Use of Community Health Workers and Patient Navigators to Improve Cancer Outcomes Among Patients Served by Federally Qualified Health Centers: A Systematic Literature Review

Abstract Introduction: In the United States, disparities in cancer screening, morbidity, and mortality are well documented, and often are related to race/ethnicity and socioeconomic indicators including income, education, and healthcare access. Public health approaches that address social determinants of health have the greatest potential public health benefit, and can positively impact health disparities. As public health interventions, community health workers (CHWs), and patient navigators (PNs) work to address disparities and improve cancer outcomes through education, connecting patients to and navigating them through the healthcare system, supporting patient adherence to screening and diagnostic services, and providing social support and linkages to financial and community resources. Clinical settings, such as federally qualified health centers (FQHCs) are mandated to provide care to medically underserved communities, and thus are also valuable in the effort to address health disparities. We conducted a systematic literature review to identify studies of cancer-related CHW/PN interventions in FQHCs, and to describe the components and characteristics of those interventions in order to guide future intervention development and evaluation. Method: We searched five databases for peer-reviewed CHW/PN intervention studies conducted in partnership with FQHCs with a focus on cancer, carried out in the United States, and published in English between January 1990 and December 2013. Results: We identified 24 articles, all reporting positive outcomes of CHW/PNs interventions in FQHCs. CHW/PN interventions most commonly promoted breast, cervical, or colorectal cancer screening and/or referral for diagnostic resolution. Studies were supported largely through federal funding. Partnerships with academic institutions and community-based organizations provided support and helped develop capacity among FQHC clinic leadership and community members. Discussion: Both the FQHC system and CHW/PNs were borne from the need to address persistent, complex health disparities among medically underserved communities. Our findings support the effectiveness of CHW/PN programs to improve completion and timeliness of breast, cervical, and colorectal cancer screening in FQHCs, and highlight intervention components useful to design and sustainability.


Introduction
In the United States, disparities in cancer screening, diagnosis, time to treatment, and morbidity and mortality are well documented, and often are related to an individual's race/ethnicity, income, education, and healthcare access. 1,2 To address health disparities, public health approaches that consider the physical, social, cultural, organizational, community, economic, legal, or policy contexts within which people live have the greatest potential benefit. [3][4][5] Specifically, increasing access to quality healthcare for the medically underserved and increasing the capacity of the prevention workforce are key recommendations to effectively address health disparities and achieve health equity. 4,[6][7][8] Community health workers (CHWs) and patient navigators (PNs) are members of the prevention workforce who increase access to care for the medically underserved. [8][9][10] A CHW is a nonclinical, frontline, public health worker who is a trusted member and/or has an unusually close understanding of the community served, and can function to bridge the gap between an individual and the healthcare system. 11 CHWs are also commonly referred to as promotores de salud, community health representatives, community health advisors, lay health educators, and lay health advisors, among other titles. 12 The PN role was originally developed in the early 1990s to address cancer disparities by reducing barriers to timely breast cancer diagnosis and treatment among poor women in Harlem. Since that time, the scope of PNs has expanded across several cancers and the entire cancer spectrum from prevention, detection, diagnosis, treatment, and survivorship to the end of life. 13 Today, both CHWs and PNs work to address health disparities across many chronic diseases, and improve health by providing education and advocacy services, addressing individuals' barriers to care, and linking and navigating patients through the healthcare system, and to financial and community resources. CHW/PN efforts have led to increases in cancer screening and timely completion of diagnostic follow-up and cancer treatment initiation. [14][15][16] Federally qualified health centers (FQHCs) are legislatively mandated to provide primary care for medically underserved communities, and thus are ideal settings for CHW/PN interventions. The U.S. Department of Health and Human Services' Health Resources and Services Administration (HRSA) currently funds *1300 FQHCs serving over 22 million patients annually. 17 FQHCs are critical to addressing cancer disparities among the med-ically underserved in the United States, 18,19 as FQHC patients often are at greater risk for developing cancer and experiencing worse cancer outcomes compared with the general U.S. population. 2 The Affordable Care Act (ACA) established the Community Health Center Fund, providing $11 billion over a 5-year period (2011-2015) for the operation, expansion, and construction of health centers. 20,21 Consequently, FQHCs as safety-net healthcare organizations have been increasingly responsible for providing crucial primary care services for vulnerable populations. 22 Beyond expanding FQHCs, ACA requires that most insurance plans provide certain in-network preventive health services, including breast, cervical, and colorectal cancer screening, at no cost to patients when obtained in-network. CHW/PN programs can facilitate prevention activities and can help the newly insured and others gain access to primary care and complete cancer screening. 19 CHW/PN programs and FQHCs are natural allies. However, little has been systematically documented about the effectiveness of CHW/PN programs conducted in FQHCs for cancer prevention and control. Therefore, we conducted a systematic review of the peer-reviewed literature to identify studies of cancerrelated CHW/PN interventions conducted in FQHCs and other HRSA-funded community health centers, and FQHC Look-Alike clinics. FQHC Look-Alikes share a mission with FQHCs to provide primary care to medically underserved communities and are eligible for FQHC reimbursement structures and discounted drug pricing, but are not funded by HRSA and therefore cannot be called FQHCs (https://bphc.hrsa.gov/ programopportunities/lookalike). Our objectives were to first identify studies that evaluated the effectiveness of these interventions in addressing cancer prevention and control disparities among the medically underserved (e.g., increasing screening, reducing time to diagnosis and treatment, reducing barriers to care) and to subsequently describe the components and characteristics of those interventions to guide future intervention development and evaluation.

Methods
In January 2014, we searched five databases: PubMed/ Medline, Scopus, Web of Science, CINAHL (Cumulative Index to Nursing and Allied Health Literature), and PsychINFO. Search terms utilized were based upon previous research 19, [23][24][25] and organized into three categories: (1) position/role, (2) clinical setting, and (3) disease focus (Table 1). We limited the search Time to diagnosis and diagnostic resolution for cervical and breast cancer (1) Navigated women had significantly shorter time to diagnosis than controls ( p = 0.003) and were more likely to achieve diagnostic resolution.
(2) Among women whose abnormal breast cancer test was resolved after 60 days, navigated women had significantly shorter time to diagnosis than controls ( p = 0.019     Mammography screening rates (claims data) After adjusting for age, income, urban versus rural location, disability, and insurance type, women exposed to the promotora intervention had a significantly higher increase in biennial mammograms than did women exposed to the printed intervention ( p = 0.03).
Warren-Mears et al. 49 Clinic and community to articles published in English between January 1990 and December 2013. A total of 495 articles were identified. Upon initial review, 58 articles were excluded because they were not original research (e.g., general descriptions of patient navigation, commentaries, editorials, book reviews, systematic literature reviews). Two coauthors independently reviewed the remaining articles (abstract and/or full-text), applying the following additional inclusion criteria: (1) U.S. study of CHW/PN intervention with results, (2) conducted in an FQHC or in partnership with an FQHC (including HRSAfunded nurse managed health clinics and community health centers, FQHC Look-Alikes and other health centers that do not receive HRSA funding but provide comprehensive primary healthcare services to medically underserved populations, and Indian Health Service clinics), and (3) focused on cancer. Discrepancies in assessment between the two reviewers were resolved through discussion, instead of a third reviewer. The two reviewers were subject matter experts and principle investigators of the study, and therefore best suited to discuss nuance of an individual article and come to a consensus of its relevancy. An objective third reviewer may not have had the subject matter expertise or the intimate understanding of the study to make a clear judgement about the relevancy of an article.
Of the 495 articles identified by the original searches, 19 met all inclusion criteria. A second tier search examined the bibliographies of the 19 identified articles, along with the bibliographies of published systematic literature review articles identified in the original search (excluded because they were not original research studies). From this secondary search, 85 additional potentially relevant articles were identified and reviewed by the two reviewers using the criteria noted above. Of these, five met the inclusion criteria (Fig. 1). In total, we identified 24 articles as relevant to this review.
Data from relevant articles were abstracted by the two coauthors. Abstracted data included study details (design, data collection method, outcomes and results, and funding source); cancer focus; study setting (HRSA affiliation of clinic, clinic type, clinic name, and number of clinics involved in study); CHW/PN position information (role/title, education/training, whether paid or volunteer, whether full-time or part-time, funding source for position, whether demographically matched to target population, goals for the position, activities conducted, location of activities, method of communi-cation with client, interaction with data systems, supervision, level of integration into medical team); broader intervention information (collaboration or partnerships, program barriers and facilitators, and relevant program policies); and intervention target population information (gender, age, race/ethnicity, rural/urban). Discrepancies in abstracted data were discussed until resolution was achieved.
Partnerships are often recognized as essential in the development and implementation of CHW/PN programs. Some studies included in this review partnered with CDC's National Breast and Cervical Cancer Early Detection Program to facilitate patients' referral to screening services. 34,[37][38][39]44,46 Other studies involved partnerships with a Community Advisory Panel to monitor and facilitate the community-based research process, 26 academic researchers, and community members to develop study methods and conduct analysis, 29,37 churches, the state department of public health, and the health center to host the sites of intervention activities, 44 and a nonprofit organization to cover costs for navigators and colonoscopies. 30 One intervention study was conducted by a coalition of community activists, public health officials, academic researchers, and the Boston Public Health Commission 27,28 (data not included in a table).

Study results
All but two studies reported statistically significant positive outcomes from the CHW/PN interventions ( p £ 0.05). One RCT that found a 35% increase in rescreening in the intervention group but reported nonsignificant confidence intervals (RR = 1.35, 95% CI: 0.95-1.92), 40 and one quasi-experimental trial identified increased mammography rates in the interven-tion group, but the increases were not significant when compared to controls ( p ‡ 0.07). 47 While all studies were conducted among subpopulations that may experience cancer disparities or barriers to care, some studies specifically targeted under-screened or never screened individuals, or those with abnormal cancer screening tests.
The studies included in this review were largely supported through federal funding and led by academic institutions. The controlled research environment allows investigators to examine the impact of CHW/PN interventions on screening and diagnostic outcomes in FQHC patients, but these controlled environments often do not reflect the strained reality of real-world CHW/PN programs where resources, training, supervision, and support are often less robust than in federally funded studies. A significant programmatic barrier to the integration of CHWs/PNs into most FQHCs is that CHW/PN services are not billable or reimbursable. 56,57 Safety net institutions, like FQHCs, which serve populations with limited resources to support themselves and their families when cancer is diagnosed, are unlikely to have sufficient resources for CHW/PN programs and interventions (although it has occurred). On the contrary, health systems targeting and caring for insured, employed, and educated patients are more likely to have cancer patient navigation programs. 58 Ongoing cost-analysis studies and healthcare utilization studies of chronic disease CHW/PN programs are critical, 59 have documented costs and healthcare savings when CHWs are utilized, and may provide evidence of the value of sustainable funding for these services in clinical settings serving the medically underserved. [60][61][62] In addition to sustainable funding strategies, inconsistent training and nonuniform competency standards have been recognized as barriers to broader integration of CHW/PNs into public health programs. 14,51 This study found that training content and educational/professional background varied for each of these studies, and that aspects of occupational regulation critical to establishing credibility and scope of practice, such CHW/PN supervision, integration the into the medical team, paid or volunteer status, and part-time or full-time status, were not as often discussed.

Noted barriers and facilitators to FQHC-affiliated CHW/PN programs
Barriers reported in the literature should be considered when conducting future intervention research. For patients, the inability to take time off work to attend screening, lack of reliable transportation and childcare, and cost of copayments 43 ; housing concerns and instability 27,32,33 ; and migrant or immigrant status 32,33 were noted as impediments to participating in screening. Barriers faced by programs and health centers that may impact program outcomes include the inability to retain skilled bilingual PNs 47 ; lack of onsite mammography 27 ; framing a navigation program for ''cancer patients'' 49 ; and the paper records and the inability to track screening tests conducted outside the clinic. 49 Several facilitators to implementation of CHW/PN interventions in FQHCs were reported, and include partnering with churches when working with Hispanic communities, 43 ensuring a common language is spoken between CHWs/PNs and their clients, 48 ensuring open communication between clinicians and PNs working in the clinic, 32,35 incorporating Community Guiderecommended strategies into the CHW/PN intervention, 32 allowing CHWs/PNs flexible work hours and scheduling, 32 supporting initial and ongoing training, 26 allowing CHW/PN access to EHRs, 30 providing reducedcost screening, 35 promoting multiple types of screening exams at one time, 40 incorporating a community advisory panel into CHW/PN program activities, 26 and facilitating access follow-up care through National Breast and Cervical Cancer Early Detection Program (NBCCEDP). 34

Policy implications
Numerous policy initiatives light the path forward for the integration of CHW/PNs into primary care and public health. Effective January 2014, CMS created a final rule (CMS-2334-F) that opens up payment opportunities for preventive services by nonlicensed individuals (e.g., CHWs) recommended by physicians or other licensed practitioners of the health arts. 63 The rule change presents an important opportunity for enhancing the focus on prevention through the Medicaid program. 64 ACA also offers state Medicaid programs the opportunity to create Health Homes for beneficiaries living with chronic illness, and several states have Medicaid state plan amendments that explicitly include or refer to CHWs 59,64-66 Finally, ACA creates funding for state innovation models (SIM) designed to support states in the development and testing of state-based models for multi-payer payment and healthcare delivery system transformation. 67 Of six states currently implementing their SIM designs, four have included CHWs in their plans. In Round One of the SIM initiative, nearly $300 million was awarded to 25 states to design or test improvements to their public and private health payment and delivery systems (https:// innovation.cms.gov/initiatives/state-innovations/). 64 Another opportunity to support integration of CHWs/ PNs into FQHCs and other community-based primary care setting is the patient-centered medical home model. [68][69][70] The patient-centered medical home is a way of organizing primary care that emphasizes care coordination and communication, treatment of the many needs of patients at the same time, increased access to care, and empowerment of patients to be partners in their own care. The development of a CHW/PN program in a health center may assist in meeting the requirements for patient-centered medical home designation. 71 Strengths and limitations. To our knowledge, there has been no assessment of CHW and PN activities in FQHCs on a national, state, or local scale. The results of this systematic literature review provide an overview regarding cancer prevention and diagnostic CHW/PN programs in FQHCs targeting the medically underserved that can be used to design future interventions. We note several limitations to our systematic literature review methods and results. Studies were limited to those published in the peer-reviewed literature. This may have limited study to those conducted by or in partnership with academic researchers. The peerreview literature does not capture all CHW/PN activities ongoing at FQHCs as programs may not have the capacity to effectively evaluate and publish their work, and FQHC-designation may not have been included in the study site description. The studies included in this review varied in design and methodology (RCTs, quasiexperimental trials, and pre-post comparison) and the impact of those variations to study outcomes was not assessed, but should be acknowledged when interpreting the results of this literature review. Additionally, the reporting period for this review ended in December 2013, potentially excluding additional literature relevant to the search.

Conclusion
Better partnering and integration of public health and primary care interventions and systems can change the context within which chronic disease occurs and reduce health disparities. As evident in this review, CHW/PN interventions implemented in FQHCs or coordinated with FQHCs are effective in increasing cancer screening and the timeliness of diagnostic resolution among medically underserved populations. Bridging the community-clinical divide is critical to supporting disadvantaged communities to gain access to primary care, including cancer screening. Although evidence supports engaging CHW/PNs in the national health delivery system, lack of sustainable resources for these programs, including reimbursement for services, remains a challenge. Local, regional, and state programs will likely need to continue innovating and collaborating to develop and sustain systems and programs for the medically underserved in their communities. Looking forward, national public health agencies must continue to promote the development and adoption of evidence-based interventions and strategies that will reduce health disparities. Achieving health equity in cancer and other chronic diseases is a real and pressing priority for public health, and fostering collaboration between CHWs/PN programs and FQHCs and other community-based settings is potentially a very powerful tool to achieve public health goals.