Abstract
Objectives:
Supporting medically underserved and socially disadvantaged populations, particularly in relation to cervical cancer, requires identifying coordination gaps. However, approaches to address the cervical cancer screening process between cancer centers and safety-net settings of care (hereinafter, safety-net settings) are poorly understood. We describe interactions and identify opportunities to guide cancer centers that aim to strengthen cervical cancer prevention, screening, and treatment for patients referred to them from safety-net settings.
Methods:
We administered a 15-item online survey from January 12 through February 9, 2022, to National Cancer Institute (NCI) cancer centers; the intended audience was associate directors of community outreach and engagement and/or associate directors of population sciences. Of 64 eligible cancer centers, 47 (73.4%) completed the survey; however, 7 cancer centers were excluded from analysis because they reported not having a formal arrangement with safety-net settings. We developed survey items in consultation with subject matter experts and conducted pilot testing before administration to sites.
Results:
The most common forms of partnership between NCI cancer centers and safety-net settings were referrals and consultations (34 of 40; 85.0%). We identified multilevel barriers affecting coordination and follow-up of abnormal cervical cancer screening test results. Communication between safety-net settings and cancer center staff was the most reported systems-level challenge to care coordination (35 of 40; 87.2%). Collection and synthesis of patient data presented the primary systems-level challenge to following up to abnormal cancer screening (34 of 40; 85.0%).
Conclusions:
Collaborations between cancer centers and safety-net settings are common but limited by challenges in care delivery and coordination. Our findings underscore the importance of identifying intervention points to optimize the management of cervical cancer care for patients in safety-net settings.
Cervical cancer prevention, screening, and treatment present important public health challenges, particularly for medically underserved and socially disadvantaged populations in the United States.1-4 Despite advances in all 3 areas, these populations have disproportionate morbidity and mortality from cervical cancer. 2 Contributing factors include limited access to cancer prevention, screening, and treatment services; low levels of health literacy; cultural and linguistic barriers; and socioeconomics. 5
Safety-net settings, such as federally qualified health centers, play a crucial role in reducing health disparities by providing care regardless of patients’ ability to pay. They mainly deliver primary care (88.2%), provide care to special populations (82.4%), and offer supportive services, including patient navigation (61.8%) and financial navigation services (44.1%). These settings also provide essential cancer screening services, particularly free services, under the 2010 Patient Protection and Affordable Care Act.6-8 However, many safety-net settings rely on partnerships with National Cancer Institute (NCI)–designated cancer centers for postscreening services, consultations, and access to therapeutic treatments, highlighting the critical nature of these collaborations.
To learn more about the role of cancer centers in caring for medically underserved and socially disadvantaged populations, NCI, in partnership with the Federal Cervical Cancer Collaborative (FCCC), led the development and dissemination of a survey. 9 One goal of the FCCC is to strengthen partnerships between NCI-designated cancer centers and clinical cancer centers 10 and safety-net settings, such as federally qualified health centers, which have been recognized as a promising approach to ending inequities in cervical cancer morbidity and mortality.11,12 However, the level of collaboration between these 2 groups and how they coordinate cervical cancer screening and related follow-up services are poorly understood. Identifying common barriers, opportunities, and issues faced by NCI cancer centers in supporting medically underserved and socially disadvantaged populations from safety-net settings may help increase equitable follow-up care for cervical cancer screening abnormalities and treatment.
To this end, NCI led a survey of NCI cancer centers to understand the current level of collaboration between NCI cancer centers and safety-net settings and to understand how they coordinate cervical cancer screening services to meet the needs of medically disadvantaged populations. The findings will inform policy and practice to improve cervical cancer outcomes for these populations.
Methods
To begin to understand the interactions between cancer centers and safety-net settings, NCI researchers developed a survey instrument in collaboration with FCCC partners and offered it as an online link to associate directors at NCI cancer centers. NCI managed and analyzed responses with support from an external contracting organization, ICF International.
Study Procedures
We sent a survey announcement followed by invitations to associate directors of community outreach and engagement and/or associate directors of population sciences at 64 NCI cancer centers in January 2022. We excluded 7 centers because of their exclusive focus on preclinical laboratory research. We sent personalized email invitations to each center’s associate director. To gather accurate and complete information, we encouraged respondents to consult others at their institution; each center completed a single survey. We sent nonrespondents up to 4 emails and 2 telephone reminders during the data collection period and were offered a 1-week extension. We provided no honorarium. We sent a summary report to all NCI cancer centers. The ICF International Institutional Review Board determined this study was exempt from human subjects’ review because it posed minimal risk to participants.
Survey Instrument
We developed an online survey to assess NCI cancer centers’ interactions with safety-net settings and determine patterns of care related to cervical cancer management. The survey had 15 multiple-choice and open-ended questions and incorporated skip logic, which allowed different response frequencies based on participant relevance to certain items. We developed the survey in consultation with external subject matter experts from NCI’s grants portfolio, NCI cancer center staff, and selected members of the FCCC. The initial version of the survey was refined through cognitive interviews and pilot tests (Supplementary Material, Survey Instrument available online). 9 We used an online survey platform (Voxco) to create and administer the survey.
Measures
For the purposes of this survey, collaboration refers to NCI cancer centers and safety-net settings working together and sharing resources to provide cervical cancer screening services. Safety-net settings refer to community-based health care settings that provide health care services in medically underserved areas. Survey items examined partnerships and interactions with safety-net settings. Respondents described the formality of their partnerships and characterized ways NCI cancer centers collaborate with safety-net settings (Supplementary Material). 9 We also asked respondents about specific population services they provide (eg, interpretation and outreach services) and population needs (eg, childcare, housing, transportation) and whether these services are provided by external organizations with which they collaborate. We also asked about their response to special population needs (eg, individuals experiencing homelessness, people with HIV/AIDS, immigrant populations) and plans for strengthening services using current resources (eg, partnering with nonhealth community organizations, improving transparency of treatment costs, creating additional tools or resources to enhance cancer screening uptake). We assessed priorities for strengthening services by asking respondents which approaches they would modify if additional funding were available for their center. We assessed barriers across the patient, clinician, and health care system levels related to follow-up on abnormal cancer screening test results and coordination with safety-net settings. Lastly, we asked respondents to specify services offered related to abnormal cervical cancer screening test results. We then asked respondents to estimate what percentage of patients with an abnormal cervical cancer screening test result were referred from a safety-net setting and how they follow up with safety-net settings regarding patients referred with an abnormal cervical cancer screening test result.
Analysis
We generated frequencies and percentages for each question by using SAS version 9.4 (SAS Institute Inc). We analyzed data based on the total number of respondents while accounting for nonresponses because of survey design, which used skip logic for certain questions. Most respondents completed the entire survey, although a few NCI cancer centers responded only to questions pertaining to partnerships with safety-net settings, omitting items related to cervical cancer control services. Our analysis focused on reporting the items most relevant to recent FCCC/NCI activities and priorities, excluding items not directly related to these efforts.
Results
Forty-seven of 64 (73.4%) NCI cancer centers responded to the survey. Most NCI cancer centers reported having a formal arrangement with at least 1 safety-net setting (68.1%; 32 of 47), 2.1% (1 of 47) reported no longer having a formal arrangement, and 14.9% (7 of 47) did not know how to describe the partnership between their cancer center and safety-net settings of care. The 7 NCI cancer centers that reported not having a formal arrangement were ineligible to complete the rest of the survey and were redirected to a thank-you message (14.9%; 7 of 47).
General Relationships
Of the 40 respondents, NCI cancer centers primarily partnered with safety-net settings through referrals and consultations 85.0% (n = 34). Most partnership activities involved research collaborations (77.5%; n = 31) and community outreach (72.5%; n = 29) (Table 1). Safety-net settings played a crucial role in delivering primary care (88.2%; 30 of 34) and providing services to special populations (82.4%; 28 of 34) (Table 2), particularly those with limited access to health care because of socioeconomic challenges. Additional services were offered by these settings, such as patient navigation (61.8%; 21 of 34) and financial navigation services (44.1%; 15 of 34). While less common, these services were identified as important for addressing barriers to timely follow-up care after cervical cancer screening. The variability in services across settings was noted (Table 2).
Results of a survey question among NCI cancer centers on how cancer centers partner with safety-net settings to strengthen cervical cancer prevention, screening, and treatment, United States, 2022 a
Abbreviation: NCI, National Cancer Institute.
The authors administered a 15-item online survey to associate directors at 64 NCI cancer centers from January 12 through February 9, 2022; 47 respondents completed the survey. Of these, 7 reported not having a formal arrangement with ≥1 safety-net setting and were excluded.
Values total to >100% because respondents were instructed to select all that apply.
Results of a survey question among NCI cancer centers on the role of safety-net settings in cervical cancer prevention, screening, and treatment, United States, 2022 a
Abbreviation: NCI, National Cancer Institute.
The authors administered a 15-item online survey to associate directors at 64 NCI cancer centers from January 12 through February 9, 2022; 47 respondents completed the survey. Of these, 7 reported not having a formal arrangement with ≥1 safety-net setting and were excluded. Of the 40 eligible respondents, 34 answered this question.
Values total to >100% because respondents were instructed to select all that apply.
Challenges to Follow-up and Coordination of Care
Respondents identified barriers to follow-up of abnormal cancer screening and coordinating care between cancer centers and safety-net settings at the patient, clinician, and system level. Each surveyed barrier was identified by at least 65.0% (26 of 40) of respondents (Figure).
Patient, clinician, and systems-level challenges reported by cancer center staff in coordinating care for patients from safety-net settings, United States, 2022.
Challenges to following up on abnormal cervical cancer screening test results at the patient level included transportation (97.5%; 39 of 40), caregiving responsibilities (95.0%; 38 of 40), health literacy (95.0%; 38 of 40), comorbidities (90.0%; 36 of 40), and patients’ busy schedules (87.5%; 35 of 40). At the clinician level, communication with patients and caregivers was the most reported challenge (87.5%; 35 of 40).
NCI cancer centers reported systems-level barriers less frequently than patient or clinician-level barriers. The main challenges related to coordination of care were communication between safety-net settings and cancer center staff (87.2%; 35 of 40), collection and synthesis of pertinent patient data (82.5%; 33 of 40) (eg, prior screening and test results), and interoperable electronic referral pathways between cancer centers and safety-net settings (77.5%; 31 of 40). Challenges to following up on abnormal cancer screening included collection and synthesis of patient data (85.0%; 34 of 40), budgetary concerns (eg, limited cancer center budgets) (82.5%; 33 of 40), and reimbursement levels for care (72.5%; 29 of 40). Communication challenges included technology (75.0%; 30 of 40) (eg, interoperable electronic referral pathways between cancer centers and safety-net settings) and staff (70.0%; 28 of 40) (eg, communication between safety-net settings and cancer center staff).
Cervical Cancer Referral Challenges
When asked to quantify the number of referrals from safety-net settings after the identification of an abnormal cervical cancer screening test result (Table 3), 16 of 37 (43.2%) cancer centers were unaware or responded “I don’t know.” Nine cancer centers (24.3%) indicated receiving at least 75% of referrals for abnormal screening follow-up from safety-net settings. Patients were referred to cancer centers primarily through a call line or telephone call (91.9%; 34 of 37), followed by email (59.5%; 22 of 37), electronic health records (54.1%; 20 of 37), and interoperable patient portals (16.2%; 6 of 37). In response to how cancer centers follow up with patients who have an abnormal cervical cancer screening test result and are referred from safety-net settings, 81.1% (30 of 37) reported that they send reminders for postscreening follow-up appointments and 72.9% (27 of 37) send patients reminders for posttreatment follow-up appointments (Table 4). Fewer NCI cancer centers reported offering open-access scheduling (13.5%; 5 of 37) or evening or weekend clinic access (5.4%; 2 of 37).
Results of survey questions among NCI cancer centers on processes for referring patients with abnormal cervical cancer screening test results from safety-net settings to cancer centers, United States, 2022 a
Abbreviation: NCI, National Cancer Institute.
The authors administered a 15-item online survey to associate directors at 64 NCI cancer centers from January 12 through February 9, 2022; 47 respondents completed the survey. Of these, 7 reported not having a formal arrangement with ≥1 safety-net setting and were excluded. Of the 40 eligible respondents, 37 answered this question.
Results of a survey question among NCI cancer centers on how cancer centers follow up with patients referred from safety-net settings, United States, 2022 a
Abbreviation: NCI, National Cancer Institute.
The authors administered a 15-item online survey to associate directors at 64 NCI cancer centers from January 12 through February 9, 2022; 47 respondents completed the survey. Of these, 7 reported not having a formal arrangement with ≥1 safety-net setting and were excluded. Of the 40 eligible respondents, 37 answered this question.
Values total to >100% because respondents were instructed to select all that apply.
Discussion
To our knowledge, this survey is the first to examine formal partnerships and types of interactions between NCI cancer centers and safety-net settings. Our findings reveal that most cancer centers have formal arrangements in place with at least 1 safety-net setting, including written agreements or signed contracts. These partnerships predominantly revolve around referrals/consultations, research collaborations, and collaborative community outreach initiatives. Furthermore, our research highlights the integral role of safety-net settings in providing primary care services and extending their reach to special populations.
Building on our understanding of NCI cancer centers’ engagement with safety-net settings and their proactive strategies to enhance collaboration, we also examined their patient engagement efforts. NCI cancer centers use various methods to ensure continuity for patients referred from safety-net settings, including patient reminders for postscreening and posttreatment follow-up appointments. Nevertheless, effective patient-level follow-up faces hurdles, including caregiving responsibilities, transportation limitations, and extended travel times.
Findings of this study align with earlier work highlighting challenges in care coordination between cancer centers and safety-net settings and the reliance on patient navigation services.13,14 These challenges contribute to missed opportunities for follow-up care, delays in diagnosis and treatment, and reduced screening rates, particularly in rural or medically underserved areas. Given the importance of patient navigation in addressing these systemic barriers, NCI cancer centers continue to provide essential services, emphasizing the importance of facilitating a seamless transition between settings, particularly in the face of transportation and caregiving challenges.
Socially, socioeconomically, and medically disadvantaged groups are more likely than those from a higher socioeconomic strata to have low functional health literacy levels and are underscreened for cervical cancer.15,16 Aligning with these findings, our study revealed that health literacy was the most commonly identified patient-level barrier to coordination among patients referred from safety-net settings. Long understood to present care challenges, health literacy should be readily amendable to intervention in care delivery settings. For example, engaging patient navigators to assist patients with low levels of literacy and developing cultural and literacy-tailored messages aligned with the needs of catchment area populations can improve patient outcomes. Health system strategies to address social risk factors could also be informed by the Addressing Social Risk Factors in Cancer Care Delivery Report. 17
Our study found that a high proportion of NCI cancer centers were unaware of the proportion of patients who were referred to their center for follow-up care after an abnormal cervical cancer screening test result from a safety-net setting. The reasons for this knowledge gap are unclear; however, NCI cancer centers indicated that patients from safety-net settings are primarily referred for follow-up care through telephone calls, with fewer referrals through interoperable patient portals. Similarly, most NCI cancer centers cited a lack of interoperable electronic referral pathways between cancer centers and safety-net settings as a challenge to follow-up and care coordination. Taken together, these findings suggest that increasing the interoperability of referral pathways between cancer centers and safety-net institutions may improve communication and comprehensive patient care.
The issue of interoperability continues to be a national priority in efforts to enhance cancer screening and prevention, particularly in medically underserved communities. Federal and state agencies, along with academic and health system partners, are advancing initiatives to improve virtual care infrastructure, streamline health information technology workflows, and strengthen coordination of care and referrals. These efforts are critical to achieving access to timely and effective cervical cancer screening, especially in care settings where populations face structural barriers to care.
In addition, the NCI’s Persistent Poverty Initiative will establish 5 centers for cancer control research in locations identified as persistent poverty areas. 18 This initiative is critical to addressing institutional and structural factors related to cancer care. Federal funding also supports a partnership between the University of Southern California Norris Cancer Center and the Chinatown Service Center to establish referral pathways to reducing the time from screening to diagnosis and follow-up. 19
NCI cancer centers reported challenges contributing to inadequate communication between safety-net settings and cancer center staff. Improving communication is essential for ensuring care coordination and optimal outcomes for cancer patients. Created in 2004, the Office of the National Coordinator for Health Information Technology (ONC) supports interconnected data infrastructure, enhances access to health and social services, and fosters a whole-of-government approach for enhancing population health and well-being. 20 Recently, the ONC launched the “CancerX” National Innovation Accelerator Initiative to develop tools, such as digital solutions for improved cancer patient care coordination and communication and new software technology to address patients’ social needs in posttreatment care. 21
The FCCC recently disseminated 2 new resources to strengthen approaches to reduce cervical cancer disparities in safety-net settings: (1) a federal opportunities report that identifies further opportunities to address social and structural issues to reduce cervical cancer in safety-net settings and (2) a safety-net provider toolkit of resources and tools to support diverse patient engagement and adherence to human papillomavirus vaccine uptake, screening, and management guidelines.22,23 In addition, research partners of the FCCC are actively engaged in research initiatives aimed at mitigating cervical cancer disparities among medically underserved and socially disadvantaged populations.
While this study primarily focused on cervical cancer screening, its insights into barriers and opportunities related to cervical cancer care can inform similar partnerships in other areas of cancer prevention and early detection including breast and colorectal cancer screening. Strengthening existing partnerships is crucial for meeting the current and future guidelines in cancer screening for underinsured or uninsured populations. 24
Limitations
This study had several limitations. First, the study primarily reflects the perspectives of staff at NCI cancer centers, and safety-net settings were not included in the survey. Including these settings would have required a separate approval and survey administration process, extending up to 3 years, and the cost was beyond our budget. Future research may benefit from including safety-net settings to capture a more comprehensive view of coordination gaps and enhance care quality for the medically underserved and socially disadvantaged populations served by NCI cancer centers and safety-net settings. Second, patient-level barriers were reported based on survey respondent perspectives; however, patient perspectives may differ. We were therefore unable to externally validate survey responses with either safety-net settings or patients.
Third, we excluded some survey items from the final analysis because of their limited relevance to the study’s focus on NCI cancer centers’ partnerships with safety-net settings. Fourth, the survey’s skip logic, while essential for tailoring relevant questions to respondents, led to some variability in response frequencies, thereby limiting comprehensive comparisons across certain survey items. Fifth, 1 NCI cancer center described itself as a matrix center and noted its partnership between the university and 2 health systems. Because the 2 health systems were distinct, the participant requested that the health systems complete 2 separate surveys. As a result, this matrix NCI cancer center is represented twice. The sample may have included other matrix centers that did not request more than 1 survey. Sixth, data constraints limited information on the referral process and outcomes, especially regarding the average number of abnormal cervical cancer referrals and follow-up from safety-net settings to NCI cancer centers. To mitigate potential biases, our recruitment materials emphasized that survey responses would not affect current or future funding from NCI.
Conclusions
This study provides a comprehensive assessment of barriers and opportunities in the engagement and partnership between NCI cancer centers and safety-net settings. Our findings shed light on the challenges faced in establishing effective collaborations between these entities. While this study focused on the ability to coordinate cervical cancer screening and follow-up services across NCI cancer centers and safety-net settings, the findings may have broader implications for the management of other cancer screening services, such as colorectal and lung cancer screening. To strengthen approaches to cervical cancer screening, prevention, and treatment and ensure timely and appropriate care, future research should prioritize addressing limitations in current models of care and collaboration. Exploring novel communication methods for patient reminders in future studies has the potential to unlock valuable insights, optimizing patient engagement and follow-up. Strengthening formal arrangements and interoperability between safety-net settings and NCI cancer centers presents opportunities to improve cervical cancer screening, treatment, and management and eliminate cancer-related health care disparities.
Supplemental Material
sj-docx-1-phr-10.1177_00333549251316190 – Supplemental material for Cervical Cancer Screening Collaborations Between National Cancer Institute Cancer Centers and Safety-Net Settings of Care, 2022
Supplemental material, sj-docx-1-phr-10.1177_00333549251316190 for Cervical Cancer Screening Collaborations Between National Cancer Institute Cancer Centers and Safety-Net Settings of Care, 2022 by Veronica Y. Chollette, Blair H. Altman, Jennifer K. McGee-Avila, Emily M. Grenen, Paul B. Jacobsen and Sarah Kobrin in Public Health Reports
Footnotes
Acknowledgements
The authors thank Henry Ciolino, PhD, director of the Office of Cancer Centers at the National Cancer Institute, for his invaluable guidance and support in the successful administration of the survey to NCI cancer centers. Dr. Ciolino’s insights played a pivotal role in ensuring the quality and effectiveness of our research project. We are deeply appreciative of his commitment to advancing cancer research and his dedication to our study’s success.
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Disclaimer
This article was produced by employees of the US government as part of their official duties. The findings and conclusions are those of the authors and do not necessarily represent the official position of the National Institutes of Health, National Cancer Institute, National Institute on Minority Health and Health Disparities, or other federal agencies.
Supplemental Material
Supplemental material for this article is available online. The authors have provided these supplemental materials to give readers additional information about their work. These materials have not been edited or formatted by Public Health Reports’s scientific editors and, thus, may not conform to the guidelines of the AMA Manual of Style, 11th Edition.
References
Supplementary Material
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