Evaluation of a transition to survivorship program for pediatric, adolescent, and young adult cancer patients and caregivers

Survivorship education and anticipatory guidance represent an unmet need for pediatric, adolescent, and young adult (AYA) cancer survivors and their caregivers when treatment ends. This pilot study evaluated the feasibility, acceptability, and preliminary efficacy of a structured transition program, bridging treatment to survivorship, to reduce distress and anxiety and increase perceived preparedness for survivors and caregivers.


INTRODUCTION
The period when pediatric, adolescent, and young adult (AYA) cancer patients complete treatment and transition to follow-up care is an important touchpoint in the cancer care continuum. While survivors and caregivers express excitement about completing treatment, they also report feelings of uncertainty and anxiety about the future. [1][2][3][4][5] Survivors and caregivers express an unmet need in receipt of survivorship information and support during this critical transition phase. 2,6,7 Studies assessing end-of-treatment needs indicate that pediatric and AYA survivors and caregivers desire specific education on their treatment history and follow-up care and increased communication among the survivor, caregivers, primary care providers, and oncology team. 1,3,[6][7][8] Karst and colleagues 6 found that 84% of survivors preferred receiving transition to survivorship education 1-2 months before completing treatment (42%) or at the end of treatment (42%). Similarly, 76% of caregivers indicated that they would like to receive survivorship education 1-2 months before the end of treatment (46%) or at the end of treatment (30%). 6 Results from another study indicated that parents wanted survivorship education, but expressed uncertainty about the timing of receiving the information. 8 Annual psychosocial screening in survivorship is a standard-of-care in pediatric oncology. This should include ongoing education about the importance of long-term follow-up throughout survivorship. 9 Recognizing this unmet need, pediatric oncology programs are increasingly creating programs to prepare survivors and caregivers for transition from active treatment to survivorship care. The impact of these programmatic approaches remains largely unknown. In one study, pediatric patients within 6 months from completing cancer treatment (n = 3, M age = 21 years) and/or parents (n = 14) participated in a transition visit with a research nurse practitioner in a survivorship clinic. 10 Most participants found the visit and materials helpful, recommending all survivors and caregivers receive such materials immediately after treatment ends (58%), during treatment (17%), or several months after treatment ends (17%). Many participants demonstrated limited knowledge about their potential late effects based upon their treatment and how long they needed follow-up care. 10 Another study demonstrated increased survivorship knowledge (treatment exposures and late effect risks) for AYA survivors (ages 16-25 years) and parents who attended one to three survivorship clinics during which education was provided. Results also highlighted the importance of providing survivorship education for both survivors and their parents. 11 Recognizing the knowledge and support gaps during the transition from treatment to survivorship, this study evaluated a two-visit transition program. Bridge to Next Steps ("Bridge") was designed based upon input from survivors, caregivers, and multidisciplinary pediatric oncology providers. 6 This pilot study aimed to evaluate the acceptability and preliminary efficacy of a structured program, bridging active treatment to survivorship care, to reduce distress and anxiety and increase feelings of preparedness for survivors and caregivers. It was hypothesized that a structured transition intervention would be feasible and acceptable and would be associated with reduced distress and anxiety and increased feeling of preparedness for transition for pediatric and AYA cancer survivors and caregivers.

Structured two-visit transition program intervention
Patient and caregiver feedback from a previous study 6 11 and confirmation of established care with a primary care provider and dentist discussed (referrals provided if needed). During Visit 2 (30 minutes), a survivorship provider discusses the survivor's therapy summary, distributes a treatment "passport" (credit card-size individualized treatment summary and follow-up care plan) and individualized healthy living resources (COG Health Links pertinent to risk of late effects based on treatment), and discusses potential late effects, a follow-up schedule, and recommended surveillance tests/labs. After meeting with a survivorship provider, survivors meet with a psychologist (additional 30 minutes) for a psychosocial assessment, which is a verbal, semi-structured interview, to identify transition needs or concerns related to emotional adjustment, school/vocational functioning, and socialization/activity, and provide anticipatory guidance referrals and resources as needed. The survivorship care plan is then transmitted to the survivor's primary care provider. Survivors continue to be followed for regular-interval follow-up care visits with their primary oncology team until 2-3 years after completing treatment, when they are transitioned to the Next Steps Survivorship Long-Term   Figure 1). This study received human subjects research approval from the children's hospital's institutional review board.

Study design and procedure
This was a single-arm, pre-post study design utilizing a convenience sample of patients recruited from the oncology service from a large

Emotional distress of survivor and caregiver
The Distress Thermometer (DT) is a valid and reliable self-report measure used to assess cancer-related emotional distress in adults. 13,14 It also has been adapted and validated for use for children with can-

Preparedness
Survey questions from the previous needs assessment study 6

Statistical analyses
Box plots and summary statistics were computed for group and pre-versus post-intervention comparisons for continuous data.
Cross-tabulations and percentages were generated for categorical data between groups and paired data within subjects (pre vs. post intervention

Participants
Fifty cancer survivors and 46 caregivers (all parents) completed both clinical visits of Bridge and both the pre and post measures were included in the analysis (see Table 2). There were no differences on key demographic or treatment variables between participants who completed the study versus those who were withdrawn. Survivors' median age was 7.5 years (range = 1-23 years). There were slightly more male survivors (56%); most survivors were White (92%) and non-Hispanic/Latinx (92%). The majority had a solid tumor (36%) or leukemia (36%) diagnosis, followed by other cancer diagnosis (16%), and lymphoma (12%). Treatment intensity was balanced between least to moderately intensive (52%) and very to most intensive (48%). There was variability in treatment length, with a median of 8 months and range of 1-39 months. Median age of caregivers was 38 years, with most being mothers (82.6%).

Program feasibility
Eighty-one patients consented and enrolled in the study out of 101 eligible patients (80.20%, see Figure 1). Sixty-three participants (63/81, 77.8%) completed both Bridge visits while on-study (see Figure 1 Consort for reasons for study withdrawals). Twelve survivors (out of the 18 participants who were withdrawn from the study) were able to complete both visits of Bridge as this program is standard-of-care.

Program acceptability
Of the AYA (14 years and older) and caregiver participants who com-

Distress and anxiety
There was no significant difference between survivors' (≥8 years old) distress scores from pre to post intervention (p = .67). There was no significant change in survivors' anxiety scores between pre and post intervention (p = .28). In contrast, caregivers' distress scores significantly decreased from pre to post intervention (p < .01, see Figure 2A).
Caregivers' median distress score prior to participation in Bridge was at or above the critical cutoff for significant distress (median score = 5), but decreased to below the critical cutoff after completing the program (median score = 2). Caregivers' anxiety scores significantly decreased from pre to post intervention (p < .01, see Figure 2B) For survivors with a longer time since diagnosis and longer treatment duration, their caregiver's anxiety tended to stay the same from pre to post Bridge. Survivor and caregiver anxiety and distress scores did not significantly differ by demographic variables or treatment intensity, except for caregivers with an annual household income of less than $50,000 (p = .046). There was no other significant association among treatment duration, time since diagnosis, and survivor and caregiver distress and anxiety.

Perceived preparedness
Survivors' (≥14 years old) and caregivers' understanding of the plan after treatment ends did not significantly change from pre to post intervention (p = .12, .35, respectively). Survivors' and caregivers' understanding of their or their child's potential future health issues after treatment did not significantly differ from pre to post intervention (p = .09, .10, respectively). In contrast, both survivors and caregivers felt significantly more prepared for survivorship care by the oncology team post compared to pre intervention (p = .02, <.01, respectively, see Figure 2C). Survivors and caregivers endorsed a moderate level of preparation across all survey questions prior to participation in Bridge. Survivor and caregiver perceived preparedness scores did not significantly differ by demographic variables, treatment intensity, treatment duration, or time since diagnosis, with the exception of gender. Most mothers had increased preparedness, but most fathers had decreased preparedness from pre to post Bridge (p = .04).

DISCUSSION
The study objective was to evaluate the preliminary impact of a newly developed structured, two-visit program designed to prepare pediatric and AYA survivors and caregivers for the transition from cancer treatment to survivorship care. As hypothesized, Bridge was feasible to participate in and acceptable for most survivors and caregivers.
Specifically, two 30-60-minute visits before and after treatment, which are typically attached to oncology appointments, and the amount and Findings highlight the need for caregiver support and education during their child's transition to survivorship care; augmented survivorship education may be one approach to mitigate caregiver distress.
The importance of providing family-centered psychosocial assessment and supportive care interventions across the cancer care continuum was evidenced by meta-analyses of pediatric cancer studies conducted by Bakula and colleagues, 25,26 which demonstrated a significant relationship between parent distress and child quality of life (small magnitude correlation) and parent and child distress (medium to large magnitude correlation). Early and ongoing assessment and access to interventions for parents and caregivers of children with cancer is a standard of psychosocial care. 27 Delivery of these core psychosocial services to families at the end of treatment or during survivorship visits range from 39.5% to 54.3% based upon a survey of 144 pediatric oncology programs in the United States. 28 A unique component of Bridge was the inclusion of a family-centered psychosocial assessment and consultation for survivors and caregivers. This was included based upon their self-reported need for anticipatory guidance on emotional adjustment and information on psychosocial services at the time of transition to survivorship care. 6 Inclusion of survivor and caregiver feedback as key stakeholders in intervention development and implementation is essential for program acceptability and utilization. 29 This study's preliminary results suggest that Bridge helped AYA cancer survivors and caregivers of survivors feel more prepared for survivorship care and decreased caregivers' anxiety and distress.
Several limitations could impact study results. The decrease in caregivers' anxiety and distress from pre to post intervention may have been related to normative adjustment since treatment ended. Since Bridge is delivered as standard-of-care, it was unethical to evaluate the program using a randomized controlled trial study design as some