Review Article
Summing It Up: An Integrative Review of Studies of Cancer Survivorship Care Plans (2006-2013) Deborah K. Mayer, PhDRN1,2; Sarah A. Birken, PhD3; Devon K. Check, BA3; and Ronald C. Chen, MD, MPH2,4
In 2006, the Institute of Medicine recommended that cancer survivors who are completing primary treatment receive a survivorship care plan (SCP) based on face validity. The state of scientific knowledge regarding the SCP is unclear. The authors conducted an integrative review of existing evidence regarding SCPs. The MEDLINE/PubMed database, the Excerpta Medica Database (EMBASE), and the Cumulative Index to Nursing and Allied Health Literature (CINAHL) database were searched for relevant studies published between 2006 and 2013 using a combination of keywords: “survivors,” “survivorship,” “care plans,” “care planning,” “treatment summaries,” and “cancer.” Articles were included if they 1) reported results from an empirical study, 2) included cancer survivors who were diagnosed at age 18 years, 3) related to SCP, and 4) were published in English. In total, 781 records were retrieved; 77 were identified as duplicates, and 665 were abstracts or presentations that did not relate to SCPs for adults or were not empirical, which left 42 articles for inclusion in this review. Studies regarding SCP fell into 3 categories: 1) content (n514), 2) dissemination and implementation (n514), and 3) survivor and provider outcomes (n514). SCPs have been endorsed and are associated with improved knowledge, but SCP use remains sporadic. Only 4 studies were randomized controlled trials (RCTs) that avoided many biases associated with observational studies. Other limitations included cross-sectional or pre-SCP–post-SCP (“pre-post”) designs, limited generalizability caused by a lack of sample diversity, and a lack of systematic testing of data-collection tools. The quantity and quality of SCP research are limited. SCPs have been endorsed, but evidence of improved outcomes associated with SCP is limited. Future research that addresses the methodological concerns of extant studies is needed regarding SCP use, content, and outcomes. Cancer C 2014 American Cancer Society. 2015;121:978-96. V KEYWORDS: survivorship, cancer, dissemination, implementation, content, outcomes..
INTRODUCTION There are now almost 14 million cancer survivors in the United States, and it is projected that this number will increase in the next 10 years as the population ages.1 As improvements in cancer treatments increase the numbers of long-term survivors, survivorship health issues have emerged as an important public health concern.2 Multiple recent studies have demonstrated that cancer survivors are less likely to receive general preventive care and care associated with noncancer-related medical conditions than individuals without cancer.3 Consequently, there is increasing attention on research and interventions to improve the health care, and the health, of cancer survivors. The 2005 Institute of Medicine (IOM) report From Cancer Patient to Cancer Survivor: Lost in Transition2 highlighted concerns about care for cancer survivors and recommended survivorship care plans (SCPs), documents that include a patient’s personalized treatment summary, information on possible long-term and late effects, information about signs of recurrence, and guidelines for follow-up care as a “common sense” approach to addressing these concerns.2 The IOM report recognized that this recommendation was not supported by empirical evidence at that time but had face validity in improving communication among health care providers (eg, between the oncologist and primary care providers [PCPs]) and survivors and, consequently, improving quality of care and outcomes after cancer treatment. More recently, the American College of Surgeon’s Commission on Cancer, which accredits US cancer programs, announced that SCP implementation will be required for accreditation starting in 2015 (Fig. 1).4,5 In light of these high-profile endorsements of SCP as a means of improving care and outcomes for cancer survivors, a body of research on the use, content, and outcomes of SCP has developed. The results of this research and conclusions
Corresponding author: Deborah K. Mayer, PhD, RN, University of North Carolina School of Nursing, CB 7406, Chapel Hill, NC 27599-7460; Fax: (800) 372-9815; [email protected] 1 School of Nursing, University of North Carolina, Chapel Hill, North Carolina; 2University of North Carolina Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina; 3Department of Health Policy and Management, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina; 4Department of Radiation Oncology, School of Medicine, University of North Carolina, Chapel Hill, North Carolina.
We thank Jennifer Walker, Research Librarian, for her assistance in the literature search. DOI: 10.1002/cncr.28884, Received: March 3, 2014; Revised: April 14, 2014; Accepted: April 29, 2014, Published online September 23, 2014 in Wiley Online Library (wileyonlinelibrary.com)
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Figure 1. Donabedian’s model provided a framework for this review. Adapted from Donabedian A. Evaluating the quality of medical care. Milbank Mem Fund Q.44(3):Suppl:166–206, 1966.
that may be drawn from it have not previously been summarized. A summary of SCP research could inform efforts to refine content, improve associated outcomes, and promote use. Therefore, our objective was to summarize the state of scientific knowledge currently available regarding SCPs for adult cancer survivors. In addition to achieving this objective, we identify gaps in knowledge regarding SCPs to be addressed in future research. MATERIALS AND METHODS To summarize the empirical literature regarding SCP use in adult cancer survivors, we conducted an integrative review.6,7 An integrative review differs from other types of reviews like meta-analyses, which use statistical analyses to synthesize studies that have similar study designs and hypotheses, and systematic reviews, which combine evidence from several studies using a statistical or quasistatistical approach to answer a particular clinical question. Integrative reviews summarize evidence from studies with diverse methodologies (eg, experimental and nonexperimental studies) to provide information regarding the state of the science for a particular phenomenon.7 We used the Preferred Reporting Items for Cancer
April 1, 2015
Systematic Reviews and Meta-Analyses (PRISMA) guidelines in preparing our strategy and this report.6,8 Search Strategy
We searched the following databases: 1) PubMed, 2) the Excerpta Medica Database (EMBASE), and 3) the Cumulative Index to Nursing and Allied Health Literature (CINAHL). An experienced research librarian with expertise in cancer used a list of terms and Medical Subject Heading (MeSH) terms developed by the first and second authors. Table 1 lists the search terms and limits for each database. We searched for articles that were published between 2006 and 2013, because the 2005 IOM report From Cancer Patient to Cancer Survivor: Lost in Transition2 recommended SCPs while recognizing that empirical evidence was needed. Our objective was to summarize research that responded to the IOM report. In total, 781 articles were identified using this approach. Review Process
To be included in the full-text review, articles had to meet the following inclusion criteria: 1) report results of an 979
Review Article TABLE 1. Search Terms by Databasea Search No.b PubMed 1 2 3 4 5
6 EMBASE 1 2 3 4 5 CINAHL 1 2 3 4 5 6 7 8 9 10
No. of Items Identified
Query
Search Survivors[MesH] OR survivorship OR survivors OR survivor Search Survivors[MesH] OR survivorship OR survivors OR survivor (filters: English) Search Survivors[MesH] OR survivorship OR survivors OR survivor (filters: publication date from 01/01/2006 to 12/31/2014; English) Search neoplasms[MeSH] OR cancer[all fields] (filters: publication date from 01/01/2006 to 12/31/2014; English) Search patient care planning[MeSH] OR “care plan”[all fields] OR “care plans”[all fields] OR “care planning”[all fields] OR “treatment summary”[all fields] OR “treatment summaries”[all fields] (filters: publication date from 01/01/2006 to 12/31/2014; English) Searches 3 AND 4 AND 5 (filters, publication date from 01/01/2006 to 12/31/2014; English)
815,323 748,414 349,794 823,568 13,917
345
“cancer survivor”/exp OR “survivor”/exp OR survivors OR survivorship “neoplasm”/exp OR “cancer” “Patient care planning:/exp OR “nursing care plan”/exp OR “care plan” OR “care plans” OR “care planning” OR “treatment summary” OR “treatment summaries” Searches 1 AND 2 AND 3 Searches 1 AND 2 AND 3 AND [English]/lim AND [embase]/lim AND [2006-2014]/py
78,605 3,853,791 110,106
(MH “Neoplasms1”) OR “cancer” (MH “Survivors1”) OR “survivors” OR (MH “Cancer Survivors”) “survivor” OR “survivorship” Search 2 OR 3 (MH “Patient Care Plans1”) OR (MH “Nursing Care Plans1”) OR “care plans” “care plan” OR “care planning” OR “patient care planning” OR “treatment summary” OR “treatment summaries” Search 5 OR 6 Searches 1 AND 4 AND 7 Searches 1 AND 4 AND 7 (limiters: published date from 01/01/2006 to 12/31/2014; English language) Searches 1 AND 4 AND 7 (limiters: published date from 01/01/2006 to 12/31/2014; English language; exclude MEDLINE records)
204,338 16,886 3071 18,119 6369 4202 9590 121 115 39
537 397
Abbreviations: CINAHL, Cumulative Index to Nursing and Allied Health Literature; EMBASE, Excerpta Medica Database; MeSH, Medical Subject Headings. a All searches were conducted on December 6, 2013 and included publication dates through 2014 to account for publication online ahead of print. b The final search listed for each database represents the number of articles reviewed. Duplicate records were identified across databases. Records that were identified in Medline only were excluded, but items that were indexed by both EMBASE and Medline were included, and some of those also may have appeared in CINAHL.
empirical study, 2) relate to survivors diagnosed at age 18 years, 3) relate to cancer, and 4) report findings associated with SCP. Three authors reviewed abstracts from the first 50 articles and reached agreement on whether or not 37 articles (75%) should be included in the full-text review. Discrepancies were then reviewed and discussed until consensus was reached. In most cases, the reason for disagreement was obvious (eg, misapplication of inclusion/ exclusion criteria). Each of the same 3 authors then independently reviewed one-third of the remaining abstracts. Articles that met inclusion criteria based on the review of abstracts underwent full-text review. Further exclusions were made when the articles did not meet the inclusion criteria at this level of review (eg, they were abstracts or presentations, they focused on adult survivors of childhood cancers, or they did not include empirical data). Data Abstraction
Data from articles that met the inclusion criteria based on a full-text review were abstracted. Each author abstracted 980
information regarding study characteristics and the Population, Intervention, Comparator, Outcomes, Timing, and Setting (PICOTS) framework for 33% of the included articles. Articles were graded based on levels of evidence identified by the National Cancer Institute9,10 as follows: level I, prospective, randomized controlled trials (RCTs) and meta-analyses of prospective, RCTs; level II, prospective, non-RCTs; prospective cohort studies; prospective case series; and cross-sectional studies; level III, retrospective studies, including case-control and case studies or reports; and level IV, opinions of respected authorities based on clinical experience, consensus statements from expert committees, or authoritative reviews. The first author reviewed all abstractions for completeness and accuracy. Articles also were classified based on their methods (eg, observational, RCT, etc), outcomes assessed (eg, survivor preferences, health care service use), and other relevant characteristics (eg, study population). Cancer
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5 were conducted with breast cancer survivors; and 3 were conducted specifically with African American women who had breast cancer. Interviews (n56) were conducted more often with providers (oncologists, PCPs, nurses, and navigators or cancer program administrators) than with survivors. In the 5 studies that used surveys, both survivors and providers were surveyed.12,24-27 Only 1 survey study had a pre-SCP–post-SCP (“pre-post”) design,17 and 3 had a post-SCP delivery design.16,24,28 SCP content preferences
Figure 2. Adapted from: Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement [serial online]. BMJ. 2009;339:b2535.8
Many of the studies used SCP templates to elicit feedback; the most common were templates from the American Society of Clinical Oncology (ASCO) or JourneyForward. Most participants endorsed the concept of an SCP, whereas some identified it as “necessary but not sufficient” when transitioning a survivor to survivorship care. There were differing opinions about what content should be included: survivors wanted more content on health promotion, psychosocial support, and financial and other resources and emphasized a need for flexibility and tailoring; whereas providers preferred a streamlined version that clearly identified which components of care were their responsibility. SCP delivery preferences
RESULTS Figure 2 describes the number of articles that were identified as evidence associated with SCPs. From an initial yield of 781 articles, 42 articles were empirical studies of cancer SCPs for survivors aged 18 years published in English between 2006 and 2013 and, thus, met the criteria for inclusion in the integrative review. Based on a review of the final selection of articles, articles were grouped into 1 of 3 areas: 1) SCP content and delivery, including formative work on what should be included in an SCP (n514 articles); 2) dissemination and implementation studies to evaluate SCP use (n514 articles); and 3) survivor-level and provider-level outcomes associated with SCP use (n514 articles). Most of these studies were published since 2011; 19% were published between 2006 and 2011, 26.2% were published in 2011, 16.7% were published in 2012, and 38.1% were published in 2013. SCP Content
There were 14 studies that focused on SCP content and delivery preferences using several methods.11-23 Each of these studies is summarized in Table 2. Focus groups were used in 8 of the studies, including 7 with cancer survivors; Cancer
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Both paper and electronic SCPs were identified as useful by survivors, but some preferred to receive both. Mayer et al20 and Haq et al14 observed that respondents preferred the delivery of SCP either directly before or directly after treatment. Survivors wanted a treatment plan to be delivered at the time of diagnosis. Most of these studies did not address preferences for timing or who should deliver the SCP. Limitations
The strength of evidence for content studies was low, and all studies used observational designs. Studies that used focus groups included primarily white breast cancer survivors. Data-collection tools (eg, surveys, interview guides) were not tested systematically, limiting reliability and validity. Dissemination and Implementation
Outcomes of interest included SCP use in cancer programs and among cancer care providers (6 of 14 studies); survivor and PCP receipt of SCP (5 of 14 studies); retention of SCP (1 of 14 studies); and determinants of SCP use (7 of 14 studies).26,29-39 All of these studies are summarized in Table 3. To measure these outcomes, most SCP dissemination and implementation studies used surveys (11 of 14 studies); 2 used interviews; and 1 used both 981
982
Focus groups
Survey and interviews
Focus groups
Focus groups and interviews
Focus groups and interviews
Baravelli 200912
Burg 200913
Haq 201314
Hewitt 200715
IV
IV
IV
IV
Data Collection/ Methods
Ashing-Giwa 201311
Primary Author and Year
IV
Evidence Level
Three focus groups of survivors; 3 focus groups with 34 oncology nurses; 2 focus groups of PCPs; 20 interviews with oncologists
N520 survivors, ages 31-81 y, completed the survey regarding survivorship experiences; 14 PCPs participated in interviews; 12 survivors reviewed a sample SCP; 95 health care professionals completed the survey regarding SCP elements Purposive sampling of 32 BCS from Sister’s Network; 29 African American, 1 Hispanic, 2 white Purposive sampling of 61 BCS (mean age, 55.5 y), family physicians, and oncologists
N525 African American BCS and 3 advocates; ages 3279 y; 60% 5 y postdiagnosis
Sample and Setting
Intervention
SCP
SCP
ASCO SCP template
SCP with ASCO colorectal cancer flow sheet
ASCO SCP template
TABLE 2. Survivorship Care Plan Content-Focused Studies (n514)
SCP concept endorsed, but survivors and nurses wanted more supportive care and psychosocial elements included in the SCP than PCPs
Current SCP lacked cultural responsiveness and patientcenteredness.
Conclusions
Survivors were dissatisfied with the amount SCPs were viewed as important, but of information they received on cancerASCO template too technical and related side effects, including race-specific limited in information on side information effects and self-care approaches In the first study phase, BCS indicated that BCS and family physicians believed both web-based and paper-based SCPs participants thought that the SCP with human resources components were developed in the study’s second desirable and described their evolving phase was an improvement over needs throughout their cancer journey; the standard of care family physicians indicated that they needed key information in a user-friendly format. Survivors expressed support for SCP; PCPs Endorsed SCP concept but identified indicated that SCPs would help with barriers that might interfere with follow-up care; nurses suggested that they implementation could play a key role in developing and delivering SCPs, whereas physicians recognized the value of SCPs but were unwilling to assist in their use because of time constraints
African American BCS believed that increased mortality may be caused by comorbidities and inadequate surveillance and follow-up care; participants recommended that the SCP document all comorbidities and medications; allow PCP to participate; and make referrals to providers familiar with treating African American BCS, who note the importance of spirituality and disproportionately high levels of socioecologic stress Participants expressed strong support for SCP use but had differing opinions on content and when to deliver SCP
Results (Data)
Review Article
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Cancer
Survey
Survey
Survey and interviews
Hill-Kayser 201256
Jefford 201117
IV
II
Data Collection/ Methods
Hill-Kayser 200916
Primary Author and Year
IV
Evidence Level
TABLE 2. Continued
Total survivors, 3343; median age at cancer diagnosis, 48 y (range, 18 to 100 y); median current age, 51 y (range, 18 to 100 y); 71% women; 86% white; 78% college-educated; 2% reported >1 cancer diagnosis; 1880 users completed OncoLife surveys and, of these, 64.2% were survivors (n51198), 25% were health care providers, and 12% were friends/family members of survivors; 150 users completed satisfaction surveys and, of these, 57% were survivors or family members/friends of survivors, and 43% were health care providers Between May 2007 and October 2009, 8717 SCPs were created; 48% were for BCS; mean age at diagnosis, 48.5 y (range, 18-85 y); mean current age, 51.6 y (range, 19-89 y); mean time since diagnosis, 3 y (range, from 25% of cancer programs’ providers had ever used an SCP; 61% began using an SCP because of professional societies’ recommendations; key barriers to SCP use were insufficient organizational resources (75%) and systems for SCP use; patterns were observed in SCP use across location, program type, and professional society membership 15% of cancer programs developed SCPs for 75% survivors; 25% delivered 75% of SCPs to survivors; 23% delivered 75% of SCPs to PCPs; 4% met all 3 of these criteria; SCP use consistency was associated with geographic region (P5.05), initiating SCP use in response to survivors’ requests (P5.03), and membership in the NCI National Community Cancer Centers Program (P5.01) Only 2 of 20 survivors and 11 of 21 physicians or dentists could locate or remember receiving the SCP 3 y later; 18 of 20 survivors were unsure of the value of SCP 25% of respondents were not familiar with SCPs; 12.5% used an SCP; electronic health records were used as a communication tool; respondents’ survivorship services were mostly educational Mean SCP preparation time, 53.9 min; the perceived optimal time to deliver SCP was 3-6 mo after
Each survivorship program developed and implemented unique types of SCP documents
Results (Data)
TABLE 3. Survivorship Care Plan Dissemination and Implementation-Focused Studies (n514)
Time to develop SCP may be a barrier to widespread implementation; survivors find SCPs useful, but
Interview participants were aware of survivorship care planning, but approaches varied
Neither head and neck cancer survivors nor their PCPs were aware of SCPs 3-4 y after receiving them
SCP use is highly inconsistent; survivors may improve SCP use consistency by initiating SCP use; cancer care quality--improvement organizations might improve it by specifying how SCP use compliance will be assessed
Most cancer programs have adopted SCP, but use remains inconsistent; efforts to promote SCP use should address barriers, particularly in cancer programs that are susceptible to barriers to SCP use
The SCP document is a flexible tool that can be successfully adapted for use in extremely varied settings, from primary care to hospitals, to inform and educate survivors and providers
Conclusions
Survivorship Care Plan Integrative Review/Mayer et al
985
986
Survey
Survey
Interviews and focus groups
Friedman 200926
Hewitt 200715
IV
IV
Data Collection/ Methods
Forsythe 201335
Primary Author and Year
IV
Evidence Level
TABLE 3. Continued
Thirty-four nurses, including advanced practice nurses and ambulatory office-based nurses; 20 oncologists (urologists and radiation, medical, and gynecologic oncologists); PCPs were family practitioners and internists; survivors were men and women ages 25-70 y with different types of cancer
N567 non-Hodgkin lymphoma survivors ages 29-86 y and 22 physicians
Nationally representative sample of 1130 medical oncologists and 1020 PCPs
academic medical center and a rural community academic cancer center in Vermont
Sample and Setting
SCP
SCP
Oncologist provision and PCP receipt of SCP
Intervention
Survivors reported satisfaction with post-treatment medical care but believed that their psychosocial needs were not met; survivors expressed enthusiastic support for receipt of SCP; PCPs viewed themselves as playing an important role during the post-treatment period and indicated that a written SCP for follow-up would help them improve their survivorship practices; nurses recognized the need to improve survivorship care and suggested that they could play an active role in creating and
treatment ended; 64% of PCPs cited limited access to survivors as a barrier to providing follow-up care; 58% reported insufficient knowledge of survivorship issues; 83% of survivors said the SCP visit was very useful Nearly half of oncologists reported always/almost always providing a TS, whereas 20% reported always/ almost always providing a SCP (TS and follow-up plan); 33% of PCPs indicated always/almost always receiving a TS; 13.4% reported always/almost always receiving an SCP; oncologists who reported training in late and long-term effects of cancer and use of electronic medical records were more likely to report providing an SCP (P90% of survivors and health care providers reported satisfaction levels of “good” to “excellent” using OncoLife 56% of cancer specialist physicians reported that they, or their staff, prepared TS for their survivors; however, only 14% reported preparing SCPs; 54% of PCPs reported ever receiving a TS, but only 16% ever received a SCP; cancer specialists cited lack of training, reimbursement, and templates as barriers to preparing SCPs 43% used SCPs for BCS and/or CCS; 50% indicated that they planned to use SCPs; none of the
Results (Data)
Adoption and implementation of SCP is poor, possibly because of barriers such as lack of time and staff
Interventions, such as specific training, reimbursement, and templates that capture automated data, are needed to make TS and SCPs a part of standard care
Survivors and health care providers appear both willing to use this type of tool and satisfied with the information provided; most users had never before received survivorship information
Conclusions
Survivorship Care Plan Integrative Review/Mayer et al
987
988
SCP SCPs for 65 survivors in 13 LIVESTRONG Centers of Excellence Survey Stricker 201139 IV
Abbreviations: BCS, breast cancer survivor; CCS, colorectal cancer survivor; CI, confidence interval; IOM, Institute of Medicine; NCI, National Cancer Institute; PCP, primary care provider; QOL, quality of life; RCT, randomized controlled trial; SCP, survivorship care plan; TS, treatment summary.
Accordance with IOM recommendations is limited in most cancer programs; time may be a barrier to completeness; research is needed to identify essential SCP elements
Rural survivors face many health challenges; interventions should be adapted to meet their needs SCP and TS Survey Schootman 201338
N59530 survivors who completed the Missouri Behavioral Risk Factor Surveillance System
programs that used SCP included all IOM-recommended elements 24% of respondents received a TS; there were no significant differences between those who received a TS and those who did not with respect to a variety of sociodemographic factors; rural survivors were less likely to receive an SCP than urban survivors In total, 61.5% used institutionally created templates; concordance of content with IOM recommendations for TS and SCP varied from 0.01 to 98l SCP chart abstraction took from 31 to >60 min in 12 of 13 sites IV
Primary Author and Year Evidence Level
TABLE 3. Continued
Data Collection/ Methods
Sample and Setting
Intervention
Results (Data)
Conclusions
Review Article
interviews and focus groups. In most of these studies, the unit of analysis was the individual provider or survivor (9 of 14 studies); for the remaining 5 studies, the unit of analysis was the cancer program. The stakeholder of interest for most studies was survivors (7 of 14 studies); PCPs, cancer care providers, and cancer programs were represented in 3 studies each. Determinants of SCP use
Only 3 studies conducted statistical tests of correlations between SCP use and hypothesized determinants. In 2013, Birken and colleagues30 studied 23 cancer programs in the South Atlantic division of the American Cancer Society and observed that the cancer programs reporting no SCP use were located in a single state, and the cancer programs reporting no SCP use were all teaching hospitals, none of which was a member of the American Hospital Association. A study of 81 cancer programs throughout the United States with a wide range of annual incident cancers, program types, and cancer care qualityimprovement organization memberships31 indicated that consistent SCP use (ie, development and delivery of SCPs to all survivors and their PCPs) was associated with geographic region, initiating SCP use in response to survivors’ requests, and membership in the National Cancer Institute’s National Community Cancer Centers Program. Also 2013, Forsythe et al35 conducted a study using a nationally representative sample of oncologists and observed that that oncologists who had training in late and long-term effects of cancer and those who used electronic medical records were more likely to report SCP use. Several descriptive studies reported that barriers to SCP use included insufficient resources, such as time, staff, training, templates, and funding.15,30,32,37 Nurses indicated that their involvement could facilitate SCP use.15 SCP use in cancer programs and among cancer care providers
The 11 studies that assessed SCP use were consistent in reporting that SCP use was limited. Most US cancer programs reported some SCP use, but
Summing It Up: An Integrative Review of Studies of Cancer Survivorship Care Plans (2006-2013) Deborah K. Mayer, PhDRN1,2; Sarah A. Birken, PhD3; Devon K. Check, BA3; and Ronald C. Chen, MD, MPH2,4
In 2006, the Institute of Medicine recommended that cancer survivors who are completing primary treatment receive a survivorship care plan (SCP) based on face validity. The state of scientific knowledge regarding the SCP is unclear. The authors conducted an integrative review of existing evidence regarding SCPs. The MEDLINE/PubMed database, the Excerpta Medica Database (EMBASE), and the Cumulative Index to Nursing and Allied Health Literature (CINAHL) database were searched for relevant studies published between 2006 and 2013 using a combination of keywords: “survivors,” “survivorship,” “care plans,” “care planning,” “treatment summaries,” and “cancer.” Articles were included if they 1) reported results from an empirical study, 2) included cancer survivors who were diagnosed at age 18 years, 3) related to SCP, and 4) were published in English. In total, 781 records were retrieved; 77 were identified as duplicates, and 665 were abstracts or presentations that did not relate to SCPs for adults or were not empirical, which left 42 articles for inclusion in this review. Studies regarding SCP fell into 3 categories: 1) content (n514), 2) dissemination and implementation (n514), and 3) survivor and provider outcomes (n514). SCPs have been endorsed and are associated with improved knowledge, but SCP use remains sporadic. Only 4 studies were randomized controlled trials (RCTs) that avoided many biases associated with observational studies. Other limitations included cross-sectional or pre-SCP–post-SCP (“pre-post”) designs, limited generalizability caused by a lack of sample diversity, and a lack of systematic testing of data-collection tools. The quantity and quality of SCP research are limited. SCPs have been endorsed, but evidence of improved outcomes associated with SCP is limited. Future research that addresses the methodological concerns of extant studies is needed regarding SCP use, content, and outcomes. Cancer C 2014 American Cancer Society. 2015;121:978-96. V KEYWORDS: survivorship, cancer, dissemination, implementation, content, outcomes..
INTRODUCTION There are now almost 14 million cancer survivors in the United States, and it is projected that this number will increase in the next 10 years as the population ages.1 As improvements in cancer treatments increase the numbers of long-term survivors, survivorship health issues have emerged as an important public health concern.2 Multiple recent studies have demonstrated that cancer survivors are less likely to receive general preventive care and care associated with noncancer-related medical conditions than individuals without cancer.3 Consequently, there is increasing attention on research and interventions to improve the health care, and the health, of cancer survivors. The 2005 Institute of Medicine (IOM) report From Cancer Patient to Cancer Survivor: Lost in Transition2 highlighted concerns about care for cancer survivors and recommended survivorship care plans (SCPs), documents that include a patient’s personalized treatment summary, information on possible long-term and late effects, information about signs of recurrence, and guidelines for follow-up care as a “common sense” approach to addressing these concerns.2 The IOM report recognized that this recommendation was not supported by empirical evidence at that time but had face validity in improving communication among health care providers (eg, between the oncologist and primary care providers [PCPs]) and survivors and, consequently, improving quality of care and outcomes after cancer treatment. More recently, the American College of Surgeon’s Commission on Cancer, which accredits US cancer programs, announced that SCP implementation will be required for accreditation starting in 2015 (Fig. 1).4,5 In light of these high-profile endorsements of SCP as a means of improving care and outcomes for cancer survivors, a body of research on the use, content, and outcomes of SCP has developed. The results of this research and conclusions
Corresponding author: Deborah K. Mayer, PhD, RN, University of North Carolina School of Nursing, CB 7406, Chapel Hill, NC 27599-7460; Fax: (800) 372-9815; [email protected] 1 School of Nursing, University of North Carolina, Chapel Hill, North Carolina; 2University of North Carolina Lineberger Comprehensive Cancer Center, University of North Carolina, Chapel Hill, North Carolina; 3Department of Health Policy and Management, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, North Carolina; 4Department of Radiation Oncology, School of Medicine, University of North Carolina, Chapel Hill, North Carolina.
We thank Jennifer Walker, Research Librarian, for her assistance in the literature search. DOI: 10.1002/cncr.28884, Received: March 3, 2014; Revised: April 14, 2014; Accepted: April 29, 2014, Published online September 23, 2014 in Wiley Online Library (wileyonlinelibrary.com)
978
Cancer
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Survivorship Care Plan Integrative Review/Mayer et al
Figure 1. Donabedian’s model provided a framework for this review. Adapted from Donabedian A. Evaluating the quality of medical care. Milbank Mem Fund Q.44(3):Suppl:166–206, 1966.
that may be drawn from it have not previously been summarized. A summary of SCP research could inform efforts to refine content, improve associated outcomes, and promote use. Therefore, our objective was to summarize the state of scientific knowledge currently available regarding SCPs for adult cancer survivors. In addition to achieving this objective, we identify gaps in knowledge regarding SCPs to be addressed in future research. MATERIALS AND METHODS To summarize the empirical literature regarding SCP use in adult cancer survivors, we conducted an integrative review.6,7 An integrative review differs from other types of reviews like meta-analyses, which use statistical analyses to synthesize studies that have similar study designs and hypotheses, and systematic reviews, which combine evidence from several studies using a statistical or quasistatistical approach to answer a particular clinical question. Integrative reviews summarize evidence from studies with diverse methodologies (eg, experimental and nonexperimental studies) to provide information regarding the state of the science for a particular phenomenon.7 We used the Preferred Reporting Items for Cancer
April 1, 2015
Systematic Reviews and Meta-Analyses (PRISMA) guidelines in preparing our strategy and this report.6,8 Search Strategy
We searched the following databases: 1) PubMed, 2) the Excerpta Medica Database (EMBASE), and 3) the Cumulative Index to Nursing and Allied Health Literature (CINAHL). An experienced research librarian with expertise in cancer used a list of terms and Medical Subject Heading (MeSH) terms developed by the first and second authors. Table 1 lists the search terms and limits for each database. We searched for articles that were published between 2006 and 2013, because the 2005 IOM report From Cancer Patient to Cancer Survivor: Lost in Transition2 recommended SCPs while recognizing that empirical evidence was needed. Our objective was to summarize research that responded to the IOM report. In total, 781 articles were identified using this approach. Review Process
To be included in the full-text review, articles had to meet the following inclusion criteria: 1) report results of an 979
Review Article TABLE 1. Search Terms by Databasea Search No.b PubMed 1 2 3 4 5
6 EMBASE 1 2 3 4 5 CINAHL 1 2 3 4 5 6 7 8 9 10
No. of Items Identified
Query
Search Survivors[MesH] OR survivorship OR survivors OR survivor Search Survivors[MesH] OR survivorship OR survivors OR survivor (filters: English) Search Survivors[MesH] OR survivorship OR survivors OR survivor (filters: publication date from 01/01/2006 to 12/31/2014; English) Search neoplasms[MeSH] OR cancer[all fields] (filters: publication date from 01/01/2006 to 12/31/2014; English) Search patient care planning[MeSH] OR “care plan”[all fields] OR “care plans”[all fields] OR “care planning”[all fields] OR “treatment summary”[all fields] OR “treatment summaries”[all fields] (filters: publication date from 01/01/2006 to 12/31/2014; English) Searches 3 AND 4 AND 5 (filters, publication date from 01/01/2006 to 12/31/2014; English)
815,323 748,414 349,794 823,568 13,917
345
“cancer survivor”/exp OR “survivor”/exp OR survivors OR survivorship “neoplasm”/exp OR “cancer” “Patient care planning:/exp OR “nursing care plan”/exp OR “care plan” OR “care plans” OR “care planning” OR “treatment summary” OR “treatment summaries” Searches 1 AND 2 AND 3 Searches 1 AND 2 AND 3 AND [English]/lim AND [embase]/lim AND [2006-2014]/py
78,605 3,853,791 110,106
(MH “Neoplasms1”) OR “cancer” (MH “Survivors1”) OR “survivors” OR (MH “Cancer Survivors”) “survivor” OR “survivorship” Search 2 OR 3 (MH “Patient Care Plans1”) OR (MH “Nursing Care Plans1”) OR “care plans” “care plan” OR “care planning” OR “patient care planning” OR “treatment summary” OR “treatment summaries” Search 5 OR 6 Searches 1 AND 4 AND 7 Searches 1 AND 4 AND 7 (limiters: published date from 01/01/2006 to 12/31/2014; English language) Searches 1 AND 4 AND 7 (limiters: published date from 01/01/2006 to 12/31/2014; English language; exclude MEDLINE records)
204,338 16,886 3071 18,119 6369 4202 9590 121 115 39
537 397
Abbreviations: CINAHL, Cumulative Index to Nursing and Allied Health Literature; EMBASE, Excerpta Medica Database; MeSH, Medical Subject Headings. a All searches were conducted on December 6, 2013 and included publication dates through 2014 to account for publication online ahead of print. b The final search listed for each database represents the number of articles reviewed. Duplicate records were identified across databases. Records that were identified in Medline only were excluded, but items that were indexed by both EMBASE and Medline were included, and some of those also may have appeared in CINAHL.
empirical study, 2) relate to survivors diagnosed at age 18 years, 3) relate to cancer, and 4) report findings associated with SCP. Three authors reviewed abstracts from the first 50 articles and reached agreement on whether or not 37 articles (75%) should be included in the full-text review. Discrepancies were then reviewed and discussed until consensus was reached. In most cases, the reason for disagreement was obvious (eg, misapplication of inclusion/ exclusion criteria). Each of the same 3 authors then independently reviewed one-third of the remaining abstracts. Articles that met inclusion criteria based on the review of abstracts underwent full-text review. Further exclusions were made when the articles did not meet the inclusion criteria at this level of review (eg, they were abstracts or presentations, they focused on adult survivors of childhood cancers, or they did not include empirical data). Data Abstraction
Data from articles that met the inclusion criteria based on a full-text review were abstracted. Each author abstracted 980
information regarding study characteristics and the Population, Intervention, Comparator, Outcomes, Timing, and Setting (PICOTS) framework for 33% of the included articles. Articles were graded based on levels of evidence identified by the National Cancer Institute9,10 as follows: level I, prospective, randomized controlled trials (RCTs) and meta-analyses of prospective, RCTs; level II, prospective, non-RCTs; prospective cohort studies; prospective case series; and cross-sectional studies; level III, retrospective studies, including case-control and case studies or reports; and level IV, opinions of respected authorities based on clinical experience, consensus statements from expert committees, or authoritative reviews. The first author reviewed all abstractions for completeness and accuracy. Articles also were classified based on their methods (eg, observational, RCT, etc), outcomes assessed (eg, survivor preferences, health care service use), and other relevant characteristics (eg, study population). Cancer
April 1, 2015
Survivorship Care Plan Integrative Review/Mayer et al
5 were conducted with breast cancer survivors; and 3 were conducted specifically with African American women who had breast cancer. Interviews (n56) were conducted more often with providers (oncologists, PCPs, nurses, and navigators or cancer program administrators) than with survivors. In the 5 studies that used surveys, both survivors and providers were surveyed.12,24-27 Only 1 survey study had a pre-SCP–post-SCP (“pre-post”) design,17 and 3 had a post-SCP delivery design.16,24,28 SCP content preferences
Figure 2. Adapted from: Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement [serial online]. BMJ. 2009;339:b2535.8
Many of the studies used SCP templates to elicit feedback; the most common were templates from the American Society of Clinical Oncology (ASCO) or JourneyForward. Most participants endorsed the concept of an SCP, whereas some identified it as “necessary but not sufficient” when transitioning a survivor to survivorship care. There were differing opinions about what content should be included: survivors wanted more content on health promotion, psychosocial support, and financial and other resources and emphasized a need for flexibility and tailoring; whereas providers preferred a streamlined version that clearly identified which components of care were their responsibility. SCP delivery preferences
RESULTS Figure 2 describes the number of articles that were identified as evidence associated with SCPs. From an initial yield of 781 articles, 42 articles were empirical studies of cancer SCPs for survivors aged 18 years published in English between 2006 and 2013 and, thus, met the criteria for inclusion in the integrative review. Based on a review of the final selection of articles, articles were grouped into 1 of 3 areas: 1) SCP content and delivery, including formative work on what should be included in an SCP (n514 articles); 2) dissemination and implementation studies to evaluate SCP use (n514 articles); and 3) survivor-level and provider-level outcomes associated with SCP use (n514 articles). Most of these studies were published since 2011; 19% were published between 2006 and 2011, 26.2% were published in 2011, 16.7% were published in 2012, and 38.1% were published in 2013. SCP Content
There were 14 studies that focused on SCP content and delivery preferences using several methods.11-23 Each of these studies is summarized in Table 2. Focus groups were used in 8 of the studies, including 7 with cancer survivors; Cancer
April 1, 2015
Both paper and electronic SCPs were identified as useful by survivors, but some preferred to receive both. Mayer et al20 and Haq et al14 observed that respondents preferred the delivery of SCP either directly before or directly after treatment. Survivors wanted a treatment plan to be delivered at the time of diagnosis. Most of these studies did not address preferences for timing or who should deliver the SCP. Limitations
The strength of evidence for content studies was low, and all studies used observational designs. Studies that used focus groups included primarily white breast cancer survivors. Data-collection tools (eg, surveys, interview guides) were not tested systematically, limiting reliability and validity. Dissemination and Implementation
Outcomes of interest included SCP use in cancer programs and among cancer care providers (6 of 14 studies); survivor and PCP receipt of SCP (5 of 14 studies); retention of SCP (1 of 14 studies); and determinants of SCP use (7 of 14 studies).26,29-39 All of these studies are summarized in Table 3. To measure these outcomes, most SCP dissemination and implementation studies used surveys (11 of 14 studies); 2 used interviews; and 1 used both 981
982
Focus groups
Survey and interviews
Focus groups
Focus groups and interviews
Focus groups and interviews
Baravelli 200912
Burg 200913
Haq 201314
Hewitt 200715
IV
IV
IV
IV
Data Collection/ Methods
Ashing-Giwa 201311
Primary Author and Year
IV
Evidence Level
Three focus groups of survivors; 3 focus groups with 34 oncology nurses; 2 focus groups of PCPs; 20 interviews with oncologists
N520 survivors, ages 31-81 y, completed the survey regarding survivorship experiences; 14 PCPs participated in interviews; 12 survivors reviewed a sample SCP; 95 health care professionals completed the survey regarding SCP elements Purposive sampling of 32 BCS from Sister’s Network; 29 African American, 1 Hispanic, 2 white Purposive sampling of 61 BCS (mean age, 55.5 y), family physicians, and oncologists
N525 African American BCS and 3 advocates; ages 3279 y; 60% 5 y postdiagnosis
Sample and Setting
Intervention
SCP
SCP
ASCO SCP template
SCP with ASCO colorectal cancer flow sheet
ASCO SCP template
TABLE 2. Survivorship Care Plan Content-Focused Studies (n514)
SCP concept endorsed, but survivors and nurses wanted more supportive care and psychosocial elements included in the SCP than PCPs
Current SCP lacked cultural responsiveness and patientcenteredness.
Conclusions
Survivors were dissatisfied with the amount SCPs were viewed as important, but of information they received on cancerASCO template too technical and related side effects, including race-specific limited in information on side information effects and self-care approaches In the first study phase, BCS indicated that BCS and family physicians believed both web-based and paper-based SCPs participants thought that the SCP with human resources components were developed in the study’s second desirable and described their evolving phase was an improvement over needs throughout their cancer journey; the standard of care family physicians indicated that they needed key information in a user-friendly format. Survivors expressed support for SCP; PCPs Endorsed SCP concept but identified indicated that SCPs would help with barriers that might interfere with follow-up care; nurses suggested that they implementation could play a key role in developing and delivering SCPs, whereas physicians recognized the value of SCPs but were unwilling to assist in their use because of time constraints
African American BCS believed that increased mortality may be caused by comorbidities and inadequate surveillance and follow-up care; participants recommended that the SCP document all comorbidities and medications; allow PCP to participate; and make referrals to providers familiar with treating African American BCS, who note the importance of spirituality and disproportionately high levels of socioecologic stress Participants expressed strong support for SCP use but had differing opinions on content and when to deliver SCP
Results (Data)
Review Article
Cancer
April 1, 2015
Cancer
Survey
Survey
Survey and interviews
Hill-Kayser 201256
Jefford 201117
IV
II
Data Collection/ Methods
Hill-Kayser 200916
Primary Author and Year
IV
Evidence Level
TABLE 2. Continued
Total survivors, 3343; median age at cancer diagnosis, 48 y (range, 18 to 100 y); median current age, 51 y (range, 18 to 100 y); 71% women; 86% white; 78% college-educated; 2% reported >1 cancer diagnosis; 1880 users completed OncoLife surveys and, of these, 64.2% were survivors (n51198), 25% were health care providers, and 12% were friends/family members of survivors; 150 users completed satisfaction surveys and, of these, 57% were survivors or family members/friends of survivors, and 43% were health care providers Between May 2007 and October 2009, 8717 SCPs were created; 48% were for BCS; mean age at diagnosis, 48.5 y (range, 18-85 y); mean current age, 51.6 y (range, 19-89 y); mean time since diagnosis, 3 y (range, from 25% of cancer programs’ providers had ever used an SCP; 61% began using an SCP because of professional societies’ recommendations; key barriers to SCP use were insufficient organizational resources (75%) and systems for SCP use; patterns were observed in SCP use across location, program type, and professional society membership 15% of cancer programs developed SCPs for 75% survivors; 25% delivered 75% of SCPs to survivors; 23% delivered 75% of SCPs to PCPs; 4% met all 3 of these criteria; SCP use consistency was associated with geographic region (P5.05), initiating SCP use in response to survivors’ requests (P5.03), and membership in the NCI National Community Cancer Centers Program (P5.01) Only 2 of 20 survivors and 11 of 21 physicians or dentists could locate or remember receiving the SCP 3 y later; 18 of 20 survivors were unsure of the value of SCP 25% of respondents were not familiar with SCPs; 12.5% used an SCP; electronic health records were used as a communication tool; respondents’ survivorship services were mostly educational Mean SCP preparation time, 53.9 min; the perceived optimal time to deliver SCP was 3-6 mo after
Each survivorship program developed and implemented unique types of SCP documents
Results (Data)
TABLE 3. Survivorship Care Plan Dissemination and Implementation-Focused Studies (n514)
Time to develop SCP may be a barrier to widespread implementation; survivors find SCPs useful, but
Interview participants were aware of survivorship care planning, but approaches varied
Neither head and neck cancer survivors nor their PCPs were aware of SCPs 3-4 y after receiving them
SCP use is highly inconsistent; survivors may improve SCP use consistency by initiating SCP use; cancer care quality--improvement organizations might improve it by specifying how SCP use compliance will be assessed
Most cancer programs have adopted SCP, but use remains inconsistent; efforts to promote SCP use should address barriers, particularly in cancer programs that are susceptible to barriers to SCP use
The SCP document is a flexible tool that can be successfully adapted for use in extremely varied settings, from primary care to hospitals, to inform and educate survivors and providers
Conclusions
Survivorship Care Plan Integrative Review/Mayer et al
985
986
Survey
Survey
Interviews and focus groups
Friedman 200926
Hewitt 200715
IV
IV
Data Collection/ Methods
Forsythe 201335
Primary Author and Year
IV
Evidence Level
TABLE 3. Continued
Thirty-four nurses, including advanced practice nurses and ambulatory office-based nurses; 20 oncologists (urologists and radiation, medical, and gynecologic oncologists); PCPs were family practitioners and internists; survivors were men and women ages 25-70 y with different types of cancer
N567 non-Hodgkin lymphoma survivors ages 29-86 y and 22 physicians
Nationally representative sample of 1130 medical oncologists and 1020 PCPs
academic medical center and a rural community academic cancer center in Vermont
Sample and Setting
SCP
SCP
Oncologist provision and PCP receipt of SCP
Intervention
Survivors reported satisfaction with post-treatment medical care but believed that their psychosocial needs were not met; survivors expressed enthusiastic support for receipt of SCP; PCPs viewed themselves as playing an important role during the post-treatment period and indicated that a written SCP for follow-up would help them improve their survivorship practices; nurses recognized the need to improve survivorship care and suggested that they could play an active role in creating and
treatment ended; 64% of PCPs cited limited access to survivors as a barrier to providing follow-up care; 58% reported insufficient knowledge of survivorship issues; 83% of survivors said the SCP visit was very useful Nearly half of oncologists reported always/almost always providing a TS, whereas 20% reported always/ almost always providing a SCP (TS and follow-up plan); 33% of PCPs indicated always/almost always receiving a TS; 13.4% reported always/almost always receiving an SCP; oncologists who reported training in late and long-term effects of cancer and use of electronic medical records were more likely to report providing an SCP (P90% of survivors and health care providers reported satisfaction levels of “good” to “excellent” using OncoLife 56% of cancer specialist physicians reported that they, or their staff, prepared TS for their survivors; however, only 14% reported preparing SCPs; 54% of PCPs reported ever receiving a TS, but only 16% ever received a SCP; cancer specialists cited lack of training, reimbursement, and templates as barriers to preparing SCPs 43% used SCPs for BCS and/or CCS; 50% indicated that they planned to use SCPs; none of the
Results (Data)
Adoption and implementation of SCP is poor, possibly because of barriers such as lack of time and staff
Interventions, such as specific training, reimbursement, and templates that capture automated data, are needed to make TS and SCPs a part of standard care
Survivors and health care providers appear both willing to use this type of tool and satisfied with the information provided; most users had never before received survivorship information
Conclusions
Survivorship Care Plan Integrative Review/Mayer et al
987
988
SCP SCPs for 65 survivors in 13 LIVESTRONG Centers of Excellence Survey Stricker 201139 IV
Abbreviations: BCS, breast cancer survivor; CCS, colorectal cancer survivor; CI, confidence interval; IOM, Institute of Medicine; NCI, National Cancer Institute; PCP, primary care provider; QOL, quality of life; RCT, randomized controlled trial; SCP, survivorship care plan; TS, treatment summary.
Accordance with IOM recommendations is limited in most cancer programs; time may be a barrier to completeness; research is needed to identify essential SCP elements
Rural survivors face many health challenges; interventions should be adapted to meet their needs SCP and TS Survey Schootman 201338
N59530 survivors who completed the Missouri Behavioral Risk Factor Surveillance System
programs that used SCP included all IOM-recommended elements 24% of respondents received a TS; there were no significant differences between those who received a TS and those who did not with respect to a variety of sociodemographic factors; rural survivors were less likely to receive an SCP than urban survivors In total, 61.5% used institutionally created templates; concordance of content with IOM recommendations for TS and SCP varied from 0.01 to 98l SCP chart abstraction took from 31 to >60 min in 12 of 13 sites IV
Primary Author and Year Evidence Level
TABLE 3. Continued
Data Collection/ Methods
Sample and Setting
Intervention
Results (Data)
Conclusions
Review Article
interviews and focus groups. In most of these studies, the unit of analysis was the individual provider or survivor (9 of 14 studies); for the remaining 5 studies, the unit of analysis was the cancer program. The stakeholder of interest for most studies was survivors (7 of 14 studies); PCPs, cancer care providers, and cancer programs were represented in 3 studies each. Determinants of SCP use
Only 3 studies conducted statistical tests of correlations between SCP use and hypothesized determinants. In 2013, Birken and colleagues30 studied 23 cancer programs in the South Atlantic division of the American Cancer Society and observed that the cancer programs reporting no SCP use were located in a single state, and the cancer programs reporting no SCP use were all teaching hospitals, none of which was a member of the American Hospital Association. A study of 81 cancer programs throughout the United States with a wide range of annual incident cancers, program types, and cancer care qualityimprovement organization memberships31 indicated that consistent SCP use (ie, development and delivery of SCPs to all survivors and their PCPs) was associated with geographic region, initiating SCP use in response to survivors’ requests, and membership in the National Cancer Institute’s National Community Cancer Centers Program. Also 2013, Forsythe et al35 conducted a study using a nationally representative sample of oncologists and observed that that oncologists who had training in late and long-term effects of cancer and those who used electronic medical records were more likely to report SCP use. Several descriptive studies reported that barriers to SCP use included insufficient resources, such as time, staff, training, templates, and funding.15,30,32,37 Nurses indicated that their involvement could facilitate SCP use.15 SCP use in cancer programs and among cancer care providers
The 11 studies that assessed SCP use were consistent in reporting that SCP use was limited. Most US cancer programs reported some SCP use, but
