Advertisement

Annals of Biomedical Engineering

, Volume 46, Issue 9, pp 1376–1384 | Cite as

Immersive Virtual Reality to Improve Walking Abilities in Cerebral Palsy: A Pilot Study

  • Chiara Gagliardi
  • Anna Carla Turconi
  • Emilia Biffi
  • Cristina Maghini
  • Alessia Marelli
  • Ambra Cesareo
  • Eleonora Diella
  • Daniele Panzeri
Article

Abstract

Immersive virtual reality (IVR) offers new possibilities to perform treatments in an ecological and interactive environment with multimodal online feedbacks. Sixteen school-aged children (mean age 11 ± 2.4 years) with Bilateral CP—diplegia, attending mainstream schools were recruited for a pilot study in a pre–post treatment experimental design. The intervention was focused on walking competences and endurance and performed by the Gait Real-time Analysis Interactive Lab (GRAIL), an innovative treadmill platform based on IVR. The participants underwent eighteen therapy sessions in 4 weeks. Functional evaluations, instrumental measures including GAIT analysis and parental questionnaire were utilized to assess the treatment effects. Walking pattern (stride length left and right side, respectively p = 0.001 and 0.003; walking speed p = 0.001), endurance (6MWT, p = 0.026), gross motor abilities (GMFM-88, p = 0.041) and most kinematic and kinetic parameters significantly improved after the intervention. The changes were mainly predicted by age and cognitive abilities. The effect could have been due to the possibility of IVR to foster integration of motor/perceptual competences beyond the training of the walking ability, giving a chance of improvement also to older and already treated children.

Keywords

Immersive virtual reality Gait rehabilitation Children Cerebral palsy 

References

  1. 1.
    Andersson, C., L. Asztalos, and E. Mattsson. Six-minute walk test in adults with cerebral palsy. A study of reliability. Clin. Rehabil. 20:488–495, 2006.CrossRefPubMedGoogle Scholar
  2. 2.
    Bax, M., M. Goldstein, P. Rosenbaum, A. Leviton, N. Paneth, B. Dan, B. Jacobsson, D. Damiano, and Executive Committee for the Definition of Cerebral Palsy. Proposed definition and classification of cerebral palsy, April 2005. Dev. Med. Child Neurol. 47(571–576):2005, 2005.Google Scholar
  3. 3.
    Beltran, E. J., J. B. Dingwell, and J. M. Wilken. Margins of stability in young adults with traumatic transtibial amputation walking in destabilizing environments. J. Biomech. 47:1138–1143, 2014.CrossRefPubMedGoogle Scholar
  4. 4.
    Biffi, E., E. Beretta, A. Cesareo, C. Maghini, A. C. Turconi, G. Reni, and S. Strazzer. An immersive virtual reality platform to enhance walking ability of children with acquired brain injuries. Methods Inf. Med. 56(2):119–126, 2017.CrossRefPubMedGoogle Scholar
  5. 5.
    Bohannon, R. W., and M. B. Smith. Interrater reliability of a modified Ashworth scale of muscle spasticity. Phys. Ther. 67:206–207, 1987.CrossRefPubMedGoogle Scholar
  6. 6.
    Bottcher, L. Children with spastic cerebral palsy, their cognitive functioning, and social participation: a review. Child. Neuropsychol. 16:209–228, 2010.CrossRefPubMedGoogle Scholar
  7. 7.
    Cameirao, M. S., S. B. Badia, E. Duarte, A. Frisoli, and P. F. Verschure. The combined impact of virtual reality neurorehabilitation and its interfaces on upper extremity functional recovery in patients with chronic stroke. Stroke 43:2720–2728, 2012.CrossRefPubMedGoogle Scholar
  8. 8.
    Cho, C., W. Hwang, S. Hwang, and Y. Chung. Treadmill training with virtual reality improves gait, balance, and muscle strength in children with cerebral palsy. Tohoku J. Exp. Med. 238:213–218, 2016.CrossRefPubMedGoogle Scholar
  9. 9.
    Damiano, D. L., K. E. Alter, and H. Chambers. New clinical and research trends in lower extremity management for ambulatory children with cerebral palsy. Phys. Med. Rehabil. Clin. N. Am. 20:469–491, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Darter, B. J., and J. M. Wilken. Gait training with virtual reality-based real-time feedback: improving gait performance following transfemoral amputation. Phys. Ther. 91:1385–1394, 2011.CrossRefPubMedGoogle Scholar
  11. 11.
    Druzbicki, M., W. Rusek, S. Snela, J. Dudek, M. Szczepanik, E. Zak, J. Durmala, A. Czernuszenko, M. Bonikowski, and G. Sobota. Functional effects of robotic-assisted locomotor treadmill therapy in children with cerebral palsy. J. Rehabil. Med. 45:358–363, 2013.CrossRefPubMedGoogle Scholar
  12. 12.
    Druzbicki, M., W. Rusek, M. Szczepanik, J. Dudek, and S. Snela. Assessment of the impact of orthotic gait training on balance in children with cerebral palsy. Acta Bioeng. Biomech. 12:53–58, 2010.PubMedGoogle Scholar
  13. 13.
    Fung, J., C. L. Richards, F. Malouin, B. J. McFadyen, and A. Lamontagne. A treadmill and motion coupled virtual reality system for gait training post-stroke. Cyberpsychol. Behav. 9:157–162, 2006.CrossRefPubMedGoogle Scholar
  14. 14.
    Gagliardi, C., A. Tavano, A. C. Turconi, and R. Borgatti. Sequence memory skills in spastic bilateral cerebral palsy are age independent as in normally developing children. Disabil. Rehabil. 35:506–512, 2013.CrossRefPubMedGoogle Scholar
  15. 15.
    Geijtenbeek, T., F. Steenbrink, B. Otten, and O. Even-Zohar. D-flow: immersive virtual reality and real-time feedback for rehabilitation. Proceedings of the VRCAI 2011, 2011, pp. 201–208.Google Scholar
  16. 16.
    Gutierrez, R. O., F. Galan Del Rio, R. Cano de la Cuerda, I. M. Alguacil Diego, R. A. Gonzalez, and J. C. Page. A telerehabilitation program by virtual reality-video games improves balance and postural control in multiple sclerosis patients. NeuroRehabilitation 33:545–554, 2013.PubMedGoogle Scholar
  17. 17.
    Hak, L., H. Houdijk, P. van der Wurff, M. R. Prins, A. Mert, P. J. Beek, and J. H. van Dieen. Stepping strategies used by post-stroke individuals to maintain margins of stability during walking. Clin. Biomech. (Bristol, Avon) 28:1041–1048, 2013.CrossRefGoogle Scholar
  18. 18.
    Kaufman, K. R., M. P. Wyatt, P. H. Sessoms, and M. D. Grabiner. Task-specific fall prevention training is effective for warfighters with transtibial amputations. Clin. Orthop. Relat. Res. 472:3076–3084, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Lamontagne, A., J. Fung, B. J. McFadyen, and J. Faubert. Modulation of walking speed by changing optic flow in persons with stroke. J. Neuroeng. Rehabil. 4:22, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Luna-Oliva, L., R. M. Ortiz-Gutierrez, R. Cano-de la Cuerda, R. M. Piedrola, I. M. Alguacil-Diego, C. Sanchez-Camarero, and C. Martinez Culebras Mdel. Kinect Xbox 360 as a therapeutic modality for children with cerebral palsy in a school environment: a preliminary study. NeuroRehabilitation 33:513–521, 2013.PubMedGoogle Scholar
  21. 21.
    McAndrew, P. M., J. B. Dingwell, and J. M. Wilken. Walking variability during continuous pseudo-random oscillations of the support surface and visual field. J. Biomech. 43:1470–1475, 2010.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Meyer-Heim, A., C. Ammann-Reiffer, A. Schmartz, J. Schafer, F. H. Sennhauser, F. Heinen, B. Knecht, E. Dabrowski, and I. Borggraefe. Improvement of walking abilities after robotic-assisted locomotion training in children with cerebral palsy. Arch. Dis. Child. 94:615–620, 2009.CrossRefPubMedGoogle Scholar
  23. 23.
    Mutlu, A., K. Krosschell, and D. G. Spira. Treadmill training with partial body-weight support in children with cerebral palsy: a systematic review. Dev. Med. Child Neurol. 51:268–275, 2009.CrossRefPubMedGoogle Scholar
  24. 24.
    Novacheck, T. F., J. L. Stout, and R. Tervo. Reliability and validity of the Gillette Functional Assessment Questionnaire as an outcome measure in children with walking disabilities. J. Pediatr. Orthop. 20:75–81, 2000.PubMedGoogle Scholar
  25. 25.
    Oeffinger, D., A. Bagley, S. Rogers, G. Gorton, R. Kryscio, M. Abel, D. Damiano, D. Barnes, and C. Tylkowski. Outcome tools used for ambulatory children with cerebral palsy: responsiveness and minimum clinically important differences. Dev. Med. Child Neurol. 50:918–925, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    O’Neil, R. L., R. L. Skeel, and K. I. Ustinova. Cognitive ability predicts motor learning on a virtual reality game in patients with TBI. NeuroRehabilitation 33:667–680, 2013.PubMedGoogle Scholar
  27. 27.
    Palisano, R., P. Rosenbaum, S. Walter, D. Russell, E. Wood, and B. Galuppi. Development and reliability of a system to classify gross motor function in children with cerebral palsy. Dev. Med. Child Neurol. 39:214–223, 1997.CrossRefPubMedGoogle Scholar
  28. 28.
    Palisano, R. J., L. A. Chiarello, M. Orlin, D. Oeffinger, M. Polansky, J. Maggs, A. Bagley, G. Gorton, and Children’s Activity and Participation Group. Determinants of intensity of participation in leisure and recreational activities by children with cerebral palsy. Dev. Med. Child Neurol. 53:142–149, 2011.CrossRefPubMedGoogle Scholar
  29. 29.
    Peri, E., A. C. Turconi, E. Biffi, C. Maghini, D. Panzeri, R. Morganti, A. Pedrocchi, and C. Gagliardi. Effects of dose and duration of robot-assisted gait training on walking ability of children affected by cerebral palsy. Technol. Health Care 25(4):671–681, 2017.CrossRefPubMedGoogle Scholar
  30. 30.
    Rosie, J. A., S. Ruhen, W. A. Hing, and G. N. Lewis. Virtual rehabilitation in a school setting: is it feasible for children with cerebral palsy? Disabil. Rehabil. Assist. Technol. 10:19–26, 2015.CrossRefPubMedGoogle Scholar
  31. 31.
    Sessoms, P. H., M. Wyatt, M. Grabiner, J. D. Collins, T. Kingsbury, N. Thesing, and K. Kaufman. Method for evoking a trip-like response using a treadmill-based perturbation during locomotion. J. Biomech. 47:277–280, 2014.CrossRefPubMedGoogle Scholar
  32. 32.
    Sigurdardottir, S., A. Eiriksdottir, E. Gunnarsdottir, M. Meintema, U. Arnadottir, and T. Vik. Cognitive profile in young Icelandic children with cerebral palsy. Dev. Med. Child Neurol. 50:357–362, 2008.CrossRefPubMedGoogle Scholar
  33. 33.
    Sloot, L. H., J. Harlaar, and M. M. van der Krogt. Self-paced versus fixed speed walking and the effect of virtual reality in children with cerebral palsy. Gait Posture 42:498–504, 2015.CrossRefPubMedGoogle Scholar
  34. 34.
    Sloot, L. H., M. M. van der Krogt, and J. Harlaar. Self-paced versus fixed speed treadmill walking. Gait Posture 39:478–484, 2014.CrossRefPubMedGoogle Scholar
  35. 35.
    Stadskleiv, K., R. Jahnsen, G. L. Andersen, and S. von Tetzchner. Neuropsychological profiles of children with cerebral palsy. Dev. Neurorehabil 2017.  https://doi.org/10.1080/17518423.2017.1282054.PubMedCrossRefGoogle Scholar
  36. 36.
    Turconi, A. C., E. Biffi, C. Maghini, E. Peri, F. Servodio Iammarone, and C. Gagliardi. Can new technologies improve upper limb performance in grown-up diplegic children? Eur. J. Phys. Rehabil. Med. 52:672–681, 2016.PubMedGoogle Scholar
  37. 37.
    van den Bogert, A. J., T. Geijtenbeek, O. Even-Zohar, F. Steenbrink, and E. C. Hardin. A real-time system for biomechanical analysis of human movement and muscle function. Med. Biol. Eng. Comput. 51:1069–1077, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    van der Krogt, M. M., L. H. Sloot, A. I. Buizer, and J. Harlaar. Kinetic comparison of walking on a treadmill versus over ground in children with cerebral palsy. J. Biomech. 48:3577–3583, 2015.CrossRefPubMedGoogle Scholar
  39. 39.
    van der Krogt, M. M., L. H. Sloot, and J. Harlaar. Overground versus self-paced treadmill walking in a virtual environment in children with cerebral palsy. Gait Posture 40:587–593, 2014.CrossRefPubMedGoogle Scholar
  40. 40.
    van Gelder, L., A. T. Booth, I. van de Port, A. I. Buizer, J. Harlaar, and M. M. van der Krogt. Real-time feedback to improve gait in children with cerebral palsy. Gait Posture 52:76–82, 2017.CrossRefPubMedGoogle Scholar
  41. 41.
    Wechsler, D. Wechsler Intelligence Scale for Children Revised. New York: Psychological Corporation, 1974.Google Scholar
  42. 42.
    Yu, Y., and T. A. Stoffregen. Postural and locomotor contributions to affordance perception. J. Mot. Behav. 44:305–311, 2012.CrossRefPubMedGoogle Scholar

Copyright information

© Biomedical Engineering Society 2018

Authors and Affiliations

  1. 1.Scientific Institute, IRCCS Eugenio MedeaBosisio PariniItaly

Personalised recommendations