Every year, 14.1 million people worldwide (GLOBOCAN/International Agency for Research on Cancer, 2012), including 1.7 million Americans (Siegel, Miller, & Jemal, 2017), are diagnosed with cancer. Cancer treatment can cause significant morbidity, including fatigue, lymphedema, pain, neuropathies, balance problems, mobility issues, bowel and bladder dysfunction, dysphonia and other communication difficulties, dysphagia, cardiopulmonary function declines, sexual dysfunction, and cognitive and psychosocial problems, among others (Silver, Baima, & Mayer, 2013). Problems that arise during treatment are compounded by late effects of treatment affecting bone, cardiac, and other organ systems that can emerge years after cancer treatment (Hewitt, Greenfield, & Stovall, 2006 ; Hewitt, Weiner, & Simone, 2003) and can cause premature aging (Cupit-Link et al., 2017). The prevalence of these problems varies by factors including type of treatment, patient age, and preexisting comorbidities; however, as many as 20% of childhood cancer survivors (Ness et al., 2005), 53% of adult-onset cancer survivors (Ness, Wall, Oakes, Robison, & Gurney, 2006), and 65% of older adults with cancer (Pergolotti, Deal, Lavery, Reeve, & Muss, 2015) report functional limitations.
The functional limitations from cancer-related impairments contribute to depression, anxiety, and poor quality of life (Bodurka-Bevers et al., 2000 ; Hopwood & Stephens, 2000 ; Zebrack, Yi, Petersen, & Ganz, 2008). Together, these problems limit the ability to work (Islam et al., 2014 ; Mehnert, 2011 ; Stein, Syrjala, & Andrykowski, 2008 ; Stergiou-Kita et al., 2014 ; Sun, Shigaki, & Armer, 2017) and increase healthcare utilization, driving up healthcare costs (Chang et al., 2004). Functional limitations also increase the risk of mortality (Brown, Harhay, & Harhay, 2016 ; Kenis et al., 2017 ; Sehl, Lu, Silliman, & Ganz, 2013).
Comprehensive cancer rehabilitation care involves diverse coordinated interventions, which include physical, occupational, or speech therapy; tailored therapeutic exercise prescription; psychosocial and cognitive interventions; and physician-directed diagnostic imaging, injections, and pharmacological symptom management. Comprehensive cancer rehabilitation has the potential to treat many treatment-related impairments, improving physical functioning, social well-being, and quality of life (Duijts, Faber, Oldenburg, van Beurden, & Aaronson, 2011 ; Mewes, Steuten, Ijzerman, & van Harten, 2012 ; Monga et al., 2007 ; Silver et al., 2013) and the ability to function in the workplace (de Boer et al., 2015).
Despite the benefits of cancer rehabilitation interventions, very few patients receive these services. Research has shown that referral rates for cancer rehabilitation are as low as 1%–2% (Cheville, Beck, Petersen, Marks, & Gamble, 2009). The underutilization of cancer rehabilitation has not always been the problem it is today (Alfano, Ganz, Rowland, & Hahn, 2012). Decades ago, cancer rehabilitation was more integrated with cancer care. The National Cancer Act of 1971 funded clinical cancer research centers, including demonstration projects to assess rehabilitation needs and evaluate rehabilitation interventions (National Cancer Institute, 2016). By the early 1980s, a number of hospital-based multidisciplinary cancer rehabilitation teams provided services to patients with cancer (Harvey, Jellinek, & Habeck, 1982). However, since the 1980s, there has been a shift in cancer treatment to less intensive surgery requiring shorter or no hospital stays and outpatient rather than inpatient chemotherapy, and an increasing number of patients are being treated in community cancer centers with no connection to interdisciplinary rehabilitation teams. Thus, even as the cancer survivorship movement has risen, focusing attention on quality of life among long-term survivors, these changes to cancer care delivery have resulted in reduced referrals to interdisciplinary cancer rehabilitation, and many services closed (Alfano et al., 2012). Illustrating this point, the first National Cancer Policy Board report in 1999, “Ensuring Quality Cancer Care,” contained no recommendations for integrating cancer rehabilitation into cancer care (Institute of Medicine and National Research Council, 1999).
The current cancer care system does not routinely screen patients for impairments, nor is there a focus on preventing disability from treatments. Thus, impairments often go unidentified and unaddressed (Cheville et al., 2009). The loss of cancer rehabilitation services means that, when cancer rehabilitation services are prescribed today, they tend to have a one-dimensional focus rather than comprehensive assessment and coordinated delivery of interventions by an interdisciplinary team. Some highly efficacious interventions, especially tailored aerobic exercise prescriptions (Furmaniak, Menig, & Markes, 2016 ; Jones & Alfano, 2013 ; Mishra et al., 2012), are rarely prescribed at all and are not covered by insurance. Compounding this situation, the shortage of oncologists (Erikson, Salsberg, Forte, Bruinooge, & Goldstein, 2007) means that posttreatment follow-up care is often being delivered by primary care providers who lack training and awareness of the long-term and late effects of cancer treatment (Potosky et al., 2011) and are thus unlikely to be a source for rehabilitation referrals. The confluence of these factors means that impairments are often detected very late if at all, and survivors struggle with these problems years after treatment ends (Schmitz, Speck, Rye, DiSipio, & Hayes, 2012).
More recently, national reports and guidelines demonstrate that the field is recognizing the importance of cancer rehabilitation. In 2005, the National Cancer Policy Forum’s landmark second survivorship report “From Cancer Patient to Cancer Survivor: Lost in Transition” (Hewitt et al., 2006) included cancer rehabilitation as part of cancer survivorship care (Hewitt et al., 2006). A subsequent report (Institute of Medicine, 2013) emphasized the role that rehabilitation providers play as part of a coordinated cancer care team in optimizing patient recovery. Furthermore, an increasing number of scientific papers focus on cancer rehabilitation topics, and numerous “calls to action” aim to stimulate research and clinical efforts to improve referral to and delivery of cancer rehabilitation interventions (Alfano, Cheville, & Mustian, 2016 ; Alfano et al., 2012 ; Cheville et al., 2017 ; Lyons et al., 2017 ; Silver, 2013 ; Silver et al., 2013, 2015 ; Stubblefield, Schmitz, & Ness, 2013).
In the United States, the importance of cancer rehabilitation referrals is reflected in current American Cancer Society and American Society of Clinical Oncology guidelines for cancer follow-up (survivorship) care (Cohen et al., 2016 ; El-Shami et al., 2015 ; Runowicz et al., 2016 ; Skolarus et al., 2014). To address the continuing problem of the lack of referrals from oncology (Pergolotti et al., 2015), cancer rehabilitation educational sessions have been highlighted at the annual meetings of the American Society of Clinical Oncology (Alfano et al., 2016). As a further testament to the progress in establishing the role of cancer rehabilitation, in 2015, the National Institutes of Health convened a meeting of cancer rehabilitation experts to prioritize future efforts that promote quality cancer rehabilitation care. The report recommended integrating cancer rehabilitation with oncology care beginning at diagnosis (Stout et al., 2016).
Next-Generation Cancer Rehabilitation
Embedding comprehensive rehabilitation care as a standard part of cancer care has the potential to improve patient outcomes while simultaneously easing the burden on the healthcare system. However, this will take more than simply recreating the cancer rehabilitation system from the early 1980s. Just as next-generation DNA sequencing has spurred scientific discovery (Schuster, 2008) and transformed precision medicine (Collins & Varmus, 2015), cancer rehabilitation needs a similar transformation. To achieve next-generation cancer rehabilitation, current national efforts must focus on innovating in four critical areas: (1) innovating cancer rehabilitation care delivery, (2) expanding the team of providers, (3) creating precision medicine cancer rehabilitation to better predict and tailor the optimal therapies for given patients, and (4) demonstrating the value of cancer rehabilitation to drive referrals and reimbursement. Progress and needs in each of these areas will be described below.
Innovating Cancer Rehabilitation Care Delivery
A team of stakeholders has developed (Stout et al., 2012) and refined (Alfano et al., 2016) a prospective surveillance model as a best practice model for cancer rehabilitation delivery. This model specifies that rehabilitative referrals to an interdisciplinary team of providers begin at the time of cancer diagnosis and continue according to patient need, throughout and beyond cancer treatment. Ideally, a multidimensional, comprehensive assessment of symptoms, impairments, comorbidities, and exercise habits is conducted preoperatively to establish baseline functioning, identify patients with preexisting conditions that may place them at higher risk for the development of treatment toxicities and impairments during/after treatment, and refer patients with current problems for interventions to improve their symptoms and function. After the initial assessment, ongoing surveillance (through repeated assessments) occurs throughout and beyond cancer therapy, allowing for monitoring of the development of treatment toxicities or impairments and facilitation of timely referrals to cancer rehabilitation providers (see Figure 1).
The prospective surveillance model presents the opportunity for prehabilitation or initiating tailored exercise prescription, psychological treatments, or other rehabilitation interventions before cancer therapy starts (Silver et al., 2013). The goal of prehabilitation is either to deploy preventive interventions to keep problems from occurring or to treat already existing impairments and preserve functioning. Recent reviews of this emerging literature suggest that prehabilitation interventions may reduce functional impairments and improve psychosocial symptoms and, at least for patients with lung cancer, reduce surgical complications and the length of hospitalization (Carli et al., 2017 ; Treanor, Kyaw, & Donnelly, 2018 ; Tsimopoulou et al., 2015). However, future research must determine which patients are most likely to benefit from which prehabilitation interventions and investigate the effects of prehabilitation on patient functioning, perioperative complications, timeliness and adherence to oncology treatment, and healthcare utilization (Carli et al., 2017).
Implementing the prospective surveillance model in busy oncology clinics necessitates testing ways to deliver this care that does not create undue burden on practices. Cancer centers across the country are engaging in the routine collection of patient-reported outcomes that could be used to detect symptoms and impairments and generate referrals to cancer rehabilitation. Effectively using patient-reported outcome data has the potential to improve patient quality of life, reduce healthcare utilization, and improve survival (Basch et al., 2016, 2017). However, a systematic review of the trials evaluating the efficacy of patient-reported outcome measurement in oncology settings found that, although these instruments aid recognition of and patient–provider communication about symptoms, there is only modest evidence this process results in better patient outcomes (Chen, Ou, & Hollis, 2013). One possible explanation for this is that oncology teams lack information about the appropriate interventions or local providers where they should refer patients for a given problem. Thus, to be maximally useful for oncology, a two-component solution is needed that includes (1) a comprehensive assessment of patient needs that is (2) linked to treatment algorithms that specify interventions and aid referrals to rehabilitation. Such a solution could be embedded in the electronic medical record in a way that it is also linked to local providers with appropriate oncology expertise so that oncology teams know both the right intervention and the right provider for a specific referral.
Implementing the prospective surveillance model also will require testing ways to deliver cancer rehabilitation care that will address education, logistical, and cost hurdles that limit patients’ uptake of rehabilitation services (Binkley et al., 2012 ; Lattanzi et al., 2010 ; Ryans & Lichtman, 2014). Telemedicine interventions are being tested that deliver care electronically in geographic areas that lack formal cancer rehabilitation providers (Cheville et al., 2018), for example, by engaging cancer rehabilitation experts to provide support to rehabilitation providers with limited cancer expertise. In addition to improving access to rehabilitation interventions, new models of care must address the cost challenges. Financial problems stemming from cancer (often referred to as “financial toxicity”) are evident in up to 50% of survivors, leading them to delay or forgo medical care and prescriptions (Altice, Banegas, Tucker-Seeley, & Yabroff, 2017 ; Kent et al., 2013 ; Yabroff et al., 2016). Survivors with comorbid conditions have even greater financial problems from additional prescription medications and ambulatory visits (Guy et al., 2017). Financial toxicity compounds as insurance companies attempt to control costs through increasing the patient’s share of the costs, leading patients to pay higher deductibles and greater co-payments and co-insurance. Finding ways to deliver cancer rehabilitation care that is coordinated with oncology care limits out-of-pocket costs (through bundled co-pays with oncology care for example), or other ways to make cancer rehabilitation more feasible for patients are greatly needed.
Expanding the Team of Cancer Rehabilitation Providers
Implementing this new approach to cancer rehabilitation will involve generating referrals for both traditional and nontraditional cancer rehabilitation interventions. To optimize patient functioning and quality of life, comprehensive cancer rehabilitation must take a whole-person view of functioning, disability, and health, focusing on not just restoring function but also restoring a patient’s ability to participate fully in work, play, and other life activities (Loh & Jonsson, 2016). Thus, a prospective surveillance model for comprehensive cancer rehabilitation must incorporate assessment of multiple physical, psychosocial, and cognitive sequelae of cancer and referral for interventions that restore function and participation in activities. The World Health Organization’s International Classification of Functioning, Disability, and Health (ICF) model (World Health Organization, 2001) provides a comprehensive framework of health and functioning that can guide assessments and determine appropriate rehabilitation referrals. The ICF examines a person’s health condition in a transactional relationship with multiple components: body systems, activities and participation, and environmental and personal factors. Considering adults with cancer, impairments can be in the form of body systems (e.g., neuromuscular), activity level (e.g., ability to pick up a cup and bring it to the mouth), or participation level (e.g., ability to work or go out to dinner with friends).
Authors have proposed that the ICF be used with the prospective surveillance model as a rationale for measuring function to better understand impairments caused by cancer (Campbell et al., 2012). We propose that next-generation cancer rehabilitation consider a more comprehensive perspective for the prospective surveillance model, moving beyond just identification of neuromusculoskeletal and cognitive impairments to identifying and treating activity limitations and participation in work and leisure activity at each time point (Figure 1). Understanding whether participation in work and other life roles is affected by cancer can help distinguish patients in need of rehabilitation referrals from those with less acute impairments or symptoms and recognizes the complex orchestration of the multiple components in health and function. Overlaying the ICF within the prospective surveillance model also can be used to indicate the multiple providers necessary for a given patient and streamline coordination of care toward four goals of (1) improving function due to preexisting or cancer treatment-related impairments, (2) reducing risk of late effects (e.g., the cardiac, pulmonary, endocrine, or bone complications), and improving (3) participation in work and life activities and (4) quality of life. As shown in Figure 2, meeting these goals may involve providers including physical or occupational therapists, speech-language pathologists, physiatrists and rehabilitation nurses, audiologists, dieticians, exercise physiologists, psychologists, social workers, endocrinologists, cardiologists, and other specialists along with the oncology team. This interdisciplinary team of providers must work together to design coordinated interventions to effectively improve patient participation in life, work, and leisure. When impairments occur, mild or otherwise, it can cause a disruption in the complex orchestration of body systems out of tune. For cancer survivors, this disruption in the coordination of symptoms may appear to be just a symptom of cancer or treatment; however, if left untreated, could potentially impact quality of life. For example, cancer fatigue that limits overall endurance and strength may also limit the patient’s ability to work full time. In this case, an occupational therapist could intervene, specifically targeting participation in work, by breaking down the activities required (sitting in a chair at a desk or lifting items onto a shelf) while understanding the coordination of those activities (working on computer and engaging with others in conversation in a meeting) needed to participate in work and could rehabilitate and adapt as needed. A physical therapist may address underlying impairments in core strength causing increased fatigue at work, whereas an exercise physiologist might address the ongoing needs for aerobic exercise and be able to prescribe the best type and amount of exercise needed. An oncologist or nurse could prescribe or adjust any needed medications, and/or a psychologist can help treat the cognitive aspects of fatigue and the psychological barriers to returning to work. The choice of providers depends on the etiologic factors at multiple levels contributing to an individual patient’s fatigue.
Creating Precision Medicine Cancer Rehabilitation
Melding the prospective surveillance model and the ICF model present a framework for creating personalized cancer rehabilitation interventions rather than a “one-size-fits-all” approach. Current efforts to personalize exercise training prescription for cancer rehabilitation provide an example (Sasso et al., 2015). Unlike lifestyle recommendations for general health, therapeutic exercise prescriptions need to be tailored to the needs of an individual patient (Jones, Eves, & Scott, 2017 ; Sasso et al., 2015). Tailoring is necessary because of heterogeneity of response to exercise training (Jones, Hornsby, et al., 2014 ; Sasso et al., 2015), because of safety concerns about exercise training in patients with cancer with impaired ability to respond to repeated stress (Huang et al., 2010 ; Jones, Douglas, et al., 2014 ; Schaadt, Christensen, Kristensen, & Henriksen, 2016), and because different goals of exercise prescriptions (e.g., to treat fatigue vs. depression) might require different doses and types of intervention. To aid prescription, personalizing cancer rehabilitation interventions involves leveraging diverse types of patient and clinical data to understand how to predict and tailor the best intervention for a given problem in a given patient (Alfano et al., 2017). For example, current research is testing whether multidimensional patient data (e.g., from blood tests and clinical markers, comorbidities, omic data, behavioral data) can be aggregated to phenogroup patients to tailor their exercise prescription to optimize response to exercise and outcomes (Scott, Nilsen, Gupta, & Jones, 2018). Future research is needed to understand how to tailor dose and type of exercise and other rehabilitation interventions based on –omic and other data and depending on whether the desired outcome is restoring function (e.g., cardiorespiratory function), enhancing participation (e.g., in a specific type of work role), or preventing a late effect of treatment (e.g., bone loss).
Demonstrating the Value of Cancer Rehabilitation
The prospective surveillance model has the potential to lead to early identification of symptoms and impairments and appropriate referral and timely treatment. This should, in turn, represent better value care, that is, achieving the triple aim set forth by the Institute for Healthcare Improvement (n.d.) of better care, better health (patient functioning, quality of life, and the ability to engage in work and life roles), and lower costs (through improved healthcare utilization, relieving the burden on the primary care workforce unprepared to deal with cancer toxicities).
To demonstrate the value of cancer rehabilitation to payers and healthcare administrators, we must ask novel research questions and collect outcomes beyond patient functioning and quality of life that have not traditionally been included in rehabilitation research studies. For example, do cancer rehabilitation interventions affect the efficacy of anticancer treatments? Both preclinical and human studies have suggested that therapeutic exercise may improve tumor perfusion and drug delivery as well as engage an antitumor systemic immune response (Wiggins, Opoku-Acheampong, Baumfalk, Siemann, & Behnke, 2018), but more research is needed to confirm this hypothesis. Although cancer rehabilitation can help manage many of the chronic effects of cancer therapy, research should investigate whether cancer rehabilitation interventions may prevent late effects of cancer treatment such as bone loss and osteoporosis, sarcopenia or myopenia, chemotherapy-induced peripheral neuropathy, or cardiovascular disease; decrease frailty and fall risk; or reduce risk of recurrence or second cancers. Also, research must test whether earlier access to cancer rehabilitation care improves oncology clinic efficiency by triaging symptom management visits to rehabilitation teams facilitating the provision of more timely and completed chemotherapy visits for the growing number of patients with cancer and improving downstream healthcare utilization and healthcare costs. Finally, research needs to examine the impact of cancer rehabilitation on decreasing the financial burden of cancer for patients, caregivers, and families, as well as to society. Answers to all of these questions are needed to demonstrate the value of cancer rehabilitation to oncologists, hospital administrators, and healthcare payers; drive referrals to cancer rehabilitation providers; and make the case for better reimbursement of this care.
A Call to Action
This is a critical time for cancer rehabilitation. The switch to value-based care and the need to identify interventions that improve patient outcomes while reducing cost have increased interest in aligning cancer rehabilitation with cancer care. National efforts are focusing on educating providers and patients about the benefits of cancer rehabilitation. There is increased interest among researchers in testing the impact of cancer rehabilitation on outcomes at multiple levels (Ugolini et al., 2012). There is a pressing need to coordinate these efforts within a unified framework to position them for greatest impact.
Four synergistic efforts are needed now to embed next-generation comprehensive rehabilitation care as a standard part of cancer care. First, we need to implement a prospective surveillance model of rehabilitation into cancer care, assessing and referring patients to rehabilitation from diagnosis forward. Implementation efforts should leverage emerging technology for assessment and automated referral algorithms and use telemedicine, bundled care, or other approaches to overcome access, logistical, and cost barriers to patients accessing care. Second, comprehensive cancer rehabilitation assessments must take a whole-person view of functioning, disability, and health, and care goals must focus on improving function in activities and improving a patient’s ability to participate fully in work, leisure, and other life roles. This whole-person view focused on participation in roles will help distinguish patients with problematic impairments from those who do not require referrals and will also point to an expanded team of interdisciplinary cancer rehabilitation providers who may be needed to effectively improve participation in work and life. Third, the dose and type of cancer rehabilitation interventions need to be tailored based on –omic and other clinical, physiological, psychosocial, and patient-generated data and depending on whether the desired outcome is restoring function (e.g., cardiorespiratory function), enhancing participation (e.g., in a specific type of work role), and/or preventing a late effect of treatment (e.g., bone loss). Bringing a more precision medicine lens to cancer rehabilitation will involve leveraging and integrating these diverse types of data as they become available. Finally, we look to the research community to conduct different types of studies with novel outcomes, including cancer treatment efficacy and completion, prevention of late effects of treatment, patient participation in work, and downstream healthcare utilization and costs that can demonstrate the value of cancer rehabilitation to clinicians and healthcare payers. Showing return on investment from referrals to cancer rehabilitation should improve both referral rates and reimbursement challenges. Simultaneous pursuit of these four areas has the potential to improve patient outcomes and ease the burden on the healthcare system and improve the lives of the growing population of cancer survivors.
Key Practice Points
- Embedding interdisciplinary comprehensive rehabilitation care as a standard part of cancer care from diagnosis forward has the potential to improve patient outcomes and ease the burden on the healthcare system.
- To optimize patient functioning and quality of life, comprehensive cancer rehabilitation assessments must take a whole-person view of functioning, disability, and health and care goals must focus on improving function in activities and improving a patient’s ability to participate fully in work, leisure, and other life activities.
- Rehabilitative interventions should be tailored depending on whether the desired outcome is restoring function (e.g., cardiorespiratory function), enhancing participation (e.g., in a specific type of work role), or preventing a late effect of treatment (e.g., bone loss).
- Research must test the effects of cancer rehabilitation interventions on novel outcomes that will drive referrals and reimbursement for these services, including cancer treatment efficacy and completion, prevention of late effects of treatment, patient participation in work, and downstream healthcare utilization and costs.
Conflict of Interest
The authors declare no conflict of interest.
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