Abstract
Background
Survivorship care plans seek to improve the transition to survivorship, but the required resources present implementation barriers. This randomized controlled trial aimed to identify the simplest, most effective approach for survivorship care planning.
Methods
Stage 1-3 breast, colorectal, and prostate cancer patients aged 21 years or older completing treatment were recruited from an urban-academic and rural-community cancer center. Participants were randomly assigned, stratified by recruitment site and cancer type 1:1:1 to a mailed plan, plan delivered during a 1-time transition visit, or plan delivered during a transition visit plus 6-month follow-up visit. Health service use data were collected from participants and medical records for 18 months. The primary outcome, receipt of all plan-recommended care, was compared across intervention arms using logistic regression adjusting for cancer type and recruitment site, with P less than .05 considered statistically significant.
Results
Of 378 participants randomly assigned, 159 (42.1%) were breast, 142 (37.6%) prostate, and 77 (20.4%) colorectal cancer survivors; 207 (54.8%) from the academic site and 171 (45.2%) from the community site; 316 were analyzable for the primary outcome. There was no difference across arms in the proportion of participants receiving all plan-recommended care: 45.2% mail, 50.5% 1-visit, 42.7% 2-visit (2-sided P = .60). Adherence by cancer type for mail, 1-visit, and 2-visit, respectively, was 52.2%, 53.3%, and 40.0% for breast cancer; 48.6%, 64.1%, and 57.1% for prostate cancer; and 23.8%, 19.0%, and 26.1% for colorectal cancer. There were no statistically significant interactions by recruitment site or cancer type.
Conclusions
This study did not find differences in receipt of recommended follow-up care by plan delivery approach. Feasibility and other factors may determine the best approach for survivorship care planning.
When the Institute of Medicine recommended survivorship care plans (SCPs) in its 2006 report, 1 goal was ensuring that cancer survivors knew what follow-up care they needed when (1). However, many randomized controlled trials (RCTs) evaluating SCPs conducted to date have focused on patient-reported outcomes (PROs) and, generally, have not found benefits of SCPs (2-7). Fewer RCTs have evaluated health service use (3,8), and many RCTs have included single, primarily female cancers (2,3,7,8). Further, in the 15 years since the report’s publication, numerous studies have documented the resource burdens of completing SCPs (9-14).
The “Simplifying Survivorship Care Planning” RCT’s objective was to evaluate 3 SCP delivery approaches to identify the simplest, most effective approach, with receipt of SCP-recommended care as the effectiveness measure. Secondary outcomes, reported elsewhere, included feasibility of the intervention arms (15), content of the SCP recommendations and their concordance with guidelines (16-18), PROs (Smith et al., unpublished data), and overuse of tests or procedures not recommended for routine care (eg, laboratory tests in breast cancer survivors) (Sheng et al., unpublished data). Here, we report the primary outcome results.
Methods
Study Design and Purpose
We conducted an RCT in breast, prostate, and colorectal cancer patients recruited from an urban-academic and a rural-community health system to identify the simplest, most effective approach for survivorship care planning (NCT03035773) (19). Three approaches for plan delivery were compared: a mailed plan (“mail”), a plan delivered during a 1-time transition visit (“1-visit”), or a plan delivered during a transition visit plus a 6-month follow-up visit (“2-visit”). Participants were randomly assigned 1:1:1 to the 3 study arms, which were generated by the statistician using randomized blocks of sizes 1 and 2 in the statistical program R (20), separately by cancer type and study site. The assignments were uploaded into REDCap (21) using its built-in randomization module. Study staff generated the REDCap study assignment in real-time for survivors after consent. Due to the nature of the interventions, the study was unblinded.
Participants were followed for 18 months, or until death, diagnosis of recurrent or new cancer, or withdrawal of consent. Health service use was collected from participants and medical records. The primary analysis compared the proportion of patients who received all plan-recommended care during this first year of survivorship. Secondary outcomes included receipt of individual care recommendations (visits, tests or procedures, nonoral medications).
Study Sites and Participants
The study was conducted at 2 sites in Maryland: an urban-academic medical center with separate clinics based on cancer type and specialty (eg, medical vs radiation oncology) and a rural-regional community medical center with 1 general oncology program. Both sites participate in the Johns Hopkins Clinical Research Network, and the Johns Hopkins School of Medicine Institutional Review Board reviewed and approved this study for both sites. Participants had to provide written informed consent to be included.
Eligible participants were aged 21 years or older; diagnosed with new or recurrent stage 1-3 breast, colorectal, or prostate cancer; treated with intent to cure; able to complete data collection in English; and insured privately or by Medicare or Medicaid . Participants had to have completed acute treatment in the past 3 months but could be receiving long-term (>1 year) adjuvant treatment. A participating site had to be “responsible” for the participant’s survivorship care. Participants enrolled in another clinical trial that could influence their health service use were excluded.
Interventions
At the time of study design, the Commission on Cancer (CoC) accreditation standards required survivorship care planning (22), so a “no intervention” arm was not considered relevant. The American Society of Clinical Oncology survivorship care plan templates were adapted by the clinical teams and implemented in the Epic electronic health record (23). Clinical teams were provided with the American Society of Clinical Oncology survivorship guidelines for reference but could use their judgement regarding the patient’s needs when completing the templates and recommending follow-up care. Detailed analyses of the content of these SCPs and their recommendations’ concordance with national guidelines have been published elsewhere (16-18).
The SCP was completed by a nurse, nurse practitioner, or physician assistant within approximately 3 months of treatment completion; added to the patient’s medical record; and delivered via 1 of these interventions: 1) mail: participants were mailed a copy of the SCP with a cover letter signed by a member of the clinical team; 2) 1-visit: participants received their SCP during an in-person visit with a nurse, nurse practitioner, or physician assistant. The visit focused on review of the SCP and offered an opportunity for patients to ask questions about the SCP or associated treatment and survivorship issues; or 3) 2-visit: participants received the 1-visit arm intervention plus a follow-up survivorship visit approximately 6 months after the transition visit. The follow-up visit provided another opportunity to review and discuss the SCP and any persistent or emerging survivorship issues.
Data Collection
At random assignment, we collected basic socio-demographic information (eg, age, race, education), and participants were given a calendar and instructions on tracking their health service use. Participants were asked to record provider visits, tests and procedures, medications, emergency department visits, and hospitalizations. To avoid bias, participants were asked to track all health service use, not only SCP-recommended care. During the 18-month study period, we contacted participants by phone at 6-month intervals to collect their tracked health service use. We also abstracted participants’ medical records for the 18-month study period. In most cases, the records were available to the team electronically, but when necessary, records were ordered from outside providers.
Outcomes
The primary outcome analysis evaluated whether participants received the care recommended by the SCP for the first 12 months of survivorship. However, participants had up to 18 months to receive the recommended care. We used 18 months because care is not always delivered in exact intervals (eg, annual tests might not be received exactly 12 months apart).
First, we abstracted the recommendations from the SCP for visits to specific providers (eg, medical oncologist, surgeon) or to the cancer care team generally (includes radiation oncology, medical oncology, or surgery). We also abstracted recommended tests and procedures and nonoral medications. When the recommendations provided ranges (eg, medical oncologist visit every 3-6 months), we specified a minimum (eg, 2) and maximum (eg, 4) number of visits. If the recommendation was “as needed,” we specified minimum = 0 and no maximum; if “at least,” we specified the relevant minimum and no maximum. If a care plan recommended against a procedure (eg, “routine PET scans are not recommended”), we set maximum = 0.
Second, using data from the participants’ reports by phone and/or their medical record, we categorized the reasons for visits and tests and procedures as cancer related or not and whether the health service use was part of routine follow-up or because of an illness or issue. For the nonoral medications, we recorded the administration dates. We used all health service use data regardless of whether the source was the participant, the medical record, or both.
Third, we compared care receipt with the SCP care recommendations and categorized the results as adherent (≥minimum over 18 months and ≤maximum over 12 months), overuse (>maximum over 12 months), or underuse (<minimum in 18 months). We only included care in the routine cancer-related categories. We examined adherence for specific line items (eg, surgeon visits, colonoscopies) and for the 3 health service use categories: physician visits, tests and procedures, and nonoral medications. For the primary outcome, we combined adherence across all 3 health service use categories to determine overall adherence (yes or no). For the overall outcome, we could not use overuse or underuse because a participant might, for example, have overuse for visits but underuse for tests and procedures.
We only evaluated adherence for care recommended on the SCP. For example, we evaluated adherence, overuse, and underuse for participants who were recommended to see a medical oncologist, but we did not evaluate adherence for patients who were not recommended to see one. However, for the nonoral medications, if patients received medications not on their care plan, it counted as overuse. All health service use data abstraction was checked by a second reviewer, with a research nurse either completing the primary abstraction or secondary review.
Sample Size and Power
We powered our study to detect differences in the primary outcome, the proportion of participants adherent to all SCP recommendations, among study arms with Fisher’s exact test and a 2-sided type I error rate of 5%. A range of adherence proportions was considered, and the target sample size was 375 participants. Assuming 20% attrition, a sample of 300 participants yielded 80% power to detect differences of 5% to 22.5% between study arms. For example, we had 84.2% power to detect differences in the 3 arms of 30.0% vs 37.5% vs 52.5% or 82.2% power to detect differences of 70.0% vs 75.0% vs 87.5%.
Statistical Analysis
To be included in the primary analysis, which was intent to treat, patients must have received an SCP and completed all 18 months of follow-up. We summarized the participant characteristics by cancer type and intervention arm. For SCP recommendations, we descriptively report the mean and range of the minimum, maximum, and total number of visits and tests and procedures recommended. For each type of provider visit, test or procedure, and nonoral medication recommendation, we calculated the proportion of survivors whose care receipt was adherent, overuse, or underuse; we descriptively compared these proportions using Fisher’s exact tests overall, by cancer type, and by recruitment site. The primary analysis evaluated the summary measure of adherence across all recommendations between study arms using logistic regression adjusting for the randomization stratification factors (cancer type and recruitment site). The P value for the primary analysis was calculated from a χ2 test with 2 degrees of freedom comparing models with and without the study arm terms. The consistency of the odds ratios for the primary outcome across cancer types and recruitment sites was assessed with interaction tests. For the primary outcome, 2-sided P less than .05 was considered statistically significant; all other P values are descriptive. Analyses were completed using R version 4.0.3 (20).
Results
Study Population
Between December 2016 and November 2018, 475 patients were screened for eligibility, 97 (20.4%) were excluded (5 ineligible; 92 declined), and 378 were randomly assigned: 126 mail, 125 1-visit, and 127 2-visit (Table 1). The sample included 159 (42.1%) breast, 142 (37.6%) prostate, and 77 (20.4%) colorectal cancer survivors; 207 (54.8%) from the academic site and 171 (45.2%) from the community site. The mean age was 62 years and 77.2% were White. There were 316 (83.6%) participants analyzable for the primary outcome (n = 107 mail; n = 105 1-visit; n = 104 2-visit); reasons for exclusion were similar across arms (Figure 1).
Table 1.
Participant characteristics by cancer type and random assignment arm
| Characteristic | Breast (n = 159) |
Prostate (n = 142) |
Colorectal (n = 77) |
||||||
|---|---|---|---|---|---|---|---|---|---|
| Mail (n = 52) | 1-visit (n = 53) | 2-visit (n = 54) | Mail (n = 48) | 1-visit (n = 47) | 2-visit (n = 47) | Mail (n = 26) | 1-visit (n = 25) | 2-visit (n = 26) | |
| Study site, No. (%) | |||||||||
| Urban academic | 29 (55.8) | 30 (56.6) | 30 (55.6) | 23 (47.9) | 23 (48.9) | 22 (46.8) | 17 (65.4) | 16 (64.0) | 17 (65.4) |
| Rural community | 23 (44.2) | 23 (43.4) | 24 (44.4) | 25 (52.1) | 24 (51.1) | 25 (53.2) | 9 (34.6) | 9 (36.0) | 9 (34.6) |
| Mean age (SD), y | 59.4 (10.7) | 58.4 (11.9) | 56.5 (12.6) | 68.3 (8.1) | 67.9 (7.4) | 67.6 (6.4) | 60.8 (10.8) | 55.8 (14.0) | 57.3 (13.7) |
| Stage, No. (%) | |||||||||
| 1 | 32 (61.5) | 22 (41.5) | 23 (42.6) | 0 (0) | 2 (4.3) | 1 (2.1) | 2 (7.7) | 1 (4.0) | 1 (3.8) |
| 2 | 11 (21.2) | 19 (35.8) | 17 (31.5) | 19 (39.6) | 17 (36.2) | 15 (31.9) | 4 (15.4) | 4 (16.0) | 3 (11.5) |
| 3 | 2 (3.8) | 3 (5.7) | 3 (5.6) | 5 (10.4) | 2 (4.3) | 7 (14.9) | 2 (7.7) | 5 (20.0) | 4 (15.4) |
| Recurrent, No. (%) | 2 (3.8) | 1 (1.9) | 1 (1.9) | 1 (2.1) | 2 (4.3) | 2 (4.3) | 0 (0) | 0 (0) | 0 (0) |
| TNM only/stage unknown, No. (%) | 5 (9.6) | 8 (15.1) | 10 (18.5) | 23 (47.9) | 24 (51.1) | 22 (46.8) | 18 (69.2) | 15 (60.0) | 18 (69.2) |
| Sex, No. (%) | |||||||||
| Male | 0 (0) | 0 (0) | 0 (0) | 48 (100) | 47 (100) | 47 (100) | 16 (61.5) | 12 (48.0) | 16 (61.5) |
| Female | 52 (100) | 53 (100) | 54 (100) | 0 (0) | 0 (0) | 0 (0) | 10 (38.5) | 13 (52.0) | 10 (38.5) |
| Race, No. (%) | |||||||||
| Black/African American | 10 (19.2) | 13 (24.5) | 12 (22.2) | 12 (25.0) | 10 (21.3) | 9 (19.1) | 2 (7.7) | 5 (20.0) | 2 (7.7) |
| White | 38 (73.1) | 40 (75.5) | 39 (72.2) | 36 (75.0) | 37 (78.7) | 37 (78.7) | 23 (88.5) | 20 (80.0) | 22 (84.6) |
| Other | 4 (7.7) | 0 (0) | 3 (5.6) | 0 (0) | 0 (0) | 1 (2.1) | 1 (3.8) | 0 (0) | 2 (7.7) |
| Hispanic ethnicity | 2 (3.8) | 1 (1.9) | 3 (5.6) | 1 (2.1) | 1 (2.1) | 0 (0) | 3 (11.5) | 1 (4.0) | 1 (3.8) |
| Education, No. (%)a | |||||||||
| <High school graduate | 4 (7.7) | 4 (7.5) | 2 (3.7) | 1 (2.1) | 4 (8.5) | 0 (0) | 0 (0) | 0 (0) | 0 (0) |
| High school graduate | 7 (13.5) | 5 (9.4) | 9 (16.7) | 7 (14.6) | 11 (23.4) | 10 (21.3) | 4 (15.4) | 5 (20.0) | 7 (26.9) |
| Some college | 11 (21.2) | 12 (22.6) | 13 (24.1) | 9 (18.8) | 7 (14.9) | 10 (21.3) | 4 (15.4) | 4 (16.0) | 4 (15.4) |
| College graduate | 13 (25.0) | 16 (30.2) | 10 (18.5) | 15 (31.2) | 9 (19.1) | 9 (19.1) | 10 (38.5) | 10 (40.0) | 9 (34.6) |
| Any postgraduate work | 17 (32.7) | 16 (30.2) | 20 (37) | 16 (33.3) | 16 (34.0) | 18 (38.3) | 8 (30.8) | 6 (24.0) | 5 (19.2) |
| Marital status, No. (%)a | |||||||||
| Married (or civil union) | 35 (67.3) | 33 (62.3) | 34 (63.0) | 35 (72.9) | 36 (76.6) | 36 (76.6) | 18 (69.2) | 16 (64.0) | 17 (65.4) |
| Divorced | 8 (15.4) | 9 (17.0) | 9 (16.7) | 4 (8.3) | 7 (14.9) | 5 (10.6) | 3 (11.5) | 3 (12.0) | 3 (11.5) |
| Widowed | 5 (9.6) | 5 (9.4) | 4 (7.4) | 7 (14.6) | 1 (2.1) | 4 (8.5) | 3 (11.5) | 1 (4.0) | 2 (7.7) |
| Separated | 1 (1.9) | 1 (1.9) | 2 (3.7) | 1 (2.1) | 1 (2.1) | 0 (0) | 0 (0) | 1 (4.0) | 0 (0) |
| Never married | 3 (5.8) | 5 (9.4) | 5 (9.3) | 1 (2.1) | 2 (4.3) | 2 (4.3) | 2 (7.7) | 4 (16.0) | 3 (11.5) |
| Employment, No. (%) | |||||||||
| Work for pay full-time | 24 (46.2) | 20 (37.7) | 25 (46.3) | 17 (35.4) | 17 (36.2) | 13 (27.7) | 14 (53.8) | 10 (40.0) | 13 (50) |
| Work for pay part-time | 2 (3.8) | 5 (9.4) | 4 (7.4) | 2 (4.2) | 5 (10.6) | 5 (10.6) | 2 (7.7) | 4 (16.0) | 1 (3.8) |
| Not working | 13 (25) | 18 (34.0) | 15 (27.8) | 14 (29.2) | 16 (34.0) | 17 (36.2) | 6 (23.1) | 8 (32.0) | 6 (23.1) |
| Not answered | 13 (25) | 10 (18.9) | 10 (18.5) | 15 (31.2) | 9 (19.1) | 12 (25.5) | 4 (15.4) | 3 (12.0) | 6 (23.1) |
| Has internet access, No. (%)a | |||||||||
| Dial-up/low-speed | 1 (1.9) | 1 (1.9) | 1 (1.9) | 2 (4.2) | 0 (0) | 3 (6.4) | 1 (3.8) | 1 (4.0) | 1 (3.8) |
| High-speed | 42 (80.8) | 41 (77.4) | 38 (70.4) | 29 (60.4) | 32 (68.1) | 33 (70.2) | 19 (73.1) | 16 (64.0) | 18 (69.2) |
| Other/type unknown | 2 (3.8) | 1 (1.9) | 5 (9.3) | 4 (8.3) | 2 (4.2) | 0 (0) | 3 (11.5) | 5 (20.0) | 1 (3.8) |
| None | 7 (13.5) | 10 (18.9) | 10 (18.5) | 13 (27.1) | 13 (27.7) | 11 (23.4) | 3 (11.5) | 3 (12.0) | 5 (19.2) |
Missing for 1 colorectal “2-visit” participant.
Figure 1.
CONSORT flow diagram. SCP = survivorship care plan; w/d = withdrew.
SCP Recommendations
Recommendations for visits, tests and procedures, and nonoral medications by cancer type are reported in Table 2. Of the 159 breast cancer survivors, 128 had visit recommendations, with medical oncology, surgery, radiation oncology, and primary care most common. On average, the minimum total number of recommended visits was at least 4 and the maximum nearly 11. In terms of tests and procedures, 136 had recommendations, with physical (with or without history) and mammogram most common. There were 9 recommendations for nonoral medications.
Table 2.
Recommendations from the survivorship care plans for visits, tests or procedures, and nonoral medications for the first 12 months of survivorship
| Recommended visits and tests or procedures | Breast (n = 159) |
Prostate (n = 142) |
Colorectal (n = 77) |
||||||
|---|---|---|---|---|---|---|---|---|---|
| No. for, againsta | Minimum, mean (range) | Maximum,b mean (range) | No. for, againsta | Minimum, mean (range) | Maximum,b mean (range) | No. for, againsta | Minimum, mean (range) | Maximum,b mean (range) | |
| Visits | |||||||||
| Medical oncology | 67, 0 | 2 (2, 2) | 4.96 (3, 5) | 0, 0 | — | — | 24, 0 | 2.21 (2, 4) | 4.96 (4, 5) |
| Urology | 0, 0 | — | — | 66, 0 | 2 (2, 2) | 3 (3, 3) | 1, 0 | 1 (1, 1) | 2 (2, 2) |
| Surgery | 67, 0 | 2 (1, 3) | 4.94 (2, 5) | 0, 0 | — | — | 33, 0 | 2.58 (1, 4) | 4.77 (3, 5) |
| Radiation oncology | 67, 0 | 2 (2, 2) | 4.96 (3, 5) | 66, 0 | 2 (2, 2) | 3 (3, 3) | 4, 0 | 2.75 (2, 4) | 4.75 (4, 5) |
| Primary care | 94, 0 | 1 (1, 1) | 2.2 (2, 3) | 66, 0 | 1 (1, 1) | 2 (2, 2) | 23, 0 | 1 (1, 1) | 2.05 (2, 3) |
| Cancer care teamc | 38, 0 | 2.71 (1, 4) | 4.84 (3, 5) | 0, 0 | — | — | 19, 0 | 2.16 (1, 4) | 4.94 (4, 5) |
| Otherd | 7, 0 | — | — | 0, 0 | — | — | 6, 0 | 1 (1, 1) | 2 (2, 2) |
| Totale | 128, 0 | 4.63 (1, 7) | 10.73 (2, 17) | 66, 0 | 5 (5, 5) | 8 (8, 8) | 60, 0 | 3.64 (1, 12) | 7.61 (3, 15) |
| Tests or procedures | |||||||||
| Physical ± history | 134, 0 | 2.04 (1, 4) | 4.54 (2, 5) | 0, 0 | — | — | 31, 0 | 2.1 (1, 4) | 4.52 (2, 5) |
| MRI | 5, 1 | 1 (1, 1) | 2 (2, 2) | 0, 0 | — | — | 0, 0 | — | — |
| Mammogram | 114, 13 | 1.06 (1, 2) | 2.08 (2, 3) | 0, 0 | — | — | 0, 0 | — | — |
| Colonoscopy | 3, 0 | 1 (1, 1) | 2 (2, 2) | 0, 0 | — | — | 60, 0 | 1 (1, 1) | 2 (2, 2) |
| CT imaging | 0, 15 | — | — | 0, 0 | — | — | 63, 0 | 1.70 (1, 3) | 2.81 (2, 5) |
| PET or CT | 0, 15 | — | — | 0, 0 | — | — | 1, 0 | 2 (2, 2) | 3 (3, 3) |
| CEA | 0, 0 | — | — | 0, 0 | — | — | 65, 0 | 3. 31 (1, 4) | 4.94 (3, 5) |
| CBC | 0, 0 | — | — | 0, 0 | — | — | 22, 0 | 2.73 (2, 4) | 5 (5, 5) |
| PSA | 0, 0 | — | — | 111, 0 | 1.46 (1, 4) | 3.28 (3, 5) | 0, 0 | — | — |
| Bone density | 16, 6 | 2.67 (1, 6) | 2.71 (2, 7) | 3, 0 | — | — | 0, 0 | — | — |
| Testosterone | 0, 0 | — | — | 14, 0 | 2 (2, 2) | 3.33 (3, 5) | 0, 0 | — | — |
| Flu vaccine | 1, 0 | 1 (1, 1) | 2 (2, 2) | 0, 0 | — | — | 0, 0 | — | — |
| Pap smear | 2, 0 | 1 (1, 1) | 2 (2, 2) | 0, 0 | — | — | 0, 0 | — | — |
| Pelvic exam | 3, 0 | 1 (1, 1) | 2 (2, 2) | 0, 0 | — | — | 0, 0 | — | — |
| Totale | 135, 1 | 3.07 (1, 10) | 6.6 (3, 12) | 111, 0 | 1.68 (1, 4) | 3.71 (3, 10) | 65, 0 | 8.75 (4, 17) | 15.09 (5, 27) |
| Nonoral medications | |||||||||
| Leuprolide | 0, 0 | — | — | 35, 7 | 1.2 (1, 2) | 4.2 (2, 13) | 0, 0 | — | — |
| Goserelin | 4, 1 | 1 (1, 1) | 13 (13, 13) | 0, 0 | — | — | 0, 0 | — | — |
| Trastuzumab | 3, 0 | 1 (1, 1) | 13 (13, 13) | 0, 0 | — | — | 0, 0 | — | — |
| Pertuzumab | 1,0 | 1 (1,1) | 13 (13,13) | 0, 0 | — | — | 0, 0 | — | — |
| Triptorelin | 0, 0 | — | — | 2, 0 | 2 (2, 2) | 3 (3, 3) | 0, 0 | — | — |
| Degarelix | 0, 0 | — | — | 1, 0 | 1 (1, 1) | — | 0, 0 | — | — |
| Leuprolide/triptorelinf | 0, 0 | — | — | 5, 0 | 2.2 (1, 4) | 3.2 (2, 5) | 0, 0 | — | — |
The first number is the number of participants whose SCPs recommended visits or tests or procedures, including recommendations of “as needed” or “at least” a minimum; the second number reflects the frequency of SCP recommendations against a test/procedure. “—” = not applicable; CBC = complete blood count; CEA = carcinoembryonic antigen; CT = computed tomography; MRI = magnetic resonance imaging; PET = positron emission tomography; PSA = prostate-specific antigen.
Calculation of the mean (range) maximum excludes participants with recommendations against or a recommendation of “as needed” or “at least.”
Cancer care team includes visits to providers in any of the following specialties: radiation oncology, medical oncology, or surgery.
Other includes gynecology, plastic surgery, physical therapy, and genetic counseling.
Total was calculated by taking the sum of the minimum number of recommendations and sum of the maximum number of recommendations across visits, tests or procedures, and nonoral medications for each patient and then calculating the corresponding summary statistics (mean, range) among the patient-level sums.
For some participants, a combination of the 2 medications was recommended.
Of 142 prostate cancer survivors, 66 had visit recommendations to urology, radiation oncology, and primary care, with a minimum of 5 visits and maximum of 8 visits recommended, on average (Table 2). Prostate-specific antigen was the most common test or procedure recommended. There were 50 recommendations for nonoral medications.
Of the 77 colorectal survivors, 60 had recommendations for visits, with medical oncology, surgery, and primary care most common; total visits recommended ranged from a minimum of 3.64 to a maximum of 7.61, on average (Table 2). Carcinoembryonic antigen, computed tomography, and colonoscopy were the most commonly recommended tests and procedures.
Adherence to SCP Recommendations
Overall, there was no difference across arms in the primary outcome, the proportion of participants who received all plan-recommended care: 45.2% mail, 50.5% 1-visit, and 42.7% 2-visit (P = .60) (Figure 2). The associated adjusted odds ratios (95% confidence intervals) were 1.22 (0.70 to 2.15) for 1-visit vs mail, 0.92 (0.52 to 1.63) for 2-visit vs mail, and 0.75 (0.43 to 1.33) for 2-visit vs 1-visit. The differences between arms did not vary by cancer type (Pinteraction = .56) or recruitment site (Pinteraction = .86). Overall adherence by cancer type for mail, 1-visit, and 2-visit, respectively, was 52.2%, 53.3%, and 40.0% for breast cancer; 48.6%, 64.1%, and 57.1% for prostate cancer; and 23.8%, 19.0%, and 26.1% for colorectal cancer.
Figure 2.
Proportion of survivors who received all recommended care from the survivorship care plan by intervention arm overall, by cancer type, and by recruitment site. P value for the overall analysis is from a logistic regression model adjusting for randomization stratification factors (cancer type, recruitment site). Interaction P values are from logistic regression analyses that tested for the interaction between either cancer type and intervention arm, or recruitment site and intervention arm. All statistical tests were 2-sided. There were 4 patients who had no recommendations in their survivorship care plan who are excluded from this analysis.
There were also no differences in receipt of recommended care by category of health service use (Tables 3 and 4; Supplementary Tables 1 and 2, available online). The proportion of participants who had the recommended number of visits was 53.4% mail, 54.8% 1-visit, and 53.7% 2-visit (P = .99). The proportion undergoing recommended tests or procedures was 78.8% mail, 77.2% 1-visit, and 73.0% 2-visit (P = .62). The proportion receiving recommended nonoral medications was 66.7% mail, 75.0% 1-visit, and 73.7% 2-visit (P = .87). Figure 3 displays adherence to recommended visits and tests and procedures by cancer type.
Table 3.
Proportion of patients who received recommended visits overall and by recruitment site
| Adherence with visit recommendations | Overall (n = 254) |
Academic (n = 102) |
Community (n = 152) |
|||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1-visit | 2-visit | P a | 1-visit | 2-visit | P a | 1-visit | 2-visit | P a | ||||
| Medical oncology, No. | 31 | 29 | 31 | 3 | 5 | 2 | 28 | 24 | 29 | |||
| Adherent, No. (%) | 28 (90.3) | 25 (86.2) | 25 (80.6) | .54 | 1 (3.33) | 2 (40.0) | 0 (0) | >.99 | 27 (96.4) | 23 (95.8) | 25 (86.2) | .10 |
| Underuse, No. (%) | 3 (9.7) | 3 (10.3) | 6 (19.4) | 2 (66.7) | 3 (60.0) | 2 (100) | 1 (3.6) | 0 (0) | 4 (13.8) | |||
| Overuse, No. (%) | 0 (0) | 1 (3.4) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 1 (4.2) | 0 (0) | |||
| Urology, No. | 25 | 22 | 20 | 0 | 1 | 0 | 25 | 21 | 20 | |||
| Adherent, No. (%) | 22 (88.0) | 16 (72.7) | 16 (80.0) | .14 | — | 0 (0) | — | — | 22 (88) | 16 (76.2) | 16 (80.0) | .24 |
| Underuse, No. (%) | 1 (4.0) | 6 (27.3) | 3 (15.0) | — | 1 (100) | — | 1 (4.0) | 5 (23.8) | 3 (15.0) | |||
| Overuse, No. (%) | 2 (8.0) | 0 (0) | 1 (5.0) | — | 0 (0) | — | 2 (8.0) | 0 (0) | 1 (5.0) | |||
| Surgery, No. | 29 | 35 | 36 | 3 | 8 | 7 | 26 | 27 | 29 | |||
| Adherent, No. (%) | 26 (89.7) | 29 (82.9) | 31 (86.1) | .67 | 1 (33.3) | 5 (62.5) | 5 (74.1) | .68 | 25 (96.2) | 24 (88.9) | 26 (89.7) | .69 |
| Underuse, No. (%) | 3 (10.3) | 6 (17.1) | 5 (13.9) | 2 (66.7) | 3 (37.5) | 2 (28.6) | 1 (3.8) | 3 (11.1) | 3 (10.3) | |||
| Overuse, No. (%) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | |||
| Radiation oncology, No. | 48 | 45 | 44 | 2 | 3 | 0 | 46 | 42 | 44 | |||
| Adherent, No. (%) | 36 (75.0) | 32 (71.1) | 42 (95.5) | .004 | 0 (0) | 2 (66.7) | — | — | 36 (78.3) | 30 (71.4) | 42 (95.5) | .007 |
| Underuse, No. (%) | 11 (22.9) | 12 (26.7) | 1 (2.3) | 2 (100) | 1 (33.3) | — | 9 (19.6) | 11 (26.2) | 1 (2.3) | |||
| Overuse, No. (%) | 1 (2.1) | 1 (2.2) | 1 (2.3) | 0 (0) | 0 (0) | — | 1 (2.2) | 1 (2.4) | 1 (2.3) | |||
| Primary care,b No. | 66 | 56 | 61 | 12 | 8 | 10 | 53 | 48 | 51 | |||
| Adherent, No. (%) | 48 (72.7) | 40 (71.4) | 43 (70.5) | .98 | 8 (61.5) | 5 (62.5) | 8 (80.0) | .62 | 40 (75.5) | 35 (72.9) | 35 (68.6) | .75 |
| Underuse, No. (%) | 18 (27.3) | 16 (28.6) | 18 (29.5) | 5 (38.5) | 3 (37.5) | 2 (20.0) | 13 (24.5) | 13 (27.1) | 16 (31.4) | |||
| Cancer care team,c No. | 20 | 21 | 16 | 20 | 21 | 16 | 0 | 0 | 0 | |||
| Adherent, No. (%) | 10 (50.0) | 16 (76.2) | 9 (56.2) | .03 | 10 (50.0) | 16 (76.2) | 9 (56.2) | .03 | — | — | — | — |
| Underuse, No. (%) | 5 (25.0) | 0 (0) | 0 (0) | 5 (25.0) | 0 (0) | 0 (0) | — | — | — | |||
| Overuse, No. (%) | 5 (25.0) | 5 (23.8) | 7 (43.8) | 5 (25.0) | 5 (23.8) | 7 (43.8) | — | — | — | |||
| Other,d No. | 3 | 7 | 3 | 3 | 7 | 3 | 0 | 0 | 0 | |||
| Adherent, No. (%) | 2 (66.7) | 5 (71.4) | 3 (100) | >.99 | 2 (66.7) | 5 (71.4) | 3 (100) | >.99 | — | — | — | — |
| Underuse, No. (%) | 1 (33.3) | 2 (28.6) | 0 (0) | 1 (33.3) | 2 (28.6) | 0 (0) | — | — | — | |||
| Overuse, No. (%) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0 (0) | — | — | — | |||
| Total, No. | 88 | 84 | 82 | 35 | 36 | 31 | 53 | 48 | 51 | |||
| Adherent, No. (%) | 47 (53.4) | 46 (54.8) | 44 (53.7) | .99 | 17 (48.6) | 22 (61.1) | 18 (58.1) | .56 | 30 (56.6) | 24 (50.0) | 26 (50.9) | .77 |
| Nonadherent, No. (%) | 41 (46.6) | 38 (45.2) | 38 (46.3) | 18 (51.4) | 14 (38.9) | 13 (41.9) | 23 (43.4) | 24 (50.0) | 25 (49.0) | |||
Fisher’s exact test. All statistical tests were 2-sided. “—” = not applicable.
Overuse of primary care was not considered an option.
Cancer care team includes visits to providers in any of the following specialties: radiation oncology, medical oncology, or surgery.
Other includes gynecology, plastic surgery, physical therapy, genetics counseling.
Table 4.
Proportion of patients who received recommended visits by cancer type
| Adherence with visit recommendations | Breast (n = 128) |
Prostate (n = 66) |
Colorectal (n = 60) |
|||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1-visit | 2-visit | P a | 1-visit | 2-visit | P a | 1-visit | 2-visit | P a | ||||
| Medical oncology, No. | 21 | 23 | 23 | 0 | 0 | 0 | 10 | 6 | 8 | |||
| Adherent, No. (%) | 20 (95.2) | 22 (95.7) | 19 (82.6) | .10 | — | — | — | — | 8 (80.0) | 3 (50.0) | 6 (75.0) | .53 |
| Underuse, No. (%) | 1 (4.8) | 0 (0) | 4 (17.4) | — | — | — | 2 (20.0) | 3 (50.0) | 2 (25.0) | |||
| Overuse, No. (%) | 0 (0) | 1 (4.3) | 0 (0) | — | — | — | 0 (0) | 0 (0) | 0 (0) | |||
| Urology, No. | 0 | 0 | 0 | 25 | 21 | 20 | 0 | 1 | 0 | |||
| Adherent, No. (%) | — | — | — | — | 22 (88) | 16 (76.2) | 16 (80.0) | .24 | — | 0 (0) | — | — |
| Underuse, No. (%) | — | — | — | 1 (4.0) | 5 (23.8) | 3 (15.0) | — | 1 (100) | — | |||
| Overuse, No. (%) | — | — | — | 2 (8.0) | 0 (0) | 1 (5.0) | — | 0 (0) | — | |||
| Surgery, No. | 21 | 22 | 24 | 0 | 0 | 0 | 8 | 13 | 12 | |||
| Adherent, No. (%) | 21 (100) | 20 (90.9) | 22 (91.7) | .54 | — | — | — | — | 5 (62.5) | 9 (69.2) | 9 (75.0) | .89 |
| Underuse, No. (%) | 0 (0) | 2 (9.1) | 2 (8.3) | — | — | — | 3 (37.5) | 4 (30.8) | 3 (25.0) | |||
| Overuse, No. (%) | 0 (0) | 0 (0) | 0 (0) | — | — | — | 0 (0) | 0 (0) | 0 (0) | |||
| Radiation oncology, No. | 21 | 23 | 23 | 25 | 21 | 20 | 2 | 1 | 1 | |||
| Adherent, No. (%) | 17 (81.0) | 15 (65.2) | 22 (95.7) | .03 | 19 (76) | 16 (76.2) | 19 (95.0) | .18 | 0 (0) | 1 (100) | 1 (100) | .33 |
| Underuse, No. (%) | 4 (19.0) | 8 (34.8) | 1 (4.3) | 5 (20.0) | 4 (19.0) | 0 (0) | 2 (100) | 0 (0) | 0 (0) | |||
| Overuse, No. (%) | 0 (0) | 0 (0) | 0 (0) | 1 (4.0) | 1 (4.8) | 1 (5.0) | 0 (0) | 0 (0) | 0 (0) | |||
| Primary care,b No. | 32 | 29 | 33 | 25 | 21 | 20 | 9 | 6 | 8 | |||
| Adherent, No. | 24 (75.0) | 21 (72.4) | 21 (63.6) | .61 | 18 (72.0) | 16 (76.2) | 15 (75.0) | >.99 | 6 (66.7) | 3 (50.0) | 7 (87.5) | .33 |
| Underuse, No. | 8 (25.0) | 8 (27.6) | 12 (36.4) | 7 (28.0) | 5 (23.8) | 5 (25.0) | 3 (33.3) | 3 (50.0) | 1 (12.5) | |||
| Cancer care team,c No. | 12 | 15 | 11 | 0 | 0 | 0 | 8 | 6 | 5 | |||
| Adherent, No. (%) | 5 (41.7) | 11 (73.3) | 4 (36.4) | .09 | — | — | — | — | 5 (62.5) | 5 (83.3) | 5 (100) | .17 |
| Underuse, No. (%) | 2 (16.7) | 0 (0) | 0 (0) | — | — | — | 3 (37.5) | 0 (0) | 0 (0) | |||
| Overuse, No. (%) | 5 (41.7) | 4 (26.7) | 7 (63.6) | — | — | — | 0 (0) | 1 (16.7) | 0 (0) | |||
| Other,d No. | 2 | 3 | 2 | 0 | 0 | 0 | 1 | 4 | 1 | |||
| Adherent, No. (%) | 2 (100) | 3 (100) | 2 (100) | >.99 | — | — | — | — | 0 (0) | 2 (50.0) | 1 (100) | >.99 |
| Underuse, No. (%) | 0 (0) | 0 (0) | 0 (0) | — | — | — | 1 (100) | 2 (50.0) | 0 (0) | |||
| Overuse, No. (%) | 0 (0) | 0 (0) | 0 (0) | — | — | — | 0 (0) | 0 (0) | 0 (0) | |||
| Total, No. | 43 | 42 | 43 | 25 | 21 | 20 | 20 | 21 | 19 | |||
| Adherent, No. | 25 (58.1) | 24 (57.1) | 20 (46.5) | .50 | 12 (48.0) | 12 (57.1) | 11 (55.0) | .82 | 10 (50.0) | 10 (47.6) | 13 (68.4) | .38 |
| Nonadherent, No. | 18 (41.9) | 18 (42.9) | 23 (53.5) | 13 (52.0) | 9 (42.9) | 9 (45.0) | 10 (50.0) | 11 (52.4) | 6 (31.6) | |||
Fisher’s exact test. All statistical tests were 2-sided. “—” = not applicable.
Overuse of primary care was not considered an option.
Cancer care team includes visits to providers in any of the following specialties: radiation oncology, medical oncology, or surgery.
Other includes gynecology, plastic surgery, physical therapy, genetics counseling.
Figure 3.
Proportion of survivors who received all recommended visits and tests or procedures from the survivorship care plan by intervention arm and cancer type. There was 1 breast cancer patient, 1 prostate cancer patient, and 2 colorectal cancer patients who had no recommendations in their survivorship care plan who are excluded from this analysis.
In descriptive analyses examining the visits to specific provider specialties, differences in adherence were found for radiation oncology and cancer care team (Tables 3 and 4). The radiation oncology differences favored the 2-visit arm overall (75.0% mail, 71.1% 1-visit, 95.5% 2-visit; P = .004) as well as in the community site (78.3% mail, 71.4% 1-visit, 95.5% 2-visit; P = .007) and breast cancer (81.0% mail, 65.2% 1-visit, 95.7% 2-visit; P = .03). The cancer care team visit differences favored the 1-visit arm (50.0% mail, 76.2% 1-visit, 56.2% 2-visit; P = .03), a difference also found for the academic site. In descriptive analyses examining adherence to specific tests or procedures overall, the only statistically significant difference was computed tomography imaging at the academic site favoring 1-visit (62.5% mail, 95.2% 1-visit, 70.0% 2-visit; P = .04) (Supplementary Tables 1 and 2, available online).
Discussion
This study evaluated 3 approaches for survivorship care planning to find the simplest, most effective approach. We found no statistically significant differences in overall adherence to SCP recommendations by SCP delivery method. Overall adherence rates ranged from 42.7% (2-visit) to 50.5% (1-visit). Although it may represent simple statistical variation, that the 2-visit arm had lower adherence than the 1-visit and mail arms suggests that greater intervention intensity does not necessarily lead to greater effectiveness. Notably, as reported separately (15), intervention fidelity was higher at the community site than at the academic site, yet there were still similar patterns of adherence across study arms. We also found no statistically significant differences by intervention arm by health service use category (ie, visits, tests and procedures, nonoral medications). Although descriptive analyses identified statistically significant differences favoring the 2-visit arm for radiation oncology and 1-visit arm for cancer care team visits and computed tomography imaging, the differences were most likely due to chance; even if not due to chance, they favor different arms and do not support the superiority of 1 arm.
Strengths of the study include the randomized design, comparison of 3 intervention arms, and broad representation (3 cancer types including males and females, 1 urban-academic and 1 rural-community health system). Unlike other studies that focused on PRO endpoints (2–7), this study evaluated how SCP delivery approaches affected adherence to follow-up care recommendations. Unlike other studies that assessed adherence (3,8), we collected data on health service use from both patients and medical records. Because we used the medical record rather than administrative claims, we could categorize the reasons for health service use (ie, cancer-related or not) and whether it was routine or in response to a problem. In addition to the quantitative findings reported here, we have qualitative and PRO data (Smith et al., unpublished data) and are undertaking an analysis of overuse that focuses on a predefined list of tests or procedures (eg, breast cancer tumor markers, PET scans) and how often they were performed in the absence of an SCP recommendation.
Limitations include requiring insurance for study eligibility and the inability to blind. Although 22.8% of the sample was non-White, there were few Hispanic participants; other studies have demonstrated differences in Hispanic populations’ needs and SCP impact (7,8). Because this was not an equivalence trial, we cannot conclude that the 3 approaches are equally effective, but the evidence from this study does not support promoting 1 approach over another. The observed differences of 2.5% to 7.8% between arms would have required a much larger sample size to detect, and the clinical meaningfulness of these differences are questionable. The CoC was mandating SCP delivery at the time of study design (22), so we did not include a control arm. SCPs remain important in the current CoC Survivorship Program standards (24). We cannot comment on whether any of the SCP delivery methods is better than none. An RCT comparing SCPs with usual care did not find differences in adherence to follow-up guidelines or health service use (3), though this study examined health service use more broadly and evaluated all SCP-recommended care. The appropriate level of overall adherence is unclear, and adherence to recommendations is an incomplete surrogate for clinical outcomes, which are the ultimate evidence of effectiveness. Based on these findings and the changes in the CoC standards, we suggest that future studies focus on evaluating survivorship care more broadly rather than focusing on SCP content and delivery specifically.
Several factors might influence the absolute estimates of adherence but not the comparison among intervention arms. We included health service use reported in the medical record and/or by the patient without prioritizing 1 source over the other. Because this approach applied across arms, it would not be expected to bias the comparison. Missing outside information, incomplete clinic notes, or other reasons could result in misclassifying care as cancer related (vs not) and routine (vs for-cause), which would affect our absolute estimates, but not the comparison across arms. The COVID-19 pandemic occurred towards the end of the 18-month observation period for the last enrolled participants and might have influenced health-care utilization, but, again, not the comparison among arms.
We evaluated whether survivors received recommended care within 12 months, but not whether the timing within the 12 months was appropriate (eg, 4 visits in 12 months, but not 4 visits every 3 months). Because SCPs are a static document, our analysis does not account for changes made to recommendations after the SCP was delivered. For example, the nurse completing SCPs at the community site was not always aware of whether the patient would be recommended nonoral medications. If the patient received a nonoral medication but the SCP did not indicate that this was recommended, s/he would be counted as an overuser. Although such situations would not bias the comparison across SCP intervention arms, static documents are a weakness of SCPs overall, and this example highlights this limitation (15).
In summary, this RCT found no differences in 3 different SCP delivery approaches of varying intensity. Although we cannot conclude that the 3 approaches are equivalent, the evidence here does not support recommending 1 approach over another. Health systems may consider feasibility and other factors in implementing SCPs.
Funding
This work was supported by a Patient-Centered Outcomes Research Institute (PCORI) Award (IHS-1409-22534). Drs Snyder, Peairs, Tran, Johnston, Wolff, and Smith are members of the Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins (P30CA006973).
Notes
Role of the funder: The funder had no role in the design of the study; execution, collection, or analysis of the data; or decision to submit this article for publication.
Disclosures: Dr Snyder receives research funding from Genentech and Pfizer through Johns Hopkins and previously received royalties from UptoDate for authorship related to survivorship. Dr Tran received research funding from Astellas Pharm, Bayer Healthcare, and RefleXion Medial Inc; personal fees from Consulting from RefleXion, grants from RefleXion, personal fees from Noxopharm, Janssen-Taris Biomedical, Myovant and AstraZeneca outside the submitted work; and has a patent 9114158—Compounds and Methods of Use in Ablative Radiotherapy licensed to Natsar Pharm. Dr Johnston is funded through the AHRQ 1K08HS024736. Dr Peairs and Dr Choi receive research funding from a Merck Foundation grant through Johns Hopkins. All other authors have no conflicts of interest to declare.
Author contributions: Conceptualization (CFS, ET, ACW, KCS), Data Curation (ALB, JD, NM, SR, SW), Formal analysis (ALB), Funding acquisition (CFS, ALB, JB, JM, KSP, EDT, PTT, ACW, KCS), Investigation (all authors), Methodology (CFS, YC, ALB, JD, NM, SR, SW, KCS), Project administration (CFS, DEC, RLJ, JM, KCS), Resources (FJ, PTT, ACW), Supervision (CFS, DEC, RLJ, JM, KCS), Validation (CFS, ALB, JD, NM, SR, SW, KCS), Visualization (CFS), Writing—original draft (CFS), Writing—review and editing (all authors).
Prior presentations: Presented at a Poster Discussion session at the 2021 ASCO Annual Meeting.
Disclaimers: The statements in this publication are solely the responsibility of the authors and do not necessarily represent the views of PCORI, its Board of Governors or Methodology Committee.
Acknowledgements: We thank David Lim for assistance with data analysis reproducibility. We are most grateful to the study participants and the clinic staff members who implemented the interventions.
Data Availability
The data underlying this article cannot be shared publicly due to participant privacy concerns and because of the protected health information collected. The data will be shared on reasonable request to the corresponding author.
Supplementary Material
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Data Availability Statement
The data underlying this article cannot be shared publicly due to participant privacy concerns and because of the protected health information collected. The data will be shared on reasonable request to the corresponding author.