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Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer
YGYNO-977096; No. of pages: 5; 4C: Gynecologic Oncology xxx (2018) xxx–xxx
Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer☆ Denise Uyar a,⁎, Jamie Neary a, Amy Monroe b, Melodee Nugent c, Pippa Simpson c, Jennifer L. Geurts d a
Department of Obstetrics and Gynecology, Medical College of Wisconsin, Milwaukee, WI, United States Clinical Cancer Center, Froedtert & The Medical College of Wisconsin, Milwaukee, WI, United States Department of Pediatrics, Section of Quantitative Health Sciences, Medical College of Wisconsin, United States d Department of Surgery, Medical College of Wisconsin, United States b c
H I G H L I G H T S • • • •
Improvement needed in efforts for universal testing in gynecology oncology. Implementation of simple measures can have large impact on achieving this goal. Education of providers is an effective way of impacting universal testing rates. Patients who see genetic counselors have a high rate of testing completion.
a r t i c l e
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Article history: Received 14 December 2017 Received in revised form 21 March 2018 Accepted 25 March 2018 Available online xxxx Keywords: Ovarian cancer Universal genetic testing Gynecologic oncology Quality improvement
a b s t r a c t Objective. The National Comprehensive Cancer Network recommends all women with ovarian cancer be offered genetic testing. Despite a decade of endorsement, many oncology practitioners have yet to make this a part of routine practice. Referral to genetic counseling and completion of genetic testing among patients at substantial risk of germline mutations are significantly lacking, adversely affecting patient care and squandering an opportunity to maximize cancer prevention efforts. This project determined the impact and feasibility of implementing a basic model for universal referral to genetic counseling and completion of genetic testing in women with a diagnosis of ovarian cancer in an academic gynecology oncology practice with access to electronic health records (EHRs). Methods. Patients diagnosed with ovarian cancer from January 2008 to November 2013 were retrospectively reviewed to determine the baseline referral rate for genetic counseling and testing completion in our practice. Implementation of a process change model combining provider training, patient education, enhanced electronic health record documentation and improved patient appointment scheduling strategies were implemented. We then prospectively collected data on all newly diagnosed ovarian cancer patients that had not already undergone genetic testing presenting from December 1, 2013 to November 30, 2016. Results. Genetic referral rates, genetic counseling and testing completion rates were markedly improved. Pre-implementation our genetic testing rate was 27% and post implementation our testing rate was 82% (p-value ≤ 0.001). Conclusions. Low cost interventions that target education of both providers and patients regarding the importance of genetic testing along with utilization of the EHR and streamlined patient appointment services can significantly increase rates of genetic testing completion. © 2018 Elsevier Inc. All rights reserved.
1. Background Epithelial ovarian cancer (EOC), inclusive of fallopian tube and primary peritoneal cancers, are the leading cause of mortality from ☆ No conflicts of interest or financial disclosures. ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Medical College of Wisconsin, 9200 Wisconsin Avenue, Milwaukee, WI 53226, United States. E-mail address: [email protected] (D. Uyar).
gynecologic cancers. Approximately 10–20% of high grade ovarian, fallopian tube and peritoneal cancers are hereditary [1]. Recognition of hereditary cancer syndromes serves an increasingly important role in the care of women with gynecologic cancers. Previously, testing for hereditary cancer syndromes was reserved for select patients with an extensive personal or family history of cancer. However, over 50% of individuals with a BRCA1 or BRCA2 gene mutations do not have a personal or family history that would fulfill clinical criteria for testing [2]. Strict adherence to family history as the main criteria for testing omits
https://doi.org/10.1016/j.ygyno.2018.03.059 0090-8258/© 2018 Elsevier Inc. All rights reserved.
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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tubal and peritoneal cancers. Review of the guidelines ensured that all providers would be able to initiate the discussion and the counseling for patients with applicable diagnoses. Creation of an electronic “smart phrase” (a quickly accessible standardized text) for use in the electronic health record (EHR). This “smart phrase” when added to a clinical encounter efficiently documented that the rationale behind genetic testing was reviewed and that the genetic counseling recommendation was made. Providers were educated on the use of this standard text to efficiently document in the EHR. The “smart phrase” essentially standardized and simplified documentation. Patient education regarding the role of genetic testing at the time of their diagnosis began as early as their initial consultation visit. An electronic “smart phrase” was also created for patient instructions. This text included the explanation of the rationale and benefits of seeking genetic counseling and testing in lay language. This text was added to all patient instructions in the EHR. These instructions were printed and given to patient at conclusion of their appointment with the after-visit summary, creating an efficient means of providing patient education. Scheduling of the genetic counseling appointment at the time of patient check out (point of care) from the gynecology oncology clinic was initiated to avoid delay in scheduling appointments and facilitate a more patient centered experience. Tumor Board conference documentation was updated as well to include whether genetic counseling was recommended, pending or completed as a part of all treatment recommendations for ovarian cancer patients. Tumor Board notes were made more comprehensive by including the recommendation for genetic testing in the final recommendations for applicable patients and were part of the patient's EHR. Genetic counselors also regularly attend and participate in our Tumor Board conferences.
a significant proportion of at risk women from obtaining testing. In 2005 the United States Preventative Task Force opened the scope of eligibility and began to more formally recommend that genetic counseling and testing be offered to all at risk individuals [3]. Shortly after that, the National Comprehensive Cancer Network (NCCN) updated their guidelines in 2007 and recommended that all women with ovarian cancer and their immediate family members be offered genetic counseling and testing regardless of age at diagnosis or family history of cancer [4]. Similarly, other societies have endorsed this recommendation such as the American College of Obstetrics and Gynecology [5], American Society of Clinical Oncology and the American College of Medical Genetics [6,7]. Recently, the Society of Gynecologic Oncology issued a position statement emphasizing the importance of genetic testing for women affected by gynecologic cancers [8]. Germline mutations in BRCA1 and BRCA2 are reported to occur in 15–20% of ovarian cancer patients and are known to increase the lifetime risk of ovarian cancer by 20–50% and breast cancer by 50–80% [9,10]. Additional genes have been associated with homologous recombination and hereditary ovarian carcinoma including RAD51C, RAD51D, BRIP1, PALB2, as well as mismatch repair genes (MLH1, MSH2, MSH6, PMS2) which are believed to contribute an additional 2–4% of ovarian cancers [10–12]. BARD1 may be a rare ovarian cancer susceptibility gene but more study is needed to define its absolute risk [10]. The potential benefits of identifying patients with genetic mutations continues to expand and includes offering risk reducing prophylactic measures, enhanced surveillance, individualization of prognosis for patients, potential utilization of targeted therapy, and increasingly inclusion in clinical trials. Despite these benefits, national and international studies have consistently shown low utilization of genetic counseling and genetic testing completion among ovarian cancer patients [13–21]. A recent study by Childers et al. found that only 1 in 5 women in the United States with history of breast or ovarian cancer meeting NCCN guidelines have undergone genetic testing [17]. Oncologists are a critical part of identifying, educating and referring eligible patients for genetic counseling. Identifying efficient strategies to incorporate this philosophy into practice, promote the referral to genetic counselors and strategies to enable oncologists to take a more active role in assisting the completion of genetic testing are needed. We compared historical rates of referrals to genetic counseling and completion rates of genetic testing for patients with ovarian cancer in our practice to rates of genetic counseling referrals and genetic testing completion post-implementation of the process change model. The goal of the project was to establish an efficient process for universal genetic testing for ovarian cancer patients in our practice.
The rates of completion of genetic counseling and genetic testing before and after the implementation measures were compiled and compared. For independent group comparisons, a non-parametric two-sided Fisher's exact test was used for the categorical variables and the Mann-Whitney test was used to compare continuous variables. Continuous variables are summarized as median (range). Unadjusted p-values b 0.05 were considered significant. SPSS version 24 (IBM Software, Chicago, IL, USA) was used to analyze the data.
2. Methods
4. Results
All patients ≥18 years presenting to a single gynecologic oncology practice at an academic cancer center with a new diagnosis of nonmucinous epithelial ovarian, fallopian tube or primary peritoneal cancers from January 1, 2008 to November 30, 2016 were included in the data determining our baseline genetic referral and genetic testing completion rates. Patients with previous germline gene testing were excluded. Patients were divided into two cohorts based on when they presented: patients who presented prior to quality improvement measures to establish the baseline (Jan 2008–November 2013) and patients who presented after the implementation of quality improvement measures (December 2013–November 2016). Our model aimed at establishing a uniform practice norm for universal genetic counseling and testing in our clinic and included implementation of the following measures:
Data was collected entirely from the EHR which captures the patient's diagnosis, documentation of genetic counseling in the chart, whether a referral to genetics was placed, scheduling of appointment with genetics, completion of genetic counseling, completion of genetic testing and results of genetic testing. There are 2 cohorts; a retrospective portion (January 2008–November 2013) and a prospective portion (December 2013–November 2016). There was no statistical difference in patient age (years); 60 (26–88) vs 64 (22–85) (p = 0.26). In the retrospective portion of the study, 207 patients met inclusion criteria. Forty-two (20%) patients received documented education by their provider at the time of diagnosis regarding referral to a genetic counselor for genetic testing. Ninety-six (46%) patients had a referral order to genetic counseling placed by their provider at the time of initial diagnosis. Of the 207 patients, 67 (32%) were seen by a genetic counselor. Of those 67 patients counseled and seen by a genetic counselor, 55 (82%) patients underwent genetic testing. In summary, of the 207 patients eligible for genetic testing from January 2008–November 2013, only 27% (55 of 207 patients) completed genetic testing. As anticipated, our baseline referral rate and testing completion rate were poor, similar to national
• All gynecologic oncology providers in our practice received a review of the rationale behind universal genetic testing and the current NCCN and Society of Gynecologic Oncology guidelines recommending genetic testing for all women with non-mucinous epithelial ovarian,
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3. Statistical analysis
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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rates. Notable however, is the finding that of the 67 total patients seen by genetics for counseling, the majority completed genetic testing (82%, 55 of 67 patients). The process change model for universal genetic testing as detailed above was then instituted on December 1, 2013 in our practice. All providers and all new patients with non-mucinous EOC in our gynecologic oncology clinic were included in the implementation of the model. Implementation of the initiatives was phased in over approximately 3 months. One hundred and sixty-two patients with newly diagnosed ovarian cancer in our clinic were initially identified for inclusion in the prospective portion of the study from December 2013–November 2016. Thirtyseven patients were excluded since they had already undergone genetic testing, leaving 125 patients in the final analysis. After the measures were implemented, the rate of documented recommendation in the EHR for genetic counseling, rate of referral to genetics, rate of completion of genetic counseling and rate of completion of genetic testing were calculated and there were significant differences from pre- to post-implementation (Table 1). One hundred and ten patients (88%) had appropriate documentation of the genetics recommendation in the EHR and 122 patients (98%) had a genetics referral placed. One hundred and eight of the 125 patients (86%) underwent genetic counseling and 103 of 108 patients (95%) ultimately completed genetic testing. Thus, after the implementation of these measures, 103 of 125 eligible patients (82%) completed genetic testing improved from 27% in the previous cohort. The number of patients with a gene mutation detection in this group was 22 (22%) which was not statistically different from the pre-implementation detection rate of 18% (10 of 55 patients). Overall, the genetic testing completion rate increased from 27% (55 of 207 patients) to 82% (103 of 125 patients) (p-value ≤ 0.001). Per anecdotal reports from providers, the incorporation of smart phrases into their work flow was not time intensive and was an acceptable process change. Enhancing EHR alone and combined with other strategies to increase provider referral for genetic testing has been successful in other studies as well [18,19]. Incorporating a more efficient method of scheduling patient appointments was instrumental was also instituted and was helpful in optimizing scheduling for patients. Scheduling genetic counseling consults had previously been performed by the genetics clinic but we eliminated that step and had our gynecology oncology schedulers assume the responsibility for directly scheduling appointments. This more patient focused approach allowed patients to schedule their own genetics appointment in the gynecology oncology clinic at the time of check out rather than waiting for a phone call from the genetics clinic. Per informal questioning of patients, streamlining the process required to make appointments was an important factor for them. Having the patient education printed out for them at the time of checkout also helped reinforce the significance of the recommendation at the time of check out when the referral appointment was being made. 5. Discussion Standard of care guidelines dictate that all women with ovarian cancer receive genetic counseling and genetic testing. Several societies and
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institutions have reached consensus regarding the recommendation for universal genetic testing and yet referrals to genetics and completion of genetic testing for this high-risk population remain suboptimal. Every year that does not see these guidelines executed represents missed opportunities for the thousands of women diagnosed with gynecologic cancers and their at-risk family members. Several barriers to the uptake of genetic counseling and completion of genetic testing have been noted. These barriers include lack of familiarity with guidelines on the part of the clinician, lack of time on the part of providers, lack of access to genetic counselors, lack of understanding by patients regarding the importance of genetics/genetic testing which may contribute to fears of testing, and in some cases patient cost and convenience [22]. Oncology providers are charged with incorporating discussions regarding the importance and rationale behind the recommendation for genetic counseling and genetic testing to patients that meet criteria for testing. For universal testing to become a reality it is essential that providers are able to identify appropriate patients, understand the impact that genetic testing has on their treatment and their prognosis and feel comfortable initiating these discussions. Research has shown that the physician's recommendation is one of the strongest factors influencing a patient's decision to meet with a genetic counselor [23]. Beginning our initiative with education for providers on the guidelines for risk assessment addressed the barrier of provider education. This first step was necessary for reinforcing the current guidelines for all providers and the importance of genetic testing for high risk populations. In both academic and non-academic practices, the EHR is well established and may represent an underutilized resource for assisting practice change in many different ways. Creation of electronic phrases to expedite documentation and enhance printed patient education were found to be very acceptable to our providers, required very little training and standardized the EHR. Part of a successful recommendation to genetics includes proper documentation in the medical record and our strategy represents one method of accomplishing this goal. Once properly recorded, it is simple for any provider to confirm genetic counseling and/or testing has been completed. It is notable that once patients met with genetic counselors the rate of testing was quite high: 55 of 67 (82%) patients who met genetic counselors prior to the quality improvements and 103 of 108 (95%) patients who met genetic counselors post intervention completed genetic testing. It has been shown previously that uptake of cancer risk management strategies, including genetic testing, are increased when patients are effectively counseled by a genetics provider [1] and our study supports this finding as well. Thus, a strong emphasis should be placed on the genetics referral to ensure a successful implementation of universal genetic testing. Given the increasing complexity of available genetic testing and interpretation of results, incorporating the expertise of genetic counselors as consultants continues to play an important role in patient care for our practice. Kentwell et al. and Senter et al. [24,25], found that embedding a genetic counselor within their clinic was most effective at improving their performance of completing genetic counseling and genetic testing. We do not have the ability to replicate this model in our clinic owing to the few genetic counselors in our facility, however the services are provided in the same building. The
Table 1 Patients with ovarian cancer eligible for genetic testing.
EHR documentation Referral placed to genetic counseling Genetic counseling completed Genetic testing completed/genetic counseling completed Patients with identified gene mutations a
Pre-implementation (N = 207) Jan 2008–Nov 2013
Post-implementation (N = 125) Dec 2013–Nov 2016
N Evala
N (%)
N Eval
N (%)
207 207 207 67 55
42 (20) 96 (46) 67 (32) 55 (82) 10 (18)
125 125 125 108 101
110 (88) 122 (98) 108 (86) 103 (95) 22 (22)
p-Value
≤0.001 ≤0.001 ≤0.001 0.007 0.68
N Eval = evaluable patients.
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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inability to embed a counselor in the clinic is likely to be an obstacle for other practices as well. We found we could still positively impact our performance of acceptance of genetic counseling and testing without having an embedded genetic counselor within our clinic. Timing of genetic counseling/testing for patients with EOC has also been studied but there is currently no standard guideline or recommendation. Novetsky et al. [23] found that women's views regarding the optimal time to be referred and undergo testing varied greatly but the study concluded that early discussion regarding referral was preferable. Fox et al. concluded that the majority of women (59%) with serous ovarian cancer prefer to have genetic counseling at the time of diagnosis [26]. We are proponents of beginning the discussion as early as possible. Earlier testing may be useful in discussions regarding prognosis, may contribute to efficient identification of patients for clinical trials, allows for more opportunity to counsel hesitant patients regarding additional cancer associated risks and, given the rapidly changing landscape of targeted therapy, such as poly-ribose ADP polymerase inhibitor (PARPi) treatment, earlier testing may be an advantage for determining eligibility for clinical trial participation or for initiating maintenance therapy in the near future. Tumor Board conferences, although a cornerstone in academic practices, may not be applicable to all types of oncology practices. This conference has been instrumental in our transition to universal testing as it is serves as another means of reinforcing genetics as an important resource that is assimilated into our multidisciplinary practice. All of our Tumor Board discussions now include documentation about whether genetic counseling has been recommended and completed; Tumor Board notes become part of the patient's EHR. This also serves as a document that can be shared with outside providers and formal inclusion of the recommendation for genetic counseling and testing in this format may also enhance compliance. Our genetic counselors attend the Tumor Board conferences and contribute to our patient discussions. Some have noted the presence of genetics providers at Tumor Board has been shown to increase the rate of referral and gene testing [27]. Others have found that despite having multidisciplinary conferences there are still patients who do not receive an appropriate cancer risk assessment [28]. We have found it to be useful in our practice to have genetic counselors present in multidisciplinary conferences. In addition, we have residents and fellows in attendance at these conferences and our discussions surrounding cancer risk assessment for high risk patients reinforces the significance of obtaining genetic counseling and testing, as well as obtaining a thorough family history for those in training. Our referral rate to genetics after implementation of this project was nearly 100% and yet we did not have 100% completion rate of genetic counseling or testing. We tracked the patients that did not ultimately see a genetic counselor or complete testing (missed opportunities) to determine if any pattern was apparent. The missed opportunities are detailed in Table 2. In total 18 patients over the course of the three years of this project did not complete genetic counseling or testing. Half (n = 9) of those patients did not complete the recommendation due transferring care (lost to our follow-up) or they passed away soon after diagnosis prior to being able to complete genetic counseling. In only one case did the patient site cost as the reason for her resistance, however after gratis funding for genetic services was obtained, the Table 2 Post-implementation missed opportunities. No. of patients Deceased Never scheduled appointment Cancelled appointment Genetic counseling appointment pending Declined testing after genetic counseling Transferred care Insurance denial
4 2 4 2 5 2 1
patient still declined. Patients that met with counselors and declined testing in our experience felt particularly overwhelmed and when asked stated they were not sure they wanted to know about additional cancer risks. These patients may reconsider this option in the future once the initial shock of the diagnosis is faded and time has elapsed. We have concluded that our increased genetic counseling and testing rates from 2013 to 2016 are attributable to the success of our described process change however, we also realize that a multitude of factors have likely influenced the completion of genetic testing during this time period. The decreasing cost of genetic testing [29] and the emerging role of targeted PARPi therapy for the treatment of relapsed platinum-sensitive EOC [30] are examples of factors potentially influencing rates of genetic testing in the last few years. The pivotal phase II study of PARPi in relapsed platinum-sensitive EOC demonstrating greater efficacy in patients with BRCA 1/2 mutations was published in 2012 [31], just prior to the roll out of our process change. In addition, high profile celebrity disclosures of gene mutation status have the capacity to influence genetic testing rates in unanticipated ways. In 2013 Angelina Jolie disclosed in the New York Times her BRCA1 status and urged women to undergo genetic testing, this remains one of the most viewed health related articles in the social media age [32,33]. Within months of the Angelina Jolie story another impactful event occurred, with a Supreme Court ruling that effectively invalidated the patents for the BRCA1 and BRCA2 genes. Immediately after this ruling, additional laboratories began offering testing, including BRCA1 and BRCA2 on multi-gene sequencing panels at a fraction of the previous cost for BRCA1 and BRCA2 only [34]. The national increased awareness along with enhanced access and reduced cost of testing may have played a role in our observation of increased uptake of genetic counseling and testing. Our process change, however, may have made it possible for our practice to efficiently evolve with this dynamic landscape. Although access to genetic services was not a barrier in our study as our institution has genetic counselors available 5 days per week, it is worthy to note that many health centers do not have local genetic counseling readily available [35–38]. In response to the increase in demand for access to genetic counselors, new services models have emerged including virtual visits, group sessions and telephone counseling [39]. Professional societies and national guidelines reinforce the need for adequate pre-test genetic counseling [4,7]. Unfortunately, in the absence of involvement by a genetic counselor, numerous instances of adverse outcomes have been documented [40–42] emphasizing the positive role of genetics professionals and their ability to impact delivery of care. It is acceptable to forgo referral to genetic specialist if the treating provider has the time during the patient visit to provide genetic counseling, the expertise on genetic testing methodologies and results interpretation, along with being able to educate the patient on the potential risks, limitations and benefits of testing [7,43,44]. This alternate model has the potential benefits of streamlining testing and reducing barriers yet increases the time and specialized training required of the treating provider. 6. Conclusion Oncology providers have a pivotal role to play in establishing universal genetic testing as the standard of care for women with ovarian cancer. How to achieve this may take several different forms. The pace at which universal testing needs to be accomplished has been hastened by advances in tumor biology and cancer genomics. This process change illustrates that universal genetic testing for women with ovarian cancer is very attainable in a short interval of time with minimal work-flow disruption and low cost. We demonstrate the methods we utilized to address several of the known barriers to universal genetic testing but it is likely that a compilation of several techniques can effect change. The results obtained here were sustained over the course of several years which demonstrates the ability for this to be a durable change. With the incorporation of universal genetic testing into our practice,
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer☆ Denise Uyar a,⁎, Jamie Neary a, Amy Monroe b, Melodee Nugent c, Pippa Simpson c, Jennifer L. Geurts d a
Department of Obstetrics and Gynecology, Medical College of Wisconsin, Milwaukee, WI, United States Clinical Cancer Center, Froedtert & The Medical College of Wisconsin, Milwaukee, WI, United States Department of Pediatrics, Section of Quantitative Health Sciences, Medical College of Wisconsin, United States d Department of Surgery, Medical College of Wisconsin, United States b c
H I G H L I G H T S • • • •
Improvement needed in efforts for universal testing in gynecology oncology. Implementation of simple measures can have large impact on achieving this goal. Education of providers is an effective way of impacting universal testing rates. Patients who see genetic counselors have a high rate of testing completion.
a r t i c l e
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Article history: Received 14 December 2017 Received in revised form 21 March 2018 Accepted 25 March 2018 Available online xxxx Keywords: Ovarian cancer Universal genetic testing Gynecologic oncology Quality improvement
a b s t r a c t Objective. The National Comprehensive Cancer Network recommends all women with ovarian cancer be offered genetic testing. Despite a decade of endorsement, many oncology practitioners have yet to make this a part of routine practice. Referral to genetic counseling and completion of genetic testing among patients at substantial risk of germline mutations are significantly lacking, adversely affecting patient care and squandering an opportunity to maximize cancer prevention efforts. This project determined the impact and feasibility of implementing a basic model for universal referral to genetic counseling and completion of genetic testing in women with a diagnosis of ovarian cancer in an academic gynecology oncology practice with access to electronic health records (EHRs). Methods. Patients diagnosed with ovarian cancer from January 2008 to November 2013 were retrospectively reviewed to determine the baseline referral rate for genetic counseling and testing completion in our practice. Implementation of a process change model combining provider training, patient education, enhanced electronic health record documentation and improved patient appointment scheduling strategies were implemented. We then prospectively collected data on all newly diagnosed ovarian cancer patients that had not already undergone genetic testing presenting from December 1, 2013 to November 30, 2016. Results. Genetic referral rates, genetic counseling and testing completion rates were markedly improved. Pre-implementation our genetic testing rate was 27% and post implementation our testing rate was 82% (p-value ≤ 0.001). Conclusions. Low cost interventions that target education of both providers and patients regarding the importance of genetic testing along with utilization of the EHR and streamlined patient appointment services can significantly increase rates of genetic testing completion. © 2018 Elsevier Inc. All rights reserved.
1. Background Epithelial ovarian cancer (EOC), inclusive of fallopian tube and primary peritoneal cancers, are the leading cause of mortality from ☆ No conflicts of interest or financial disclosures. ⁎ Corresponding author at: Department of Obstetrics and Gynecology, Medical College of Wisconsin, 9200 Wisconsin Avenue, Milwaukee, WI 53226, United States. E-mail address: [email protected] (D. Uyar).
gynecologic cancers. Approximately 10–20% of high grade ovarian, fallopian tube and peritoneal cancers are hereditary [1]. Recognition of hereditary cancer syndromes serves an increasingly important role in the care of women with gynecologic cancers. Previously, testing for hereditary cancer syndromes was reserved for select patients with an extensive personal or family history of cancer. However, over 50% of individuals with a BRCA1 or BRCA2 gene mutations do not have a personal or family history that would fulfill clinical criteria for testing [2]. Strict adherence to family history as the main criteria for testing omits
https://doi.org/10.1016/j.ygyno.2018.03.059 0090-8258/© 2018 Elsevier Inc. All rights reserved.
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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tubal and peritoneal cancers. Review of the guidelines ensured that all providers would be able to initiate the discussion and the counseling for patients with applicable diagnoses. Creation of an electronic “smart phrase” (a quickly accessible standardized text) for use in the electronic health record (EHR). This “smart phrase” when added to a clinical encounter efficiently documented that the rationale behind genetic testing was reviewed and that the genetic counseling recommendation was made. Providers were educated on the use of this standard text to efficiently document in the EHR. The “smart phrase” essentially standardized and simplified documentation. Patient education regarding the role of genetic testing at the time of their diagnosis began as early as their initial consultation visit. An electronic “smart phrase” was also created for patient instructions. This text included the explanation of the rationale and benefits of seeking genetic counseling and testing in lay language. This text was added to all patient instructions in the EHR. These instructions were printed and given to patient at conclusion of their appointment with the after-visit summary, creating an efficient means of providing patient education. Scheduling of the genetic counseling appointment at the time of patient check out (point of care) from the gynecology oncology clinic was initiated to avoid delay in scheduling appointments and facilitate a more patient centered experience. Tumor Board conference documentation was updated as well to include whether genetic counseling was recommended, pending or completed as a part of all treatment recommendations for ovarian cancer patients. Tumor Board notes were made more comprehensive by including the recommendation for genetic testing in the final recommendations for applicable patients and were part of the patient's EHR. Genetic counselors also regularly attend and participate in our Tumor Board conferences.
a significant proportion of at risk women from obtaining testing. In 2005 the United States Preventative Task Force opened the scope of eligibility and began to more formally recommend that genetic counseling and testing be offered to all at risk individuals [3]. Shortly after that, the National Comprehensive Cancer Network (NCCN) updated their guidelines in 2007 and recommended that all women with ovarian cancer and their immediate family members be offered genetic counseling and testing regardless of age at diagnosis or family history of cancer [4]. Similarly, other societies have endorsed this recommendation such as the American College of Obstetrics and Gynecology [5], American Society of Clinical Oncology and the American College of Medical Genetics [6,7]. Recently, the Society of Gynecologic Oncology issued a position statement emphasizing the importance of genetic testing for women affected by gynecologic cancers [8]. Germline mutations in BRCA1 and BRCA2 are reported to occur in 15–20% of ovarian cancer patients and are known to increase the lifetime risk of ovarian cancer by 20–50% and breast cancer by 50–80% [9,10]. Additional genes have been associated with homologous recombination and hereditary ovarian carcinoma including RAD51C, RAD51D, BRIP1, PALB2, as well as mismatch repair genes (MLH1, MSH2, MSH6, PMS2) which are believed to contribute an additional 2–4% of ovarian cancers [10–12]. BARD1 may be a rare ovarian cancer susceptibility gene but more study is needed to define its absolute risk [10]. The potential benefits of identifying patients with genetic mutations continues to expand and includes offering risk reducing prophylactic measures, enhanced surveillance, individualization of prognosis for patients, potential utilization of targeted therapy, and increasingly inclusion in clinical trials. Despite these benefits, national and international studies have consistently shown low utilization of genetic counseling and genetic testing completion among ovarian cancer patients [13–21]. A recent study by Childers et al. found that only 1 in 5 women in the United States with history of breast or ovarian cancer meeting NCCN guidelines have undergone genetic testing [17]. Oncologists are a critical part of identifying, educating and referring eligible patients for genetic counseling. Identifying efficient strategies to incorporate this philosophy into practice, promote the referral to genetic counselors and strategies to enable oncologists to take a more active role in assisting the completion of genetic testing are needed. We compared historical rates of referrals to genetic counseling and completion rates of genetic testing for patients with ovarian cancer in our practice to rates of genetic counseling referrals and genetic testing completion post-implementation of the process change model. The goal of the project was to establish an efficient process for universal genetic testing for ovarian cancer patients in our practice.
The rates of completion of genetic counseling and genetic testing before and after the implementation measures were compiled and compared. For independent group comparisons, a non-parametric two-sided Fisher's exact test was used for the categorical variables and the Mann-Whitney test was used to compare continuous variables. Continuous variables are summarized as median (range). Unadjusted p-values b 0.05 were considered significant. SPSS version 24 (IBM Software, Chicago, IL, USA) was used to analyze the data.
2. Methods
4. Results
All patients ≥18 years presenting to a single gynecologic oncology practice at an academic cancer center with a new diagnosis of nonmucinous epithelial ovarian, fallopian tube or primary peritoneal cancers from January 1, 2008 to November 30, 2016 were included in the data determining our baseline genetic referral and genetic testing completion rates. Patients with previous germline gene testing were excluded. Patients were divided into two cohorts based on when they presented: patients who presented prior to quality improvement measures to establish the baseline (Jan 2008–November 2013) and patients who presented after the implementation of quality improvement measures (December 2013–November 2016). Our model aimed at establishing a uniform practice norm for universal genetic counseling and testing in our clinic and included implementation of the following measures:
Data was collected entirely from the EHR which captures the patient's diagnosis, documentation of genetic counseling in the chart, whether a referral to genetics was placed, scheduling of appointment with genetics, completion of genetic counseling, completion of genetic testing and results of genetic testing. There are 2 cohorts; a retrospective portion (January 2008–November 2013) and a prospective portion (December 2013–November 2016). There was no statistical difference in patient age (years); 60 (26–88) vs 64 (22–85) (p = 0.26). In the retrospective portion of the study, 207 patients met inclusion criteria. Forty-two (20%) patients received documented education by their provider at the time of diagnosis regarding referral to a genetic counselor for genetic testing. Ninety-six (46%) patients had a referral order to genetic counseling placed by their provider at the time of initial diagnosis. Of the 207 patients, 67 (32%) were seen by a genetic counselor. Of those 67 patients counseled and seen by a genetic counselor, 55 (82%) patients underwent genetic testing. In summary, of the 207 patients eligible for genetic testing from January 2008–November 2013, only 27% (55 of 207 patients) completed genetic testing. As anticipated, our baseline referral rate and testing completion rate were poor, similar to national
• All gynecologic oncology providers in our practice received a review of the rationale behind universal genetic testing and the current NCCN and Society of Gynecologic Oncology guidelines recommending genetic testing for all women with non-mucinous epithelial ovarian,
•
•
•
•
3. Statistical analysis
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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rates. Notable however, is the finding that of the 67 total patients seen by genetics for counseling, the majority completed genetic testing (82%, 55 of 67 patients). The process change model for universal genetic testing as detailed above was then instituted on December 1, 2013 in our practice. All providers and all new patients with non-mucinous EOC in our gynecologic oncology clinic were included in the implementation of the model. Implementation of the initiatives was phased in over approximately 3 months. One hundred and sixty-two patients with newly diagnosed ovarian cancer in our clinic were initially identified for inclusion in the prospective portion of the study from December 2013–November 2016. Thirtyseven patients were excluded since they had already undergone genetic testing, leaving 125 patients in the final analysis. After the measures were implemented, the rate of documented recommendation in the EHR for genetic counseling, rate of referral to genetics, rate of completion of genetic counseling and rate of completion of genetic testing were calculated and there were significant differences from pre- to post-implementation (Table 1). One hundred and ten patients (88%) had appropriate documentation of the genetics recommendation in the EHR and 122 patients (98%) had a genetics referral placed. One hundred and eight of the 125 patients (86%) underwent genetic counseling and 103 of 108 patients (95%) ultimately completed genetic testing. Thus, after the implementation of these measures, 103 of 125 eligible patients (82%) completed genetic testing improved from 27% in the previous cohort. The number of patients with a gene mutation detection in this group was 22 (22%) which was not statistically different from the pre-implementation detection rate of 18% (10 of 55 patients). Overall, the genetic testing completion rate increased from 27% (55 of 207 patients) to 82% (103 of 125 patients) (p-value ≤ 0.001). Per anecdotal reports from providers, the incorporation of smart phrases into their work flow was not time intensive and was an acceptable process change. Enhancing EHR alone and combined with other strategies to increase provider referral for genetic testing has been successful in other studies as well [18,19]. Incorporating a more efficient method of scheduling patient appointments was instrumental was also instituted and was helpful in optimizing scheduling for patients. Scheduling genetic counseling consults had previously been performed by the genetics clinic but we eliminated that step and had our gynecology oncology schedulers assume the responsibility for directly scheduling appointments. This more patient focused approach allowed patients to schedule their own genetics appointment in the gynecology oncology clinic at the time of check out rather than waiting for a phone call from the genetics clinic. Per informal questioning of patients, streamlining the process required to make appointments was an important factor for them. Having the patient education printed out for them at the time of checkout also helped reinforce the significance of the recommendation at the time of check out when the referral appointment was being made. 5. Discussion Standard of care guidelines dictate that all women with ovarian cancer receive genetic counseling and genetic testing. Several societies and
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institutions have reached consensus regarding the recommendation for universal genetic testing and yet referrals to genetics and completion of genetic testing for this high-risk population remain suboptimal. Every year that does not see these guidelines executed represents missed opportunities for the thousands of women diagnosed with gynecologic cancers and their at-risk family members. Several barriers to the uptake of genetic counseling and completion of genetic testing have been noted. These barriers include lack of familiarity with guidelines on the part of the clinician, lack of time on the part of providers, lack of access to genetic counselors, lack of understanding by patients regarding the importance of genetics/genetic testing which may contribute to fears of testing, and in some cases patient cost and convenience [22]. Oncology providers are charged with incorporating discussions regarding the importance and rationale behind the recommendation for genetic counseling and genetic testing to patients that meet criteria for testing. For universal testing to become a reality it is essential that providers are able to identify appropriate patients, understand the impact that genetic testing has on their treatment and their prognosis and feel comfortable initiating these discussions. Research has shown that the physician's recommendation is one of the strongest factors influencing a patient's decision to meet with a genetic counselor [23]. Beginning our initiative with education for providers on the guidelines for risk assessment addressed the barrier of provider education. This first step was necessary for reinforcing the current guidelines for all providers and the importance of genetic testing for high risk populations. In both academic and non-academic practices, the EHR is well established and may represent an underutilized resource for assisting practice change in many different ways. Creation of electronic phrases to expedite documentation and enhance printed patient education were found to be very acceptable to our providers, required very little training and standardized the EHR. Part of a successful recommendation to genetics includes proper documentation in the medical record and our strategy represents one method of accomplishing this goal. Once properly recorded, it is simple for any provider to confirm genetic counseling and/or testing has been completed. It is notable that once patients met with genetic counselors the rate of testing was quite high: 55 of 67 (82%) patients who met genetic counselors prior to the quality improvements and 103 of 108 (95%) patients who met genetic counselors post intervention completed genetic testing. It has been shown previously that uptake of cancer risk management strategies, including genetic testing, are increased when patients are effectively counseled by a genetics provider [1] and our study supports this finding as well. Thus, a strong emphasis should be placed on the genetics referral to ensure a successful implementation of universal genetic testing. Given the increasing complexity of available genetic testing and interpretation of results, incorporating the expertise of genetic counselors as consultants continues to play an important role in patient care for our practice. Kentwell et al. and Senter et al. [24,25], found that embedding a genetic counselor within their clinic was most effective at improving their performance of completing genetic counseling and genetic testing. We do not have the ability to replicate this model in our clinic owing to the few genetic counselors in our facility, however the services are provided in the same building. The
Table 1 Patients with ovarian cancer eligible for genetic testing.
EHR documentation Referral placed to genetic counseling Genetic counseling completed Genetic testing completed/genetic counseling completed Patients with identified gene mutations a
Pre-implementation (N = 207) Jan 2008–Nov 2013
Post-implementation (N = 125) Dec 2013–Nov 2016
N Evala
N (%)
N Eval
N (%)
207 207 207 67 55
42 (20) 96 (46) 67 (32) 55 (82) 10 (18)
125 125 125 108 101
110 (88) 122 (98) 108 (86) 103 (95) 22 (22)
p-Value
≤0.001 ≤0.001 ≤0.001 0.007 0.68
N Eval = evaluable patients.
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
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inability to embed a counselor in the clinic is likely to be an obstacle for other practices as well. We found we could still positively impact our performance of acceptance of genetic counseling and testing without having an embedded genetic counselor within our clinic. Timing of genetic counseling/testing for patients with EOC has also been studied but there is currently no standard guideline or recommendation. Novetsky et al. [23] found that women's views regarding the optimal time to be referred and undergo testing varied greatly but the study concluded that early discussion regarding referral was preferable. Fox et al. concluded that the majority of women (59%) with serous ovarian cancer prefer to have genetic counseling at the time of diagnosis [26]. We are proponents of beginning the discussion as early as possible. Earlier testing may be useful in discussions regarding prognosis, may contribute to efficient identification of patients for clinical trials, allows for more opportunity to counsel hesitant patients regarding additional cancer associated risks and, given the rapidly changing landscape of targeted therapy, such as poly-ribose ADP polymerase inhibitor (PARPi) treatment, earlier testing may be an advantage for determining eligibility for clinical trial participation or for initiating maintenance therapy in the near future. Tumor Board conferences, although a cornerstone in academic practices, may not be applicable to all types of oncology practices. This conference has been instrumental in our transition to universal testing as it is serves as another means of reinforcing genetics as an important resource that is assimilated into our multidisciplinary practice. All of our Tumor Board discussions now include documentation about whether genetic counseling has been recommended and completed; Tumor Board notes become part of the patient's EHR. This also serves as a document that can be shared with outside providers and formal inclusion of the recommendation for genetic counseling and testing in this format may also enhance compliance. Our genetic counselors attend the Tumor Board conferences and contribute to our patient discussions. Some have noted the presence of genetics providers at Tumor Board has been shown to increase the rate of referral and gene testing [27]. Others have found that despite having multidisciplinary conferences there are still patients who do not receive an appropriate cancer risk assessment [28]. We have found it to be useful in our practice to have genetic counselors present in multidisciplinary conferences. In addition, we have residents and fellows in attendance at these conferences and our discussions surrounding cancer risk assessment for high risk patients reinforces the significance of obtaining genetic counseling and testing, as well as obtaining a thorough family history for those in training. Our referral rate to genetics after implementation of this project was nearly 100% and yet we did not have 100% completion rate of genetic counseling or testing. We tracked the patients that did not ultimately see a genetic counselor or complete testing (missed opportunities) to determine if any pattern was apparent. The missed opportunities are detailed in Table 2. In total 18 patients over the course of the three years of this project did not complete genetic counseling or testing. Half (n = 9) of those patients did not complete the recommendation due transferring care (lost to our follow-up) or they passed away soon after diagnosis prior to being able to complete genetic counseling. In only one case did the patient site cost as the reason for her resistance, however after gratis funding for genetic services was obtained, the Table 2 Post-implementation missed opportunities. No. of patients Deceased Never scheduled appointment Cancelled appointment Genetic counseling appointment pending Declined testing after genetic counseling Transferred care Insurance denial
4 2 4 2 5 2 1
patient still declined. Patients that met with counselors and declined testing in our experience felt particularly overwhelmed and when asked stated they were not sure they wanted to know about additional cancer risks. These patients may reconsider this option in the future once the initial shock of the diagnosis is faded and time has elapsed. We have concluded that our increased genetic counseling and testing rates from 2013 to 2016 are attributable to the success of our described process change however, we also realize that a multitude of factors have likely influenced the completion of genetic testing during this time period. The decreasing cost of genetic testing [29] and the emerging role of targeted PARPi therapy for the treatment of relapsed platinum-sensitive EOC [30] are examples of factors potentially influencing rates of genetic testing in the last few years. The pivotal phase II study of PARPi in relapsed platinum-sensitive EOC demonstrating greater efficacy in patients with BRCA 1/2 mutations was published in 2012 [31], just prior to the roll out of our process change. In addition, high profile celebrity disclosures of gene mutation status have the capacity to influence genetic testing rates in unanticipated ways. In 2013 Angelina Jolie disclosed in the New York Times her BRCA1 status and urged women to undergo genetic testing, this remains one of the most viewed health related articles in the social media age [32,33]. Within months of the Angelina Jolie story another impactful event occurred, with a Supreme Court ruling that effectively invalidated the patents for the BRCA1 and BRCA2 genes. Immediately after this ruling, additional laboratories began offering testing, including BRCA1 and BRCA2 on multi-gene sequencing panels at a fraction of the previous cost for BRCA1 and BRCA2 only [34]. The national increased awareness along with enhanced access and reduced cost of testing may have played a role in our observation of increased uptake of genetic counseling and testing. Our process change, however, may have made it possible for our practice to efficiently evolve with this dynamic landscape. Although access to genetic services was not a barrier in our study as our institution has genetic counselors available 5 days per week, it is worthy to note that many health centers do not have local genetic counseling readily available [35–38]. In response to the increase in demand for access to genetic counselors, new services models have emerged including virtual visits, group sessions and telephone counseling [39]. Professional societies and national guidelines reinforce the need for adequate pre-test genetic counseling [4,7]. Unfortunately, in the absence of involvement by a genetic counselor, numerous instances of adverse outcomes have been documented [40–42] emphasizing the positive role of genetics professionals and their ability to impact delivery of care. It is acceptable to forgo referral to genetic specialist if the treating provider has the time during the patient visit to provide genetic counseling, the expertise on genetic testing methodologies and results interpretation, along with being able to educate the patient on the potential risks, limitations and benefits of testing [7,43,44]. This alternate model has the potential benefits of streamlining testing and reducing barriers yet increases the time and specialized training required of the treating provider. 6. Conclusion Oncology providers have a pivotal role to play in establishing universal genetic testing as the standard of care for women with ovarian cancer. How to achieve this may take several different forms. The pace at which universal testing needs to be accomplished has been hastened by advances in tumor biology and cancer genomics. This process change illustrates that universal genetic testing for women with ovarian cancer is very attainable in a short interval of time with minimal work-flow disruption and low cost. We demonstrate the methods we utilized to address several of the known barriers to universal genetic testing but it is likely that a compilation of several techniques can effect change. The results obtained here were sustained over the course of several years which demonstrates the ability for this to be a durable change. With the incorporation of universal genetic testing into our practice,
Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059
D. Uyar et al. / Gynecologic Oncology xxx (2018) xxx–xxx
we are now in a better position to meet the expanding role of genetic assessment for the treatment decisions of patients with EOC. Continued efforts still need to be directed towards increasing cancer predisposition testing. We have found the dilemma of how to best complete cascade testing in family members to be especially challenging and continue to work on how best to accomplish this next goal. Ethical statement All authors declare that they have no conflict of interest. IRB approval was obtained for the publication of this project for the purposes of publication. The IRB waived the requirement for obtaining informed consent for this as it was a quality improvement project thus they deemed that informed consent was not required. There was no funding obtained for this project. References [1] T. Pal, J.H. Lee, A. Besharat, Z. Thompson, A.N. Monteiro, C. Phelan, J.M. Lancaster, K. Metcalfe, T.A. Sellers, S. Vadaparampil, S.A. 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Please cite this article as: D. Uyar, et al., Implementation of a quality improvement project for universal genetic testing in women with ovarian cancer, Gynecol Oncol (2018), https://doi.org/10.1016/j.ygyno.2018.03.059