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Walking on four limbs: A systematic review of Nordic Walking in Parkinson disease
Parkinsonism and Related Disorders 38 (2017) 8e12
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Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Review article
Walking on four limbs: A systematic review of Nordic Walking in Parkinson disease Federica Bombieri a, Federico Schena a, Barbara Pellegrini a, b, Paolo Barone c, Michele Tinazzi a, *, 1, Roberto Erro c, d, 1 di Verona, Verona, Italy Department of Neuroscience, Biomedicine and Movement Sciences, Universita CeRiSM (Research Centre of Mountain Sport and Health), University of Verona, Rovereto, Italy c Center for Neurodegenerative Diseases (CEMAND), Department of Medicine and Surgery, Neuroscience Section, University of Salerno, Salerno, Italy d Sobell Department of Motor Neuroscience and Movement Disorders, University College London (UCL) Institute of Neurology, London, United Kingdom a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 October 2016 Received in revised form 2 January 2017 Accepted 5 February 2017
Nordic Walking is a relatively high intensity activity that is becoming increasingly popular. It involves marching using poles adapted from cross-country skiing poles in order to activate upper body muscles that would not be used during normal walking. Several studies have been performed using this technique in Parkinson disease patients with contradictory results. Thus, we reviewed here all studies using this technique in Parkinson disease patients and further performed a meta-analysis of RCTs where Nordic Walking was evaluated against standard medical care or other types of physical exercise. Nine studies including four RCTs were reviewed for a total of 127 patients who were assigned to the Nordic Walking program. The majority of studies reported beneficial effects of Nordic Walking on either motor or nonmotor variables, but many limitations were observed that hamper drawing definitive conclusions and it is largely unclear whether the benefits persist over time. It would appear that little baseline disability is the strongest predictor of response. The meta-analysis of the 4 RCTs yielded a statistically significant reduction of the UPDRS-3 score, but its value of less than 1 point does not appear to be clinically meaningful. Well-designed, large RCTs should be performed both against standard medical care and other types of physical exercise to definitively address whether Nordic Walking can be beneficial in PD. © 2017 Published by Elsevier Ltd.
Keywords: Physical activity Non-pharmacological Rehabilitation Physiotherapy Treadmill
1. Introduction Nordic Walking (NW) is a relatively high intensity activity that involves marching using poles adapted from cross-country skiing poles in order to activate upper body muscles that would not be used during normal walking [1,2]. NW is becoming increasingly popular [3e7]. This probably owes to different reasons including participation in group exercise programmes, which has been shown to be a motivating factor [8], and the low level of perceived exertion. Moreover, NW has the practical advantage that can be done year round in any climate and does not require dedicated facilities or expensive equipments. NW programmes performed in healthy subjects have been demonstrated to increase physical activity levels, muscular
* Corresponding author. P.le L.A. Scuro, 10 Verona, Italy. E-mail address: [email protected] (M. Tinazzi). 1 Equally contributed. http://dx.doi.org/10.1016/j.parkreldis.2017.02.004 1353-8020/© 2017 Published by Elsevier Ltd.
endurance, functional exercise capacity, flexibility, postural stability, stride length and gait pattern [1,9e12]. All these latter become progressively compromised in Parkinson disease (PD) and are only partly ameliorated by pharmacological and/or surgical approaches [13]. As such, NW has been construed to be potentially efficacious in PD [14] and it is increasingly gaining momentum in this condition. However, evidence in this regard is scarce and different studies have produced somewhat contradictory results [14e16]. A recent (2014) Cochrane review aimed to compare different rehabilitation techniques to assess whether any could be recommended over the others in PD [17]. Whereas definitive recommendations could not be provided [17], this review did not include studies using NW programmes so that the efficacy and/or possible superiority of NW over other techniques remains to be determined. Hence, we performed a systematic review of the literature in order to clarify whether NW programmes are: (1) indeed useful in PD; and (2) superior or equivalent to other physical exercise based approaches.
F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
1.1. Search strategy and methods We searched the Medline database (via PubMed: http://www. ncbi.nlm.nih.gov), the EMBASE database and the Physiotherapy Evidence Database e PEDro - (available at http://www.pedro.org. au) for publications until December 2016, using the search terms “Nordic walking”, “Pole walking”, “Pole striding,” AND “Parkinson*”. Only original full articles written in English were selected and the reference lists of the retrieved articles were checked for relevant reports not indexed in the electronic databases. Data were extracted by two authors (FB, RE) using a standardized proforma gathering information about study design (e.g, controlled, blinded, etc.), number and type (in terms of disability) of patients enrolled, characteristics of the intervention (duration, number of sessions, etc), analysed outcomes and results. Descriptive analyses were performed on all studies, whereas data from randomized controlled trials (RCT) were pooled into a random-effects model with regard of the Unified Parkinson's Disease Rating Scale (UPDRS), motor subscale (UPDRS-3), e.g., a specific disability score almost invariably used as primary outcome in RCTs in PD, in line with the Cochrane Handbook for Systematic Reviews of Interventions (version 5.0.0). If the RCT had more than 2 interventional groups, the NW arm was compared to the least active treatment (e.g., unassisted domestic exercise or flexibility/relaxation program). We additionally undertook consideration of all the included studies in the pooled analysis to estimate clinical heterogeneity. This was done employing, primarily, the I2 statistic, which provides an estimate of the percentage of inconsistency thought to be due to chance, alongside the Chi-2 p value that provides the strength of evidence for heterogeneity. The latter analyses were performed with RevMan, version 5.3, Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014. These results are indicated as standardized mean difference (SMD) with 95% confidence intervals (CIs).
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only study evaluating patients 5 months after the end of the intervention program showed that benefits on both functional [6 min walking test, 10 m walking test and timed up and go test (TUG)] and clinical (PDQ-39) outcomes persisted [14]. Only 3 studies [15,19,20,23] compared NW to either free walking, flexibility/relaxation training or LSVT®BIG (a technique derived from the Lee Silverman Voice Treatment featuring highintensity training of movement amplitude). Thus, one study found NW to be superior to free walking and flexibility/relaxation training in ameliorating stride length, gait variability and rest hearth rate [19]. In another one NW was superior to free-walking in improving self-speeded TUG and self-selected speed [23]. In the remaining one (e.g., the Berlin LSVT®BIG Study, for which two papers on different outcomes are available) NW did not show any improvements on functional/clinical outcomes, but improved reaction time (using the Testbattery for attentional performance) compared to domestic exercise but not to LSVT®BIG [20]. In the majority of studies compliance was reported to be high (at least 87%) either in terms of patients who completed the intervention or number of sessions attended [14,19e22]. Data regarding adverse events (AE) due to intervention was very scarce. Two studies reported no AE [14,23], whereas such data were not available for 6 studies. The remaining one [19] detailed AE occurring during the intervention and it was thus reported that 9 patient out of 30 (30%) had some sort of AE (Table 1). Of these, 3 (10% of the entire cohort) had to miss up to 3 consecutive sessions (3.8% of the scheduled sessions) but completed the intervention thereafter [19]. UPDRS-3 scores for the four RCTs were obtained from the original papers or upon direct requesting to the authors. Fig. 1 represents the forest plot indicating the SMD in UPDRS-3 score across the 4 included RCTs including 73 patients in the active group and 74 in the control group. This analysis had an overall pooled outcome value of 0.64 (95% CI -0.98 to 0.30; p < 0.001). The I2 value was of 3% (p ¼ 0.38), indicative of a little degree of heterogeneity.
2. Results 3. Discussion Nine papers were included in the current review [14e16,18e23]. Two studies included the same population of patients [15,20]. However, the outcomes were different and, hence, both have been considered here. Table 1 provides a detailed overview of the included studies. Overall, 4 RCTs [15,19,20,22,23] and 4 observational studies [14,16,18,21] were identified, for a total of 127 patients studied. For all studies but one [19], patients had mild to moderate motor disability [e.g., Hoehn and Yahr (H&Y) stage 1e3]. One study included also advanced patients (e.g., H&Y ¼ 4) [19]. In all studies, NW programmes were similar and usually featured 2 sessions of 60 min per week (Table 1). Duration of the intervention ranged from 6 to 24 weeks (mean ± standard deviation ¼ 11.4 ± 5.6). For all studies but one [14], follow-up evaluation was performed only at the end of the intervention period. One study performed an additional evaluation 5 months after the end of the intervention period [14]. The majority of studies (n ¼ 5) considered both functional and clinical outcomes, 2 only functional outcomes and 2 only clinical outcomes (Table 1). Six studies succeeded in showing an improvement of the considered outcomes (Table 1), whereas 3 (for a total of 49 patients, 38.5% of the entire population of 127 patients considered here) did not [15,16,21]. Considering the studies where positive results were found, both functional and clinical outcomes (reflecting motor disability and quality of life) improved in most cases (Table 1). Importantly, two studies additionally showed an amelioration following NW in terms of a number of non-motor symptoms (NMS) including pain, apathy, attention and concentration [19,22]. The
The results of this systematic review would suggest that NW might be useful in PD, but the low quality and/or observational nature of many studies as well as the small samples included hamper drawing definitive conclusions. Although the pooled analysis on the 4 RCTs (for a total of 73 patients in the NW arm) yielded a significant result favouring the NW program, the low value of the SMD (e.g., 0.64) raises the question of whether this is clinically meaningful. NW has been shown in healthy subjects to determine higher cardiorespiratory fıtness as compared to free walking because of the higher amount of muscle mass used through additional motor activity of the upper body [3,10]. In turn, this leads to higher energy expenditure with obvious beneficial effects on several parameters such as resting heart rate, blood pressure, exercise capacity and maximal oxygen consumption [2,3,9]. This makes NW suitable for primary and secondary prevention of cardiovascular/metabolic conditions. Moreover, NW has been shown to exert additional benefits in a wide range of different conditions, including low back pain, fibromyalgia, and cancer (for a review see Ref. [3]). Beyond these results, NW has been shown to ameliorate specific locomotion parameters including stride length, stride length variability, double stance and postural stability [3,9,12]. Based on these premises, it was seemingly obvious to test the efficacy of NW in PD, the second most common neurodegenerative disease that typically manifests with walking disturbances. While the majority of studies showed an improvement of either functional or clinical outcomes (Table 1), 3 studies did not
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Table 1 Summary of the studies performed on NW in PD. Clinical Other outcomes AE outcomes
Compliance
Results
3
Up to 60 e
UPDRS, PDQ-39
e
NR
95% of the sessions
Significant improvement of all outcomes
2
60
6MWT, 10MWT, TUG
PDQ-39
e
None
100%
2
60
10MWT, TUG
UPDRS3, e PDQ39
NR
NR
Improvement of all outcomes (for 9 patients it was shown that benefit persisted for up to 5 months). No benefit for any outcomes.
3 (1 60 unsupervised)
STS and kinematic measures during the test
e
NR
NR
Moderate 24 to advanced (H&Y 2 to 4)
3
70
UPDRS, PDQ39, BSS
Yes (vs 19 LSVT®BIG and domestic nonsupervised exercise)
8 Mild to moderate (H&Y 1 to 3)
2
60
Yes
No
10
12 Mild to moderate (H&Y 1 to 3)
2
60
Max walking speed on treadmill, 12MWT, 24MWT, stride lengths, gait variability Reaction times using the Testbattery for attentional performance 6MWT, TUG, FTSST, HGT, RST, BST
PFS, BDI, SAS, H&Y, UPDRS3, NMSS BSS
None
87% of all sessions
No
No
No
12 18 (only Mild to akinetic- moderate (max rigid) UPDRS3 ¼ 44)
3 (1 60 unsupervised)
e
UPDRS3 e
NR
No
Yes
Yes (vs free walking)
14
2
e TUG (at both H&Y, self-selected UPDRS3, and forced BSS speed), SSW, LRI
NR
Type of N of treated patients patients included
Baatile,2000 No
No
No
6
No van Eijkeren, 2008
No
No
19
Ebersbach, 2010
Yes
Yes
Fritz, 2011
No
No
Yes (vs 19 LSVT®BIG and domestic nonsupervised exercise) 12 No 11 (only Mild to akinetic- moderate (max rigid) UPDRS3 ¼ 42)
Reuter, 2011
Yes
Yes
Yes (vs free walking or flexibility/ relaxation training)
Ebersbach, 2014*
Yes
Yes
Cugusi, 2015
No
Herfurth, 2015
Monteiro, 2016
30
8 Mild to moderate (H&Y 2 to 3) 6 Mild to moderate (H&Y 1 to 3) 8 Mild to moderate (H&Y 1 to 3)
9 Mild to advanced (H&Y 1 to 4)
60
e
No benefit for any outcomes (when stratifying patients in two groups according to motor disability, patients with low UPDRS3 values had benefit on STS). All patients NW improved all outcomes and Cardiovascular 2 patients had exercise induced hypotension; 4 performed at was superior to either parameters, least 70/78 alternative approach in fell; 5 twisted their pain NRS ameliorating stride length, gait ankles (but only 1 missed sessions variability and rest hearth rate. 3 sessions); 2 developed Analysis of UPDRS sub-scales shoulder pain requiring showed NW to improve some NSAD and missed 3 NMS, including concentration session and attention. e NR 1 patient NW improved cued-RT (in discontinued comparison with domestic exercise, but not with LSVT®BIG). e
Significant improvement of some functional (6MWT, FTSST, TUG, RST) and clinical outcomes (BSS, UPDRS-3, H&Y). Moreover, all examined NMS improved. No benefit for the group as a 2 patients missed more whole. Baseline gait velocity and step length predicted UPDRS3 than 1 session and improvement. were excluded for the analysis NR Improvement of both NW and free walking of all outcomes. However, NW was superior to free-walking in improving selfspeeded TUG and SSW.
*This sample includes the same sample as in Ebersbach, 2010, but explored different outcomes. H&Y: Hoehn and Yahr stage; UPDRS: Unified Parkinson's Disease Rating Scale; UPDRS-3: UPDRS part 3 (motor subscale); 6MWT: 6 min walking test; 10MWT: 10 m walking test; TUG: Timed up and go test; STS: Sit to stand performance; 12MWT: 12 m walking test; 24MWT: 24 m walking test; FTSST: Five Time Sit to Stand Test; HGT: hand grip-strength evaluation; RST: Sit and Reach Test; BST: Back Scratch Test; SSW: Self-selected speed; LRI: locomotor rehabilitation index; PDQ-39: PD Quality 39; BBS: Berg balance scale; PFS: Parkinson Fatigue Scale; BDI: Beck depression Inventory; SAS: Starkstein apathy scale; NMSS: Non-motor symptoms scale. NR: not reported.
F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
Duration/ Functional outcomes session (min)
Treatment N sessions/ week period (weeks)
First author, Blinded Controlled Comparison year with other techniques
F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
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Fig. 1. Forest plot: Standardized Mean Difference in UPDRS-3 score. [Random: random-effects model; IV: inverse variance; NW: Nordic Walking; * when RCTs had more than one control arm, the least active treatment was considered (see text for details)].
[15,16,21]. It is anticipated, however, that a number of flaws might undermine the reliability of these negative studies. For example, Ebersbach et al. compared NW training against LSVT®BIG and domestic walking, but patients were not requested to abstain from additional exercise and this was found to be relatively higher in the LSVT®BIG arm [15]. Additionally, all three negative studies had a sample size as small to not guarantee adequate study power. Nonetheless, an interesting finding shared by these 3 studies is that only patients with little disability or gait impairment would benefit from NW [15,16,21] and this appears a key point to address in future RCTs. As mentioned above, the majority of the studies [14,17e20,22,23] have demonstrated a significant benefit of NW on a number of clinical and/or functional parameters in PD patients (Table 1). Thus, NW would improve motor disability as demonstrated by decreased total UPDRS-3 score [18,22,23]. Nonetheless, there are some caveats hindering the generalization of these findings. In fact, patients were assessed either in the ON- [15,20,23] or OFF-medication state [21]; for 5 other studies this information was not available [14,16,18,19,22]. In one study, patients in different arms of treatment were different in some baseline features [23]. Moreover, only one study specifically reported that during the training technical skills related to NW were checked on videorecordings using a specific checklist, thus ensuring that NW technique was learnt and performed properly [19]. Furthermore, none of these studies compared NW to other physical exercise techniques that are more commonly used in PD such as the treadmill training. Finally, with the exception of one study [14], there are no long-term follow-up studies to see whether the benefits induced by NW might persist in time. Moreover, there remains the question as to whether NW has additional, disease-specific, benefits in PD. In fact, the use of poles might theoretically enhance arm swing also during normal walking. In PD, reduced arm swing is one of the earliest manifestations and might, by itself, alter walking dynamics and contribute to postural instability during walking and lead to falls. Recent evidence have been in fact produced that arm swing improves lateral balance and dynamic stability in healthy subjects [25,26]. Furthermore, PD patients characteristically have a forward flexion of the trunk, which could be in theory also ameliorated by the use of poles. While a number of studies demonstrated a significant improvement on specific gait parameters including step length and walking velocity [14,19,22,23], only one study analysed and demonstrated an improvement of such clinical features as freezing, posture, and postural instability [19]. In summary, there exists preliminary evidence that NW might be beneficial in PD, but definitive conclusions cannot be drawn, despite the pooled analysis on a total of 73 patients in the active group being significant. Our precautionary approach owes to the
aforementioned limitations of the original studies and to the very small SMD favouring NW in the meta-analysis, which raises the question as to whether such a reduction is clinically meaningful. Several reports attempted to define what should be regarded as “clinically meaningful change” in PD, at least when interpreting pharmacological trials. Thus, a report from the Parkinson Study Group calculated a minimal clinically important change to be in early PD patients of at least 3 UPDRS points [27]. More conservatively, Schrag et al. found a change of 5 points on the UPDRS-3 to best reflect a clinical meaningful change for H&Y stages 1e3 [28]. Either way, a reduction of 0.64 points of the UPDRS-3 observed across 4 different RCTs should be deemed as not meaningful, despite reaching statistical significance. Beyond the results on the motor features of PD, a few studies further showed a potential benefit of NW on NMS [19,22], including apathy, pain and concentration. This is in line with previous studies on different populations [3,8,24] and calls for the need for RCTs of NW with NMS as primary outcomes [29].
3.1. Future directions and conclusions In conclusion, there is still need for large, well designed, RCTs with a reasonable follow-up period of at least six months, to assess whether NW could be useful in PD and it will be important to compare NW both against standard medical care and other types of physical exercise. Patients should be firstly enrolled upon their baseline motor burden, since it would appear that little motor disability is the strongest predictor for improvement. However, an effort should be made to understand whether other clinical factors that might be influencing the outcome including age, type/velocity of PD progression and cognitive status, play a role [30]. It is obvious that the total UPDRS-3 might be uninformative to depict specific improvements on gait and posture features and additional tools could be considered such as videotaping patients, also to further check whether the technique is properly performed. Finally, the putative motor improvement should be reflected by an amelioration of certain daily living activities and, more in general, of the QoL. As for now, NW cannot be recommended in PD.
Financial disclosures RE received consultancies from Zambon. PB reports personal fees from Acorda, personal fees from Union Chimique Belge, personal fees from Zambon, grants from Abbvie, grants from Biotie, and grants from Zambon. All other authors have nothing to disclose.
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F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
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Review article
Walking on four limbs: A systematic review of Nordic Walking in Parkinson disease Federica Bombieri a, Federico Schena a, Barbara Pellegrini a, b, Paolo Barone c, Michele Tinazzi a, *, 1, Roberto Erro c, d, 1 di Verona, Verona, Italy Department of Neuroscience, Biomedicine and Movement Sciences, Universita CeRiSM (Research Centre of Mountain Sport and Health), University of Verona, Rovereto, Italy c Center for Neurodegenerative Diseases (CEMAND), Department of Medicine and Surgery, Neuroscience Section, University of Salerno, Salerno, Italy d Sobell Department of Motor Neuroscience and Movement Disorders, University College London (UCL) Institute of Neurology, London, United Kingdom a
b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 18 October 2016 Received in revised form 2 January 2017 Accepted 5 February 2017
Nordic Walking is a relatively high intensity activity that is becoming increasingly popular. It involves marching using poles adapted from cross-country skiing poles in order to activate upper body muscles that would not be used during normal walking. Several studies have been performed using this technique in Parkinson disease patients with contradictory results. Thus, we reviewed here all studies using this technique in Parkinson disease patients and further performed a meta-analysis of RCTs where Nordic Walking was evaluated against standard medical care or other types of physical exercise. Nine studies including four RCTs were reviewed for a total of 127 patients who were assigned to the Nordic Walking program. The majority of studies reported beneficial effects of Nordic Walking on either motor or nonmotor variables, but many limitations were observed that hamper drawing definitive conclusions and it is largely unclear whether the benefits persist over time. It would appear that little baseline disability is the strongest predictor of response. The meta-analysis of the 4 RCTs yielded a statistically significant reduction of the UPDRS-3 score, but its value of less than 1 point does not appear to be clinically meaningful. Well-designed, large RCTs should be performed both against standard medical care and other types of physical exercise to definitively address whether Nordic Walking can be beneficial in PD. © 2017 Published by Elsevier Ltd.
Keywords: Physical activity Non-pharmacological Rehabilitation Physiotherapy Treadmill
1. Introduction Nordic Walking (NW) is a relatively high intensity activity that involves marching using poles adapted from cross-country skiing poles in order to activate upper body muscles that would not be used during normal walking [1,2]. NW is becoming increasingly popular [3e7]. This probably owes to different reasons including participation in group exercise programmes, which has been shown to be a motivating factor [8], and the low level of perceived exertion. Moreover, NW has the practical advantage that can be done year round in any climate and does not require dedicated facilities or expensive equipments. NW programmes performed in healthy subjects have been demonstrated to increase physical activity levels, muscular
* Corresponding author. P.le L.A. Scuro, 10 Verona, Italy. E-mail address: [email protected] (M. Tinazzi). 1 Equally contributed. http://dx.doi.org/10.1016/j.parkreldis.2017.02.004 1353-8020/© 2017 Published by Elsevier Ltd.
endurance, functional exercise capacity, flexibility, postural stability, stride length and gait pattern [1,9e12]. All these latter become progressively compromised in Parkinson disease (PD) and are only partly ameliorated by pharmacological and/or surgical approaches [13]. As such, NW has been construed to be potentially efficacious in PD [14] and it is increasingly gaining momentum in this condition. However, evidence in this regard is scarce and different studies have produced somewhat contradictory results [14e16]. A recent (2014) Cochrane review aimed to compare different rehabilitation techniques to assess whether any could be recommended over the others in PD [17]. Whereas definitive recommendations could not be provided [17], this review did not include studies using NW programmes so that the efficacy and/or possible superiority of NW over other techniques remains to be determined. Hence, we performed a systematic review of the literature in order to clarify whether NW programmes are: (1) indeed useful in PD; and (2) superior or equivalent to other physical exercise based approaches.
F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
1.1. Search strategy and methods We searched the Medline database (via PubMed: http://www. ncbi.nlm.nih.gov), the EMBASE database and the Physiotherapy Evidence Database e PEDro - (available at http://www.pedro.org. au) for publications until December 2016, using the search terms “Nordic walking”, “Pole walking”, “Pole striding,” AND “Parkinson*”. Only original full articles written in English were selected and the reference lists of the retrieved articles were checked for relevant reports not indexed in the electronic databases. Data were extracted by two authors (FB, RE) using a standardized proforma gathering information about study design (e.g, controlled, blinded, etc.), number and type (in terms of disability) of patients enrolled, characteristics of the intervention (duration, number of sessions, etc), analysed outcomes and results. Descriptive analyses were performed on all studies, whereas data from randomized controlled trials (RCT) were pooled into a random-effects model with regard of the Unified Parkinson's Disease Rating Scale (UPDRS), motor subscale (UPDRS-3), e.g., a specific disability score almost invariably used as primary outcome in RCTs in PD, in line with the Cochrane Handbook for Systematic Reviews of Interventions (version 5.0.0). If the RCT had more than 2 interventional groups, the NW arm was compared to the least active treatment (e.g., unassisted domestic exercise or flexibility/relaxation program). We additionally undertook consideration of all the included studies in the pooled analysis to estimate clinical heterogeneity. This was done employing, primarily, the I2 statistic, which provides an estimate of the percentage of inconsistency thought to be due to chance, alongside the Chi-2 p value that provides the strength of evidence for heterogeneity. The latter analyses were performed with RevMan, version 5.3, Copenhagen: The Nordic Cochrane Centre, The Cochrane Collaboration, 2014. These results are indicated as standardized mean difference (SMD) with 95% confidence intervals (CIs).
9
only study evaluating patients 5 months after the end of the intervention program showed that benefits on both functional [6 min walking test, 10 m walking test and timed up and go test (TUG)] and clinical (PDQ-39) outcomes persisted [14]. Only 3 studies [15,19,20,23] compared NW to either free walking, flexibility/relaxation training or LSVT®BIG (a technique derived from the Lee Silverman Voice Treatment featuring highintensity training of movement amplitude). Thus, one study found NW to be superior to free walking and flexibility/relaxation training in ameliorating stride length, gait variability and rest hearth rate [19]. In another one NW was superior to free-walking in improving self-speeded TUG and self-selected speed [23]. In the remaining one (e.g., the Berlin LSVT®BIG Study, for which two papers on different outcomes are available) NW did not show any improvements on functional/clinical outcomes, but improved reaction time (using the Testbattery for attentional performance) compared to domestic exercise but not to LSVT®BIG [20]. In the majority of studies compliance was reported to be high (at least 87%) either in terms of patients who completed the intervention or number of sessions attended [14,19e22]. Data regarding adverse events (AE) due to intervention was very scarce. Two studies reported no AE [14,23], whereas such data were not available for 6 studies. The remaining one [19] detailed AE occurring during the intervention and it was thus reported that 9 patient out of 30 (30%) had some sort of AE (Table 1). Of these, 3 (10% of the entire cohort) had to miss up to 3 consecutive sessions (3.8% of the scheduled sessions) but completed the intervention thereafter [19]. UPDRS-3 scores for the four RCTs were obtained from the original papers or upon direct requesting to the authors. Fig. 1 represents the forest plot indicating the SMD in UPDRS-3 score across the 4 included RCTs including 73 patients in the active group and 74 in the control group. This analysis had an overall pooled outcome value of 0.64 (95% CI -0.98 to 0.30; p < 0.001). The I2 value was of 3% (p ¼ 0.38), indicative of a little degree of heterogeneity.
2. Results 3. Discussion Nine papers were included in the current review [14e16,18e23]. Two studies included the same population of patients [15,20]. However, the outcomes were different and, hence, both have been considered here. Table 1 provides a detailed overview of the included studies. Overall, 4 RCTs [15,19,20,22,23] and 4 observational studies [14,16,18,21] were identified, for a total of 127 patients studied. For all studies but one [19], patients had mild to moderate motor disability [e.g., Hoehn and Yahr (H&Y) stage 1e3]. One study included also advanced patients (e.g., H&Y ¼ 4) [19]. In all studies, NW programmes were similar and usually featured 2 sessions of 60 min per week (Table 1). Duration of the intervention ranged from 6 to 24 weeks (mean ± standard deviation ¼ 11.4 ± 5.6). For all studies but one [14], follow-up evaluation was performed only at the end of the intervention period. One study performed an additional evaluation 5 months after the end of the intervention period [14]. The majority of studies (n ¼ 5) considered both functional and clinical outcomes, 2 only functional outcomes and 2 only clinical outcomes (Table 1). Six studies succeeded in showing an improvement of the considered outcomes (Table 1), whereas 3 (for a total of 49 patients, 38.5% of the entire population of 127 patients considered here) did not [15,16,21]. Considering the studies where positive results were found, both functional and clinical outcomes (reflecting motor disability and quality of life) improved in most cases (Table 1). Importantly, two studies additionally showed an amelioration following NW in terms of a number of non-motor symptoms (NMS) including pain, apathy, attention and concentration [19,22]. The
The results of this systematic review would suggest that NW might be useful in PD, but the low quality and/or observational nature of many studies as well as the small samples included hamper drawing definitive conclusions. Although the pooled analysis on the 4 RCTs (for a total of 73 patients in the NW arm) yielded a significant result favouring the NW program, the low value of the SMD (e.g., 0.64) raises the question of whether this is clinically meaningful. NW has been shown in healthy subjects to determine higher cardiorespiratory fıtness as compared to free walking because of the higher amount of muscle mass used through additional motor activity of the upper body [3,10]. In turn, this leads to higher energy expenditure with obvious beneficial effects on several parameters such as resting heart rate, blood pressure, exercise capacity and maximal oxygen consumption [2,3,9]. This makes NW suitable for primary and secondary prevention of cardiovascular/metabolic conditions. Moreover, NW has been shown to exert additional benefits in a wide range of different conditions, including low back pain, fibromyalgia, and cancer (for a review see Ref. [3]). Beyond these results, NW has been shown to ameliorate specific locomotion parameters including stride length, stride length variability, double stance and postural stability [3,9,12]. Based on these premises, it was seemingly obvious to test the efficacy of NW in PD, the second most common neurodegenerative disease that typically manifests with walking disturbances. While the majority of studies showed an improvement of either functional or clinical outcomes (Table 1), 3 studies did not
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Table 1 Summary of the studies performed on NW in PD. Clinical Other outcomes AE outcomes
Compliance
Results
3
Up to 60 e
UPDRS, PDQ-39
e
NR
95% of the sessions
Significant improvement of all outcomes
2
60
6MWT, 10MWT, TUG
PDQ-39
e
None
100%
2
60
10MWT, TUG
UPDRS3, e PDQ39
NR
NR
Improvement of all outcomes (for 9 patients it was shown that benefit persisted for up to 5 months). No benefit for any outcomes.
3 (1 60 unsupervised)
STS and kinematic measures during the test
e
NR
NR
Moderate 24 to advanced (H&Y 2 to 4)
3
70
UPDRS, PDQ39, BSS
Yes (vs 19 LSVT®BIG and domestic nonsupervised exercise)
8 Mild to moderate (H&Y 1 to 3)
2
60
Yes
No
10
12 Mild to moderate (H&Y 1 to 3)
2
60
Max walking speed on treadmill, 12MWT, 24MWT, stride lengths, gait variability Reaction times using the Testbattery for attentional performance 6MWT, TUG, FTSST, HGT, RST, BST
PFS, BDI, SAS, H&Y, UPDRS3, NMSS BSS
None
87% of all sessions
No
No
No
12 18 (only Mild to akinetic- moderate (max rigid) UPDRS3 ¼ 44)
3 (1 60 unsupervised)
e
UPDRS3 e
NR
No
Yes
Yes (vs free walking)
14
2
e TUG (at both H&Y, self-selected UPDRS3, and forced BSS speed), SSW, LRI
NR
Type of N of treated patients patients included
Baatile,2000 No
No
No
6
No van Eijkeren, 2008
No
No
19
Ebersbach, 2010
Yes
Yes
Fritz, 2011
No
No
Yes (vs 19 LSVT®BIG and domestic nonsupervised exercise) 12 No 11 (only Mild to akinetic- moderate (max rigid) UPDRS3 ¼ 42)
Reuter, 2011
Yes
Yes
Yes (vs free walking or flexibility/ relaxation training)
Ebersbach, 2014*
Yes
Yes
Cugusi, 2015
No
Herfurth, 2015
Monteiro, 2016
30
8 Mild to moderate (H&Y 2 to 3) 6 Mild to moderate (H&Y 1 to 3) 8 Mild to moderate (H&Y 1 to 3)
9 Mild to advanced (H&Y 1 to 4)
60
e
No benefit for any outcomes (when stratifying patients in two groups according to motor disability, patients with low UPDRS3 values had benefit on STS). All patients NW improved all outcomes and Cardiovascular 2 patients had exercise induced hypotension; 4 performed at was superior to either parameters, least 70/78 alternative approach in fell; 5 twisted their pain NRS ameliorating stride length, gait ankles (but only 1 missed sessions variability and rest hearth rate. 3 sessions); 2 developed Analysis of UPDRS sub-scales shoulder pain requiring showed NW to improve some NSAD and missed 3 NMS, including concentration session and attention. e NR 1 patient NW improved cued-RT (in discontinued comparison with domestic exercise, but not with LSVT®BIG). e
Significant improvement of some functional (6MWT, FTSST, TUG, RST) and clinical outcomes (BSS, UPDRS-3, H&Y). Moreover, all examined NMS improved. No benefit for the group as a 2 patients missed more whole. Baseline gait velocity and step length predicted UPDRS3 than 1 session and improvement. were excluded for the analysis NR Improvement of both NW and free walking of all outcomes. However, NW was superior to free-walking in improving selfspeeded TUG and SSW.
*This sample includes the same sample as in Ebersbach, 2010, but explored different outcomes. H&Y: Hoehn and Yahr stage; UPDRS: Unified Parkinson's Disease Rating Scale; UPDRS-3: UPDRS part 3 (motor subscale); 6MWT: 6 min walking test; 10MWT: 10 m walking test; TUG: Timed up and go test; STS: Sit to stand performance; 12MWT: 12 m walking test; 24MWT: 24 m walking test; FTSST: Five Time Sit to Stand Test; HGT: hand grip-strength evaluation; RST: Sit and Reach Test; BST: Back Scratch Test; SSW: Self-selected speed; LRI: locomotor rehabilitation index; PDQ-39: PD Quality 39; BBS: Berg balance scale; PFS: Parkinson Fatigue Scale; BDI: Beck depression Inventory; SAS: Starkstein apathy scale; NMSS: Non-motor symptoms scale. NR: not reported.
F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
Duration/ Functional outcomes session (min)
Treatment N sessions/ week period (weeks)
First author, Blinded Controlled Comparison year with other techniques
F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
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Fig. 1. Forest plot: Standardized Mean Difference in UPDRS-3 score. [Random: random-effects model; IV: inverse variance; NW: Nordic Walking; * when RCTs had more than one control arm, the least active treatment was considered (see text for details)].
[15,16,21]. It is anticipated, however, that a number of flaws might undermine the reliability of these negative studies. For example, Ebersbach et al. compared NW training against LSVT®BIG and domestic walking, but patients were not requested to abstain from additional exercise and this was found to be relatively higher in the LSVT®BIG arm [15]. Additionally, all three negative studies had a sample size as small to not guarantee adequate study power. Nonetheless, an interesting finding shared by these 3 studies is that only patients with little disability or gait impairment would benefit from NW [15,16,21] and this appears a key point to address in future RCTs. As mentioned above, the majority of the studies [14,17e20,22,23] have demonstrated a significant benefit of NW on a number of clinical and/or functional parameters in PD patients (Table 1). Thus, NW would improve motor disability as demonstrated by decreased total UPDRS-3 score [18,22,23]. Nonetheless, there are some caveats hindering the generalization of these findings. In fact, patients were assessed either in the ON- [15,20,23] or OFF-medication state [21]; for 5 other studies this information was not available [14,16,18,19,22]. In one study, patients in different arms of treatment were different in some baseline features [23]. Moreover, only one study specifically reported that during the training technical skills related to NW were checked on videorecordings using a specific checklist, thus ensuring that NW technique was learnt and performed properly [19]. Furthermore, none of these studies compared NW to other physical exercise techniques that are more commonly used in PD such as the treadmill training. Finally, with the exception of one study [14], there are no long-term follow-up studies to see whether the benefits induced by NW might persist in time. Moreover, there remains the question as to whether NW has additional, disease-specific, benefits in PD. In fact, the use of poles might theoretically enhance arm swing also during normal walking. In PD, reduced arm swing is one of the earliest manifestations and might, by itself, alter walking dynamics and contribute to postural instability during walking and lead to falls. Recent evidence have been in fact produced that arm swing improves lateral balance and dynamic stability in healthy subjects [25,26]. Furthermore, PD patients characteristically have a forward flexion of the trunk, which could be in theory also ameliorated by the use of poles. While a number of studies demonstrated a significant improvement on specific gait parameters including step length and walking velocity [14,19,22,23], only one study analysed and demonstrated an improvement of such clinical features as freezing, posture, and postural instability [19]. In summary, there exists preliminary evidence that NW might be beneficial in PD, but definitive conclusions cannot be drawn, despite the pooled analysis on a total of 73 patients in the active group being significant. Our precautionary approach owes to the
aforementioned limitations of the original studies and to the very small SMD favouring NW in the meta-analysis, which raises the question as to whether such a reduction is clinically meaningful. Several reports attempted to define what should be regarded as “clinically meaningful change” in PD, at least when interpreting pharmacological trials. Thus, a report from the Parkinson Study Group calculated a minimal clinically important change to be in early PD patients of at least 3 UPDRS points [27]. More conservatively, Schrag et al. found a change of 5 points on the UPDRS-3 to best reflect a clinical meaningful change for H&Y stages 1e3 [28]. Either way, a reduction of 0.64 points of the UPDRS-3 observed across 4 different RCTs should be deemed as not meaningful, despite reaching statistical significance. Beyond the results on the motor features of PD, a few studies further showed a potential benefit of NW on NMS [19,22], including apathy, pain and concentration. This is in line with previous studies on different populations [3,8,24] and calls for the need for RCTs of NW with NMS as primary outcomes [29].
3.1. Future directions and conclusions In conclusion, there is still need for large, well designed, RCTs with a reasonable follow-up period of at least six months, to assess whether NW could be useful in PD and it will be important to compare NW both against standard medical care and other types of physical exercise. Patients should be firstly enrolled upon their baseline motor burden, since it would appear that little motor disability is the strongest predictor for improvement. However, an effort should be made to understand whether other clinical factors that might be influencing the outcome including age, type/velocity of PD progression and cognitive status, play a role [30]. It is obvious that the total UPDRS-3 might be uninformative to depict specific improvements on gait and posture features and additional tools could be considered such as videotaping patients, also to further check whether the technique is properly performed. Finally, the putative motor improvement should be reflected by an amelioration of certain daily living activities and, more in general, of the QoL. As for now, NW cannot be recommended in PD.
Financial disclosures RE received consultancies from Zambon. PB reports personal fees from Acorda, personal fees from Union Chimique Belge, personal fees from Zambon, grants from Abbvie, grants from Biotie, and grants from Zambon. All other authors have nothing to disclose.
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F. Bombieri et al. / Parkinsonism and Related Disorders 38 (2017) 8e12
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