OBJECTIVE:

To investigate the effectiveness of an 8-week aquatic program on cancer-related fatigue, as well as physical and psychological outcomes in breast cancer survivors.

DESIGN:

A randomized controlled trial.

SETTING:

Outpatient clinic, urban, academic medical center, and a sport university swimming pool.

PARTICIPANTS:

Breast cancer survivors (N=68) were randomly assigned to either an experimental (aquatic exercise group in deep water pool) group or a control (usual care) group.

INTERVENTIONS:

The intervention group attended aquatic exercise sessions 3 times per week for 8 weeks in a heated deep swimming pool. Sessions lasted 60 minutes in duration: 10 minutes of warm-up, 40 minutes of aerobic and endurance exercises, and 10 minutes of cool-down exercises. Patients allocated to the usual care group followed the oncologist's recommendations in relation to a healthy lifestyle.

MAIN OUTCOME MEASURES:

Values for fatigue (Piper Fatigue Scale), mood state (Profile of Mood States), and abdominal (trunk curl static endurance test) and leg (multiple sit-to-stand test) strength were collected at baseline, after the last treatment session, and at a 6-month follow-up.

RESULTS:

Immediately after discharge, the aquatic exercise group showed a large effect size in total fatigue score (d=.87; 95% confidence interval, .48-1.26), trunk curl endurance (d=.92; 95% confidence interval, 1.97-3.83), and leg strength (d=1.10; .55-2.76), but negligible effects in vigor, confusion, and disturbance of mood (d<.25). At the 6-month follow-up period, the aquatic exercise group maintained large to small effect sizes in fatigue scores, multiple sit-to-stand test, and trunk curl static endurance (.25>d>.90) and negligible effects for the fatigue-severity dimension and different scales of the Profile of Mood States (d<.25).

CONCLUSION:

An aquatic exercise program conducted in deep water was effective for improving cancer-related fatigue and strength in breast cancer survivors.

Cancer-related fatigue (CRF) is mainly characterized by tiredness to exhaustion that is not precipitated by activity. It can also occur after activity if it is out of proportion to the level of exertion and is not relieved by or in fact may be worsened with rest.¹ Between 56% and 95% of breast cancer survivors experience CRF after treatment.² Close to 20% of breast cancer survivors can suffer CRF several years after finishing their curative treatment.^{3, 4} A moderate to high level of CRF is associated with reduced quality of life in these patients^{1, 5, 6, 7} and is perceived as a barrier to include exercise in their lifestyle,⁸ justifying the need to seek different methods of treatment for these patients.

Previous research has investigated the effects of exercise as nonpharmacologic treatment for CRF,^{9, 10, 11} with clinical impact ranging from small to moderate effect sizes on CRF.^{10, 11, 12} There continues to exist limited research examining the effects of exercise for patients with cancer who experience CRF.^{7, 12, 13} New studies are necessary to identify optimal treatment options for individuals with CRF to improve their quality of life.

A potential contributor to CRF may be abnormalities of energy balance,¹⁴ which are associated with diminution of muscle biosynthesis.¹⁵ These deficits are sensitive to neuromuscular measures of skeletal muscle endurance.¹⁶ In fact, deficits in muscular performance are associated with a reduction in the quality of life and increase in symptoms related to cancer in breast cancer survivors.^{17, 18}

Previous research has mainly focused on land-based exercise programs, but many benefits can be obtained with the aquatic environment. Different properties of water such as buoyancy, which significantly decreases the stress on weight-bearing joints, bones, and muscles, thereby reducing pain, can increase the potential benefits of exercise.¹⁹ Water immersion decreases axial loading, allowing patients to perform exercises that they are otherwise unable to do on land.²⁰ Different resources can be used in aquatic therapy. A chest-high pool is used to reduce pain and stiffness during weight-bearing exercise. A recent report²¹ found that water exercise in a chest-high pool had no effect on CRF in breast cancer survivors suffering from hormone therapy–associated arthralgia pain. Exercises such as running in deep water produce a lower heart rate, which may relate to hydrostatic pressure and water depth and the subsequent increase in venous return and stroke volume.²² These physiological responses result in lower perceived exertion than would be experienced with the same exercise intensity conducted on land.²³ It is not known whether an aquatic exercise program could result in reductions in CRF.

Exercise has shown the ability to reduce depression²⁴ and anxiety²⁵ and improve mood²⁶ state in breast cancer survivors. Aquatic group exercise interventions have also been shown to improve the psychological state in several conditions.^{27, 28} To the best of our knowledge, there are no studies reporting psychological effects of aquatic exercise in breast cancer survivors. We hypothesized that an exercise program in deep water could improve the physical and psychological states in fatigued breast cancer survivors.

Thus, the purpose of the present clinical trial was to analyze the effects of an 8-week aquatic exercise program in a deep water pool and 6 months after finishing the program on fatigue, psychological outcomes, muscular strength, and endurance in breast cancer survivors.

During the study period, 126 women with cancer agreed to attend the prescreening session (fig 1). No differences between 68 patients (54%) included and 58 patients (46%) who were excluded or declined to participate were found, except that the excluded group was older (48 vs 55y; P<.05). Furthermore, no differences in sociodemographic and medical features between the patients assigned to exercise and control groups were identified (table 2). There were also no differences in variables at baseline between groups (table 3). Seven patients were not assessed at 6 months for different reasons (see fig 1). Thirty-four patients finished the aquatic exercise program and completed 84% of the 24 physical therapy sessions (mean ± SD, 20±4 sessions). Adverse effects reported during the study included discomfort or low-intensity pain/stiffness after an exercise session in 3 patients; nevertheless, they continued the program.

Fig 1

Flow diagram of subject recruitment and retention throughout the course of the study.

 

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This study found that an 8-week supervised aquatic exercise program in deep water decreased fatigue and improved leg-abdominal muscle endurance and several aspects of mood state such as tension, depression, anger, and mental fatigue in breast cancer survivors suffering moderate CRF. The effects were maintained at 6 months after discharge except for mood state.

Our results are similar to findings of previous research examining the effects of exercise on fatigue^{13, 35, 36} and confirm suggestions provided by clinical guidelines about the effects of exercise on fatigue.^{9, 37, 38} However, we reported a large effect size that is not consistent with a previous meta-analysis reporting small to moderate effect sizes.^{12, 39} The larger effect size in the current trial could be related to our selected population that had a moderate to high level of CRF, allowing for a greater margin of improvements. This study helps to reduce the gap in the literature about the effectiveness of supervised exercise programs in a subgroup of patients with special requirements or at risk to develop other symptoms associated with CRF.⁶ It has recently been reported that there was no benefit from a water exercise program in a chest-high pool for CRF in breast cancer survivors suffering from hormone therapy–associated arthralgia pain.²¹ Current results were obtained with an exercise program in a deep water pool including aerobic/endurance exercise as a principal component (70% of each session), which could require more exertion than exercises in a chest-high pool with reduced cardiovascular demands (20% of each exercise session). It is possible that the decreased stress on weight-bearing joints and decreased axial loading facilitated aquatic exercise. Aquatic exercise could improve the fitness level of participants, which is known as one of the pillars to attenuate CRF.^{5, 7} Hydrostatic pressure during water exercise redistributes blood from the limbs to the thoracic cavity; this redistribution may have reduced the heart rate and transiently increased the blood pressure.⁴⁰ Unfortunately, we did not use a heart rate monitor during immersion to provide support to these speculations. Future studies in a larger and multisite sample are recommended to determine the physiological adaptations during water exercise in breast cancer survivors.

The results of the current study also showed significant and clinical improvements in leg and abdominal muscle strength. The decreased muscle function in cancer survivors during and after the oncology treatment is well known.^{6, 41, 42} This reduced force had been associated with an increase in CRF and reduction in quality of life.^{17, 18} Recent research provides support to the positive influence of aerobic and strength training exercise interventions in breast cancer survivors mediated by different physiological responses such as decreases in insulin levels,⁴³ reduction in C-reactive protein levels,⁴⁴ or an increase in the adiponectin/leptin ratio.⁴⁵ Large effect sizes in muscle strength were reported in our study and could possibly be linked to the resistance effects offered by water. We used an increase in the velocity of movement during the exercises as a major component of progression with intensity of the exercise with less joint stress as compared with land-based exercise.⁴⁶ Future studies should be carried out to determine the effect of these types of programs on muscle metabolism (ie, adenosine triphosphate and cytokines dysregulation, deprivation of satellite cells) associated with oncology treatment⁴⁷ to promote the maintenance of muscle mass.

The reduction in CRF and the increase in strength reported in the current study are similar to recent studies that have demonstrated that fitness improves quality of life by reducing CRF in breast cancer survivors.⁴⁸ Our results give preliminary support to the implementation of aquatic exercise programs to promote the recovery of functional limitations following initial breast cancer treatment that have been associated with an important reduction in all-cause and competing-cause survival.⁴⁹

The current results on mood state partially agree with the results from previous studies using a land-exercise approach.²⁶ The reported psychological positive effects of aquatic exercise could help to explain the reduction in CRF of our population. Exercise facilitators were included in this aquatic exercise program being group-based, high therapist/patient supervision ratio (1 therapist for each 5–7 patients), individually tailored, and gradually progressed. These exercise motivators can be related to self-perceived exercise benefits.⁸ Relief of CRF and improvement in strength reported in this study may improve the patients’ ability to perform daily activities and to interact with others.⁵⁰ These improvements in the relationship between survivors and proxy environment could help to improve several aspects of mood state as identified in this trial.

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  SPSS, version 19.0; SPSS, Inc, 233 S Wacker Dr, 11th Floor, Chicago IL 60606.