Abstract
Purpose:
We developed and tested a multi-level intervention, ConnectedCancerCare (CCC), which includes a tailored website and appointment reminder system for women with early-stage breast cancer and a provider summary letter sent to their medical oncologist and primary care provider to improve the delivery of team-based survivorship care.
Methods:
We conducted a pilot randomized controlled trial to establish the feasibility and acceptability of CCC. Women diagnosed with stages 0-II breast cancer within one year of completing primary treatment were randomized to CCC (intervention), or a static online survivorship care plan (control). Participants completed baseline and 3 month follow-up surveys online. Post-trial interviews with 5 PCPs, 6 oncology providers, and 8 intervention patients were conducted.
Results:
Of the 160 eligible women invited to participate, 66 completed the baseline survey and were randomized (41%), and 54 completed a follow-up survey (83%). Participants in the intervention arm found the CCC content to be acceptable, with 82% reporting it was easy to use, and 86% reporting they would recommend it to other patients. Women randomized to CCC (vs. control) more often reported scheduling a PCP follow-up visit (64% vs. 42%), communicating with their PCP about provider roles (67% vs. 18%), and higher mean team-based cancer care knowledge scores (3.7 vs. 3.4).
Conclusions:
Deploying CCC in medical oncology practices was feasible, and the intervention content was acceptable. CCC shows promise for improving patient knowledge and patient-provider communication about provider roles in team-based cancer care, and encouraging patients to engage with their PCP early in the survivorship period.
Keywords: team-based cancer care, cancer survivorship, primary care, care coordination
INTRODUCTION
The delivery of high-quality, comprehensive cancer survivorship care remains suboptimal in the United States, and the coordination of this care remains a pervasive challenge.[2, 3, 10, 26] The National Academy of Medicine recommends the implementation of team-based cancer care, defined as primary care providers working with oncology and geriatric care teams to deliver high-quality, coordinated, patient-centered care in the survivorship period. [19]Accumulating evidence from international studies suggests team-based cancer survivorship care can improve the quality of care and lower costs with similar recurrence detection rates and quality of life.[7, 12, 22, 29]
Despite this evidence, team-based cancer survivorship care models have been very difficult to implement in the US, in part due to a lack of effective and scalable interventions that promote these models. Survivorship care plans are intended to promote collaboration and communication between primary care and oncology providers,[6] yet adoption is limited.[8, 9] They have also not been found to improve care coordination,[11] nor have they eliminated patients’ confusion about team-based care and primary care provider (PCP) and oncologists’ roles in delivering it.[15, 16, 33] Prior research suggests that barriers to team-based cancer care exist at both the patient and provider-levels. Barriers include gaps in knowledge about what team-based survivorship care entails, particularly around specific provider roles in this care, suboptimal patient-provider communication about team-based survivorship care, and limited PCP involvement in survivorship care. [30, 31, 34–36]
To target these identified barriers and address the lack of effective interventions, we developed a multi-level intervention for women with early-stage breast cancer and their primary care any medical oncology care teams called ConnectedCancerCare (CCC). CCC includes tailored educational content for patients in a personalized website, reminders to schedule PCP follow-up visits, and a provider summary letter to promote patient-provider communication about team-based survivorship care. We then conducted a pilot randomized controlled trial of CCC vs. a static survivorship care plan (control) and post-trial process evaluation in an academic medical oncology practice to assess the feasibility and acceptability of CCC, and explore its influence on patient-reported knowledge about team-based survivorship care, patient communication with their providers about provider roles, and scheduling a PCP follow-up visit.
METHODS
Intervention:
CCC is a patient and provider intervention that includes a personalized, patient-facing website targeted towards women with breast cancer transitioning into survivorship, and tailored feedback letters sent to the patients’ PCP and medical oncologist. The goal of CCC is to improve the delivery of patient-centered, team-based survivorship care by addressing gaps in patient knowledge and patient-provider communication about team-based cancer care delivery, clarifying oncology and primary care providers roles in delivering it, and patients following up with their PCP. The CCC intervention was developed in collaboration with the University of Michigan Center for Health Communications Research (CHCR) using an iterative, agile cycle[5, 18, 21], with input from cancer care delivery researchers, oncologists, primary care physicians and breast cancer survivors. The development built upon the existing platform of the iCanDecide tool, a treatment decision-making tool previously evaluated in a multi-site trial.[13] Using this existing platform and tailoring algorithms allowed for easier and more efficient programming of the new survivorship content. The content of CCC was directly informed by the Chronic Care Model and NCI Quality of Survivorship Care Framework, which were used to select the levels of the intervention (patient and provider), and identify both process (knowledge and communication) and distal outcomes (PCP visits) that the intervention is targeting. We then used the core-function-form framework to identify goals, select key functions of the intervention, and map corresponding forms (components) at each level (patient and provider).[1, 23]
Patient-level components:
CCC features a personalized, mobile-optimized website, which uses a baseline survey to assess patients’ preferences for provider roles in survivorship care, their ratings of their communication with their current oncologist and PCP, and their diagnostic and clinical information. This information is then used to tailor the educational content within the website. CCC includes the following modules and features: (1) Inform: key facts about breast cancer survivorship care and what to expect from team-based care; (2) Clarify: tailored content to clarify provider roles in delivering team-based care according to patients’ baseline preferences, and outlining how oncology, PCP and specialist roles change over time; (3) Communicate: tailored tips and suggestions to empower patients to communicate with their oncologist and PCP about their roles in survivorship care, and how to get the most out of their clinic visits based on their baseline ratings of communication with their providers; (4) Follow-up care to-do list: list of services needed during survivorship, based on survivorship care guidelines,[24, 32] tailored to their diagnosis and treatment. (5) Additional features to support transition to survivorship: a list of local, regional and national support services. Upon completion of the baseline questionnaire, participants randomized to the intervention arm received weekly reminders via email or text (based on reported contact preferences) about scheduling a follow-up appointment with their PCP. The intervention goals, specific functions and corresponding forms at the patient-level are described in detail in Table 1.
Table 1:
Connected Cancer Care development goals, intervention forms and functions at the patient and provider levels
| Intervention Functions | Intervention Forms PATIENT-LEVEL | Intervention Forms PROVIDER-LEVEL |
|---|---|---|
| Goal: Improve patient knowledge gaps about team-based survivorship care | ||
| Patient education about team-based cancer care Provider awareness of patient knowledge gaps |
-Educational module (Inform) highlighting key facts about breast cancer survivorship care, and what to expect of team-based care -Tailored module (Clarify) clarifying provider roles according to patients’ baseline preferences -Patient testimonials -Tailored survivorship to-do list |
-Provider letters highlighting gaps in patient knowledge |
| Goal: Improve patient-MD communication about team-based care | ||
| Patient education and support Provider awareness of patient preferences for provider roles |
-Tailored communication module (Communicate) and tips to communicate with providers about provider roles, based on baseline ratings of communication with PCP and oncologist-Tips for communicating with MDs | -Provider letters highlighting patient preferences for provider roles |
| Goal: Improve PCP involvement in survivorship care | ||
| Patient education about PCP roles in survivorship care Provider awareness of patient preferences for provider roles |
-Tailored education module clarifying provider roles in team-based care -Tailored survivorship care to-do list, tailored to diagnosis and treatment -Patient scheduling alerts |
-Provider letters highlighting patient preferences for provider roles |
| Goal: Scheduling a PCP follow-up visit | ||
| Patient: schedule PCP follow-up visit (per guidelines) | -Tailored educational modules highlighting role of PCP in team-based care -Patient scheduling alerts -Tailored survivorship to-do list -PCP referral service number for those without PCP |
-Provider letter to oncologist flags if patient does not have a PCP |
| Goal: Supporting transition to survivorship care | ||
| Addressing ongoing patient support and resource needs | -Links to local, regional and support services -Link to NCI text-based lifestyle interventions (exercise, smoking cessation) -Information about side-effects, when to call MD |
-Provider letter highlights top 3: concerns going into survivorship, worry about recurrence, endocrine therapy adherence |
Provider-level components:
CCC includes a summary letter sent to the participating patient’s PCP and oncologist three months post-enrollment that feeds back information collected from the baseline tailoring survey in the CCC website. The content of the summary was informed by stakeholder interviews with oncologists and PCPs about what information would be most helpful to them early in patients’ transition to survivorship. The letter highlights key patient-reported information, collected via the baseline survey: (1) knowledge gaps about survivorship care (e.g. patient reports they need survivorship services that are not guideline-recommended); (2) patient preferences for PCP and oncologist roles in their survivorship care; (3) top three concerns going into survivorship; (4) hormone therapy adherence issues (for those on hormone therapy at time of enrollment); and (5) high levels of worry about recurrence. (Table 1)
Control:
The control group received a fillable static survivorship care plan template via the website in PDF format, which could be printed. The content of this care plan was adapted from the ASCO breast cancer survivorship template and the NCCN breast cancer guide.[24, 25]
Study design and population:
We conducted a two-arm pilot RCT of CCC vs. control in 66 women receiving care after initial breast cancer treatment at an academic breast oncology practice. Women, ages 21–84, with stages 0-II breast cancer who were completing initial breast cancer treatment (surgery, radiation, chemotherapy) and being followed by a medical oncologist, who had access to the internet and spoke or understood English were eligible for the study.
Study recruitment and enrollment (Figure 1):
Figure 1.
The CONSORT flow diagram for the pilot ConnectedCancerCare trial
Eligible patients for the pilot study were identified by reviewing scheduled oncology visits for patients nearing the end of their treatment, and eligibility was then verified by the breast oncology providers (nurse practitioners and/or oncologists). Providers excluded 101 women who were not yet finished with primary treatment or on adjuvant therapies (not including endocrine), or who had new clinical information that changed their treatment plans. An additional 23 women could not be approached due oncology appointment cancellations or changes, 29 had stage III or IV breast cancer, and 1 did not have access to the internet. The remaining 160 eligible women were given an introductory packet by a trained research assistant or the oncology provider which included: (1) a cover letter written at a 6th grade reading level containing information about the study; (2) unique log-in information to access the study website and complete an online informed consent; (3) a printed copy of the informed consent; (4) a $20.00 Amazon gift card. The pilot trial was approved by the University of Michigan Institutional Review Board, and registered at Clinicaltrials.gov (NCT03618017).
The participants who logged into the website first verified personal information and contact preferences (email/text) and were then prompted to complete the online consent form. They were then randomized 1:1 to either the CCC intervention or control arm. (Figure 1) Because both arms were randomized to receive something via the website, they were blinded to their study arm assignment. Block randomization was used, with block sizes of six, and was performed using PROC PLAN in SAS 9.4 (SAS Institute, Cary, NC).
Baseline tailoring survey:
The baseline survey ascertained information about their breast cancer diagnosis and treatment, knowledge about breast cancer survivorship guidelines, whether or not they had a PCP, preferences for provider roles (PCP and oncology) in team-based cancer care, and ratings of prior communication with their PCP and medical oncologist. As described above, this information was then used to tailor the content of the modules in the CCC website. We also asked participants to provide the contact information for their medical oncologist and primary care provider as part of the baseline questionnaire, which was used to send the provider summary letter to both physicians’ offices via fax. Using follow-up protocols successfully deployed in our prior cancer care delivery trials, participants received one automated email reminder 2 days after logging into the website if the baseline questionnaire was not completed, and up to 2 reminder phone calls from the study coordinator.
Follow-up survey:
An online follow-up survey (accessed via the general CCC website) was emailed to participants three months after enrollment. This survey included multiple measures of acceptability and usability in the intervention group only (primary endpoints) and secondary patient-reported endpoints in both groups. As done successfully in our prior studies, we employed a modified version of the Dillman method to maximize response rates.[4]
Primary endpoints:
Our primary endpoint was feasibility, defined as: (1) the proportion of women who completed the baseline survey and were enrolled, (2) the proportion who completed the follow-up survey, and (3) the successful recruitment of ≥60 women in 9 months.
Secondary (exploratory) endpoints:
All secondary endpoints were patient-reported and collected via the online follow-up survey three months after enrollment. Acceptability was defined by asking participants in the intervention arm to rate their experiences in 6 domains with the tool on 5-point Likert-type scales, as follows: (1) CCC was easy to use, (2) CCC was helpful during my transition to survivorship, (3) CCC helped me think about when to see my PCP and when to see my oncologist, (4) I would recommend CCC to other patients, (5) The time it took to go through the website (6) The amount of information was just right. Based on our prior work, we employed a cut off of 50% of more reporting a score above 3 as acceptable within each domain. The responses to the 6 items were then averaged to create an acceptability summary score, with a score of 3 or more indicating the tool was acceptable to most participating patients. PCP follow-up visit scheduling (yes/no) was ascertained by asking participants whether or not they had scheduled a visit with their PCP since viewing the website. Knowledge about team-based survivorship care was measured utilizing an 8-item scale (with individual response categories ranging from strongly agree to strongly disagree) adapted from the Perceived Primary Care Delivery of Survivorship Care Scale.[27] It includes items specific to patients’ knowledge of PCPs roles in team-based care delivery, (e.g. second cancer screening, symptom management). The responses to the 8 items were then averaged to create a knowledge summary score. Communication with provider about provider roles was measured using an item adapted to the patient perspective from a prior study of providers’ views about shared cancer care roles.[17, 28] Patients were asked if they communicated in the past 3 months with their PCP about who will manage specific aspects of their survivorship care. Patient-reported preferences for provider roles in team-based cancer care, an 8-item scale used in our prior studies which ascertains patient preferences (PCP or oncologist) for delivering key survivorship care services (surveillance, general preventive care, screening for second cancers). Satisfaction with coordination of care was measured using a single item as used in prior studies, tailored to the timing of transition. Participants were asked how satisfied they were with the coordination of their care between the oncologist and PCP, with response categories on a 5-point Likert-type scale from “not at all satisfied” to “extremely satisfied.”
Statistical analyses:
The distribution of baseline sociodemographic and clinical characteristics by study arm were examined. The proportion of patients who enrolled and completed the baseline questionnaire, and the proportion of participants who completed the follow-up questionnaire were estimated (feasibility). (Figure 1) The distribution and mean scores within each of the 6 measures of acceptability was determined, and the distribution of the acceptability summary score was then assessed. Mean knowledge scores, the proportion of women reporting they communicated with their PCP about provider roles in team-based care, and the proportion of women who reported scheduling a follow-up PCP visit were then compared by study arm. As this study was designed as a pilot to assess the feasibility and acceptability of the intervention, and explore whether patients who engage with the CCC tool score higher on key knowledge, communication, utilization measures compared to those who received the control, no formal statistical tests were performed.
Process evaluation:
Participants in the intervention arm and their PCPs and oncology providers (NPs or oncologists) were invited to participate in semi-structured interviews to collect feedback regarding their experience with CCC, and identify key determinants to implementing CCC in practice. Email invitations were sent to the participating intervention patients, PCPs and oncology providers, and 5 PCPs, 6 oncology providers (both MDs and NPs) and 8 intervention patients were interviewed via phone. Semi-structured interview guides were informed by the Guided by the Tailored Implementation for Chronic Diseases Framework (TICD).[37, 38] An initial list of codes was generated from our a priori thematic categories derived from the TICD domains. We then developed a coding structure inductively using the constant-comparative method, and employed an iterative, consensus-based process with two coders. Dedoose was used organize and manage the interview data.
RESULTS
Figure 1 displays the CONSORT diagram outlining study enrollment. Of the 160 eligible women who were invited to participate, 71 (44%) logged into the website, and the majority of those who logged in (97%) then completed the informed consent (N=69). Of the 160 women who were given a packet and invited to participate, 66 women completed the baseline survey and were enrolled (41% participation rate), and were randomized to either CCC (N=28) or control (N=28). Of those enrolled, 82% completed the three-month post-enrollment follow-up survey.
Table 2 displays the baseline characteristics by assigned study arm. Women randomized to the intervention were older and more likely to be on endocrine therapy at the time of enrollment, compared to those randomized to the control. All other baseline characteristics were well balanced across arms. Overall, 6% of participants reported not having an established PCP at time of enrollment.
Table 2:
Baseline participant characteristics by randomization status (N=66)
| Control (n=33) | Intervention (n=33) | |
|---|---|---|
|
| ||
| Demographic | N (%) | N (%) |
|
| ||
| Age (mean, SD) | 54.1 (11.4) | 57.8 (10.8) |
|
| ||
| Race/ethnicity | ||
| White | 27 (81.8) | 29 (87.9) |
| Black | 1 (3.0) | 1 (3.0) |
| Hispanic | 1 (3.0) | 1 (3.0) |
| Asian | 3 (9.1) | 1 (3.0) |
| Other | 1 (3.0) | 1 (3.0) |
|
| ||
| Education | ||
| High school/some college | 10 (30.3) | 13 (39.4) |
| College graduate or more | 23 (69.7) | 20 (60.6) |
|
| ||
| Insurance | ||
| Medicare | 10 (30.3) | 8 (24.4) |
| Medicaid/Other govt. | 3 (9.1) | 1 (3.0) |
| Private | 20 (60.6) | 24 (72.7) |
|
| ||
| Employment | ||
| Employed | 17 (51.5) | 17 (51.5) |
| Retired | 10 (30.3) | 8 (24.2) |
| Other not employed | 6 (18.2) | 8 (24.2) |
|
| ||
| Clinical | ||
|
| ||
| Breast Cancer Stage at Diagnosis | ||
| 0 | 3 (9.7) | 2 (8.3) |
| I | 14 (45.2) | 15 (62.5) |
| II | 14 (45.2) | 7 (29.2) |
|
| ||
| Primary Surgical Treatment | ||
| Lumpectomy | 20 (60.6) | 17 (51.5) |
| Unilateral mastectomy | 5 (15.2) | 10 (30.3) |
| Bilateral mastectomy | 8 (24.3) | 6 (18.2) |
|
| ||
| Received radiation | ||
| No | 9 (27.3) | 11 (33.3) |
| Yes | 24 (72.7) | 22 (66.7) |
|
| ||
| Received chemotherapy | ||
| No | 17 (51.5) | 19 (57.6) |
| Yes | 16 (48.5) | 14 (42.4) |
|
| ||
| On endocrine therapy | ||
| No | 7 (21.2) | 2 (6.1) |
| Yes | 26 (78.8) | 31 (93.9) |
|
| ||
| Number of comorbidities | ||
| 0 | 15 (45.5) | 15 (45.5) |
| 1 | 14 (42.4) | 12 (36.4) |
| 2+ | 4 (12.1) | 6 (18.2) |
|
| ||
| Had a PCP at enrollment | ||
| No | 2 (6.1) | 2 (6.1) |
| Yes | 31 (93.9) | 31 (93.9) |
Table 3 displays acceptability measures among women randomized to the intervention arm. CCC was found to be highly acceptable (mean summary score 4.4). Most women found CCC easy to use (82%), the content to be helpful during their transition to survivorship (72%) and the amount of information (68%) and time to go through the website (64%) to be just right. The majority (86%) of participants reported they would recommend CCC to other patients.
Table 3:
Patient-reported outcomes and acceptability 3 months post-randomization (N=54)
| Control N=26 | Intervention N=28 | |
|---|---|---|
|
| ||
| Patient-reported outcomes | ||
|
| ||
|
Knowledge about team-based survivorship care mean, SD |
3.4 (0.9) | 3.7 (0.6) |
|
| ||
| Scheduled PCP follow-up visit | ||
| No | 15 (57.7) | 10 (35.7) |
| Yes | 11 (42.3) | 18 (64.3) |
|
| ||
| Communicated with PCP about provider roles (Among those who saw PCP N=29) | ||
| No | 9 (81.8) | 6 (33.3) |
| Yes | 2 (18.2) | 12 (66.7) |
|
| ||
| Increased my understanding of team-based cancer care | ||
| No | 11 (42.3) | 8 (28.6) |
| Yes | 15 (57.5) | 20 (71.4) |
|
| ||
| Confident in PCPs ability to handle survivorship care | ||
| Less confident | 13 (50.0) | 11 (39.3) |
| More confident | 13 (50.0) | 17 (60.7) |
|
| ||
|
Satisfaction with coordination of care mean (SD) |
3.1 (1.2) | 3.7 (1.0) |
|
| ||
| Patient preferences for PCP (vs. oncologist) | ||
| Surveillance (mammogram) | 0 (0.0) | 3 (10.7) |
| Screening for second primary cancers | 5 (19.2) | 14 (50.0) |
| General preventive care | 23 (88.5) | 25 (89.3) |
| Comorbidity management | 24 (92.3) | 24 (92.3) |
| Physical effects | 2 (7.7) | 3 (10.7) |
| Psychological effects | 15 (57.7) | 20 (71.4) |
| Reassurance about recurrence risk | 1 (3.9) | 1 (3.6) |
| Endocrine therapy management | 13 (81.3) | 15 (75.0) |
|
| ||
| Acceptability (intervention arm only) | ||
|
| ||
| CCC was easy to use | -- | 23 (82.1) |
|
| ||
| Helpful during transition to survivorship | -- | 21 (72.4) |
|
| ||
| Amount of information in CCC was just right | -- | 19 (67.9) |
|
| ||
| Amount of time to go through CCC website was just right | -- | 18 (64.3) |
|
| ||
| CCC helped me think about when to see PCP & oncologist | -- | 20 (71.4) |
|
| ||
| I would recommend CCC to other patients | -- | 24 (85.7) |
|
| ||
| Acceptability summary score (mean, SD) | -- | 4.4 (2.0) |
Table 3 also displays secondary patient-reported endpoints among participants randomized to CCC and control. Participants who engaged with CCC website reported higher mean knowledge scores about team-based survivorship care (3.7 vs. 3.4). Among those who reported seeing their PCP (n=29), a greater proportion of women in the intervention arm reported communicating with their PCP about provider roles than those in the control arm (67% vs. 18%). A greater proportion of woman in the intervention arm also reported that CCC increased their understanding of team-based cancer care (71 vs 58%), and helped them feel more confident in the PCP’s ability to handle their survivorship care (60 vs. 50%).
Table 4 displays key themes and corresponding excerpts that emerged from the debriefing interviews with intervention patients and their PCPs and oncology providers. Key determinants of implementation included recommendations (clarity of provider roles), attitudes about the recommendations, team and referral processes, patient needs, beliefs and knowledge, and information system (EMR integration). Multiple providers noted challenges to accessing the provider letters, and cited EMR integration issues as a potential barrier to scaling CCC.
Table 4:
Selected TICD determinants and corresponding excerpts from debriefing interviews with participating oncology (N=6) and primary care providers (N= 5), and breast cancer patients (N=8)
| TICD determinants | Construct | Quote [stakeholder] |
|---|---|---|
| Guideline Factors | ||
| Recommendations | Clarity (of provider roles) | It’s something I sort of negotiate with patients. Most patients want to come back to see me and some patients would rather see their PCP and depending on what they want, I tell them the same survivorship guidelines. [oncologist] We often feel confused as to who is in charge and I also feel like there is sometimes not clear communication of what the primary care person should do or when they should refer back to oncology as well as if there is any surveillance stuff that we are supposed to be in charge of. [PCP] |
| Recommended clinical intervention | Accessibility (of provider letters) | I would personally want [the letter] within a day or so before their visit. Because in general I’m not looking forward, especially for follow up patients, I’m not looking forward a week or more to see what, if any active issues the patient might have unless something has come to my attention. So I don’t need it weeks ahead of time. [Oncology NP] I would also say that I personally wouldn’t want any of this coming to my email. I would want it to all go through [the EMR] because I think that’s the best way to keep it within their electronic records so that everybody has access to it. [Oncology NP] |
| Individual Healthcare Professional Factors | ||
| Cognitions: Attitudes | Agreement with recommendations | First of all, I don’t think a breast cancer patient should be transitioning this soon after treatment to the care of a primary care provider. This does not make me at all comfortable without a lot more information and detail about the patient’s prognosis. It seems to me that they should remain under the care of their oncologist for the first few years afterward. [PCP] I personally feel very strongly that it’s not the patient’s preference, who is going to manage what portion of their healthcare, right? …Because I believe there are patients that want us as their oncologist to manage everything, and that’s really not what our focus and what our role should be. [oncology] I feel like to be safe I would feel more comfortable with the cancer center perhaps identifying problems early. I don’t know if the primary care would have the expertise. [patient] |
| Professional Interactions | ||
| Team Processes | Team processes | I think the oncologists are so specialized in their lingo and jargon that they might forget that we – we don’t listen to this a lot, right?... I think sometimes they have to maybe remember to spell it out even in the way that they would to their patients, do the same for the PCP. Word their notes for our understanding of the patient status and recommendations for care. [PCP] [It’s] not always spelled out in the oncology note very well what the prognosis or progression of the disease might be in the particular patient. [PCP] Well, I think, first, I don’t know that on our end that we are that good at saying to people, “Okay, now, this is a different phase and we’ll share the treatment or the monitoring with your primary care.” So I don’t think that there’s a clear demarcation there. [oncologist] |
| Referral processes | Well, there was a lot of reactions I had to the chemo. I called the Cancer Center and I was told I should contact my primary care. I called my primary care and they said, “That is a common side effect of the chemo you’re on, go back to your oncologist.” So I just suffered with no care. [patient] | |
| Patient Factors | ||
| Patient needs | Perceived needs | It needs to be setup for these people who come from Newaygo, Michigan and they drove in two hours just to see the oncologist. Because obviously you can make their quality of life much better if you would educate and make it safe for those people to go back to their PCPs a lot earlier. [PCP] |
| Patient beliefs and knowledge | motivations | It’s hard. It’s a hard journey because everything is fear of recurrence. [oncologist] To be honest in some way it’s a great idea, in another way sometimes you just want to get back to your life and you don’t want to be reminded of the cancer so sometimes for me anything related cancer I give like a small sigh when I see an email.” [patient] I think the main thing is my emotional state is probably the most important thing because a lot of times doctors are concentrating on other things. Like where am I at in my head right now. [patient] |
| Incentives and Resources | ||
| Information system | EMR integration | We’re sort of inundated with information and to some degree, the more time I spend reviewing something, the less time I spend actually talking to the patient. I already spend half my visit, I feel like, staring at a computer screen instead of the patient because the exam rooms aren’t set up right. So, when I have another piece of information to review before I go into the patient, that’s one or two minutes that I’m sitting there doing that. [oncologist] |
| Acceptability of intervention | ||
| Acceptability of CCC content | It helped me figure out when to talk to PCP and oncologist [patient] I like when it would tell you the stuff to follow-up on, like things that you need to do, you know. Down the road those things like the directions - like whether it be vaccines and follow-up and things like that. [patient] I guess just knowing that it’s out there, that there are people that still are interested in me and care about my recovery. Knowing that it’s there is a very pleasant thought. [patient] Well, the most helpful thing for was, you know, like I said I enjoyed looking up the information. It had basically like stories or whatever that things that goes on you could look up different type of problem areas or whatever. It gave you options that you can talk to people. [patient] I think the concern part was the most helpful. [PCP] Her preferences were really unique and I liked seeing that. [PCP] The knowledge about follow-up care was most helpful. [oncologist] I think we identified gaps in knowledge. I think that’s, for me, the most useful thing. It might just be things that are on our patient’s mind that we haven’t discussed in clinic because we maybe didn’t necessarily see them as relevant but are things that our patients are potentially having anxiety or worry about. [oncologist] I think it improved it in the sense that we were able to distill just some of the concerns that patients had or at least address some of the things patients had about additional testing that wasn’t required. [oncologist] |
|
DISCUSSION
ConnectedCancerCare, a multi-level intervention focused on patients and providers to improve team-based cancer care was feasible to deploy in an academic medical oncology practice, and was highly acceptable among women with early-stage breast cancer. In our pilot RCT CCC showed promise for improving knowledge and communication about provider roles in team-based survivorship care, and patients following up with their PCP early in the survivorship period. However, interviews with primary care and oncology providers underscored challenges of implementing survivorship care interventions like CCC, including EMR integration challenges, and supporting sustained engagement among providers and patients over time.
Our pilot study results support that recruiting women with breast cancer to use CCC in an academic medical oncology practices is feasible. We over recruited our initial target of 60 women, and had a 41% participation rate and 82% follow-up survey response rate. Our participation rate, while lower than initially anticipated based on our prior cancer care delivery trial in breast cancer patients during treatment[13], is similar to other survivorship intervention studies[14, 20]. Early survivorship can be an overwhelming and confusing time for many patients with cancer, who often feel they are “lost in transition”, and are living with a number of side-effects of their initial treatments.[3] Therefore, intervening early in the survivorship period is often challenging, and as a result, not many interventions are deployed during this transition in care. [20] Such interventions should meet patients “where they are,” acknowledge the emotions patients face when transitioning to survivorship, and offer broader support of this transition. We designed CCC to target multiple aspects to team-based survivorship care and used a theory-based approach to identify a priori goals, and map functions and forms of the intervention to maximize its potential effect on patient-provider communication, patient knowledge and PCP visits. But, CCC also offers information about necessary surveillance and follow-up care they need, and identifies resources and support services for common psychosocial effects among cancer survivors.
Participants in the intervention group consistently reported high acceptability and usability of CCC. We specifically developed CCC with the end users in mind, employing user-centric design and rigorously beta testing the tool prior to the RCT among breast cancer patients. Interviews with patient participants at the end of trial also highlighted key aspects of acceptability, including finding the content of the website helpful in understanding when to talk to a PCP or oncologist about an issue, what follow-up services are needed in survivorship, local/regional/national resources, and patient stories and testimonials. Interviewed patient participants also reported wanting new “fresh” content as they move through initial survivorship, and fewer alerts about when to schedule their PCP follow-up visit.
Participating PCPs and medical oncology providers also noted multiple determinants of implementation, including the lack of clarity of current guidelines about specific provider roles, the timing and accessibility of the provider letter, EMR interoperability, and provider attitudes and disagreement with team-based care recommendations. This information will be used to enhance the existing version of CCC to include more provider-level intervention components specifically focused on promoting communication about provider roles, aligning the timing of the provider letters to clinic visits, and integrating the provider-level components into the EMR.
While we conducted a pilot study which included both a rigorous pilot RCT and process evaluation with a diverse set of stakeholders, there are limitations that warrant comment. First, this pilot study was conducted at a single academic breast oncology clinic, thus the generalizability of these findings to other practice locations and patient populations is limited. However, our planned next steps include conducting a cluster RCT to evaluate CCC and study its implementation in community-based practices. Second, this study only included women with early-stage breast cancer. However, CCC was designed with scalability to other cancers in mind. If found effective, the modular team-based cancer care content is highly applicable and easily transferable to other favorable-prognosis adult cancers (e.g. prostate and colon). Third, it is possible that women who are more activated and engaged in their care were more likely to participate in this pilot study. Our future plans include evaluating CCC in more diverse care settings, and collecting information about non-participants. Finally, the issues with accessibility and the timing of the provider letters most likely limited their influence on the outcomes. However, the content of the letters was found to be acceptable among participating providers during the post-trial interviews, and the next version of CCC will integrate these letters into the EMR and time them to upcoming clinic visits.
In conclusion, our findings suggest that deploying CCC in a medical oncology practice is feasible, the intervention content is acceptable among women with breast cancer, and shows promise for improving patient knowledge and patient-provider communication about provider roles in team-based cancer care, and patients following up with their PCP early in the survivorship period. Future evaluation plans will include assessing the effectiveness and implementation of CCC across diverse practice settings.
Funding:
This study was funded by the National Cancer Institute K07 CA201052. Research reported in this publication was also supported by the NCI under award number P30 CA46592, and through the use of the following Cancer Center Shared Resources: Health Communications, Biostatistics. Dr. Mullins received research support from the National Cancer Institute institutional training grant T32-CA-236621.
Footnotes
Conflicts of interest/Competing interests: Not applicable
Ethics approval: University of Michigan IRBMED March 2019
Consent to participate: Not applicable
Consent for publication: Not applicable
Availability of data and material: Not applicable
Code availability: Not applicable
Publisher's Disclaimer: This Author Accepted Manuscript is a PDF file of an unedited peer-reviewed manuscript that has been accepted for publication but has not been copyedited or corrected. The official version of record that is published in the journal is kept up to date and so may therefore differ from this version.
References
- 1.Bodenheimer T, Wagner EH, Grumbach K (2002) Improving primary care for patients with chronic illness: the chronic care model, part 2. JAMA 288:1909–1914. [DOI] [PubMed] [Google Scholar]
- 2.Bower JE, Ganz PA, Desmond KA, Bernaards C, Rowland JH, Meyerowitz BE, Belin TR (2006) Fatigue in long-term breast carcinoma survivors: a longitudinal investigation. Cancer 106:751–758. doi: 10.1002/cncr.21671 [DOI] [PubMed] [Google Scholar]
- 3.National Academy of Medicine (2006) From Cancer Patient to Cancer Survivor: Lost in Transition. In: Press TNA (ed), Washington DC [Google Scholar]
- 4.Dillman DA (2007) Mail and internet surveys: the tailored design method. Wiley [Google Scholar]
- 5.Dybå T, Dingsøyr T (2008) Empirical studies of agile software development: A systematic review. Information and software technology 50:833–859. [Google Scholar]
- 6.Earle CC (2006) Failing to plan is planning to fail: improving the quality of care with survivorship care plans. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 24:5112–5116. doi: 10.1200/jco.2006.06.5284 [DOI] [PubMed] [Google Scholar]
- 7.Emery JD, Jefford M, King M, Hayne D, Martin A, Doorey J, Hyatt A, Habgood E, Lim T, Hawks C, Pirotta M, Trevena L, Schofield P (2017) ProCare Trial: a phase II randomized controlled trial of shared care for follow-up of men with prostate cancer. BJU international 119:381–389. doi: 10.1111/bju.13593 [DOI] [PubMed] [Google Scholar]
- 8.Faul LA, Luta G, Sheppard V, Isaacs C, Cohen HJ, Muss HB, Yung R, Clapp JD, Winer E, Hudis C, Tallarico M, Wang J, Barry WT, Mandelblatt JS (2014) Associations among survivorship care plans, experiences of survivorship care, and functioning in older breast cancer survivors: CALGB/Alliance 369901. Journal of cancer survivorship : research and practice. doi: 10.1007/s11764-014-0371-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Forsythe LP, Parry C, Alfano CM, Kent EE, Leach CR, Haggstrom DA, Ganz PA, Aziz N, Rowland JH (2013) Use of survivorship care plans in the United States: associations with survivorship care. Journal of the National Cancer Institute 105:1579–1587. doi: 10.1093/jnci/djt258 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Fu MR (2014) Breast cancer-related lymphedema: Symptoms, diagnosis, risk reduction, and management. World journal of clinical oncology 5:241–247. doi: 10.5306/wjco.v5.i3.241 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Grunfeld E, Julian JA, Pond G, Maunsell E, Coyle D, Folkes A, Joy AA, Provencher L, Rayson D, Rheaume DE, Porter GA, Paszat LF, Pritchard KI, Robidoux A, Smith S, Sussman J, Dent S, Sisler J, Wiernikowski J, Levine MN (2011) Evaluating survivorship care plans: results of a randomized, clinical trial of patients with breast cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 29:4755–4762. doi: 10.1200/jco.2011.36.8373 [DOI] [PubMed] [Google Scholar]
- 12.Grunfeld E, Levine MN, Julian JA, Coyle D, Szechtman B, Mirsky D, Verma S, Dent S, Sawka C, Pritchard KI, Ginsburg D, Wood M, Whelan T (2006) Randomized trial of long-term follow-up for early-stage breast cancer: a comparison of family physician versus specialist care. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 24:848–855. doi: 10.1200/JCO.2005.03.2235 [DOI] [PubMed] [Google Scholar]
- 13.Hawley ST, Li Y, An LC, Resnicow K, Janz NK, Sabel MS, Ward KC, Fagerlin A, Morrow M, Jagsi R, Hofer TP, Katz SJ (2018) Improving Breast Cancer Surgical Treatment Decision Making: The iCanDecide Randomized Clinical Trial. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 36:659–666. doi: 10.1200/JCO.2017.74.8442 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Hershman DL, Greenlee H, Awad D, Kalinsky K, Maurer M, Kranwinkel G, Brafman L, Jayasena R, Tsai W-Y, Neugut AI (2013) Randomized controlled trial of a clinic-based survivorship intervention following adjuvant therapy in breast cancer survivors. Breast cancer research and treatment 138:795–806. [DOI] [PubMed] [Google Scholar]
- 15.Jacobsen PB, Derosa AP, Henderson TO, Mayer D, Moskowitz CS, Paskett ED, Rowland JH (2018) Impact of cancer survivorship care plans (SCPs) on health outcomes and health care delivery: A systematic review. In:American Society of Clinical Oncology [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Jacobsen PB, DeRosa AP, Henderson TO, Mayer DK, Moskowitz CS, Paskett ED, Rowland JH J J o C O (2018) Systematic review of the impact of cancer survivorship care plans on health outcomes and health care delivery. 36:2088–2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Klabunde CN, Han PK, Earle CC, Smith T, Ayanian JZ, Lee R, Ambs A, Rowland JH, Potosky AL (2013) Physician roles in the cancer-related follow-up care of cancer survivors. Family medicine 45:463–474. [PMC free article] [PubMed] [Google Scholar]
- 18.Larman C (2004) Agile and iterative development: a manager's guide. Addison-Wesley Professional [Google Scholar]
- 19.National Academy of Medicine (2013) Delivering High Quality Cancer Care: Charting a New Course for a System in Crisis. In: Levit LABE, Nass SJ, and Ganz PA (ed)National Academy of Medicine; [PubMed] [Google Scholar]
- 20.Meneses KD, McNees P, Loerzel VW, Su X, Zhang Y, Hassey LA (2007) Transition from treatment to survivorship: effects of a psychoeducational intervention on quality of life in breast cancer survivors. In: Oncology nursing forum. Oncology Nursing Society, p 1007. [DOI] [PubMed] [Google Scholar]
- 21.Meso P, Jain R (2006) Agile software development: adaptive systems principles and best practices. Information Systems Management 23:19–30. [Google Scholar]
- 22.Mittman N (2018) Evaluating the impact of survivorship models on health system resources and costs. J Clin Oncol 36:abstr 1. [Google Scholar]
- 23.Nekhlyudov L, Mollica MA, Jacobsen PB, Mayer DK, Shulman LN, Geiger AM (2019) Developing a Quality of Cancer Survivorship Care Framework: Implications for Clinical Care, Research and Policy. Journal of the National Cancer Institute. doi: 10.1093/jnci/djz089 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.National Comprehensive Cancer Network (2018) NCCN Clinical Practice Guidelines in Oncology : Survivorship. In:National Comprehensive Cancer Network, Inc. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.American Society of Clinical Oncology (2018) Survivorship Compendium. In:American Society of Clinical Oncology [Google Scholar]
- 26.Pachman DR, Barton DL, Swetz KM, Loprinzi CL (2012) Troublesome symptoms in cancer survivors: fatigue, insomnia, neuropathy, and pain. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 30:3687–3696. doi: 10.1200/JCO.2012.41.7238 [DOI] [PubMed] [Google Scholar]
- 27.Palmer SC, Stricker CT, Panzer SL, Arvey SA, Baker KS, Casillas J, Ganz PA, McCabe MS, Nekhlyudov L, Overholser L, Partridge AH, Risendal B, Rosenstein DL, Syrjala KL, Jacobs LA (2015) Outcomes and Satisfaction After Delivery of a Breast Cancer Survivorship Care Plan: Results of a Multicenter Trial. 11:e222–e229. doi: 10.1200/jop.2014.001404 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Potosky AL, Han PK, Rowland J, Klabunde CN, Smith T, Aziz N, Earle C, Ayanian JZ, Ganz PA, Stefanek M (2011) Differences between primary care physicians' and oncologists' knowledge, attitudes and practices regarding the care of cancer survivors. Journal of general internal medicine 26:1403–1410. doi: 10.1007/s11606-011-1808-4 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.NHS Improving Quality (2019) Stratified Cancer Pathways: redesigning services for those living with or beyond cancer. In: [Google Scholar]
- 30.Radhakrishnan A, Chandler McLeod M, Hamilton AS, Ward KC, Katz SJ, Hawley ST, Wallner LP (2019) Preferences for Physician Roles in Follow-up Care During Survivorship: Do Patients, Primary Care Providers, and Oncologists Agree? Journal of general internal medicine 34:184–186. doi: 10.1007/s11606-018-4690-5 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31.Radhakrishnan A, Li Y, Furgal AKC, Hamilton AS, Ward KC, Jagsi R, Katz SJ, Hawley ST, Wallner LP (2019) Provider Involvement in Care During Initial Cancer Treatment and Patient Preferences for Provider Roles After Initial Treatment. Journal of oncology practice / American Society of Clinical Oncology 15:e328–e337. doi: 10.1200/JOP.18.00497 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT, Cowens-Alvarado RL, Cannady RS, Pratt-Chapman ML, Edge SB, Jacobs LA, Hurria A, Marks LB, LaMonte SJ, Warner E, Lyman GH, Ganz PA (2016) American Cancer Society/American Society of Clinical Oncology Breast Cancer Survivorship Care Guideline. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 34:611–635. doi: 10.1200/jco.2015.64.3809 [DOI] [PubMed] [Google Scholar]
- 33.Sprague BL, Dittus KL, Pace CM, Dulko D, Pollack LA, Hawkins NA, Geller BM (2013) Patient satisfaction with breast and colorectal cancer survivorship care plans. Clinical journal of oncology nursing 17:266–272. doi: 10.1188/13.cjon.17-03ap [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Wallner LP, Abrahamse P, Uppal JK, Friese CR, Hamilton AS, Ward KC, Katz SJ, Hawley ST (2016) Involvement of Primary Care Physicians in the Decision Making and Care of Patients With Breast Cancer. Journal of clinical oncology : official journal of the American Society of Clinical Oncology 34:3969–3975. doi: 10.1200/JCO.2016.67.8896 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Wallner LP, Li Y, Furgal AKC, Friese CR, Hamilton AS, Ward KC, Jagsi R, Katz SJ, Hawley ST (2017) Patient Preferences for Primary Care Provider Roles in Breast Cancer Survivorship Care. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 35:2942–2948. doi: 10.1200/JCO.2017.73.1307 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Wallner LP, Li Y, McLeod MC, Gargaro J, Kurian AW, Jagsi R, Radhakrishnan A, Hamilton AS, Ward KC, Hawley ST, Katz SJ (2019) Primary care provider-reported involvement in breast cancer treatment decisions. Cancer 125:1815–1822. doi: 10.1002/cncr.31998 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Wensing M (2017) The Tailored Implementation in Chronic Diseases (TICD) project: introduction and main findings. Implementation science : IS 12:5. doi: 10.1186/s13012-016-0536-x [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Wensing M, Huntink E, van Lieshout J, Godycki-Cwirko M, Kowalczyk A, Jager C, Steinhauser J, Aakhus E, Flottorp S, Eccles M, Baker R (2014) Tailored implementation of evidence-based practice for patients with chronic diseases. PloS one 9:e101981. doi: 10.1371/journal.pone.0101981 [DOI] [PMC free article] [PubMed] [Google Scholar]