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Long-term follow-up after cancer rehabilitation using high-intensity resistance training: persistent improvement of physical performance and quality of life

Long-term follow-up after cancer rehabilitation using high-intensity resistance training:... Clinical Studies British Journal of Cancer (2008) 99, 30 – 36 & 2008 Cancer Research UK All rights reserved 0007 – 0920/08 $30.00 www.bjcancer.com Long-term follow-up after cancer rehabilitation using high-intensity resistance training: persistent improvement of physical performance and quality of life ,1 2 2 3 4 1 IC De Backer , G Vreugdenhil , MR Nijziel , AD Kester , E van Breda and G Schep 1 2 Department of Sports Medicine, Ma´xima Medical Centre, Veldhoven, The Netherlands; Department of Internal Medicine, Ma´xima Medical Centre, Veldhoven and Eindhoven, The Netherlands; Department of Methodology and Statistics, Maastricht University, Maastricht, The Netherlands; Department of Movement Science, Nutrition and Toxicology Research Institute Maastricht (NUTRIM), Maastricht University, Maastricht, The Netherlands The short-term beneficial effects of physical rehabilitation programmes after cancer treatment have been described. However, little is known regarding the long-term effects. The purpose of this study was to investigate the long-term effects of high-intensity resistance training compared with traditional recovery. A total of 68 cancer survivors who completed an 18-week resistance training programme were followed for 1 year. During the 1-year follow-up, 19 patients dropped out (14 due to recurrence of cancer). The remaining 49 patients of the intervention group were compared with a group of 22 patients treated with chemotherapy in the same period but not participating in any rehabilitation programme. Outcome measures were muscle strength, cardiopulmonary function, fatigue, and health-related quality of life. One year after completion of the rehabilitation programme, the outcome measures in the intervention group were still at the same level as immediately after rehabilitation. Muscle strength at 1 year was significantly higher in patients who completed the resistance training programme than in the comparison group. High-intensity resistance training has persistent effects on muscle strength, cardiopulmonary function, quality of life, and fatigue. Rehabilitation programmes for patients treated with chemotherapy with a curative intention should include high-intensity resistance training in their programme. British Journal of Cancer (2008) 99, 30–36. doi:10.1038/sj.bjc.6604433 www.bjcancer.com Published online 24 June 2008 & 2008 Cancer Research UK Keywords: exercise; fatigue; long-term effects; muscle strength; quality of life; rehabilitation Oncologists and scientists have made substantial progress in tional decline (Demark-Wahnefried et al, 2005). In several cross- cancer treatment in the last few decades. Currently, the average sectional and intervention studies in healthy populations and in 5-year survival rate is approaching 60% for female and 46% for patients with chronic diseases, regular physical activity is male patients (Signaleringscommissie Kanker, 2004). Between 2000 associated with enhanced health and reduced risk of all-cause and 2015 the number of cancer survivors in the Netherlands is mortality (Blair et al, 1995, 1996; Roberts and Barnard, 2005; expected to double. Not only improved medical treatment but also Lindstrom et al, 2006). greying of the population and a longer life expectancy are Rehabilitation programmes are currently being incorporated contributing to increased cancer prevalence worldwide. As both more and more in the care of cancer patients as well (Lucia et al, the number of cancer survivors and the length of their survival are 2003; Galvao and Newton, 2005; Knols et al, 2005). Systematic increasing, long-term health issues related to cancer and its review evidence shows that exercise in cancer survivors improves treatment are becoming more important (Demark-Wahnefried quality of life, cardiorespiratory fitness, physical functioning, and et al, 2005; Ganz, 2005). fatigue (Stevinson et al, 2004; Galvao and Newton, 2005; Knols Cancer treatment is associated with substantial psychosocial and et al, 2005; McNeely et al, 2006). However, several intervention physical side effects, including muscular atrophy, weight changes, studies incorporated in these reviews have some shortcomings. decreased resistance, depression, fatigue, and an overall decrease First, most rehabilitation programmes are relatively short in in quality of life (Berglund et al, 1991; Dimeo et al, 1997, 2004; duration (less than 12 weeks) (Irwin and Ainsworth, 2004). Courneya and Friedenreich, 1999; Courneya, 2003; Wagner and Second, in these programmes, patients were not stimulated to Cella, 2004). Furthermore, cancer survivors are at increased risk remain physically active after the programme. Finally, most studies for cancer recurrence and for secondary effects, such as use aerobic exercises such as walking or stationary cycling (Irwin cardiovascular disease, diabetes, obesity, osteoporosis, and func- and Ainsworth, 2004). Few studies incorporated resistance training in their programmes. A recent systematic review by Cheema et al (2007) located only 10 trials that used progressive resistance *Correspondence: IC De Backer, Department of Sports Medicine, training in breast cancer patients. However, even this limited Ma´xima Medical Centre, De Run 4600, Veldhoven 5500 MB, The number of studies indicates that resistance training has a great Netherlands; E-mail: I.deBacker@mmc.nl potential to counteract side effects of cancer, such as muscle Revised 1 May 2008; accepted 2 May 2008; published online 24 June wasting, reduced bone mineral density, and fatigue (Cunningham 2008 et al, 1986; Ferrando et al, 1997; Twiss et al, 2001; Segal et al, 2003; Long-term effects of cancer rehabilitation IC De Backer et al Oldervoll et al, 2004; Ott et al, 2004; Galvao and Newton, 2005; Centre, Veldhoven (hospital 2). The project was approved by the Ohira et al, 2006). Ethical Review Committee of the Maxima Medical Centre, and As cancer rehabilitation is a relatively new area of research, informed consent was obtained from all patients. Eligibility criteria published studies mainly report the short-term effects of exercise included histologically confirmed cancer with no indication of training. This is a major drawback, as physical and psychological recurrent or progressive disease, age between 25 and 70 years, impairment may persist for many years after cancer treatment chemotherapy with curative intention administered between (Berglund et al, 1991; Dimeo, 2001). Only four training studies in January 2001 and December 2003, and completion of surgical cancer patients reported data of long-term follow-up. Two of them treatment or radiotherapy. Patients suffering from other serious involved a home-based training programme and one study used diseases that might hamper physical performance capacity, for only questionnaires to follow up the patients (Berglund et al, 1994; example, heart failure, COPD, and neurological disorders, were Carlson et al, 2006; Demark-Wahnefried et al, 2006; Thorsen et al, excluded. 2007). The fourth study examined the effects of supervised training From 2001 onwards, rehabilitation using a high-intensity after allogeneic stem cell transplantation (Carlson et al, 2006). resistance training programme was implemented as standard Our study investigated the long-term effects of high-intensity medical care after chemotherapy in hospital 2. Medical oncologists resistance training on muscle strength, cardiopulmonary function, recruited all eligible patients treated with chemotherapy with a fatigue, and quality of life in a more general population of cancer curative intention. These patients were assigned to the intervention patients after chemotherapy. To distinguish the observed long- group and were prospectively followed from the start of the term effects from spontaneous recovery, a comparison was rehabilitation programme up to 12 months after completing the performed with a similar group of patients who did not participate programme. The comparison group, treated in hospital 1, was a in a rehabilitation programme. We hypothesised that cancer similar group of cancer patients who underwent chemotherapy in patients benefit from high-intensity resistance training in terms of the same period as the intervention group. This group of patients muscle strength, cardiopulmonary function, fatigue, and quality of was not offered any exercise or rehabilitation programme. The life immediately after rehabilitation and 1 year after completing the same inclusion and exclusion criteria were applied as in the rehabilitation programme. intervention group. The oncologists and the patients in hospital 1 were not aware of the benefit of the rehabilitation programme in hospital 2 in 2001 and 2002. Figure 1 shows the flowchart of the study and the patient selection. One year after completion of the METHODS training programme, 49 consecutive patients were included in the follow-up. Twenty-two patients were included in the comparison Study design and patient selection group. These patients did not exercise under supervision. There This study was conducted in two teaching hospitals, Maxima was no further information from these patients about their activity Medical Centre, Eindhoven (hospital 1) and Maxima Medical level. The characteristics of these patients are shown in Table 1. Chemotherapy in Chemotherapy in 2001–2002 in hospital 1 2001–2003 in hospital 2 Week 0 test 18 weeks TRAINING PROGRAMME (68 patients) Week 18 test 7 dropouts: recurrence (5), personal reasons (2) Week 22 test 4 dropouts: recurrence (3), co-morbidity (1) Week 26 test 27 eligible patients were contacted 0 dropouts Week 30 test 5 dropouts: 1 dropout: recurrence (1) moved house (2), not interested (3) Week 34 test 7 dropouts: recurrence (5), personal reasons (2) Long-term test Week 68 test (22 patients) (49 patients) Figure 1 Flow chart of the study. & 2008 Cancer Research UK British Journal of Cancer (2008) 99(1), 30 – 36 Clinical Studies Clinical Studies Long-term effects of cancer rehabilitation IC De Backer et al Table 1 Patient characteristics of the intervention and comparison follows: (1) vertical row (focusing on longissimus, biceps brachii, groups rhomboideus); (2) leg press (quadriceps, glutei, gastrocnemius); (3) bench press (pectoralis major, triceps); (4) pull over Intervention Comparison (pectoralis, triceps brachii, deltoideus, trapezius); (5) abdominal group (n¼ 49) group (n¼ 22) crunch (rectus abdominis); and (6) lunge (quadriceps, glutei, hamstrings). First, resistance exercises were performed at 65–80% n % n % of one-repetition maximum (1-RM) and consisted of two sets of 10 repetitions. After the 12th week, the emphasis shifted from muscle Gender strength to muscle endurance involving training with less Male 9 18 4 18 resistance (35–40% of 1-RM) but more (20) repetitions. Every 4 Female 40 82 18 82 weeks the training progress was evaluated, and the result was Type of tumour adjusted by means of a 1-RM test. Breast 32 65 14 64 Ovarian 3 6 0 0 Interval training Interval training consisted of cycling two times HL 48 29 for 8 min, before and after the resistance exercises. In the first 8 NHL 3 6 3 14 weeks, those 8 min consisted of alternating 30 s at 65% of the Colorectal 5 10 3 14 maximal short exercise capacity (MSEC) and 60 s at 30%. A steep Testis 2 4 0 0 ramp test was performed to determine the MSEC. After 30 s of Treatment cycling at 25 W, the load was increased by 25 W every 10 s until Chemotherapy 49 100 22 100 exhaustion. From week 9, those 8 min consisted of alternating 30 s +Radiotherapy 3 6 0 0 at 65% and 30 s at 30% of the MSEC. Results of the steep ramp test +Surgery 14 29 4 18 were described in a previous publication (De Backer et al, 2007a). +Radiotherapy+surgery 28 57 17 77 Chemotherapy Follow-up At the end of the rehabilitation programme (week 18), AC, breast 14 29 9 41 patients were advised by a sports physician to continue physical CMF, breast 7 14 3 14 activity at home. These personalised advices were based on the FEC, breast 11 22 2 9 patient’s individual interests and motivation. In the follow-up Carboplatin – paclitaxel, ovarian 3 6 0 0 period, there were five appointments (week 22, 26, 30, 34, and 68) ABVD/EBVP/BEACOPP, HL 4 8 2 9 with a physical therapist to encourage the patients to stay active CHOP/CVP, NHL 3 6 3 14 and to perform a muscle strength test. In week 68, cardiopulmon- 5-FU leucovorin, colorectal 5 10 3 14 ary function, Multidimensional Fatigue Inventory (MFI), and BEP, testis 2 4 0 0 health-related quality of life (HRQOL) were reported along with muscle strength. Mean s.d. Mean s.d. Age (years) Outcome measures Mean 48 8 51 11 Muscle strength For the determination of muscle strength, the Anthropometry indirect 1-RM test was used (Sale and MacDougall, 1981; Mayhew Height (cm) 170 7 173 8 et al, 1995). One-repetition maximum is the maximum amount of Weight (kg) 78 11 77 14 weight that can be lifted once. Indirect 1-RM values were Time since last chemotherapy calculated from the Brzycki’s equation (Sale and MacDougall, Weeks between last 96 26 169 26 1981; Mayhew et al, 1995). One-repetition maximum is stated in chemotherapy and test week 68 kilograms in proportion to body weight. Muscle groups were tested with the resistance equipment that was also used for the training ABVD¼ doxorubicin, bleomycin, vinblastine, dacarbazine; AC¼ adriamycin, cyclo- (leg press, vertical row, bench press, lunge, pull over, and phosphamide; BEACOPP¼ bleomycin, etoposide, doxorubicin, cyclophosphamide, vincristine, procarbazine, prednisone; BEP¼ bleomycin, etoposide, cisplatin; abdominal crunch). This test was performed seven times: at the CHOP¼ cyclophosphamide, doxorubicin, vincristine, prednisone; CMF¼ cyclopho- start (week 0) and the end of the programme (week 18) and in the sphamide, methotrexate, fluorouracil; CVP¼ cyclophosphamide, vincristine, predni- follow-up period (weeks 22, 26, 30, 34, and 68). sone; EBVP¼ epirubicin, bleomycin, vincristine, prednisone; FEC¼ fluorouracil, epirubicin, cyclophosphamide; HL¼ Hodgkin’s lymphoma; NHL¼ non-Hodgkin’s Cardiopulmonary function Cardiopulmonary function was as- lymphoma. sessed by cardiopulmonary exercise testing, which was performed on a cycle ergometer (Corival, Lode, The Netherlands). Expired gases were collected and analysed breath by breath for O ,CO , 2 2 and volume. Electrocardiogram was continuously monitored. Training intervention Patients were instructed and encouraged to continue exercise The 18-week training programme consisted of high-intensity until exhaustion. The test was ended if patients were unable to resistance and interval training. To counteract bias resulting from maintain the required pedalling frequency of 70 r.p.m. At the end spontaneous recovery after chemotherapy, training started not of the test, peak oxygen consumption (peak VO ), peak power earlier than 6 weeks after completing chemotherapy. The patients output, and peak heart rate were registered. Ventilatory threshold trained in groups of six to eight persons on specialised resistance was determined by using the oxygen equivalent method training equipment and on bicycle ergometers under the super- (Wasserman et al, 1999). In addition, cardiopulmonary exercise vision of physical therapists. During the first 12 weeks, patients testing was used to identify potential cardiopulmonary limitations were trained twice a week. In the last six weeks, patients were caused by cardiotoxic (e.g. anthracyclins) or pulmotoxic (e.g. trained once a week. bleomycin) medications or by radiation therapy to the breast (Dimeo, 2001; Winningham, 2001; Myers, 2005). High-intensity resistance training The resistance programme This test was performed before (week 0) and after the training consisted of six exercises targeting the large muscle groups as programme (week 18) and in week 68 according to the standard British Journal of Cancer (2008) 99(1), 30 – 36 & 2008 Cancer Research UK Long-term effects of cancer rehabilitation IC De Backer et al protocol (ERS Task Force on Standardization of Clinical Exercise diagnosis between the dropouts and those patients completing the Testing and European Respiratory Society, 1997). study. The time interval between last treatment and long-term test was shorter in the training group than in the comparison group (96 vs 169 weeks, Po0.01). Fatigue The MFI is a questionnaire consisting of 20 statements for which the person has to indicate on a 7-point scale the extent to which the particular statement applies to him or her. The Long-term effects on muscle strength and differences in statement refers to aspects of fatigue experienced during the muscle strength between the training and the comparison previous few days. Higher scores indicate a higher degree of groups fatigue. This self-report instrument consists of five subscales based Table 2 shows the test results at baseline, post-rehabilitation, and on different dimensions: general fatigue, physical fatigue, reduced after long-term follow-up (week 68) in the intervention group and activity, reduced motivation, and mental fatigue. This question- the comparison group. Muscle strength improved significantly naire was completed in weeks 0, 18, and 68. after training. Repeated measure analysis shows that the improve- ment of muscle strength was maintained in the long term. There Health-related quality of life Quality of life was assessed using were no significant differences between long-term measurements the European Organisation for Research and Treatment of Cancer and post-rehabilitation in all resistance exercises. Figure 2 shows Core Quality of Life Questionnaire C30 (EORTC QLQ-C30). This the progress in muscle strength in all exercises at seven different questionnaire has a high reliability and validity (Aaronson et al, time points. After 18 weeks of training, muscle strength stabilises 1993; Groenvold et al, 1997). The EORTC QLQ-C30 encompasses until week 68. All 1-RM test results were significantly higher in the 30 items divided into six functional scales (physical, role, intervention group than in the comparison group for vertical row cognitive, emotional and social functioning, and global quality of (50%), leg press (33%), bench press (57%), pull over (100%), lunge life), three symptom scales (fatigue, nausea, and pain), and six (119%), and abdominal crunch (37%). individual items. This questionnaire was completed in weeks 0, 18, and 68. Long-term effects on cardiopulmonary function and differences between the training and the comparison Statistical analyses groups In the training group, dropouts and patients who continued the Table 2 shows the data of cardiopulmonary outcomes. There was a study were analysed for differences in gender, age, cancer significant effect of training on the peak oxygen consumption diagnosis, time from last treatment, and initial muscle strength 2 (þ 12%), maximal workload (þ 15%), peak heart rate (þ 3%), and by means of w tests or independent samples t-tests. 2 ventilatory threshold (þ 16%). This effect was maintained in the w Tests for categorical data and independent samples t-tests for long term, as shown by the fact that there were no significant continuous data were used to examine group differences in terms differences in cardiopulmonary function between week 18 and of gender, age, cancer diagnosis, time between completion of week 68. Results of the comparison group were not significantly treatment, and long-term outcome between the training group and different from those of the intervention group. the comparison group. A repeated measure analysis (SPSS mixed linear) was used to assess differences in muscle strength between seven different time Long-term effects on fatigue and quality of life and points (weeks 0, 18, 22, 26, 30, 34, and 68). Post hoc Bonferroni differences between the training and the comparison correction was used as a protection against Type I error. groups Paired sample t-tests were used to test the significance of Table 2 shows the data of different subscales of fatigue (MFI) and changes in mean scores for cardiopulmonary function, fatigue, and quality of life (HRQOL). All subscales of MFI, except for reduction HRQOL from baseline (week 0) to post-intervention (week 18), in motivation, improved significantly after training. The improve- post-intervention to week 68, and week 0 to week 68. The last ment in the fatigue outcome measures persisted 1 year after measured values for the dropouts were used for the week 68 test completing the training programme. However, in the long term, (intention-to-treat analysis). there were no differences between the comparison group and the Independent sample t-tests were used to analyse differences in intervention group in MFI. Health-related quality of life also muscle strength, cardiopulmonary function, HRQOL, and fatigue improved significantly post-treatment, and this effect continued in between the training group and the comparison group. the long term. There were no differences between the training All statistical analyses were performed using the statistics group and the comparison group on all subscales of HRQOL. program SPSS (version 13.0). DISCUSSION RESULTS This is the first study that describes the long-term effects of a high- Adherence and baseline characteristics intensity resistance training programme in cancer patients. The In the intervention group, 68 patients were monitored for 12 tolerance and effects noted immediately post-rehabilitation have months after the rehabilitation programme. Fourteen patients were already been published (De Backer et al, 2007b). After completion excluded because of cancer recurrence, and one patient was of the programme, repeated testing showed a continuation and excluded because of serious co-morbidity. Four patients left during stabilisation of the muscle strength level (Figure 2) and peak VO . the follow-up period for personal reasons and were considered Muscle strength was significantly higher in patients who completed non-adherent dropouts, resulting in a dropout rate of 6%. Of the the resistance training programme than in the comparison group. 27 patients who proved eligible to participate in the comparison Questionnaire outcomes indicate an overall improvement imme- group, 22 took part in the exercise tests and completed the diately after rehabilitation on several scales of quality of life and of questionnaires, resulting in a dropout rate of 23%. There were no fatigue, especially physical fatigue. This improvement was also significant differences in gender, age, and cancer diagnosis maintained 1 year later. However, there were no differences in between the intervention and the comparison groups. Moreover, quality of life, fatigue, and peak VO between the intervention and there were no significant differences in gender, age, and cancer the comparison groups. & 2008 Cancer Research UK British Journal of Cancer (2008) 99(1), 30 – 36 Clinical Studies Clinical Studies Long-term effects of cancer rehabilitation IC De Backer et al Table 2 Effects of training on muscle strength, cardiopulmonary function, fatigue, and quality of life on different time points Long-term (week 68) Baseline (week 0) Post-rehabilitation (week 18) Outcome measure Intervention group Intervention group Intervention group Comparison group Muscle strength (1-RM/kg) a c e Vertical row 0.48 (0.16) 0.69 (0.20) 0.68 (0.20) 0.46 (0.11) a c e Leg press 1.96 (0.51) 2.79 (0.62) 2.89 (0.74) 2.20 (0.51) a c e Bench press 0.30 (0.11) 0.46 (0.15) 0.45 (0.15) 0.30 (0.11) a c e Pull over 0.12 (0.05) 0.25 (0.08) 0.26 (0.10) 0.13 (0.06) a c e Lunge 0.20 (0.09) 0.42 (0.17) 0.46 (0.16) 0.21 (0.10) a c e Abdominal crunch 0.39 (0.14) 0.60 (0.17) 0.64 (0.18) 0.46 (0.13) Cardiopulmonary outcomes 1 1 b d Peak oxygen consumption (ml min kg ) 25.7 (6.3) 28.9 (6.7) 29.3 (8.4) 27.8 (5.6) 1 b d Peak power output (W kg ) 2.0 (0.6) 2.3 (0.7) 2.5 (0.8) 2.2 (0.6) b d Peak heart rate (beats per min) 167 (17) 172 (14) 168 (20) 165 (18) 1 1 b d Ventilatory threshold (ml min kg ) 19.2 (4.7) 22.3 (5.7) 23.5 (7.1) 22.2 (4.9) MFI b d General fatigue 13.1 (4.5) 9.2 (4.1) 9.9 (4.4) 10.6 (4.4) b d Reduced activity 11.8 (4.4) 8.1 (3.4) 8.2 (3.8) 8.8 (4.3) b d Mental fatigue 10.0 (4.4) 8.8 (3.8) 8.4 (4.0) 7.9 (4.2) Physical fatigue 13.7 (4.1) 8.1 (3.5) 9.2 (4.0) 9.9 (4.8) Reduced motivation 8.7 (3.1) 7.7 (2.8) 7.8 (3.5) 8.4 (4.1) HRQOL b d Physical functioning 72.4 (19.2) 84.2 (19.0) 85.5 (18.5) 81.8 (18.4) b d Role functioning 60.3 (24.0) 79.5 (21.1) 79.4 (22.5) 83.3 (20.6) b d Emotional functioning 75.6 (20.2) 85.7 (18.8) 84.1 (18.4) 81.3 (20.7) Cognitive functioning 76.5 (24.4) 83.8 (21.5) 85.6 (17.3) 82.6 (19.3) b d Social functioning 68.4 (29.3) 82.5 (21.6) 82.3 (24.2) 84.1 (20.8) b d Fatigue 43.6 (23.4) 22.0 (18.8) 24.8 (22.0) 29.8 (21.3) HRQOL¼ health-related quality of life; MFI¼ multidimensional fatigue index; 1-RM¼ one-repetition maximum. All data are means (s.d.). Significant difference, Po0.01, baseline b c and post-rehabilitation (repeated measure analyses). Significant difference, Po0.01, baseline and post-rehabilitation (paired t-tests). Significant difference, Po0.01, baseline and d e week 68 (repeated measure analyses). Significant difference, Po0.01, baseline and week 68 (paired t-tests). Significant difference, Po0.01, the intervention and comparison groups (independent sample t-tests). 3.5 on their quality of life (Lucia et al, 2003; Knols et al, 2005). Despite the mounting evidence of the significance of physical activity 3.0 after cancer treatment, there are presently only four studies that leg press (kg) have assessed the long-term effects of physical rehabilitation 2.5 programmes. Two studies examined the long-term effect of a home-based 2.0 training programme (Demark-Wahnefried et al, 2006; Thorsen 1.5 et al, 2007). Demark-Wahnefried et al evaluated a 6-month home- based diet and exercise programme (telephone counselling and 0.8 mailed materials) by telephone interview at 6 and 12 months after 0.7 the start. This study included only older breast and prostate cancer vertical row (kg) 0.6 patients (X65 years). In the long term (12 months), there were no abdominal crunch (kg) 0.5 significant differences between the intervention and the compar- lunge (kg) 0.4 ison groups in physical functioning, diet quality index, fatigue, and bench press (kg) 0.3 pull over (kg) energy expenditure as measured by telephone questionnaires 0.2 (Demark-Wahnefried et al, 2006). Thorsen et al recently published 0.1 their long-term data of a randomised study of a 3-month home- based training programme. In contrast to our study, the favourable 0 8 16 24 32 40 48 56 64 72 effect on cardiopulmonary functioning could not be sustained Time period (weeks) during a 12-month follow-up. The researchers concluded that for a Figure 2 Muscle strength from start of rehabilitation up to 12 months longer-lasting effect over time, a longer intervention period and after completing rehabilitation. more intense exercise were needed (Thorsen et al, 2007). Another possible explanation for the lack of long-term effects is the supervised training used in our study rather than the home-based There is preliminary evidence that physical activity plays a role training programmes used in the previous studies. The multiple in the primary and secondary prevention of cancer (Stein and visits after the programme for testing may have contributed to the Colditz, 2004; Holmes et al, 2005). Several randomised, controlled persistent effect in our programme. trials have examined the short-time effects of physical activity after The third study that examined the long-term effects of training the diagnosis of cancer. Overall, most studies demonstrated that in cancer patients is by Carlson et al. This study examined the physical training programmes had beneficial effects on cancer effects of supervised aerobic exercise training after 12 months in 12 patients’ physical or psychosocial capacity and, as a consequence, patients after allogeneic haematopoietic stem cell transplantation. British Journal of Cancer (2008) 99(1), 30 – 36 & 2008 Cancer Research UK Relative strength (1−RM/body weight (kg)) Long-term effects of cancer rehabilitation IC De Backer et al Significant improvements in fatigue, ventilatory threshold, and Our study design has some shortcomings. First, the different stroke volume were found (Carlson et al, 2006). The fourth study time intervals between last treatment and long-term test for the of Berglund et al evaluated a training programme over a 1-year comparison group (169 weeks) and the training group (96 weeks). follow-up period. The intervention group improved significantly However, we expect that this longer time span (if it has caused more than the comparison group in physical strength and physical bias) will be in favour of the comparison group because this group activity levels, both of which were evaluated by means of has more time for spontaneous recovery after intensive treatment. questionnaires. In our study, the cardiopulmonary function and Second, the lack of baseline measurements in the comparison muscle strength were assessed by exercise tests (peak VO and group is a limitation of the current study. These shortcomings 1-RM), which are more valid and reliable outcome measures. could be overcome by a prospective, randomised, controlled As cancer rehabilitation is a relatively new area of research, clinical trial. However, such a study design is not practical for there is no consensus about the optimal type of training in a exercise intervention trials. First, patients cannot be blinded to rehabilitation programme. Exercise interventions vary consider- their treatment; only the outcome assessor can be blinded to group ably from brief instructions of home-based exercises to highly allocation. Second, when patients are participating in a training structured, supervised exercise sessions on strength equipment study and are randomised to the control or waiting group, they (Conn et al, 2006). It is remarkable that most studies only used start to get more active spontaneously. Particularly in a group of aerobic exercises such as walking or stationary cycling in their cancer patients, subjects might come into contact with other rehabilitation programmes (Courneya et al, 2003), as one of the subjects. Finally, the short-term benefits of exercise are recognised side effects of cancer and its treatment is muscle atrophy (Argiles in research and clinics. It could be considered unethical to restrain et al, 2005). To improve muscle strength and increase muscle patients from an exercise-containing rehabilitation programme. mass, resistance training is more important than aerobic exercise. Therefore, we believe that our study design is appropriate in Also, considerable evidence now suggests that the ability to cancer rehabilitation research, especially when long-term effects perform physical tasks in daily life is determined by a threshold are studied. level of muscular resistance (Brill et al, 2000). As a consequence, resistance training seems to be the programme of choice for regaining muscle strength and, in this way, improving activities of CONCLUSION daily living and HRQOL (Brill et al, 2000). In addition, in cancer patients, muscle strength is related to quality-of-life aspects with This is the first study that describes the long-term effects of a high- correlations ranging from 0.47 to 0.75 (De Backer et al, 2007b). intensity resistance training programme in cancer patients. Results The results of the questionnaires, HRQOL, and MFI, did not indicate that after a 12-month follow-up, the beneficial effects on muscle strength, cardiopulmonary function, HRQOL, and fatigue differ between the two groups. A possible explanation for this is were sustained. Muscle strength was significantly higher in the the high outcome values in the questionnaires. It is most likely that intervention group than in the comparison group. Based on these a ceiling effect is reached a rather long time after cancer treatment. results, we suggest that guidelines for rehabilitation in oncology Cancer patients may be satisfied with their ‘survival status’ and patients should include high-intensity resistance training. score high in all QOL questionnaires despite existing limitations and complaints. This experience is familiar to other researchers (van de Poll-Franse et al, 2006). 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Long-term follow-up after cancer rehabilitation using high-intensity resistance training: persistent improvement of physical performance and quality of life

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Publisher
Springer Journals
Copyright
Copyright © 2008 by The Author(s)
Subject
Biomedicine; Biomedicine, general; Cancer Research; Epidemiology; Molecular Medicine; Oncology; Drug Resistance
ISSN
0007-0920
eISSN
1532-1827
DOI
10.1038/sj.bjc.6604433
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See Article on Publisher Site

Abstract

Clinical Studies British Journal of Cancer (2008) 99, 30 – 36 & 2008 Cancer Research UK All rights reserved 0007 – 0920/08 $30.00 www.bjcancer.com Long-term follow-up after cancer rehabilitation using high-intensity resistance training: persistent improvement of physical performance and quality of life ,1 2 2 3 4 1 IC De Backer , G Vreugdenhil , MR Nijziel , AD Kester , E van Breda and G Schep 1 2 Department of Sports Medicine, Ma´xima Medical Centre, Veldhoven, The Netherlands; Department of Internal Medicine, Ma´xima Medical Centre, Veldhoven and Eindhoven, The Netherlands; Department of Methodology and Statistics, Maastricht University, Maastricht, The Netherlands; Department of Movement Science, Nutrition and Toxicology Research Institute Maastricht (NUTRIM), Maastricht University, Maastricht, The Netherlands The short-term beneficial effects of physical rehabilitation programmes after cancer treatment have been described. However, little is known regarding the long-term effects. The purpose of this study was to investigate the long-term effects of high-intensity resistance training compared with traditional recovery. A total of 68 cancer survivors who completed an 18-week resistance training programme were followed for 1 year. During the 1-year follow-up, 19 patients dropped out (14 due to recurrence of cancer). The remaining 49 patients of the intervention group were compared with a group of 22 patients treated with chemotherapy in the same period but not participating in any rehabilitation programme. Outcome measures were muscle strength, cardiopulmonary function, fatigue, and health-related quality of life. One year after completion of the rehabilitation programme, the outcome measures in the intervention group were still at the same level as immediately after rehabilitation. Muscle strength at 1 year was significantly higher in patients who completed the resistance training programme than in the comparison group. High-intensity resistance training has persistent effects on muscle strength, cardiopulmonary function, quality of life, and fatigue. Rehabilitation programmes for patients treated with chemotherapy with a curative intention should include high-intensity resistance training in their programme. British Journal of Cancer (2008) 99, 30–36. doi:10.1038/sj.bjc.6604433 www.bjcancer.com Published online 24 June 2008 & 2008 Cancer Research UK Keywords: exercise; fatigue; long-term effects; muscle strength; quality of life; rehabilitation Oncologists and scientists have made substantial progress in tional decline (Demark-Wahnefried et al, 2005). In several cross- cancer treatment in the last few decades. Currently, the average sectional and intervention studies in healthy populations and in 5-year survival rate is approaching 60% for female and 46% for patients with chronic diseases, regular physical activity is male patients (Signaleringscommissie Kanker, 2004). Between 2000 associated with enhanced health and reduced risk of all-cause and 2015 the number of cancer survivors in the Netherlands is mortality (Blair et al, 1995, 1996; Roberts and Barnard, 2005; expected to double. Not only improved medical treatment but also Lindstrom et al, 2006). greying of the population and a longer life expectancy are Rehabilitation programmes are currently being incorporated contributing to increased cancer prevalence worldwide. As both more and more in the care of cancer patients as well (Lucia et al, the number of cancer survivors and the length of their survival are 2003; Galvao and Newton, 2005; Knols et al, 2005). Systematic increasing, long-term health issues related to cancer and its review evidence shows that exercise in cancer survivors improves treatment are becoming more important (Demark-Wahnefried quality of life, cardiorespiratory fitness, physical functioning, and et al, 2005; Ganz, 2005). fatigue (Stevinson et al, 2004; Galvao and Newton, 2005; Knols Cancer treatment is associated with substantial psychosocial and et al, 2005; McNeely et al, 2006). However, several intervention physical side effects, including muscular atrophy, weight changes, studies incorporated in these reviews have some shortcomings. decreased resistance, depression, fatigue, and an overall decrease First, most rehabilitation programmes are relatively short in in quality of life (Berglund et al, 1991; Dimeo et al, 1997, 2004; duration (less than 12 weeks) (Irwin and Ainsworth, 2004). Courneya and Friedenreich, 1999; Courneya, 2003; Wagner and Second, in these programmes, patients were not stimulated to Cella, 2004). Furthermore, cancer survivors are at increased risk remain physically active after the programme. Finally, most studies for cancer recurrence and for secondary effects, such as use aerobic exercises such as walking or stationary cycling (Irwin cardiovascular disease, diabetes, obesity, osteoporosis, and func- and Ainsworth, 2004). Few studies incorporated resistance training in their programmes. A recent systematic review by Cheema et al (2007) located only 10 trials that used progressive resistance *Correspondence: IC De Backer, Department of Sports Medicine, training in breast cancer patients. However, even this limited Ma´xima Medical Centre, De Run 4600, Veldhoven 5500 MB, The number of studies indicates that resistance training has a great Netherlands; E-mail: I.deBacker@mmc.nl potential to counteract side effects of cancer, such as muscle Revised 1 May 2008; accepted 2 May 2008; published online 24 June wasting, reduced bone mineral density, and fatigue (Cunningham 2008 et al, 1986; Ferrando et al, 1997; Twiss et al, 2001; Segal et al, 2003; Long-term effects of cancer rehabilitation IC De Backer et al Oldervoll et al, 2004; Ott et al, 2004; Galvao and Newton, 2005; Centre, Veldhoven (hospital 2). The project was approved by the Ohira et al, 2006). Ethical Review Committee of the Maxima Medical Centre, and As cancer rehabilitation is a relatively new area of research, informed consent was obtained from all patients. Eligibility criteria published studies mainly report the short-term effects of exercise included histologically confirmed cancer with no indication of training. This is a major drawback, as physical and psychological recurrent or progressive disease, age between 25 and 70 years, impairment may persist for many years after cancer treatment chemotherapy with curative intention administered between (Berglund et al, 1991; Dimeo, 2001). Only four training studies in January 2001 and December 2003, and completion of surgical cancer patients reported data of long-term follow-up. Two of them treatment or radiotherapy. Patients suffering from other serious involved a home-based training programme and one study used diseases that might hamper physical performance capacity, for only questionnaires to follow up the patients (Berglund et al, 1994; example, heart failure, COPD, and neurological disorders, were Carlson et al, 2006; Demark-Wahnefried et al, 2006; Thorsen et al, excluded. 2007). The fourth study examined the effects of supervised training From 2001 onwards, rehabilitation using a high-intensity after allogeneic stem cell transplantation (Carlson et al, 2006). resistance training programme was implemented as standard Our study investigated the long-term effects of high-intensity medical care after chemotherapy in hospital 2. Medical oncologists resistance training on muscle strength, cardiopulmonary function, recruited all eligible patients treated with chemotherapy with a fatigue, and quality of life in a more general population of cancer curative intention. These patients were assigned to the intervention patients after chemotherapy. To distinguish the observed long- group and were prospectively followed from the start of the term effects from spontaneous recovery, a comparison was rehabilitation programme up to 12 months after completing the performed with a similar group of patients who did not participate programme. The comparison group, treated in hospital 1, was a in a rehabilitation programme. We hypothesised that cancer similar group of cancer patients who underwent chemotherapy in patients benefit from high-intensity resistance training in terms of the same period as the intervention group. This group of patients muscle strength, cardiopulmonary function, fatigue, and quality of was not offered any exercise or rehabilitation programme. The life immediately after rehabilitation and 1 year after completing the same inclusion and exclusion criteria were applied as in the rehabilitation programme. intervention group. The oncologists and the patients in hospital 1 were not aware of the benefit of the rehabilitation programme in hospital 2 in 2001 and 2002. Figure 1 shows the flowchart of the study and the patient selection. One year after completion of the METHODS training programme, 49 consecutive patients were included in the follow-up. Twenty-two patients were included in the comparison Study design and patient selection group. These patients did not exercise under supervision. There This study was conducted in two teaching hospitals, Maxima was no further information from these patients about their activity Medical Centre, Eindhoven (hospital 1) and Maxima Medical level. The characteristics of these patients are shown in Table 1. Chemotherapy in Chemotherapy in 2001–2002 in hospital 1 2001–2003 in hospital 2 Week 0 test 18 weeks TRAINING PROGRAMME (68 patients) Week 18 test 7 dropouts: recurrence (5), personal reasons (2) Week 22 test 4 dropouts: recurrence (3), co-morbidity (1) Week 26 test 27 eligible patients were contacted 0 dropouts Week 30 test 5 dropouts: 1 dropout: recurrence (1) moved house (2), not interested (3) Week 34 test 7 dropouts: recurrence (5), personal reasons (2) Long-term test Week 68 test (22 patients) (49 patients) Figure 1 Flow chart of the study. & 2008 Cancer Research UK British Journal of Cancer (2008) 99(1), 30 – 36 Clinical Studies Clinical Studies Long-term effects of cancer rehabilitation IC De Backer et al Table 1 Patient characteristics of the intervention and comparison follows: (1) vertical row (focusing on longissimus, biceps brachii, groups rhomboideus); (2) leg press (quadriceps, glutei, gastrocnemius); (3) bench press (pectoralis major, triceps); (4) pull over Intervention Comparison (pectoralis, triceps brachii, deltoideus, trapezius); (5) abdominal group (n¼ 49) group (n¼ 22) crunch (rectus abdominis); and (6) lunge (quadriceps, glutei, hamstrings). First, resistance exercises were performed at 65–80% n % n % of one-repetition maximum (1-RM) and consisted of two sets of 10 repetitions. After the 12th week, the emphasis shifted from muscle Gender strength to muscle endurance involving training with less Male 9 18 4 18 resistance (35–40% of 1-RM) but more (20) repetitions. Every 4 Female 40 82 18 82 weeks the training progress was evaluated, and the result was Type of tumour adjusted by means of a 1-RM test. Breast 32 65 14 64 Ovarian 3 6 0 0 Interval training Interval training consisted of cycling two times HL 48 29 for 8 min, before and after the resistance exercises. In the first 8 NHL 3 6 3 14 weeks, those 8 min consisted of alternating 30 s at 65% of the Colorectal 5 10 3 14 maximal short exercise capacity (MSEC) and 60 s at 30%. A steep Testis 2 4 0 0 ramp test was performed to determine the MSEC. After 30 s of Treatment cycling at 25 W, the load was increased by 25 W every 10 s until Chemotherapy 49 100 22 100 exhaustion. From week 9, those 8 min consisted of alternating 30 s +Radiotherapy 3 6 0 0 at 65% and 30 s at 30% of the MSEC. Results of the steep ramp test +Surgery 14 29 4 18 were described in a previous publication (De Backer et al, 2007a). +Radiotherapy+surgery 28 57 17 77 Chemotherapy Follow-up At the end of the rehabilitation programme (week 18), AC, breast 14 29 9 41 patients were advised by a sports physician to continue physical CMF, breast 7 14 3 14 activity at home. These personalised advices were based on the FEC, breast 11 22 2 9 patient’s individual interests and motivation. In the follow-up Carboplatin – paclitaxel, ovarian 3 6 0 0 period, there were five appointments (week 22, 26, 30, 34, and 68) ABVD/EBVP/BEACOPP, HL 4 8 2 9 with a physical therapist to encourage the patients to stay active CHOP/CVP, NHL 3 6 3 14 and to perform a muscle strength test. In week 68, cardiopulmon- 5-FU leucovorin, colorectal 5 10 3 14 ary function, Multidimensional Fatigue Inventory (MFI), and BEP, testis 2 4 0 0 health-related quality of life (HRQOL) were reported along with muscle strength. Mean s.d. Mean s.d. Age (years) Outcome measures Mean 48 8 51 11 Muscle strength For the determination of muscle strength, the Anthropometry indirect 1-RM test was used (Sale and MacDougall, 1981; Mayhew Height (cm) 170 7 173 8 et al, 1995). One-repetition maximum is the maximum amount of Weight (kg) 78 11 77 14 weight that can be lifted once. Indirect 1-RM values were Time since last chemotherapy calculated from the Brzycki’s equation (Sale and MacDougall, Weeks between last 96 26 169 26 1981; Mayhew et al, 1995). One-repetition maximum is stated in chemotherapy and test week 68 kilograms in proportion to body weight. Muscle groups were tested with the resistance equipment that was also used for the training ABVD¼ doxorubicin, bleomycin, vinblastine, dacarbazine; AC¼ adriamycin, cyclo- (leg press, vertical row, bench press, lunge, pull over, and phosphamide; BEACOPP¼ bleomycin, etoposide, doxorubicin, cyclophosphamide, vincristine, procarbazine, prednisone; BEP¼ bleomycin, etoposide, cisplatin; abdominal crunch). This test was performed seven times: at the CHOP¼ cyclophosphamide, doxorubicin, vincristine, prednisone; CMF¼ cyclopho- start (week 0) and the end of the programme (week 18) and in the sphamide, methotrexate, fluorouracil; CVP¼ cyclophosphamide, vincristine, predni- follow-up period (weeks 22, 26, 30, 34, and 68). sone; EBVP¼ epirubicin, bleomycin, vincristine, prednisone; FEC¼ fluorouracil, epirubicin, cyclophosphamide; HL¼ Hodgkin’s lymphoma; NHL¼ non-Hodgkin’s Cardiopulmonary function Cardiopulmonary function was as- lymphoma. sessed by cardiopulmonary exercise testing, which was performed on a cycle ergometer (Corival, Lode, The Netherlands). Expired gases were collected and analysed breath by breath for O ,CO , 2 2 and volume. Electrocardiogram was continuously monitored. Training intervention Patients were instructed and encouraged to continue exercise The 18-week training programme consisted of high-intensity until exhaustion. The test was ended if patients were unable to resistance and interval training. To counteract bias resulting from maintain the required pedalling frequency of 70 r.p.m. At the end spontaneous recovery after chemotherapy, training started not of the test, peak oxygen consumption (peak VO ), peak power earlier than 6 weeks after completing chemotherapy. The patients output, and peak heart rate were registered. Ventilatory threshold trained in groups of six to eight persons on specialised resistance was determined by using the oxygen equivalent method training equipment and on bicycle ergometers under the super- (Wasserman et al, 1999). In addition, cardiopulmonary exercise vision of physical therapists. During the first 12 weeks, patients testing was used to identify potential cardiopulmonary limitations were trained twice a week. In the last six weeks, patients were caused by cardiotoxic (e.g. anthracyclins) or pulmotoxic (e.g. trained once a week. bleomycin) medications or by radiation therapy to the breast (Dimeo, 2001; Winningham, 2001; Myers, 2005). High-intensity resistance training The resistance programme This test was performed before (week 0) and after the training consisted of six exercises targeting the large muscle groups as programme (week 18) and in week 68 according to the standard British Journal of Cancer (2008) 99(1), 30 – 36 & 2008 Cancer Research UK Long-term effects of cancer rehabilitation IC De Backer et al protocol (ERS Task Force on Standardization of Clinical Exercise diagnosis between the dropouts and those patients completing the Testing and European Respiratory Society, 1997). study. The time interval between last treatment and long-term test was shorter in the training group than in the comparison group (96 vs 169 weeks, Po0.01). Fatigue The MFI is a questionnaire consisting of 20 statements for which the person has to indicate on a 7-point scale the extent to which the particular statement applies to him or her. The Long-term effects on muscle strength and differences in statement refers to aspects of fatigue experienced during the muscle strength between the training and the comparison previous few days. Higher scores indicate a higher degree of groups fatigue. This self-report instrument consists of five subscales based Table 2 shows the test results at baseline, post-rehabilitation, and on different dimensions: general fatigue, physical fatigue, reduced after long-term follow-up (week 68) in the intervention group and activity, reduced motivation, and mental fatigue. This question- the comparison group. Muscle strength improved significantly naire was completed in weeks 0, 18, and 68. after training. Repeated measure analysis shows that the improve- ment of muscle strength was maintained in the long term. There Health-related quality of life Quality of life was assessed using were no significant differences between long-term measurements the European Organisation for Research and Treatment of Cancer and post-rehabilitation in all resistance exercises. Figure 2 shows Core Quality of Life Questionnaire C30 (EORTC QLQ-C30). This the progress in muscle strength in all exercises at seven different questionnaire has a high reliability and validity (Aaronson et al, time points. After 18 weeks of training, muscle strength stabilises 1993; Groenvold et al, 1997). The EORTC QLQ-C30 encompasses until week 68. All 1-RM test results were significantly higher in the 30 items divided into six functional scales (physical, role, intervention group than in the comparison group for vertical row cognitive, emotional and social functioning, and global quality of (50%), leg press (33%), bench press (57%), pull over (100%), lunge life), three symptom scales (fatigue, nausea, and pain), and six (119%), and abdominal crunch (37%). individual items. This questionnaire was completed in weeks 0, 18, and 68. Long-term effects on cardiopulmonary function and differences between the training and the comparison Statistical analyses groups In the training group, dropouts and patients who continued the Table 2 shows the data of cardiopulmonary outcomes. There was a study were analysed for differences in gender, age, cancer significant effect of training on the peak oxygen consumption diagnosis, time from last treatment, and initial muscle strength 2 (þ 12%), maximal workload (þ 15%), peak heart rate (þ 3%), and by means of w tests or independent samples t-tests. 2 ventilatory threshold (þ 16%). This effect was maintained in the w Tests for categorical data and independent samples t-tests for long term, as shown by the fact that there were no significant continuous data were used to examine group differences in terms differences in cardiopulmonary function between week 18 and of gender, age, cancer diagnosis, time between completion of week 68. Results of the comparison group were not significantly treatment, and long-term outcome between the training group and different from those of the intervention group. the comparison group. A repeated measure analysis (SPSS mixed linear) was used to assess differences in muscle strength between seven different time Long-term effects on fatigue and quality of life and points (weeks 0, 18, 22, 26, 30, 34, and 68). Post hoc Bonferroni differences between the training and the comparison correction was used as a protection against Type I error. groups Paired sample t-tests were used to test the significance of Table 2 shows the data of different subscales of fatigue (MFI) and changes in mean scores for cardiopulmonary function, fatigue, and quality of life (HRQOL). All subscales of MFI, except for reduction HRQOL from baseline (week 0) to post-intervention (week 18), in motivation, improved significantly after training. The improve- post-intervention to week 68, and week 0 to week 68. The last ment in the fatigue outcome measures persisted 1 year after measured values for the dropouts were used for the week 68 test completing the training programme. However, in the long term, (intention-to-treat analysis). there were no differences between the comparison group and the Independent sample t-tests were used to analyse differences in intervention group in MFI. Health-related quality of life also muscle strength, cardiopulmonary function, HRQOL, and fatigue improved significantly post-treatment, and this effect continued in between the training group and the comparison group. the long term. There were no differences between the training All statistical analyses were performed using the statistics group and the comparison group on all subscales of HRQOL. program SPSS (version 13.0). DISCUSSION RESULTS This is the first study that describes the long-term effects of a high- Adherence and baseline characteristics intensity resistance training programme in cancer patients. The In the intervention group, 68 patients were monitored for 12 tolerance and effects noted immediately post-rehabilitation have months after the rehabilitation programme. Fourteen patients were already been published (De Backer et al, 2007b). After completion excluded because of cancer recurrence, and one patient was of the programme, repeated testing showed a continuation and excluded because of serious co-morbidity. Four patients left during stabilisation of the muscle strength level (Figure 2) and peak VO . the follow-up period for personal reasons and were considered Muscle strength was significantly higher in patients who completed non-adherent dropouts, resulting in a dropout rate of 6%. Of the the resistance training programme than in the comparison group. 27 patients who proved eligible to participate in the comparison Questionnaire outcomes indicate an overall improvement imme- group, 22 took part in the exercise tests and completed the diately after rehabilitation on several scales of quality of life and of questionnaires, resulting in a dropout rate of 23%. There were no fatigue, especially physical fatigue. This improvement was also significant differences in gender, age, and cancer diagnosis maintained 1 year later. However, there were no differences in between the intervention and the comparison groups. Moreover, quality of life, fatigue, and peak VO between the intervention and there were no significant differences in gender, age, and cancer the comparison groups. & 2008 Cancer Research UK British Journal of Cancer (2008) 99(1), 30 – 36 Clinical Studies Clinical Studies Long-term effects of cancer rehabilitation IC De Backer et al Table 2 Effects of training on muscle strength, cardiopulmonary function, fatigue, and quality of life on different time points Long-term (week 68) Baseline (week 0) Post-rehabilitation (week 18) Outcome measure Intervention group Intervention group Intervention group Comparison group Muscle strength (1-RM/kg) a c e Vertical row 0.48 (0.16) 0.69 (0.20) 0.68 (0.20) 0.46 (0.11) a c e Leg press 1.96 (0.51) 2.79 (0.62) 2.89 (0.74) 2.20 (0.51) a c e Bench press 0.30 (0.11) 0.46 (0.15) 0.45 (0.15) 0.30 (0.11) a c e Pull over 0.12 (0.05) 0.25 (0.08) 0.26 (0.10) 0.13 (0.06) a c e Lunge 0.20 (0.09) 0.42 (0.17) 0.46 (0.16) 0.21 (0.10) a c e Abdominal crunch 0.39 (0.14) 0.60 (0.17) 0.64 (0.18) 0.46 (0.13) Cardiopulmonary outcomes 1 1 b d Peak oxygen consumption (ml min kg ) 25.7 (6.3) 28.9 (6.7) 29.3 (8.4) 27.8 (5.6) 1 b d Peak power output (W kg ) 2.0 (0.6) 2.3 (0.7) 2.5 (0.8) 2.2 (0.6) b d Peak heart rate (beats per min) 167 (17) 172 (14) 168 (20) 165 (18) 1 1 b d Ventilatory threshold (ml min kg ) 19.2 (4.7) 22.3 (5.7) 23.5 (7.1) 22.2 (4.9) MFI b d General fatigue 13.1 (4.5) 9.2 (4.1) 9.9 (4.4) 10.6 (4.4) b d Reduced activity 11.8 (4.4) 8.1 (3.4) 8.2 (3.8) 8.8 (4.3) b d Mental fatigue 10.0 (4.4) 8.8 (3.8) 8.4 (4.0) 7.9 (4.2) Physical fatigue 13.7 (4.1) 8.1 (3.5) 9.2 (4.0) 9.9 (4.8) Reduced motivation 8.7 (3.1) 7.7 (2.8) 7.8 (3.5) 8.4 (4.1) HRQOL b d Physical functioning 72.4 (19.2) 84.2 (19.0) 85.5 (18.5) 81.8 (18.4) b d Role functioning 60.3 (24.0) 79.5 (21.1) 79.4 (22.5) 83.3 (20.6) b d Emotional functioning 75.6 (20.2) 85.7 (18.8) 84.1 (18.4) 81.3 (20.7) Cognitive functioning 76.5 (24.4) 83.8 (21.5) 85.6 (17.3) 82.6 (19.3) b d Social functioning 68.4 (29.3) 82.5 (21.6) 82.3 (24.2) 84.1 (20.8) b d Fatigue 43.6 (23.4) 22.0 (18.8) 24.8 (22.0) 29.8 (21.3) HRQOL¼ health-related quality of life; MFI¼ multidimensional fatigue index; 1-RM¼ one-repetition maximum. All data are means (s.d.). Significant difference, Po0.01, baseline b c and post-rehabilitation (repeated measure analyses). Significant difference, Po0.01, baseline and post-rehabilitation (paired t-tests). Significant difference, Po0.01, baseline and d e week 68 (repeated measure analyses). Significant difference, Po0.01, baseline and week 68 (paired t-tests). Significant difference, Po0.01, the intervention and comparison groups (independent sample t-tests). 3.5 on their quality of life (Lucia et al, 2003; Knols et al, 2005). Despite the mounting evidence of the significance of physical activity 3.0 after cancer treatment, there are presently only four studies that leg press (kg) have assessed the long-term effects of physical rehabilitation 2.5 programmes. Two studies examined the long-term effect of a home-based 2.0 training programme (Demark-Wahnefried et al, 2006; Thorsen 1.5 et al, 2007). Demark-Wahnefried et al evaluated a 6-month home- based diet and exercise programme (telephone counselling and 0.8 mailed materials) by telephone interview at 6 and 12 months after 0.7 the start. This study included only older breast and prostate cancer vertical row (kg) 0.6 patients (X65 years). In the long term (12 months), there were no abdominal crunch (kg) 0.5 significant differences between the intervention and the compar- lunge (kg) 0.4 ison groups in physical functioning, diet quality index, fatigue, and bench press (kg) 0.3 pull over (kg) energy expenditure as measured by telephone questionnaires 0.2 (Demark-Wahnefried et al, 2006). Thorsen et al recently published 0.1 their long-term data of a randomised study of a 3-month home- based training programme. In contrast to our study, the favourable 0 8 16 24 32 40 48 56 64 72 effect on cardiopulmonary functioning could not be sustained Time period (weeks) during a 12-month follow-up. The researchers concluded that for a Figure 2 Muscle strength from start of rehabilitation up to 12 months longer-lasting effect over time, a longer intervention period and after completing rehabilitation. more intense exercise were needed (Thorsen et al, 2007). Another possible explanation for the lack of long-term effects is the supervised training used in our study rather than the home-based There is preliminary evidence that physical activity plays a role training programmes used in the previous studies. The multiple in the primary and secondary prevention of cancer (Stein and visits after the programme for testing may have contributed to the Colditz, 2004; Holmes et al, 2005). Several randomised, controlled persistent effect in our programme. trials have examined the short-time effects of physical activity after The third study that examined the long-term effects of training the diagnosis of cancer. Overall, most studies demonstrated that in cancer patients is by Carlson et al. This study examined the physical training programmes had beneficial effects on cancer effects of supervised aerobic exercise training after 12 months in 12 patients’ physical or psychosocial capacity and, as a consequence, patients after allogeneic haematopoietic stem cell transplantation. British Journal of Cancer (2008) 99(1), 30 – 36 & 2008 Cancer Research UK Relative strength (1−RM/body weight (kg)) Long-term effects of cancer rehabilitation IC De Backer et al Significant improvements in fatigue, ventilatory threshold, and Our study design has some shortcomings. First, the different stroke volume were found (Carlson et al, 2006). The fourth study time intervals between last treatment and long-term test for the of Berglund et al evaluated a training programme over a 1-year comparison group (169 weeks) and the training group (96 weeks). follow-up period. The intervention group improved significantly However, we expect that this longer time span (if it has caused more than the comparison group in physical strength and physical bias) will be in favour of the comparison group because this group activity levels, both of which were evaluated by means of has more time for spontaneous recovery after intensive treatment. questionnaires. In our study, the cardiopulmonary function and Second, the lack of baseline measurements in the comparison muscle strength were assessed by exercise tests (peak VO and group is a limitation of the current study. These shortcomings 1-RM), which are more valid and reliable outcome measures. could be overcome by a prospective, randomised, controlled As cancer rehabilitation is a relatively new area of research, clinical trial. However, such a study design is not practical for there is no consensus about the optimal type of training in a exercise intervention trials. First, patients cannot be blinded to rehabilitation programme. Exercise interventions vary consider- their treatment; only the outcome assessor can be blinded to group ably from brief instructions of home-based exercises to highly allocation. Second, when patients are participating in a training structured, supervised exercise sessions on strength equipment study and are randomised to the control or waiting group, they (Conn et al, 2006). It is remarkable that most studies only used start to get more active spontaneously. Particularly in a group of aerobic exercises such as walking or stationary cycling in their cancer patients, subjects might come into contact with other rehabilitation programmes (Courneya et al, 2003), as one of the subjects. Finally, the short-term benefits of exercise are recognised side effects of cancer and its treatment is muscle atrophy (Argiles in research and clinics. It could be considered unethical to restrain et al, 2005). To improve muscle strength and increase muscle patients from an exercise-containing rehabilitation programme. mass, resistance training is more important than aerobic exercise. Therefore, we believe that our study design is appropriate in Also, considerable evidence now suggests that the ability to cancer rehabilitation research, especially when long-term effects perform physical tasks in daily life is determined by a threshold are studied. level of muscular resistance (Brill et al, 2000). As a consequence, resistance training seems to be the programme of choice for regaining muscle strength and, in this way, improving activities of CONCLUSION daily living and HRQOL (Brill et al, 2000). In addition, in cancer patients, muscle strength is related to quality-of-life aspects with This is the first study that describes the long-term effects of a high- correlations ranging from 0.47 to 0.75 (De Backer et al, 2007b). intensity resistance training programme in cancer patients. Results The results of the questionnaires, HRQOL, and MFI, did not indicate that after a 12-month follow-up, the beneficial effects on muscle strength, cardiopulmonary function, HRQOL, and fatigue differ between the two groups. A possible explanation for this is were sustained. Muscle strength was significantly higher in the the high outcome values in the questionnaires. It is most likely that intervention group than in the comparison group. Based on these a ceiling effect is reached a rather long time after cancer treatment. results, we suggest that guidelines for rehabilitation in oncology Cancer patients may be satisfied with their ‘survival status’ and patients should include high-intensity resistance training. score high in all QOL questionnaires despite existing limitations and complaints. This experience is familiar to other researchers (van de Poll-Franse et al, 2006). 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Published: Jun 24, 2008

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