Tai Ji Quan for the aging cancer survivor:Mitigating the accelerated development of disability,falls,and cardiovascular disease from cancer treatment

Kerri M.W inters-Stone

School of Nursing and Knight Cancer Institute,Oregon Health&Science University,Portland,OR 97239,USA

Tai Ji Quan for the aging cancer survivor:Mitigating the accelerated development of disability,falls,and cardiovascular disease from cancer treatment

Kerri M.W inters-Stone

School of Nursing and Knight Cancer Institute,Oregon Health&Science University,Portland,OR 97239,USA

Currently there are more than 13.7 million cancer survivors living in the U.S.,and that figure is projected to increase by 31%in the next decade,adding another 4 m illion cancer survivors into the healthcare system.Cancer is largely a disease of aging,and the aging of the population will sharply raise the proportion of older cancer survivors,many of whom will be long-term survivors(5+years post diagnosis).This review will address the potential utility of exercise to address three health problems that are of particular concern for the aging cancer survivor and the healthcare system,i.e.,disability,falls,and cardiovascular disease,because the development of these age-related problems may be accelerated by cancer treatment.While there are many different modes of exercise that each produce specific adaptations,Tai Ji Quan may be a particularly suitable strategy to mitigate the development of age-and cancer-treatment-related problems.Based on studies in older adults with out cancer,Tai JiQuan produces musculoskeletal and cardiometabolic adaptations and is more easily performed by older adults due to its low energy costand slowermovement patterns.Since cancer survivors are mostly older,inactive,and often physically limited by the lingering side effects of treatment,they need to engage in safe,practical,and effective modes of exercise.The dearth of published controlled trials examining the efficacy of Tai Ji Quan to mitigate cancer-treatment-related musculoskeletal and cardiovascular side effects points to ample research opportunities to explore the application of this non-Western exercise modality to improve long-term outcomes for aging cancer survivors.

Aging;Cancer survivor;Chemotherapy;Exercise;Neoplasm;Physical activity;Physical function;Tai Ji Quan

1.Introduction

One in two men and one in three women willbe diagnosed with cancer in his or her lifetime.1From the momenta person is diagnosed with cancer until the time of death,he or she is considered a cancer survivor.Due to improved screening methods and the development of more effective treatments,the number of cancer survivors has steadily risen over the past few decades.As of January 1,2012,approximately 13.7 million cancer survivors were alive in the U.S.2In less than 10 years, the number of cancer survivors is projected to increase by 31%,adding another 4 million cancer survivors into the healthcare system.

Cancer is a disease of aging.with the aging of the population,the number of survivors who are older will rise dramatically in the next decade;and regardless of age,78% will be long-term survivors(5+years post diagnosis).The growing number of aging cancer survivors will pose a significant challenge for the healthcare system because of the combined effects of cancer treatment and aging on the development of comorbid disease,disability,and accidentaldeath from injuries such as falls.The Institute of Medicine (IOM)has declared that the cancer care delivery system is in crisis,in part due to a lack of evidence-based approaches for delivering high-quality cancer care.The IOM has called for improving the evidence base by expanding the breadth and depth of evidence derived from interventions in older cancer survivors and health behaviors.3Studies of aging cancer survivors comprise only a small proportion of research,especially exercise research,which could provide evidence for a singular behavioral strategy that could comprehensively maintain functioning,reduce the risks of comorbid conditions,and improve quality of life.4,5

This review will address the potential utility of exercise on three health problems that are of particular concern for the aging cancer survivor and the healthcare system:disability, falls,and cardiovascular disease(CVD).These are especially important because the development of these age-related problems may be accelerated by cancer treatment.While there are many different modes of exercise that each produce specific adaptations,Tai JiQuan may be a particularly suitable strategy to mitigate the development of age-and cancertreatment-related problems.Based on studies in older adults with out cancer,Tai Ji Quan produces musculoskeletal and cardiometabolic adaptations and is more easily performed by older adults due to its low energy cost and slower movement patterns.Since cancer survivors are mostly older,inactive,and often physically limited by the lingering side effects of treatment,they need to engage in safe,practical,and effective modes of exercise.We will lim it this discussion to Tai Ji Quan and not to other types of exercise that are often thought of as variations of Tai Ji Quan,such as Qigong,because Tai Ji Quan is a unique form of exercise with distinct training properties. Nor will this discussion refer to trials that combined Tai Ji Quan with other modalities.

2.The intersection of cancer treatment and aging: accelerated development of disability,falls,and CVD

In addition to increasing the risk of cancer,aging is associated with declines in physical function,increases in fall risk,and the development of CVD,suggesting a natural pathogenesis that underlies these conditions.The cellular mechanisms of agingper semay result from prolonged oxidative stress,accumulation of DNA damage,and chromosomal instability that ultimately results in cell death that also leads to dysfunction and disease.6,7Paradoxically,many types of cancer treatment,such as chemotherapy,operate by causing early death of tumor cells;but,since treatments are usually delivered system ically,they invariably kill cells in non-malignant tissues.8As such,cancer survivors may be susceptible to accelerated aging triggered by chemotherapy and in turn may experience age-related problems sooner or worse than personswith out cancer.9,10The intersection between aging and cancer treatment and the resultant consequences are becom ing increasingly illum inated as clinical practice moves toward aggressive treatment of cancer in older patients.

2.1.Disability

Age and illness can cause physiologic impairments that lead to limitations in physical functioning,which could progress to disability.Sweeney etal.11were among the first to reporta greater prevalence of functional limitations,including reduced mobility,among older female cancer survivors(＜5 years post-diagnosis)compared to older women with no cancer history.Cancer survivors were more likely to report that they were unable to do heavy household work(odds ratio (OR)=1.47,95%CI:1.27,1.69),walk one-half mile (OR=1.31,95%CI:1.1,1.54),or walk up and down stairs (OR=1.34,95%CI:1.05,1.72).Functional lim itations may begin a cascade to disability,dependence,and death.12In fact, slower 20-m walk speeds are associated with higher mortality (OR=1.09,95%CI:1.02,1.16)and faster progression to disability(OR=1.25,95%CI:1.13,1.35)among older cancer survivors.13Cancer treatment can alter physical functioning in ways that are similar to aging(i.e.,weakness)butalso in ways unique to treatment.Chemotherapy is associated with sarcopenia,14—18fatigue,19and deconditioning.20Regimens that contain neurotoxic agents also cause peripheral neuropathy21and vestibulotoxicity22,23that affect balance and mobility.Neuropathy and vestibulotoxicity in older adults are associated with poor balance,low mobility,and subsequent falls.24—26The relative contributions of muscle weakness, neuropathy,and vestibular dysfunction to physical functioning in cancer survivors are not yet known,but approaches that strengthen muscles used in everyday movements and strengthen the damaged sensory systems that contribute to instability during movement could be the best rehabilitation strategy for reversing functional declines caused by neurotoxic cancer treatment.

2.2.Falls

Falls and disability share common risk factors(e.g., weakness,instability,and altered gait)that typically increase with age;and,like disability,falls are a significant concern for cancer survivors.Chen etal.27reported an elevated risk of falls after women developed breast cancer compared to women never diagnosed with cancer(hazard ratio(HR)=1.15, 95%CI:1.06,1.25),and others have observed fall rates in cancer survivors that are double those of cancer-free peers28or community-dwelling older adults.29Cancer treatment itself and inactivity that often accompanies treatment can worsen age-related weakening.For cancer survivors treated with chemotherapies that are toxic to the nervous system,neuropathy and vestibular dysfunction(e.g.,damage to the inner ear) are common side effects.In a single report of patients who received neurotoxic chemotherapies(n=109),20%experienced a fall during treatment and fallers had higher scores on self-report measures of neuropathy than non-fallers.30Using posturography tests that evaluate sensory inputs to balance control,breast cancer survivors with a history of falls have worse performance in conditions challenging vestibular input to balance control compared to survivors with no fall history.31Exercise,and in particular Tai Ji Quan,can reverse weakness, restore balance,and reduce falls in older adults.32,33The specific ways that cancer treatment changes fall risk factors suggest that strength training or Tai Ji Quan might also best reduce falls in female cancer survivors or that they might be equally effective.

2.3.CVD

Due to steady improvements in survival rates for cancer, CVD is now a competing cause of morbidity and mortality for cancer survivors.34For example,Bardia and colleagues35reported that 80%of breast cancer survivors(60—67 years old) had a CVD risk equivalent to or greater than the odds that they would experience a recurrence of their cancer.The risk of death from CVD was greater(HR:1.24)than that for death from other cancers(HR:1.13),chronic obstructive pulmonary disease(HR:1.10),or diabetes(HR:1.10).34From a study of more than 30,000 U.S.veterans,treatment of prostate cancer with anti-androgen therapy was associated with a significantly elevated risk of coronary heart disease,myocardial infarction, sudden cardiac death,and stroke.36Radiation,chemotherapy, and anti-estrogen or anti-androgen therapy may all contribute to quickened CVD development after cancer treatment due to direct cardiotoxic effects on the heart,causing damage to cardiac muscle and the vasculature,leading to premature coronary artery disease,heart failure,and stroke and heart failure that is progressive and irreversible.37,38Cancer treatment can also change the endocrine milieu,leading to increased inflammation,insulin resistance,and dyslipidemia that may further contribute to the accelerated development of CVD.Exercise training is known to improve cardiovascular health in persons with out cancer;thus,exercise could also mitigate negative changes in cardiovascular health among cancer survivors.

3.Tai Ji Quan for aging cancer survivors:translating evidence from older adults without cancer

Tai Ji Quan is a series of individual dance-like movements linked in a continuous sequence,flow ing slow ly and smoothly from one movement to another.33It has been used for centuries as a martial arts form.It emphasizes 1)changing the distribution of one’s body weight to provide overload sufficient to challenge control of body balance and 2)coordinating breathing and posture changes with mental concentration.The integrated physical and mental effort demanded by Tai Ji Quan distinguishes it from other modes of exercise.These qualities may translate to improved body awareness and control,to improved fluid flow through vessels,and to reduced workload on the heart.Due to its slow and controlled movement patterns and low metabolic demand,Tai Ji Quan has been extensively studied as a mode of exercise that can be safely performed by older adults regardless of exercise capacity and that may reverse or slow the development of age-related conditions such as disability,falls,and CVD.

In older adults,Tai Ji Quan is an exercise modality that reduces falls in older adults because it addresses the underlying reasons people fall in old age.Those reasons,e.g., weakness and poor mobility,also lie on the pathway toward disability development.Tai Ji Quan emphasizes weight transfer and movement of the body outside of its base of support.By doing so,it improves strength,postural control, and balance,39all of which help prevent falls.A recentmetaanalysis that pooled the effect of all studies reported a 49% reduction in fall incidence from Tai Ji Quan(incidence rate ratio(IRR)=0.51,95%CI:0.38,0.68).40As one example,in a randomized,controlled trial among persons over 70 years old(n=256)by Lietal.,326 months of Tai Ji Quan exercise improved several measures of functional balance compared to stretching control participants,who showed no change in these outcomes(p＜0.01 for all tests).At the end of the 6-month intervention,significantly fewer falls(38vs.73,p＜ 0.01),a lower proportion of fallers(28%vs.46%,p=0.01),and fewer injurious falls(7%vs.18%,p=0.03) were observed in the Tai Ji Quan group compared to stretching controls.Risk of multiple falls in the Tai Ji Quan group was 55%lower than that of the stretching controls (risk ratio=0.45,95%CI:0.30,0.70).In women treated for cancer,Tai Ji Quan might be particularly effective when neuropathy and/or vestibular dysfunction from chemotherapy contribute to instability that increases fall risk.41In a single group study,Li et al.42reported improvement in plantar sensation and functional gait in a small sample of persons (n=25)with peripheral neuropathy who participated in a 24-week Tai Ji Quan program.Several studies that evaluated sensory input to balance control via computerized dynam ic posturography demonstrated that Tai Ji Quan improved vestibular control of balance in older adults,43—46including stroke survivors.47

In addition to reducing the risk of disability and falls,Tai Ji Quan may have cardiometabolic benefits that could slow the progression of CVD.In older adults with out cancer,Tai Ji Quan is consistently shown to improve hemodynamic indices compared to usual care,both in persons with and with out CVD.48,49Though fewer controlled trials have evaluated serum profiles after Tai Ji Quan training,two reports have shown significant improvements in triglycerides, total cholesterol,low density lipoprotein-cholesterol,and High density lipoprotein cholesterol(allp＜ 0.05).50,51A small trial reported significant with in-group reductions in the inflammatory marker C-reactive protein,circulating insulin levels,and an index of insulin resistance among Tai Ji Quan participants.50Among heart failure patients,the addition of Tai Ji Quan to a traditional endurance exercise program resulted in greater reductions in systolic blood pressure and a blood marker of cardiac muscle damage than endurance exercise alone.52Interestingly,the consistent improvements in cardiovascular hemodynam ics from Tai Ji Quan largely occur independently of changes in aerobic fitness or body composition,which is less consistently improved by Tai Ji Quan,suggesting that a different mechanism is in play.53

4.Tai Ji Quan in cancer survivors:em erging evidence and abundant opportunities

The increasing awareness of the benefits and suitability of Tai Ji Quan for older adults has piqued the interest of practitioners and researchers in determining whether Tai Ji Quan m ight be sim ilarly effective at preventing adverse outcomes related to chronic diseases and their treatments,because Tai Ji Quan might be a form of exercise that their often debilitated patients can safely participate in.There are a grow ing number of studies involving Tai Ji Quan in cancer survivors,but they remain relatively few in number,range vastly in methodologic quality,exam ine w idely differing outcomes(mostly by selfreport),and target diverse samples of patients that vary in cancer type and treatments.54In fact,there are virtually no controlled trials that have examined the potential benefits of Tai Ji Quan on risk factors associated with disability,falls,or CVD in cancer survivors.Mustian et al.55reported that 12 weeks of Tai Ji Quan improved aerobic capacity and muscle strength better than a psychotherapy supportgroup program in breast cancer survivors,while two controlled trials of Tai Ji Quan in breast cancer survivors failed reduce markers of inflammation and/or insulin resistance,though these studies had quite small sample sizes.56,57In a small sample of postsurgical,non-small cell lung cancer survivors(n=27),16 weeks of Tai Ji Quan favorably altered immune cell ratios compared to no exercise,providing some suggestion of a beneficial effect on immune function,which has a role in both atherogenesis and carcinogenesis.58

Clearly,there is an abundance of opportunities to examine the potential benefits of Tai Ji Quan to address major concerns facing cancer survivors,including those that are the focus of this review.There have been no controlled trials examining the potential efficacy of fall prevention exercise programs that are known to reduce fall risk in older adults in reducing the risk of falls that are linked to cancer treatment.We are currently conducting the GET FIT(Group Exercise Training for Functional Improvement after Treatment;Clinical Trials.gov NCT01635413)trial that aims to compare the efficacy of two distinct types of exercise,Tai Ji Quan versus strength training,which are known to prevent falls in older adults with out cancer,to determine whether or not they also prevent falls in women who have completed treatment for cancer.41The GET FIT trial will be the first to examine whether Tai Ji Quan and/or strength training reduces falls in women cancer survivors who are at higher fall risk because of chemotherapy. We will also determine whether Tai Ji Quan and/or strength training improves postural stability,including vestibular and somatosensory inputs to balance control,using both laboratory-based(posturography)and functional measures (gait)in female cancer survivors in order to evaluate whether improvements in strength or stability are the keys to reducing falls in cancer survivors.GET FIT is a 3-group,single-blind, parallel design,randomized controlled trial in women 50—75 years old who have completed chemotherapy for cancer, comparing 1)Tai Ji Quan,2)strength training,and 3)a placebo control group of seated stretching exercise.Women participate in supervised study programs twice per week for 6 months and are followed for an additional 6 months after formal training stops.The primary outcome in GET FIT is falls,which is prospectively tracked by monthly self-report, and secondary outcomes are maximal leg strength,postural stability,and physical function measured at baseline,3,6,and 12 months.The sample for GET FIT is large(n=429, assuming 25%attrition),but will provide adequate statistical power to detect at least a 47%reduction in the fall rate over 1 year by being in either of the two exercise groups versus the control group.GET FIT has enrolled 154 women into the study to date and is on track to disseminate study findings in 2017.The trial is expected to yield important new know ledge about improving strength or balance and preventing falls using evidence-based exercise interventions for women following chemotherapy for cancer.

5.Summary

Exercise interventions are helpful in improving quality of life in cancer survivors and curbing side effects during active treatment.59The American College of Sports Medicine, American Cancer Society,and National Comprehensive Cancer Network have issued guidelines for exercise in cancer survivors that are consistent with exercise recommendations for the general public,calling for individuals to engage in at least150 min of moderate-intensity aerobic exercise perweek plus 2—3 weekly strength training sessions.59—61While these recommendations were based primarily on studies of QoL outcomes in breast cancer survivors,there was very little evidence coming from controlled trials in men or women with other cancers and little evidence at all from controlled trials with outcomes relevant to disability,falls,or CVD.Both sets of guidelines recommend a substantial volume of aerobic and resistance exercise that may be an unachievable goal for aging cancer survivors,because many already report difficulty with simple functional tasks after cancer treatment.11Nearly 70% of cancer survivors fail to achieve recommended amounts of aerobic exercise,and few engage in any resistance exercise.20,62,63Thus,it is unlikely that older cancer survivors can achieve target goals to engage in at least 150 m in of aerobic exercise plus 2—3 resistance training sessions per week.

The current recommendations,however,do not include non-traditional exercise modalities,such as Tai Ji Quan training,which are attractive forms of exercise for adults deconditioned from cancer treatment because both cardiovascular and mobility outcomes can be improved even in those with low exercise tolerance.There is an urgent need to determine whether Tai Ji Quan can reverse or slow the acceleration of aging and onset of side effects associated with cancer treatment,which has implications for reducing clinically meaningful outcomes of disability,falls,and CVD.Only through convincing evidence accumulated from controlled trials with sufficient sample sizes and objectively measured outcomes can it be determined whether engaging in a nontraditional exercise modality,such as Tai Ji Quan,is beneficial for aging cancer survivors,and whether this could lead tomore specific and achievable recommendations for cancer survivors for improving motivation.This evidence would strengthen current guidelines and add specificity to recommendations for older cancer survivors,which represent the majority of this burgeoning proportion of the U.S.population.

Acknowledgment

The work presented in this paper is supported by a research grant from the National Cancer Institute,USA(CA163474).

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Received 9 November 2013;revised 18 November 2013;accepted 19 November 2013

E-mail address:w intersk@ohsu.edu.

Peer review under responsibility of Shanghai University of Sport

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