Baseline Gross Motor Function Affects the Outcome of Robot-Assisted Therapy in Ambulatory Individuals with Spastic Cerebral Palsy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Protocols
2.3. Assessment Protocol
2.3.1. Functional Assessment
- (a)
- Gross motor function: the 88-item GMFM (GMFM-88) was tested according to the instruction manual [18].
- (b)
- Ambulatory function: the GMFCS was used to classify individuals with CP into five levels of ambulatory ability, where level I means independent walking with minimal limitation and level V means no ambulation ability.
2.3.2. Clinical Assessments
- (a)
- Strength: manual muscle test (MMT) grading muscle strength from 1 to 5 was used. Standard positions and procedures for MMT were applied for the following muscles: hip flexors, hip extensors, knee flexors, knee extensors, ankle dorsiflexors, and the ankle plantar flexors of each lower limb [19].
- (b)
- (c)
- Selective motor control (SMC): SMC of the hip, knee, and ankle were graded from 2 (completely isolated of movement) to 1 (partially isolated movement) or to 0 (lack of ability to perform isolated movement) [22].
- (d)
- Passive range of motion (ROM): measured with a manual goniometer in standard positions and procedures for hip, knee, and ankle joint of each lower limb in all three anatomical planes; the Thomas test, unilateral and bilateral popliteal angle test, and hip anteversion angle were also measured [19].
2.3.3. Instrumental Strength Assessment
2.4. Data Analysis
2.5. Outcome Measures
- GMFM-88 total score: achieved percentage of the total possible score;
- Clinical examination: range of motion measured in degrees by manual goniometer;
- Motor impairments (weakness, lack of SMC, spasticity): changes in the severity of symptoms.
3. Results
3.1. Functional Assessment
3.2. Clinical Assessment
3.3. Instrumental Strength Assessment
3.4. Impact on Improvement
4. Discussion
Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Bayón, C.; Martín-Lorenzo, T.; Moral-Saiz, B.; Ramírez, Ó.; Pérez-Somarriba, Á.; Lerma-Lara, S.; Martínez, I.; Rocon, E. A robot-based gait training therapy for pediatric population with cerebral palsy: Goal setting, proposal and preliminary clinical implementation. J. Neuroeng. Rehabil. 2018, 15, 69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Novak, I.; McIntyre, S.; Morgan, C.; Campbell, L.; Dark, L.; Morton, N.; Stumbles, E.; Wilson, S.-A.; Goldsmith, S. A systematic review of interventions for children with cerebral palsy: State of the evidence. Dev. Med. Child. Neurol. 2013, 55, 885–910. [Google Scholar] [CrossRef]
- O’Shea, T.M. Diagnosis, Treatment, and Prevention of Cerebral Palsy. Clin. Obstet. Gynecol. 2008, 51, 816–828. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Patritti, B.L.; Sicari, M.; Deming, L.C.; Romaguera, F.; Pelliccio, M.M.; Kasi, P.; Benedetti, M.G.; Nimec, D.L.; Bonato, P. The role of augmented feedback in pediatric robotic-assisted gait training: A case series. Technol. Disabil. 2010, 22, 215–227. [Google Scholar] [CrossRef]
- Wessels, M.; Lucas, C.; Eriks, I.; de Groot, S. Body weight-supported gait training for restoration of walking in people with an incomplete spinal cord injury: A systematic review. J. Rehabil. Med. 2010, 42, 513–519. [Google Scholar] [CrossRef] [Green Version]
- Swinnen, E.; Duerinck, S.; Baeyens, J.; Meeusen, R.; Kerckhofs, E. Effectiveness of robot-assisted gait training in persons with spinal cord injury: A systematic review. J. Rehabil. Med. 2010, 42, 520–526. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cho, C.; Hwang, W.; Hwang, S.; Chung, Y. Treadmill Training with Virtual Reality Improves Gait, Balance, and Muscle Strength in Children with Cerebral Palsy. Tohoku J. Exp. Med. 2016, 238, 213–218. [Google Scholar] [CrossRef] [Green Version]
- Aycardi, L.F.; Cifuentes, C.A.; Múnera, M.; Bayón, C.; Ramírez, O.; Lerma, S.; Frizera, A.; Rocon, E. Evaluation of biomechanical gait parameters of patients with Cerebral Palsy at three different levels of gait assistance using the CPWalker. J. Neuroeng. Rehabil. 2019, 16, 15. [Google Scholar] [CrossRef] [PubMed]
- Zwicker, J.G.; Mayson, T.A. Effectiveness of Treadmill Training in Children with Motor Impairments: An Overview of Systematic Reviews. Pediatr. Phys. Ther. 2010, 22, 361–377. [Google Scholar] [CrossRef] [Green Version]
- Warken, B.; Graser, J.V.; Ulrich, T.; Borggraefe, I.; Heinen, F.; Meyer-Heim, A.; van Hedel, H.J.A.; Schroeder, A.S.; Aurich, T. Practical Recommendations for Robot-Assisted Treadmill Therapy (Lokomat) in Children with Cerebral Palsy: Indications, Goal Setting, and Clinical Implementation within the WHO-ICF Framework. Neuropediatrics 2015, 46, 248–260. [Google Scholar] [CrossRef] [PubMed]
- Lefmann, S.; Russo, R.; Hillier, S. The effectiveness of robotic-assisted gait training for paediatric gait disorders: Systematic review. J. Neuroeng. Rehabil. 2017, 14, 1. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Drużbicki, M.; Rusek, W.; Snela, S.; Dudek, J.; Szczepanik, M.; Zak, E.; Durmala, J.; Czernuszenko, A.; Bonikowski, M.; Sobota, G. Functional effects of robotic-assisted locomotor treadmill thearapy in children with cerebral palsy. J. Rehabil. Med. 2013, 45, 358–363. [Google Scholar] [CrossRef] [Green Version]
- Moreau, N.G.; Bodkin, A.W.; Bjornson, K.; Hobbs, A.; Soileau, M.; Lahasky, K. Effectiveness of Rehabilitation Interventions to Improve Gait Speed in Children with Cerebral Palsy: Systematic Review and Meta-analysis. Phys. Ther. 2016, 96, 1938–1954. [Google Scholar] [CrossRef] [Green Version]
- Cherng, R.-J.; Liu, C.-F.; Lau, T.-W.; Hong, R.-B. Effect of Treadmill Training with Body Weight Support on Gait and Gross Motor Function in Children with Spastic Cerebral Palsy. Am. J. Phys. Med. Rehabil. 2007, 86, 548–555. [Google Scholar] [CrossRef] [PubMed]
- Provost, B.; Dieruf, K.; Burtner, P.A.; Phillips, J.P.; Bernitsky-Beddingfield, A.; Sullivan, K.J.; Bowen, C.A.; Toser, L. Endurance and Gait in Children with Cerebral Palsy After Intensive Body Weight-Supported Treadmill Training. Pediatr. Phys. Ther. 2007, 19, 2–10. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Willoughby, K.L.; Dodd, K.J.; Shields, N. A systematic review of the effectiveness of treadmill training for children with cerebral palsy. Disabil. Rehabil. 2009, 31, 1971–1979. [Google Scholar] [CrossRef]
- Mutlu, A.; Krosschell, K.; Gaebler-Spira, D. Treadmill training with partial body-weight support in children with cerebral palsy: A systematic review. Dev. Med. Child. Neurol. 2009, 51, 268–275. [Google Scholar] [CrossRef] [PubMed]
- Russell, D.J.; Rosenbaum, P.L.; Avery, L.M.; Lane, M. Gross Motor Function Measure (GMFM-66 and GMFM-88) User’s Manual; Cambridge University Press: Cambridge, UK, 2002. [Google Scholar] [CrossRef]
- Hislop, H.; Avers, D.; Brown, M. Daniels and Worthingham’s Muscle Testing-E-Book: Techniques of Manual Examination and Performance Testing; Elsevier: Amsterdam, The Netherlands, 2013. [Google Scholar]
- Bohannon, R.W.; Smith, M.B. Interrater Reliability of a Modified Ashworth Scale of Muscle Spasticity. Phys. Ther. 1987, 67, 206–207. [Google Scholar] [CrossRef] [PubMed]
- Boyd, R.N.; Graham, H.K. Objective measurement of clinical findings in the use of botulinum toxin type A for the management of children with cerebral palsy. Eur. J. Neurol. 1999, 6, s23–s35. [Google Scholar] [CrossRef]
- Trost, J.P. Physical assessment and observational gait analysis. In The Treatment of Gait Problems in Cerebral Palsy; Gage, J.R., Ed.; MacKeith Press: London, UK, 2004; pp. 71–89. ISBN 9781898683377. [Google Scholar]
- Biodex System 4 Pro User Manual; Biodex Medical Systems, Inc.: Shirley, NY, USA, 2021.
- Meyer-Heim, A.; Borggraefe, I.; Ammann-Reiffer, C.; Berweck, S.; Sennhauser, F.H.; Colombo, G.; Knecht, B.; Heinen, F. Feasibility of robotic-assisted locomotor training in children with central gait impairment. Dev. Med. Child. Neurol. 2007, 49, 900–906. [Google Scholar] [CrossRef] [PubMed]
- Meyer-Heim, A.; Ammann-Reiffer, C.; Schmartz, A.; Schäfer, J.; Sennhauser, F.H.; Heinen, F.; Knecht, B.; Dabrowski, E.; Borggraefe, I. Improvement of walking abilities after robotic-assisted locomotion training in children with cerebral palsy. Arch. Dis. Child. 2009, 94, 615–620. [Google Scholar] [CrossRef] [Green Version]
- Borggraefe, I.; Kiwull, L.; Schaefer, J.S.; Koerte, I.; Blaschek, A.; Meyer-Heim, A.; Heinen, F. Sustainability of motor performance after robotic-assisted treadmill therapy in children: An open, non-randomized baseline-treatment study. Eur. J. Phys. Rehabil. Med. 2010, 46, 125–131. [Google Scholar] [CrossRef] [PubMed]
- Borggraefe, I.; Schaefer, J.S.; Klaiber, M.; Dabrowski, E.; Ammann-Reiffer, C.; Knecht, B.; Berweck, S.; Heinen, F.; Meyer-Heim, A. Robotic-assisted treadmill therapy improves walking and standing performance in children and adolescents with cerebral palsy. Eur. J. Paediatr. Neurol. 2010, 14, 496–502. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, A.S.; Homburg, M.; Warken, B.; Auffermann, H.; Koerte, I.; Berweck, S.; Jahn, K.; Heinen, F.; Borggraefe, I. Prospective controlled cohort study to evaluate changes of function, activity and participation in patients with bilateral spastic cerebral palsy after Robot-enhanced repetitive treadmill therapy. Eur. J. Paediatr. Neurol. 2014, 18, 502–510. [Google Scholar] [CrossRef] [PubMed]
- van Hedel, H.; Meyer-Heim, A.; Rüsch-Bohtz, C. Robot-assisted gait training might be beneficial for more severely affected children with cerebral palsy. Dev. Neurorehabilit. 2015, 19, 410–415. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, A.S.; Von Kries, R.; Riedel, C.; Homburg, M.; Auffermann, H.; Blaschek, A.; Jahn, K.; Heinen, F.; Borggraefe, I.; Berweck, S. Patient-specific determinants of responsiveness to robot-enhanced treadmill therapy in children and adolescents with cerebral palsy. Dev. Med. Child. Neurol. 2014, 56, 1172–1179. [Google Scholar] [CrossRef]
- Borggraefe, I.; Meyer-Heim, A.; Kumar, A.; Schaefer, J.S.; Berweck, S.; Heinen, F. Improved gait parameters after robotic-assisted locomotor treadmill therapy in a 6-year-old child with cerebral palsy. Mov. Disord. 2008, 23, 280–283. [Google Scholar] [CrossRef]
10 Min on Gamma VAST (AC International East, Knurów, Poland): |
|
|
5-Min break |
10 Min on Alfa VAST (AC International East, Knurów, Poland): |
|
|
10-Min break |
45 Min of EksoGT (Ekso Bionics, Richmond, CA, USA): |
|
|
The training starts from a shorter period (10 to 15 min). Depending on endurance, the usual walking time range from 30 min to 1 h. |
15-Min break |
2 × 15 Min on Zebris THQ-M-3i Treadmill (zebris Medical GmbH, Isny im Allgäu, Germany): |
|
|
5-Min Break |
The whole therapy program was performed under the supervision of two physical therapists experienced with RAT. |
All Groups | Group I (GMFCS = I and II) | Group II (GMFCS = III and IV) | |||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
t1 | t2 | p | t1 | t2 | p | t1 | t2 | p | |||||||||||||
Min [%] | Max [%] | Mean [%] | Min [%] | Max [%] | Mean [%] | Min [%] | Max [%] | Mean [%] | Min [%] | Max [%] | Mean [%] | Min [%] | Max [%] | Mean [%] | Min [%] | Max [%] | Mean [%] | ||||
GMFM | 19.93 | 99.44 | 99.44 | 21.63 | 21.63 | 21.63 | <0.01 | 65.21 | 65.21 | 65.21 | 65.59 | 65.59 | 65.59 | <0.01 | 19.63 | 19.63 | 19.63 | 21.56 | 21.56 | 21.56 | <0.01 |
GMFM part A | 76.47 | 100.00 | 100.00 | 80.39 | 80.39 | 80.39 | <0.01 | 92.15 | 92.15 | 92.15 | 96.07 | 96.07 | 96.07 | 0.04 | 76.47 | 76.47 | 76.47 | 80.39 | 80.39 | 80.39 | 0.03 |
GMFM part B | 21.67 | 100.00 | 100.00 | 20.00 | 20.00 | 20.00 | 0.02 | 85.00 | 85.00 | 85.00 | 96.66 | 96.66 | 96.66 | 0.03 | 21.67 | 21.67 | 21.67 | 20.00 | 20.00 | 20.00 | 0.26 |
GMFM part C | 0.00 | 100.00 | 100.00 | 7.14 | 7.14 | 7.14 | <0.01 | 14.28 | 14.28 | 14.28 | 14.28 | 14.28 | 14.28 | 0.02 | 0.00 | 0.00 | 0.00 | 7.14 | 7.14 | 7.14 | 0.01 |
GMFM part D | 0.00 | 100.00 | 100.00 | 0.00 | 0.00 | 0.00 | <0.01 | 61.54 | 61.54 | 61.54 | 61.54 | 61.54 | 61.54 | <0.01 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.13 |
GMFM part E | 0.00 | 97.22 | 97.22 | 0.00 | 0.00 | 0.00 | <0.01 | 19.44 | 19.44 | 19.44 | 54.17 | 54.17 | 54.17 | <0.01 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.00 | 0.08 |
Parameter | t1 | t2 | p | ||||
---|---|---|---|---|---|---|---|
Minimum [°] | Maximum [°] | Mean [°] | Minimum [°] | Maximum [°] | Mean [°] | ||
Hip flexion | 80 | 80 | 80 | 85 | 85 | 85 | 0.53 |
Hip abduction | 15 | 15 | 15 | 20 | 20 | 20 | 0.50 |
Hip internal rotation | 10 | 10 | 10 | 25 | 25 | 25 | 0.18 |
Hip external rotation | 0 | 0 | 0 | 0 | 0 | 0 | 0.87 |
Hip anteversion angle | 15 | 15 | 15 | 10 | 10 | 10 | 0.54 |
Knee extension | −10 | −10 | −10 | −15 | −15 | −15 | 0.76 |
Knee flexion | 100 | 100 | 100 | 100 | 100 | 100 | 0.05 |
Unilateral popliteal angle | 30 | 30 | 30 | 30 | 30 | 30 | 0.21 |
Bilateral popliteal angle | 25 | 25 | 25 | 20 | 20 | 20 | <0.01 |
Ankle dorsiflexion (knee flexion = 0°) | −35 | −35 | −35 | −40 | −40 | −40 | 0.56 |
Ankle dorsiflexion (knee flexion = 90°) | −10 | −10 | −10 | −20 | −20 | −20 | 0.76 |
Ankle plantarflexion | 15 | 15 | 15 | 20 | 20 | 20 | 0.17 |
Parameter | t1 | t2 | p | ||||
---|---|---|---|---|---|---|---|
Minimum (Nm) | Maximum (Nm) | Mean (Nm) | Minimum (Nm) | Maximum (Nm) | Mean (Nm) | ||
Knee extension | 5.5 | 5.5 | 5.5 | 8.8 | 8.8 | 8.8 | 0.47 |
Knee flexion | 0.1 | 0.1 | 0.1 | 0.0 | 0.0 | 0.0 | 0.05 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Manikowska, F.; Krzyżańska, A.; Chmara, P.; Chen, B.P.-J.; Jóźwiak, M. Baseline Gross Motor Function Affects the Outcome of Robot-Assisted Therapy in Ambulatory Individuals with Spastic Cerebral Palsy. Brain Sci. 2021, 11, 1563. https://doi.org/10.3390/brainsci11121563
Manikowska F, Krzyżańska A, Chmara P, Chen BP-J, Jóźwiak M. Baseline Gross Motor Function Affects the Outcome of Robot-Assisted Therapy in Ambulatory Individuals with Spastic Cerebral Palsy. Brain Sciences. 2021; 11(12):1563. https://doi.org/10.3390/brainsci11121563
Chicago/Turabian StyleManikowska, Faustyna, Anna Krzyżańska, Paweł Chmara, Brian Po-Jung Chen, and Marek Jóźwiak. 2021. "Baseline Gross Motor Function Affects the Outcome of Robot-Assisted Therapy in Ambulatory Individuals with Spastic Cerebral Palsy" Brain Sciences 11, no. 12: 1563. https://doi.org/10.3390/brainsci11121563
APA StyleManikowska, F., Krzyżańska, A., Chmara, P., Chen, B. P.-J., & Jóźwiak, M. (2021). Baseline Gross Motor Function Affects the Outcome of Robot-Assisted Therapy in Ambulatory Individuals with Spastic Cerebral Palsy. Brain Sciences, 11(12), 1563. https://doi.org/10.3390/brainsci11121563