Cancer Prehabilitation & Its Role In Improving Health Outcomes and Reducing Health Care Costs

Seminars in Oncology Nursing, Vol 31, No 1 (February), 2015: pp 13-30

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CANCER PREHABILITATION AND ITS ROLE IN IMPROVING HEALTH OUTCOMES AND REDUCING HEALTH CARE COSTS JULIE K. SILVER OBJECTIVES: To examine the current state of cancer prehabilitation care and the impact that it may have on health-related and financial outcomes.

DATA SOURCES: Clinical trials, reviews and meta-analyses.

CONCLUSION: Research demonstrates that prehabilitation interventions may improve physical and/or psychological outcomes and help patients function at a higher level throughout their cancer treatment. Establishing a baseline status at diagnosis provides an opportunity to gain insight into the burden that cancer and its treatment can place on survivors with respect to physical and psychological impairments, function, and disability. Targeted interventions may reduce the incidence and/or severity of future impairments that often lead to reduced surgical complications, hospital lengths of stay, hospital readmissions, and overall health care costs. Thus, cancer prehabilitation is an opportunity to positively impact patient healthrelated and financial outcomes from diagnosis onward and, by decreasing the financial impact that cancer can have on individuals, may prove to be a sound investment for patients, hospitals, payers and society.

IMPLICATIONS FOR NURSING PRACTICE: Nurses, and particularly navigators, have an opportunity to significantly impact care through patient screening, prehabilitation assessments, documentation of baseline patient status and, in some cases, especially when impairments are not present at baseline,

Julie K. Silver, MD: Associate Professor, Department of Physical Medicine and Rehabilitation, Harvard Medical School, Boston, MA; Attending Physician, Spaulding Rehabilitation Hospital Network, Boston, MA; Clinical Associate, Massachusetts General Hospital, Boston, MA; and, Associate in Physiatry, Brigham and Women’s Hospital, Boston, MA.

Financial Disclosures: Cofounder of Oncology Rehab Partners, LLC, which developed the STAR Program.

Address correspondence to Julie K. Silver, MD, Massachusetts General Hospital, Boston, MA. e-mail: julie_silver@hms.harvard.edu Ă“ 2015 Elsevier Inc. All rights reserved.

0749-2081/3101-$36.00/0. http://dx.doi.org/10.1016/j.soncn.2014.11.003

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provide interventions designed to improve physical and psychological health before the start of upcoming oncology treatments and reduce the likelihood of patients developing future impairments.

KEY WORDS: Prehabilitation, preoperative exercise, presurgical exercise, cancer survivorship, cancer rehabilitation

A

LTHOUGH prehabilitation is not a new concept in medicine, it has recently gained noteworthy acceptance in the field of oncology care. An early description of prehabilitation appeared in the British Medical Journal in 1946 and focused on the need to get men ready for military duty–not unlike modern day boot camp.1 Mainstays of this military preparation included prescribed exercise to improve strength and endurance, improved nutritional intake, and general education. Not surprisingly, the preparation regimen appeared to help performance. Over time, health care professionals began to recognize opportunities to better prepare patients for upcoming medical stressors and research appropriate interventions. Much of the prehabilitation research focused on improving outcomes by preparing patients for upcoming elective cardiac2,3 and orthopedic surgeries4-8 and cancer-related operations.9 In particular, orthopedic-related prehabilitation research led to the development and offering of workshops (often referred to as joint camp or joint class) that patients (and family members) attend before total hip or knee replacement arthroplasty (surgery). In a recent meta-analysis

by Santa Mina et al,10 researchers reviewed twenty-one studies and found that preoperative exercise interventions did indeed provide postoperative physical health benefits and, moreover, may reduce hospital lengths of stay. Additional research suggests that physically preparing patients for upcoming surgery may also have a psychological benefit.11 Furthermore, emerging research has demonstrated that prehabilitation may improve cancer-related outcomes and thereby reduce cancer-related health care costs.12

WHAT IS CANCER PREHABILITATION? To understand cancer prehabilitation, it is necessary to define rehabilitation. Although there are many definitions in the literature, The National Association of Insurance Commissioners

and the Center for Insurance Policy and Research define rehabilitation as ‘‘health care services that help a person keep, get back or improve skills and functioning for daily living that have been lost or impaired because a person was sick, hurt or disabled.’’13 Cancer rehabilitation is generally focused on treating impairments with interventions that are designed to decrease pain and disability once someone has developed a significant physical problem due to a cancer-related illness or injury.

Cancer prehabilitation is part of the cancer rehabilitation care continuum and is defined as: ‘‘[A] process on the cancer continuum of care that occurs between the time of cancer diagnosis and the beginning of acute treatment and includes physical and psychological assessments that establish a baseline functional level, identify impairments, and provide interventions that promote physical and psychological health to reduce the incidence and/or severity of future impairments.’’14 Cancer prehabilitation is really the first part of the cancer rehabilitation care continuum and, by definition, occurs between the time of diagnosis and the start of acute oncology treatment (Fig. 1). Therefore, prehabilitation is time-based and involves only those assessments and interventions that are delivered before the start of acute cancer treatment. It must be noted, however, that interventions used during prehabilitation are not limited in use to the time before cancer treatments begin, and use of these interventions may continue throughout survivorship. For example, a newly diagnosed breast cancer survivor may be taught specific exercises to strengthen and improve mobility in the affected shoulder before receiving cancer treatments that are associated with shoulder impairments. It may then be recommended that the patient continue with these exercises even after her mastectomy and throughout her treatment to recover her presurgical strength and mobility.

CANCER PREHABILITATION

Cancer Diagnosis

Cancer Treatment

Prehabilitation Assessments and Interventions

Rehabilitation Assessments and Interventions

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FIGURE 1. Timing of prehabilitation in the cancer care continuum.

Reproduced from the STAR Program and used with permission from McKesson Corporation and/ or one of its subsidiaries. Copyright Ó 2014. All Rights Reserved.

Survivorship Care Continuum

Improving the health of cancer patients is not a new concept. In 1980, Dietz described preventive rehabilitation as a strategy to decrease surgical morbidity in patients ‘‘.when such training can be expected to eliminate inadequate performance or reduce subsequent disability or handicap..15 Their recommendations were multimodal and included counseling and teaching patients specific strategies to lessen anxiety and fear as well as physical interventions to improve respiratory function. Later, Courneya and Friedenreich16 described the Physical Exercise Across the Cancer Experience (PEACE) Framework and recommended buffering exercise therapy before cancer treatment.

REDEFINING RECOVERY The focus on finding a cure for cancer and measuring the growth in numbers of disease-free years has often dominated the reporting of outcomes and the dialogue about what it means to recover from cancer. As these outcomes have continued to improve, increasingly oncology clinicians are turning their efforts to not only treating the malignancy but also the sequelae from the treatments themselves. In a review in the Annals of Surgery that focused on prehabilitation for colorectal cancer patients, Cheema et al stated: ‘‘Research is needed to address the development and application of interventions that will prevent or reduce adverse outcomes of cancer and its treatment. Clinically important endpoints of this work should include patient-centered outcomes such as longterm physical, psychological, and social functioning in patients receiving surgical and medical cancer therapies. Postoperative interventions such as acute rehabilitation would be the obvious strategies that come to mind. However, the preoperative window

for both assessment and intervention is an underexplored area that may be critical for identifying at-risk patients and developing effective interventions that can impact long-term, postsurgical outcomes. Mobility impairments and disabilities with ADL [activities of daily living] are highly dynamic constructs and patients can develop and recover from disability states with great frequency.’’17 Indeed, measuring both objective and clinically relevant outcomes as well as patient-reported outcomes is important, because patients are developing their own definitions of recovery that often equate to the absence of symptoms and a return to their prediagnosis functional status. In the aforementioned review, Cheema et al described how patients often shift from worrying about their mortality to being concerned with their ability to function. They explained: ‘‘Colorectal cancer surgical patients are older and have more complex comorbid conditions. Fortunately, more of these patients are receiving curative surgical resection with improving 5-year survival rates despite their clinical complexity. The focus of preoperative assessment thus needs to switch from short-term mortality and morbidity to both short and long-term patient-centered outcomes such as quality of life, functional independence and community reintegration.

Patients now expect more from their physicians and the health services they receive.

Once they look beyond the horizon of cancer mortality, patients (often unrealistically) expect to return to normal daily activities without any functional dependency or limitations. ‘You’ve cured me doctor, why haven’t I gotten back to normal’ is often the refrain.’’17

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As a result, these researchers advocated for new prehabilitation assessment and intervention approaches that will address the gap between survivors’ expectations for their recovery and their actual (and often disappointing) functional outcomes.

DOCUMENTING ASSESSMENTS, PROVIDING SPECIFIC INTERVENTIONS AND DEMONSTRATING OUTCOMES

High

Although prehabilitation by definition is timebased and includes only those assessments and interventions that are initiated before the start of acute cancer treatment, this does not mean that everything done during this time period qualifies as prehabilitation (Fig. 2). For example, patient education, particularly before surgery, chemotherapy or radiation therapy, while fairly standard care, would not typically be considered prehabilitation. Therefore, it is important to not only consider the timing of services but also whether there has been a delivery of services that can produce measureable health care outcomes. Perhaps one way to determine whether health care services qualify as prehabilitation (versus more traditional patient education) is to ask this question: Do the assessments result in quantitative data?

To illustrate the difference between traditional patient education and prehabilitation, consider the case of a woman recently diagnosed with breast cancer. Under usual care, this patient might receive a handout describing some upper extremity exercises that may promote maintenance or recovery of strength and mobility. While distribution of this handout might qualify as delivery of health care services, it would generally not be considered prehabilitation unless baseline assessments of upper extremity strength and mobility were performed and progress tracked to determine the efficacy of the intervention.

In contrast to traditional patient education, prehabilitation of a newly diagnosed breast cancer patient would include a physical assessment that might consist of an upper extremity evaluation consisting of measurement of shoulder range of motion with a goniometer and manual muscle testing for strength using the standard 0–5 scale.

Validated tools such as the 30-question DASH (Disabilities of the Arm, Shoulder and Hand) or 11-question QuickDASH Outcome Measure could also be used.18 The patient would be given an educational handout along with verbal instruction in appropriate exercise techniques and instructed to document her compliance with the prescribed exercises. So while this patient may receive the same educational handout as the usual care patient, this patient’s record now includes a series

Usual Care + Prehabilitation Assessments & Interventions

Quality of Cancer Care

Baseline established with physical & psychosocial assessments Usual Care + Education No baseline established

Usual Care

Low

No baseline established

Specific interventions to improve physical & psychological health prior to acute cancer treatment are variable with poor control and no baseline to compare results

Specific interventions employed to improve physical & psychological health above baseline prior to acute cancer treatment Ongoing assessments measured against baseline and new or progressive impairments identified and treated early

No specific interventions to improve physical & psychological health prior to acute cancer treatment Low

Ability to Assess & Potentially Improve Physical & Psychological Outcomes

High

FIGURE 2. Cancer prehabilitation versus usual care and education.

Reproduced from the STAR Program and used with permission from McKesson Corporation and/ or one of its subsidiaries. Copyright Ó 2014. All Rights Reserved.

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of assessments that result in numbers that can clearly and graphically demonstrate baseline and ongoing status. In this case, the answer to the question about whether the assessment results in quantitative data is yes, and therefore it is likely that the care provided would fall into the prehabilitation category. Clinicians must note that while a yes response to whether the outcomes qualify as quantitative data may suggest that the intervention(s) could be considered prehabilitation, that answer does not ensure that the interventions are evidence-based or best practices care.

Although prehabilitation interventions have not been well studied in the breast cancer population, it is well recognized that survivors exhibit many upper extremity problems that may affect their ability to function. Traditionally, research has focused on treating lymphedema in an upper extremity once it has developed. However, new studies are demonstrating that significant disability and quality-of-life issues may be attributed to other upper extremity problems that cause pain, weakness, and loss of range of motion.19 In fact, one study by Martins da Silva and Rezende20 assessed the impact of late postoperative physical functional disabilities on quality of life in breast cancer survivors. In this study, 82 women in the postoperative period after conservative surgery were evaluated. All patients were treated with axillary lymph node dissection and the mean time since surgery was approximately 6 years. Quality of life was assessed via the FACT-B, functional capacity was evaluated using the QuickDASH Outcome Measure, and a physical therapy evaluation was used to measure arm range of motion and extremity volume. Within this population, the researchers found significant limitations in shoulder range of motion, particularly in flexion, abduction, and external rotation, and that these limitations had a negative impact on function and quality of life. Interestingly and although approximately 28% of the participants had lymphedema, it did not affect functional capacity or quality of life.

This is an important study to consider because physical limitations in shoulder range of motion were linked to a negative impact on functional capacity and quality of life. Moreover, a Cochrane Database Systematic Review supported use of early postoperative exercise interventions to prevent and/or reduce upper limb dysfunction.21 Therefore, it seems reasonable to conclude that evaluating this population, establishing a baseline for comparison of upper extremity strength and

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mobility at diagnosis, identifying potential postoperative shoulder problems during the prehabilitation period, providing appropriate prehabilitation interventions, and ordering early referral to physiatry, physical therapy, or occupational therapy may help improve outcomes and prevent more serious disability later. Furthermore, even newly diagnosed patients with breast cancer who are screened and found to have normal range of motion may benefit from specific prehabilitation exercises aimed at maintaining strength and range of motion to help prevent postsurgical problems in the future. Importantly, prehabilitation also exposes the newly diagnosed breast cancer survivor to specific shoulder exercises that she may continue to use after a mastectomy and throughout her treatment, potentially increasing familiarity and compliance throughout survivorship. In fact, research has indicated that introducing prehabilitation exercises may facilitate later adherence to exercise.11 When assessments are conducted, it is vital that any specialist who is part of a prehabilitation program or protocol identify patients who need or might benefit from referral to the next level of care (Fig. 3). For example, a patient with a physical impairment should be referred to a rehabilitation clinician for treatment. A patient who may have normal function but is scheduled for surgery or other oncology therapies that may be associated with future impairments should be referred for prehabilitation. Similarly, a patient in a prehabilitation setting who is highly distressed should be referred to a mental health professional. As this care evolves, it is critical to recognize that while prehabilitation is designed to improve outcomes, it is also an opportunity to perform baseline assessments and refer patients appropriately to other health care professionals right from the start.

IMPROVING SURVIVOR HEALTH OUTCOMES AND REDUCING HEALTH CARE COSTS In a study using the 2008–2010 Medical Expenditure Panel Survey, Guy et al22 compared a series of personal, physical and financial characteristics of 4,960 adult cancer survivors with those of 64,431 individuals without a history of cancer. They found that, among recently diagnosed survivors, the annual excess economic burden of cancer survivorship was $16,213 per person aged 18 to 64 years and $16,441 per

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FIGURE 3. Cancer prehabilitation algorithm. Reproduced from the STAR Program and used with permission from McKesson Corporation and/or one of its subsidiaries. Copyright Ó 2014. All Rights Reserved.

New Cancer Diagnosis

Prehabilitation Assessments

Physical Impairments

Referral to Rehabilitation Services

No Physical or Psychological Impairments

Psychological Impairments

Prehabilitation Interventions

Referral to Mental Health Services

Acute Cancer Treatments

person aged 65 years and older. Among previously diagnosed cancer survivors, the annual economic burden of survivorship was lower, but still significant at $4,427 and $4,519 per person, respectively. Using this data, the researchers estimated that the plausible range of national cancer-related direct annual medical costs to be $25.2 to 41.7 billion for those under the age of 65 and $37.3 to 48.1 billion for those aged 65 years and older. The largest burden of aggregate direct costs came from ambulatory care, followed by inpatient care, prescription medications, and other services. Similarly, Guy et al estimated the plausible range of national cancer-related indirect annual medical costs to be $9.6 to 16 billion for those under the age of 65 and $8.2 to 10.6 billion for those aged 65 years and older.22 Lost productivity across both age groups was primarily because of employment disability; followed by missed worked days and lost household productivity. Notably, the authors stated that they likely underestimated the total burden of cancer survivorship because they did not include additional costs associated with issues such as caregivers’ productivity losses, intangible pain and suffering, presenteeism, and patient transportation. A subsequent report compiled by the Centers for Disease Control noted that half of the estimated 13.4 million cancer survivors in the United States are of working age and summarized the public health implications in this manner.23 ‘‘As the population of cancer survivors increases, the economic impact of cancer for

patients, families, employers, the healthcare system, and society overall is expected to grow. Given the increased health-care needs and medical costs of cancer survivors, continued access to health care and ways to reduce disruptions in work and daily activities are important when survivors complete their cancer treatment. Such efforts could reduce the economic burden caused by cancer and could help maximize employment opportunities and productivity among cancer survivors.’’23 Cancer is a complex disease that often requires complex and physically and psychologically demanding treatments. As health care professionals look toward reducing the economic burden that cancer places upon individuals and society, we must consider those issues that significantly impact the cost of cancer care. In a recent review of unexpected readmissions in the United States after major cancer surgery, Rochefort and Tomlinson24 noted that readmission rates following oncology operations are between 16% and 25% at 30 days and 53% and 66% at 1 year. They go on to note that although hospital readmissions are extremely costly to institutions and payers, the patients are the ones that suffer the most. In fact, studies have demonstrated that patients who are readmitted tend to have worse survival outcomes than those who are not rehospitalized.25,26 Similarly, a Canadian Institute for Health Information report on all-cause readmission to inpatient acute care identified oncology patients as having higher than average readmission rates.27 The authors reported that overall

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approximately 8.5% of acute care patients were readmitted to hospitals within 30 days of discharge and, of the patients admitted, the highest readmission volumes were attributed to cancer. In 2010–2011, during an 11-month study period, a total of 211,670 patients were hospitalized with a cancer diagnosis. Approximately half of the adult oncology patients were hospitalized for medical care and the other half for surgical procedures. The percent of unplanned readmission to acute inpatient care within 30 days was 14.6%.

Lung, colorectal, and lymphoma cancers were listed within the top five diagnoses associated with both medical and surgical readmission, and for surgical readmission, the most commonly listed reason for readmission was surgical complication or gastrointestinal obstruction. Despite the many challenges associated with collecting accurate readmission data, the consensus is that many hospital readmissions are preventable.24,28 Previously mentioned success in preparing cardiac and orthopedic patient populations for surgical interventions suggests that prehabilitation in the oncology patient population may help better prepare patients for upcoming cancer treatments, whether medical or surgical. Improved patient health outcomes could concomitantly lead to reductions in surgical complication and hospital readmission rates, thereby reducing health care costs. However, implementation of new models of oncology care requires evaluation of not only individual patient outcomes but also the outcomes associated with patient populations as well as the direct and indirect costs of the health care provided.2 To further explore the potential for improved health and financial outcomes following implementation of prehabilitation, consider the lung cancer population. Lung cancer is responsible for more cancer-related deaths worldwide than any other malignancy.29 This patient population’s particular vulnerability is founded upon a host of common baseline comorbidities. Problems with deconditioning and poor cardiorespiratory status are very common even in newly diagnosed lung cancer survivors. Additional complicating factors can include nicotine and/or other addiction issues, mental health conditions including anxiety and/or depression, insomnia, sleep apnea, mobility problems that may include a history of falls, osteopenia and/or osteoporosis, as well as others.

Particularly (though not exclusively) in the case of newly diagnosed patients with early stage and

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localized non–small cell lung cancer, surgical resection with curative intent is the most effective treatment. Remarkably, although less than 15% of these patients have localized disease at the time of initial presentation, more than half of them (54%) have a >5-year survival rate.29 Therefore, the utilization of both preoperative and postoperative physical therapy with the goal of reducing morbidity and providing functional benefits in patients with lung cancer has received considerable study.9,30 To better understand the potential for prehabilitation to improve health and financial outcomes, it is helpful first to consider the reasons why oncology patients have either extended hospital lengths of stay or readmissions. For surgical patients, risk factors for extended stay or readmission generally fall into four groups: 1. Preoperative risk factors (eg, age, cancer diagnosis and disease extent, comorbidities, functional status) 2. Perioperative risk factors (eg, type of surgery, length of the operation, length of hospital stay, complications) 3. Discharge disposition status (home alone, home with supportive caregivers and/or home health services, inpatient rehabilitation facility, subacute nursing facility) 4. Reasons for readmission (postoperative infection or other complication, pneumonia, dehydration, bowel obstruction, bleeding) These risk factors for extended stay or readmission include both nonmodifiable (eg, age or diagnosis) and modifiable (eg, weight or infection rate) components. In general, the focus of medical intervention has been on reducing the number or severity of modifiable risk factors, whether they are facility-related or patient-related. For example, the patient’s risk for infection could be affected by the cleanliness of the surgical equipment (facility-related) or by nutritional status, mobility/functional status, weight and nicotine addiction (patient-related).

Although it may make sense initially to focus primarily on modifiable risk factors, risk assessment should take into account nonmodifiable risk factors such as age. For example, a patient who is 75 years old may be at higher risk for mobility issues and falls than a patient who is 35 years old. A history of falls may affect surgical outcomes,31 which may in turn result in a significant impact on health care costs, particularly in the

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elderly.32,33 Risk assessments that address both modifiable and nonmodifiable factors may help clinicians triage patients more appropriately for prehabilitation and early postoperative rehabilitation interventions.

Several studies have suggested that a critical risk factor for hospital readmission is the preoperative condition of the patient.34,35 Specifically, recent studies have focused on patient frailty as a surgical risk factor.36 In a prospective study by Ponzetti et al,37 350 consecutive patients were followed for 4 months after discharge. Frailty was assessed using a multidimensional tool and the occurrence of chemotherapy interruption, urgent hospital readmission or death was recorded. These researchers found that approximately 40% of the patients were classified as frail, and reduced functional performance status was a strong predictor of short-term hospital readmission or death. Findings of this study are consistent with other studies demonstrating that morbidity and functional disability are the most common risk factors for hospital readmission in elderly patients.38 Research has demonstrated that prehabilitation interventions may be beneficial in the subset of patients with lung cancer that are operative candidates.12 For example, in a prospective single-group study that included 83 patients with COPD and non–small cell lung cancer, prehabilitation that occurred 2 to 4 weeks before resection improved the majority of spirometry parameters, 6-minute walk test scores and dyspnea symptoms.39 Importantly, the beneficial effects were most emphasized in the study participants who initially had the worst pulmonary function and functional capacity. Furthermore, in a recent systematic review

by Rodriguez-Larrad et al,40 researchers evaluated eight studies assessing preoperative and postoperative physical therapy interventions in patients with lung cancer. Overall, this review included 599 patients, two studies of preoperative only interventions, four studies of preoperative and postoperative interventions, and two studies of postoperative only interventions. The authors noted that the most important finding was that presurgical interventions (prehabilitation) ‘‘improve functional capacity and reduce postoperative morbidity, whereas interventions performed only during the postoperative period do not seem to reduce postoperative pulmonary complications or length of hospital stay.’’40 This body of research has led to the recommendation by several prominent organizations, including the

American College of Chest Physicians, European Society of Thoracic Surgeons and the European Respiratory Society, that both preoperative and postoperative physical therapy interventions be included in the treatment plan for patients with lung cancer who will be undergoing surgical excision.41,42 Although preoperative exercise has been studied more than other prehabilitation interventions, researchers are looking toward multimodal approaches to prehabilitation that may improve physical health (surgical) and financial outcomes more than unimodal interventions. For example, combining targeted preoperative exercise interventions with smoking cessation may prove to be more effective at improving outcomes than utilizing either of these alone. Nicotine addiction has a documented association with numerous surgical complications including impaired healing, increased infection, delayed and/or impaired fracture union, and inferior joint replacement outcomes.43 Moreover, infections are a leading cause of major surgical complications and often lead to increased health care costs, hospital lengths of stay, and 30-day readmissions.44 Thus, strategies such as smoking cessation that can reduce the rate of surgical wound infection and the incidence of respiratory infections such as pneumonia may play an important role, especially when used with preoperative exercise, in reducing health care costs.

Indeed, several recent studies have confirmed that smoking negatively impacts surgical outcomes. In a review of Veterans Administration data from over 20,000 patients who underwent cancer surgery during 2002 to 2008, Gajdos et al45 found that smoking status statistically and significantly negatively affected all postoperative outcomes. In this study, not only did active smoking increase the likelihood of perioperative complications, it also led to the delay or omission of adjuvant chemotherapy or radiation therapy that was deemed necessary for optimal treatment.

Moreover, smoking has been shown to be a known risk factor for complications in breast cancer surgery, particularly procedures associated with reconstruction,46 and may be a factor in hospital readmission.47 In other recent reviews, researchers found that nicotine addiction increased neurosurgical complications as well and recommended preoperative smoking cessation to mitigate perioperative morbidity,48 and that smoking cessation in those with lung cancer results in

CANCER PREHABILITATION

both immediate and long-term improvements.49 Finally, a Cochrane Database Review found that not only did smoking cessation before surgery reduce postoperative morbidity, but that preoperative nicotine addiction interventions did significantly increase smoking cessation at the time of surgery.50 Given the significant deleterious effect that active nicotine addiction has on surgical outcomes, particularly infections but also delayed wound healing and other musculoskeletal issues, prehabilitation protocols and pathways should routinely include smoking cessation.

A discussion of prehabilitation-related improvements in health and financial outcomes would be remiss without considering the effects that distress, anxiety, and other mental health issues may have in cancer patients. Rochefort and Tomlinson’s review of unexpected readmissions following cancer surgery begins with this sentence, ‘‘A major oncologic operation carries a significant level of stress on the physical and mental well-being of a patient.’’24 A subsequent study by Li et al51 demonstrated that mental health service utilization and expenditures were higher in people diagnosed with cancer than in those without a history of cancer. Indeed, one would fully anticipate that a cancer diagnosis combined with an upcoming surgery would be both physically and emotionally challenging. Moreover, one could hypothesize, based upon the current state of research in wound healing, that prehabilitation interventions designed to decrease preoperative psychological stress and anxiety (eg, guided imagery, meditation, progressive muscle relaxation) might positively impact surgical wound healing.52 So, while certainly, strategies to reduce preoperative stress and anxiety would fall under the category of best practices patient-centered care and prehabilitation, these same strategies might also reduce hospital readmission; addressing the potential for the very anxious patient to request readmission prematurely.53 In addition to providing specific strategies aimed at decreasing stress and anxiety, participation in prehabilitation itself might be both empowering and reassuring to patients. Patients often lack knowledge about how quickly and how well they will recover from surgery or other cancer therapies. They may perceive relatively simple setbacks or minor complications as more serious than trained health care professionals would consider them. Further complicating often unrealistic expectations for healing and function shortly

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after surgery, is a decrease in access to the health care team once the patient is discharged. In a systematic review evaluating interventions to reduce 30-day rehospitalizations, Hansen et al54 described how patients may experience a critical ‘‘voltage drop’’ in the course of a discharge pathway as they are subject to a change in the availability of care and knowledge base between the hospital inpatient setting and ambulatory follow-up. Prehabilitation provides an opportunity to pre-emptively counsel patients about the recovery process, set realistic expectations and explain the postdischarge follow-up plan, one that may even include early rehabilitation. Furthermore, the case for multimodal prehabilitation interventions can be taken one step further by linking preoperative exercise and smoking cessation with mental health interventions, all working in concert to better prepare the patient for upcoming cancer treatments. Providing patients with quantified assessments, education, and specific strategies that facilitate going into surgery physically and emotionally stronger, is likely to reassure both patients and their loved ones and positively impact health and financial outcomes.

CANCER PREHABILITATION IS EVOLVING Many of the early studies of prehabilitation in cancer patients that evaluated the use of general exercise–often defined as exercise during the preoperative or perioperative period–demonstrated improved physical activity, fatigue, and qualityof-life outcomes in limited patient populations.55 Over time, this body of literature has evolved, including more varied patient populations, diagnoses, interventions, and outcomes. For example, in a recent systematic review of preoperative exercise intervention studies conducted by Singh et al,9 the authors included 18 studies representing a total of 966 participants. Even with this more varied patient sampling, the majority of the studies in this review demonstrated significant improvements in physical and/or functional capacity such that the authors concluded that surgical oncologists should consider preoperative exercise interventions as a potential adjuvant therapy to improve patient outcomes. A fascinating study

by Gillis et al56 recently evaluated the impact of preoperative interventions only (n ¼ 38) versus postoperative interventions only (n ¼ 39) in a parallel-arm single-blind superiority randomized

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controlled trial in patients undergoing colorectal cancer surgery. While this study demonstrates how prehabilitation research is moving from simple case studies to well-controlled studies of larger patient populations, importantly, the authors found that the prehabilitation group did indeed exhibit better recovery outcomes than the rehabilitation only group. This randomized control study, if reproduced over time by other researchers and in other cancer populations, would pivotally change the delivery of oncology care as it would mean that it may be easier (and presumably quicker and less costly) to prevent physical impairments than to treat them once they have developed. Intuitively, this makes sense, but it represents a significant change from the current state of oncology care delivery. Clearly, more studies are needed to address whether outcomes following prehabilitation will truly prove to be superior to those resulting from postoperative and other posttreatment rehabilitation only.

Despite these advances, this review also clearly demonstrates that the prehabilitation literature does not match the rehabilitation literature in scope. For example, while breast cancer rehabilitation has been extensively studied, there are very few examples of prehabilitation research in this population. In fact, the extensive review by Singh et al did not include a single breast cancer study.9 Of the 18 studies reviewed, the majority were focused on lung cancer followed by prostate cancer and colorectal cancer. Clearly, more research into the efficacy of prehabilitation in varied cancer populations is warranted.

Although general exercise has been the focus of numerous prehabilitation studies, it is important to recognize that there are other factors that may significantly improve a survivor’s ability to withstand or recover from upcoming cancer treatments. More recently, research has been focusing on targeted exercise interventions such as swallowing exercises for newly diagnosed head and neck cancer survivors57-60 that would improve postoperative swallowing function or pelvic floor exercises that would improve preoperative and postoperative urinary continence in men who have just been diagnosed with prostate cancer.61,62 Furthermore, the important role that proper preoperative and perioperative nutrition can play in improving postoperative recovery is actively being studied.63,64 Thus, while general exercises may improve overall health and well-being, targeted exercises and interventions may improve

specific outcomes better than usual care and general exercise.

As noted earlier, researchers are also evaluating the efficacy of not only single interventions, such as preoperative exercise, but also combinations of interventions such as preoperative exercise plus smoking cessation and, further, what combinations of interventions might work best when used together in the limited time before cancer treatments begin (multimodal versus unimodal approaches). For example, a multimodal prehabilitation protocol for a head and neck cancer survivor might combine targeted swallowing exercises, general conditioning, smoking cessation, nutritional recommendations (eg, protein supplementation before surgery) and psychological strategies for stress and anxiety that are designed to work in combination to better prepare patients for upcoming cancer treatments.12 Moreover, prehabilitation assessments and interventions may be part of a protocol that can be conducted as a single consultative one-to-one visit with a newly diagnosed patient, as several consultations linked together as part of a multidisciplinary clinic, or as a group workshop that can operate with or without integral individual sessions. As shown in Table 1, the interconnected, yet flexible, nature of this type of multimodal approach to prehabilitation care is well-suited for application within varied yet targeted populations.

One of the most intriguing questions yet to be fully considered in the prehabilitation research is whether these types of interventions can influence the options for oncology treatment. That is to say, can prehabilitation make surgery a viable option for a newly diagnosed patient with lung cancer who is initially deemed to be too high of a risk for surgical resection? The significant risks associated with this type of major surgical procedure (ie, thoracotomy) combined with a population profile that typically reflects pre-existing health conditions that increase surgical morbidity and even mortality, often make surgical treatment a nonviable option. However, this is a population in which prehabilitation interventions should be strongly considered, because the research to date suggests that preoperative interventions may significantly improve physical outcomes, decrease surgical risk factors, and reduce hospital lengths of stay.9,12,40 Although this question of whether prehabilitation can sufficiently reduce the surgical risk in some patients such that they are qualified to safely undergo resection of their cancer needs further

CANCER PREHABILITATION

TABLE 1.

Examples of Multimodal Prehabilitation Interventions in Cancer Patients Lung cancer Breathing exercises Balance exercises Total body strengthening and cardiovascular exercises Psychosocial support with specific stress reduction strategies Nutrition Smoking cessation Head and neck cancer Swallowing exercises Balance exercises Cervical range of motion exercises Total body strengthening and cardiovascular exercises Psychosocial support with specific stress reduction strategies Nutrition Smoking cessation Prostate cancer Pelvic floor exercises Balance exercises Total body strengthening and cardiovascular exercises Psychosocial support with specific stress reduction strategies Nutrition Smoking cessation Breast cancer Shoulder and cervical range of motion exercises Upper body strengthening exercises Balance exercises Total body strengthening and cardiovascular exercises Psychosocial support with specific stress reduction strategies Nutrition Smoking cessation

study, there is early evidence that it may. For example, an Italian study evaluated prehabilitation in patients with lung cancer with comorbid lung disease.65 In this study, the researchers assessed patients who were not candidates for lobectomy due to markedly impaired pulmonary function. The prehabilitation intervention consisted of supervised aerobic exercise, breathing exercise, and smoking cessation education. The time commitment for these patients was 3 hours daily, 5 days a week, for 4 weeks. Upon completion of the prehabilitation protocol, these patients achieved the pulmonary function status presumed necessary to tolerate surgery. All eight patients survived the lobectomy operations. This early study suggests that in some high-risk patients with lung cancer, prehabilitation may be able to favorably improve treatment options. In this sce-

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nario, without surgery, the result would be certain mortality. Theoretically, if prehabilitation is able to offer some patients who are not deemed to be surgical candidates safe passage through an operation, these interventions may improve not only morbidity but also mortality. So although prehabilitation has been studied for many years in the lung cancer surgical population, more research is needed before it can be confirmed that prehabilitation can indeed open treatment options for those previously limited by their physical condition and comorbidities.

Another intriguing question yet to be fully considered in research and the literature is whether prehabilitation might help facilitate improvements in physical and functional status such that after cancer treatment, patients are in better health than they were at diagnosis (Fig. 4). A recent case study reported on the treatment and outcomes of a 75-year-old woman diagnosed with stage IA lung cancer concurrent with significant respiratory comorbidities as well as osteoarthritis and chronic knee and back pain.66 Her initial symptoms included dyspnea at rest and with exertion, limited functional mobility, and severe deconditioning. Three weeks after her initial diagnosis, the patient underwent bronchoscopy for staging. Unfortunately, the treating thoracic surgeon subsequently decided that her baseline health status ranked her as too high risk for an operation. He referred the patient for prehabilitation that included physical therapy and she started therapy within that week. Following 6 weeks of physical therapy, the patient was deemed a surgical candidate and was able to undergo resection of her cancer. Postoperatively, she received 6 additional weeks of physical therapy that was followed by transition to a communitybased exercise program. In this case, prehabilitation: 1) improved the patient’s health such that she became a surgical candidate; 2) decreased the patient’s surgical risk; 3) decreased the patient’s hospital length of stay; and 4) when combined with rehabilitation after surgery, resulted in better overall health and functional status than at diagnosis.

Future research may also focus on inclusion of prehabilitation in the surgical enhanced recovery programs or pathways (ERPs) that have been shown to be effective in reducing hospital lengths of stay and overall complication rates across surgical specialties.67 A recent systematic review evaluating the economic impact of ERPs in

J.K. SILVER

FIGURE 4. Prehabilitation may improve health above baseline status. Reproduced from the STAR Program and used with permission from McKesson Corporation and/ or one of its subsidiaries. Copyright Ó 2014. All Rights Reserved.

Health / Function

Excellent

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P

H RE

AB

RE

HA

B

REHAB

BASELINE

NO PREHAB

NO REH REHA

AB

B

Poor

NO RE HA B

Diagnosis

Before Treatment

Acute Treatment

colorectal cancer surgery, found them to likely be cost-effective.68 Moreover, including prehabilitation in oncology clinical pathways may improve patient outcomes, lengths of stay, and hospital costs.69 Going forward, it will be important that researchers evaluating prehabilitation as a component of ERPs include patient-reported outcomes, particularly postdischarge functional status, as this has been identified as a deficit in the current literature.70 Indeed, having survivors report on their functional status and recovery from surgery and other oncology interventions is a crucial component of patient-centered care.

BARRIERS TO OPTIMIZING OUTCOMES: COST, TIMING, PATIENT SAFETY AND CORE COMPETENCIES There is no doubt that numerous models of prehabilitation care for cancer patients will emerge and be tested. Ideally, and regardless of the model, prehabilitation clinical services will involve both physical and psychosocial assessments combined with specific interventions designed to improve a given patient’s outcomes. Therefore, in the ideal prehabilitation model, a well-trained multidisciplinary team would be working together to deliver these services. However, there are significant barriers to delivering prehabilitation in this manner.

Survivorship

The first barriers to address include cost and timing of prehabilitation interventions. There is no doubt that it is expensive to assemble an multidisciplinary team of clinicians, and the relatively quick timeline during which clinicians can deliver prehabilitation services before acute cancer treatment is scheduled to begin creates a need for efficiency in prehabilitation planning.

Therefore, as prehabilitation care models are tested, it will be important to assess how best to deliver these services in a streamlined and costeffective manner.

It is also critical that health care professionals consider the safety of cancer patients undergoing surgery and other treatments, including pre/rehabilitation.71 Beyond their cancer-related issues such as cardiac, renal, orthopedic, or communication problems, just to name a few, many cancer patients fall into categories that make them particularly vulnerable to additional complications. They may be elderly and/or they may have one or more comorbidities. In a recent review titled ‘‘Patient Frailty: The Elephant in the Operating Room,’’ Hubbard and Story36 focused on the risks associated with operating on elderly patients with comorbidities, including falls, delirium, and vulnerability to stressors. Having an understanding of which patients may be at high risk for complications gives the health care professional an advantage in seizing the

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opportunities during which to intervene early– often before surgery or other cancer treatments– in an effort to improve outcomes. For example, Carli et al72 reported a case study involving an 88-year-old woman who had prehabilitation to facilitate her postoperative recovery from a hysterectomy for endometrial cancer. In addition to her advanced age, she exhibited cardiac comorbidity and a history of neurocognitive decline after previous surgeries that included episodes of postoperative delirium. This patient underwent functional, nutritional, and neuropsychological assessments followed by a 3-week prehabilitation program consisting of strength and endurance exercises, as well as nutritional interventions.

The authors noted that, remarkably, this patient had no episodes of postoperative confusion and over the following 8 weeks showed sustained improvement in exercise tolerance, cognitive function, and functional capacity, as measured by validated instruments.

As health care focuses on improving patientcentered care and outcomes while at the same time reducing costs, there is a need to identify opportunities along the care continuum at which these goals can be achieved. Clearly, the first opportunity for impact is at diagnosis or shortly thereafter and would involve the provision of evidence-based prehabilitation services. As oncology nurses, particularly navigators, are often the primary patient contact immediately following diagnosis, they may be ideally positioned to provide effective prehabilitation assessments and interventions. It is worth repeating that prehabilitation consists of clinical assessments and interventions and is not the same as patient education. So although nurses may be ideally positioned to improve outcomes and reduce health care costs through use of prehabilitation assessments and interventions, it will be important to ensure that they have or develop the necessary clinical competencies.

Before nurses can lead or participate in highquality cancer prehabilitation assessments and interventions that are timely, cost-effective, safe, and efficacious, there is a need to identify the prerequisite core competencies, opportunities to develop and/or obtain the appropriate initial and ongoing education needed, and protocols for documenting baseline status and treatment outcomes. This will necessitate a close working relationship with multidisciplinary colleagues and a focus on the evidence-base as it grows over time.

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Many oncology nurses may need to transition from their current role in oncology care to one that incorporates the delivery of sophisticated and evidence-based pretreatment assessments and interventions that are accompanied by the careful documentation of outcomes. While this transition is likely to be challenging and will require a genuine commitment of time and resources, it will help ensure that nurses develop expertise in cancer prehabilitation care. Importantly, with this challenge comes a unique opportunity to demonstrate the impact and value that nurses can have at the beginning of the cancer care continuum.

Unfortunately, nursing education, both initial and continuing education, generally does not emphasize and may not even include evidencebased pre/rehabilitation assessments and interventions. In a survey of 401 members of the Academy of Oncology Nurse Navigators, approximately half of the respondents reported that their own knowledge of cancer rehabilitation and appropriate referrals for care was relatively low.73 However, in the same survey, 90% of participants responded that cancer rehabilitation services were important. Therefore, although nurses value cancer rehabilitation care, they will need specific training in this area of health care before they will be able to effectively implement prehabilitation. Furthermore, because the field of cancer prehabilitation is rapidly evolving, it will be critical that the education and training be ongoing to keep current with advances in the scientific literature.

DEMONSTRATING THE VALUE OF NURSING IN PREHABILITATION CARE My work in cancer rehabilitation has included development of a best practices service line approach to cancer pre/rehabilitation–the STAR (Survivorship Training and Rehabilitation) Program–which is focused on improving outcomes.

In an effort to better understand the value that navigators/nurse navigators add to multidisciplinary rehabilitation teams, my colleagues and I surveyed the service line directors (STAR Program Coordinators) working in hospitals throughout the United States.74 Survey participants (n ¼ 94) were asked to rate the value of navigators/nurse navigators within their service lines. Over 95% of the 84 respondents rated navigators/nurse

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J.K. SILVER

FIGURE 5. Recent growth in the cancer prehabilitation and rehabilitation literature. (*PubMed was utilized to perform the searches in March 2013 and September 2014.)

navigators as an ‘‘Exceptional’’ or ‘‘Important’’ value. When asked about barriers to improving the value of navigators/nurse navigators, respondents identified the top three barriers as 1) navigators needed to be more involved in the screening process on the oncology side (44%); 2) navigators needed more time and support from administration (33%); and, 3) navigators were not adequately involved in prehabilitation (26%). Importantly, the fourth barrier cited was navigators need more education in rehabilitation (20%).

In this same survey, we asked these service line directors whether they thought that nurses could provide some prehabilitation assessments and interventions.75 Survey participants were asked, ‘‘As there is a need to streamline care, reduce health care expenses, and improve early referrals to rehabilitation professionals, do you agree that nurses (navigators, etc.) can provide basic screening and interventions for prehabilitation (eg, QuickDASH and upper extremity physical examination in newly diagnosed breast cancer patients) if they received appropriate training and demonstrated competency?’’ Of the 87 participants who answered the question, the overwhelming majority (75%) agreed with the statement; 18% were unsure and only 7% disagreed. Of particular note is that <15% of the survey participants were nurses, with the majority identifying themselves as rehabilitation clinicians (62%) and administrative personnel (25%).

This survey study demonstrated that, in general, non-nurse service line directors believed

that nurses can provide some prehabilitation assessments and interventions and, furthermore, suggested that nurses would receive encouragement and support from non-nurse colleagues.

However, it is important to note that regardless of who does the initial assessments, if patients are found to have physical impairments, they should be appropriately triaged to rehabilitation health care professionals (eg, physiatrists and/or physical, occupational, and speech therapists) who have expertise in diagnosing and treating these impairments. Similarly, if distress screening or other mental health screening is performed and problems are identified, patients should be referred to experts in mental health. Indeed, during the screening process, nurses (or other nonrehabilitation health care professionals) have an important opportunity to facilitate early referrals to clinical experts who can provide the next level of care. Importantly, navigators may be particularly suited to assist with this care coordination.76

CONCLUSION The value of including cancer prehabilitation in the oncology care continuum is supported by a growing body of scientific evidence that demonstrates its potential to improve health outcomes while at the same time reduce health care costs (Fig. 5).12 Notably, improved physical function is inextricably linked to improved psychological health and quality-of-life outcomes. Moreover,

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improving a cancer survivorâ&#x20AC;&#x2122;s ability to function undoubtedly decreases the financial burden that cancer-related occupational disability exerts on individuals and society. Cancer prehabilitation is also patient-centered care that encourages newly diagnosed individuals to participate in better preparing themselves for the rigors of upcoming treatments. This active participation in specific strategies that are aimed at improving their health outcomes is empowering and may have lasting positive effects throughout a patientâ&#x20AC;&#x2122;s lifetime.

Prehabilitation is an evolving field and does have the potential to significantly change the delivery of cancer care as we now know it. As this article demonstrates, there is a body of evidence to suggest that preoperative prehabilitation (often combined with postoperative rehabilitation) improves the health outcomes of a variety of patients. Certainly, it stands to reason that the sickest and weakest of the patients who are scheduled to undergo a major operation (or other treatment) for cancer are those most likely to be readmitted with complications. Indeed, many elderly people are diagnosed with cancer when they are already physically and psychologically depleted. They have little reserve to withstand the rigors of upcoming oncology treatments.

Safely navigating the oldest and the sickest cancer patients through the oncology care continuum is of paramount importance and improving health status with targeted interventions before surgery may reduce postoperative complications and increase the likelihood that the patient will recover without hospital readmission.

While cancer predominantly affects older individuals, many children and young adults are diagnosed with cancer at the height of good health.

Inevitably, cancer treatments will cause these patients significant pain and fatigue. More likely than not, they will become weaker and increasingly deconditioned. With traditional cancer treatment, return to their former level of health is unlikely and they are often counseled to accept a new normal. Working-age adult cancer patients often find themselves at risk for life-altering functional problems that may lead to loss of work productivity, early retirement, or health-related total disability. Therefore, anticipating future impairments and their associated functional disability and prescribing targeted prehabilitation interventions that can help improve health outcomes, return these survivors to their highest functional potential, and thereby allow them to help support

27

their loved ones will reduce the burden of cancer on these individuals and society.77,78 Of course, as prehabilitation care evolves, there will be a need to develop best practice models that include multidisciplinary and multimodal care. It will be critical to define the scope of practice for clinicians who participate in this care and prehabilitation protocols and pathways must be carefully constructed so as to ensure that health care professionals are not treating patients for existing medical problems that are outside of their scope of practice. Ideally, trained clinicians, including nurses and navigators, will be involved in screening, prehabilitation assessments, and documentation of baseline patient status. If physical impairments are not present at baseline, then these same clinicians can provide interventions designed to reduce the likelihood of developing future impairments. However, documented medical problems, including physical and/or psychological impairments should be treated by health care professionals who are specialists. Therefore, if physical impairments are present, these patients should be triaged to rehabilitation health care professionals, including physiatrists and physical/ occupational/speech therapists, for appropriate preoperative or pretreatment interventions. Similarly, if screening demonstrates significant psychological issues, these patients can be triaged to mental health professionals.

While early prehabilitation studies are encouraging, there are many gaps in the current research. For example, prehabilitation interventions have been studied far more often in lung, colorectal, prostate, and head and neck cancer patients than in patients with breast cancer. Given the significant physical and functional problems that are well documented in the breast cancer literature, it is likely that future prehabilitation studies in this population will show a reduction in pain and disability and an increase in quality of life. Current prehabilitation research has also primarily focused on patient physical outcomes.

Future research should endeavor to more fully examine the cost of this care and the benefits applicable to patients, payers and society. These studies might focus on whether prehabilitation is efficacious in reducing hospital lengths of stay, unplanned readmissions, unnecessary tests such as bone scans, MRIs, PET scans, and other studies that are ordered so as to rule out cancer progression in patients that actually have undiagnosed and/or untreated musculoskeletal pain.

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J.K. SILVER

Even if studies fail to demonstrate significant cost savings in a given oncology patient population, it is important to consider whether the physical and psychological health benefits of prehabilitation interventions are substantial (ie, impact quality of life) enough to warrant an investment in this care. Cancer prehabilitation, although an evolving area of research and clinical care, has the potential to improve physical and psychological health outcomes while simultaneously reducing the cost

of care, thereby reducing the burden that the disease itself places on survivors and the financial burden that it places on both individuals and society.

ACKNOWLEDGMENT The author acknowledges and thanks Julie A. Poorman, PhD, for her assistance with manuscript preparation.

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