Viewing exercise oncology through the lens of multidisciplinarity

Ch. 18 Viewing exercise oncology through the lens of multidisciplinarity

Martijn M. Stuiver, PT, PhD

Netherlands Cancer Institute, Amsterdam, the Netherlands & Amsterdam University of Applied Sciences, Faculty of Health, Amsterdam, the Netherlands & AmsterdamUMC, Department of Clinical

Epidemiology Biostatistics and Bioinformatics, Amsterdam, the Netherlands

keywords: multidisciplinarity, rehabilitation, exercise programming, shared decision making, goal setting, referral

Abstract

Exercise is an important addition to cancer care. Individuals with cancer, however, may face health problems which can be improved with exercise, but which can also be barriers to exercise. Thus, exercise support is pivotal throughout the cancer care trajectory. Which (health care) professionals should be involved in providing exercise support is dependent on the context, and related to the

complexity of the health condition and the self-management skills of the patient. Because these factors will change over time, the need for multidisciplinary involvement needs to be regularly reevaluated. In this chapter, a framework to aid decisions on this topic will be discussed, and illustrated using cases.

1

2

3 4 5 6 7 8 9 10 11 12 13 14

15

16

17

18

19

20

21

Introduction

From the previous chapters, it has become evident that physical activity, and exercise in particular, is important throughout the cancer care continuum; exercise may help patients prepare for treatment[1-3], exercise can help to reduce treatment-related side effects during and after treatment[4,5], to maintain or regain an acceptable level of functioning and quality of life[6], and reduce the health risks related to late effects. [7] Thus, all individuals with cancer should be encouraged to be physically active, and to start or continue exercising. [8,9]

One might argue that exercising, like healthy eating, is a lifestyle choice, instead of a responsibility of the health care system. However, from the previous chapters, it has also become clear that exercising for individuals with cancer is often easier said than done. Even for people without cancer, there can be many barriers to exercising, in many dimensions. Barriers can be practical, social, psychological, be- havioural or physical, or a combination of those. [10,11] Being diagnosed with and treated for cancer is not going to diminish any of those barriers, and is likely to add a few. Therefore, to become or stay physically active, including starting or continuing structured exercise, many individuals with cancer will at some point need the support from health care professionals.

Exercise support can take many forms, ranging from providing print materials with information on the benefits of physical activity or on how to perform exercises, all the way up to supervised exercise as part of full multidisciplinary cancer rehabilitation. Exercise support can also be delivered by a wide range of professionals. Within the context of medical care, physical therapists, occupational therapists, clinical exercise physiologists, physiatrists, sports-physicians, behavioural psychologists and nurses or nurse practitioners all can be involved to support exercise in one way or another. While there are good reasons to involve health care professionals to support exercise and physical activity behaviour of pa- tients with cancer, at the same time care must be taken to avoid over-medicalisation of exercise. Pa- tients and survivors who are able to exercise without supervision or other interference of health care professionals should be empowered to do so. In the community, exercise physiologists and fitness pro- fessionals can support patients to increase or maintain their physical activity level and physical fitness,

22

23

24

25

26

27

28

29

30

31

32

33

34

35

36

37

38

39

40

41

42

43

44

45

46

provided that they are sufficiently knowledgeable about the consequences of cancer and cancer treat- ment. To support exercise in such a way that it aligns with patients' clinical state, circumstances, pref- erences, values and beliefs, there is no one-size fits all solution. Also, there is considerable overlap in the domains of various health professions, which means that there is no general rule to determine who should do what when it comes to delivering exercise support - unless, of course, specific skills or knowledge are required that are unique to a profession. Thus, to determine the best way to support in- dividual patients in their endeavour to start or continue exercising during or after cancer treatment, ex- ercise should be viewed through a lens of multidisciplinary.

A second reason to view exercise through this lens of multidisciplinary is the multidimensional nature of the barriers for physical activity and exercise that individuals with cancer can experience. Barriers are also not static; they will arise, evolve, and maybe even disappear again, throughout cancer treat- ment and survivorship. Professionals, be they health care providers or exercise professionals in the community, need to be able to recognise these barriers, and act on them timely and effectively. The same is true for recognising and utilising potential facilitators. Health care providers are well trained to do so, within the context of their own profession. However, they should also have a grasp of how cer- tain barriers might be successfully addressed by involving or referring to other professionals. Most of all, they should be able to discuss the available options of exercise and physical activity support with patients, and provide advice, while recognising and respecting the preferences and values, as well as the clinical and practical context of each individual patient.

The objective of this chapter is to discuss how a multidisciplinary perspective on exercise for health is useful to successfully support physical activity or exercise for individuals with cancer, in different phases of cancer treatment and survivorship.

48

49

50

51

52

53

54

55

56

57

58

59

60

61

62

63

64

65

66

67

68

69

70

Contextualising exercise

The ability to adapt

Obviously, the objective of health care is to improve health. Health has traditionally been defined as

"A state of complete physical, mental and social well-being and not merely the absence of disease or infirmity". More recently, Huber et al. stated that in the current era, in which many people live with chronic conditions, such a state is likely unattainable for many. Instead, they proposed to consider health as "the ability to adapt and self manage in the face of physical, psychological and social chal- lenges".[12]

Adaptation is a familiar concept in exercise physiology. Muscles and bones grow stronger, and maxi- mal oxygen uptake increases, as a result of adaptation to adequate exercise stimuli. But also; individu- als can learn to cope with maladaptive or dysfunctional organ systems related to physical activity, by learning alternative ways to move or by increasing the capacity of one system to compensate for fail- ure of another. For example; if exercise capacity is decreased because lung volume and compliance are irreversibly impaired due to surgery and radiotherapy for lung cancer, there is no room for local adap- tation (as the damaged lung tissue cannot be trained back to health). However, muscle strength of the breathing muscles can still be optimised to improve respiration efficiency, and peripheral muscle strength, efficiency, and local endurance of other skeletal muscles can be optimised, for example to improve walking ability. In this case, increasing the capacity of the musculoskeletal system can com- pensate, at least in part, the structural damage of the lung tissue and function.

Adaptation, or maladaptation, can also occur on a psychological or behavioural level. After a cancer diagnosis, people have to psychologically adapt to the distress caused by the diagnosis. In relation to exercise, psychological maladaptation can occur in the form of fear to physically exert oneself, be- cause signs of exertion such as increased breathing frequency or post-exercise muscle aches are per- ceived as threatening. This can then be a barrier to physical activity. [13] People who experience steep declines in physical fitness, due to the disease or its treatment, need to adapt to this new reality by al-

71

72

73

74

75

76

77

78

79

80

81

82

83

84

85

86

87

88

89

90

91

92

93

94

95

a way that they can make it through the day. Maladaptation in the form of inadequate activity regula- tion can be a driver for chronic fatigue[14,15] and eventually lead to physical inactivity when people stop trying. Sometimes, adaptations with regard to societal roles (i.e. work) or the physical environ- ment are needed in order to enable acceptable functioning. All this illustrates that the concept of "the ability to adapt" is particularly suited to the context of cancer rehabilitation.

ICF

Another useful concept to contextualise exercise in cancer care is the International Classification of Functioning, Disability and Health (ICF). ICF adds to the International Classification of Disease by re- garding a health problem from the perspective of the impact of a disease or health condition on human functioning. It does so by describing human functioning in domains of anatomical structure and func- tions, activities and participation, and personal and environmental characteristics. The ICF distin- guishes capacity (reflecting what an individual can do in a standardized environment, e.g. walking ability as evaluated with a 6-minute walking test) from performance (reflecting what an individual ac- tually does in his or her usual environment, e.g. ability to walk from home to the nearest metro sta- tion). Discrepancies can exist between capacity and performance. By recognising the non-linear inter- play and interactions within and between the different ICF domains, one can understand a health prob- lem from a bio-psycho-social perspective, and decide on health care interventions accordingly. [16]

The ICF and the concept of the ability to adapt complement each other strongly. To understand a health problem, and to help deciding on interventions, a 3-step process can be followed (Figure 1).

Step #1 involves recognising the overall health problem and identifying the factors that are related to that health problem ("mediators") in each domain of ICF. If there is maladaptation to these problems, in step #2, the "room for adaptation" is evaluated. This involves assessing the current capacity and per- formance of the individual and evaluating his or her possibilities to improve or maintain capacity or performance, which includes the identification of barriers and potential facilitators for successful adap- tation. In step #3, interventions are chosen. These interventions are aimed at improving the individu- als’ adaptation by increasing or maintaining capacity, optimizing performance, diminishing (biologi- cal, psychosocial or environmental) barriers, and/or at creating or capitalising on existing facilitators.

97

98

99

100

101

102

103

104

105

106

107

108

109

110

111

112

113

114

115

116

117

118

119

120

121

122

123

Following this process, exercise could be considered as an intervention, when step #1 reveals symp- toms or impairments that might be alleviated through exercise. If, in step#2, we decide that exercise is indeed a suitable intervention, an evaluation should be made to decide whether or not the patient is able to exercise safely and/ or effectively on his/her own. This includes an evaluation of the prerequi- sites for successful physical adaptation to the exercise stimulus, such as anatomical integrity, or nutri- tional status, but also an evaluation of self-management skills (Figure 1). Finally, in Step #3 these considerations are synthesized, leading to referral to appropriate exercise programming (Figure 2). The choice for the appropriate type of exercise program (i.e. the level of healthcare involvement) should be periodically reevaluated, and referrals up and down the chain should be made if necessary.

If physical activity is not the intervention, but the intended outcome - i.e. when not being able to be physically active on the desired level is the health problem addressed, or when activity promotion is part of a secondary prevention approach - the same three step process can be followed. In this situa- tion, mediators identified in step #1 would in fact then be the factors that restrict the ability to be phys- ically active (dark grey box in Figure 1).

When there are problems in multiple body systems, or in multiple ICF domains, appropriate exercise programming often means involving other disciplines than those delivering exercise interventions. For example, if a patient is found to be malnourished, a dietitian would need to be involved to treat the malnourishment to enable successfull physical adaptation to the exercise stimulus. In that case, the physiotherapist and the dietitian need to coordinate their intervention for optimal effect. If the health problem is very complex, and several interrelated physical, psychosocial/behavioural and environmen- tal issues need to be addressed simultaneously and coherently, multidisciplinary

Figure 1 A 3-step approach to choosing appropriate exercise programming

Multidisciplinarity

124

125

126

127

128

129

130

131

132

133

134

135

136

137

138

139

140

141

142

143

144

145

146

147

148

The level of multidisciplinary involvement required can be seen as a function of the level of complex- ity of health problems on one hand, and the ability to adapt and self-manage on the other (Figure 2)

Figure 2 The level of health care professional (HCP) involvement, and multidisciplinarity required, is dependent on the presence and complexity of health issues, and on the individuals ability to adapt to

149

150

151

152

and self manage. Referrals up and down the chain of exercise programming can be made accordingly.

153

For example, if, shortly after cancer treatment, a patient is found to be malnourished as well as decon- ditioned, a dietitian would need to be involved to treat the malnourishment, in order to enable success- ful physical adaptation to the training stimulus applied to improve exercise capacity. In that case, the dietitian and the physical therapist or clinical exercise physiologist need to coordinate their interven- tions for optimal effect. Once the nutritional status is stabilized and the individual is capable of main- taining his or her own exercise behavior, referral to community exercise programming (or self-directed exercise) would be warranted. One could also imagine a patient whose health problem is an inability to be physically active on any level, because of chronic severe fatigue. Let's assume that the most impor- tant mediators for this chronic fatigue are anxiety disorder and depression, in combination with kine- siophobia. It is likely that this individual is physically deconditioned, and that exercise will improve the fatigue. However, there is also room and need for adaptation in other areas: the depression should be treated, and the patient should learn to effectively cope with feelings of anxiety. Hence, referral to a health psychologist for counselling or cognitive behavioral therapy might be considered for this indi- vidual, in addition to a graded physical activity program. In the community setting, a breast cancer sur- vivor exercising in a local gym may at some point in time develop lymphedema. This condition should be managed by a specialized physical therapist. The sports instructor should therefore recognize the need for referral as soon as this individual complains about feelings of swelling and heaviness. The physical therapist, in addition to starting lymphedema treatment as needed, needs to brief the sports in- structor with regard to if and how the exercise program should be adapted for this individual, in the presence of lymphedema. If a health problem is very complex, and several interrelated physical, psy- chosocial/behavioural and environmental issues need to be addressed simultaneously and coherently, interdisciplinary rehabilitation by a dedicated oncology rehabilitation team is recommended. Figure 3 provides some exemplary clinical vignettes to illustrate the type of cases that would match the various levels of multidisciplinarity.

In the remaining part of this Chapter, the multidisciplinary approach to exercise oncology and cancer rehabilitation will be illustrated in more detail. A number of cases will be discussed, looking at exercise through the lens of multidisciplinary, and applying the process described above.

155

156

157

158

159

160

161

162

163

164

165

166

167

168

169

170

171

172

173

174

175

176

177

178 179

180

181

182

6 0 y e a r s o l d p a t i e n t , s e l f - e m p l o y e d . R e c e n t l y c o m p le t e d t r e a t m e n t w it h c o n c o m i t a n t c h e m o - r a d i o t h e r a p y f o r

o r o p h y a r y n g e a l c a n c e r. H is t o r y o f a l c o h o l a b u s e a n d s m o k in g . C O P D

s t a g e G O L D I I

. S e v e r e ly d e c o n d i t io n e d a n d s a r c o p e n ic . P r o b le m s w it h e a t in g d u e t o m il d d y s p h a g i a a n d s e v e r e a n x ie t y f o r a s p i r a t i o n . C li n i c a l ly d e p r e s s e d . F in a n c ia l p r o b l e m s d u e t o

d i s e a s e - r e la t e d lo s s o f i n c o m e . I n t e r d i s c i p l i n a r y R e h a b i l i t a t i o n

5 0 - y e a r o l d p a t i e n t , t r e a t e d F o r b r e a s t c a n c e r w i t h m a s t e c t o m y a n d a x il la r y ly m p h n o d e d is s e c t i o n , a n d a d j u v a n t r a d io t h e r a p y . C u r r e n t l y o n T a m o x if e n . B M I

3 8 . M i ld ly m p h e d e m a in t h e a r m , a n d li m i t e d r a n g e o f m o t i o n o f t h e h o m o l a t e r a l s h o u ld e r. F a t i g u e d . N o h i s t o r y o f e x e r c is i n g . W a n t s t o b e c o m e f it t e r a n d lo s e w e i g h t .

M u l t i d i s c i p l i n a r y c o l l a b o r a t i o n

M a l e s u r v iv o r o f s t a g e - I I c o lo n c a n c e r. S u r g i c a ll y t r e a t e d w i t h c u r a t i v e in t e n t , 3 m o n t h s a g o . N o a d j u v a n t t h e r a p y . S t a b le w e i g h t , B M I

3 0 . 5 , n o c o m o r b id it y .

N o h is t o r y o f e x e r c i s i n g , b u t m o t iv a t e d t o s t a r t e x e r c is in g t o im p r o v e f i t n e s s a n d o v e r a l l h e a lt h .

C o m m u n i t y b a s e d e x e r c i s e

p r o g r a m

3 0 - y e a r o l d f e m a le p a t i e n t , O n e m o n t h a f t e r c o m p l e t io n o f c h e m o t h e r a p y t r e a t m e n t ( R - C H O P

) w i t h c u r a t i v e in t e n t , f o r s t a g e - I I I lo w g r a d e n o n - H o d g k in L y m p h o m a . S t a b le w e i g h t . H is t o r y o f e x e r c i s i n g , n o c o m o r b i d i t y . W a n t s t o r e g a in m u s c le s t r e n g t h a n d f i t n e s s , a n d i m p r o v e b o n e h e a lt h a s p e r d o c t o r s a d v i s e .

M o n o d i s c i p l i n a r y H C P - g u i d e d e x e r c i s e p r o g r a m

Figure 3 - Levels of multidisciplinarity with corresponding exemplary patient vignettes\

* Chronic Obstructive Pulmonary Disease; **Global Initiative for Chronic Obstructive Lung Disease criteria - GOLD 2 reflects moderate airflow limitations: 50% ≤FEV1 <80% predicted; †R-CHOP:

combination therapy of Doxorubicine, Cyclofosfamide, Vincristine and Rituximab; ‡ BMI: Body Mass Index (kg/m

).

Case 1

C., a senior financial consultant employed by a large firm, was 43 when she was diagnosed with stage II breast cancer. The tumor was HER2 negative and ER positive. When she got her diagnosis, C. was shocked. It struck her as unfair that she should have cancer; she had always been minding her health.

She used to exercise regularly; two times per week she made a 45' minute run through the park, and she took spinning classes once a week at the gym. She adhered to a healthy diet, had never smoked and was not a heavy drinker. Being very successful in a competitive field of work, she had come to believe that through hard work and dedication one can achieve anything. She had always made her own choices in life, deliberately and with confidence, and she was not one to crumble under pressure. But

183 184 185 186 187 188 189 190 191

192

193

194

195

196

197

198

199

this diagnosis completely swept her off her feet. Looking back, she explains that she saw no other op- tion but to "surrender her body to the doctors and just wait for it to be over".

She went through neoadjuvant chemotherapy treatment with AC-T (adriamycine, cyclofosfamide and taxotere) and underwent breast-conserving surgery with a sentinel node procedure, which was nega- tive. Post-surgery, she received radiotherapy to the chest-wall and anti-hormonal treatment with ta- moxifen. Her treatment had been successful, the doctor had said, and her chance of survival high. Re- lieved, she returned to work as soon as she could, with a desire to put this episode behind her. Soon, she found that she was not able to concentrate very well. Also, she was tired all the time and some- times it felt as if, without warning, all her energy would drain from her body. She did not sleep very well and she increasingly had trouble getting up in the morning. At times she would wake up in the middle of the night, with a rushing pulse, feeling anxious, but not quite able to discern why. Four months after returning to work, she had to call in sick. She has not resumed working ever since. Her fatigue and sleeping problems have not improved since; she regularly needs to take a nap during the day, but at the same time has trouble sleeping at night. When she lies awake, she finds herself worry- ing about the future, in particular with regard to her work ability. Her fatigue also restricts her in her social activities; she simply does not have the energy left to go out with friends in the evening.

She recognises that the treatment has taken its toll on her body and that this is part of the problem. At times she tells herself she should start exercising again, but she can't get herself to do it. Actually, she is not even sure that it would be a good idea, considering how tired she already feels after completing her daily chores, while she is not even working, and considering the pain she feels in her joints at times. On the other hand, she has also noticed that she is starting to put on weight, which she believes is probably due to her diminished physical activity.

Looking at C.'s case, it is clear that she has not adapted very well in many domains of ICF: on the level of physical functions, she is deconditioned, fatigued and putting on weight, and has sleeping problems.

On the level of activities and social participation, she has had problems with activity regulation, and

200

201

202

203

204

205

206

207

208

209

210

211

212

213

214

215

216

217

218

219

220

221

222

223

224

225

has now become largely inactive. Her role functioning (work) is severely restricted. Also, it seems as though there are several personal factors that hinder successful adaptation, which include not knowing what is the right course of action or even fear of making matters worse. An environmental factor at play is her highly demanding work setting, which requires her to be focused and fully dedicated.

Exercise support during treatment

In hindsight, could more attention to supporting C's self-management at the time of diagnosis and dur- ing treatment have made a difference? Especially: would participation in an exercise program at that time have been useful to improve her ability to adapt and support her health? Looking at the evidence about exercise during breast cancer treatment, it seems that this could indeed have been the case. Tak- ing part in an exercise intervention during chemotherapy would likely have prevented her physical de- conditioning, and would have attenuated fatigue. [17]

Clearly, at the time of diagnosis and treatment, there were some barriers to exercising that would have needed to be addressed. First of all, C. did not adapt very well to the emotional distress the diagnosis caused her, and lost her sense of self-efficacy. At this stage, aside from providing psychological sup- port to cope with the emotional distress of the diagnosis, C.'s self-efficacy could have been strength- ened by empowering her to stay physically active, instead of "surrendering her body to the doctors and waiting for it to be over". At diagnosis and throughout cancer treatment, the role of the primary health care providers, the doctor in particular, is of pivotal importance in exercise promotion. [18] C's oncolo- gist could have asked her about her current physical activity, and have encouraged her to stay physi- cally active, explaining that this was something she could do herself to improve her treatment outcome and manage the symptoms that she was going to experience.[19]

The same applies to the nurses and nurse-practitioners that C. encountered during her neo-adjuvant treatment. Even better, the oncologist could have actively referred her to a supervised exercise pro- gram, as the outcome of supervise exercise tends to be better compared to unsupervised exercise. [20]

Still, considering her history of exercising, and her low risk profile at diagnosis, this might initially

226

227

228

229

230 231

232

233

234

235

236

237

238

239

240

241

242

243

244

245

246

247

248

249

250

251

of exercise, and to be reassured that it was safe to continue her regular exercise for now. On the other hand, her treatment with chemotherapy and the subsequent surgery did put her at risk for upcoming physical problems that might impede successful exercise, and for developing symptoms that would re- quire adjustments to the exercise program. Managing these issues would require the competencies of a health care professional, such as a physical therapist, with sufficient oncological knowledge. So, refer- ral to a clinical exercise program might also have been considered. Alternatively, a combination of community based exercise with low-frequent support and advice from a physical therapist with onco- logical knowledge might have been enough to keep C. largely self-managing her exercise program.

Additionally, such prospective surveillance by the physical therapist would have ensured timely health care interventions to help manage new physical problems, should these have arised. [21] Throughout treatment, regular inquiries about C's physical activity level by the doctors, nurse practitioners and nurses would have affirmed her belief of the importance of exercising, which would have helped her to adhere to the exercise program. [18]

So, viewing through the lens of multidisciplinarity, exercise support for C. in this stage of cancer treat- ment would have required the involvement of physicians, nurses and nurse-practitioners to increase awareness and express support, and from a physical therapist working together with a community ex- ercise professional, referring back and forth as needed, to optimize the exercise program.

Exercise in the context of Rehabilitation

As described in parts II and III of this book, in the early stages of the cancer care continuum - that is:

at diagnosis as well as during and shortly after medical treatment - exercise-based rehabilitation is of- ten impairment driven. [22] During treatment, a major focus of exercise is on maintaining physical function, improving treatment tolerance, and controlling symptoms. Shortly after treatment, rehabilita- tion is aimed at regaining and/or improving physical functions to at least the level where survivors can engage in their regular activities of daily living. Exercise interventions in these phases may be generic (aimed at exercise tolerance in general), therapeutic (i.e. aimed at restoring shoulder function), or both.

253

254

255

256

257

258

259

260

261

262

263

264

265

266

267

268

269

270

271

272

273

274

275

276

277

278

Exercise prescription factors (e.g; frequency, intensity, time, and type) and temporisation are chosen to optimize the physiological stimulus, taking into account the influence of cancer treatment where ap- propriate. Success might be declared when symptom management is adequate and physical capacity and performance are maintained or improved. However, when a health problem provoked by the can- cer treatment manifests itself not only on the level of functions, but also on the level of activities and/or societal participation, additional considerations need to be made.

For an exercise program to improve a specific activity of daily life, it is not sufficient to simply im- prove exercise capacity in general. Just like a sports-specific exercise prescription is needed to improve jumping for a basketball player or pitching for a baseball player, a functional approach to exercise pre- scription is needed to improve regular activities of daily life. [23]

Case #2

Mrs. R., is an older female patient who has been hospitalized for several weeks after treatment with lower abdominal surgery for ovarian cancer. This was followed by adjuvant chemotherapy. Mrs. R.

lives on her own in her home, and never had to rely on help from anyone. She regards her indepen- dence as a very important value in life. Now, she feels insecure when moving about and she is quickly fatigued. This means she cannot undertake the physical activities that she used to - in particular, work- ing in her garden. Working in her garden involves, among other movements, being able to kneel and get up again, and working with her arms overhead; body movements from which she now experiences physical limitations. Due to the treatment and her general inactivity during treatment, she is decondi- tioned. In addition, she now suffers from a limited range of motion of the shoulders, lack of strength in the arms, shoulders and lower extremities, and lack of balance. This is making her insecure, and she is afraid to use a ladder to reach the higher branches of the trees she needs to prune. She has tried several times to do some gardening work, but she was exhausted afterwards, and dissatisfied with what she had been able to achieve. As she also has other daily chores to do, such as tidying the house. She cur- rently no longer takes care of the garden herself, but instead relies on the help of a professional gar-

279

280

281

282

283

284

285

286

287

288

289

290

291

292

293

294

295

296

297

298

299

300

301

302

303

304

dener. Consequently, she is less physically active. Also, the need to hire a gardener is bothering her, as she loved to be busy outside and because she does not want to have to rely on others. Her rehabilitation goal is therefore to take care of her garden by herself once again.

Multidisciplinary collaboration

In the example of Mrs. R, a high intensity interval training program on a stationary bike and a circuit of six strength exercises for all large muscle groups is probably not going to help her achieve her goal - even though it will likely result in improved overall physical fitness. Rather, it would be useful to first observe how exactly Mrs. R. is normally doing her gardening work, and what she needs to be able to conduct this again in a satisfactory manner. On the level of capacity, there may be room for adaptation in terms of improving physiological functions. Exercises to improve muscle strength of the trunk, lower and upper extremities, and therapeutic exercises to increase the mobility of her shoulders could be the starting point of an exercise program, as offered by a physical therapist. The type of strength training should of course be aligned with the rehabilitation goal. For example, for the shoulder

muscles, increasing muscle endurance is much more relevant to the rehabilitation goal than increasing maximum strength. Increasing maximum grip strength may be useful however. But the rehabilitation plan does not end with improving the basic physical functions. As functions improve, exercises should be added that mimick the actions Mrs. R. needs to perform when working in her garden. Such

functional exercises are intended to improve performance in addition to capacity. These exercises should also be gradually increased in intensity and complexity, to maintain the progressive overload needed to trigger adaptation. Such an approach will ensure sufficient specificity of the exercises, and additionally help build Mrs. R.'s self-confidence in performing her gardening activities. On the level of performance, there may also be room for adaptation in other areas that do not even require

improvement of exercise capacity. For example, Mrs. R. could maybe change her (movement) strategies, to improve the ergonomics or safety of certain actions. Maybe she could partition and alternate the gardening activities in such a way that they would require less energy. Also, there may be possibilities to improve performance of her gardening activities by changing environmental factors, such as equipment used. An occupational therapist may therefore offer valuable insights, both to the

305

306

307 308

309

310

311

312

313

314

315

316

317

318

319

320

321

322

323

324

325

326

327

328

329

330

331

332

patient and to the physical therapist. [24] The occupational therapist should make sure to inform the physical therapist about the advice provided. In this way, the physical therapist can shape the functional exercises in such a way that they align with the instructions of the occupational therapist regarding how Mrs. R. can perform her gardening activities most safely or economically. As soon as her capacity and performance (in terms of functions and skills) start to improve in the rehabilitation environment, Mrs. R needs to practice her activities in real life too, gradually taking up her gardening again. If needed, the occupational therapist may also play a role in this phase by helping Mrs. R. to plan her gardening activities carefully, in such a way that she has sufficient energy left to engage in other activities of her daily life, and sufficient time to rest and recover. To do this effectively, the occupational therapist needs to be informed by the physical therapist, about the current capacity of Mrs R.

In this example, multidisciplinarity translates into two health care professionals, a physical therapist and an occupational therapist, who collaborate to benefit from each others’ expertise while they both contribute to help a patient achieve a single, relatively low-complex rehabilitation goal.

Interdisciplinary rehabilitation

A limited number of patients may develop more complex, interrelated problems in several domains of functioning (physical, psychological, social), to such a degree that these issues need to be addressed si- multaneously and coherently. Usually, this requires a much more intensive collaboration of several health care professsionals in an interdisciplinary oncology rehabilitation team. [25] Like rehabilitation for other chronic health conditions, such cancer rehabilitation often uses a goal-directed approach. That is; in a process of shared decision making, patients first prioritize the problems that they experience and want to improve through rehabilitation. Next, they set a number of specific goals they want to achieve, which are formulated and operationalized at the level of activities and societal participation.

Finally, a treatment plan is developed to achieve those goals, for example using the three step approach described earlier to identify and address the key-factors to successful adaptation. The treatment plan

333

334

335

336

337

338

339

340

341

342

343

344

345

346

347

348

349

350

351

352

353

354

355

356

357

358

involves actions from several health care professions, which need to be closely aligned. As a result, it may happen that, instead of being designed to achieve optimal physiological capacity and specific functional performance, the exercise prescription needs to be adapted to accommodate the overall team strategy. For example, the team may decide on a general treatment strategy of diminishing anxiety, in- creasing self-efficacy and behavioral control, and improving self-management, through graded expo- sure to activities of daily living. This then implies that the exercise program that is part of the multidis- ciplinary intervention is progressed much more slowly than would be desirable from an exercise physi- ology point of view.

C's case is a good example of a health situation in which the level complexity and interrelatedness of the problems may initially require such a comprehensive approach to rehabilitation. C. has problems in several areas of functioning: she has physical limitations (deconditioning, weight changes, joint pain), psychological issues (anxiety, low self-efficacy and problem solving ability with regard to her activity levels), cognitive problems, and role-functioning problems with regard to work and social interactions.

All of these problems are connected in several ways: her anxiety, her worries about her work ability, her dysregulated sleeping pattern, and her low physical activity level all maintain her sleeping problems. Her deconditioned state, physical inactivity, sleeping problems and anxiety are drivers for her fatigue. Fatigue, anxiety and cognitive problems (concentration) may also very well be

interconnected. Finally, her low self-efficacy, fatigue, and joint complaints are important barriers to exercising.

So, C. is enrolled in a cancer rehabilitation program. Because some of the physical problems she is experiencing may be related to treatment side-effects, she is medically screened by a physiatrist and an oncologist. She gets a cardiopulmonary exercise test with ECG and breath-gas exchange, to rule out cancer treatment induced cardiac problems that may underlie her fatigue and exercise intolerance, and to obtain a good starting point for prescribing aerobic exercise. The joint problems are recognized as related to the anti-hormonal treatment, and inflammatory joint-problems are ruled out. The physiatrist explains that exercise is likely to improve these complaints, and will not increase them. [26] Through shared decision making, C. and the rehabilitation team set several goals for the rehabilitation. The most

359

360

361

362

363

364

365

366

367

368

369

370

371

372

373

374

375

376

377

378

379

380

381

382

383

384

385

important goals are; 1) to take up self-directed exercise again, 2) to self-manage daily chores and activities while maintaining sufficient energy for social activities in the evening, and 3) to make a start with return to work. Several disciplines will be involved: The psychologist will be treating the anxiety disorder, and help C. with getting a grip on her thoughts and worries. The occupational therapist will first address sleeping behavior, and teach relaxation exercises. The occupational therapist will also work with C. to help her regulate her activities (including those activities related to the rehabilitation program) adequately. In a next step, the occupational therapist will support C. to take control in developing a work reintegration plan together with the occupational physician at her workplace. The physical therapist will start with an exercise program, which will have 2 major goals. The first goal is to improve exercise tolerance and physical functions such as increasing aerobic fitness and muscle strength. To achieve this, in the first weeks, C. will be coached to increase her physical activity level using home based walking and moderate intensity strength exercises, as well as twice weekly moderate intensity exercise at the rehabilitation facility. Next, a non-linear exercise prescription for aerobic training, incorporating high intensity interval training [27,28] will be employed, in addition to progressive strength training based on repeated 1-repetition maximum tests. The second goal for physical therapy is to improve exercise-self efficacy and self-management. To achieve this goal, C.

will be educated on general principles such as overload vs rest, and temporization, and learn to recognize signals of overexertion (topics that are also addressed during the occupational therapy sessions in the broader context of daily functioning). Also, weekly exercise goals are set and documented in an exercise log, so C. can track her improvement. The exercise program will start generic, and will be made more specific to C's own preferences with regard to self-directed exercise, i.e. running. Because regular strength exercises are recommended for breast cancer survivors[29], C.

will also be taught strength exercises using body weight, which she can implement in her own training schedule. Participation in a group-based sports/game module, led by a dedicated sports instructor, will also be part of the rehabilitation program. The main goal of this module is to have C. exercise in a way that is fun and challenging, while the games used are also designed to help participants improve their self-management and self-efficacy. Finally, a dietitian will be consulted to evaluate whether

386

387

388

389

390

391

392

393

394

395

396

397

398

399

400

401

402

403

404

405

406

407

408

409

410

411

412

adjustments are needed to C's diet, in addition to her exercise program, to manage her weight. [30] The rehabilitation team expects that goal attainment will be achieved in within 15 weeks.

This is just one example of the interdisciplinary approach to cancer rehabilitation. Other types of interventions, including different exercise prescriptions, and other combinations of disciplines

involved may be applicable for different individuals. For some types of cancer or treatment, especially those that have a very high symptom load, adopting an interdisciplinary approach to rehabilitation and integrating this into the standard clinical pathway of cancer care, may desirable. An example of this is the integrated head and neck cancer rehabilitation program of the Netherlands Cancer Institute. [31]

Concluding remarks

To summarize, exercise can contribute to the health of individuals with cancer, but to successfully and safely employ exercise as an intervention, several prerequisites must be met. Physical, psychosocial and environmental barriers may need to be addressed, and support of health care professionals may be required accordingly. The more complex the health state, and the lower the ability of an individual to adapt to and self-manage their health problems, the more need there is for involvement of health care professionals and for a multidisciplinary approach to support exercise. All professionals working with individuals with cancer, both within and outside of the healthcare system, need to maintain a broad perspective and escalate or de-escalate the level of support as needed. Viewing exercise through the lens of multidisciplinarity will ensure adequate exercise support, tailored to the needs of each individual with cancer, throughout all phases of cancer treatment and survivorship.

In order to attain a situation in which every individual with cancer receives the appropriate level of exercise support, the health care infrastructure must be such that screening is standard, referral pathways are in place, and practical and financial barriers for patients are minimized. But most importantly, the when and how of multidisciplinary collaboration should integrated firmly into the standard educational curricula of health care professionals, as well as in those of exercise professionals training to work with individuals with cancer.

413

414

415

416

417

418

419

420

421

422

423

424

425

426

427

428

429

430

431

432

433

434

435

436

437

438

References

1 Silver JK, Baima J. Cancer Prehabilitation. American Journal of Physical Medicine &

Rehabilitation 2013;92:715–27. doi:10.1097/PHM.0b013e31829b4afe

2 Hijazi Y, Gondal U, Aziz O. A systematic review of prehabilitation programs in abdominal cancer surgery. International Journal of Surgery 2017;39:156–62. doi:10.1016/j.ijsu.2017.01.111 3 Driessen EJ, Peeters ME, BONGERS BC, et al. Effects of prehabilitation and rehabilitation

including a home-based component on physical fitness, adherence, treatment tolerance, and recovery in patients with non-small cell lung cancer: A systematic review. Critical Reviews in Oncology / Hematology 2017;114:63–76. doi:10.1016/j.critrevonc.2017.03.031

4 Kessels E, Husson O, Van der Feltz-Cornelis CM. The effect of exercise on cancer-related fatigue in cancer survivors: a systematic review and meta-analysis. NDT 2018;Volume 14:479–94.

doi:10.2147/NDT.S150464

5 Stout NL, Baima J, Swisher AK, et al. A Systematic Review of Exercise Systematic Reviews in the Cancer Literature (2005-2017). PM&R 2017;9:S347–84. doi:10.1016/j.pmrj.2017.07.074 6 Mishra SI SRSCGPBDTO. Exercise interventions on health-related quality of life for people with

cancer during active treatment (Review). 2012;:1–447.

7 Jones LW, Habel LA, Weltzien E, et al. Exercise and Risk of Cardiovascular Events in Women With Nonmetastatic Breast Cancer. JCO 2016;34:2743–9. doi:10.1200/JCO.2015.65.6603 8 Cormie P, Zopf EM, Zhang X, et al. The Impact of Exercise on Cancer Mortality, Recurrence,

and Treatment-Related Adverse Effects. Epidemiologic Reviews 2017;39:71–92.

doi:10.1093/epirev/mxx007

9 Schmitz KH, Courneya KS, Matthews C, et al. American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. 2010. 1409–26. doi:10.1249/MSS.0b013e3181e0c112 10 Blaney JM, Lowe-Strong A, Rankin-Watt J, et al. Cancer survivors' exercise barriers, facilitators

and preferences in the context of fatigue, quality of life and physical activity participation: a questionnaire-survey. Psycho-Oncology 2011;22:186–94. doi:10.1002/pon.2072

11 van Waart H, van Harten WH, Buffart LM, et al. Why do patients choose (not) to participate in an exercise trial during adjuvant chemotherapy for breast cancer? Psycho-Oncology 2015;25:964–

70. doi:10.1002/pon.3936

12 Huber M, van Vliet M, Giezenberg M, et al. Towards a ‘patient-centred’ operationalisation of the new dynamic concept of health: a mixed methods study. BMJ Open 2016;6:e010091–12.

doi:10.1136/bmjopen-2015-010091

13 Velthuis MJ, Peeters PH, Gijsen BC, et al. Role of Fear of Movement in Cancer Survivors Participating in a Rehabilitation Program: A Longitudinal Cohort Study. YAPMR 2012;93:332–8.

doi:10.1016/j.apmr.2011.08.014

439

440 441

442 443 444 445 446 447

448 449 450 451

452 453 454

455 456

457 458 459 460

461 462 463

464 465 466 467 468 469 470 471

472 473 474

475

476

477

14 Timmerman JG, Dekker-van Weering MGH, Tönis TM, et al. Relationship between patterns of daily physical activity and fatigue in cancer survivors. Eur J Oncol Nurs 2015;19:162–8.

doi:10.1016/j.ejon.2014.09.005

15 Wolvers MDJ, Bussmann JBJ, Bruggeman-Everts FZ, et al. Physical Behavior Profiles in Chronic Cancer-Related Fatigue. 2018;:1–8. doi:10.1007/s12529-017-9670-3

16 Steiner WA, Ryser L, Huber E, et al. Use of the ICF model as a clinical problem-solving tool in physical therapy and rehabilitation medicine. Physical Therapy 2002;82:1098–107.

17 van Waart H, Stuiver MM, van Harten WH, et al. Effect of Low-Intensity Physical Activity and Moderate- to High-Intensity Physical Exercise During Adjuvant Chemotherapy on Physical Fitness, Fatigue, and Chemotherapy Completion Rates: Results of the PACES Randomized Clinical Trial. J Clin Oncol 2015;33:1918–27. doi:10.1200/JCO.2014.59.1081

18 Jones LW, Courneya KS, Fairey AS, et al. Effects of an oncologist’s recommendation to exercise on self-reported exercise behavior in newly diagnosed breast cancer survivors: a single-blind, randomized controlled trial. Annals of Behavioral Medicine 2004;28:105–13.

doi:10.1207/s15324796abm2802_5

19 Buffart LM, Kalter J, Sweegers MG, et al. Effects and moderators of exercise on quality of life and physical function in patients with cancer: An individual patient data meta-analysis of 34 RCTs. Cancer Treatment Reviews 2017;52:91–104. doi:10.1016/j.ctrv.2016.11.010

20 Stout NL, Binkley JM, Schmitz KH, et al. A prospective surveillance model for rehabilitation for women with breast cancer. Cancer 2012;118:2191–200. doi:10.1002/cncr.27476

21 Silver JK, Baima J, Mayer RS. Impairment-driven cancer rehabilitation: an essential component of quality care and survivorship. CA: A Cancer Journal for Clinicians 2013;63:295–317.

doi:10.3322/caac.21186

22 de Vreede PL, Samson MM, van Meeteren NLU, et al. Functional-task exercise versus resistance strength exercise to improve daily function in older women: a randomized, controlled trial. J Am Geriatr Soc 2005;53:2–10. doi:10.1111/j.1532-5415.2005.53003.x

23 Rijpkema C, Van Hartingsveldt M, Stuiver MM. Occupational therapy in cancer rehabilitation:

going beyond physical function in enabling activity and participation. Expert Review of Quality of Life in Cancer Care 2018;00:1–3. doi:10.1080/23809000.2018.1438844

24 Dutch National Guideline 'Cancer Rehabilitation’: modular revision 2017. Netherlands Comprehensive Cancer Organization. 2017

25 Irwin ML, Cartmel B, Gross CP, et al. Randomized Exercise Trial of Aromatase Inhibitor–

Induced Arthralgia in Breast Cancer Survivors. JCO 2015;33:1104–11.

doi:10.1200/JCO.2014.57.1547

26 Kampshoff CS, Dongen JM, Mechelen W, et al. Long-term effectiveness and cost-effectiveness of high versus low-to-moderate intensity resistance and endurance exercise interventions among cancer survivors. 2018;:1–13. doi:10.1007/s11764-018-0681-0

1 Silver JK, Baima J. Cancer Prehabilitation. American Journal of Physical Medicine &

Rehabilitation 2013;92:715–27. doi:10.1097/PHM.0b013e31829b4afe

478 479 480

481 482 483 484

485 486 487 488 489 490 491 492 493 494 495 496 497

498 499 500

501 502 503

504 505 506

507 508 509 510 511

512 513 514

515

516

517

518

2 Hijazi Y, Gondal U, Aziz O. A systematic review of prehabilitation programs in abdominal cancer surgery. International Journal of Surgery 2017;39:156–62. doi:10.1016/j.ijsu.2017.01.111 3 Driessen EJ, Peeters ME, BONGERS BC, et al. Effects of prehabilitation and rehabilitation

including a home-based component on physical fitness, adherence, treatment tolerance, and recovery in patients with non-small cell lung cancer: A systematic review. Critical Reviews in Oncology / Hematology 2017;114:63–76. doi:10.1016/j.critrevonc.2017.03.031

4 Kessels E, Husson O, Van der Feltz-Cornelis CM. The effect of exercise on cancer-related fatigue in cancer survivors: a systematic review and meta-analysis. NDT 2018;Volume 14:479–94.

doi:10.2147/NDT.S150464

5 Stout NL, Baima J, Swisher AK, et al. A Systematic Review of Exercise Systematic Reviews in the Cancer Literature (2005-2017). PM&R 2017;9:S347–84. doi:10.1016/j.pmrj.2017.07.074 6 Mishra SI SRSCGPBDTO. Exercise interventions on health-related quality of life for people with

cancer during active treatment (Review). 2012;:1–447.

7 Jones LW, Habel LA, Weltzien E, et al. Exercise and Risk of Cardiovascular Events in Women With Nonmetastatic Breast Cancer. JCO 2016;34:2743–9. doi:10.1200/JCO.2015.65.6603 8 Cormie P, Zopf EM, Zhang X, et al. The Impact of Exercise on Cancer Mortality, Recurrence,

and Treatment-Related Adverse Effects. Epidemiologic Reviews 2017;39:71–92.

doi:10.1093/epirev/mxx007

9 Schmitz KH, Courneya KS, Matthews C, et al. American College of Sports Medicine roundtable on exercise guidelines for cancer survivors. 2010. 1409–26. doi:10.1249/MSS.0b013e3181e0c112 10 Blaney JM, Lowe-Strong A, Rankin-Watt J, et al. Cancer survivors' exercise barriers, facilitators

and preferences in the context of fatigue, quality of life and physical activity participation: a questionnaire-survey. Psycho-Oncology 2011;22:186–94. doi:10.1002/pon.2072

11 van Waart H, van Harten WH, Buffart LM, et al. Why do patients choose (not) to participate in an exercise trial during adjuvant chemotherapy for breast cancer? Psycho-Oncology 2015;25:964–

70. doi:10.1002/pon.3936

12 Huber M, van Vliet M, Giezenberg M, et al. Towards a ‘patient-centred’ operationalisation of the new dynamic concept of health: a mixed methods study. BMJ Open 2016;6:e010091–12.

doi:10.1136/bmjopen-2015-010091

13 Velthuis MJ, Peeters PH, Gijsen BC, et al. Role of Fear of Movement in Cancer Survivors Participating in a Rehabilitation Program: A Longitudinal Cohort Study. YAPMR 2012;93:332–8.

doi:10.1016/j.apmr.2011.08.014

14 Timmerman JG, Dekker-van Weering MGH, Tönis TM, et al. Relationship between patterns of daily physical activity and fatigue in cancer survivors. Eur J Oncol Nurs 2015;19:162–8.

doi:10.1016/j.ejon.2014.09.005

15 Wolvers MDJ, Bussmann JBJ, Bruggeman-Everts FZ, et al. Physical Behavior Profiles in Chronic Cancer-Related Fatigue. 2018;:1–8. doi:10.1007/s12529-017-9670-3

16 Steiner WA, Ryser L, Huber E, et al. Use of the ICF model as a clinical problem-solving tool in physical therapy and rehabilitation medicine. Physical Therapy 2002;82:1098–107.

17 van Waart H, Stuiver MM, van Harten WH, et al. Effect of Low-Intensity Physical Activity and

519 520

521 522 523 524

525 526 527

528 529 530 531

532 533 534 535 536 537 538

539 540 541

542 543 544

545 546 547

548 549 550

551 552 553 554 555

556 557

558

Fitness, Fatigue, and Chemotherapy Completion Rates: Results of the PACES Randomized Clinical Trial. J Clin Oncol 2015;33:1918–27. doi:10.1200/JCO.2014.59.1081

18 Jones LW, Courneya KS, Fairey AS, et al. Effects of an oncologist’s recommendation to exercise on self-reported exercise behavior in newly diagnosed breast cancer survivors: a single-blind, randomized controlled trial. Annals of Behavioral Medicine 2004;28:105–13.

doi:10.1207/s15324796abm2802_5

19 Schmitz, K. H., Campbell, A. M., Stuiver, M. M., Pinto, B. M., Schwartz, A. L., Morris, G. S., et al. (2019). Exercise is medicine in oncology: Engaging clinicians to help patients move through cancer. CA: a Cancer Journal for Clinicians, 69(6), 468–484. http://doi.org/10.3322/caac.21579 20 Buffart LM, Kalter J, Sweegers MG, et al. Effects and moderators of exercise on quality of life

and physical function in patients with cancer: An individual patient data meta-analysis of 34 RCTs. Cancer Treatment Reviews 2017;52:91–104. doi:10.1016/j.ctrv.2016.11.010

21 Stout NL, Binkley JM, Schmitz KH, et al. A prospective surveillance model for rehabilitation for women with breast cancer. Cancer 2012;118:2191–200. doi:10.1002/cncr.27476

22 Silver JK, Baima J, Mayer RS. Impairment-driven cancer rehabilitation: an essential component of quality care and survivorship. CA: A Cancer Journal for Clinicians 2013;63:295–317.

doi:10.3322/caac.21186

23 de Vreede PL, Samson MM, van Meeteren NLU, et al. Functional-task exercise versus resistance strength exercise to improve daily function in older women: a randomized, controlled trial. J Am Geriatr Soc 2005;53:2–10. doi:10.1111/j.1532-5415.2005.53003.x

24 Rijpkema C, Van Hartingsveldt M, Stuiver MM. Occupational therapy in cancer rehabilitation:

going beyond physical function in enabling activity and participation. Expert Review of Quality of Life in Cancer Care 2018;00:1–3. doi:10.1080/23809000.2018.1438844

25 Dutch National Guideline 'Cancer Rehabilitation’: modular revision 2017. Netherlands Comprehensive Cancer Organization. 2017

26 Irwin ML, Cartmel B, Gross CP, et al. Randomized Exercise Trial of Aromatase Inhibitor–

Induced Arthralgia in Breast Cancer Survivors. JCO 2015;33:1104–11.

doi:10.1200/JCO.2014.57.1547

27 Kampshoff CS, Dongen JM, Mechelen W, et al. Long-term effectiveness and cost-effectiveness of high versus low-to-moderate intensity resistance and endurance exercise interventions among cancer survivors. 2018;:1–13. doi:10.1007/s11764-018-0681-0

28 Mugele H, Freitag N, Wilhelmi J, et al. High-intensity interval training in the therapy and aftercare of cancer patients: a systematic review with meta-analysis. J Cancer Surviv 2019;23:3633–19. doi:10.1007/s11764-019-00743-3

29 Campbell, K. L., Winters-Stone, K. M., Wiskemann, J., May, A. M., Schwartz, A. L., Courneya, K. S., et al. (2019). Exercise Guidelines for Cancer Survivors: Consensus Statement from

International Multidisciplinary Roundtable. Medicine & Science in Sports & Exercise, 51(11), 2375–2390. http://doi.org/10.1249/MSS.0000000000002116

30 Basen-Engquist K, Alfano CM, Maitin-Shepard M, et al. Moving Research Into Practice:

Physical Activity, Nutrition, and Weight Management for Cancer Patients and Survivors. NAM Perspectives 2018;8. doi:10.31478/201810g

560 561

562 563 564 565

566 567 568

569 570 571

572 573

574 575 576

577 578 579

580 581 582

583 584 585 586 587 588 589 590 591 592 593

594

595

596

597

598

599

600

31 Passchier E, Stuiver MM, Molen L, et al. Feasibility and impact of a dedicated multidisciplinary rehabilitation program on health-related quality of life in advanced head and neck cancer patients Ellen Passchier, Martijn M. Stuiver, Lisette van der Molen, Stefanie I. C. Kerkhof, Michiel W. M.

van den Brekel, et al. Eur Arch Otorhinolaryngol 2015;:1–13. doi:10.1007/s00405-015-3648-z

601

602

603

604

605