Professional Documents
Culture Documents
2013;47(3):170---178
www.elsevier.es/rh
REVIEW
a
Physical and Rehabilitation Medicine Department, Alto Ave Hospital Centre, Guimarães, Portugal
b
Physical and Rehabilitation Medicine Department, Porto Hospital Centre, Porto, Portugal
KEYWORDS Abstract
Cancer; Objective: The incidence of oncological diseases as well as the survival rates of cancer patients
Exercise; has risen in recent years. Cancer-related research has also increased, particularly with respect
Oncology; to the role of exercise. We performed a review of the literature on exercise prescription in
Physical activity oncology patients.
Materials and methods: A search was conducted in reference textbooks and electronic
databases.
Results: Exercise bestows benefits to oncology patients with respect to fatigue, functional and
physical performance. In addition, exercise exhibits promising effects in the maintenance of the
body composition, metabolism, immune and psychological functioning. International Societies
recommend 30 min of moderate aerobic physical activity at least five times per week, strength
training three times per week, and flexibility exercises. Exercise must be prescribed on an
individual basis, taking age, previous activity level, tolerance to exertion, diagnosis, disease
stage, therapeutic approach, and the patients’ comorbidities into account.
Conclusions: Exercise plays an important role as an adjuvant of oncological treatment.
© 2012 Elsevier España, S.L. and SERMEF. All rights reserved.
∗ Corresponding author.
E-mail address: mjazevedo@net.sapo.pt (M.J. Azevedo).
0048-7120/$ – see front matter © 2012 Elsevier España, S.L. and SERMEF. All rights reserved.
http://dx.doi.org/10.1016/j.rh.2013.04.002
Exercise prescription in oncology patients: General principles 171
Las sociedades internacionales recomiendan 30 min de actividad física aeróbica moderada, por
lo menos 5 veces a la semana, entrenamiento de fuerza 3 veces por semana, y ejercicios
de flexibilidad. El ejercicio debe ser prescrito en una base individual, teniendo en cuenta la
edad, el nivel de actividad anterior, la tolerancia al esfuerzo, el diagnóstico, el estadio de la
enfermedad, el enfoque terapéutico, y las comorbilidades de los pacientes.
Conclusiones: El ejercicio juega un papel importante como adyuvante del tratamiento
oncológico.
© 2012 Elsevier España, S.L. y SERMEF. Todos los derechos reservados.
Data were collected from the Guidelines for oncologic exer- Fatigue
cise prescription of the ACSM (American College of Sports
Medicine) and the ACS (American Cancer Society) and from Cancer-related fatigue is a complex, multifactorial, and
reference textbooks: Delisa’s Physical Medicine & Rehabili- poorly understood phenomenon. Nevertheless, there is
tation. strong evidence that exercise reduces fatigue in patients
In addition, the electronic databases PubMed, Science with oncological diseases, including patients subjected to
Direct, EMBASE and Scopus were searched to identify intensive treatment or with advanced disease. This exercise
mainly review articles using the terms ‘‘cancer exercise effect is consistent whether the exercise is supervised or
172 M.J. Azevedo et al.
not, whether aerobic or resistance training, and whether it Several studies demonstrate that exercise helps main-
occurs during or after oncological treatment.14---16 taining the flexibility and mobility of the shoulders and
upper limbs18---20 and did not observe a significant difference
Insulin regulation in the triggering or exacerbation of lymphedema.5
Several studies in animal and human models have demon- Pre-exercise assessment
strated that endurance training bestows protection against
cancer by increasing the activity of macrophages and Natural Exercise is usually a safe and well-tolerated activity
killer cells.12 for oncology patients both during and after adjuvant
The hypothesis that exercise might induce immunity in treatment.1,23
oncological patients has been the target of countless stud- Cancer patients are generally elderly, exhibit a large
ies, however, the results are controversial. number of comorbidities, and are subjected to a large
number of loco-regional and systemic cytotoxic treatments
that can increase the risk of complications associated with
Bone mineral density
exercise.23
A careful clinical history and physical examination seek-
Reductions in bone mineral density have been documented ing cardiac, respiratory, neurological (including screening
in breast and prostate cancer survivors. The benefits of load- of peripheral neuropathies), and musculoskeletal assess-
bearing exercise in the maintenance and improvement of ment as well as laboratory tests comprising complete blood
the bone mass of non-oncological individuals has been well count, lipid profile, and pulmonary function tests ensure
established. However, studies with cancer populations are the safety of the exercise practise or point out the need
few, and their results are contradictory. Further research in to perform a more thorough investigation.4,9 For individuals
this area is needed.12 who received hormone therapy, evaluation of fracture risk
is recommended.9
Upper limbs function Most of the haematological parameters of exercise
are empirical. Thrombocytopenia are associated with the
Oncological treatments that include axillary dissection and increase in blood pressure that occurs during isometric exer-
irradiation of the upper limbs predispose patients to impair- cise, which can result in intracranial haemorrhage, and with
ment of upper limb function and lymphedema. Traditionally, the risk of intra-articular haemorrhage inherent to high-
such patients are oriented to avoid hard labour and intense impact activities.3 Therefore, exercise can be performed
exercise involving the affected limb due to a putative risk of without any restriction if the patient has a platelet count
increasing lymphedema. However, the evidence supporting above 50,000/L, and aerobic (but not resistance) train-
this practice is limited. ing might be performed with counts above 10,000/L. Any
Exercise prescription in oncology patients: General principles 173
modality of active exercise is contraindicated with platelet aerobic, resistance, and flexibility training according to the
counts below 10,000/L.3,5,9 FITT principle (Frequency, Intensity, Type, and Time).
Patients subjected to chemotherapy with cardiotoxic Such recommendations, which are listed in Table 1, agree
agents, namely anthracyclines can develop permanent heart with the ones by ACS24 as well as with those by Courneya
alterations that affect their physical performance. In such et al.25 for patients in the initial stages of cancer without
patients, assessment of cardiovascular function, including other comorbidities.
stress tests, is of paramount importance to define their exer- There is no sufficient evidence supporting precise guide-
cise programmes.3 lines for exercise prescription for each different type of
Additional tumour site-specific assessment is also rec- cancer. However, ACSM gives some recommendations for
ommended: breast cancer survivors should have arm patients with breast (supervised resistance exercise pro-
and shoulder mobility assessed; prostate cancer survivors gramme and progress slowly), colon (lower resistance and
require detailed evaluation of muscle strength and wasting; slower progression), gynecologic (additional supervision)
colon cancer survivors who have an ostomy need practices and hematologic cancer (aerobic exercise is recommend
for management of infection risk; obese survivors (spe- starting with lighter intensity and slower progression).5,9
cially pertinent for the endometrial cancer population) may The frequency of exercise corresponds to the num-
require additional clearance and supervision.9 ber of times it is practised per week. Aerobic exercise is
recommended4,25 three to five times per week, and its pro-
gression must be adjusted to the side effects of treatment
Stress test performance (e.g. daily and shorter sessions). Resistance training is rec-
ommended two to three times per week on non-consecutive
Stress tests are not indicated in all patients, but they are days, and flexibility training is recommended 2---7 days per
especially important in those patients treated with car- week, ideally before and after the other modalities of exer-
diotoxic agents or who have underlying heart disease. In such cise.
cases, it is useful to establish the training HR. The intensity of exercise can be easily explained to the
In spite of the lack of consensus on the safety of the stress patients using the talk test, whereby moderate exercise
test and training in oncological patients, a set of guidelines does not interfere with conversation, whereas vigorous exer-
for this population based on current evidence and clinical cise impedes conversation.
experience has been established.4 The methods used to establish the intensity of exercise
Such guidelines are explicitly conservative and do not include HR monitoring, subjective perception of exertion
necessarily apply to all cancer patients given their wide indi- as reported by the patients, maximal oxygen consump-
vidual variability. However, these guidelines have paramount tion (VO2 max), oxygen consumption at rest, and metabolic
importance for healthcare professionals with respect to the equivalents (METs).4 It is worth observing that the first are
stress test performance and exercise prescription.4,9 more easily applied.
The stress test protocols applied to the overall population The calculation of the training HR can be performed using
(generally the Bruce protocol) are as a whole also appro- the formulas described in Fig. 1, or they can be based on per-
priate for the oncological population. Some modifications centages of the maximal HR (HRmax), which is estimated
may be required as a function of comorbidities, symptoms using the formula for age-predicted maximal heart rate
specifically related with the disease, or the side effects of (APMHR) (Fig. 1) or based on the stress test.4 The heart rate
treatment.4,9 reserve (HRR) is calculated using Karvonen formula (Fig. 1).4
In the case of elderly patients or patients with advanced The most widely used method to assess the subjective
disease, in whom the main aim of exercise is to increase or perception of exertion is the Borg scale, whose score must
to maintain their ability to perform everyday activities, less vary between 11 and 14 (light to somewhat hard).25
demanding protocol (Naughton or Balke-Ware protocols) or Exercise is rated light when it uses less than 3 METs, mod-
submaximal tests may be more appropriate.4 erate when between 3 and 6 METs, and vigorous when more
The test modality must take into account the specifici- than 6 METs.4
ties of disease and the limitations imposed by treatment The ACSM recommends oncology patients exercise at an
(e.g. patients subjected to rectal or prostatic surgery intensity between 40 and 60% of their HRR and VO2 reserve
or radiation, treadmills are more appropriate than cycle (VO2 R), whereas Courneya et al.25 advocate a percentage
ergometers).4
Table 1 Exercise prescription for oncological patients. Adapted from the ACSM and ACS guidelines4,5 and Courneya et al.25
Frequency Intensity Time Type
ACS
Aerobic training 5 or more days/wk Moderate-to-vigorous At least 30′ (45′ to 60′ Daily usual activities
physical activity of intentional using the major
physical activity are muscle groups
preferable)
Courneya et al.
Aerobic training 3---5 days/wk • 50---75% HRR/VO2 R At least 20′ to 30′ Long-lasting and
• 60---80% HRmax continuously/session rhythmic, using the
• Borg 11---14 major muscle groups
(walking, bicycle,
swimming)
ACSM
Aerobic training 3---5 days/wk • 40 to <60% 20′ to 60′ /session Long-lasting and
VO2 max/HRR (interrupted rhythmic, using the
whenever needed) major muscle groups
(walking, bicycle,
swimming)
Resistance training 2---3 days/wk (with 40---60% 1RM 1---3 sets of 8---12 Elastic bands,
48-h recovery) repetitions per weights, resistance
exercise to a machines, weight
maximum of 15 lifting in functional
repetitions in tasks, major muscle
deconditioned groups
individuals or with
fatigue.
Flexibility training 2---7 days/wk Slow and static 4 repetitions of 10′′ to Elongation of all the
stretching 30′′ per elongation major muscle groups
with attention to
areas with limitations
due to treatment
Abbreviations: wk, week; HRR, heart rate reserve; VO2 R, maximum oxygen consumption reserve; VO2 max, maximum oxygen consump-
tion; HRmax, maximal heart rate; MR, maximal repetition.
of HRR and VO2 max rates corresponding to 50---75% and of less than 60 min, and flexibility training must include muscle
HRmax between 60% and 80%.4,26 Several studies defend elongations for 10---30 s repeated 2---4 times.4 The majority
that high intensity exercise tended to increase DNA dam- of studies emphasised long term (>6 months) interventions
age, so data suggest that exercise in cancer survivors might to produce benefits.2
warrant a focus on moderate-intensity, rather than vigorous Progression is defined as the rate of increase of the fre-
activities.2 quency, intensity and duration of exercise from the initial
Walking is the type of exercise preferred by most peo- to the maintenance stages. Progression varies according to
ple. However, the static bicycle might be more appropriate numerous factors, including the aims of exercise, tolerance
for individuals with gait or coordination disorders.24 Aquatic to exertion, and age. Patients undergoing oncological treat-
exercise might be an excellent solution in such cases, but ment recover in a poorly predictable and often non-linear
it should be avoided by patients with nephrostomy tubes, manner. The progression of such patients can vary accord-
central venous access devices, or urinary catheters. Sim- ing to multiple factors, including the treatment protocol,
ilarly, aquatic exercise must also be avoided by patients oscillating cell counts, and abnormal symptoms. Therefore,
with white blood cells counts below 0.5 × 109 /L due to risk the prescribed exercise may not always be tolerated and
of bacterial infection.25 Survivors subjected to radiotherapy may even be contraindicated on some days. There are no
must avoid exposing irradiated skin to chlorine.25 The static recommendations for the progression of exercise in onco-
bicycle should not be prescribed after prostate or rectal logical patients. Nevertheless, Courneya et al.25 describe
surgery and patients with bone metastases or osteoporosis some principles for patients during the initial stage of dis-
risk should avoid high impact or contact activities.4 ease. They suggest that the frequency and length goals must
The duration of aerobic exercise should be between 20 be met first and only then should intensity be increased.
and 60 min per session. The duration can be modified over Those authors further advocate that progression must be
the progression of the exercise programme or as a function slower and more gradual in patients without physical condi-
of the treatment side effects (e.g. several exercise periods tioning and in patients exhibiting important treatment side
separated by resting intervals). Resistance training must last effects.
Exercise prescription in oncology patients: General principles 175
Resistance training is essential to increase muscle mass greater as the minimum goals are surpassed. Such benefits
and avoid strength impairment in all cancer patients. can be achieved by means of variations in the intensity, fre-
Cachectic patients or those in whom aerobic exercise is con- quency, duration, and type of exercise every 2---3 weeks23
traindicated must give preference to resistance training.23 (Fig. 2).
The decision of when to start this modality depends on indi- Patients who do not follow the ACSM guidelines (Table 1)
vidual needs. must start the exercise programme following an initial indi-
Resistance training might initially comprise resistance vidualised prescription. When they exhibit tolerance to the
exercises using elastic bands, free weights (0.5---2 Kg), or initial prescription, the frequency and duration might be
medicine balls. Patients who are physically able to per- increased 2---3 weeks later. Resistance training and exercise
form more resistance training must be subjected to muscle variation can be started at least 12 weeks later23 (Fig. 2).
strength assessment. The most widely used method for
assessing muscle strength is one-repetition maximum (1RM),
Recommendations for advanced disease
which corresponds to the maximal amount of weight that
can be lifted at one time. Alternatively, gradually increasing
Although some patients are cured or their disease is steadily
repetitions can be used to establish the training intensity.4
controlled, other patients live with advanced disease.
Resistance training must be performed rhythmically, at a
In such patients, physical activity is important to estab-
slow to moderate speed, extending across the entire avail-
lish or maintain an overall feeling of well-being and quality
able joint amplitude, while maintaining breathing control.
of life,24 but there are few studies exploring these benefits.
The major muscle groups must be trained first, and exer-
Thus, the available evidence does not suffice to make rec-
cises involving the upper and the lower limbs should be
ommendations, which are consequently based on individual
alternated.4
abilities and needs.24
The key to the prescription of effective and safe exer-
cise is the individualisation of programmes to the particular
needs of each patient. Such prescription poses a challenge Neuromuscular electrical stimulation
when the variability of individuals, pathophysiology, ther-
apeutic approaches, and prognoses within the context of Patients too weak to perform any type of physical activity
oncological disease is taken into account. might start transcutaneous neuromuscular electrical stim-
The basis for individualised prescriptions relies on the ulation (NMES), which is easy to perform also in bedridden
current performance of each individual. The patients fol- patients. NMES may also be useful in patients with conditions
lowing ACSM guidelines (Table 1) must be encouraged to that transiently contraindicate intense exercise.26
keep them. However, such guidelines represent the min- After several weeks of use, this method can mimic
imum effort needed to produce benefits, which will be the effects of regular training---muscle hypertrophy and
Present or
previous
physical
performance *
* **
**
(last month)
Initial Progression:
Does not prescription: F: 5/wk
follow ACSM *2-3 wk
F: 3/wk I: moderate
guidelines I: moderate Tp: fast walking
(Table 1) Tp: fast walking Tm: 30’/session
Tm: 20’/session
**
Figure 2 Overall approach to individualised exercise prescription. Adapted from Jones et al.23 Abbreviations: F, frequency; I,
intensity; Tp, type; Tm, time; ACSM, American College of Sports Medicine; *tolerance of prescription; **non-tolerance of prescrip-
tion.
176 M.J. Azevedo et al.
increased capillarisation and type I and II fibres. Such results COPD suggest electrical stimulation of the major muscles
have been observed in patients with chronic obstructive pul- individually or in groups (quadriceps, ischiotibial, gastroc-
monary disease (COPD) and chronic heart failure, in whom nemius, and glutei) using a biphasic current, a frequency
studies demonstrate increases in functional capacity when of stimulation between 10 and 50 Hz (high frequencies
NMES was applied to the femoral quadriceps muscle for 6---8 (>50 Hz) to induce muscle strength gain, and high and low
weeks.26 (<50 Hz) frequencies to increase the oxidative capacity),
There are no specific NMES protocols for oncologi- pulse durations between 300 and 400 s, and cycles varying
cal patients. However, studies performed in patients with between 1:1 and 1:5. However, the ideal levels to achieve
Table 2 Contraindications and precautions for exercise and stress tests in cancer patients.
Factors Contraindications Precautions requiring modifications
Related to oncological treatment • On the day of or up to 24 h • Under treatment with pulmonary or cardiac
after IV ChT; effects: requires medical supervision
• Before blood harvesting; • Aphthous stomatitis: avoid mouthpieces in
• Severe tissue reaction to maximal tests; wear facemask
radiotherapy
Haematological • Platelets <50,000/L; • Platelets 50,000---150,000/L: avoid tests
• Leukocytes <3000/L; with haemorrhage risk
• Haemoglobin <10 g/dL • Leukocytes 3000---4000/L: ensure proper
sterilisation of equipment
• Haemoglobin >10 ---11.5/13.5: care with
maximal tests
Musculoskeletal • Recent bone or spinal pain; • If pain or cramp: investigate
• Uncommon muscle weakness; • Osteopenia: avoid high-risk exercise if risk of
• Extreme cachexia; fracture exists
• Uncommon/extreme fatigue; • Corticoid-induced myopathy
• Poor functional state: avoid • Cachexia: multidisciplinary assessment
stress test if Karnofsky scale • Slight to moderate fatigue: monitor response
(Table 3) ≤60% to exercise
Systemic • Acute infections; • Recent systemic disease or infection: avoid
• Fever >38 ◦ C; exercise until symptoms-free >48 h
• Overall ill feeling
Gastrointestinal • Severe nausea • Altered water or food intake:
• Vomiting or diarrhoea for multidisciplinary assessment/assessment by
24---36 h nutritionist
• Dehydration
• Malnutrition: inappropriate
water/food intake
Cardiovascular • Chest pain; • Attention to risk of cardiovascular disease:
• RHR >100 bpm or <50 bpm; medical supervision of tests and training is
• SAP rest >145 mmHg and/or recommended
DAP rest >95 mmHg; • Undertreatment with anti-hypertensive drugs
• SAP rest <85 bpm; that affect the HR: training HR might not be
• Arrhythmia; achieved
Oedema of LL • Lymphedema: wear compression sleeves in
the affected limb during exercise
Pulmonary • Severe dyspnoea; • Slight to moderate dyspnoea: avoid maximal
• Cough, wheezing; tests
• Chest pain increases with
deep breathing
Neurological • Significant impairment of • Mild cognitive disorders: ensure the patients
cognitive functions; is able to understand and obey commands
• Dizziness/vertigo; • Equilibrium disorders/peripheral sensitive
• Disorientation; neuropathy: employ more stable postures
• Blurred vision; during exercise
• Ataxia
Adapted from ACSM.4,29
Abbreviations: ChT, chemotherapy; IV, intravenous; Karnofsky index (Table 3); RHR, resting heart rate; HR, heart rate; SAP, systolic
arterial pressure; DAP, diastolic arterial pressure; LL, lower limbs.
Exercise prescription in oncology patients: General principles 177
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