- Email: [email protected]
Gait velocity and step length at baseline predict outcome of Nordic walking training in patients with Parkinson's disease
Parkinsonism and Related Disorders 21 (2015) 413e416
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Short communication
Gait velocity and step length at baseline predict outcome of Nordic walking training in patients with Parkinson's disease Manon Herfurth b, Jana Godau e, Barbara Kattner f, Silvia Rombach c, Stefan Grau d, Walter Maetzler a, b, Daniela Berg a, b, * a
Center of Neurology, Hertie Institute for Clinical Brain Research, Department of Neurodegeneration, Germany German Center of Neurodegenerative Diseases, University of Tübingen, Germany Department of Sports Medicine, University Clinic Tübingen, Germany d Department of Food and Nutrition, and Sport Science, University of Gothenburg, Sweden e Klinikum Kassel, Department of Neurology and Kassel Medical School, University of Southampton, Kassel, Germany f Department of Internal Medicine, University Clinic Tübingen, Germany b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 4 September 2014 Received in revised form 25 January 2015 Accepted 27 January 2015
Background: The impact of Nordic walking (NW) in Parkinson's disease (PD) has been investigated in several studies but results are inconsistent. This may be due to different cohorts studied and the heterogeneity of their PD symptoms which impact the outcome of NW. This study aimed at determining predictive factors for a positive effect of NW on PD. Methodology and principal findings: Primary outcome was to define the baseline disease-associated and demographic parameters that distinguish patients who demonstrate improvement in the Unified PD rating scale (UPDRS) motor part following NW training (“Uþ”) from those patients with no improvement after the same intervention (“U“). The potentially predictive parameters were: age, age at onset, disease duration, gait velocity, step length, daily step number, UPDRS-motor part, Berg-Balance-Scale, ParkinsonNeuropsychometric-Dementia-Assessment, verbal-fluency-test and Becks-Depression-Inventory-II. Twenty-two PD patients (H&Y stage 2e2.5) performed twelve weeks of NW training. Eighteen patients were included in the final analysis. Overall, the UPDRS motor part did not improve significantly; however, eight patients had an improvement in the UPDRS motor part from baseline to end of study (Uþ). When comparing the potentially predictive factors of the Uþ cohort with those ten patients who did not improve (U), there was a notable difference in gait velocity and step length, and showed a significant correlation with an improvement in the UDPRS motor part scores. Conclusion: Gait velocity and step length can predict the outcome of NW training as determined by the UPDRS motor part, indicating that PD patients with only slightly impaired gait performance benefit most. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Parkinson's disease Nordic walking Predictive factors UPDRS motor part Gait velocity Step length
1. Introduction Physical activity has positive effects in general and also in patients with Parkinson's disease (PD). Nordic walking (also called pole walking) is regarded as an endurance sport. The cyclical motion sequences share similarities
* Corresponding author. Department of Neurodegeneration, Hertie Institute for Clinical Brain Research, German Center of Neurodegenerative Diseases, University of Tuebingen, Hoppe-Seyler-Str. 3, 72076 Tübingen, Germany. Tel.: þ49 7071 29 83119; fax: þ49 7071 29 4490. E-mail address: [email protected] (D. Berg). http://dx.doi.org/10.1016/j.parkreldis.2015.01.016 1353-8020/© 2015 Elsevier Ltd. All rights reserved.
with cross-country skiing: Fast walking is supported by two poles. Every time the left heel touches the ground, the right pole should hit the ground, and vice versa. Nordic walking (NW) is a particularly appealing physical activity as it takes place outdoors, can be performed almost everywhere and is safe. The effect of NW in PD patients has been investigated in several studies [1e6]; however results regarding whether PD patients benefit from NW or not are inconsistent. For example, whereas two studies [1,5] found positive effects using the best-accepted outcome measure of PD motor symptoms (the motor part of the Unified PD rating scale (UPDRS)), another study did not [3]. This might, at least partly, be due to differences in the cohorts studied and the heterogeneity of their PD. Based on the wish to develop a more “personalized” treatment
414
M. Herfurth et al. / Parkinsonism and Related Disorders 21 (2015) 413e416
regimen for chronic diseases including PD [7], we designed this study to determine whether specific demographic, motor, cognitive and behavioral parameters predict a clinical improvement as measured with the UPDRS motor part. 2. Patient and methods
weeks. Two sessions per week were led by a professional NW trainer; the third session was performed without a trainer. We separated the cohort in two groups A (n ¼ 10) and B (n ¼ 8). Group A trained first, during that time group B received no training and was designated as the control group. At 12 weeks group B started the training sessions.
2.1. Ethics The study protocol was approved by the ethical committee of the University of Tübingen, and all subjects provided written informed consent.
4. Data analysis and statistics
2.2. Subjects
Data were analyzed with SPSS 22 for Windows (SPSS Inc, Chicago, IL, USA). Because we used primarily ordinal data in this analysis we used median and range to present these data. Significance levels were calculated with the Wilcoxon signed rank or the ManneWhitney-U tests, and the Spearman's rank correlation coefficient. The decision to use these tests was based on the small numbers of subjects and the fact that almost none of the variables were distributed normally. The uncorrected alpha level was set at P ¼ 0.05 based on the exploratory nature of this study. However, for the correlation coefficient, we also present significance levels after Bonferroni correction because of multiple testing.
Thirty-four patients were recruited from the neurological outpatient clinic of the University of Tübingen and by newspaper advertisement. Twenty-two met the inclusion criteria and were included in the baseline assessment. They all fulfilled the UK Brain Bank criteria for PD [8], and had an akinetic-rigid or equivalent subtype of PD. Inclusion criteria were walking without assistance, >10 points on the UPDRS motor part during the medication OFF phase, improvement of at least 20 percent of the UPDRS motor part after medication intake, Hoehn and Yahr stage of 2 or 2.5, Schwab and England scale >50%, no previous experience with NW and less than 1.5 h exercise activity per week. Exclusion criteria were: history and presence of concurrent conditions which would influence NW training performance (e.g., musculoskeletal, psychiatric problems, dementia).
3. Assessment 5. Results All tests took place in the “OFF” state, i.e. at least twelve hours after the last dose of PD medication. UPDRS motor part was assessed at BL and after twelve weeks of NW. To determine baseline predictive factors, we assessed age, age at onset, disease duration, Berg Balance Scale (BBS), Parkinson neuropsychometric dementia assessment (PANDA), the verbal fluency test (patients were asked to generate as many S-words as possible during one minute) and the Becks Depression Inventory II (BDI II). In addition, we performed quantitative testing of gait velocity and step length. The participants were instructed to walk along a six meter path at a comfortable pace in our designated test laboratory. Gait parameters were measured with 6 infrared cameras and a Plug-In-Gait marker placement set, consisting of 39 anatomic markers (VICON®, Oxford Metrics, Oxford, UK). We also calculated the number of steps per day during the study period with a pedometer (Silva, Bromma, Sweden) that the subjects wore on the hip. Table 1 provides a summary of these parameters. All study participants performed three training sessions per week lasting approximately one hour each, for a total of twelve
Of the 22 study participants who were initially included, two had to change their Parkinson's medication during the training period, and 2 missed more than one session per week. Thus we were able to include the data of 18 study participants in the final analysis. Overall, the cohort as a whole showed no significant difference in the UPDRS motor part at BL and post training (BL: 30 (15e44), post training: 27 (13e47)jmedian (range), P ¼ 0.30), (Table 1). Similar results were found for the controls (group B during the first 12 weeks, BL: 27 (17e40), pre training: 27 (15e44), P ¼ 0.87). 8 study participants (from now on referred to as Uþ cohort), however, did improve from BL to the end of the study (2e13 points), 10 participants (U) did not improve (8 to 0 points). At BL, the UPDRS motor part of the Uþ BL 27 (17e37) and the U BL: 31 (15e44) cohorts did not differ significantly (P ¼ 0.408) but, as expected, was significantly different at the end of the study (post training Uþ: 20 (13e30)jU: 34 (18e44), P ¼ 0.002), (Table 1). When comparing the potentially predictive factors between Uþ and U, gait velocity (uncorrected P ¼ 0.02) and step length
Table 1 Baseline clinical and demographical data, and comparison of potentially predictive factors for a good outcome after a standardized Nordic walking training. For significantly different measures and UPDRS motor part also post training (pT) values are shown.
Age at onset [Y] Disease duration [Y] Age [Y] Steps per day [N] UPDRS motor part (0e108) BBS (0e56) verbal fluency [N] PANDA (0e30) BDI II (0e63) Gait velocity [m/s] Step length [mm]
Whole cohort [N ¼ 18] median (range)
Uþ [N ¼ 8] median (range)
U [N ¼ 10] median (range)
Mann-Whitey-U test U⁺/U (P value)
67 (55e75) 3 (0e16) 63 (50e73) 4550 (1094e11,982) 30 (15e44) pT:27 (13e47) 54 (44e56) 13 (7e24) 25 (9e30) 8 (1e24) 1.19 (0.95e1.63) pT:1.19 (0.92e1.67) 622 (500e767) pT:607 (504e768)
68 (55e73) 3 (0e7) 73 (55e75) 5066 (2710e7000) 27 (17e37) pT:20 (13e30) 54 (46e56) 13 (7e24) 25 (9e29) 5 (1e15) 1.27 (1.08e1.63) pT:1.36 (1.00e1.67) 650 (544e767) pT:661 (504e768)
60 (50e68) 5 (1e16) 66 (58e73) 3272 (1094e11,982) 31 (15e44) pT:34 (18e44) 52 (44e56) 12 (8e19) 22.5 (16e30) 8 (4e24) 1.09 (0.95e1.29) pT:1.12 (0.92e1.36) 587 (500e662) pT:575 (515e658)
0.114 0.236 0.274 0.364 0.408 pT:0.002 0.573 0.633 1.000 0.315 0.021 pT:0.08 0.043 pT:0.15
Demographic, motor, cognitive and behavioral parameters from the baseline assessment are presented with respect to e improvement (Uþ) or lack of improvement (U) on the Unified Parkinson's disease rating scale (UPDRS) motor part after a standardized 12 weeks Nordic walking training. BBS, Berg Balance Scale; BDI, Becks Depression Inventory; .m/s, meter per second; mm, millimeter; N, number; PANDA, Parkinson Neuropsychometric Dementia Assessment; UPDRS, Unified Parkinson's Disease Rating Scale, y, years.
M. Herfurth et al. / Parkinsonism and Related Disorders 21 (2015) 413e416
(uncorrected P ¼ 0.04) but none of the other parameters approached significance (Table 1). Correlation analyses between predictive factors, and change of the UPDRS motor part from BL to end of study basically confirmed this result: there was a significant correlation between the degree of improvement in the UPDRS motor part from BL to the end of study, and gait velocity and step length (Table 2).
6. Discussion This study focused on the determination of predictive factors associated with an improvement of the UPDRS motor part in PD patients who performed a standardized NW training program. The concept of this study and analysis was based on inconsistent results obtained in previous studies focusing on the investigation of the effect of NW in PD patients [1,3,5] and the hypothesis that specific subpopulations of PD patients may particularly benefit from this training whereas others may not. We hypothesized that a more individualized recruitment strategy, based on parameters predictive for beneficial outcome following a standardized NW training program, could help to clarify the issue. When comparing the Uþ with the U cohort, we found that BL gait velocity and step length were the only parameters which correlated with an improvement on the UPDRS motor part after NW. This suggests that particularly highly mobile PD patients benefit from NW. Gait velocity correlates with the axial items of the UPDRS motor part and step length also correlates with bradykinesia [9]. We hypothesize that patients with initially high gait velocity and step length are able to perform the training with greater flexibility and safety, which could influence the individual intensity of the NW training. The intensity of the training has repeatedly been shown to influence the outcome of physical activity interventions [5,10]. Our findings were unexpected, as we initially hypothesized that age at onset, disease duration, depression and cognitive state in particular might predict the outcome of the UPDRS motor part after Nordic walking with the idea that the influence exercise is associated with them [11]. However, our results do not support this hypothesis. For further studies it would be interesting to compare
415
larger cohorts with specific phenotypes such as depressed vs. nondepressed, younger vs. older age of onset etc. In particular, the inclusion of cognitively impaired PD patients may be an interesting approach as physical training has been shown to be effective in demented patients [12]. It would also be interesting to test the effect of the training on parameters such as muscle strength and general fitness as the correlation of improvements of gait velocity and step length with improvement in UPDRS motor part could also be explained by such more general factors. However, this was a pilot study which aimed at a “personalized approach”, and we argue that our results may justify the design of larger multicenter studies with a comparable study design. 7. Conclusion Gait velocity and step length can predict the outcome of NW training as determined by the UPDRS motor part, indicating that in particular PD patients with no or minor axial motor impairment benefit from NW training. Financial disclosures and competing interests Dr. Maetzler currently receives funding from the European Union and the Michael J Fox Foundation. In the past, he received funding from the Robert Bosch Foundation and speaker honoraria from GlaxoSmithKline. He reports no competing interests. Dr. Grau is supported by grants from Bauerfeind Germany, Elten GmbH, Reno Schuh GmbH and by honoraria from Bauerfeind Germany and Elten GmbH. He reports no competing interests. Dr. Berg has served on scientific consultancies and advisory boards for UCB Pharma and Novartis and received speaker honoraria from UCB Pharma, GlaxoSmithKline, TEVA Pharma, Lundbeck. Her scientific work is supported by grants from the Michael J. Fox Foundation, Janssen Pharmaceutica, UCB Pharma, Boehringer Ingelheim, Internationale Parkinson Fonds, German Parkinson's Disease Association (dPV) and TEVA. She reports no competing interests. Acknowledgments
Table 2 Spearman Rho correlation: correlations (P ¼ 0.05) between values of potentially predictive factors for positive outcome after NW-training, and improvement of the UPDRS motor part. Predictive factors
Age at onset Disease duration Age Steps per day UPDRS motor part BBS Verbal fluency PANDA BDI II Gait velocity Step length
Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance
0.285 0.134 0.341 0.090 0.106 0.338 0.285 0.134 0.053 0.418 0.020 0.469 0.136 0.296 0.075 0.384 0.013 0.480 0.646 0.002a 0.458 0.028
a Correlation is significant after Bonferroni correction (P ¼ 0.005). BBS, Berg Balance Scale; BDI, Becks Depression Inventory; PANDA, Parkinson Neuropsychometric Dementia Assessment; UPDRS, Unified Parkinson's Disease Rating Scale.
We thank all individuals who took part in the study. WM is supported by the EU project SENSE-PARK (no. 288557), funded under the Seventh Framework Programme, Cooperation e ICT. References [1] Baatile J, Langbein WE, Weaver F, Maloney C, Jost MB. Effect of exercise on perceived quality of life of individuals with Parkinson's disease. J Rehabil Res 2010;37:529e34. [2] van Eijkeren FJ, Reijmers RS, Kleinveld MJ, Minten A, Bruggen JP, Bloem BR. Nordic walking improves mobility in Parkinson's disease. Mov Disord 2008;23:2239e43. [3] Ebersbach G, Ebersbach A, Edler D, Kaufhold O, Kusch M, Kupsch A, et al. Comparing exercise in Parkinson's diseaseethe Berlin LSVT(R)BIG study. Mov Disord 2010;25:1902e8. [4] Fritz B, Rombach S, Godau J, Berg D, Horstmann T, Grau S. The influence of Nordic walking training on sit-to-stand transfer in Parkinson patients. Gait Posture 2011;34:234e8. [5] Reuter I, Mehnert S, Leone P, Kaps M, Oechsner M, Engelhardt M. Effects of a flexibility and relaxation programme, walking, and Nordic walking on Parkinson's disease. J Aging Res 2011. 232473. [6] Ebersbach G, Ebersbach A, Gandor F, Wegner B, Wissel J, Kupsch A. Impact of physical exercise on reaction time in patients with Parkinson's disease-data from the Berlin BIG Study. Arch Phys Med Rehabil 2014;95:996e9. [7] Maetzler W, Nieuwhof F, Hasmann SE, Bloem BR. Emerging therapies for gait disability and balance impairment: promises and pitfalls. Mov Disord 2013;28:1576e86. [8] Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992;55:181e4.
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[9] Vieregge P, Stolze H, Klein C, Heberlein I. Gait quantitation in Parkinson's diseaseelocomotor disability and correlation to clinical rating scales. J Neural Transm 1997;104:237e48. [10] Gerecke KM, Jiao Y, Pani A, Pagala V, Smeyne R. Exercise protects against MPTP-induced neurotoxicity in mice. Brain Res 2010;1341:72e83.
[11] Hirsch MA, Farley BG. Exercise and neuroplasticity in persons living with Parkinson's disease. Eur J Phys Rehabil Med 2009;45:215e29. [12] Schwenk M, Dutzi I, Englert S, Micol W, Najafi B, Mohler J, et al. An intensive exercise program improves motor performances in patients with dementia: translational model of geriatric rehabilitation. J Alzheimers Dis 2014;39:487e98.
Contents lists available at ScienceDirect
Parkinsonism and Related Disorders journal homepage: www.elsevier.com/locate/parkreldis
Short communication
Gait velocity and step length at baseline predict outcome of Nordic walking training in patients with Parkinson's disease Manon Herfurth b, Jana Godau e, Barbara Kattner f, Silvia Rombach c, Stefan Grau d, Walter Maetzler a, b, Daniela Berg a, b, * a
Center of Neurology, Hertie Institute for Clinical Brain Research, Department of Neurodegeneration, Germany German Center of Neurodegenerative Diseases, University of Tübingen, Germany Department of Sports Medicine, University Clinic Tübingen, Germany d Department of Food and Nutrition, and Sport Science, University of Gothenburg, Sweden e Klinikum Kassel, Department of Neurology and Kassel Medical School, University of Southampton, Kassel, Germany f Department of Internal Medicine, University Clinic Tübingen, Germany b c
a r t i c l e i n f o
a b s t r a c t
Article history: Received 4 September 2014 Received in revised form 25 January 2015 Accepted 27 January 2015
Background: The impact of Nordic walking (NW) in Parkinson's disease (PD) has been investigated in several studies but results are inconsistent. This may be due to different cohorts studied and the heterogeneity of their PD symptoms which impact the outcome of NW. This study aimed at determining predictive factors for a positive effect of NW on PD. Methodology and principal findings: Primary outcome was to define the baseline disease-associated and demographic parameters that distinguish patients who demonstrate improvement in the Unified PD rating scale (UPDRS) motor part following NW training (“Uþ”) from those patients with no improvement after the same intervention (“U“). The potentially predictive parameters were: age, age at onset, disease duration, gait velocity, step length, daily step number, UPDRS-motor part, Berg-Balance-Scale, ParkinsonNeuropsychometric-Dementia-Assessment, verbal-fluency-test and Becks-Depression-Inventory-II. Twenty-two PD patients (H&Y stage 2e2.5) performed twelve weeks of NW training. Eighteen patients were included in the final analysis. Overall, the UPDRS motor part did not improve significantly; however, eight patients had an improvement in the UPDRS motor part from baseline to end of study (Uþ). When comparing the potentially predictive factors of the Uþ cohort with those ten patients who did not improve (U), there was a notable difference in gait velocity and step length, and showed a significant correlation with an improvement in the UDPRS motor part scores. Conclusion: Gait velocity and step length can predict the outcome of NW training as determined by the UPDRS motor part, indicating that PD patients with only slightly impaired gait performance benefit most. © 2015 Elsevier Ltd. All rights reserved.
Keywords: Parkinson's disease Nordic walking Predictive factors UPDRS motor part Gait velocity Step length
1. Introduction Physical activity has positive effects in general and also in patients with Parkinson's disease (PD). Nordic walking (also called pole walking) is regarded as an endurance sport. The cyclical motion sequences share similarities
* Corresponding author. Department of Neurodegeneration, Hertie Institute for Clinical Brain Research, German Center of Neurodegenerative Diseases, University of Tuebingen, Hoppe-Seyler-Str. 3, 72076 Tübingen, Germany. Tel.: þ49 7071 29 83119; fax: þ49 7071 29 4490. E-mail address: [email protected] (D. Berg). http://dx.doi.org/10.1016/j.parkreldis.2015.01.016 1353-8020/© 2015 Elsevier Ltd. All rights reserved.
with cross-country skiing: Fast walking is supported by two poles. Every time the left heel touches the ground, the right pole should hit the ground, and vice versa. Nordic walking (NW) is a particularly appealing physical activity as it takes place outdoors, can be performed almost everywhere and is safe. The effect of NW in PD patients has been investigated in several studies [1e6]; however results regarding whether PD patients benefit from NW or not are inconsistent. For example, whereas two studies [1,5] found positive effects using the best-accepted outcome measure of PD motor symptoms (the motor part of the Unified PD rating scale (UPDRS)), another study did not [3]. This might, at least partly, be due to differences in the cohorts studied and the heterogeneity of their PD. Based on the wish to develop a more “personalized” treatment
414
M. Herfurth et al. / Parkinsonism and Related Disorders 21 (2015) 413e416
regimen for chronic diseases including PD [7], we designed this study to determine whether specific demographic, motor, cognitive and behavioral parameters predict a clinical improvement as measured with the UPDRS motor part. 2. Patient and methods
weeks. Two sessions per week were led by a professional NW trainer; the third session was performed without a trainer. We separated the cohort in two groups A (n ¼ 10) and B (n ¼ 8). Group A trained first, during that time group B received no training and was designated as the control group. At 12 weeks group B started the training sessions.
2.1. Ethics The study protocol was approved by the ethical committee of the University of Tübingen, and all subjects provided written informed consent.
4. Data analysis and statistics
2.2. Subjects
Data were analyzed with SPSS 22 for Windows (SPSS Inc, Chicago, IL, USA). Because we used primarily ordinal data in this analysis we used median and range to present these data. Significance levels were calculated with the Wilcoxon signed rank or the ManneWhitney-U tests, and the Spearman's rank correlation coefficient. The decision to use these tests was based on the small numbers of subjects and the fact that almost none of the variables were distributed normally. The uncorrected alpha level was set at P ¼ 0.05 based on the exploratory nature of this study. However, for the correlation coefficient, we also present significance levels after Bonferroni correction because of multiple testing.
Thirty-four patients were recruited from the neurological outpatient clinic of the University of Tübingen and by newspaper advertisement. Twenty-two met the inclusion criteria and were included in the baseline assessment. They all fulfilled the UK Brain Bank criteria for PD [8], and had an akinetic-rigid or equivalent subtype of PD. Inclusion criteria were walking without assistance, >10 points on the UPDRS motor part during the medication OFF phase, improvement of at least 20 percent of the UPDRS motor part after medication intake, Hoehn and Yahr stage of 2 or 2.5, Schwab and England scale >50%, no previous experience with NW and less than 1.5 h exercise activity per week. Exclusion criteria were: history and presence of concurrent conditions which would influence NW training performance (e.g., musculoskeletal, psychiatric problems, dementia).
3. Assessment 5. Results All tests took place in the “OFF” state, i.e. at least twelve hours after the last dose of PD medication. UPDRS motor part was assessed at BL and after twelve weeks of NW. To determine baseline predictive factors, we assessed age, age at onset, disease duration, Berg Balance Scale (BBS), Parkinson neuropsychometric dementia assessment (PANDA), the verbal fluency test (patients were asked to generate as many S-words as possible during one minute) and the Becks Depression Inventory II (BDI II). In addition, we performed quantitative testing of gait velocity and step length. The participants were instructed to walk along a six meter path at a comfortable pace in our designated test laboratory. Gait parameters were measured with 6 infrared cameras and a Plug-In-Gait marker placement set, consisting of 39 anatomic markers (VICON®, Oxford Metrics, Oxford, UK). We also calculated the number of steps per day during the study period with a pedometer (Silva, Bromma, Sweden) that the subjects wore on the hip. Table 1 provides a summary of these parameters. All study participants performed three training sessions per week lasting approximately one hour each, for a total of twelve
Of the 22 study participants who were initially included, two had to change their Parkinson's medication during the training period, and 2 missed more than one session per week. Thus we were able to include the data of 18 study participants in the final analysis. Overall, the cohort as a whole showed no significant difference in the UPDRS motor part at BL and post training (BL: 30 (15e44), post training: 27 (13e47)jmedian (range), P ¼ 0.30), (Table 1). Similar results were found for the controls (group B during the first 12 weeks, BL: 27 (17e40), pre training: 27 (15e44), P ¼ 0.87). 8 study participants (from now on referred to as Uþ cohort), however, did improve from BL to the end of the study (2e13 points), 10 participants (U) did not improve (8 to 0 points). At BL, the UPDRS motor part of the Uþ BL 27 (17e37) and the U BL: 31 (15e44) cohorts did not differ significantly (P ¼ 0.408) but, as expected, was significantly different at the end of the study (post training Uþ: 20 (13e30)jU: 34 (18e44), P ¼ 0.002), (Table 1). When comparing the potentially predictive factors between Uþ and U, gait velocity (uncorrected P ¼ 0.02) and step length
Table 1 Baseline clinical and demographical data, and comparison of potentially predictive factors for a good outcome after a standardized Nordic walking training. For significantly different measures and UPDRS motor part also post training (pT) values are shown.
Age at onset [Y] Disease duration [Y] Age [Y] Steps per day [N] UPDRS motor part (0e108) BBS (0e56) verbal fluency [N] PANDA (0e30) BDI II (0e63) Gait velocity [m/s] Step length [mm]
Whole cohort [N ¼ 18] median (range)
Uþ [N ¼ 8] median (range)
U [N ¼ 10] median (range)
Mann-Whitey-U test U⁺/U (P value)
67 (55e75) 3 (0e16) 63 (50e73) 4550 (1094e11,982) 30 (15e44) pT:27 (13e47) 54 (44e56) 13 (7e24) 25 (9e30) 8 (1e24) 1.19 (0.95e1.63) pT:1.19 (0.92e1.67) 622 (500e767) pT:607 (504e768)
68 (55e73) 3 (0e7) 73 (55e75) 5066 (2710e7000) 27 (17e37) pT:20 (13e30) 54 (46e56) 13 (7e24) 25 (9e29) 5 (1e15) 1.27 (1.08e1.63) pT:1.36 (1.00e1.67) 650 (544e767) pT:661 (504e768)
60 (50e68) 5 (1e16) 66 (58e73) 3272 (1094e11,982) 31 (15e44) pT:34 (18e44) 52 (44e56) 12 (8e19) 22.5 (16e30) 8 (4e24) 1.09 (0.95e1.29) pT:1.12 (0.92e1.36) 587 (500e662) pT:575 (515e658)
0.114 0.236 0.274 0.364 0.408 pT:0.002 0.573 0.633 1.000 0.315 0.021 pT:0.08 0.043 pT:0.15
Demographic, motor, cognitive and behavioral parameters from the baseline assessment are presented with respect to e improvement (Uþ) or lack of improvement (U) on the Unified Parkinson's disease rating scale (UPDRS) motor part after a standardized 12 weeks Nordic walking training. BBS, Berg Balance Scale; BDI, Becks Depression Inventory; .m/s, meter per second; mm, millimeter; N, number; PANDA, Parkinson Neuropsychometric Dementia Assessment; UPDRS, Unified Parkinson's Disease Rating Scale, y, years.
M. Herfurth et al. / Parkinsonism and Related Disorders 21 (2015) 413e416
(uncorrected P ¼ 0.04) but none of the other parameters approached significance (Table 1). Correlation analyses between predictive factors, and change of the UPDRS motor part from BL to end of study basically confirmed this result: there was a significant correlation between the degree of improvement in the UPDRS motor part from BL to the end of study, and gait velocity and step length (Table 2).
6. Discussion This study focused on the determination of predictive factors associated with an improvement of the UPDRS motor part in PD patients who performed a standardized NW training program. The concept of this study and analysis was based on inconsistent results obtained in previous studies focusing on the investigation of the effect of NW in PD patients [1,3,5] and the hypothesis that specific subpopulations of PD patients may particularly benefit from this training whereas others may not. We hypothesized that a more individualized recruitment strategy, based on parameters predictive for beneficial outcome following a standardized NW training program, could help to clarify the issue. When comparing the Uþ with the U cohort, we found that BL gait velocity and step length were the only parameters which correlated with an improvement on the UPDRS motor part after NW. This suggests that particularly highly mobile PD patients benefit from NW. Gait velocity correlates with the axial items of the UPDRS motor part and step length also correlates with bradykinesia [9]. We hypothesize that patients with initially high gait velocity and step length are able to perform the training with greater flexibility and safety, which could influence the individual intensity of the NW training. The intensity of the training has repeatedly been shown to influence the outcome of physical activity interventions [5,10]. Our findings were unexpected, as we initially hypothesized that age at onset, disease duration, depression and cognitive state in particular might predict the outcome of the UPDRS motor part after Nordic walking with the idea that the influence exercise is associated with them [11]. However, our results do not support this hypothesis. For further studies it would be interesting to compare
415
larger cohorts with specific phenotypes such as depressed vs. nondepressed, younger vs. older age of onset etc. In particular, the inclusion of cognitively impaired PD patients may be an interesting approach as physical training has been shown to be effective in demented patients [12]. It would also be interesting to test the effect of the training on parameters such as muscle strength and general fitness as the correlation of improvements of gait velocity and step length with improvement in UPDRS motor part could also be explained by such more general factors. However, this was a pilot study which aimed at a “personalized approach”, and we argue that our results may justify the design of larger multicenter studies with a comparable study design. 7. Conclusion Gait velocity and step length can predict the outcome of NW training as determined by the UPDRS motor part, indicating that in particular PD patients with no or minor axial motor impairment benefit from NW training. Financial disclosures and competing interests Dr. Maetzler currently receives funding from the European Union and the Michael J Fox Foundation. In the past, he received funding from the Robert Bosch Foundation and speaker honoraria from GlaxoSmithKline. He reports no competing interests. Dr. Grau is supported by grants from Bauerfeind Germany, Elten GmbH, Reno Schuh GmbH and by honoraria from Bauerfeind Germany and Elten GmbH. He reports no competing interests. Dr. Berg has served on scientific consultancies and advisory boards for UCB Pharma and Novartis and received speaker honoraria from UCB Pharma, GlaxoSmithKline, TEVA Pharma, Lundbeck. Her scientific work is supported by grants from the Michael J. Fox Foundation, Janssen Pharmaceutica, UCB Pharma, Boehringer Ingelheim, Internationale Parkinson Fonds, German Parkinson's Disease Association (dPV) and TEVA. She reports no competing interests. Acknowledgments
Table 2 Spearman Rho correlation: correlations (P ¼ 0.05) between values of potentially predictive factors for positive outcome after NW-training, and improvement of the UPDRS motor part. Predictive factors
Age at onset Disease duration Age Steps per day UPDRS motor part BBS Verbal fluency PANDA BDI II Gait velocity Step length
Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance Correlation coefficient Significance
0.285 0.134 0.341 0.090 0.106 0.338 0.285 0.134 0.053 0.418 0.020 0.469 0.136 0.296 0.075 0.384 0.013 0.480 0.646 0.002a 0.458 0.028
a Correlation is significant after Bonferroni correction (P ¼ 0.005). BBS, Berg Balance Scale; BDI, Becks Depression Inventory; PANDA, Parkinson Neuropsychometric Dementia Assessment; UPDRS, Unified Parkinson's Disease Rating Scale.
We thank all individuals who took part in the study. WM is supported by the EU project SENSE-PARK (no. 288557), funded under the Seventh Framework Programme, Cooperation e ICT. References [1] Baatile J, Langbein WE, Weaver F, Maloney C, Jost MB. Effect of exercise on perceived quality of life of individuals with Parkinson's disease. J Rehabil Res 2010;37:529e34. [2] van Eijkeren FJ, Reijmers RS, Kleinveld MJ, Minten A, Bruggen JP, Bloem BR. Nordic walking improves mobility in Parkinson's disease. Mov Disord 2008;23:2239e43. [3] Ebersbach G, Ebersbach A, Edler D, Kaufhold O, Kusch M, Kupsch A, et al. Comparing exercise in Parkinson's diseaseethe Berlin LSVT(R)BIG study. Mov Disord 2010;25:1902e8. [4] Fritz B, Rombach S, Godau J, Berg D, Horstmann T, Grau S. The influence of Nordic walking training on sit-to-stand transfer in Parkinson patients. Gait Posture 2011;34:234e8. [5] Reuter I, Mehnert S, Leone P, Kaps M, Oechsner M, Engelhardt M. Effects of a flexibility and relaxation programme, walking, and Nordic walking on Parkinson's disease. J Aging Res 2011. 232473. [6] Ebersbach G, Ebersbach A, Gandor F, Wegner B, Wissel J, Kupsch A. Impact of physical exercise on reaction time in patients with Parkinson's disease-data from the Berlin BIG Study. Arch Phys Med Rehabil 2014;95:996e9. [7] Maetzler W, Nieuwhof F, Hasmann SE, Bloem BR. Emerging therapies for gait disability and balance impairment: promises and pitfalls. Mov Disord 2013;28:1576e86. [8] Hughes AJ, Daniel SE, Kilford L, Lees AJ. Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 1992;55:181e4.
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[9] Vieregge P, Stolze H, Klein C, Heberlein I. Gait quantitation in Parkinson's diseaseelocomotor disability and correlation to clinical rating scales. J Neural Transm 1997;104:237e48. [10] Gerecke KM, Jiao Y, Pani A, Pagala V, Smeyne R. Exercise protects against MPTP-induced neurotoxicity in mice. Brain Res 2010;1341:72e83.
[11] Hirsch MA, Farley BG. Exercise and neuroplasticity in persons living with Parkinson's disease. Eur J Phys Rehabil Med 2009;45:215e29. [12] Schwenk M, Dutzi I, Englert S, Micol W, Najafi B, Mohler J, et al. An intensive exercise program improves motor performances in patients with dementia: translational model of geriatric rehabilitation. J Alzheimers Dis 2014;39:487e98.