Literature DB >> 26743698

Progressive resistance training in Parkinson's disease: a systematic review and meta-analysis.

Mikhail Saltychev1, Esa Bärlund2, Jaana Paltamaa3, Niina Katajapuu4, Katri Laimi1.   

Abstract

OBJECTIVES: To investigate if there is evidence on effectiveness of progressive resistance training in rehabilitation of Parkinson disease.
DESIGN: Systematic review and meta-analysis. DATA SOURCES: Central, Medline, Embase, Cinahl, Web of Science, Pedro until May 2014. Randomised controlled or controlled clinical trials. The methodological quality of studies was assessed according to the Cochrane Collaboration's domain-based evaluation framework. DATA SYNTHESIS: random effects meta-analysis with test for heterogeneity using the I² and pooled estimate as the raw mean difference. PARTICIPANTS: Adults with primary/idiopathic Parkinson's disease of any severity, excluding other concurrent neurological condition.
INTERVENTIONS: Progressive resistance training defined as training consisting of a small number of repetitions until fatigue, allowing sufficient rest between exercises for recovery, and increasing the resistance as the ability to generate force improves. COMPARISON: Progressive resistance training versus no treatment, placebo or other treatment in randomised controlled or controlled clinical trials. PRIMARY AND SECONDARY OUTCOME MEASURES: Any outcome.
RESULTS: Of 516 records, 12 were considered relevant. Nine of them had low risk of bias. All studies were randomised controlled trials conducted on small samples with none or 1 month follow-up after the end of intervention. Of them, six were included in quantitative analysis. Pooled effect sizes of meta-analyses on fast and comfortable walking speed, the 6 min walking test, Timed Up and Go test and maximal oxygen consumption were below the level of minimal clinical significance.
CONCLUSIONS: There is so far no evidence on the superiority of progressive resistance training compared with other physical training to support the use of this technique in rehabilitation of Parkinson's disease. SYSTEMATIC REVIEW REGISTRATION NUMBER: PROSPERO 2014:CRD42014009844. Published by the BMJ Publishing Group Limited. For permission to use (where not already granted under a licence) please go to http://www.bmj.com/company/products-services/rights-and-licensing/

Entities:  

Keywords:  GENERAL MEDICINE (see Internal Medicine); REHABILITATION MEDICINE

Mesh:

Year:  2016        PMID: 26743698      PMCID: PMC4716165          DOI: 10.1136/bmjopen-2015-008756

Source DB:  PubMed          Journal:  BMJ Open        ISSN: 2044-6055            Impact factor:   2.692


Search in six major databases. More relevant studies identified compared to previous meta-analyses. Reviewing process followed recommendations by Cochrane Collaboration. Owing to the uncertain definition of progressive resistance training, it is possible that some relevant studies remained undetected.

Introduction

Principles of progressive resistance training (PRT) have remained essentially unchanged since 1945–1949, when US Army physician Captain Thomas L. Delorme introduced this technique as an efficient way to rehabilitate soldiers.1 2 For 70 years, PRT has been widely used in rehabilitation of young and physically active people. During the past two decades, use of PRT has also been studied among people with chronic diseases and disabilities3 4 such as hypertension, chronic obstructive pulmonary disorders, chronic low back and neck pain, osteoarthritis, cerebral palsy, stroke and diabetes. In these conditions, PRT may reduce pain, and improve muscle strength and the level of physical activity without significant side effects.3 The data on the effectiveness of PRT in the rehabilitation of people with Parkinson's disease are scarce. The conclusions of recent reviews on the topic show inconsistency of inferences. In a recent systematic review by Brienesse et al5 of five randomised controlled trials (RCT), PRT was found to have a positive effect on muscle strength, mobility, endurance, fat-free mass and performance in functional tasks. Another recent systematic review by Lima et al6 of four controlled trials suggested that PRT could be effective in increasing walking capacity in Parkinson's disease. A narrative review by David et al7 reported a favourable effect of PRT on muscle strength and function and non-motor symptoms of Parkinson's disease. Also, a narrative review by Falvo et al8 emphasised the lack of robust data on the topic. While Lima et al and David et al ended up with a strong conclusion that there is evidence that progressive resistance training should be implemented in Parkinson's disease rehabilitation, the conclusions of Brienesse et al and Falvo et al indicated more cautiously that data are insufficient to make robust recommendations and further research is needed. The purpose of this study was to evaluate the evidence on the effectiveness of PRT in the rehabilitation of people with Parkinson's disease, and to make concrete recommendations for clinical practice.

Methods

Data sources and searches

Criteria for considering studies for this review were based on the PICO (Population, Intervention, Comparison, and Outcome) framework as follows: Patients: Adults with primary/idiopathic Parkinson's disease of any severity, excluding any other concurrent neurological condition. Intervention: Progressive resistance training defined as training which (A) consists of a small number of repetitions until fatigue, (B) allows sufficient rest between exercises for recovery and (C) increases the resistance as patient's ability to generate force improves.3 Comparison: Progressive resistance training versus no treatment, placebo or other treatment in randomised controlled or controlled clinical trials. Outcome: Any outcome. Cochrane Controlled Trials Register (CENTRAL), MEDLINE (via PubMed), EMBASE, CINAHL, Web of Science and Physiotherapy Evidence (Pedro) databases were searched in May 2014 with no restrictions by date or language. The search clauses are presented in online supplementary file 1. In order to avoid missing relevant studies, the use of limits was restricted and further selection was conducted manually. The references of identified articles and reviews were also checked for relevancy.

Study selection

Two independent reviewers (EB and MS) screened the titles and abstracts of articles, assessed the full texts of potentially relevant studies, and rated the methodological quality of included trials (figure 1).
Figure 1

Flow chart of reviewing process.

Flow chart of reviewing process. Disagreements between reviewers were resolved by consensus or by the third reviewer (JP). The more detailed description of the exclusion process is available on request from the corresponding author.

Data extraction and quality assessment

Data needed for meta-analysis were extracted from the included trials using a standardised form based on recommendations by the Cochrane Handbook for Systematic Reviews of Interventions V.5.1.0, part 7.6.9 If a study was reported in more than one publication, the information from multiple reports was collated by extracting data from each report separately and then combining the information of all data collection forms. The methodological quality was assessed according to the Cochrane Collaboration's domain-based evaluation framework.10 Main domains were assessed in the following sequence: (1) selection bias (randomised sequence generation and allocation concealment); (2) performance bias (blinding of participants and personnel); (3) detection bias (blinding of outcome assessment); (4) attrition bias (incomplete outcome data, eg, due to dropouts); (5) reporting bias (selective reporting); (6) other sources of bias. The scores for each bias domain and the final score of risk of systematic bias were graded as low, high or unclear risk.

Data synthesis and analysis

We used a random effects meta-analysis to quantify the pooled effect size of included studies as a more natural choice than fixed effects in the context of multiple clinical trials conducted in diverse settings. In addition, test for heterogeneity supported this choice. The test for heterogeneity was conducted using the I2 statistic describing the percentage of variation across studies originating more from heterogeneity than from chance. We calculated the non-standardised means of difference in change of means for each study and for the pooled study sample. When the SD of difference of changes of groups’ means was not reported, the coefficient of correlation between prevariance and postvariance was set at 0.6. The potential publication bias was evaluated by Egger's test for asymmetry of the funnel plot (test for the Y intercept=0 from the linear regression of normalised effect estimate against precision), where the trim-and-fill method was used to impute studies into a funnel plot to correct asymmetry. All calculations for the meta-analysis were performed using MIX 2.0. V.2.0.1.4. BiostatXL, 2011, available from http://www.meta-analysis-made-easy.com, Comprehensive Meta Analysis CMA, V.2.2.064, available from http://www.meta-analysis.com, and Microsoft Excel 2013.

Results

The search resulted in 516 records. Of them, 297 study reports were removed as being duplicates, conference proceedings, posters, theses, etc. After including five reports found from the reference lists of identified review articles, 224 records were screened on the basis of their titles and abstracts. Of these records, full texts of 58 reports were screened more thoroughly, and 12 were considered relevant for qualitative analysis11–22 (details in figure 1). Similarity of outcome measures, needed for meta-analysis, was found among five different reports.11 14 20–22 Additionally, two subgroups in the study by DiFrancisco-Donoghue et al17 (one sample comparing PRT with usual care and another comparing PRT and vitamins with vitamins alone) were used in meta-analysis.

Qualitative analysis of 12 included studies

Table 1 shows the descriptive characteristics of included studies. Publication years varied from 1997 to 2014.
Table 1

Descriptive characteristics of included studies

Study/year/countryCases/controls, N (% men)Intensity and durationResponse to treatment
BaselineFollow-upAge *Case treatmentControl treatment
Allen2010Australia24 (54)/24 (54)21/2466/68Progressive lower limb strengthening and balance exercises (a monthly exercise class, remaining exercise sessions at home). Standardised falls prevention advice (booklet)40–60 min 3 times per week for 6 monthsUsual care. Standardised falls prevention advice (booklet)Insignificant difference
Bloomer2008USA8 (50)/8 (50)6/761/57Three sets of 5–8 repetitions: leg press, leg curl and calf press. Increased weight by 5–10% when 8 repetitions were completed for all 3 setsTwo times per week for 2 monthsUsual activityPositive
Bridgewater1997Australia13 (69)/13 (54)13/1367/6615 min warm-up. Trunk muscles (back extensors and abdominals): 10 repetitions of 7 s isometric contractions with 7 s rest. Progression: as individual ability and improvement allowedTwo times per week for 3 monthsUsual activity and ‘interest talks’ on health issues Once every 3 weeksPositive
Combs2013USA17 (65)/14 (71)11/1167/6815 min warm-up. Boxing circuit, endurance. Progression: self-progressed by completing more repetitions during each training bout as intensely as tolerated24–36×90 min for 3 monthsStrengthening, endurance and balance exercisesPositive
Corcos2013USA24 (58)/24 (58)20/1859/59Strength: 1–3 sets of 8×6–9 s repetitions; speed: 2 sets of 12 repetitions. Progression: 5% depending on one repetition maximumTwo times per week for 24 monthsStretches, balance exercises, breathing and non-progressive strengtheningPositive
Cruise2011Australia15 (60)/13 (69)14/1059/615 min warm-up (walking, stationary cycling and stretching), 6 resistance exercises. Progression: 5–10% based on one repetition maximum. Aerobic component 25–30 min60 min 2 times per week for 3 monthsUsual activitiesPositive
DiFrancisco-Donoghue2012USA10 (77)/9 (33) †12 (56)/10 (56)‡9/9†9 9‡68/68†67/69‡20 min aerobic exercise, weight training 2 sets of 8–15 repetitions with 30 s rest between. Progression: weight increased by 5 lbs when 15 repetitions per set were achieved40 min 2 times per week for 1½ monthsUsual activities.Vitamins: folic acid, B12 and B6Insignificant difference
Hass2012USA9 (77)/9 (77)9/964/675 min warm-up, 2 sets of 12–20 repetitions of six exercises, 5 min break between sets. Progression based on one repetition maximumTwo times per week for 2½ monthsUsual activitiesPositive
Hirsch2003USA6/96/7§6/9¶71/76Balance+resistance training. Resistance training: 15 min lower extremities, 1 set of 12 repetitions, and 2 min rest between exercises. Progression based on 4 repetitions maximumThree times per week for 2½ monthsBalance trainingPositive
Paul2014Australia20 (65)/20 (60)18/18§ 19/19**68/65Three sets of 8 repetitions for 4 muscle groups. Progression: increase by 5% when 10 repetitions achieved45 min 2 times per week for 3 monthsLow intensity exercises for the trunk, leg flexors, leg extensors and hip abductorsPositive
Schilling2010USA9/98 (63)/7 (57)61/57Warm-up, 3 sets of 5–8 repetitions of the leg press, leg curl and calf press. Progression: when 8 repetitions for all 3 sets were completed, the weight was increased by 5–10%Two times per week for 2 monthsStandard carePositive
Shulman2013USA28††/26‡‡22 (82)††/22(73)‡‡65††/66‡‡Resistance exercises: 2 sets of 10 repetitions (leg press, leg extension and leg curl). Progression: weight increased as toleratedThree times per week for 3 months50 min of lower intensity treadmillPositive on muscle strength

*Years in means.

†Training versus controls.

‡Training and vitamins versus vitamins.

§Strength.

¶Balance.

**Mobility and balance.

††Stretching and Resistance Training.

‡‡Lower-Intensity treadmill training (higher-intensity treadmill excluded as progressive training of different type).

Descriptive characteristics of included studies *Years in means. †Training versus controls. ‡Training and vitamins versus vitamins. §Strength. ¶Balance. **Mobility and balance. ††Stretching and Resistance Training. ‡‡Lower-Intensity treadmill training (higher-intensity treadmill excluded as progressive training of different type). Eight studies were conducted in the USA and four in Australia. The size of the intervention groups at the end of follow-up varied from 6 to 22. Most of the studies only reported pretreatment/post-treatment results. Two of 12 studies also had a short 1 month follow-up after intervention.13 19 In the samples, male gender predominated and the mean age of participants varied from 59 to 71 years. The implementation schemes of PRT varied widely across the studies. The progression of training load was usually defined by one repetition maximum, by participant's fatigue, or by achieving an agreed amount of repetitions. The duration of intervention varied from 1.5 to 24 months with a frequency of two or three times per week. Of 12 studies, 10 reported a positive effect of intervention. Six studies compared progressive resistance training with weakly defined ‘usual activities’,11–13 16–18 four with different low-intensity strengthening, endurance or balance exercises,14 15 19 20 one with the use of vitamins,17 and one with treadmill training.22 It is self-evident that most of the patients with PD have more than one treatment. Thus, when comparing PRT and vitamins against only vitamins, omitting vitamins was accepted by us as approximation and the study by DiFrancisco-Donoghue et al17 could be included into this review. The outcome measures of included studies spread across a wide spectrum and are presented in online supplementary file 2 along with their reported main results. The risk of bias was considered low for nine studies and high for three studies (table 2). The most frequent source of potential bias was the performance bias related to the inadequate or insufficiently reported blinding procedure.
Table 2

Risk of bias of included studies

StudyRandom sequence generationAllocation concealmentBlinding of participants and personnelBlinding of outcome assessmentIncomplete outcome dataSelective reportingOther sources of biasTotal risk of bias
Allen et al11LowLowHighLowLowLowLowLow
Bloomer et al12LowUnclearHighLowLowLowLowLow
Bridgewater et al13HighUnclearHighHighLowLowLowHigh
Combs et al14LowLowHighLowLowLowLowLow
Corcos et al15LowLowHighLowLowLowLowLow
Cruise et al16HighUnclearHighHighLowLowLowHigh
DiFrancisco-Donoghue et al17LowUnclearHighHighLowLowLowLow
Hass et al18LowUnclearHighHighLowLowLowLow
Hirsch et al19HighUnclearHighHighLowLowLowHigh
Paul et al20LowUnclearHighLowLowLowLowLow
Schilling et al21LowUnclearHighHighLowLowLowLow
Shulman et al22LowLowLowLowLowLowLowLow
Risk of bias of included studies The included studies reported positive effects of PRT on the score of the Freezing of Gait Questionnaire,11 oxidative stress,12 gait velocity and endurance,14 the scores of Parkinson's Disease Rating Scale and Modified Fitness Counts,15 cognitive functioning (demonstrating no effect on mood or disease-specific quality of life),16 gait initiation performance18 and muscle strength of trunk and/or lower extremities.13 19–22 One study found PRT to be more effective at increasing glutathione levels and decreasing homocysteine levels compared with controls but without differences when compared with vitamin intake.17

Meta-analyses of six included studies

The risk of bias of all six studies was considered low. Five different meta-analyses were conducted on two to four samples sized from 6 to 22 participants each. When appropriate, measurement units were converted into metric units. Table 3 and online supplementary figures 3A–E present the input data and the results of all five syntheses.
Table 3

Results of meta-analyses

Outcome (units), studyCases, mean (SD)
Controls, mean (SD)
Effect size
I2 (%)Egger's regression
BaselineFollow-upNBaselineFollow-upNRaw mean difference95% CIIntercept95% CI
Fast walking speed (ms)0.060.02 to 0.1161−3.27−69.0 to 62.4
 Allen et al111.47 (0.38)1.61 (0.35)211.54 (0.35)1.48 (0.43)240.2−0.001 to 0.40
 Paul et al200.02 (0.16)*60.01 (0.19)*90.01−0.18 to 0.2
 Shulman et al220.84 (0.05)0.84 (0.05)220.85 (0.05)0.79 (0.05)220.060.03 to 0.09
Comfortable walking speed (ms)0.030.01 to 0.0515−1.34−13.8 to 11.2
 Allen et al111.07 (0.27)1.09 (0.26)211.04 (0.25)1.06 (0.32)240.0−0.15 to 0.15
 Combs et al141.06 (1.08)1.10 (1.10)111.15 (0.72)1.22 (0.64)110.03−0.65 to 0.71
 Paul et al200.06 (0.16)*60.05 (0.12)*90.01−0.13 to 0.15
 Shulman et al220.72 (0.05)0.71 (0.05)220.73 (0.04)0.69 (0.04)220.030.01 to 0.05
Timed Up and Go Test (s)−0.71−1.47 to 0.060−5.28−61.1 to 50.5
 Combs et al148.05 (15.12)7.12 (14.62)117.64 (7.39)7.12 (5.47)11−0.41−9.04 to 8.22
 Paul et al20−1.3 (2.7)*6−0.1 (2.0)*9−1.2−3.57 to 1.17
 Schilling et al215.8 (0.50)5.7 (0.80)97.5 (1.18)6.75 (1.21)9−0.65−0.47 to 0.06
6 min walk (m)16.677.86 to 25.4847−6.14−42.8 to 30.5
 Combs et al14405.0 (549.1)457.0 (669.7)11484.4 (301.2)478.7 (183.9)1157.7−300.21 to 415.6
 Schilling et al21537.7 (88.1)586.9 (51.0)9468.8 (83.3)493.9 (64.3)924.1−39.97 to 88.17
 Shulman et al22§32.6 (14.6)*2249.1 (15.5)*2216.57.86 to 25.48
Maximal oxygen consumption (mL/kg/min)−1.6−1.93 to −1.278526.18−103.5 to 155.9
 DiFrancisco-Donoghue et al1713.3 (2.7)11.6 (2.4)913.0 (2.8)12.8 (2.9)9−1.5−3.74 to 0.74
 DiFrancisco-Donoghue et al17**11.5 (2.1)10.0 (2.0)913.9 (2.8)14.6 (2.6)9−2.2−4.19 to −0.22
 Shulman et al22−0.052 (0.4) *221.53 (0.7)*22−1.6−1.93 to −1.25

*Change from baseline for each group.

†Converted from seconds (50 feet distance) to ms.

‡Converted from seconds (10 m distance) to ms.

§Converted from feet to metres.

¶Exercise versus controls.

**Exercise+vitamins versus vitamins.

Results of meta-analyses *Change from baseline for each group. †Converted from seconds (50 feet distance) to ms. ‡Converted from seconds (10 m distance) to ms. §Converted from feet to metres. ¶Exercise versus controls. **Exercise+vitamins versus vitamins. The effect of PRT on fast walking speed was assessed by pooling samples of three studies.11 20 22 The pooled sample consisted of 49 cases versus 55 controls. The pooled effect size was 0.06 ms (95% CI 0.02 to 0.11) in favour of intervention, but below the minimal detectable change of 0.25 ms as suggested previously.23 The I2 was 61%, indicating substantial heterogeneity. The effect of PRT on comfortable walking speed was assessed by pooling samples of four studies.11 14 20 22 The pooled sample consisted of 60 cases versus 66 controls. The pooled effect size was 0.03 ms (95% CI 0.01 to 0.05) in favour of intervention, but below the minimal detectable change of 0.18 ms as suggested previously.23 The I2 was 15%, indicating insignificant heterogeneity. The effect of PRT on Timed Up and Go test was assessed by pooling samples of three studies.14 20 21 The size of pooled sample was 26 cases versus 29 controls. The pooled effect size was statistically insignificant −0.71 s (95% CI −1.47 to 0.06) in favour of intervention and below the minimal detectable change of 3.5 s as suggested previously.24 The I2 was 0%, indicating insignificant heterogeneity. The effect of PRT on the 6 min walk test was assessed by pooling samples of three studies.14 21 22 The pooled sample was 42 cases versus 42 controls. The pooled effect size was 16.67 m (95% CI 7.86 to 25.48) in favour of intervention, but below the minimal detectable change of 82 m as suggested previously.23 The I2 was 47%, indicating moderate heterogeneity. The effect of PRT on maximal oxygen consumption was assessed by pooling samples of two studies17 22 including three samples: two different samples from the study by DiFrancisco-Donoghue et al and one sample from the study by Shulman et al. The pooled sample was 40 cases versus 40 controls. The pooled effect size was −1.6 mL/kg/min (95% CI −1.93 to −1.27) in favour of intervention and below the minimal clinically significant difference of 2 mL/kg/min as suggested previously.25 The I2 was 85%, indicating substantial heterogeneity. The Egger's test for asymmetry of the funnel plot did not reveal a potential publication bias in any of the syntheses.

Discussion

In this systematic review of 12 RCTs, no evidence was found on the superiority of PRT in the rehabilitation of people with idiopathic Parkinson's disease when compared to other training or to usual activities. Few studies conducted on small sample sizes with short periods of follow-up reported some positive effects of PRT on freezing symptoms, gait, cognitive performance and muscle strength. Meta-analyses of these studies did not find clinically significant effects of PRT on walking speed, walking distance, Timed Up and Go test or aerobic performance. The case and control treatments, as well as intensity, duration and frequency of PRT, employed in the selected studies were diverse and sometimes hardly comparable. The included studies have been conducted on relatively small samples and the effects were followed up for only a few months at most. In this review, a ‘small number of repetitions’ was defined according to the classic work of DeLorme and Watkins in 1948.2 The use of a more precise definition given by the American College of Sports Medicine, defining a ‘small number of repetitions’ as ≤12 repetitions, might alter our results.26 Owing to the uncertain definition of PRT, it is possible that some relevant studies remained undetected. However, we used very wide search clauses and performed the rest of the search and selection manually in order to avoid missing the potentially relevant reports. The data from the included records were extracted by one researcher, which might affect the objectivity of the process, even if the data extracted were presented to all the authors for the discussion and approved. When compared to recent systematic reviews on the topic, we identified considerably more relevant studies. The reason for being able to identify more relevant reports than previous reviews on the topic did was probably the fact that the search we performed used very few limits, relying on the manual (though time-consuming) fine-tuning of initial search results. Our results are in line with a recent review by Brienesse et al5 which reported lack of evidence on the effectiveness of PRT. We ended up, however, with a more robust conclusion that, based on several small-sample good-quality RCTs, there is limited evidence on PRT being no more effective in Parkinson's disease than other physical training schemes. In contrast to our finding, a review by Lima et al6 suggested that “progressive resistance training should be implemented in Parkinson’s disease rehabilitation” and a review by David et al7 concluded that “…there is a strong rationale for the use of PRE [progressive resistance exercise] as an adjunct treatment in PD [Parkinson's disease]…” Such strong recommendations cannot be supported by our results. Since there is no evidence on the superiority or better safeness of one specific training scheme over another in patients with PD, rehabilitation providers may include or avoid PRT depending on the settled practice and costs of a particular rehabilitation programme. In our review, the risk of bias was considered low in 9 of 12 studies. Problems, however, arise from other than methodological issues covered by the scale we used. It is likely that the included studies had insufficient statistical power, undetermined clinical significance and mostly insufficiently described treatment in control groups. They also differed in the degree of disease severity. Implemented schemes of PRT varied from weightlifting to boxing exercises. Even if a study was methodologically well planned and executed, the level of statistical significance is rarely achieved in small samples. Only very large treatment effect sizes could be detected in trials with 20 or less participants. Additionally, statistically significant results, if observed, may not exceed the level of clinical significance, and this should also be taken into account when making clinical recommendations. For example, our meta-analyses on fast and comfortable walking speed and maximal oxygen consumption showed statistical but not clinical significance of pooled effect sizes. The statistically significant pooled effect size observed in meta-analysis on the 6 min walk test fell below the level of minimal detectable change for this test. Unexpectedly, none of the trials followed the effects of PRT for more than 1 month after the end of a supervised training programme. It has been reported previously that the beneficial effects of training may persist for several months after the cessation of training.27 The most common source of potential systematic bias in the selected studies was the lack of blinding of participants and personnel. This source of bias is hardly avoidable when physical therapy is involved as the involvement is based on the close participation of the patient and the therapist in the entire chain of planning, performing and assessing the intervention. While it is barely preventable, it could be statistically controlled, for example, by using repeated measures of expectancy and beliefs about the demands of the research throughout the trial.28 The search was a year old at the time of accepting this review for publication. Thus, the additional verifying search was conducted on Pubmed seeking relevant papers published between April 2014 and October 2015 and using the same clauses as did previous search. Only one potentially relevant trial was identified. That RCT by Prodoehl et al29 compared the effects of progressive resistance exercises and a modified Fitness Counts program on the physical function of people with moderate PD. That study used the subset of data used previously in the paper by Corcos et al included in our analysis. The main outcome used by Prodoehl et al included a Modified Physical Performance Test, five times sit to stand test, Functional Reach Test, Timed Up and Go, Berg Balance Scale, 6 min walk test and 50 feet walking speed. In a 2-year follow-up, both groups showed improvements across all studied outcome measures, except for the 6 min walk test without significant differences between treatment methods. It is reasonable to assume that the findings of that trial would not affect our main results. To make definite clinical recommendations possible, further research should focus on randomised trials on larger sample sizes and with sufficient follow-up periods after the end of the intervention. The safety of PRT in a target population should also be evaluated in comparison with other types of physical training. Further studies may also reveal the effects of resistance training on such important outcome measures as quality of life, activities of daily living, cost-effectiveness, and muscle strength, which are left out of the scope of this review.

Conclusions

Even if physical training is important for health and functioning, there is so far no evidence on the superiority of progressive resistance training compared with other treatments to support the use of this technique in rehabilitation of idiopathic Parkinson's disease. There is limited evidence on progressive resistance training being ineffective in Parkinson's disease compared with other physical training schemes.
  25 in total

1.  Progressive resistance training improves gait initiation in individuals with Parkinson's disease.

Authors:  Chris J Hass; Thomas A Buckley; Chris Pitsikoulis; Ernest J Barthelemy
Journal:  Gait Posture       Date:  2012-01-23       Impact factor: 2.840

2.  Technics of progressive resistance exercise.

Authors:  T L DELORME; A L WATKINS
Journal:  Arch Phys Med Rehabil       Date:  1948-05       Impact factor: 3.966

Review 3.  Progressive resistance exercise improves strength and physical performance in people with mild to moderate Parkinson's disease: a systematic review.

Authors:  Lidiane Oliveira Lima; Aline Scianni; Fátima Rodrigues-de-Paula
Journal:  J Physiother       Date:  2013-03       Impact factor: 7.000

4.  The effects of balance training and high-intensity resistance training on persons with idiopathic Parkinson's disease.

Authors:  Mark A Hirsch; Tonya Toole; Charles G Maitland; Robert A Rider
Journal:  Arch Phys Med Rehabil       Date:  2003-08       Impact factor: 3.966

5.  Two-year exercise program improves physical function in Parkinson's disease: the PRET-PD randomized clinical trial.

Authors:  Janey Prodoehl; Miriam R Rafferty; Fabian J David; Cynthia Poon; David E Vaillancourt; Cynthia L Comella; Sue E Leurgans; Wendy M Kohrt; Daniel M Corcos; Julie A Robichaud
Journal:  Neurorehabil Neural Repair       Date:  2014-06-24       Impact factor: 3.919

6.  Effect of short-term exercise training on aerobic fitness in patients with abdominal aortic aneurysms: a pilot study.

Authors:  E Kothmann; A M Batterham; S J Owen; A J Turley; M Cheesman; A Parry; G Danjoux
Journal:  Br J Anaesth       Date:  2009-07-23       Impact factor: 9.166

7.  Effect of resistance training on blood oxidative stress in Parkinson disease.

Authors:  Richard J Bloomer; Brian K Schilling; Robyn E Karlage; Mark S Ledoux; Ronald F Pfeiffer; Jonathan Callegari
Journal:  Med Sci Sports Exerc       Date:  2008-08       Impact factor: 5.411

8.  Randomized clinical trial of 3 types of physical exercise for patients with Parkinson disease.

Authors:  Lisa M Shulman; Leslie I Katzel; Frederick M Ivey; John D Sorkin; Knachelle Favors; Karen E Anderson; Barbara A Smith; Stephen G Reich; William J Weiner; Richard F Macko
Journal:  JAMA Neurol       Date:  2013-02       Impact factor: 18.302

9.  Leg muscle power is enhanced by training in people with Parkinson's disease: a randomized controlled trial.

Authors:  Serene S Paul; Colleen G Canning; Jooeun Song; Victor S C Fung; Catherine Sherrington
Journal:  Clin Rehabil       Date:  2013-11-04       Impact factor: 3.477

10.  Addressing risk of bias in trials of cognitive behavioral therapy.

Authors:  Katherine S Button; Marcus R Munafò
Journal:  Shanghai Arch Psychiatry       Date:  2015-06-25
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  9 in total

Review 1.  Can Resistance Training Improve Upper Limb Postural Tremor, Force Steadiness and Dexterity in Older Adults? A Systematic Review.

Authors:  Justin W L Keogh; Sinead O'Reilly; Ethan O'Brien; Steven Morrison; Justin J Kavanagh
Journal:  Sports Med       Date:  2019-08       Impact factor: 11.136

2.  Efficacy and evaluation of therapeutic exercises on adults with Parkinson's disease: a systematic review and network meta-analysis.

Authors:  Yong Yang; Guotuan Wang; Shikun Zhang; Huan Wang; Wensheng Zhou; Feifei Ren; Huimin Liang; Dongdong Wu; Xinying Ji; Makoto Hashimoto; Jianshe Wei
Journal:  BMC Geriatr       Date:  2022-10-21       Impact factor: 4.070

Review 3.  Exercise-induced increase in brain-derived neurotrophic factor in human Parkinson's disease: a systematic review and meta-analysis.

Authors:  Mark A Hirsch; Erwin E H van Wegen; Mark A Newman; Patricia C Heyn
Journal:  Transl Neurodegener       Date:  2018-03-20       Impact factor: 8.014

Review 4.  Systematic review on strength training in Parkinson's disease: an unsolved question.

Authors:  Ileana Ramazzina; Benedetta Bernazzoli; Cosimo Costantino
Journal:  Clin Interv Aging       Date:  2017-03-31       Impact factor: 4.458

Review 5.  Role of Physical Activity in Parkinson's Disease.

Authors:  Ketaki S Bhalsing; Masoom M Abbas; Louis C S Tan
Journal:  Ann Indian Acad Neurol       Date:  2018 Oct-Dec       Impact factor: 1.383

6.  Concussion Guidelines Step 2: Evidence for Subtype Classification.

Authors:  Angela Lumba-Brown; Masaru Teramoto; O Josh Bloom; David Brody; James Chesnutt; James R Clugston; Michael Collins; Gerard Gioia; Anthony Kontos; Avtar Lal; Allen Sills; Jamshid Ghajar
Journal:  Neurosurgery       Date:  2020-01-01       Impact factor: 4.654

7.  Effectiveness of aerobic and resistance training on the motor symptoms in Parkinson's disease: Systematic review and network meta-analysis.

Authors:  Xiao Zhou; Peng Zhao; Xuanhui Guo; Jialin Wang; Ruirui Wang
Journal:  Front Aging Neurosci       Date:  2022-08-01       Impact factor: 5.702

8.  Effects of Olympic Combat Sports on Health-Related Quality of Life in Middle-Aged and Older People: A Systematic Review.

Authors:  Pablo Valdés-Badilla; Tomás Herrera-Valenzuela; Eduardo Guzmán-Muñoz; Pedro Delgado-Floody; Cristian Núñez-Espinosa; Matias Monsalves-Álvarez; David Cristóbal Andrade
Journal:  Front Psychol       Date:  2022-01-05

Review 9.  Cognitive and Physical Intervention in Metals' Dysfunction and Neurodegeneration.

Authors:  Anna Jopowicz; Justyna Wiśniowska; Beata Tarnacka
Journal:  Brain Sci       Date:  2022-03-03
  9 in total

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