Background

The Institute of Medicine (IOM) and National Research Council 2005 report, From Cancer Patient to Cancer Survivor: Lost in Transition, recommends that patients with cancer who are completing treatment be “provided with a comprehensive care summary and follow-up plan that is clearly and effectively explained”[1]. The 2012 American College of Surgeons Commission on Cancer “Cancer Program Standards: Ensuring Patient Centered Care” requires the development and implementation of care transition plans for all cancer survivors as a standard of care [2]. According to this standard, the survivorship care plan (SCP) should contain a record of care received, disease characteristics, and follow-up plan.

Despite the IOM’s recommendation, few care organizations have instituted standard SCPs. In a study of 53 NCI- designated and comprehensive cancer centers, Salz and colleagues found that 23 of the 53 cancer centers (43%) used SCPs for their breast cancer survivors, colorectal cancer survivors, or both [3]. Of these 23 institutions, 17 (74%) reported using SCPs only for breast cancer survivors, 2 (9%) used SCPs only for colorectal cancer survivors, and 4 (17%) used SCPs for both groups of survivors. Survivors and primary care providers were reported to welcome SCPs in the context of comprehensive breast cancer care. However, a qualitative study that included breast cancer survivors, oncology specialists, and primary care providers found that while participants felt that written survivorship care plans could be helpful, they would be insufficient to ease the transition from oncology to primary care [4]. Assessment of SCPs in these studies did not address literacy level.

Much research has explored cultural differences in survivorship experience and meaning [5–10]. A growing literature is applying these understandings to the development and implementation of SCPs with the aim of infusing SCPs with the perspectives of patients [11–13]. To date, this research suggests that existing SCP templates fail to address the information needs of specific population groups or to be particularly useful to patients as they transition from oncology to primary care [11–14]. Some of this research suggests that health literacy may be an important mitigating factor. For example, health literacy has been associated with dissatisfaction and regret about breast cancer treatment among Latino women [15]; and inequality of access to cancer information, educational materials, and information about medication among African American breast cancer survivors [16]. Preliminary research conducted by colleagues at Olive View-UCLA Medical Center, with their low literacy, low English proficiency patient population, for example, revealed that 45% (n = 35) of patients did not remember being given a commonly used treatment summary developed by the American Society of Clinical Oncology (ASCO) (http://www.asco.org/institute-quality/breast-cancer-treatment-plan-and-summary-resources), and only 8.5% of those who had received the ASCO treatment summary had shown it to another provider [17]. We are aware of no research to date that explores survivorship information needs among safety-net breast cancer patients of multiple ethnicities and across multiple languages. Further, the link between these information needs and developing approaches to survivorship care plans is understudied.

This study emerged from a community-university collaboration established to address the lack of adequate and appropriately framed information for low income, low health literacy, and low English proficient breast cancer survivors transitioning from oncology to primary care. The San Francisco Women’s Cancer Network (SFWCN) is a group of organizations working toward the preservation of vital safety net programs, leading to the provision of a continuum of high quality, comprehensive, compassionate care for women with cancer. SFWCN members serve ethnically, linguistically and culturally diverse breast cancer survivors, the majority of whom have received care at San Francisco General Hospital (SFGH). SFWCN members identified the need for adequate information resources, and partnered with Mt. Zion Breast Cancer Center (BCC) and SFGH to identify a process to meet this need. SFGH was chosen as a partner because the majority of women served by SFWCN organizations received their care there, and Mt. Zion BCC because of their previously developed survivorship resources and expertise. The partnership came together with the understanding that survivorship transition challenges cut across all populations experiencing breast cancer and SFWCN members believed that low literacy SCP materials would benefit women across education levels.

The objective of our collaboration was to conduct inductive research to identify informational and structural challenges to treatment and survivorship for safety-net breast cancer patients that could inform the content and delivery of appropriate and useful SCPs. When we use the term safety net we refer to providers who offer services to patients regardless of ability to pay, and whose patient mix includes substantial numbers of uninsured, Medicaid, and other vulnerable patients [18]. We were particularly interested in identifying content and delivery preferences that would support the care transition from oncology to primary care and ongoing learning in survivorship for low literacy, multi-lingual patients. The study was designed to include the perspectives of both providers (e.g. oncologists, nurse practitioners, patient navigators, and social workers) and patients [19]. Herein we report findings from six focus groups conducted in English, Spanish, Cantonese, Russian, and Tagalog with women who were at least two years and no more than 15 years from their diagnosis.

Methods and Study Design

Our collaboration convened a meeting with SFWCN member organizations serving predominantly low health literacy African American, Latina, Chinese, Russian, Filipina, and White medically underserved breast cancer patients in the San Francisco Bay Area. In the initial meeting, SFWCN representatives explained the study, inclusion criteria, and worked with member organizations to establish acceptable expectations for each organization. These included providing a focus group facilitator, recruiting women who fit the inclusion criteria, providing space to conduct the focus group, and providing feedback on preliminary findings. Inclusion criteria were breast cancer diagnosis, low health literacy and/or low English proficiency (LEP), at least two years and no more than fifteen years since diagnosis, and self identify as African American, Latina, Chinese, Russian, White/Euro-American, or Filipina. The range of two to fifteen years allowed for a diverse range of perspectives on information needs at different points in the survivorship experience, but all post active treatment (e.g., chemotherapy and/or radiation). Conversations with Mt. Zion BCC providers (oncologist, nurse practitioner) identified multiple time-points (i.e., 2–3 years out, 5 years out, and 10–15 years out from diagnosis) as important transitional survivorship periods when inquiries about follow-up care after treatment and management of long-term side effects (e.g., lymphedema, post-mastectomy pain syndrome, chemo brain) emerge in both oncology and primary care settings.

We chose focus groups as our primary methodology because of its capability to elucidate cultural nuance and the comparative ease of sampling population subgroups. As research on the cultural dimensions of focus group methodology [20] and our own previous research [21–23] suggest, the group process allows people to listen and to formulate their views if they are not ready to do so initially. SFWCN member organizations recruited a convenience sample of 5 African American, 7 Latina, 9 Chinese, 4 Russian, 6 White, and 7 Filipina women for participation in six focus group interviews. To facilitate recruitment, participants were offered a small stipend ($40) for their time, effort, and travel expenses. Focus groups were separated by language (e.g. English, Spanish, Cantonese, Russian, or Tagalog) and race/ethnicity (e.g. African American, Latina, Chinese, Russian, Euro-American, and Filipina). These stratifications were driven by the community-based organizations facilitating the focus groups. For example, one SFWCN member organization provided cancer support to African American women, therefore they recruited participants from their members; another provided support to Filipinas and recruited participants from their members, and so on. Although focus groups were stratified by language and race/ethnicity, mixed race/ethnicity women were also invited to participate if they were both a client of the respective SFWCN member organization facilitating the focus group and were able to participate in the language in which the focus group was conducted.

Focus groups were facilitated by bilingual, bicultural community organization staff who had undergone a half-day training with the university partners. Focus group sessions were recorded with the explicit consent of participants. Participants signed a written consent form translated into their primary language (e.g. English, Spanish, Cantonese, Russian, or Tagalog) prior to the beginning of each focus group and completed a demographic questionnaire in which they self reported their ethnicity, age, stage at diagnosis, etc. While we originally intended to administer a health literacy measure, SFWCN members felt that such a measure was unnecessary and that, due to the low income and low education levels of their clients, administering such a measure would introduce a barrier to participation in open discussion. All research activity was reviewed and approved by the University of California, San Francisco Committee on Human Research. Professional transcriptionists translated and transcribed focus groups into English for coding and analysis [24]. To ensure consistency in meaning, bilingual research team members conducted spot checks of translated transcripts (e.g. listened to portions of the original audio recording while reading the translated portion).

Focus groups were conducted in community centers and community organization offices. The purpose of the groups was to generate discussion amongst group members about the transition to primary care (Sample question: Could you share your understanding of what was supposed to happen with your healthcare after treatment ended? What were your expectations?), access to information (Sample question: Can you tell me about the kinds of information you received when you left the breast clinic?), knowledge of treatment history (Sample question: Can you tell me how you keep track of your treatment history? Who has helped?), and perspectives on SCPs (Sample question: What should be included in an SCP? When should it be provided?)

We followed standard qualitative analysis techniques in this study, including iterative data review, multiple coders, and “member checking”[25]. Three members of the research team reviewed all transcripts from group interviews with a particular focus on narrative related to informational needs and suggestions for SCP content. One team member (Napoles) coded each transcript for concepts and themes, starting with an open coding approach using inductive codes developed from transcript content and deductive codes linked to the research focus and original aims. After coding three transcripts the initial list of codes was shared with the broader study team, discussed, and refined. The resulting list formed the basis of the codebook that was applied to the remaining three transcripts. While coding was ongoing, two members of the research team developed “summary documents” which highlighted new ideas and concepts, recurrent ideas and concepts, and patterns or themes noted across transcripts. These summary documents were shared among the team and discussed in group meetings. The main themes identified in this collaborative analysis process, ongoing throughout the qualitative data collection phase, were shared and discussed with SFWCN members and their responses were incorporated into the analysis.

Results

Participant characteristics

Table 1 details demographic characteristics of the 38 focus group participants. The mean age of the participants was 61 ± 9. Forty-one percent of the participants (41%) had either less than a high school education or had completed high school or GED with the remainder equally distributed among other educational attainment categories. About a third of the participants (36%) had an annual household income of less than a $10,000.

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Table 1. Participant Demographic Summary Statistics.

https://doi.org/10.1371/journal.pone.0168383.t001

Discussion

In order to ensure the overall well being of cancer survivors, experts and policy makers agree that a comprehensive and coordinated approach to post-treatment care is required [26]. Recommended steps have been outlined by the IOM and LIVESTRONG in their brief: The Essential Elements of Survivorship Care [27], and the Commission on Cancer (COC) standard 3.3 requires a staggered implementation of the provision of SCPs between 2016 (to 25% of patients) and 2018 (to 75% of patients) [24]. However, challenges in addressing these elements of post-treatment care in a safety-net setting with non-English speaking and limited English proficiency (LEP) breast cancer patients has received little attention. A recent study of SCP preferences among Chinese American breast cancer survivors found that the women interviewed would prefer reviewing the treatment summary in person with a provider, and that follow up written information in lay language in English and Chinese would be acceptable [11]. Preferred content was similar to that identified in the data presented herein, with the addition of requests for information on Traditional Chinese Medicine. Burg’s findings from research with African American breast cancer survivors resonates with the findings reported in this study. Women in her research received variable amounts of information about their cancer treatments [14] and were discontent with the race-specific information they received. The American Society of Clinical Oncology’s (ASCO) breast cancer survivorship care plan in use at the time of the study was viewed as too technical and lacked detailed information on side effects and self-care [14]. Other research with minority breast cancer survivors reports that SCP templates are too generic [13,14,28]. In a focus group study where male and female cancer survivors reviewed an SCP template for colorectal cancer, Hewitt et al. reported that participants preferred SCPs that were more personalized, tailoring the treatment plan to the individual, and were written in layman’s terms [28]. In a recent study of the responsiveness of SCPs to the needs of African American breast cancer survivors, Ashing-Giwa and colleagues held consensus meetings with survivors and advocates to identify culturally responsive SCP content and domains [12]. Recommendations included documentation of all co-morbidities and medications regardless of relationship to cancer, referrals for cancer-related providers, and culturally informed health advisories. The authors concluded that the available SCP template lacked adequate content on health history, co-morbidity, health promotion, and functioning [12]. Further, they argue that the emerging science and implementation of SCPs are void of patient input. Overall, this research suggests gaps in the ability of existing SCP templates to address the information needs of specific population groups or to be particularly useful to patients as they transition from oncology to primary care [11–14]. The study reported here is the first that we are aware of that includes perspectives of ethnically and linguistically diverse safety-net breast cancer patients on SCP content and delivery. It demonstrates the value of and need for direct communication between patients and providers about survivorship care, thus highlighting the need for conceptualizing the SCP as a process with information provided at multiple time points and via various mechanisms (e.g. low literacy information sheets in language, direct communication, etc.).

SCPs have been recognized as having strong face validity [1]. In addition, cancer survivors have expressed enthusiastic support for SCPs [28,29]. However, the promise of an SCP as a quality improvement tool is dependent in large part on system level issues [13,14]. Oncologists often do not have the time to create individualized SCPs or to discuss the content with their patients. Despite research reporting the need to develop cancer survivorship educational strategies that are responsive to the needs of specific populations, such as those included in this study, and the psychosocial profiles that motivate requests for extensive follow up guidance [13], adoption of SCPs and development of processes for their delivery have been slow. This is likely due to the resources required for their development, lack of provider buy-in for their utility, and reimbursement issues [13]. Currently, there are no clear mechanisms for reimbursement for the time it would take oncologists or other members of the oncology team to provide elemental survivorship information such as that requested by our participants, or to spend time coordinating the flow of information between their own clinics and the PCP.

Limitations

This is preliminary work, and more needs to be done. While we note that the majority of our participants were low health literacy and LEP, we did not administer a health literacy measure in the course of this study. This decision was made in partnership with the SFWCN member organizations. These community organizations serve largely low health literacy and LEP breast cancer survivors living in poverty or precarity. Because they recruited from their organization membership, they felt that a health literacy measure was unnecessary and would introduce another barrier to participation in open discussion.

In the course of the focus groups, our participants tended to shift the conversation away from SCP content and format and back to descriptions of information needs, uncontrolled side effects and symptoms, and being generally lost in the system. The idea of a transition from cancer care to PCP, for many, was not something previously seriously considered. Perhaps because many were dealing with multiple co-morbidities, poverty, and insecure housing, and their experiences of cancer care were fraught with miscommunications, lack of information, and other structural barriers, the perceptions shared about survivorship and the SCP reflected a desire for improved communication and support.

Acknowledgments

Research reported was funded by the Avon Foundation Breast Cancer Disparities Grant (012015037, Luce PI) and the Mount Zion Health Fund (20130088, Burke PI). The partnering community-based organizations of the San Francisco Women’s Cancer Network made this research possible. The authors wish to thank the women who shared their experiences with us.