Randomized Trial of the Impact of Empowering Childhood Cancer Survivors With Survivorship Care Plans

Randomized Trial of the Impact of Empowering Childhood Cancer Survivors With Survivorship Care Plans Abstract Background A survivorship care plan (SCP), that is, individualized treatment summary and schedule of off-therapy surveillance, will be mandated by January 2019. It is unclear whether SCPs improve adherence to recommended follow-up care in the community. In this trial, we evaluated the impact of randomly assigning childhood cancer survivors to 1) SCPs to be taken to their primary care physician (PCP) to implement or 2) survivorship clinic (SC) on health care quality measures. Methods Eligibility included cancer diagnosis younger than age 18 years (2000–2012), cancer free, one or more years off therapy, and no prior survivorship clinic attendance. At 12 months, the random assignment groups were compared (SCP+PCP vs SC) by intent-to-treat analysis with two-sided statistical tests in terms of patient adherence to guideline-recommended surveillance tests (eg, echocardiogram) and number of newly identified late complications of therapy. Results From 2011 to 2013, 96 participants (46.9% female, mean age = 15.9 ± 6.1 years) were randomly assigned. Adherence to 14 evaluated guideline-recommended surveillance tests ranged from 0% to 46.9% in the SCP+PCP group (n = 47) and from 50.0% to 86.4% in the SC group (n = 47). Adherence to 10 tests was statistically significantly different between the groups (all P < .05). One mild new late complication was identified in the SCP+PCP group compared with 21 late complications, ranging from mild to severe, identified in 11 patients in the SC group (2.1% vs 23.4% of patients, respectively, P = .003). Conclusions Our randomized trial suggests that empowering childhood cancer survivors with SCPs to be implemented by their PCPs is not sufficient to meet consensus follow-up recommendations. More than 95% of childhood cancer survivors will develop chronic medical, neurocognitive, and/or emotional conditions from their cancer and its treatment by age 45 years (1). Most of these conditions are amenable to surveillance, prevention, and early intervention. Yet less than 20% of childhood cancer survivors receive recommended survivorship care post-treatment (2,3). Although specialty survivorship clinics are the often-cited gold standard, they are expensive, often geographically inaccessible, and remind patients of the cancer experience (3–6). Survivorship care by primary care physicians (PCPs) offers the advantages of convenience to patients, emphasis on wellness, and opportunity for lifelong care. The Institute of Medicine advocates the survivorship care plan (SCP) as a means to improve care (7). The SCP is an individualized document with a detailed treatment summary, surveillance schedule for recurrence and late complications of therapy, and recommended health behaviors (8). The American College of Surgeons Commission on Cancer will require that SCPs be given to all patients at accredited treatment centers as of January 1, 2019 (9). As demonstrated by a national survey (10), SCPs are already provided by at least 20% of oncologists in clinical practice. Empirical data in childhood cancer survivors are critically needed to determine whether SCPs improve care, especially among patients not attending survivorship clinics. In adults, Grunfeld et al. demonstrated the potential value of the SCP as a tool for PCPs, rather than the cancer center, to provide survivorship care (11). Off-therapy breast cancer survivors randomly assigned to an SCP and follow-up with their PCP had similar rates of recurrence and death as those with cancer center follow-up. In both primary care and cancer center settings, adult patients report high levels of satisfaction with SCPs (12–15). Randomized trials have been inconsistent. One study found that breast cancer survivors endorsed better self-reported health and psychosocial functioning when they received an SCP vs usual care (16). In contrast, other studies found no improvement in health-related quality of life, patient satisfaction, health behaviors, or coordination of care among patients randomly assigned to an SCP (17–20). None of these studies evaluated late complications aside from cancer recurrence. Less is known about the benefit of SCPs in childhood cancer survivors (diagnosed at age <18 years). In a cross-sectional study, SCPs were understood and valued by the majority of pediatric cancer patients (21). In an intervention study, mailing SCPs to adult survivors of childhood cancer, without additional counseling, increased breast cancer and cardiac surveillance (22). In a Dutch study, there were high rates of adherence to recommended surveillance after storing the SCP on a secure website for patients and their PCPs (23). Randomized trials with objective outcomes are needed to investigate feasible and generalizable interventions to increase rates of recommended survivorship care among childhood cancer survivors outside of the specialty clinic. In this clinical trial, we evaluated the impact of randomizing childhood cancer survivors to 1) upfront distribution of SCPs to be implemented by primary care physicians or 2) survivorship clinic. We compared the random assignment groups on two health care quality measures: adherence to recommended surveillance tests and newly identified late complications. Methods Study Design and Procedures This randomized trial was conducted at Yale School of Medicine from May 2011 to November 2015. The study was approved by the Yale University Institutional Review Board. Written informed consent, and assent, as appropriate, was obtained from all participants before enrollment. The trial is registered with ClinicalTrials.gov (NCT02816866) (24). Participants Potentially eligible patients were identified from the Yale-New Haven Hospital Cancer Registry (25). Inclusion criteria were 1) cancer diagnosis between January 1, 2000, and December 31, 2012, younger than age 18 years; 2) off therapy one or more years prior to enrollment; 3) living cancer-free less than 100 miles from Yale; and 4) fluent in English or Spanish (or parents of patients younger than age 18 years). Excluded were patients who had previously attended a survivorship clinic. Since 2003, it has been routine practice at Yale to encourage all off-therapy patients to attend survivorship clinic; however, there is no automatic referral system. Poor adherence to recommended follow-up has been described at Yale (3) and elsewhere (26,27). For patients younger than age 18 years, parents received study communications and surveys. All participants completed a baseline survey requesting their PCP’s contact information. Hospital medical records were reviewed by trained medical abstractors. A detailed treatment summary was created including chemotherapy exposures with cumulative dosages, radiation doses and sites, surgeries, and stem cell transplants. Any known late complications of therapy were also abstracted. Randomization and Blinding Participants were randomly assigned to either a survivorship care plan with primary care physician follow-up (SCP+PCP) or survivorship clinic (SC) using block random assignment with block sizes of four generated by a computer algorithm, stratified by sex, age at evaluation (2–12, 13–18, >18 years), and radiation exposure (yes/no) to equally distribute factors associated with late complications of therapy (28). Survivorship clinic staff were blinded to study participation. Interventions The American College of Surgeons requires that an SCP be delivered to every patient following completion of therapy (9). In accordance, participants in both groups received an individualized SCP consisting of a detailed treatment summary, a list of possible late complications, a schedule of guideline-recommended surveillance tests, and a description of desirable health behaviors. The late complications and surveillance schedule were based on the Children’s Oncology Group Long-Term Follow-Up (COG LTFU) Guidelines for Survivors of Childhood, Adolescent, and Young Adult Cancers, version 3 (29). These are risk-based, exposure-specific clinical practice guidelines based on published evidence and consensus among a multidisciplinary panel of survivorship experts, representing the best available standard for survivorship care (30). The schedule of recommended tests indicated frequency and when to start post-therapy, but not the specific dates when next due. The SCP also advised consumption of five or more fruits/vegetables per day, tobacco avoidance, and physical activity based on age-specific recommendations (31,32). Participants in the SCP+PCP group were mailed the SCP upfront, called to ensure that they received and understood the SCP, and directed to take the SCP to their PCP for a survivorship care–focused visit within the next 12 months. Patients without a PCP received help finding one. PCPs were mailed individualized letters explaining that their patient was in the trial and would be making an appointment to complete recommended surveillance and discuss the SCP. Physicians were also given general educational survivorship materials and contact information (phone, email) of study investigators for further information regarding the study and SCP. However, no communications from any PCPs were received. Participants randomly assigned to the SC group were contacted by the clinic’s nurse coordinator to schedule an appointment with the Yale pediatric survivorship clinic (33) within the next 12 months. At the clinic visit, the physician(s) took a focused history, completed a physical exam, ordered guideline-recommended surveillance tests, and provided education regarding health behaviors. Patients were given an SCP following the visit. Outcomes We assessed two measures of survivorship care quality: adherence to guideline-recommended surveillance tests and the number of new late complications of therapy identified during the 12-month intervention period. Study outcomes were ascertained by medical record abstraction of all clinic and hospital records of participants from the 12-month intervention period by trained research staff blinded to random assignment. Records were obtained from the patient’s PCP or the SC, as appropriate. A health condition was categorized as a late complication if it was a known outcome of one of the patient’s treatment exposures (29). A late complication was considered new if there was no previous documentation of it in available medical records. Late complications were graded by two clinicians using the Common Terminology Criteria for Adverse Events, version 4.03, a scoring system developed by the National Cancer Institute for adverse events of treatment (34). Scores range from grade 1 (mild) to 5 (fatal). Before data analysis, all authors agreed on all scores. Statistical Analysis All analyses were performed with SAS software, version 9.4 (SAS Institute Inc., Cary, NC). A two-sided P value of .05 for statistical significance was used in all analyses. Baseline participant characteristics were calculated as mean and standard deviation or frequency distribution. Outcomes were analyzed per the intent-to-treat approach. Medical records, or confirmation of no visit in the 12-month study period, were obtained from PCPs of patients in the SCP+PCP group. Adherence to guideline-recommended surveillance tests was compared between the two groups by the Fisher exact test for 14 tests that were indicated in at least 10% of participants (breast imaging was not examined because it was recommended in less than 10%): bone density test (dual x-ray absorptiometry), echocardiogram, electrocardiogram, pulmonary function tests, audiogram, liver function tests (alanine aminotransferase, aspartate aminotransferase, bilirubin), renal function tests (blood urea nitrogen, creatinine), thyroid function tests (free thyroxine, thyroid-stimulating hormone), electrolytes/divalents panel (potassium, sodium, calcium, chloride, bicarbonate, glucose, phosphate, magnesium), complete blood count, gonadotropins (follicle-stimulating hormone, luteinizing hormone), sex hormones (testosterone, estradiol), lipid panel, and urinalysis. Adherence for each test was calculated as the proportion of patients with relevant results in their medical records during the study period among the total number of patients recommended to receive that test. The number, distribution, and severity of newly identified late complications in each group were described. A previous study demonstrated that survivorship clinic identified new late complications in 34% of patients (35). With 47 patients in the SCP+PCP group and 47 patients in the SC group, there was 80% power at an alpha of .05 to detect a difference of 27% between the groups. Secondary analyses were also conducted. To better understand reasons for any nonadherence, we assessed the frequency of guideline-recommended tests ordered by physicians (vs those completed by patients). Also, adherence was examined in analyses restricted to patients who were compliant with the intervention. Compliance was defined for participants in the SCP+PCP and SC groups as completing a PCP or SC visit, respectively, during the 12-month intervention period. Results Participants From 748 patients assessed for eligibility, 265 did not meet inclusion criteria, 253 refused participation, 124 could not be contacted, and 106 enrolled, including 10 who withdrew prior to random assignment (Figure 1). Ninety-six patients were randomly assigned between May 2011 and November 2013. The baseline characteristics of participants are summarized in Table 1 and were similar in the two groups. Participants were generally similar to those in previous large cohort studies of childhood cancer survivors (36), with 46.9% female, mean age (SD) of 15.9 (6.1) years, and 48.9% with a history of leukemia or lymphoma. Mean time since diagnosis (SD) was 6.1 (2.7) years. One patient relapsed, and another withdrew consent after random assignment; these were not included in our intent-to-treat analysis. Based on the previously stated definition of compliance, 76.6% (36/47) of the SCP+PCP group and 72.3% (34/47) of the SC group complied. Table 1. Patient and treatment characteristics by study group Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) * P value is for a two-sided t test (continuous variables) or Fischer exact test (categorical variables) comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 1. Patient and treatment characteristics by study group Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) * P value is for a two-sided t test (continuous variables) or Fischer exact test (categorical variables) comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Figure 1. View largeDownload slide CONSORT diagram of the study. No patients in the survivorship care plan with primary care physician follow-up group relapsed during the study period or withdrew consent. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Figure 1. View largeDownload slide CONSORT diagram of the study. No patients in the survivorship care plan with primary care physician follow-up group relapsed during the study period or withdrew consent. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Adherence to Guideline-Recommended Surveillance Tests The most frequently recommended tests among all participants were urinalysis (n = 62), complete blood count (n = 61), electrolytes/divalents panel (n = 58), renal function test (n = 55), echocardiogram (n = 51), and electrocardiogram (n = 51). The number and distribution of guideline-recommended surveillance tests were similar in the two groups (Table 2). There were marked differences in adherence for all tests, but these were especially pronounced for certain studies. One of 22 patients in the SCP+PCP group (4.5%) received a recommended bone density test vs 14 of 19 patients in the SC group (73.7%, P < .001). Similarly, three of 29 patients in the SCP+PCP group (10.3%) received their recommended echocardiogram vs 19 of 22 patients in the SC group (86.4%, P < .001). Completion of blood/urine tests also was much lower in the SCP+PCP group. The largest difference was for gonadotropins, for which none of the 21 patients (0%) in the SCP+PCP group received their recommended test, vs 11 of 17 patients in the SC group (64.7%, P < .001). Table 2. Proportion of patients who received guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. Table 2. Proportion of patients who received guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. In analyses of physician adherence (ie, whether physicians ordered the guideline-recommended tests), we found almost identical results (Table 3), suggesting that the majority of patients completed the tests if they were ordered. In analyses of patient adherence restricted to patients compliant with the intervention, differences between the two groups were still statistically significant (all P < .05) for all tests (Table 4). Table 3. Proportion of patients whose physicians ordered guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. Table 3. Proportion of patients whose physicians ordered guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. Table 4. Proportion of recommended surveillance tests completed among patients who complied with intervention (ie, went to primary care physician [n = 36] or survivorship clinic [n = 34]) Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 * P value is for a two-sided Fischer exact test comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 4. Proportion of recommended surveillance tests completed among patients who complied with intervention (ie, went to primary care physician [n = 36] or survivorship clinic [n = 34]) Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 * P value is for a two-sided Fischer exact test comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Newly Identified Late Complications of Therapy New late complications were identified in one patient in the SCP+PCP group, compared with 11 patients in the SC group (2.1% and 23.4% of patients, respectively, P = .003). Twenty-one late complications were identified in the SC group (Table 5). The only complication in the SCP+PCP group was a mild cataract (Tables 5 and 6). The most common conditions identified in the SC group were endocrinopathies (n = 5) and psychosocial difficulties (n = 5). One complication was categorized as severe, seven as moderate, 13 as mild, and none as life-threatening or fatal (Table 6). Table 5. Distribution of newly identified late complications by study group (counts)* Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 5. Distribution of newly identified late complications by study group (counts)* Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 6. Severity of newly identified late complications by study group (counts)* Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † Graded using Common Terminology Criteria for Adverse Events, version 4.03. Grade 1 is mild with no intervention indicated, grade 2 is moderate with noninvasive intervention indicated, grade 3 is severe but not immediately life-threatening, grade 4 is life-threatening, and grade 5 is fatal. Table 6. Severity of newly identified late complications by study group (counts)* Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † Graded using Common Terminology Criteria for Adverse Events, version 4.03. Grade 1 is mild with no intervention indicated, grade 2 is moderate with noninvasive intervention indicated, grade 3 is severe but not immediately life-threatening, grade 4 is life-threatening, and grade 5 is fatal. Discussion This randomized trial of childhood cancer survivors without previous attendance at a survivor clinic found that solely delivering an individualized SCP to patients with directions to follow up with their PCPs was not sufficient to achieve high-quality survivorship care. Compared with the SC group, patients randomly assigned to an SCP with primary care follow-up had much lower adherence to guideline-recommended surveillance tests and less identification of late complications of therapy, despite similar treatment exposures. All 22 late complications identified were clinically meaningful (ie, amenable to medical intervention, psychosocial support, and/or health behavior modification). Many late complications are not detectable by self-report or physical examination and required specialized testing. We found that patients completed most tests ordered by their physicians, suggesting that patient compliance is not a major contributing factor to nonadherence. Our data suggest that lack of identification of late complications was due to lack of ordering the recommended surveillance tests by physicians. Unfortunately, we did not collect data examining factors associated with physician ordering practices or patient compliance with ordered tests. The strengths of our study include the randomized trial design, medical record confirmation of outcomes, and investigation of SCPs as distributed in the “real world.” The American College of Surgeons Commission on Cancer will soon mandate SCPs for all cancer patients completing treatment at accredited centers. SCPs are generally highly regarded by oncologists and patient advocates based on common sense and the “principle of beneficence” (37). They are also desired by patients (37) and associated with high satisfaction (12,38–40). Based on a recent systematic review, the overwhelming majority of oncology providers and PCPs viewed SCPs as “useful” for patients and health care providers (37). However, our randomized trial found that more intervention is likely needed beyond the minimal requirements of the mandate to improve rates of survivorship care. In contrast to our study, previous work suggested that SCPs could increase follow-up care in childhood cancer survivors. In a single-arm study, Oeffinger et al. found that SCPs mailed to 72 Hodgkin lymphoma patients (and not their PCPs) highlighting recommended mammograms and/or echocardiograms increased uptake of these tests (22). The differing results may be due to our randomized controlled design or because we did not specifically emphasize certain tests. A single-arm Dutch study concluded that making web-based SCPs available to survivors and their family physicians was associated with 83% adherence to recommended surveillance (23). However, in the Netherlands, almost everyone is on the national health plan with universal reimbursement of follow-up care. In a randomized study by Hudson et al. that targeted cardiomyopathy screening, at-risk survivors who received a mailed SCP plus telephone counseling were much more likely (52.2 % vs 22.3%, P < .001) to complete testing compared with those who only received the SCP (41). As in our study, PCPs were not directly given patients’ SCPs. This study suggests that additional patient education may be beneficial as follow-up to the SCP. Our study did not directly engage PCPs beyond informing them of their patients’ enrollment and sharing general educational materials. Studies suggest that PCPs desire more involvement in their patients’ cancer experience and are willing to provide survivorship care (42–45). However, simply sending the SCP may not suffice. In a separate study, we surveyed 141 PCPs caring for Yale patients (46). Only 31% of PCPs reported feeling “very comfortable” using the SCP. Barriers included lack of knowledge (76%), confusion about aspects of the SCP (72%), and uncertainty about what aspects of care were their responsibility (60%). Only 55% recalled receiving the SCP. In free text responses, the majority requested better communication by oncologists, and some specifically suggested 1) phone communication by oncologist with the PCP to explain the SCP and 2) easier access to oncologists to ask questions as they arise. A Delphi panel of health policy experts on childhood cancer survivorship identified targeted education of PCPs as a high-priority initiative because the typical PCP sees very few childhood cancer survivors (47). Potential limitations in our study should be considered. There could be imperfect blinding during medical record review. To guard against this, patient records were only handled by trained medical abstractors. Tests could have been done at outside facilities and not reviewed, but that is unlikely as study results are routinely sent to the ordering physicians. Participants may not have brought the SCP to their visits or discussed it with their PCPs. However, our intention was to investigate the benefit of SCPs as distributed in the “real world.” SCPs should be given directly to patients according to the American College of Surgeons (9). In the SCP+PCP group, patients made their own appointment, while in the SC arm, the nurse coordinator scheduled the visit. However, the appointment compliance rate was higher (76.6% vs 72.3%) in the SCP+PCP group, suggesting that this was not a problem. There was heterogeneity in patient characteristics. However, we stratified random assignment by radiation exposure, sex, and age, and confirmed that elapsed time since diagnosis was comparable between the groups. It will be important in future studies to investigate how to best deliver the SCP in patients newly off therapy, which is the recommended time for delivering the SCP. We acknowledge that we only studied two measures of health care quality and that other outcomes (eg, cost-effectiveness, hospitalizations, mortality) should be examined in future studies. In conclusion, this randomized trial suggests that solely delivering an SCP to childhood cancer survivors with directions to follow up with their PCPs is not sufficient to achieve high-quality survivorship care. Further research is needed to identify effective interventions for patients and/or physicians in addition to the provision of SCPs. Funding This work was supported by the American Cancer Society (grant number 119700-RSGHP-10-107-01-CPHPS). Notes Affiliations of authors: Section of Pediatric Hematology/Oncology (NSKL, WLR, HRM, JR), Department of General Internal Medicine (CPG), and Cancer Outcomes, Public Policy, and Effectiveness Research (COPPER) Center, Yale Cancer Center (NSKL, CPG, XM), Yale School of Medicine, New Haven, CT; Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT (XM); Department of Psychology, University of Miami, Coral Gables, FL (HRM). The funder had no role in the design of the study; the collection, analysis, or interpretation of the data; the writing of the manuscript; or the decision to submit the manuscript for publication. The authors have no disclosures. References 1 Hudson MM , Ness KK , Gurney JG et al. , Clinical ascertainment of health outcomes among adults treated for childhood cancer . JAMA. 2013 ; 309 ( 22 ): 2371 – 2381 . 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Health Policy. 2004 ; 69 ( 2 ): 169 – 178 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png JNCI: Journal of the National Cancer Institute Oxford University Press

Randomized Trial of the Impact of Empowering Childhood Cancer Survivors With Survivorship Care Plans

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com
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0027-8874
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1460-2105
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10.1093/jnci/djy057
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Abstract

Abstract Background A survivorship care plan (SCP), that is, individualized treatment summary and schedule of off-therapy surveillance, will be mandated by January 2019. It is unclear whether SCPs improve adherence to recommended follow-up care in the community. In this trial, we evaluated the impact of randomly assigning childhood cancer survivors to 1) SCPs to be taken to their primary care physician (PCP) to implement or 2) survivorship clinic (SC) on health care quality measures. Methods Eligibility included cancer diagnosis younger than age 18 years (2000–2012), cancer free, one or more years off therapy, and no prior survivorship clinic attendance. At 12 months, the random assignment groups were compared (SCP+PCP vs SC) by intent-to-treat analysis with two-sided statistical tests in terms of patient adherence to guideline-recommended surveillance tests (eg, echocardiogram) and number of newly identified late complications of therapy. Results From 2011 to 2013, 96 participants (46.9% female, mean age = 15.9 ± 6.1 years) were randomly assigned. Adherence to 14 evaluated guideline-recommended surveillance tests ranged from 0% to 46.9% in the SCP+PCP group (n = 47) and from 50.0% to 86.4% in the SC group (n = 47). Adherence to 10 tests was statistically significantly different between the groups (all P < .05). One mild new late complication was identified in the SCP+PCP group compared with 21 late complications, ranging from mild to severe, identified in 11 patients in the SC group (2.1% vs 23.4% of patients, respectively, P = .003). Conclusions Our randomized trial suggests that empowering childhood cancer survivors with SCPs to be implemented by their PCPs is not sufficient to meet consensus follow-up recommendations. More than 95% of childhood cancer survivors will develop chronic medical, neurocognitive, and/or emotional conditions from their cancer and its treatment by age 45 years (1). Most of these conditions are amenable to surveillance, prevention, and early intervention. Yet less than 20% of childhood cancer survivors receive recommended survivorship care post-treatment (2,3). Although specialty survivorship clinics are the often-cited gold standard, they are expensive, often geographically inaccessible, and remind patients of the cancer experience (3–6). Survivorship care by primary care physicians (PCPs) offers the advantages of convenience to patients, emphasis on wellness, and opportunity for lifelong care. The Institute of Medicine advocates the survivorship care plan (SCP) as a means to improve care (7). The SCP is an individualized document with a detailed treatment summary, surveillance schedule for recurrence and late complications of therapy, and recommended health behaviors (8). The American College of Surgeons Commission on Cancer will require that SCPs be given to all patients at accredited treatment centers as of January 1, 2019 (9). As demonstrated by a national survey (10), SCPs are already provided by at least 20% of oncologists in clinical practice. Empirical data in childhood cancer survivors are critically needed to determine whether SCPs improve care, especially among patients not attending survivorship clinics. In adults, Grunfeld et al. demonstrated the potential value of the SCP as a tool for PCPs, rather than the cancer center, to provide survivorship care (11). Off-therapy breast cancer survivors randomly assigned to an SCP and follow-up with their PCP had similar rates of recurrence and death as those with cancer center follow-up. In both primary care and cancer center settings, adult patients report high levels of satisfaction with SCPs (12–15). Randomized trials have been inconsistent. One study found that breast cancer survivors endorsed better self-reported health and psychosocial functioning when they received an SCP vs usual care (16). In contrast, other studies found no improvement in health-related quality of life, patient satisfaction, health behaviors, or coordination of care among patients randomly assigned to an SCP (17–20). None of these studies evaluated late complications aside from cancer recurrence. Less is known about the benefit of SCPs in childhood cancer survivors (diagnosed at age <18 years). In a cross-sectional study, SCPs were understood and valued by the majority of pediatric cancer patients (21). In an intervention study, mailing SCPs to adult survivors of childhood cancer, without additional counseling, increased breast cancer and cardiac surveillance (22). In a Dutch study, there were high rates of adherence to recommended surveillance after storing the SCP on a secure website for patients and their PCPs (23). Randomized trials with objective outcomes are needed to investigate feasible and generalizable interventions to increase rates of recommended survivorship care among childhood cancer survivors outside of the specialty clinic. In this clinical trial, we evaluated the impact of randomizing childhood cancer survivors to 1) upfront distribution of SCPs to be implemented by primary care physicians or 2) survivorship clinic. We compared the random assignment groups on two health care quality measures: adherence to recommended surveillance tests and newly identified late complications. Methods Study Design and Procedures This randomized trial was conducted at Yale School of Medicine from May 2011 to November 2015. The study was approved by the Yale University Institutional Review Board. Written informed consent, and assent, as appropriate, was obtained from all participants before enrollment. The trial is registered with ClinicalTrials.gov (NCT02816866) (24). Participants Potentially eligible patients were identified from the Yale-New Haven Hospital Cancer Registry (25). Inclusion criteria were 1) cancer diagnosis between January 1, 2000, and December 31, 2012, younger than age 18 years; 2) off therapy one or more years prior to enrollment; 3) living cancer-free less than 100 miles from Yale; and 4) fluent in English or Spanish (or parents of patients younger than age 18 years). Excluded were patients who had previously attended a survivorship clinic. Since 2003, it has been routine practice at Yale to encourage all off-therapy patients to attend survivorship clinic; however, there is no automatic referral system. Poor adherence to recommended follow-up has been described at Yale (3) and elsewhere (26,27). For patients younger than age 18 years, parents received study communications and surveys. All participants completed a baseline survey requesting their PCP’s contact information. Hospital medical records were reviewed by trained medical abstractors. A detailed treatment summary was created including chemotherapy exposures with cumulative dosages, radiation doses and sites, surgeries, and stem cell transplants. Any known late complications of therapy were also abstracted. Randomization and Blinding Participants were randomly assigned to either a survivorship care plan with primary care physician follow-up (SCP+PCP) or survivorship clinic (SC) using block random assignment with block sizes of four generated by a computer algorithm, stratified by sex, age at evaluation (2–12, 13–18, >18 years), and radiation exposure (yes/no) to equally distribute factors associated with late complications of therapy (28). Survivorship clinic staff were blinded to study participation. Interventions The American College of Surgeons requires that an SCP be delivered to every patient following completion of therapy (9). In accordance, participants in both groups received an individualized SCP consisting of a detailed treatment summary, a list of possible late complications, a schedule of guideline-recommended surveillance tests, and a description of desirable health behaviors. The late complications and surveillance schedule were based on the Children’s Oncology Group Long-Term Follow-Up (COG LTFU) Guidelines for Survivors of Childhood, Adolescent, and Young Adult Cancers, version 3 (29). These are risk-based, exposure-specific clinical practice guidelines based on published evidence and consensus among a multidisciplinary panel of survivorship experts, representing the best available standard for survivorship care (30). The schedule of recommended tests indicated frequency and when to start post-therapy, but not the specific dates when next due. The SCP also advised consumption of five or more fruits/vegetables per day, tobacco avoidance, and physical activity based on age-specific recommendations (31,32). Participants in the SCP+PCP group were mailed the SCP upfront, called to ensure that they received and understood the SCP, and directed to take the SCP to their PCP for a survivorship care–focused visit within the next 12 months. Patients without a PCP received help finding one. PCPs were mailed individualized letters explaining that their patient was in the trial and would be making an appointment to complete recommended surveillance and discuss the SCP. Physicians were also given general educational survivorship materials and contact information (phone, email) of study investigators for further information regarding the study and SCP. However, no communications from any PCPs were received. Participants randomly assigned to the SC group were contacted by the clinic’s nurse coordinator to schedule an appointment with the Yale pediatric survivorship clinic (33) within the next 12 months. At the clinic visit, the physician(s) took a focused history, completed a physical exam, ordered guideline-recommended surveillance tests, and provided education regarding health behaviors. Patients were given an SCP following the visit. Outcomes We assessed two measures of survivorship care quality: adherence to guideline-recommended surveillance tests and the number of new late complications of therapy identified during the 12-month intervention period. Study outcomes were ascertained by medical record abstraction of all clinic and hospital records of participants from the 12-month intervention period by trained research staff blinded to random assignment. Records were obtained from the patient’s PCP or the SC, as appropriate. A health condition was categorized as a late complication if it was a known outcome of one of the patient’s treatment exposures (29). A late complication was considered new if there was no previous documentation of it in available medical records. Late complications were graded by two clinicians using the Common Terminology Criteria for Adverse Events, version 4.03, a scoring system developed by the National Cancer Institute for adverse events of treatment (34). Scores range from grade 1 (mild) to 5 (fatal). Before data analysis, all authors agreed on all scores. Statistical Analysis All analyses were performed with SAS software, version 9.4 (SAS Institute Inc., Cary, NC). A two-sided P value of .05 for statistical significance was used in all analyses. Baseline participant characteristics were calculated as mean and standard deviation or frequency distribution. Outcomes were analyzed per the intent-to-treat approach. Medical records, or confirmation of no visit in the 12-month study period, were obtained from PCPs of patients in the SCP+PCP group. Adherence to guideline-recommended surveillance tests was compared between the two groups by the Fisher exact test for 14 tests that were indicated in at least 10% of participants (breast imaging was not examined because it was recommended in less than 10%): bone density test (dual x-ray absorptiometry), echocardiogram, electrocardiogram, pulmonary function tests, audiogram, liver function tests (alanine aminotransferase, aspartate aminotransferase, bilirubin), renal function tests (blood urea nitrogen, creatinine), thyroid function tests (free thyroxine, thyroid-stimulating hormone), electrolytes/divalents panel (potassium, sodium, calcium, chloride, bicarbonate, glucose, phosphate, magnesium), complete blood count, gonadotropins (follicle-stimulating hormone, luteinizing hormone), sex hormones (testosterone, estradiol), lipid panel, and urinalysis. Adherence for each test was calculated as the proportion of patients with relevant results in their medical records during the study period among the total number of patients recommended to receive that test. The number, distribution, and severity of newly identified late complications in each group were described. A previous study demonstrated that survivorship clinic identified new late complications in 34% of patients (35). With 47 patients in the SCP+PCP group and 47 patients in the SC group, there was 80% power at an alpha of .05 to detect a difference of 27% between the groups. Secondary analyses were also conducted. To better understand reasons for any nonadherence, we assessed the frequency of guideline-recommended tests ordered by physicians (vs those completed by patients). Also, adherence was examined in analyses restricted to patients who were compliant with the intervention. Compliance was defined for participants in the SCP+PCP and SC groups as completing a PCP or SC visit, respectively, during the 12-month intervention period. Results Participants From 748 patients assessed for eligibility, 265 did not meet inclusion criteria, 253 refused participation, 124 could not be contacted, and 106 enrolled, including 10 who withdrew prior to random assignment (Figure 1). Ninety-six patients were randomly assigned between May 2011 and November 2013. The baseline characteristics of participants are summarized in Table 1 and were similar in the two groups. Participants were generally similar to those in previous large cohort studies of childhood cancer survivors (36), with 46.9% female, mean age (SD) of 15.9 (6.1) years, and 48.9% with a history of leukemia or lymphoma. Mean time since diagnosis (SD) was 6.1 (2.7) years. One patient relapsed, and another withdrew consent after random assignment; these were not included in our intent-to-treat analysis. Based on the previously stated definition of compliance, 76.6% (36/47) of the SCP+PCP group and 72.3% (34/47) of the SC group complied. Table 1. Patient and treatment characteristics by study group Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) * P value is for a two-sided t test (continuous variables) or Fischer exact test (categorical variables) comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 1. Patient and treatment characteristics by study group Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) Characteristics All patients (N = 96) SCP+PCP group (n = 47) SC group (n = 49) P* Mean age at diagnosis (SD), y 9.8 (5.7) 10.1 (5.6) 9.5 (5.9) .59 Mean time since diagnosis (SD), y 6.1 (2.7) 6.2 (2.7) 6.1 (2.7) .82 Mean age at evaluation (SD), y 15.9 (6.1) 16.3 (6.1) 15.6 (6.1) .54 Sex, No. (%) .99  Male 51 (53.1) 25 (53.2) 26 (53.1)  Female 45 (46.9) 22 (46.8) 23 (46.9) Race, No. (%) .60  White 83 (86.5) 41 (87.2) 42 (85.7)  Black 11 (11.5) 6 (12.8) 5 (10.2)  Other 2 (2.0) 0 2 (4.1) Primary cancer diagnosis, No. (%) .51  Leukemia 30 (31.2) 14 (29.8) 16 (32.7)  Lymphoma 17 (17.7) 10 (21.3) 7 (14.3)  Bone tumor 5 (5.2) 4 (8.5) 1 (2.0)  Soft tissue sarcoma 2 (2.1) 0 2 (4.1)  Central nervous system 9 (9.4) 3 (6.4) 6 (12.2)  Other solid tumors 21 (21.9) 11 (23.4) 10 (20.4)  Other 12 (12.5) 5 (10.6) 7 (14.3) Radiation therapy, No. (%) .99  Yes 35 (36.5) 17 (36.2) 18 (36.7)  No 61 (63.5) 30 (63.8) 31 (63.3) Chemotherapy, No. (%) .99  Yes 71 (74.0) 35 (74.5) 36 (73.5)  No 25 (26.0) 12 (25.5) 13 (26.5) * P value is for a two-sided t test (continuous variables) or Fischer exact test (categorical variables) comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Figure 1. View largeDownload slide CONSORT diagram of the study. No patients in the survivorship care plan with primary care physician follow-up group relapsed during the study period or withdrew consent. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Figure 1. View largeDownload slide CONSORT diagram of the study. No patients in the survivorship care plan with primary care physician follow-up group relapsed during the study period or withdrew consent. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Adherence to Guideline-Recommended Surveillance Tests The most frequently recommended tests among all participants were urinalysis (n = 62), complete blood count (n = 61), electrolytes/divalents panel (n = 58), renal function test (n = 55), echocardiogram (n = 51), and electrocardiogram (n = 51). The number and distribution of guideline-recommended surveillance tests were similar in the two groups (Table 2). There were marked differences in adherence for all tests, but these were especially pronounced for certain studies. One of 22 patients in the SCP+PCP group (4.5%) received a recommended bone density test vs 14 of 19 patients in the SC group (73.7%, P < .001). Similarly, three of 29 patients in the SCP+PCP group (10.3%) received their recommended echocardiogram vs 19 of 22 patients in the SC group (86.4%, P < .001). Completion of blood/urine tests also was much lower in the SCP+PCP group. The largest difference was for gonadotropins, for which none of the 21 patients (0%) in the SCP+PCP group received their recommended test, vs 11 of 17 patients in the SC group (64.7%, P < .001). Table 2. Proportion of patients who received guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. Table 2. Proportion of patients who received guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 14/19 (73.7) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 0/29 (0) 15/22 (68.2) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 2/17 (11.8) 12/16 (75.0) <.001  Renal function test 8/27 (29.6) 20/28 (71.4) .003  Thyroid function test 4/15 (26.7) 11/16 (68.8) .03  Electrolytes/divalents panel 10/29 (34.5) 21/29 (72.4) .008  Complete blood count 15/32 (46.9) 21/29 (72.4) .07  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 4/15 (26.7) 10/17 (58.8) .09 Urinalysis 11/31 (35.5) 19/31 (61.3) .07 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. In analyses of physician adherence (ie, whether physicians ordered the guideline-recommended tests), we found almost identical results (Table 3), suggesting that the majority of patients completed the tests if they were ordered. In analyses of patient adherence restricted to patients compliant with the intervention, differences between the two groups were still statistically significant (all P < .05) for all tests (Table 4). Table 3. Proportion of patients whose physicians ordered guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. Table 3. Proportion of patients whose physicians ordered guideline-recommended surveillance tests by study group* Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 Surveillance test SCP+PCP group No. (%) SC group No. (%) P† Studies  Bone density test 1/22 (4.5) 15/19 (78.9) <.001  Echocardiogram 3/29 (10.3) 19/22 (86.4) <.001  Electrocardiogram 1/29 (3.4) 19/22 (86.4) <.001  Pulmonary function test 0/10 (0) 6/9 (66.7) .003  Audiogram 0/5 (0) 3/6 (50.0) .18 Blood tests  Liver function test 3/18 (16.7) 12/16 (75.0) .001  Renal function test 9/27 (33.3) 20/28 (71.4) .007  Thyroid function test 5/15 (33.3) 11/16 (68.8) .08  Electrolytes/divalents panel 11/29 (37.9) 21/29 (72.4) .02  Complete blood count 17/32 (53.1) 21/29 (72.4) .19  Gonadotropins 0/21 (0) 11/17 (64.7) <.001  Sex hormones 1/21 (4.8) 12/18 (66.7) <.001  Lipid panel 5/15 (33.3) 10/17 (58.8) .18 Urinalysis 11/31 (35.5) 21/31 (67.7) .02 * Analysis of all participants (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † P value is for a two-sided Fischer exact test comparing the two random assignment groups. Table 4. Proportion of recommended surveillance tests completed among patients who complied with intervention (ie, went to primary care physician [n = 36] or survivorship clinic [n = 34]) Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 * P value is for a two-sided Fischer exact test comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 4. Proportion of recommended surveillance tests completed among patients who complied with intervention (ie, went to primary care physician [n = 36] or survivorship clinic [n = 34]) Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 Surveillance test SCP+PCP Group No. (%) SC Group No. (%) P* Studies  Bone density test 1/14 (7.1) 14/15 (93.3) <.001  Echocardiogram 3/20 (15.0) 19/19 (100) <.001  Electrocardiogram 0/20 (0) 15/19 (78.9) <.001  Pulmonary function test 0/7 (0) 6/6 (100) <.001  Audiogram 0/4 (0) 3/3 (100) .03 Blood tests  Liver function test 2/11 (18.2) 12/12 (100) <.001  Renal function test 8/21 (38.1) 20/20 (100) <.001  Thyroid function test 4/10 (40.0) 11/11 (100) .004  Electrolytes/divalents panel 10/23 (43.5) 21/21 (100) <.001  Complete blood count 15/23 (65.2) 21/21 (100) .004  Gonadotropins 0/13 (0) 11/12 (91.7) <.001  Sex hormones 1/13 (7.7) 12/13 (92.3) <.001  Lipid panel 4/10 (40.0) 10/10 (100) .01 Urinalysis 11/23 (47.8) 19/21 (90.5) .003 * P value is for a two-sided Fischer exact test comparing the two random assignment groups. SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Newly Identified Late Complications of Therapy New late complications were identified in one patient in the SCP+PCP group, compared with 11 patients in the SC group (2.1% and 23.4% of patients, respectively, P = .003). Twenty-one late complications were identified in the SC group (Table 5). The only complication in the SCP+PCP group was a mild cataract (Tables 5 and 6). The most common conditions identified in the SC group were endocrinopathies (n = 5) and psychosocial difficulties (n = 5). One complication was categorized as severe, seven as moderate, 13 as mild, and none as life-threatening or fatal (Table 6). Table 5. Distribution of newly identified late complications by study group (counts)* Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 5. Distribution of newly identified late complications by study group (counts)* Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 Organ/system Specific late complication SCP+PCP group SC group Endocrine/metabolic Overweight 0 3 Dyslipidemia 0 1 Hypothyroidism 0 1 Cardiovascular Raynaud’s phenomenon 0 2 Vascular insufficiency 0 1 Peripheral nervous system Peripheral motor neuropathy 0 2 Peripheral sensory neuropathy 0 1 Musculoskeletal Osteopenia 0 2 Dental Xerostomia 0 2 Pulmonary Restrictive lung disease 0 1 Ocular Cataracts 1 0 Psychosocial Substance abuse 0 3 Anxiety 0 1 Fatigue 0 1 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. Table 6. Severity of newly identified late complications by study group (counts)* Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † Graded using Common Terminology Criteria for Adverse Events, version 4.03. Grade 1 is mild with no intervention indicated, grade 2 is moderate with noninvasive intervention indicated, grade 3 is severe but not immediately life-threatening, grade 4 is life-threatening, and grade 5 is fatal. Table 6. Severity of newly identified late complications by study group (counts)* Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 Severity SCP+PCP group SC group Grade 1† 1 13 Grade 2 0 7 Grade 3 0 1 Grade 4 0 0 Grade 5 0 0 Total 1 21 * Analysis of all participants randomly assigned (ie, intent-to-treat analysis). SC = survivorship clinic; SCP+PCP = survivorship care plan with primary care physician follow-up. † Graded using Common Terminology Criteria for Adverse Events, version 4.03. Grade 1 is mild with no intervention indicated, grade 2 is moderate with noninvasive intervention indicated, grade 3 is severe but not immediately life-threatening, grade 4 is life-threatening, and grade 5 is fatal. Discussion This randomized trial of childhood cancer survivors without previous attendance at a survivor clinic found that solely delivering an individualized SCP to patients with directions to follow up with their PCPs was not sufficient to achieve high-quality survivorship care. Compared with the SC group, patients randomly assigned to an SCP with primary care follow-up had much lower adherence to guideline-recommended surveillance tests and less identification of late complications of therapy, despite similar treatment exposures. All 22 late complications identified were clinically meaningful (ie, amenable to medical intervention, psychosocial support, and/or health behavior modification). Many late complications are not detectable by self-report or physical examination and required specialized testing. We found that patients completed most tests ordered by their physicians, suggesting that patient compliance is not a major contributing factor to nonadherence. Our data suggest that lack of identification of late complications was due to lack of ordering the recommended surveillance tests by physicians. Unfortunately, we did not collect data examining factors associated with physician ordering practices or patient compliance with ordered tests. The strengths of our study include the randomized trial design, medical record confirmation of outcomes, and investigation of SCPs as distributed in the “real world.” The American College of Surgeons Commission on Cancer will soon mandate SCPs for all cancer patients completing treatment at accredited centers. SCPs are generally highly regarded by oncologists and patient advocates based on common sense and the “principle of beneficence” (37). They are also desired by patients (37) and associated with high satisfaction (12,38–40). Based on a recent systematic review, the overwhelming majority of oncology providers and PCPs viewed SCPs as “useful” for patients and health care providers (37). However, our randomized trial found that more intervention is likely needed beyond the minimal requirements of the mandate to improve rates of survivorship care. In contrast to our study, previous work suggested that SCPs could increase follow-up care in childhood cancer survivors. In a single-arm study, Oeffinger et al. found that SCPs mailed to 72 Hodgkin lymphoma patients (and not their PCPs) highlighting recommended mammograms and/or echocardiograms increased uptake of these tests (22). The differing results may be due to our randomized controlled design or because we did not specifically emphasize certain tests. A single-arm Dutch study concluded that making web-based SCPs available to survivors and their family physicians was associated with 83% adherence to recommended surveillance (23). However, in the Netherlands, almost everyone is on the national health plan with universal reimbursement of follow-up care. In a randomized study by Hudson et al. that targeted cardiomyopathy screening, at-risk survivors who received a mailed SCP plus telephone counseling were much more likely (52.2 % vs 22.3%, P < .001) to complete testing compared with those who only received the SCP (41). As in our study, PCPs were not directly given patients’ SCPs. This study suggests that additional patient education may be beneficial as follow-up to the SCP. Our study did not directly engage PCPs beyond informing them of their patients’ enrollment and sharing general educational materials. Studies suggest that PCPs desire more involvement in their patients’ cancer experience and are willing to provide survivorship care (42–45). However, simply sending the SCP may not suffice. In a separate study, we surveyed 141 PCPs caring for Yale patients (46). Only 31% of PCPs reported feeling “very comfortable” using the SCP. Barriers included lack of knowledge (76%), confusion about aspects of the SCP (72%), and uncertainty about what aspects of care were their responsibility (60%). Only 55% recalled receiving the SCP. In free text responses, the majority requested better communication by oncologists, and some specifically suggested 1) phone communication by oncologist with the PCP to explain the SCP and 2) easier access to oncologists to ask questions as they arise. A Delphi panel of health policy experts on childhood cancer survivorship identified targeted education of PCPs as a high-priority initiative because the typical PCP sees very few childhood cancer survivors (47). Potential limitations in our study should be considered. There could be imperfect blinding during medical record review. To guard against this, patient records were only handled by trained medical abstractors. Tests could have been done at outside facilities and not reviewed, but that is unlikely as study results are routinely sent to the ordering physicians. Participants may not have brought the SCP to their visits or discussed it with their PCPs. However, our intention was to investigate the benefit of SCPs as distributed in the “real world.” SCPs should be given directly to patients according to the American College of Surgeons (9). In the SCP+PCP group, patients made their own appointment, while in the SC arm, the nurse coordinator scheduled the visit. However, the appointment compliance rate was higher (76.6% vs 72.3%) in the SCP+PCP group, suggesting that this was not a problem. There was heterogeneity in patient characteristics. However, we stratified random assignment by radiation exposure, sex, and age, and confirmed that elapsed time since diagnosis was comparable between the groups. It will be important in future studies to investigate how to best deliver the SCP in patients newly off therapy, which is the recommended time for delivering the SCP. We acknowledge that we only studied two measures of health care quality and that other outcomes (eg, cost-effectiveness, hospitalizations, mortality) should be examined in future studies. In conclusion, this randomized trial suggests that solely delivering an SCP to childhood cancer survivors with directions to follow up with their PCPs is not sufficient to achieve high-quality survivorship care. Further research is needed to identify effective interventions for patients and/or physicians in addition to the provision of SCPs. Funding This work was supported by the American Cancer Society (grant number 119700-RSGHP-10-107-01-CPHPS). Notes Affiliations of authors: Section of Pediatric Hematology/Oncology (NSKL, WLR, HRM, JR), Department of General Internal Medicine (CPG), and Cancer Outcomes, Public Policy, and Effectiveness Research (COPPER) Center, Yale Cancer Center (NSKL, CPG, XM), Yale School of Medicine, New Haven, CT; Department of Chronic Disease Epidemiology, Yale School of Public Health, New Haven, CT (XM); Department of Psychology, University of Miami, Coral Gables, FL (HRM). The funder had no role in the design of the study; the collection, analysis, or interpretation of the data; the writing of the manuscript; or the decision to submit the manuscript for publication. The authors have no disclosures. References 1 Hudson MM , Ness KK , Gurney JG et al. , Clinical ascertainment of health outcomes among adults treated for childhood cancer . JAMA. 2013 ; 309 ( 22 ): 2371 – 2381 . 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JNCI: Journal of the National Cancer InstituteOxford University Press

Published: May 15, 2018

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