Abstract: A growing body of evidence supports the use of remote symptom monitoring based on patient-reported outcomes (PROs) to manage symptoms, improve quality of life, and reduce inpatient hospitalizations and emergency department visits. Health systems, payers, and specialty societies support the collection of PROs. Oncology practices are integrating PROs into their electronic health records to monitor and manage patients’ health status and symptoms. Despite a growing evidence base and enthusiasm for the use of PROs, collection in routine oncology practice remains limited, with persistent gaps in our understanding of the value of PRO collection and practical methods of implementation. Ongoing research seeks to define methods to overcome these barriers and gaps. This review summarizes the practical uses and potential benefits of PROs in routine oncology care, discusses continued knowledge gaps, and highlights recent examples of successful implementation.
Introduction
Patient-reported outcomes (PROs) are reports of health status or health condition provided directly by patients without interpretation by clinical teams.1 PROs are collected with structured, standardized, validated instruments, termed patient-reported outcome measures (PROMs), which are widely used in clinical trials and are being increasingly used in routine clinical practice and research.2-4 PROs capture patient experiences with respect to disease- or treatment-related symptoms, adverse events, and health-related quality of life, among other measures. Randomized and pragmatic studies have shown that PROs improve patient-clinician communication,5 improve self-efficacy,6,7 decrease symptom burden,6 reduce distress,8 preserve and improve quality of life,9,10 reduce the use of acute care,10-12 improve survival in the metastatic setting,13 and improve survival among patients undergoing lung cancer treatment.14,15
The evidence base to support the integration of PROMs in oncology is rapidly growing. A recent systematic review and meta-analysis of randomized controlled trials found that PROM integration into cancer care was associated with decreases in all-cause mortality and improvements in health-related quality of life at 12 weeks after the initiation of treatment.16 Specialty societies have endorsed or encouraged the integration of PROMs into routine practice.17,18 Similarly, electronic health record (EHR) vendors have made remote symptom monitoring via electronic PROs (ePROs) available to their oncology practice clients.19,20 Oncology practices are integrating PROMs into their workflow, and systematically integrating PROMs to monitor and manage symptoms between clinic visits has been proposed as an effective patient-centered intervention.21,22
The collection of PROs in routine practice supports patient-centered care by monitoring patients’ symptoms, health-related global quality of life, and other outcomes in a systematic manner,23,24 and by ensuring that symptom assessment does not depend on the evaluations of individual clinicians. Although prior studies have established the benefits of PROs, gaps remain in our understanding of the practical uses of PROs in routine practice. The objectives of the review are to present the practical uses and potential benefits of PROs in routine oncology care and to highlight recent examples of successful implementation.
Practical Uses of PROs to Support Patient Care
We discuss several practical uses of PROs in routine oncology care and note that multiple studies have reported promising strategies for integrating PROs into routine clinical care (Table). By assessing patients’ symptoms, PROs maximize benefits to patients and help providers and oncology practices deliver high-quality care. In the following sections, we explore the practical uses of PROs to support patient care and describe the potential benefits to clinicians and delivery systems.
Benefits to Patients of Remote Monitoring vs In-Clinic Assessments
A growing body of research supports the use of remote symptom monitoring via PROMs. Remote monitoring has been gaining traction to prevent avoidable downstream consequences and ensure treatment success.6,25,26 Remote monitoring makes it possible for patients to report when symptoms are especially bothersome, and a clinical action at the right time can prevent worsening of symptoms or the development of more severe complications.12,27,28 Remote monitoring may be preferable to in-clinic assessment, particularly for patients with cognitive decline or memory challenges. An assessment on the day systemic therapy is administered may underestimate patients’ true symptom burden through delayed symptom capture or may not adequately capture symptoms that manifest between cycles of systemic therapies.29 Furthermore, the symptoms of patients undergoing surgery manifest differently from the symptoms of patients on systemic therapies. For example, postoperative symptoms in most cases are expected to subside with time; however, symptoms due to systemic therapies may become chronic or persistent as therapies accumulate or symptoms develop later.30,31 Acute symptoms are more likely to be missed if assessments are performed only in the clinic.
Improving Communication. Improving communication between the patient and the care team during and between visits is an added benefit of PROs. Evidence shows that remote monitoring increases the frequency of discussion of patient concerns to optimize patient-clinician communication during office visits.3,32,33 A randomized trial found that the use of PRO data in the intervention arm increased the likelihood that symptoms and quality of life would be discussed, with improved quality of conversation and no added consultation time.5,8,34
Improving Personalized Symptom Management. Symptoms that oncology patients experience vary and may be affected by the disease or its treatment. Scores generated from PROs can identify patients in need of supportive care or those who may benefit from symptom-specific interventions, such as cognitive behavioral therapy for insomnia, psychological counseling for anxiety or depression, and social support for hopelessness and loneliness, among other ongoing psychosocial needs.33,35-38 Furthermore, PRO data can help assess longitudinal patterns or trajectories of prevalent or bothersome symptoms.39 Assessing symptom trajectories and periods when symptoms may be more bothersome makes it possible to personalize supportive and cancer-directed therapies. Similarly, patients undergoing cancer treatment may report multiple concurrent symptoms, posing a management challenge.40-43 Patients with concurrent bothersome symptoms may require multiple medications that induce different adverse effects.43,44 If identified early, these symptoms can be addressed through dose or treatment modification to reduce the burden of symptoms before they become more complex. Early adjustments to therapy may increase treatment adherence and the duration of therapy, potentially affecting treatment success. PROs can also help identify patients for whom reassessment of treatment goals and referrals to palliative and end-of-life care are appropriate.45,46 Timely palliative care may also improve symptom control and quality of life, so that patients receive less aggressive care, report greater satisfaction with care, and potentially live longer.47
Improving Patient Involvement and Engagement. The collection of PROs can enhance patient empowerment and engagement and incorporate patients’ perspectives into the decision-making process.48,49 For example, decisions regarding modifications to treatment plans, cessation of therapy, and referrals to palliative and supportive care can be enhanced through shared decision making via PROs, and this increase in patient engagement may improve satisfaction with care.50 PROs improve symptom management by increasing clinicians’ awareness of patient-reported symptoms, creating an accurate view of burden51 that is often underestimated by clinicians.52,53 Greenhalgh and colleagues found that PROMs supported patient-clinician communication and prompted patients to raise concerns with clinicians, thereby raising clinicians’ awareness of patients’ symptoms.54 Clinicians’ awareness of bothersome symptoms facilitates clinical interventions to prevent downstream consequences. Randomized controlled trials have shown that when patients report adverse events, clinician action results in a reduced severity of symptoms, improved health-related quality of life, longer adherence to chemotherapy, and other meaningful outcomes.6,7,9,55
Benefits to Clinicians and Delivery Systems
PROs can generate clinically meaningful alerts for clinician action and improve quality of care and health equity. They can also be used to support advanced data analytics.
Generating Clinically Meaningful Alerts for Clinician Action. Many ePRO systems generate alerts for clinical action when patients report severe or worsening symptoms. Electronic collection of PROs makes it possible to generate scores based on symptom reports to create clinically important thresholds for clinical actions according to severity, frequency, and/or interference with the patient’s activities of daily living.56,57 PRO data can also be used to develop risk stratification algorithms to support clinical interventions. For example, the PROMPTCare platform used PRO data to develop automated algorithms that could risk-stratify patients and recommend clinical actions to provide risk-stratified, guideline-informed care.58
Patient-generated data can also be used to structure selective and clinically meaningful alerts for patients receiving cellular therapy or immunotherapy. Among patients on chimeric antigen receptor (CAR) T-cell therapy managed in the outpatient setting, a pilot program helped to identify those requiring escalation of care by alerting clinicians to adverse or worsening symptoms and vital sign changes.59 EHR rules can be adjusted for specific indications so that alerts are not generated for symptoms that are common and expected.23,60 These novel and judicious uses of PRO data to support clinical actions may lead to timelier responses, reduce the clinician burden, and prevent treatment sequelae.22,33,61
Improving Quality of Care and Health Equity. Outcomes are central to assessing the quality of care and demonstrating value to the patient. Clinician-reported outcomes are important but inadequate to evaluate the overall quality of care. Analysis of patient-reported data collected in a structured manner provides population-level estimates to assess various outcomes of interest. Population-level estimates derived from patient-level PRO data can be used to measure, monitor, and improve quality in surgical and radiation oncology care, among other settings.62,63 Population-level differences in outcomes provide a critical window into how patients tolerate a given treatment protocol. Furthermore, comparing provider or hospital performances helps to identify gaps and disparities in care, establish quality care benchmarks, and compare improvement efforts.64 When PRO data are used to measure and compare outcomes, they can spur local or regional efforts at quality improvement and the monitoring of long-term quality of care at the population level.62
Extending the Use of PROs to Support Advanced Data Analytics. PROs provide real-world data that can be used to tell the patient-reported story visually, helping to foster improvements in routine practice. Advanced analytics and dashboards can be generated for on-demand insights.65 Furthermore, PRO data can be extended to develop prediction models that estimate the risks of complications after treatment, improvements in quality of life, improvements in physical function, and mortality risks.66,67 PROs are predictors of treatment success and survival.68,69 Early interventions can be offered to patients who are predicted to have the highest risk of adverse outcomes. For example, patients with higher predicted probabilities of avoidable inpatient use may be managed differently from patients at average risk.
Case Studies
Recent advances in the use of PROs provide promising opportunities to collect patient-reported symptom data for remote symptom monitoring and active symptom management. Numerous examples of the use of PROs in routine medical and surgical oncology settings are reported in the literature. Examples of recent advances in the use of PROs in the United States appear in the Table. Below, we discuss 3 exemplary case studies.
Engaging Men in Patient Reported Outcomes (EMPRO)
The International Registry of Men with Advanced Prostate Cancer (IRONMAN) is a global registry collecting treatment, outcome, and patient-reported data from men who are living with advanced prostate cancer. Because patients are living longer, survivors face a unique set of symptom burden and quality-of-life challenges that are often different from those associated with localized disease.70,71 Engaging Men in Patient Reported Outcomes (EMPRO), an IRONMAN substudy, is prospectively recruiting a diverse group of men living with prostate cancer to test the effectiveness of remote symptom and quality-of-life monitoring. Specifically, the EMPRO study is designed to assess if remote monitoring of symptoms in patients with advanced prostate cancer improves long-term outcomes compared with the standard of care.71
Patients are asked to use the EORTC QLQ Core Questionnaire (EORTC QLQ-C30), the Brief Pain Inventory, the Functional Assessment of Cancer Therapy-Prostate Symptom Index 17 (FACT-FPSI-17), and the Expanded Prostate Cancer Index Composite (EPIC-26) to report their symptoms and quality of life.70 PROs are collected at baseline and subsequently every 3 months. Worsening symptoms or quality-of-life concerns are flagged for clinical action with self-management tips or a follow-up call from a clinical team member. The intent is to alert clinicians of changes in a patient’s symptoms that might result in serious complications if the symptoms remained unresolved. Preliminary analyses from the EMPRO study indicate that a diverse set of patients are engaging and reporting symptoms routinely, with 20% of respondents self-identifying as Black men.72 Despite this positive trend, the opportunity for improvement remains because Black men experience a disproportionate prostate cancer burden.
The Symptom Management Implementation of Patient-Reported Outcomes in Oncology (SIMPRO)
The Symptom Management Implementation of Patient-Reported Outcomes in Oncology (SIMPRO) Research Center is a collaboration involving 6 diverse, independent cancer centers in the United States. The goal of SIMPRO is to assess the effectiveness of an electronic symptom management system, eSyM, in a routine care setting. SIMPRO developed, deployed, and tested eSyM, which is now widely available through Epic Systems.20 In SIMPRO, patients with confirmed or suspected gastrointestinal, gynecologic, or thoracic malignancies were asked to complete symptom reports after the initiation of chemotherapy or after a surgical procedure.73 Between September 2019 and March 2023, more than 9500 medical oncology and 13,200 surgical oncology patients used eSyM to report symptoms.
Although the final analyses of SIMPRO data are ongoing, preliminary results point to decreases in emergency department visits and inpatient encounters among those who completed at least one symptom questionnaire vs those who did not. When symptom responders were compared with nonresponders, the responders were less likely to make emergency department visits: 5.3% vs 7.1% at 30 days and 10% vs 12.9% at 90 days. Similarly, 6.7% of responders vs 11.3% of nonresponders had been admitted to the hospital at 30 days and 14% of responders vs 19.5% of nonresponders had been admitted to the hospital at 90 days, with statistically significant differences (P<.001) for all analyses.74 The contribution of SIMPRO to the advancement of active symptom management is noteworthy. SIMPRO includes 6 cancer centers that serve a diverse patient population; results and learning may be transferable to health systems that are interested in implementing ePROs for active symptom management.75 By developing and integrating an ePRO-based system for routine clinical use, SIMPRO has paved the way for oncology practices worldwide to roll out ePROs for their patients.
Recovery Tracker
Recovery Tracker is a postoperative symptom tracker that has been implemented to monitor patients’ symptoms remotely after ambulatory cancer surgery at Memorial Sloan Kettering Cancer Center (MSKCC). This is a Web-based electronic survey incorporated into MSKCC’s patient portal. Implemented in 2016, Recovery Tracker monitors symptoms daily and provides feedback if the reported symptoms are expected to require follow-up.76 Patients undergoing ambulatory surgery for breast, gynecologic, urologic, and head and neck cancers and for benign tumors are able to report symptoms.77 Symptom surveys are triggered automatically after discharge, and patients receive daily reminders to complete the surveys for 10 postoperative days. Survey items were adapted from the PRO-CTCAE of the National Cancer Institute and include 12 common symptoms and symptoms specific to postoperative settings, including redness and discharge.12,76 A custom-built alert system that categorizes alerts as “yellow” for intermediate-level symptoms and as “red” for concerning symptoms is in place to support clinical decision making.27 An automatic notification is sent to the surgeon’s office if a yellow alert is generated. For red alerts, the patient and the surgeon are notified, and the patient is asked to contact the doctor immediately. Recovery Tracker was associated with a 22% reduction in the odds of an avoidable urgent care visit without readmission within 30 postoperative days at MSKCC urgent care centers.12
In addition to the preceding case studies, several ongoing projects are developing, deploying, and testing ePROs in routine oncology practice. The Patient-Centered Outcomes Research Institute (PCORI) has funded 9 projects to implement ePRO systems to improve symptom management after treatment.78 The funded health systems are tracking the implementation of ePROs and assessing whether they improve patient outcomes and reduce acute care use. These funded projects are implementing ePROs in routine oncology practice. When a patient submits a report of a severe or worsening symptom, clinicians are notified. Oncology nurses, navigators, social workers, or triage nurses respond to the alerts. Patients with advanced cancer or metastatic disease who are undergoing treatment receive reminders to complete symptom surveys.78 OncoPRO is another example of a PCORI-funded project that is implementing results from the randomized PRO-TECT trial9,10 into routine oncology practice.79 OncoPRO enables patients to complete surveys that elicit responses about symptoms, functioning, and other health concerns. An alert notifies clinicians of concerning or worsening symptoms. This project aims to support practices as they design, deploy, and implement, PROs while providing guidance, best practices, and standard operating procedures for long-term implementation success.17
Discussion
PROs allow patients to report and clinicians to systematically assess relevant symptoms and side effects during active treatment and survivorship. The routine use of PROs may transform symptom management into a proactive process that involves remote monitoring, identification of evolving or worsening symptoms, and clinical action to address bothersome symptoms. A proactive symptom management process intentionally monitors patients for changes in their symptoms and quality of life, facilitating bidirectional communication between patients and their clinicians. This process has the potential to improve care, but it may also become burdensome to an already-stretched clinical team. Despite the benefits and practical uses of PROs, gaps in our understanding persist.
First, most PROMs were originally developed and used in clinical trials but are now being increasingly used in routine clinical care. In clinical trials, surveillance and monitoring for adverse events are paramount. In routine practice, succinct and actionable information is prized. Thus, an exhaustive inventory of all possible symptoms may be neither judicious nor clinically useful. It is unclear if the PROMs developed for clinical trials focused on comprehensiveness are ideal for use in routine clinical settings. In routine clinical practice, pragmatic properties are important, and utility therefore must be balanced with psychometric properties to ensure clinical uptake.80
Second, the cancer treatment landscape is rapidly evolving, with new therapeutics, including immunotherapy and CAR T-cell therapy, being used to treat many cancers. The PROMs developed early for use in clinical trials assessed primarily symptoms associated with chemotherapy agents. As the treatment landscape evolves, it becomes imperative that PROMs be continually adapted to meet the needs of patients on these newer therapies, as the symptoms of patients receiving these therapies are likely to manifest differently from the symptoms of patients on conventional systemic therapies. Therefore, continued psychometric research is warranted to assess how well the current measures developed for clinical trials—with a strong emphasis on comprehensiveness, reliability, and validity—translate into clinical contexts that emphasize actionability, efficiency, and user-friendliness.
Third, remote symptom monitoring systems are designed to alert clinicians to symptoms above a certain threshold or to worsening symptoms. These alerts alone are unlikely to be helpful if resource constraints limit clinician action. For example, a patient and clinician may be left without good options if the patient reports a symptom, such as lack of physical functioning due to severe fatigue, for which no immediate solution may be available. Furthermore, when a patient is asked about bothersome symptoms, there is an expectation that the clinician will help alleviate those symptoms. When resources are unavailable to help patients (ie, lack of referral options, lack of therapeutic solutions, or limited provider training in symptom management), patients and clinicians may become discouraged.65 Thus, symptom management recommendations must be aligned with the questions being asked in the PROMs to ensure that a closed-loop symptom management system is in place. More implementation research is needed to ensure that PROMs and treatment recommendations are aligned and available to the clinicians managing patient symptoms.
Fourth, cancer care is becoming increasingly complex, with multidisciplinary teams involved in patient care. Communication and coordination of care (ie, during care transitions) between multidisciplinary teams are a challenge in oncology. Evidence demonstrating improvements in symptom management comes from studies conducted in single-discipline practice settings. For example, evidence of PROs supporting improved survival in the trial of Basch and colleagues comes from patients who underwent routine chemotherapy for metastatic solid tumors.13 Similarly, the study by Denis and colleagues, which demonstrated an association between symptom monitoring via weekly PRO reporting and increased survival, comes from patients undergoing chemotherapy for lung cancer.14 Because these studies were conducted in systemic therapy settings, it is unknown what, if any, role PROs might play in improving communication between patients and clinicians and coordination among clinicians in multidisciplinary settings.
Conclusion
Although the monitoring and management of patients’ symptoms are already part of high-quality, patient-centered cancer care, opportunities exist for further advancement. The integration of PROMs into routine practice can streamline and systematize symptom monitoring and management. Underutilization of PRO data, even if it is collected routinely, limits its effect on treatment decision making. Continued investment in improving our understanding of the effect of PROs on patient outcomes is critically important to demonstrate the value of PROs in routine practice. Private and public payers should consider PROs to be part of high-quality care and make the outcomes that matter most to patients the central part of quality measurement and reimbursement. Further research is needed to make PRO data actionable and seamlessly integrated into clinicians’ workflow as they go about making treatment decisions.
Disclosures
Dr Morgans has done consulting for Astellas, AstraZeneca, Bayer, Bristol Myers Squibb, Curium, Exelixis, Exact Sciences, Johnson & Johnson, Lantheus, Macrogenics, Merck, Novartis, Pfizer, Sumitomo Pharma, Inc, Telix, and Tolmar, and has conducted research for Astellas, Bayer, Johnson & Johnson, Lantheus, Pfizer, Sumitomo Pharma, and Telix. Dr Hassett has received funding from the National Cancer Institute. Drs Jackson and Paudel have no disclosures.
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