Abstract
Introduction
Urinary incontinence, erectile dysfunction, fatigue as well as fears and depression rank among the most common complaints in patients with prostate cancer, resulting in a reduced participation in daily life and social isolation. Consequently, the quality of life of prostate cancer patients is strongly affected in a negative way. Numerous studies focusing on physical exercise interventions in prostate cancers patients demonstrate positive physiological and psychological effects. Our objective was to evaluate the evidence of randomized controlled studies which examined exercise during medical treatment and in the aftercare of a prostate cancer disease.
Methods
Twenty-five randomized controlled trials regarding physical activities in patients with prostate cancer were obtained by systematic literature research (Medpilot). Twenty-one studies examined clinical exercise interventions during the phase of medical treatment (irradiation, pre- and/or post-op, androgen deprivation therapy) and four studies during the aftercare. In order to evaluate the evidence of the included studies, the evaluation system of the Oxford Centre for Evidence-Based Medicine was used. Within this systematic review, we differentiated between “supervised clinical exercise” and “non-supervised clinical exercise.”
Results and discussion
Current data suggest that incontinence, fitness, fatigue, body constitution, and also quality of life can be improved by clinical exercise in patients during and after prostate cancer. Studies were mostly ranked evidence level “2b.” Only four studies, all conducted during medical treatment, reached the level “1b.” It seems to be that “supervised exercise” is more effective than “non-supervised exercise.” For future research, further randomized controlled trials with high methodological quality need to be conducted in order to establish evidence-based recommendations particularly for prostate cancer patients.
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Purpose
The incidence rate of prostate cancer in Germany is currently 60.120 per year. According to data published by the Tumor Register Munich and the Robert Koch Institute, the incidence rate increased by approximately 50% within the past 8 years [1, 2]. Accounting for approximately 25% of all newly diagnosed cancer diseases, the prostate carcinoma is the most common malignant tumor in men. Despite improved treatment regimes, the therapy of prostate cancer is accompanied by numerous side effects. Urinary incontinence is one of the most common complications caused by radical prostate resection [3, 4]. Depending on the tumor stadium, BMI, comorbidity, surgical technique, operative experience of the urologist, assessment method, and definition of incontinence, 5–74% of the operated patients are affected, and unfortunately, some patients will have to live with an irreversible incontinence [5, 6]. The androgen deprivation therapy (ADT), often applied in patients with advanced prostate cancer, can also affect healthy organs, especially those that depend on sex hormones. Since androgens affect the psyche, skin, bones, muscles, and sexual function, most side effects are related to these organ systems [7]. The most common side effects caused by an ADT include missing libido, hot flushes, erectile dysfunction, anemia, and an increase in percent body fat. However, complaints may vary according to the extent of androgen deprivation [7–9]. Muscular strength decreases during and after an androgen deprivation therapy [10, 11]. Studies have also shown that a long-term ADT could increase the risk of a metabolic syndrome [12, 13]. Further side effects of a cancer disease and its medical treatment can be observed on the psychological and psychosocial level. Cancer patients often suffer from anxiety, depression, and sleep disorders [14]. Possible long-term effects of the disease and therapy weaken patients’ self-esteem. Furthermore, motivational and cognitive restrictions like hopelessness, pessimism, reduced mental capacity, and lack of concentration may arise [15], which lead to a reduced participation in activities and social life, difficulties in maintaining relationships and activities with the family, and a reduced earning capacity [15]. Taken together, these aspects bring about a social withdrawal of many cancer patients leading to a negative overall quality of life [16].
Clinical exercise in cancer patients
During the past few years, physical activities or exercise have shown to be safe, feasible, and effective in cancer patients [17, 18]. They can maintain and improve muscle mass and strength, cardiorespiratory fitness, body function, physical activity levels, flexibility, function of the immune system, body image, self-esteem, and mood [18, 19]. In addition, they contribute to less intense and less frequent symptoms and side effects (e.g., nausea, fatigue, pain), shorter duration of hospitalization, less psychological and emotional distress, depression, and anxiety [18, 19]. A positive influence of these aspects will improve quality of life and facilitate daily activities. Additionally, the metabolic and cardiorespiratory effects of exercise are of great importance in the prevention of subsequent diseases such as type 2 diabetes or cardiovascular diseases [19]. Latest investigations with breast, prostate, and bowel cancer patients suggest that mortality and probability of a relapse can be reduced by physical activity [20–22]. First evidence-based exercise recommendations for cancer patients have already been published; however, special recommendations particularly for prostate cancer patients are still missing [18, 23].
Methods
In the following review, we used the term “clinical exercise” and differentiated between “supervised clinical exercise” and “non-supervised clinical exercise” interventions. “Supervised clinical exercise” studies include movement interventions that pursue rehabilitative and curative aims and are always supervised by a therapist/physiologist. Studies with “non-supervised clinical exercise” also involve movement interventions with rehabilitative and curative aims; however, a therapist is not permanently present and in charge, e.g., home-based programs.
Within the following systematic review, our aim was to compile the data currently available on the effects of “supervised clinical exercise” and “non-supervised clinical exercise” (pelvic floor/sphincter training, resistance training, aerobic endurance training) during medical treatment (inpatient post-op, chemotherapy, irradiation, and ADT) as well as during the aftercare of a prostate cancer disease, in order to then evaluate the evidence of these studies:
How profound is the evidence of “supervised and non-supervised clinical exercise” studies in patients with prostate cancer? Through December 2010, literature was acquired using the Medpilot database. Medpilot is a medical information portal that enables the search of literature in different databases (e.g., Medline, CC MED, Cochrane Database of Systematic Reviews, Cochrane Database of Abstracts of Reviews of Effectiveness) with only one query. It is a service of the German National Library of Medicine and the German Institute of Medical Documentation and Information. German and English search terms involving physical activity and prostate cancer were entered in different combinations (prostate cancer or prostatectomy in combination with physical activity, physical exercise, exercise, moving therapy, sports therapy, sports, endurance, aerobic training, resistance training, pelvic floor and pelvic floor exercise). Table 1 contains the inclusion and exclusion criteria for the systematic literature research.
In order to evaluate the evidence of the included studies, we used the evaluation system of the Oxford Centre for Evidence-Based Medicine (OCEBM) since it is commonly used in this context [24, 25]. The evaluation is primarily based on the study’s study design; however, the quality of the study and its results are considered likewise. Usually, the ten evaluation levels are comprised to four levels of recommendation. However, in order to establish reliable levels of recommendation, treatment costs and possible benefits and risks for the patients have to be considered [26]. Since valid data have hardly ever been published or do not yet exist, the levels of recommendation were not included in this review.
The literature research was carried out by two independent researchers. Full-text articles of relevant abstracts were viewed in consideration of the inclusion and exclusion criteria. Finally, 25 studies were included in the following systematic review. Twenty-one randomized controlled trials started during medical treatment, and four randomized controlled trials were performed during the aftercare of prostate cancer (Fig. 1). The identified studies all examined one of the following aims: improving physical fitness (strength, endurance), incontinence, quality of life, fatigue, psychological parameters, and medical side effects. The involved exercising methods included endurance training, resistance training, combined endurance and resistance training, and pelvic floor/sphincter training.
Results
“Supervised clinical exercise” and “non-supervised clinical exercise” studies during medical treatment
Of the 21 included studies involving “supervised clinical exercise” and “non-supervised clinical exercise” interventions during the medical treatment of prostate cancer, 4 studies were conducted during irradiation, 3 during ADT, and 14 with inpatients prior to and/or shortly after surgery (pre- and/or post-op; Table 2). The duration of the interventions and the number of subjects in each study varied strongly. Primarily, physiological and psychological parameters were assessed (see “Methods” Section). While the studies that observed patients during irradiation or ADT chose an aerobic endurance and/or resistance training program [27–33], the remaining 14 studies examined the effects of a pelvic floor and sphincter training in inpatients pre- and/or post-op [34–47].
Resistance training during irradiation showed significant improvement in fatigue, aerobic fitness, muscle strength, and quality of life [27]. Similar results could be observed in prostate cancer patients performing aerobic endurance training during irradiation [27–29]. In addition to that, toxicity scores decreased [30]. However, resistance training brings about more positive effects than endurance training [27]. Quality of life and well-being scores increased [28].
A combination of endurance and resistance training might have positive effects on the exercise behavior of prostate cancer patients during ADT [31]. Blood pressure can be lowered, and an increase in waist and cervical girth can be prevented [32]. Yet, significant improvements in quality of life, fatigue, and fitness seem to only be accomplished by isolated resistance training during ADT [33].
Pelvic floor/sphincter training programs significantly reduce the duration of incontinence [35, 39, 41] and increase the quality of life in patients with prostate cancer [35]. A positive trend concerning the timing of the training can also be observed. Pelvic floor/sphincter training seems to be more effective the earlier it is initiated [38]. Even training sessions prior to surgery are possible and have shown positive effects [36, 37, 41, 45]. Finally, a supervised pelvic floor/sphincter training is assumingly more effective than home-based programs [34].
The current study results regarding the application of biofeedback or electrostimulation techniques to accelerate recovery from incontinence are controversial. Few studies have shown that patients who performed a biofeedback-enhanced pelvic floor/sphincter training had a shorter duration of incontinence than those who did not receive the technical support [36, 44]. However, other studies could not observe a significant effect [46]. Therefore, there seem to be no differences between a biofeedback-enhanced and a “pure” pelvic floor/sphincter training [14, 37, 43]. The application of electrostimulation or magnetic innervation during continence training is controversial as well. While some studies showed a reduced duration of incontinence in patients with prostate cancer due to one of these techniques [40], others could not confirm such an effect [42].
In two of the four studies conducted during irradiation, the interventions were supervised and therefore defined as “supervised clinical exercise” [27, 28]. Of the three studies that examined patients undergoing ADT also two interventions were classified as “supervised clinical exercise” [31, 33]. In 13 of 14 studies that examined the effects of pelvic floor/sphincter training, focusing on the incontinence of prostate cancer patients, at least parts of the training sessions were conducted home-based. The interventions of these 13 studies were classified as “non-supervised clinical exercise.” In one study, the exercise intervention of the training group was completely supervised and the intervention therefore defined as “supervised clinical exercise” [38].
The evaluated evidence levels of the studies which were performed during medical treatment of prostate cancer are shown in Table 2. Of the 21 identified studies, only five studies calculated or published the confidence intervals for their primary endpoints. Therefore, these studies were rated evidence level “1b” [27, 29, 31, 34, 44]. The remaining 16 studies lack this information and therefore had to be downgraded to the level “2b” [28, 30, 32, 33, 35–43, 45–47].
“Supervised clinical exercise” and “non-supervised clinical exercise” studies during aftercare
Four randomized controlled studies involving clinical exercise during the aftercare of a prostate cancer disease were identified (Table 3). All studies examined the effects of a pelvic floor/sphincter training on the incontinence of prostate cancer patients in the aftercare of the disease.
Pelvic floor/sphincter training programs during aftercare significantly reduce incontinence in patients with prostate cancer [48–50]. Similar to the study results mentioned above, a biofeedback-enhanced pelvic floor/sphincter training or the application of electrostimulation does not seem to have significant benefits regarding incontinence or quality of life when compared to a “pure” pelvic floor/sphincter training [48–51].
In all four studies, at least parts of the training sessions were conducted home-based. The interventions were therefore defined as “non-supervised clinical exercise” [48–51].
According to the levels of evidence of the OCEBM, all four identified studies regarding clinical exercise in patients with prostate cancer during aftercare were classified as level “2b” studies. In three studies, the reason for the ranking was based on the missing confidence intervals for the primary endpoints [48–50], while in the fourth study, a low follow-up rate (<80%), and therefore a weak methodological quality, was the decisive factor [51].
Discussion
The current data suggest that clinical exercise in patients with prostate cancer improves incontinence, fatigue, muscle strength, aerobic fitness, flexibility, quality of life, body constitution, blood lipids, and well-being. These positive effects in patients with prostate cancer were observed with regard to resistance and endurance training programs. In a review by Schmitz et al. [23], exercise intervention studies with prostate cancer patients were ranked between category A and B which underlines that exercise is safe during and after treatment. The authors used for categorization the Evidence Levels of the National Heart, Lung, and Blood Institute. Studies with breast cancer patients demonstrate similar positive results [52–54]. The current study situation also confirms that a pelvic floor/sphincter training can shorten the duration of incontinence after prostate resection [35, 36, 39, 41, 44]. Possibly, an additional pelvic floor/sphincter training prior to surgery is more effective than a post-op training alone [47]. In this context, however, study designs differ considerably. The additional application of biofeedback-enhanced techniques or electrostimulation rather than “pure” pelvic floor/sphincter training is still controversial [37, 40, 42, 43, 45]. These results support the data presented in past reviews [55–57] and underline the lack of good evidence. Further studies with high methodological quality are therefore necessary in this field of research [55].
In summary, the evidence for clinical exercise in patients with prostate cancer is rated evidence level “2.” However, it must be considered that the ranking of the studies according to the Oxford Levels of Evidence-Based Medicine was hampered due to missing confidence intervals in most of the studies. Consequently, studies might be under- or overrated. Furthermore, certain subjectivity could not be excluded since many items are described imprecisely and a standardized scheme of weighing these items does not exist. However, all evaluation systems are associated with shortcomings and restrictions [25, 57]. Schmitz et al. [23] used the categories outlined by the National Heart, Lung, and Blood Institute in order to evaluate the evidence of the studies in their review. However, the authors acknowledge that the rating criteria do not involve data about the effect size.
In literature, special recommendations particularly for prostate cancer patients are still missing. First evidence-based exercise recommendations for cancer patients have been published; yet, precise training guidelines including repetitions, duration, frequency etc. cannot be found [62, 63]. The large heterogeneity of the included studies makes it very difficult to define evidence-based recommendations. It is challenging to compare the clinical exercise programs of the single studies because, at least partly, they differ substantially in terms of intervention, duration, dosage, exercise choice, in- and exclusion criteria, outcomes or also patient supervision, an aspect that also influences the clinical effects. Home-based programs of pelvic floor/sphincter exercises, for example, show smaller effects than supervised programs [34, 36, 38, 41]. Interestingly, these effects were primarily found in studies that were published after 2003. Possibly, the method, duration, frequency, etc. of pelvic floor/sphincter training programs changed over the past few years because no significant differences between home-based and supervised pelvic floor/sphincter training programs could be determined in the studies published before 2003 [43, 45, 46, 48].
The frequently quoted sentence “sport is healthy” has to be qualified given that “exercise therapy” should not be mistaken with “sport.” We considered this aspect in our systematic review by differentiating between “supervised clinical exercise” and “non-supervised clinical exercise” (see “Methods” Section) and actually found that “supervised clinical exercise” could be more effective. To date, not much is known about what kind of exercise should be chosen, when clinical exercise should begin, or how long or intensive a patient should exercise [58]. We know that clinical exercise can effectively help prostate cancer patients; however, precise recommendations are still missing. Future research should pay more attention to therapeutic contents and concepts.
Based on the findings of our systematic review, we defined, possibly for the first time, special recommendations for exercising with prostate cancer patients (Table 4). We differentiated between PFST and endurance training and resistance training. However, these recommendations cannot be considered as evidence-based because further studies are necessary.
In this review, not only the clinical exercise interventions of the different studies are heterogeneous but also the applied assessment methods that generate the observed effects and impacts. An overall evaluation of the clinical exercise studies is therefore limited. Both the calculation of total effects as well as the realization of a meta-analysis would not be meaningful. A further unavoidable limitation of this review is the literature research. Despite the fact that a comprehensive research was performed, certainly not all relevant studies were found. Moreover, the evidence-based evaluation was challenging because the determined results may vary considerably depending on the applied evaluation system [25, 59, 60].
Nevertheless, this review—as well as similar reviews in this context—provides evidence that clinical exercises such as pelvic floor/sphincter exercises and endurance or resistance training programs are seemingly important for the health status and rehabilitation of patients with prostate cancer [11, 55–57, 61, 62]. Due to the various types of interventions, different assessment methods and endpoints of the currently published studies, fundamental and comprehensive clinical exercise recommendations cannot yet be defined.
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Acknowledgments
We would like to thank Krebsgesellschaft NRW e.V. and Barmer GEK Health Insurance Company for the support of this systematic review.
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The authors declare no conflict of interest.
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Baumann, F.T., Zopf, E.M. & Bloch, W. Clinical exercise interventions in prostate cancer patients—a systematic review of randomized controlled trials. Support Care Cancer 20, 221–233 (2012). https://doi.org/10.1007/s00520-011-1271-0
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DOI: https://doi.org/10.1007/s00520-011-1271-0