Background
With >66,000 diagnoses a year and >51,000 deaths, the incidence and burden of pancreatic cancer continues to increase in the United States.1 The vast majority of these patients are older adults (median age at diagnosis, 71 years) and have widely varying levels of fitness.2,3 Treatment involves multimodal strategies (eg, chemotherapy, surgery, radiation) that differ substantially in intensity. The most aggressive treatment approach, FOLFIRINOX chemotherapy followed by a Whipple procedure, is associated with substantial toxicity, and is only recommended for “fit” patients regardless of age.3–5 In practice, however, conducted fitness assessments are largely subjective, often incomplete, and frequently presented from the perspective of the clinician and without patient input, which may not adequately capture the patient’s functional status.6,7
The incorporation of electronic patient-reported outcomes (ePROs) into decision-making settings for pancreatic cancer represents an opportunity to accurately report patients’ overall fitness status and preferences regarding treatment.8 For example, the geriatric assessment (GA) assesses a broad array of age-related health domains and provides detailed information about individual domain impairments as well as an overall frailty profile categorizing patients as frail, prefrail, and robust.9–14 Randomized clinical trials utilizing the GA in older adults with cancer have demonstrated improved communication, reduced chemotherapy toxicities, and improved health-related quality of life (HRQoL) compared with standard of care.15–19 In particular, older patients with pancreatic cancer have high rates of GA impairments, with >40% demonstrating frailty at the time of diagnosis.20 Despite evidence-based guidelines advocating for utilization of the GA, only 20% of oncologists report using the tool consistently.12,21–24 Furthermore, despite many patients with pancreatic cancer preferring approaches that maximize quality over quantity of life, only 37% of clinicians report taking the time to discuss those preferences prior to treatment initiation.25
At The University of Alabama (UAB), we have demonstrated that the GA and patient treatment preferences can be captured directly from patients using a combination of ePROs.26–28 An electronic survey called the Web-Enabled Cancer and Aging Resilience Evaluation (WeCARE) tool includes assessments of patient functional status,29,30 physical function,31 nutrition via the Patient-Generated Subjective Global Assessment (PG-SGA),30,32–35 HRQoL,36 social support,37 social activities, psychological status via the Patient-Reported Outcomes Measurement Information System (PROMIS) anxiety and depression short forms,34,38,39 cognitive function via the PROMIS cognitive function short-form,33 comorbidities,29,40,41 and polypharmacy.27 In addition, a frailty index was developed specifically from the WeCARE survey, in which frailty was associated with increased mortality (hazard ratio, 1.75; 95% CI, 1.13–2.70; P=.01), severe chemotherapy toxicities (relative risk, 2.23; 95% CI, 1.27–3.92; P<.01), and functional decline (odds ratio, 2.37; 95% CI, 1.05–5.38; P=.03) compared with nonfrail patients after controlling for age, sex, race/ethnicity, cancer stage, cancer type, and performance status in patients with gastrointestinal cancer.42,43
This tool is now integrated into the standard of care for all patients at UAB, and currently >1,700 patients with cancer across all UAB oncology clinics and 250 patients with pancreatic cancer have had this tool administered. Despite the feasibility of data collection, implementation barriers have limited the practicality of use in routine practice. Both system- and clinician-level barriers, including lack of time, support staff, and training/knowledge about ePROs, made implementation of these results difficult to integrate into the decision-making process.21,25,44 Thus, we hypothesized that presenting ePROs during multidisciplinary tumor boards (MDTBs) would provide a feasible venue for consistent and systematic ePRO review. MDTBs are interdisciplinary conferences in which clinicians from medical oncology, surgery, radiation oncology, radiology, and pathology collaboratively discuss patients and make treatment recommendations and/or plans.45 With the current study, we sought to evaluate the implementation outcomes of incorporating ePROs into MDTBs using Proctor’s key outcomes of penetration, acceptability, appropriateness, feasibility, adoption, cost, and sustainability.46
Patients and Methods
Design
This pilot study aimed to assess potential benefits of integrating ePROs into MDTB discussions for patients with pancreatic cancer. All study procedures and data analysis plans were preapproved by the Institutional Review Board at UAB (IRB-300007868).
Setting
All study procedures were conducted at UAB, a large R1 research institution and hospital system that serves >1 million patients annually. At UAB, the collection of ePROs and their integration into the electronic health record (EHR) through the Carevive platform is standard of practice for patients entering through medical oncology.47 The Carevive platform then generates appropriate summary statistics and figures within a dashboard that is available for clinicians in the EHR for treatment decisions. Furthermore, all patients at UAB who are diagnosed or expected to be diagnosed with pancreatic cancer are presented at weekly MDTB meetings. Meetings are conducted via Zoom video conference software and structured such that the patient’s representative (typically a medical oncologist or surgeon) first introduces the patient, then the radiologist and/or pathologist shares appropriate scans and reports, and finally, the group discusses appropriate treatment options and makes recommendations.
Population
We included adults aged ≥60 years who were diagnosed with, or being evaluated for, pancreatic adenocarcinoma, and were intending to receive treatment at UAB during the study period of September 2022 and June 2023. We also abstracted data from control patients who were presented at a pancreatic MDTB and received treatment at UAB between November 2021 and February 2022. We chose 60 years of age as a criterion for enrollment given prior research showing a similar prevalence of frailty and GA impairments in adults aged 60–64, 65–74, and ≥75 years with gastrointestinal malignancies.48 Patients scheduled for MDTB presentation were approached and consented by a research coordinator (E. Ortiz-Olguin). Exclusion criteria included those unable to provide informed consent or read and/or speak English, those with a life expectancy of <3 months, those without a confirmed or suspected diagnosis of pancreatic adenocarcinoma, and/or those who were seen for a second opinion only. There were no exclusion criteria for the clinicians participating in the pancreatic MDTB at UAB, and all could opt out of study participation.
Intervention
The INtegrating Systematic PatIent-Reported Evaluations (INSPIRE) intervention consisted of 3 components. First, patients completed the WeCARE tool survey as standard of practice, which included a modified electronic version of the GA and cancer treatment concerns (see Table S1 in the supplementary materials, available online with this article).26–28 Potential treatment-related preferences included ability to work, bucket list items, burden on family, interest in clinical trials, daily life impact, emotional or mental concerns, fertility, financial impact, logistics and convenience, personal responsibilities, sexual concerns, and side effects, and patients were asked to identify their top 3.49,50 Prior to their scheduled appointment with medical oncology, a link to the WeCARE survey was sent to patients for self-completion. If not completed at the time of the appointment, a nonclinical navigator would meet the patient in clinic and help with survey completion.
Second, after the presentation list for the weekly pancreatic MDTB was released, which is typically between 36 and 48 hours prior to the meeting, a research coordinator (E. Ortiz-Olguin) would review the list to assess for eligible participants. Eligible patients were then contacted and verbally consented to have their data presented during MDTB. For patients without a completed WeCARE survey, the research coordinator facilitated completion after obtaining verbal consent for presentation. This typically occurred when the patient entered the medical system through surgical oncology, where a full roll-out of the WeCARE tool is not yet complete.
Third, the research coordinator used the WeCARE survey data from the Carevive clinician dashboard to develop a single PowerPoint slide that was presented by a clinical partner (C. Pywell, G.R. Williams) at the MDTB (Figure 1). For patients in the intervention, the GA and treatment concerns data were presented by radiologists and/or pathologists after the presentations but before initiation of group discussion. Finally, discussion continued until consensus on appropriate next steps was reached.
Sample INSPIRE slide with GA and patient preferences.
Abbreviations: GA, geriatric assessment; INSPIRE, INtegrating Systematic PatIent-Reported Evaluations.
Citation: Journal of the National Comprehensive Cancer Network 22, 9; 10.6004/jnccn.2024.7052
Data Capture
Multidisciplinary Tumor Boards
Control period tumor boards were recorded from November 2021 through February 2022 and transcribed verbatim with line-level time stamps. Transcripts were then parsed at the patient level for further analysis. The same inclusion/exclusion criteria used for the intervention patients were applied to the recorded preintervention patients. During the intervention, each MDTB in which an enrolled patient was presented was recorded and transcribed. If patients were presented more than once during the preintervention recording period, only their first presentation was included in this analysis. Recordings of the initial presentation of all 50 intervention participants occurred between September 2022 and June 2023 and were transcribed verbatim with line-level time stamps. Recording of subsequent presentations at tumor boards for intervention patients continued until December 2023. The portions of the tumor board with eligible patients were abstracted and coded. Total duration of presentation, duration of primary provider introduction, duration of patient INSPIRE data discussion, duration of presentation of GA and patient concerns data, and duration of treatment recommendation discussion were calculated using time stamps by a medical resident (G. Bourne) and reviewed for accuracy by an anthropologist (N.L. Henderson).
Surveys
The patient’s primary clinician completed a post-MDTB survey to determine the impact of the ePROs on their treatment decision-making after each intervention case was presented. Clinicians also completed exit surveys at study completion to assess implementation outcomes.
Interviews
All clinical individuals who had participated in the pancreatic MDTB during the intervention period were invited to a semistructured interview. Participating in the interview was voluntary and each interview lasted approximately 15 to 20 minutes. Interviews were conducted by an anthropologist (N.L. Henderson).
Outcomes
Proctor et al’s implementation outcomes were used to assess intervention success.46 Penetration (primary outcome) was defined as the proportion of consented patients who were presented at tumor boards. Penetration was deemed successful if 70% of the patients enrolled in the study were presented and discussed in MDTB meetings. Secondary outcomes included adoption, feasibility, acceptability, appropriateness, cost, and sustainability. Adoption was defined as the degree of uptake of an intervention and was assessed in both patient and clinician populations. Among patients, adoption was measured by the proportion of patients who enrolled and completed surveys at baseline and 3- and 6-month intervals. Among clinicians, adoption was assessed by the proportion of clinicians willing to participate and enroll patients in the intervention. The following questionnaires were administered via email, telephone, or in person to all providers who had enrolled a patient at the end of the study: the Acceptability Intervention Measure (AIM),46,51 the (IAM),46,51 and the Feasibility of Intervention Measure (FIM).46,51 Intervention cost was defined in 2 ways. First, an objective assessment of time cost was conducted using time coding analysis on preintervention and intervention MDTBs. Second, a subjective measure of intervention time cost was assessed by asking participating providers to rate their perception of time cost through a survey at study closure. Specifically, they were asked to rate their agreement on a Likert scale with the statement, “The intervention did not take too much time.” Finally, intervention sustainability was defined using 2 approaches. The first included a survey item assessing provider interest in continuing the intervention in the future. The second involved poststudy semistructured interviews with participating clinicians regarding their experiences with the intervention and recommendations for future iterations and expansion of the project.
Results
A total of 50 patients participated in the intervention out of 59 approached, for an enrollment rate of 85%. The primary refusal reasons were passive (56%), in that patients verbally consented but did not complete the survey in time for the MDTB meeting. Often, the time between initial contact and MDTB presentation was <48 hours due to timing of when the MDTB list was made available. Another 3 (33%) patients reported being “too overwhelmed” or “not well enough” to complete the survey. In the historical comparison group, 31 patients were identified for inclusion. Patient summary demographics and demonstration of sample equivalence are provided in Table 1. In the intervention sample, most patients were female (54%), White (60%) or Black (26%), and had a mean [SD] age of 72.4 [8.4] years. Furthermore, most intervention patients were insured by Medicare (78%), were officially diagnosed with pancreatic adenocarcinoma (88%), and were staged I–III (76%). In the preintervention sample, gender was more evenly split (48% female), whereas proportions of race/ethnicity (White, 68%; Black, 26%) and age (mean [SD], 71.1 [8.6] years) were similar. Additionally, most preintervention patients were insured by Medicare (77%), had a pancreatic adenocarcinoma diagnosis (84%), and were staged I–III (77%). There were no statistically significant differences in the proportional representation of any captured sociodemographic or clinical characteristics between the historical comparison and the intervention groups of patients.
Demographic and Cancer Characteristics
Penetration and Patient Adoption
All 50 participating patients completed the baseline survey and had ePRO data presented at ≥1 MDTB meetings, resulting in a baseline penetration rate of 100%. Most patients (76%) reported completing the survey themselves, 71% answered at least 90% of the survey, and 84% completed the survey in <60 minutes. Patient adoption, assessed by rates of patient survey submission, decreased over time, with 100% submitting at baseline, 60% submitting at 3 months, and 56% submitting at 6 months. Rates of complete survey data also decreased over time, with sufficient data to calculate the GA score from 96% of intervention participants at baseline, 50% at 3 months, and 42% at 6 months. Furthermore, 18% of patients were deceased within 6 months, due to the high morbidity and mortality of this patient population. During MDTB presentations, GA data (96%) was more often verbalized and discussed than patient concerns data (78%).
Physician Adoption, Acceptability, Appropriateness, and Feasibility
All clinicians agreed to participate in the intervention (physician adoption rate, 100%) and all post-MDTB surveys for intervention patients were completed. For the 50 intervention patients, presenting clinicians (n=9) reported that ePROs were useful in 90% and led to a change in their treatment plan in 30% of cases. One clinician did not complete the exit-survey due to leaving the institution prior to study end. Regarding acceptability, all clinicians either agreed or completely agreed that the intervention met their approval (57% completely agree; 43% agree) and was appealing to them (71% completely agree; 29% agree), and further that they liked (57% completely agree; 43% agree) and welcomed (57% completely agree; 43% agree) the intervention (Figure 2). Clinician survey responses were positive or neutral in regard to whether the intervention seemed fitting (71% completely agree; 29% agree), suitable (71% completely agree; 29% agree), applicable (71% completely agree; 14% agree; 14% neither agree nor disagree), and a good match (57% completely agree; 43% agree). Providers mostly agreed or completely agreed that the intervention seemed implementable (71% completely agree; 29% agree), possible (71% completely agree; 29% agree), doable (57% completely agree; 43% agree), and easy to use (57% completely agree; 29% agree; 14% neither agree nor disagree).
Provider end-of-study AIM, IAM, and FIM survey results.
Abbreviations: AIM, Acceptability Intervention Measure; FIM, Feasibility of Intervention Measure; IAM, Intervention Appropriateness Measure.
Citation: Journal of the National Comprehensive Cancer Network 22, 9; 10.6004/jnccn.2024.7052
Cost
Presentation of the INSPIRE data took a mean [SD] of 36.4 [14.7] seconds per patient (Table 2). Minor shifts were observed in time spent, with slightly less mean time spent on patient introduction (89.0 vs 96.2 seconds) and more time on the treatment discussion (102.7 vs 67.2 seconds) in the intervention group versus the preintervention group, respectively. In total, the intervention led to a modest increase in mean MDTB time of 51.1 seconds in time-per-patient in the intervention group when compared with the preintervention sample (mean [SD], 223.8 [107.1] vs 172.7 [111.4] seconds, respectively). Of the 9 clinicians who enrolled patients into the intervention, most (86%) reported that it was “true” that the intervention did not take too much time.
Time-Coding Results of Recorded MDTBs
Sustainability
A total of 10 individuals, including 2 medical oncologists, 2 surgical oncologists, 1 radiation oncologist, 2 radiologists, 2 endoscopists, and 1 nurse practitioner, participated in semistructured interviews. Clinicians commented that it “didn’t take a lot of extra time at tumor board to discuss the results” (radiologist 1). In addition, participating clinicians reported that the intervention “integrated well into the flow of the tumor board” (surgical oncologist 1). Finally, in regard to the sustainability of the intervention, 100% of surveyed clinicians indicated they would like to continue this intervention in the future. Within the interviews, one clinician expressed that “we should keep doing it” (radiologist 2), whereas another clinician believed the intervention should be standard of care: “It is easily translatable. I think you know the GA is really designed to be that way. I mean, this is…its objective. I mean it definitely should be used…but it really is basically precision cancer care for older adults. And so, this should be standard of care.” (medical oncologist 1). MDTB clinicians also suggested ePROs to include in future iterations of the intervention, including baseline patient willingness to undergo specific treatments (eg, surgery vs chemotherapy), degree of familial and social support available to the patient, and any salient travel considerations.
Discussion
In the last decade, numerous studies have demonstrated the benefits of ePROs,52,53 leading to Medicare requiring all hospital systems that participate in their payment reform demonstration project to develop ePRO capture systems.54 However, an implementation gap has remained regarding how to consistently and efficiently incorporate ePROs into daily clinical practice. This pilot study demonstrated that the integration of patient-reported fitness measures and treatment concerns into the pancreatic MDTB at UAB was acceptable, appropriate, feasible, adoptable, cost-effective, and sustainable. The intervention was readily adopted by patient and clinician participants, and presented INSPIRE data were used by the MDTB clinical team to make treatment decisions. This adds to existing literature about how ePROs can be meaningfully integrated into clinical oncologic settings55,56 and offers a promising venue for addressing previously identified barriers to clinical team engagement with ePROs.57,58
Although this was a small pilot study at an academic hospital, the results indicate a potentially novel way to ensure ePRO data are incorporated into medical decision-making, which could be applied in a variety of health care settings. The MDTB represents an environment in which team members already synthesize multiple types of data from varying sources (eg, scans and reports from radiologists and pathologists) to make appropriate treatment decisions for patients. Adding the GA and treatment preferences data to the pool of information with which the MDTB made those decisions was a natural extension that allowed the clinical team to do their jobs in a more efficient and standardized way. Thus, as one of the participating physicians said, the INSPIRE intervention is “not reinventing the wheel,” but is facilitating a more structured and complete mechanism for patient-centered care. Additionally, engaging clinicians at the team level rather than at the individual level ensured multidisciplinary consideration and discussion, which are associated with increased adherence to clinical guidelines, better screening rates for clinical trial participation, and improved patient outcomes.59,60 Ultimately, with all physicians agreeing that this should be continued, this approach provides a feasible pathway to align with recommendations about use of the GA within the NCCN Clinical Practice Guidelines in Oncology (NCCN Guidelines) for Older Adult Oncology.23
Importantly, we observed minimal to modest time costs associated with the INSPIRE intervention, with presentation of the ePRO data averaging 36.4 seconds per patient. This could be concerning, given the limited time to discuss all patients at tumor boards. However, we also saw shifts in how MDTB discussion time was spent during the intervention, with clinicians spending less time on patient introductions and more time on treatment decision discussions. This added time also likely came from the MDTB clinicians experiencing discordance between their subjective perception of the patient’s frailty and the objective measure provided by the GA, which will be discussed in future publications. Importantly, clinicians reported a change in their intended treatment pre-MDTB versus post-MDTB in nearly a third of the intervention patients. Thus, with <1 minute of added discussion, clinicians gained a better understanding of patient fitness status and their concerns, which could make more informed decisions.
Several limitations to this study merit discussion. First, the pilot intervention data were limited and results may not be applicable to other contexts. The study was only conducted among older patients with pancreatic cancer, for whom treatment decisions often consider patient fitness level and their ability to tolerate certain treatment regimens. This may be different for other cancer types with a wider range of treatment options and regimens. Furthermore, the pancreatic MDTB at UAB is structured such that all patients with pancreatic cancer are funneled through the MDTB, which may differ from other institutions whose MDTBs focus only on unique cases or late-stage cancers. Notably, the participation rate for the clinicians in this pilot study was very high and provided a wide range of clinical perspectives in this evaluation. Another limitation was that acceptability, appropriateness, and feasibility assessments were sent only to clinicians who enrolled patients into the trial and not to all participants in the MDTB; this limits the interpretability of these measures. However, all MDTB participants were invited to participate in semistructured interviews where they positively reviewed the intervention and offered key modifications for future iterations and larger scale implementation of the intervention. Greater insight into the patient’s support network and other social determinants of health needs could potentially add another psychosocial dynamic to the MDTB that could encourage even greater patient centricity. Future research on patient perception of the benefits and consequences to greater integration of ePRO data into treatment decision-making should also be explored.
Conclusions
We found that the integration of ePROs into MDTBs was feasible and acceptable for patients with pancreatic cancer, thereby providing a potential approach to increasing clinical team engagement with, and management using, ePROs. The intervention averaged only an additional 36.4 seconds per patient when compared with historical MDTBs, while increasing the systematic discussion of patient fitness and concerns. Our next steps include conducting a larger randomized controlled trial to evaluate whether ePRO integration into MDTBs positively impacts patient experiences and outcomes.
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