Interventions to improve delivery of cancer genetics services in the United States: A scoping review

Abstract

Purpose:

Interventions that decrease barriers and improve clinical processes can increase patient access to guideline-recommended cancer genetics services. We sought to identify and describe interventions to improve patient receipt of guideline-recommended cancer genetics services in the United States.

Methods:

We performed a comprehensive search in Ovid MEDLINE and Embase, Scopus, and Web of Science from January 1, 2000 to February 12, 2020. Eligible articles reported interventions to improve the identification, referral, genetic counseling (GC), and genetic testing (GT) of patients in the United States. We independently screened titles and abstracts and reviewed full-text articles. Data were synthesized by grouping articles by clinical process.

Results:

Of 44 included articles, 17 targeted identification of eligible patients, 14 targeted referral, 15 targeted GC, and 16 targeted GT. Patient identification interventions included universal tumor testing and screening of medical/family history. Referral interventions included medical record system adaptations, standardizing processes, and provider notifications. GC interventions included supplemental patient education, integrated GC within oncology clinics, appointment coordination, and alternative service delivery models. One article directly targeted the GT process by implementing provider-coordinated testing.

Conclusion:

This scoping review identified and described interventions to improve US patients’ access to and receipt of guideline-recommended cancer genetics services.

Introduction

There are well-described delays between the publication of practice-changing research and guidelines and their clinical implementation.^1–3 When clinical implementation of guideline recommendations is delayed or incomplete and combined with systematic barriers in the delivery of health care services, disparities in patient access and receipt of recommended services are observed. Guidelines, such as those from the National Comprehensive Cancer Network (NCCN), provide criteria to identify individuals who may benefit from cancer genetics services; however, disparities in patient access and receipt of these services have been identified.^4–7 For example, the NCCN guidelines were updated in 2007 to recommend genetic counseling (GC) and germline genetic testing (GT) for all patients diagnosed with invasive, epithelial ovarian cancer; however, studies of patients diagnosed after the publication of those guidelines report that only 10% to 50% of the patients receive a referral, GC, and/or GT.^6,8 Studies of other cancer types, including breast, endometrial, colorectal, and pancreatic cancers, have identified similar trends.^6,9–12

Barriers to clinical implementation of guideline-compliant cancer genetics services can occur at various points in the health care delivery process, which ultimately disrupts the equitable delivery of care to patients. Steps included in the successful delivery of cancer genetics services in a typical US clinical setting include identifying that a patient is a candidate for genetics services on the basis of existing guidelines or referral criteria, making the referral or recommendation for the patient to receive genetics services, coordination and delivery of GC and/or coordination of germline GT (with or without genetic counselor support), laboratory analysis including health insurance authorizations and billing, receipt of genetic test results, and disclosure of the results to the patient. Each step in the clinical process has systems-level, health care provider, and patient factors that interact and influence the delivery of services.⁷ Various interventions have been created that can improve the delivery of cancer genetics services; however, many health care teams face complex combinations of barriers within their clinical setting and subsequent challenges to identifying interventions that may best address those barriers.

A recent systematic review by O’Shea et al¹³ identified interventions to increase patient uptake of genetics services. The study identified a variety of interventions but did not restrict article inclusion by country or health system structure. Given the complexities of the US health insurance system, historical and cultural considerations regarding trust and access to medical care, and health care policy considerations, interventions created in international settings may have important limitations or require significant adaptation if applied in a US clinical setting. Genetics professionals, oncology care providers, health systems, policy makers, and other stakeholders seek to improve equitable access to and receipt of guideline-based cancer genetics services for patients, and a compilation of current evidence can support these efforts and provide a toolkit of intervention options for clinicians.

We aimed to complete a scoping review of the peer-reviewed literature to identify and describe clinical interventions developed to improve patient access to, and receipt of, guideline-recommended cancer genetics services in the United States. We categorized interventions by their clinical process target (identification, referral, GC, and GT) to increase their utility for clinical application and to identify opportunities for future research and intervention development.

Materials and Methods

Protocol and registration

The review protocol was registered to the International Prospective Register of Systematic Reviews (PROSPERO 2020 CRD42020162354). The Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) 2018 scoping reviews reporting checklist was used to structure the results of this report (Supplemental Table 1).¹⁴

Eligibility criteria

We performed a comprehensive search in Ovid MEDLINE, Ovid Embase, Scopus, and Web of Science from January 1, 2000 to February 12, 2020. The publication time frame was selected to identify interventions most relevant for current guidelines and practice patterns. Search structures, keywords, Medical Subject Headings, and Emtree subject headings were tailored to each database by a medical research librarian (K.J.K.) specializing in systematic reviews. Search terms included terminology related to cancer; hereditary cancer pre-dispositions/syndromes (eg, hereditary neoplastic syndromes); and rates, uptake, or use of genetics services (eg, GT, GC). We excluded animal studies, in vitro studies, and case reports. Because our goal was to identify cancer genetics services in the United States, we restricted our search to English language articles only. Searches were not restricted by study type or any other type of limit. The full search string for the Ovid MEDLINE database can be found in Supplemental Table 2.

Selection of sources of evidence

Two reviewers (R.N. and E.M.B.) completed independent reviews of titles and abstracts using the Rayyan software.¹⁵ Titles and abstracts were first screened and excluded if they were unrelated to cancer; not germline/hereditary GT focused; molecular or gene-function studies; reporting the detection of gene variants or classification of specific variants; qualitative only with no quantitative methods; case studies or case reports; studies without an intervention; guideline or consensus recommendation articles. Titles and articles marked as “include/include,” “include/maybe,” and “maybe/maybe” by reviewers were advanced to full-text review.

Full-text articles were obtained, screened, and independently reviewed (by R.N. and E.M.B.) for inclusion, and any disagreements were resolved through discussion and consensus. Articles were excluded if they were abstracts without peer-reviewed full-text articles, were modeling studies, were protocols or study design papers, focused on cancer management outcomes only, and focused on cognitive outcomes only (eg, knowledge, intention) with no change in action or behavior (eg, complete GC, complete GT). After full-text data abstraction, additional articles were excluded from analysis because they lacked intervention-specific outcomes, described interventions not aimed at improving a care delivery process, or reported studies performed outside of the United States or US studies that focused only on cascade GT (ie, GT in families with identified hereditary cancer predisposition) outcomes. The PRISMA flow diagram (Figure 1) outlines the exclusion criteria applied during each step of evidence selection process.

Figure 1.

Study inclusion and exclusion.

Data charting process

Full-text articles meeting inclusion criteria were used for data collection. Reviewers, R.N. and E.M.B., independently abstracted data from all included articles using a Research Electronic Data Capture database with discrete fields for data items.¹⁶ Discrepancies in data collection were resolved through an additional review of the full-text article, discussion, and consensus. The Research Electronic Data Capture database was designed to collect information on the following variables: study demographics (country and setting where study was performed, year of publication, and fund type); study design, including presence or absence of a comparison group; clinical process targeted for improvement; intervention description (who implemented the intervention and where, who received the intervention [patients or health care providers], duration of the intervention); and intervention outcome metrics and statistical results.

Critical appraisal of individual sources of evidence

Study design, fund source, presence/absence of a comparison group, similarity of comparison group to intervention group, and alignment of reported outcomes with study objectives/intervention were collected during full-text review to assess for potential study design flaws or biases.

Synthesis of results

Articles included for analysis were grouped by the process of genetics service delivery the intervention focused on improving. Articles that aimed to improve >1 process were defined as having multiple targets and were included in the analysis for each of the included individual processes. Study interventions were categorized as simple or complex in which simple interventions were described by studies as a single intervention activity or approach focused on a single process and/or single recipient (eg, patients or provider) and complex interventions had multiple components or intervention activities affecting >1 recipient and/or multiple processes. Each article’s interventions were described, including how (who, when, where) they were delivered and their reported outcomes, informed by the Genetic Counseling Interventions in Research and Other Studies and Template for Intervention Description and Replication standards.^17,18

Results

Selection of sources of evidence

A total of 1989 citations met initial search criteria after removal of duplicates. Our independent review of all titles and abstracts resulted in the exclusion of 1785 articles and inclusion of 204 for full-text review. Of the 204 full-text articles, 114 were excluded upon review, resulting in 90 full-text articles for data collection. Studies excluded from analysis included 41 (45.5%) that were performed outside the United States, 2 that were focused only on cascade GT, and 3 that were excluded because they had no reported intervention outcomes or interventions not specifically designed to change clinic processes. A total of 44 articles were included in the analysis. The PRISMA flow diagram (Figure 1) shows the entire review process from the original search to the final selection of studies.

Characteristics of sources of evidence

As shown in Table 1, most included articles were published recently, between 2016 and 2020, and more than half (24, 54.5%) were implemented in academic medical center settings. In total, 33 articles (75.0%) were categorized as having implemented simple interventions. The greatest number of articles (n = 17) targeted the process of increasing identification of eligible patients, which included studies that implemented universal tumor testing as the primary intervention. In addition, 14 articles targeted referral of patients to genetics services, 15 targeted delivery of GC, and 16 focused on increasing rates of GT completion. A total of 12 articles targeted >1 process; of these, 7 were categorized as complex interventions. Of the 12 articles targeting >1 process, 4 targeted the processes of referral, GC, and GT^20,25,36,49; 2 targeted both GC and GT processes^31,35; 1 targeted identification and referral processes⁴²; 1 targeted identification and GC⁴³; 1 targeted identification and GT⁴⁴; 1 targeted referral and GC⁶²; 1 targeted referral and GT³⁸; and 1 targeted all 4 clinic processes.⁵⁴ GC intervention domains, including risk content and communication, educational content, and/or psychotherapeutic content were included within the interventions of 33 articles (75.0%).¹⁷

Table 1.

Study characteristics

Included Article Characteristics (N = 44)	n	%	References
Intervention location type
Academic medical center(s)	24	54.5	19–42
Community clinic(s)	6	13.6	43–48
Health system clinic(s)	5	11.4	49–53
Public health/safety-net clinic(s)	2	4.5	54,55
More than one type of location	3	6.8	56–58
Not clinic based	4	9.1	59–62
Year of publication
2000–2005	5	11.4	27,31,41,51,56
2006–2010	6	13.6	28,33,59–62
2011–2015	11	25.0	19,21,24,26,32,34,39,45,52,53,57
2016–2020	22	50.0	20,22,23,25,29,30,35–38,40,42–44,46–50,54,55,58
Study funding source
Governmental agency	12	27.3	19,26–28,31,32,40,45,46,50,52,61
Other funding (eg, foundation, institutional)	4	9.1	30,37,60,62
For-profit organization/company	2	4.5	25,44
More than one type of funding	15	34.1	20–22,24,34,35,41,42,48,51,53–55,57,58
No funding	11	25.0	23,29,33,36,38,39,43,47,49,56,59
Study design
Cohort study	33	75	19,20,22–26,29,30,32,36–39,41–49,51–56,59–62
Randomized controlled trial	11	25	21,27,28,31,33–35,40,50,57,58
Comparison or control group
Present	30	68.2	19,21,22,24,26–29,31–38,40,41,43–45,47,48,50,51,54,56–59
Absent	14	31.8	20,23,25,30,39,42,46,49,52,53,55,60–62
Study interventions’ use of GC intervention domains
Risk content and communication included	9	20.5	27,30,42–44,46,48,52,55
Educational content includeda	22	50.0	20,24,27,31,37,38,40–42,44,46–49,51,52,54,56,59–62
Psychotherapeutic content includedb	15	34.1	20,21,25,28,31,34–36,41,43,44,49,54,57,58

GC, genetic counseling.

^aIncludes education interventions targeting providers and patients.

^bIncludes studies that had GC as a component of the intervention. Although GC typically includes risk communication and education, if not explicitly included as a discrete components of study interventions, GC was not counted in the risk and educational domains.

Critical appraisal within sources of evidence

As reported in Table 1, 33 of the 44 articles (75%) used cohort designs (retrospective and prospective) and 11 (25%) were randomized controlled trials. A total of 14 articles (31.8%) did not include or report a comparison or control group, and of the 30 articles that included a comparison or control group, 14 had relevant limitations. These limitations included groups with noted differences in demographic factors or other characteristics, no reported analysis to assess the similarities and differences between groups, or groups with different recruitment timing or recruitment sources. Funding source can be relevant when assessing for possible bias within a study, and 2 articles^25,44 reported funding solely from commercial GT laboratories and 1⁴⁸ had multiple funding sources that included a commercial GT laboratory.

Results of individual sources of evidence

The steps in the clinical delivery of genetics services and the potential factors influencing each step are highlighted in Figure 2.

Figure 2. Process and factors impacting delivery of genetics services.

White circles, policy factors; Gray circles, clinic factors/decisions; Black circles, Patient factors/decisions. GC, genetic counseling; HCP, health care provider.

Interventions to improve identification of patients eligible for genetics services

A total of 17 articles implemented interventions to improve the identification of patients eligible to receive genetics services.^{19,22–24,26,39,42–46,48,52,54,55,59,60} As outlined in Supplemental Table 3.1, 11 articles’ interventions were classified as simple and 6 as complex. Interventions used to improve identification of eligible patients included application of universal tumor testing, mass-media marketing of BRCA GT to promote self-identification, screening of clinic schedules to identify eligible patients on the basis of their cancer diagnosis, and collection and/or assessment of patients’ personal and family history using various tools (eg, National Cancer Institute Community Cancer Centers Program genetics assessment tool, MeTree tool, NCCN criteria, PREMM_1,2,6 tool, Breast Cancer Genetics Referral Screening tool, family history questionnaires). Several interventions that implemented tools to collect personal and family history information included risk assessment and either a triaging process^55,55 and/or patient education^{42,43,48,52,60} to promote awareness and action after identification.

Statistically significant improvement in patient identification was reported by 3 articles. Of these, 2 were quality improvement efforts^24,54 whose interventions targeted implementation of universal tumor testing and the other study⁴⁵ applied the National Cancer Institute Community Cancer Centers Program genetics assessment tool and reported that the initiative resulted in significantly increased identification of patients with ovarian cancer. The remaining articles either found no significant difference in rates of patient identification after the intervention^39,59 or reported no statistical comparison.

Interventions to improve referral to genetics services

As listed in Supplemental Table 3.2, 14 articles sought to improve the referral of eligible patients to genetics services, with 8 articles’ interventions categorized as simple and 6 articles’ interventions as complex.^{20,25,29,32,36–38,42,49–51,53,54,62} Interventions implemented to improve referral of eligible patients included indirect approaches of mass-media marketing, patient information and education, staffing changes such as hiring genetic counselors and positioning genetic counselors within oncology clinics, and increased documentation of family history. Direct interventions involving the referral process included implementation of physician reminders to make patient referrals, universal referral for patients as part of clinical process change or study protocol, and using electronic medical record (EMR) systems to generate referral orders and facilitate the referral process.

Statistically significant improvement in rates of patient referral were noted by 8 articles. Among interventions that indirectly targeted referral processes, a mass-media marketing campaign for GT resulted in a significant increase in patient referrals to genetics in the city receiving the campaign (increase of 240%, P < .001), compared with a health system in a city without the campaign (no significant increase, P = .94).⁵¹ The authors described the mass-media marketing campaign as a commercial laboratory produced direct-to-consumer advertising campaign for GT of BRCA1 and BRCA2 that targeted women aged 25 to 54 years and was disseminated via television, radio, and print media for 5 months during 2002–2003.⁵¹ One study reported that hiring a genetic counselor to support the clinic resulted in an increase in referrals to genetics from 80% to 96% (P < .0001).²⁹ Similarly, embedding a genetic counselor in a gynecologic oncology clinic increased referrals from 21% to 44% (P < .0001).³⁶ Another study implemented a complex intervention including provider educational efforts, patient navigator clinic screening, and hiring of genetic counselors and found significant improvements in the rates of referrals for patients with ovarian, triple-negative breast, and early-onset breast cancers (P < .05).⁴⁹

Among the direct interventions involving the referral process, an EMR referral form that automatically forwarded to the cancer genetics clinic resulted in an increase in referrals from 17% to 30%, with the intervention identified as a significant predictor of patient referral (P = .009).³² A quality improvement initiative that leveraged the EMR through developing a smart phrase for genetics and included provider education efforts yielded a 98% rate of referral compared with preinitiative rates of 46% (P < .001).³⁸ Among complex interventions, 1 quality improvement initiative that included standardized timing of referral to genetics (surgery discharge) for all patients with ovarian cancer and provider education saw an increase in referrals from 48.1% to 74.2% (P = .002).³⁷ A second complex quality improvement effort that included integrating a genetic counselor in clinic in addition to referral reminders to physicians increased referrals to genetics for patients with ovarian cancer (P = .02).⁵⁴ The reports of complex interventions did not specify which interventions within the initiatives had the greatest impact on the increased referrals. The remaining articles either found no significant difference in rates of patient identification after the intervention or reported no statistical comparison.

Interventions to improve delivery of GC

Included in Supplemental Table 3.3 are 15 articles that sought to improve the delivery of GC to patients, including 10 study interventions categorized as simple and 5 categorized as complex.^{20,25,27,30,31,33–36,40,41,43,49,54,62} Interventions to improve the delivery of GC included indirect approaches, such as referral and educational materials shared with patients and/or their primary care providers^30,31,62 and the use of an application to improve patients’ attitudes about GC.⁴⁰ Interventions that directly targeted the delivery of GC included changes to service delivery models (ie, GC performed in-person vs over telephone, embedding/integrating genetic counselors within oncology clinics, and use of genetic counselor extenders), facilitated scheduling of GC appointments, and previsit education to increase the efficiency of GC.

Statistically significant improvement in patient uptake and efficiency of GC were reported by 5 articles. Among interventions focused on service delivery model changes, embedding a genetic counselor in a gynecologic oncology clinic resulted in an increase in patients scheduled for GC from 38% to 84% (P < .00001) and a decrease in time between referral and completion of GC from 2.52 months to 1.67 months (P < .01).³⁶ Interventions to facilitate the scheduling of GC visits included implementation of a navigator to facilitate coordination of GC appointments, resulting in a decrease in time between patient referral and GC appointment (P = .002).³³ Similarly, an intervention to proactively call referred patients to assist in coordination of a GC appointment resulted in an increase from 54.6% to 83.8% in patient completion of GC (P < .0001) and an increase in the timeliness of the GC appointments related to surgery planning (P = .001).³⁵ Interventions that aimed to increase the efficiency of GC included an intervention to supplement GC using a computer-based education and decision-aid tool for patients, which saw a decrease in the time spent in the GC session from 90 minutes to 82 minutes (P = .03), with a greater reduction in time spent with patients who were at low risk of hereditary cancer predisposition.²⁷ A similar approach, which included a previsit educational compact disc read-only memory and knowledge questionnaire for patients, resulted in a decrease in time spent by patients in the GC visit overall (P < .05), including time with the genetic counselor (P = .01) and the attending medical oncologist (P < .05).⁴¹ The remaining studies reported no statistically significant improvement in GC outcomes after the intervention^31,40 or reported no statistical comparison.

Interventions to improve completion of GT

Supplemental Table 3.4 includes the 16 articles that sought to improve the completion of GT among eligible patients, including 10 study interventions categorized as simple and 6 categorized as complex.^{20,21,25,28,31,35,36,38,44,47,49,54,56–58,61} Only 1 complex quality improvement initiative included an intervention that directly targeted the GT coordination and completion process, which was done by altering the health care provider involved in the test coordination process (physician-coordinated testing).²⁰ A second article offered GT at no cost but did not intervene in the process of testing coordination.³¹ The remaining 14 articles implemented interventions that indirectly targeted the GT coordination and completion process. Indirect interventions included a mass-media marketing campaign about BRCA GT, patient and provider education, interventions to facilitate the scheduling and coordination of GC, culturally adapted GC sessions, and GC service delivery interventions (eg, in-person vs telephone, embedding/integrating genetic counselors within oncology clinics).

Statistically significant differences in GT rates were noted by 9 articles. A study evaluating the impact of a mass-media marketing campaign for GT found that providers in cities receiving the campaign reported an increase in patients requesting testing and ordered more tests compared with providers in noncampaign cities (P < .05).⁵⁶ Articles focusing on genetic counseling–related interventions included one that implemented telephone GC and found higher GT rates in the usual-care (in-person) GC arm than in the intervention (P = .04 intention to treat, P = .03 per protocol).²¹ Similar findings were reported by 2 articles that also implemented a telephone GC intervention, in which rates of GT were higher in the usual-care (in-person) counseling arms.^57,58 In addition, an intervention to proactively call referred patients to assist in coordination of a GC appointment found that patients who completed usual-care GC coordination had higher rates of GT uptake (89.8%) than those receiving the intervention (64.5%) (P = .0002).³⁵ In contrast, a GC-focused intervention replaced pretest GC with an educational video and the option of GT, which resulted in testing rates of 55% compared with 29% among patients meeting with a genetic counselor before coordination of GT (P < .001).⁴⁷

Among complex interventions, 1 article that included integration of a genetic counselor in the clinic, screening of clinic schedules, educational efforts, and referral reminders found an increase in the completion of GT for patients diagnosed with ovarian cancer during the intervention period (P = .03).⁵⁴ A second complex intervention that included hiring a genetic counselor, screening of clinic schedules, and the option of in-person and telephone GC yielded a significant increase in the proportion of patients completing GT, including those with ovarian cancer (P < .05), triple-negative breast cancer (P < .05), and early-onset breast cancer (P < .05).⁴⁹ A third study implemented educational efforts, an EMR smart phrase, coordination of genetics and oncology appointments, and documentation during tumor boards and noted an increase in the rate of GT from 27% to 82% (P < .001).³⁸ As with the interventions to improve referral, reports of complex interventions did not specify which interventions within the initiatives had the greatest impact on the increased GT. The remaining studies reported no statistically significant improvement in GT outcomes after the intervention^31,36 or reported no statistical comparison.

Synthesis of results

The highest number of articles (n = 17) targeted identification of eligible patients; however, this process intervention category also had the lowest proportion of studies reporting statistically significant improvement (n = 3, 17.6%) and the greatest proportion of studies without statistical analysis comparing the intervention to a nonintervention group (n = 12, 70.6%). Interventions to identify eligible patients were primarily focused on medical and family history screening, risk assessment tools, and implementation of universal tumor testing. Interventions to improve rates of referral had a higher rate of statistically significant improvement (8 of 14, 57%), with reported success using EMR interventions and standardized referral processes. Interventions that directly targeted GC delivery (n = 15) included 5 (33.3%) with statistically significant improvement, including interventions focused on the efficiency of GC, facilitation of GC scheduling, and increased access through embedding a genetic counselor in the oncology clinic. Finally, interventions to improve the rates of GT completion almost entirely (15 of 16, 93.8%) targeted non-GT clinical processes and included interventions that indirectly influenced rates of testing. This process intervention category notably included 4 articles showing that the intervention group had significantly lower rates of testing than those receiving usual care—primarily in studies of telegenetics/telephone GC interventions.

Discussion

This scoping review identified 44 articles of US-based clinical interventions that sought to improve access and patient receipt of guideline-recommended genetics services, with 17 targeting identification of eligible patients, 14 targeting referral of eligible patients to genetics services, 15 focused on delivery of GC, and 16 aiming to increase completion of GT. Overall, clinical interventions to increase identification of eligible patients primarily included universal tumor testing processes and systematic screening of patient medical and family histories using data collection and risk-assessment tools. Interventions to improve referral rates of eligible patients included EMR adaptations, standardizing referral processes for specific patient populations, and implementing referral notifications and reminders for providers. GC delivery interventions provided supplemental patient education to increase visit efficiency, integrated or embedded genetic counselors within relevant specialty oncology clinics, coordinated and facilitated the GC appointment scheduling process, and used alternative service delivery models such as telegenetics. Few studies implemented interventions that directly affected the process of GT coordination, but potentially useful indirect interventions included efforts to increase awareness and knowledge of GT among patients and providers and interventions that support the GT coordination process by the relevant ordering provider (the genetic counselor, in most included studies). Overall, this scoping review has identified and described the current evidence and may serve as a toolkit of intervention strategies for clinicians seeking ideas for interventions to target their particular clinical barriers and for researchers seeking opportunities for future studies of intervention adaptation, implementation, and evaluation.

Similar to the findings in the systematic review by O’Shea et al,¹³ many articles in this study did not include comparison groups or statistical analysis of their outcomes, warranting future research and further evaluation of intervention impact and effectiveness. A statement on the most effective interventions for each clinical process was not feasible due to the large proportion of included articles without a comparison group or without statistical comparison of outcome data. In addition, articles that reported statistically significant improvement after the application of an intervention, upon replication or dissemination, may have different outcomes due to variations in the implementation processes and/or setting in which the intervention(s) are used. Many of the articles included in this review were studies performed in academic medical centers, with only 8 focused on community, public health, safety-net, or federally qualified health center clinics, which may decrease the generalizability of the reported interventions’ effectiveness across settings. Furthermore, only the study by Halbert et al²⁸ included a culturally tailored intervention, and only the study by Brown et al⁴⁹ specifically focused on a large geographic area and referenced interventions for rural clinics. Adaptation and evaluation of interventions in diverse health care settings, guided by the needs of unique communities served, are needed to ensure that improvements in patient access to genetics services are achieved. Another relevant limitation to the interpretation of intervention effectiveness is that many included articles were research studies, as opposed to quality improvement or other clinical process interventions, and informed consent is required from patients before participation or data collection. The initial requirement of obtaining informed consent from patients may decrease the generalizability of intervention findings, particularly when there are limited data to describe the patients who declined to participate or were unable to provide consent.

A notable limitation identified during this scoping review was that several articles had aims and objectives that did not directly align with the clinical process in which they intervened. One example is the study by Kishan et al,²⁹ in which the intervention was described as collection and documentation of family history information and hiring of a genetic counselor, with the hypothesis that these interventions would result in “increased rates of appropriate referral.” Similarly, the study by Niendorf et al⁴² sought to increase both identification and referral of patients for cancer genetics; however, the intervention focused primarily on patient identification and relied on patients to take action to change rates of referral. Another example was the study by Drescher et al,⁵⁰ which sought to increase rates of GT by implementing an intervention to increase patient identification and referrals. The described interventions did not account for what happens between the steps in the clinical process and thus did not account for clinical processes or factors that may intervene or influence referral, GC, and GT, making interpretation of the effectiveness of the interventions difficult.

Another common finding was that many studies intervened in the process of GC but used the rates of GT as the measure of success, and studies that focused on the process of GT intervened at the level of GC delivery. GC is defined as “the process of helping people understand and adapt to the medical, psychological and familial implications of genetic contributions to disease,” and includes “interpretation of family and medical history…education…and counseling to promote informed choices and adaptation to the risk or condition.”⁶³ Notably, this definition does not include coordination of GT or ensuring that patients complete GT. In addition to genetic counselors, physicians, advanced practice providers, and other members of the health care team are qualified to coordinate diagnostic medical tests, such as GT for patients, as leveraged by interventions to implement universal tumor testing, use GC extenders, and incorporate physician-coordinated testing as identified in this study. Genetic counselors provide a specialized service to patients during the GT process; however, the 2 processes are not inherently equivalent from a process improvement or intervention perspective.

A total of 3 articles (Bowen et al,⁵⁹ Mouchawar et al,⁵¹ and the Centers for Disease Control and Prevention [CDC]⁵⁶) assessed the effects of a direct-to consumer mass-media campaign implemented by a commercial GT laboratory; however, each individual study focused on different processes (patient identification, increasing referral, and GT) and different subpopulations exposed to the intervention (survey of general public, health system referrals, health care provider survey). These included articles, if combined, evaluate the effects of a single intervention across multiple clinical processes; however, they are included as individual articles in this analysis. There are included articles by Kinney et al^57,58 and Schwartz et al,^34,35 which report on similar studies; however, differences were noted in the intervention components and/or methods and thus were not excluded as duplicate articles. In addition, the data presented in this review are limited by our search and screening strategies, which may have inadvertently excluded relevant articles.

Future studies of interventions to improve patient receipt of recommended genetics services should aim to include clear and standardized descriptions of their intervention and implementation processes by applying frameworks such as the Genetic Counseling Interventions in Research and Other Studies¹⁷ and Template for Intervention Description and Replication¹⁸ standards, which will allow improved comparisons across studies and facilitate the replication and dissemination of successful interventions. Intervention mapping techniques, such as logic models, may support the development of future interventions and ensure that the process and outcome of interest are linked by evidence-based assumptions to the intervention activities. In addition, many studies sought to improve rates of GT without direct intervention to the GT process. Future efforts that seek to increase patients’ completion of GT may consider interventions to enhance and improve the rates of informed decision-making for GT, develop pathways that increase the efficiency of accessing testing after an informed choice to proceed, and identify interventions that streamline the laboratory testing processes—including health insurance and billing considerations, which could impede a patient’s ability to complete desired testing. In addition, future studies may consider evaluation of patients’ perception of testing as a choice to ensure that the guideline-compliant care offered is also patient centered and tailored to the needs of the patient and their family. Informed patients may reasonably elect to defer or decline GT; therefore, measures of a patient’s decision about GT—and that decision’s alignment with their understanding, values, preferences, and perceived utility of testing results—are critical to increasing patient-centeredness and identifying and addressing any gaps in the delivery of care.

The results of this scoping review of the peer-reviewed literature identified and described clinical interventions developed to improve patient access to, and receipt of, guideline-recommended cancer genetics services in the United States. Identified interventions were categorized by their clinical process target (identification, referral, GC, and GT). Future studies of intervention development and evaluation are encouraged to replicate interventions in different settings, particularly nonacademic settings, to increase understanding of interventions’ impact on diverse clinical and patient populations; include comparison groups to better evaluate the impact and effect of interventions; and apply intervention reporting standards when developing and describing interventions to increase the ability to compare outcomes across studies seeking to replicate successful interventions in different settings.

Supplementary Material

Additional Information

The online version of this article (https://doi.org/10.1016/j.gim.2022.03.002) contains supplementary material, which is available to authorized users.