Integrated implementation of evidence-based interventions to increase colorectal cancer screening through public health-primary care partnerships

In 2015, the Centers for Control and Prevention funded the Colorectal Cancer Control Program (CRCCP), which partners with health systems and primary care clinics to increase CRC screening uptake. We interviewed CRCCP stakeholders to explore factors that support an integrated implementation of evidence-based interventions and supporting activities to promote CRC screening with other screening and chronic disease management activities in primary care clinics. Using Research, we conducted a literature review and identied constructs to guide data collection and analysis. We purposively selected that demonstrated engagement willingness and availability We gathered background information on the selected and conducted and We used NVivo to coecient or higher, and then implemented to identify site-specic and emergent themes. The ndings provide insights into how public health programs can support primary care clinics in integrating interventions and activities into existing workows to support ecient, coordinated delivery of quality patient-centered care. Describes how Colorectal Cancer Control Program public health and primary care partnerships support integrated implementation of evidence-based interventions and supporting activities to promote colorectal cancer screening and management of other chronic diseases. Provides insights into how public health programs and primary care clinics can collectively support integrated implementation of interventions into clinic workows to support ecient, coordinated delivery of interventions to ensure patient-centered care. Includes a dening set of theory-driven constructs relevant to integrated implementation of chronic disease management interventions and activities within clinical settings. Abstract - Summary of key elements of the study using the abstract format of the intended publication; typically includes background, purpose, methods, results, and conclusions


Introduction
Collaboration between public health and primary care is seen as an opportunity to promote health at the individual and community levels [1][2][3]. Integrated implementation of patient care interventions and activities can support primary care clinics in improving e ciency of clinic work ows and coordinating delivery of patient-centered preventive care [4,5]. Integrated implementation also may support longer-term outcomes, including clinic institutionalization of health promotion practices and cost savings [6,7]. Public health partners can play an important role in supporting the implementation of these practices in primary care settings.
In 2015, the Centers for Disease Control and Prevention (CDC) funded the Colorectal Cancer Control Program (CRCCP), which is based on a health systems change model that promotes integrating public health and primary care to improve population health; speci cally, to increase colorectal cancer (CRC) screening among medically underserved populations ( Fig. 1) [8].
CDC funded 30 CRCCP program sites (hereafter referred to as programs) that partner with primary care clinics (hereafter referred to as clinic partners) to implement evidence-based interventions (EBIs) recommended by the Community Preventive Services Task Force in The Community Guide [9] coupled with other supporting activities (SAs) to increase the uptake of CRC screening. The CRCCP DP15-1502 was funded for 5 years from 2015-2020. Participating clinic partners selected up to four EBIs prioritized by CDC-patient reminders, provider reminders, provider assessment and feedback, and reducing structural barriers to screening-and other SAs to implement based on clinic priorities and feasibility. SAs include implementing community health worker-led activities, patient navigation, health information technology, professional development, and small media. CRCCP programs and partners with relevant expertise, such as the American Cancer Society and the State Primary Care Association, provide technical support to implement these activities. Because the CRCCP is focused on health systems change-such as improving work ows and electronic health record (EHR) systems to incorporate EBIs/SAs so that they are sustainable-the opportunity exists to integrate the implementation of EBIs and SAs to promote not just CRC screening but also other screening and/or chronic disease management activities. Intended outcomes of this integrated approach to implementing EBIs and SAs include improved e ciency of clinic work ow, improved coordination of patient care, increased uptake of CRC screening, and improved patient outcomes.
This study aimed to examine CRCCP clinics where EBIs and SAs to promote CRC screening were integrated with other screening and chronic disease management activities and to identify practices facilitating this integration. CDC intends to use the study ndings for CRCCP implementation. Findings could also potentially be used by other organizations involved in promoting CRC screening and management of other chronic diseases. Lessons learned also may support cancer screening integration efforts among other chronic disease programs.

Methods
We used the Consolidated Framework for Implementation Research (CFIR) [10] to structure our approach to identify factors that support integrated implementation of EBIs and SAs, focusing on characteristics of the inner setting (clinics, in this context)-features of structural, political, and cultural context. Using the CFIR, we conducted a literature review to identify key constructs relevant to integrated implementation that aligned with CFIR inner setting constructs: readiness for implementation, structural characteristics, and networks and communication. Our literature review yielded four key integrated implementation constructs ( Table 1) that guided data collection and analysis efforts.
Our primary evaluation question was, "What factors support integrated implementation of EBIs and SAs to promote CRC screening with other screening and chronic disease management activities within primary care clinics?" We developed additional evaluation questions (see Additional le 1) related to each of the key constructs in Table 1. An overview of our methodological approach is provided in Fig. 2 and further detail about site selection, data collection, and analysis are provided below.

Data Collection
For each selected program, we interviewed staff, clinic partners, and implementation partner organizations (e.g., non-clinic partners funded to provide technical assistance to clinics). The four theorybased constructs-governance structure, information sharing, funding environment, and leadership support-and evaluation questions informed the development of unique interview guides for each of the three participant roles. We selected these participant types to gather input from multiple perspectives. Sample interview questions are provided in Additional le 2.
Prior to primary data collection, we reviewed secondary data for each program, such as budgets and survey ndings. Secondary data were not available for Nebraska because they were not receiving CRCCP funds at the time of our interviews. To gather contextual information about each program before initiating interviews, we spoke with CDC staff who provided tailored technical assistance directly to the three selected CRCCP programs.
We obtained verbal consent for interviews from each participant. Institutional Review Board approval was not required for this data collection because it did not constitute human subjects research. In total, 23 individuals, including representatives from one clinic partner location per program, participated in semistructured telephone interviews (

Analysis
Prior to analysis, we developed a coding dictionary based on our evaluation questions (see Additional le 4). A team of four analysts pilot-coded two interview transcripts using the qualitative software NVivo QSR 11.0. The team then met to develop consensus regarding re nement and application of the coding framework. Four interviews (20%) were double coded-independently coded by two analysts-and analysts achieved a Kappa coe cient of 0.8 or higher for each. The remaining interviews were divided evenly among the four analysts and independently coded. Following coding, analysts reviewed code reports to identify program-speci c emerging themes and recorded these themes in summary tables that included a description of each theme, illustrative quotes supporting the theme, and the interviewee role for each quote. Analysts convened and reviewed all theme tables and identi ed cross-cutting emergent themes, which were themes that emerged across at least two programs.

Results
Brief descriptions of clinic partner approaches to integrated implementation of CRCCP activities are provided in Additional le 5. In the following sections, we present our results based on the four guiding integrated implementation constructs. These results are summarized in Figure 3.

Funding Environment
The clinic partners received funding from the CRCCP programs, typically to support start-up and ongoing costs associated with implementing the CRCCP within their sites. Two aspects of the funding environment were identi ed as facilitating integrated implementation: (1) coordination of funding by awardees across multiple chronic disease programs to support consolidated application processes for clinic partners, and (2) contracting with expert implementation partners to provide training and technical assistance to clinic partners that emphasized integrated implementation.
Participants discussed programs providing braided funding-a process that involves coordinating separate funding streams from multiple programs, such as CRCCP and the National Breast and Cervical Cancer Early Detection Program (NBCCEDP)-to pay for common activities such as patient navigation across programs, provider reminders and patient reminders (e.g., reminders for breast, cervical, and colorectal cancer screening). However, each funding stream is kept separate so programs can track requirements and outcomes. For example, program staff discussed developing funding opportunity announcements for clinic partners that braided funding streams from multiple programs. This approach enabled clinic partners to consolidate their funding applications and reporting processes while tracking distinct activities and outcomes for each funding stream. Participants also reported that by braiding funding from multiple chronic disease programs, clinic partners could submit a single funding application and receive a larger amount of funding that could be used to integrate implementation efforts across multiple chronic diseases. For instance, participants reported the use of braided funding to support patient navigation staff who coordinate screening and follow-up for CRC, breast cancer, and cervical cancer.
"The [health department's] women's cancer screening and colorectal had patient navigation contracts with all the [Federally Quali ed Health Centers] throughout the state and in order to get the FQHCs to agree to do the colorectal, right from the beginning she integrated the contracts so we essentially were doubling the money that we were offering to them and it was an all or nothing kind of thing." -Clinic staff Participants also described how technical assistance and training, provided by expert implementation partners, facilitated integrated implementation. For example, implementation partners assisted clinics in adapting EHR or other referral systems to integrate CRC screening with existing referral systems for breast cancer screening such as mammography.
"[Implementation partner agency] is our partner in understanding how to look at [clinic] practice ows and how to coordinate, integrate, align the work we do…. They say, 'Okay, you really need to work on your electronic referrals [for screening]. Let's look at how you're doing that with mammograms. Let's look at how you're doing that with colonoscopy.'" -Program staff "We strongly encourage [clinic partners] to consider how their efforts could be better integrated with their other programs and activities in their clinic systems. For example, when they describe [clinic] work ows to us on these technical assistance calls, we try to prompt them to consider how these efforts may impact other efforts ongoing in their clinics, other screening activities…if they're going to look at, for example, whether or not a patient is due for colorectal cancer [screening as part of work ow processes], seeing if there are opportunities in their other cancer screening activities and work ows." -Implementation partner staff Governance Structure Effective team-based care, a factor related to governance structure, ensured that CRC screening was integrated into clinic practice as part of comprehensive, coordinated patient care. For example, some clinics used "health hubs" comprised of clinic staff from CRCCP, WISEWOMAN, and NBCCEDP to implement coordinated EBIs across programs. Participants reported that effective teaming supports a shared sense of responsibility for providing comprehensive (such as multiple health topics), coordinated patient care. For example, participants described training all clinic staff-such as patient registration staff, lab technicians, and nurses-to address CRC and other health conditions with each patient encounter. Workforce development (e.g., learning collaboratives) also included clinic staff representing multiple chronic disease prevention areas. Additionally, participants described the integration of CRC screening with other services (e.g., coordinated patient enrollment with WISEWOMAN and NBCCEDP; coordinated patient and provider reminders) as being consistent with their commitment to applying a Patient Centered Medical Home (PCMH) model. "So, every clinical person from our lab person to our [patient] registration staff to every nurse [and] medical assistant understands that they're required to address all of these [health topics] with every patient. It's just the way we train them when they come in…it's the way we do business." -Clinic staff "Going back to the PCMH [model] of having all staff [perform at] the highest ability that they're able to. So, our frontline, our medical assistants, our front-desk staff are very involved and very engaged in these management activities, cancer screening activities." -Clinic staff "We have a team medical assistant [who] is able to follow up on closing the loop to patients about, 'Hey, I see you haven't done this,' or 'Your [test]was high. We need you to come back in or follow up on those things.' And then the RN is able to really take the time and educate the patients on different dietary concerns, different ways to manage whatever speci c chronic condition that they have." -Clinic staff Information Sharing Access to and sharing of accurate patient information, including EHR data, were identi ed as other factors supporting integrated implementation of CRC screening. Identifying patients who are due for multiple preventive screenings, including CRC, was an example shared by participants. Once patients could be identi ed, referrals could be made and follow-up actions-such as appointment scheduling and con rming screening completion-could be carried out.
Participants indicated that clinic staff, particularly patient navigators and care coordinators, rely on the availability of accurate EHR reports to identify patients for screening and/or diagnostics for multiple chronic disease conditions. Clinic staff emphasized that the utility of the EHR data in supporting integrated implementation is contingent on data accuracy.
"The challenges we face with CRC, breast cancer, and cervical reporting [are] the same challenges we face with everything else. Making sure [EHR data] are entered correctly and data validation." -Clinic staff Aside from EHRs, participants identi ed data dashboards and meetings of the quality improvement team as strategies for sharing information that facilitated integrated implementation. Electronic dashboards presented summary metrics on multiple cancer screenings in real-time for each provider and their respective patients. Through data sharing and making comparisons between physicians that invite friendly competition, the dashboards promote action on multiple conditions that contribute to integrated implementation. Similarly, data sharing among quality improvement (QI) teams promotes a collective understanding of where clinics stand on delivery of health promotion activities that can foster understanding of opportunities to potentially improve these metrics through integrated implementation.
"All of our staff have access to the provider dashboard, which is updated once a month and that shows where their particular provider is and what the [clinic] average is and then… they can go and look at any other provider…it's just starting with the cancer screening metric, but eventually we'll put all of our metrics on that…it will give them more of a real-time feel of where they're at." -Clinic staff "We also…had monthly quality improvement meetings, where all of the clinic's leadership and the QI department got together, and we talked about things that we are working on, and things that could potentially be shared…beyond just cancer, or beyond just diabetes care, or whatever thing we were talking about." -Clinic staff Leadership Support Clinic leadership plays a primary role in promoting integrated implementation by setting and reinforcing expectations. Participants indicated that strong and ongoing support from health system and clinic leadership establishes an expectation for integrating CRC EBIs and SAs within the clinic practice and incorporating CRC screening efforts with other chronic disease activities. Additionally, leaders are crucial in encouraging staff from across the clinic team to support these activities.
"Leadership support is critical.… It's evident, if you see the [screening] numbers of the teams that have the leadership support and the ones from the team that didn't [have leadership support], it's night and day." -Implementation partner staff "I'm the clinic manager and so I set the tone for the sense that the evidence-based interventions are important. We need to integrate them and so you talk about it, you bring it up frequently. As a group, we collectively talk about what we think works for us and what doesn't work for us." -Clinic staff

Discussion
Our study examined the CRCCP, a public health program implemented in primary care clinics, to identify factors facilitating the integration of EBI and SA implementation with other screening and chronic disease management activities. Using the CFIR helped focus identi cation of factors that support integrated implementation of EBIs and SAs, including funding environment, governance, information sharing, and leadership.
We found that integration efforts in clinics were supported by programs consolidating their chronic disease funding into single contracts for partner clinics, rather than providing separate, "siloed" contracts for individual health conditions. In the CRCCP, this funding approach presents an opportunity for more e cient use of public health funding for delivering coordinated cancer screenings and other disease management interventions to support more holistic, patient-centered care. E ciencies are also achieved when clinic staff respond to a single, consolidated funding application rather than multiple applications. And the pooled funding provides both programs and clinics exibility to leverage funds and share overhead costs, offering the opportunity to achieve more with their awarded funds [26]. At the program level, consolidated funding also supports e ciency by streamlining delivery of training and technical assistance to a smaller number of funding recipients; meaning that more in-depth support can be provided to trainees.
At the clinic level, a team-based approach was found to support more integrated care for a patient, including for CRC screening. Teams of clinicians are likely able to determine how best to integrate CRC screening efforts-such as identifying patients who are due for screening and determining how to deliver a reminder to a provider-into existing clinic work ows. This is consistent with coordinated delivery of interventions to ensure patient-centered care, which can ultimately lead to improved patient outcomes EHR systems, a reservoir of patient information, also were found to be important to integrated implementation. Although investing in functional EHR systems can be costly, they are recognized as essential to enable optimal, integrated, patient-centered care because they allow for abstraction of accurate clinical information. In 2011, the Centers for Medicare & Medicaid Services established an EHR incentive program to reward meaningful use of certi ed EHR systems to improve quality of care [30]. Since then, there has been a national push for health systems to adopt EHRs to support clinical practice transformation. Meaningful use of EHRs has been associated with quality improvement in Federally Quali ed Health Centers (FQHCs) [31]. In 2012, 90% of FHQCs had adopted an EHR and about one-third had met core requirements for meaningful use [32]. The ndings from our study indicate that EHRs also can help facilitate integrated implementation of EBIs to promote cancer and other chronic disease screenings. For example, once developed, data dashboards that display provider performance metrics for CRC screening can be replicated and/or expanded to produce monitoring data for other cancer or chronic disease screenings, placing patients at the center of care provided by multiple public health programs. Additionally, EBIs that can be enabled through the EHR system, such as automated patient and provider reminders or performance metrics to populate dashboards, may be more sustainable. Once these strategies are built into EHR systems, signi cant e ciencies could be achieved.
Finally, leaders' expectations for integrated implementation sets the tone for other staff and directs practice. CRC champions, individuals serving as internal advocates for screening, help maintain a focus on screening and were found to be associated with greater screening rate increases in CRCCP clinics [8].
Champions have been found to contribute to improved public health outcomes in many areas and efforts to sustain and support them as part of the CRCCP is critical [33]. Therefore, leadership support is essential for clinic champions to effectively promote and sustain integrated implementation.
Our ndings highlight elements and practices of integrated implementation that can support clinics in achieving desired short-term outcomes, including e cient, coordinated delivery of interventions to ensure patient-centered care, which can ultimately lead to improved patient outcomes and quality of life as well as reduced health care costs [27,28].
CDC, through the CRCCP Learning Collaborative, is working with programs and clinic partners to systematically evaluate the cost and cost-effectiveness of combined implementation of EBIs for cancer screenings [7]. Lessons learned from the integrated implementation platform for CRC screening through the CRCCP might be applied to enhance other public health and primary care partnership programs, such as CDC's National Breast and Cervical Cancer Early Detection Program. For example, ndings might be applied to inform the structure of public health department partnerships with clinic and non-clinic partners; inform the nature of training and technical assistance provided to primary care clinics; encourage early efforts to seek leadership buy-in to setting the stage for integration; and reiterate the value of capturing and sharing high-quality data to support integrated programs.
There are certain limitations for our ndings. First, because the study was qualitative and engaged a subset of current and former CRCCP programs and their primary care clinic partners, these ndings are not generalizable to all CRCCP programs or primary care clinic sites. Second, the ndings re ect a relatively small number of participants included in the data collection. Third, this study was framed around exploration of four theory-driven constructs. Future analysis that incorporates a broader set of constructs may generate additional insights regarding factors that support integrated implementation of interventions for multiple conditions within primary care. Finally, we did not track outcomes in this analysis but plan to engage in such assessments in future analyses.

Conclusion
In this study, we identify factors, at the CRCCP program and clinic levels that support integrated implementation of EBIs and SAs within clinic settings to promote CRC screening and screening/management of other chronic diseases. We present our ndings within the frame of four theory-based implementation constructs. The ndings provide insights into how public health programs and primary care clinics can collectively support integrated implementation of interventions and activities into clinic work ows to support e cient, coordinated delivery of patient-centered care. The next step is for further research to explore the impact of these public health and primary care partnerships and related activities on patient and program outcomes.

Availability of Data and Materials
The qualitative data generated and/or analyzed during the current study are not publicly available because they were generated in interviews conducted by the research team, with the expectation that participant identity would be kept con dential.

Ethics Approval and Consent to Participate
The RTI Institutional Review Board determined that this study did not constitute human subjects research and therefore did not require review. Verbal consent to participate was obtained from all individuals who participated in interviews.

Consent for Publication
Consent for a de-identi ed summary of ndings was obtained from individuals who participated in the interviews.

Competing Interests
The authors declare that they have no competing interests.

Funding environment
Integrated health and social services are supported by nancing mechanisms that fund services and allow braiding or blending of funds with exibility in the use of funds to achieve population health goals [3,[11][12][13][14]. Integrated services also may be supported by partner agencies that receive funding to provide training and technical assistance to assist clinics to adapt clinical work ows.

Networks and Communication
The nature and quality of webs of social networks and the nature and quality of formal and informal communications within an organization.

Governance structure
Cooperation between and within organizations to support integrated health care delivery requires governance structures that promote coordination, joint planning, shared priorities, and a common understanding of accountability among staff [11,[15][16][17].

Information sharing
Information ow in a clinical setting is necessary for integrated health care delivery and is supported by the presence of a secure, accessible platform for storing and sharing health care information, consistent documentation, and a structured plan to facilitate seamless communication among health system care providers [11,13,18].

Readiness for Implementation: Leadership Engagement
Commitment, involvement, and accountability of leaders and managers with the implementation.

Leadership support
Leadership recognition of the importance of integration and provision of tangible support and resources are in uential in adoption and implementation of care integration [19][20][21][22][23][24]. In what ways does the health department incentivize or encourage integrated implementation at the clinic level?

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How have you used funding from the health department to support integrated implementation of EBIs?
· What in uence do policies and/or incentives (national quality incentive programs) have on improvement of integrated implementation of EBIs? · Does the health department provide your organization with funding for your role in supporting integrated implementation of EBIs in their clinic partners?
Information sharing · How is programmatic information, such as clinical or nancial information, shared between your program and other chronic disease programs with which you're collaborating at the health department? · How is information shared within clinics and health systems to support integrated implementation of EBIs?

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Thinking about the logistics of documentation-such as reporting requirements to the health department, HRSA, your health system, or other entities-have there been any challenges in terms of documentation or data reporting due to integrated implementation of EBIs? Any bene ts?

Nebraska
Integrated CRC screening within an EHR-based provider reminders system (clinical decision support rules) used for multiple screenings.
Used a FluFIT program to integrate CRC screening (FOBT kits or colonoscopy referral) with u shots.

Washington
Integrated CRC screening within EHR-based patient and provider reminders that are used for multiple screenings.
Expanded interventions focused on reducing structural barriers (e.g., providing mobile mammography and transportation vouchers) to include barriers for CRC screening (e.g., mailing FIT kits to patients due for CRC screening).

Kentucky
Integrated CRC screening into an existing patient reminder system (i.e., phone calls to remind patients about need for CRC screening, other cancer screenings).
Reduced structural barriers for CRC screening by including screening as part of "max packing" appointments that also included u shots and/or mammograms.
Note: CRC, colorectal cancer; EHR, electronic health record; FIT, fecal immunochemical test; FOBT, fecal occult blood test. Figure 1 Tenets of the Colorectal Cancer Control Program Methodological Approach