identified all relevant literature. Although it would have been beyond the scope of this review, the search terms did not include certain terms like telephone conversations, coordination of care, consultation, provider-to-provider correspondence, or group appointments that might have yielded more articles describing strategies and limitations related to traditional methods of healthcare provider collaboration and dissemination of expert information from geneticists. This discussion also did not address alternative healthcare delivery and managed care models specific to genetics that may be more common outside of the US to identify other potential integration strategies.

Conclusions

To realize genetic and genomic service integration in primary care settings, it is imperative that frontline clinicians be equipped with the knowledge and support they need to manage patients with complex genetic diseases. Multiple strategies to ameliorate access to genetic services in a timely and effective manner are identified, some of which require nominal resource investments for implementation given the ready availability of many modern technologies and overlaps in coordinated care strategies (Fig. 3). By applying the partnership trio model for service delivery, using telegenetics, and leveraging the shared knowledge base of learning communities, it may be possible to create new and enhance existing access points for genetic services for children and adults, especially those who reside in medically underserved communities.

Fig. 3
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Recommendations for strategies to integrate medical genetics and primary care

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As healthcare infrastructure in the areas of informatics and telemedicine continues to expand, it is necessary for providers to communicate effectively with one another and share information that can benefit patient health outcomes. Recommendations derived from this scoping review can be used to achieve this objective. PCPs may capitalize on these strategies and opportunities to improve genetics service delivery for their patients, which is ultimately the goal of all PCPs.