NeuroRehabilitation 33 (2013) 323–328 DOI:10.3233/NRE-130962 IOS Press
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Effects of robotic treadmill training on functional mobility, walking capacity, motor symptoms and quality of life in ambulatory patients with Parkinson’s disease: A preliminary prospective longitudinal study Nurdan Pakera , Derya Bugdaycia , Goksen Goksenoglua , Aysu Senb and Nur Kesiktasc,∗ a Istanbul
Physical Medicine and Rehabilitation Education and Research Hospital, Istanbul, Turkey Ruh ve Sinir Hastaliklari Education and Research Hospital-Neurology Department, Istanbul, Turkey c Istanbul Mehmet Akif Ersoy GKDC Education and Research Hospital, Istanbul, Turkey b Bakirkoy
Abstract. BACKGROUND: Decreased mobility and walking capacity occur frequently in Parkinson’s disease (PD). Robotic treadmill training is a novel method to improve the walking capacity in rehabilitation. OBJECTIVES: The primary aim of this study was to investigate the effects of robotic treadmill training on functional mobility and walking capacity in PD. Secondly, we aimed to assess the effects of the robotic treadmill training the motor symptoms and quality of life in patients with PD. METHODS: Seventy patients with idiopathic Parkinson’s disease who admitted to the outpatient clinic of the rehabilitation hospital were screened and 12 ambulatory volenteers who met the study criteria were included in this study. Patients were evaluated by Hoehn Yahr (HY) scale clinically. Two sessions robotic treadmill training per week during 5 weeks was planned for every patient. Patients were evaluated by the Timed Up and Go (TUG) test, 10 meter walking test (10 MWT), Unified Parkinson’s Disease Rating Scale (UPDRS) motor section and Parkinson’s Disease Questionnaire-39 (PDQ-39) at the baseline, at the 5 and 12 weeks. Cognitive and emotional states of the patients were assessed by Mini Mental State Examination (MMSE) test and Hospital Anxiety and Depression Scale (HADS) at the baseline. All patients were under medical treatment for the PD in this study and drug treatment was not changed during the study. RESULTS: Ten patients completed the study. The mean age was 65.6 ± 6.6 years. Five patients (50%) were women. Disease severity was between the HY stage 1–3. Two patients did not continue the robotic treadmill training after 7 sessions. They also did not want to come for control visits. TUG test, 10 MWT and UPDRS motor subscale scores showed statistically significant improvement after robotic treadmill training (p = 0.02, p = 0.001, p = 0.016). PDQ-39 scores improved significantly after robotic treadmill training (p = 0.03), however, the scores turned back to the baseline level at the 12. week control.
∗ Address for correspondence: Nur Kesiktas, Atakent mahallesi, Avrupa Konutlari 1, 2AA 8. blok 27 Kucukcekmece, Halkali, Istanbul, Turkey. Tel.: +90 5414557933; Fax: +90 2126931323; E-mail:
[email protected].
1053-8135/13/$27.50 © 2013 – IOS Press and the authors. All rights reserved
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CONCLUSION: As a result of this preliminary study, robotic treadmill training was useful to improve the functional mobility, walking capacity and motor symptoms in mild to moderate PD. Robotic treadmill training provided a transient improvement in the quality of life during the treatment. Keywords: Parkinson’s disease, robotic treadmill training, Timed Up and Go test, 10 meter walk test, functional status, quality of life
1. Introduction Parkinson disease (PD) is a central nervous system disorder that is characterized with tremor, rigidity and bradykinesia. Patients experience walking difficulty in the advanced stages of the disease. Both step length and step velocity are decreased in PD without levodopa. Levodopa leads to increase in step length and step velocity. Moreover, half of the patients with PD cannot stop walking easily [4]. It is suggested that the physiotherapy interventions besides the medical treatment are useful to decrease the disability and improve the quality of life [15]. Exercise helps to increase the strength of lower limbs and improve the physical functions, balance, walking and quality of life in PD [8]. The type and the duration of the exercises and the stage of the disease that exercises are most useful are not definitly known [1]. The useful effects of exercises mediated by the mechanisms such as neuroprotection, neurotransmission, plasticity, neurogenesis, homeostasis and neurotrophic factors [1]. Moreover exercises increase the level of serum calcium in the animal experiments. Calcium leads to increase in dopamin synthesis via calmodulindependent system in brain. This may explain why the exercises improve motions in PD [23]. Treadmill training may help to improve walking in the patients with PD. The speed of treadmill can be adjusted according to the capacity of the patient and if necessary speed can be increased [20]. In a previous study, treadmill training has been found to be effective in term of the improvement in the walking parameters [11]. It is concluded that the effects of treadmill training on the walking are not clear in PD; it helps to improve pace, stride length and walking distance, however, it has no effect on cadence according to the Cochrane review in 2010 [14]. Robotic treadmill training provides safer and long duration walking and is prefered more frequently in the last years. It is thought that the system is clinically useful, however, the efficacy of the robotic system did not proved clearly [10]. According to the results of a previous review, the effects of robotic gait training on
lokomotor functions have not been proved yet in PD [24]. The primary aim of this study was to investigate the effects of robotic treadmill training on the functional mobility and walking capacity in the ambulatory patients with idiopathic PD. Furthermore the efficacy of robotic training in terms of motor symptoms and quality of life were aimed to be assessed.
2. Materials and method The ambulatory patients with idiopathic PD who admitted to the outpatient clinic of the rehabilitation hospital between October 1, 2010 and June 30, 2011 were screened and the patients who met the study criteria were asked if they want to participate to the robotic treadmill training study. The inclusion criteria were to be 50–80 years and to have PD Hoehn Yahr stage 1 to 3. The patients with cognitive or cooperation disorder, another neurological disorder, uncontrolled hypertension, orthostatic hypotension, cardiovascular system disorder or rigidity that interferes with walking or who had deep brain stimulator implantation were excluded. Seventy patients with PD who admitted to the outpatient clinic of the rehabilitation hospital were screened. Forty-eight patients had at least one exclusion criteria. Ten patients did not want to participate the study because of transportation difficulty. Finally 12 volunteers with PD were included in the study. Patients were evaluated at the baseline, at the 5 and 12 weeks. Timed Up and Go (TUG) test, 10 meter walk test (10 MWT), Unified Parkinson’s Disease Rating Scale (UPDRS) motor section, Parkinson’s Disease Questionnaire (PDQ-39) were used at the baseline, at the 5 and 12 weeks. Mental State Examination (MMSE) test and Hospital Anxiety and Depression Scale (HADS) were used to assess the cognitive and emotional states at the baseline. Treatment protocol was consisted of 2 sessions of robotic treadmill training per week, total 10 sessions during 5 weeks. Robotic treadmill training was performed under the supervision of a trained physio-
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therapist. Lokomat, Hocoma Inc, Zurich, Switzerland was used for the robotic treadmill training. Patients were participated robotic treadmill training with 50% body weight support at the beginning. Body weight support was decreased by time. All patients were walking with full body weight at the end of the study. Physiotherapist made the adjustments for the robotic device before the training. Patients were equiped exoskeleton orthosis for support the lower extremities before the robotic treadmill training. Patients walked 20 minutes in every session. Robotic treadmill training and evaluation tests were programmed in three hours after dopamin intake in the patients who use this drug. Medical treatment regimens were not changed during the study.
2.4. Timed up & go (TUG) test
2.1. Hoehn and Yahr (HY) staging scale
2.5. 10-meter walk test (10 MWT)
HY is a 5 graded simple and easy to use scale that helps to indicate functional status in PD. Stage 1 indicates unilateral involvement, Stage 2 shows clinically bilateral disease. There is no balance defisit in those stages. Postural instability besides bilateral involvement occur in stage 3 and person is independent. Patient is physically dependent but still able to walk in Stage 4, however, in Stage 5 he/she is dependent to a wheelchair or bed [9]. The Task Force on Rating Scales in Parkinson’s Disease concluded that the HY scale is an important descriptive scale [7].
10 MWT is an easy test that provides information about the walking capacity. The operator gave instruction to the patients for walking at a comfortable pace over a 10 meter distance at the beginning. All patients repeated the 10 MWT twice and mean values were calculated [21]. 10 MWT is a reliable test that can be used in PD [12]. This study was approved by the Hospital Ethics Committee. Written consents were obtained from the patients.
TUG test measures the time required for standing up from the chair, walking 3 meters on the floor, turning around, returning and sitting down again. TUG is a reliable test that can be used to measure functional mobility in clinically mild to moderate PD [16]. Information about the procedure was given all the patients before the test. They worn comfortable shoes during the test. The average time of 3 tests is calculated in seconds. TUG test ≤10 seconds is generally accepted as being normal for the older people [19]. TUG test results ≤10 seconds in HY stage 1 to 2 PD, however, it is >10 seconds in the patients stage >2 [21].
3. Statistical analysis 2.2. Unified Parkinson’s disease rating scale (UPDRS) UPDRS gives information about the clinical status and the course of the PD. It has 4 sections; first section is mentation, behavior and mood, second is activities of daily living, third section is motor evaluation. The first three sections include 44 questions. Every item was evaluated on a 5 point scale (0–4). Total score for the sections 1, 2, and 3 ranges between 0–176. Motor section has 14 questions. Higher scores indicate severe disease. Complications related with the treatment were queried in the forth section. Section four is consisted of 11 questions and total score ranges between 0–23 [5]. 2.3. Parkinson’s disease questionnaire (PDQ-39) PDQ-39 helps to evaluate quality of life in the patients with PD. PDQ-39 can be used in different languages and validation study has been performed [17].
SPSS 10.0 statistical package program was used for the statistical analysis. Non-parametric tests, Friedman and Wilcoxon tests were used. 4. Results Ten patients completed the10 sessions of robotic treadmill training. Two patients were drop out the study after 7 sessions and did not come to control visits. One patient did not continue the study because of transportation difficulty. The other one gave up the robotic treadmill training because of fatique. Patient characteristics are shown in Table 1. Disease severity was mild to moderate in this study and all the patients were being ambulate independently. MMSE results indicate that the patients were cognitively normal. The mean HADS anxiety score was in the normal range, however, the mean HADS depression score was higher than the normal values.
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N. Paker et al. / A preliminary prospective longitudinal study Table 1 Demographic characteristics
Age (y) Gender F/M n(%) Marital status Married/single n(%) Employment Retired/housewife n(%) Height (cm) Weight (kg) BMI (kg/ m²)
5. Discussion
Mean
SD
Min
Max
65.5 5/5 (50/50)
6.6
54.0
76.0
9.9 14.4 4.5
150.0 50.0 20.30
178.0 100.0 35.40
8/2 (80/20) 6/4 (60/40) 161.9 74.3 28.23
Table 2 Clinical characteristics Disease duration (y) Hoehn Yahr Scale n(%) Stage 1 Stage 2 Stage 3 MMSE test score HADS Anxiety Depression Comorbidities n(%) Diabetes Hypertension COPD Osteoporosis Others Antiparkinsonian drugs n(%) Dopamine Rasagiline Pramipexole Ropirinole Entacapone
Mean
SD
Min
Max
3.6
2.9
1.0
10.0
6 (60) 3 (30) 1 (10) 27.1
1.6
25
30
4.6 7.4
3.4 3.8
0 1
8 13
3 (30) 5 (50) 1 (10) 2 (20) 3 (30) 9 (90) 6 (60) 1 (10) 1 (10) 1 (10)
MMSE: Mini Mental Strate Examination, HADS: Hospital Anxiety and Depression Scale.
Clinical characteristics are summarized in Tables 2 and 3. TUG test and 10 MWT values statistically significantly decreased after robotic treadmill training (p = 0.02, p = 0.001). UPDRS motor scores improved significantly at the 5 and 12 weeks (p = 0.016). PDQ39 total scores also improved after treatment (p = 0.03), however, the improvement in the QoL did not continue at the 12 week control (p = 0.117).
Robotic treadmill training was useful in terms of the improvement in functional mobility, walking capacity and motor symptoms in a group of cognitively ambulatory PD patients in this preliminary study. Any adverse event didnot reported during the study. Twelve volenteers were included in this study after screening 70 patients with PD. The comorbidities and problems related with the disease like rigidity, fatique and walking difficulty interfere with the robotic treadmill training in PD. In a recent study in which 334 patients with PD have been screened and 30 persons aged 67.8 years who met the study criteria, have been randomized to the robotic or conventional treadmill training; they had total 12 sessions of gait training and evaluations have been done after the treatment, at the 3 and 6 months by using 6-minute walk test (6 MWT), 10 MWT and TUG test. In the same study, it is reported that all the test scores have been improved significantly in both groups and there was no significant difference in terms of improvement between the robotic and conventional treadmill gait training groups [3]. In this study quality of life improved after treatment but the improvement did not continue after the followup period. Two patients (20%) had anxiety disorder and 5 had (50%) depression. Carda et al. [3], concluded that neither robotic nor conventional treadmill training has been provided no significant improvement in the quality of life measured by SF-12 in PD. Lo et al. [13], reported that freezing of gait showed 20.7 % improvement and some subscales of the quality of life as measured by PDQ-39 improved significantly after 10 sessions of robot assisted treadmill training with body weight support in PD. Forty percent body weight support has been used at the beginning of the study and it has been decreased by time. Walking speed has been 1.5 km/h at the beginning, however, it has been 2.2–2.5 km/h at the last measurement. All patients have been walking independently and faster at the end of the study and no adverse event was reported during the study.
Table 3 Follow up parameters Baseline
5 Week
TUG test (sec) 10 MWT (sec) PDQ-39 UPDRS motor score ∗ PDQRS
11 ± 2.58 9.4 ± 1.51 37.9 ± 20.59 20.3 ± 3.71
(baseline-5 week) Wilcoxon p < 0.03.
12 Week 10.1 ± 1.59 8.2 ± 0.92 31 ± 17.73* 19.9 ± 4.17
K
p
9.3 ± 0.95 7.8 ± 1.03 37.5 ± 29.6 19.2 ± 3.82
7.81 13.9 4.3 8.23
p = 0.02 p = 0.001 p = 0.117 p = 0.016
N. Paker et al. / A preliminary prospective longitudinal study
Ustinova et al. [25], concluded that the pace and stride length were increased and some sections of UPDRS showed improvement after 6 sessions of robot assisted treadmill training in a patient with PD. Robotic treadmill training has the advantage of one trained physiotherapist can manage the patient by means of exoskeleton orthosis during the treatment. But it is an expensive treatment that cannot be find in every rehabilitation center. In a previous review, it is concluded that there are a few studies evaluating the robotic treadmill training with the limited number of patients in spinal cord injury (SCI) and as a result robotic treadmill training may help walking the SCI patients [22]. Picelli et al. [18], reported that 4-week gait training by using a robotic stepper has been provided better improvement in terms of gait speed, walking capacity and cadance as compared with the conventional gait therapy combined with the range of motion exercises in a group of patients with PD. All the patients were under drug therapy and the medical treatment was stabil during the study. Drug treatment is essential for the control of parkinsonian symptoms in PD. Ambulation limitation occurs in the later stages in PD and patients become dependent to the wheelchair or bed. The aim of the exercise program is to facilitate the mobility and to preserve the ambulation capacity. For this reason, different exercise programs can be used in PD. In a recent study, it is concluded that warm-up, stretching, relaxation, range of motion exercises combined with gait and balance training and occupational therapy for 4 weeks inpatient rehabilitation program, could prevent the impairment in the motor symptoms and the necessity (requirement) of increase in drug dosage in PD [6]. In another study that compares the land-based and aquatic treatment results, aquatic exercises have been found to be more effective in term of the improvement in balance in the patieints with PD [26]. Canning et al. [2], reported that minimally supervised home-based treadmill training 4 sessions in a week during 6 weeks, can safely be used in PD and provides some improvement in terms of fatique and quality of life, however, it has no effect on the walking capacity, walking speed and motor symptoms as measured by 6 MWT in a controlled study. The strength of this preliminary study is the longitudinal design with 12 weeks follow-up. The limitations of this study are relatively small patient group and not to be a control group. As a result robotic treadmill training is found to be effective in terms of the improvement in the functional mobility, walking capacity and motor symptoms in PD.
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Quality of life improved after the treatment, however, the improvement did not continue during the followup period. Robotic treadmill training is a promising treatment in PD that helps ambulation.
Declaration of interest There is no conflict of interest.
References [1]
[2]
[3]
[4]
[5]
[6]
[7]
[8]
[9] [10]
[11]
Alonso-Frech, F., Sanahuja, J. J., & Rodriquez, A. M. (2011). Exercises and physical therapy in early management of Parkinson disease. Neurologist, 17(6 Suppl 1), S47-S53. Canning, C. G., Allen, N. E., Dean, C. M., Goh, L., & Fung V. S. C. (2012). Home based treadmill training for individuals with Parkinson’s disease: A randomized controlled pilot trial. Clin Rehabil, 26(9), 817-826. Carda, S., Invernizzi, M., Baricich, A., Comi, C., Croquelois, A., & Cisari, C. (2012). Robotic gait traning is not superior to conventional treadmill training in Parkinson disease: A singleblind randomized controlled trial. Neurorehabil Neural Repair, 26(9), 1027-1034. Chastan, N., Do, M. C., Bonneville, F., Torny, F., Bloch, F., Westby, G. W., Dormont, D., Agid, Y., & Welter, M. L. (2009). Gait and balance disorders in Parkinson’s disease: Impaired active braking of the fall of centre of gravity. Mov Disord, 24(2), 188-195. Fahn, S., Elton, R.L., & UPDRS Development Committeee. (1987). Unified Parkinson’s Disease Rating Scale. In S. Fahn, C. D. Marsden, D. B. Calne & M. Goldstein, eds. Recent Developments in Parkinson’s Disease. Florham Park, NJ: MacMillan 153-163. Frazzitta, G., Bertotti, G., Riboldazzi, G., Turla, M., Uccellini, D., Boveri, N., Guaglio, G., Perini, M., Comi, C., Balbi, P., & Maestri, R. (2012). Effectiveness of intensive rehabilitation treatment on disease progression in Parkinsonian patients: A randomized controlled trial with 1-year follow-up. Neurorehabil Neural Repair, 26(2), 144-150. Goetz, C. G., Poewe, W., Rascol, O., Sampaio, C., Stebbins, G. T., Counsell, C., Giladi, N., Holloway, R. G., Moore, C. G., Wenning, G. K., Yahr, M. D., & Seidl, L. (2004). Movement Disorder Society Task Force Report on the Hoehn and Yahr Staging Scale: Status and recommendations. Mov Disord, 19(9), 1020-1028. Goodwin, V. A., Richards, S. H., Taylor, R. S., Taylor, A. H., & Campbell, C. L. (2008). The effectiveness of exercise interventions for people with Parkinson’s disease: A systematic review and meta-analysis. Mov Disord, 23(5), 631-640. Hoehn, N. M., & Yahr, M. D. (1967). Parkinsonism: Onset, progression and mortality. Neurology, 17(5), 427-442. Hussain, S., Xie, S. Q., & Liu, G. (2011). Robot assisted treadmill training: Mechanisms and training strategies. Med Eng Phys, doi:10.1016/medengphy.2010.12.010. Kurtais, Y., Kutlay, S., Tur, B. S., Gok, H., & Akbostanci, C. (2008). Does treadmill training improve lower extremity tasks in Parkinson disease? A randomized controlled trial. Clin J Sport Med, 18(3), 289-291.
328 [12]
[13]
[14]
[15]
[16]
[17]
[18]
[19]
N. Paker et al. / A preliminary prospective longitudinal study Lim, L. I. I. K., van Wegen, L. L. H., de Goede, C. J. T., Jones, D., Rochester, L., Hetherington, V., Nieuwboer, A., Willems, A. E., & Kwakkel, G. (2005). Measuring gait and gait related activities in Parkinson’s patients own home environment: A reliability, responsiveness and feasibility study. Parkinsonism Relat Disord, 11, 19-24. Lo, A. C., Chang, V. C., Gianfrancesco, M. A., Friedman, J. H., Patterson, T. S., & Benedicto, D. F. (2010). Reduction of freezing of gait in Parkinson’s disease by repetitive robot-assisted treadmill training: A pilot study. J Neuroeng Rehabil 7, 5. Mehrholz, J., Friis, R., Kugler, J., Twork, S., Storch, A., & Pohl, M. (2010). Treadmill training for patients with Parkinson’s disease. Cochrane Database Syst Rev, 20(1). Morris, M. E. (2000). Movement disorders in people with Parkinson’s disease: A model for physical therapy. Phys Ther, 80(6), 578-597. Morris, S., Morris, M. E., & Iansek R. (2001). Reliability of measurements obtained with the Timed Up and Go test in people with Parkinson Disease. Phys Ther, 81, 810-818. Peto, V., Jenkinson, C., Fitzpatrick, R., & Greenhall, R. (1995). The development and validation of a short measure of functioning and well being for individuals with Parkinson’s Disease. Qual Life Res, 4(3), 241-248. Picelli, A., Melotti, C., Origano, F., Waldner, A., Fiaschi, A., Santilli, V., & Smania, N. (2012). Robot assisted gait training in patients with Parkinson disease: A randomized controlled trial. Neurorehabil Neural Repair, 26(4), 353-361. Podsiadlo, D., & Richardson, S. (1991). The Timed “Up & Go”: A test of basic functional mobility for frail elderly persons. J Am Geriatr Soc, 39, 142-148.
[20]
[21]
[22]
[23] [24]
[25]
[26]
Pohl, M., Rockstroh, G., R¨uckriem, S., Mrass, G., & Mehrholz, J. (2003). Immediate effects of speed dependent treadmill training on gait parameters in Parkinson’s disease. Arch Phys Med Rehabil, 84(12), 1760-1766. Schenkman, M., Ellis, T., Christiansen, C., Baron, A. E., Tickle-Degnen, L., Hall, D. A., & Wagenaar, D. (2011) Profile of functional limitations and task performance among people with early- and middle stage Parkinson disease. Phys Ther 91(9), 1339-1354. Swinnen, E., Duerinck, S., Baeyens, J. P., Meeusen, R., & Kerckhofs, E. (2010). Effectiveness of robot-assisted gait training in persons with spinal cord injury: A systematic review. J Rehabil Med, 42, 520-526. Sutoo, D., & Akiyama, K. (2003). Regulation of brain function by exercise. Neurobiol Dis, 13(1), 1-14. Tefertiller, C., Pharo, B., Evans, N., & Winchester, P. (2011). Efficacy of rehabilitation robotics for walking training in neurological disorders: A review. J Rehabil Res Dev, 48(4), 387-416. Ustinova, K., Chernikova, L., Bilimenko, A., Telenkov, A., & Einstein, N. (2011). Effect of robotic locomotor training in an individual with Parkinson’s disease: A case report. Disabil Rehabil Assist Technol, 6(1), 77-85. Vivas, J., Arias, P., & Cudeiro, J. (2011). Aquatic therapy versus conventional land-based therapy for Parkinson’s disease: An open-label pilot study. Arch Phys Med Rehabil, 92, 1202-1210.
