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Adaptive Ankle Resistance from a Wearable Robotic Device to Improve Muscle Recruitment in Cerebral Palsy

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Abstract

Individuals with cerebral palsy can have weak and poorly coordinated ankle plantar flexor muscles that contribute to inefficient walking patterns. Previous studies attempting to improve plantar flexor function have had inconsistent effects on mobility, likely due to a lack of task-specificity. The goal of this study was to develop, validate, and test the feasibility and neuromuscular response of a novel wearable adaptive resistance platform to increase activity of the plantar flexors during the propulsive phase of gait. We recruited eight individuals with spastic cerebral palsy to walk with adaptive plantar flexor resistance provided from an untethered exoskeleton. The resistance system and protocol was safe and feasible for all of our participants. Controller validation demonstrated our ability to provide resistance that proportionally- and instantaneously-adapted to the biological ankle moment (R = 0.92 ± 0.04). Following acclimation to resistance (0.16 ± 0.02 Nm/kg), more-affected limbs exhibited a 45 ± 35% increase in plantar flexor activity (p = 0.02), a 26 ± 24% decrease in dorsiflexor activity (p < 0.05), and a 46 ± 25% decrease in co-contraction (tibialis anterior and soleus) (p = 0.02) during the stance phase. This adaptive resistance system warrants further investigation for use in a longitudinal intervention study.

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Abbreviations

CP:

Cerebral palsy

PT:

Physical therapy

GUI:

Graphical user interface

GMFCS:

Gross Motor Function Classification System

MVC:

Maximum voluntary contraction

EMG:

Electromyography

SOL:

Soleus

TA:

Tibialis anterior

R :

Correlation coefficient

d :

Cohen’s d

References

  1. Anttila, H., I. Autti-Rämö, J. Suoranta, M. Mäkelä, and A. Malmivaara. Effectiveness of physical therapy interventions for children with cerebral palsy: a systematic review. BMC Pediatr. 8:14, 2008.

    PubMed  PubMed Central  Google Scholar 

  2. Bastiaanse, C. M., J. Duysens, and V. Dietz. Modulation of cutaneous reflexes by load receptor input during human walking. Exp. Brain Res. 135:189–198, 2000.

    CAS  PubMed  Google Scholar 

  3. Bayón, C., S. Lerma, O. Ramírez, J. I. Serrano, M. D. Del Castillo, R. Raya, J. M. Belda-Lois, I. Martínez, and E. Rocon. Locomotor training through a novel robotic platform for gait rehabilitation in pediatric population: short report. J. Neuroeng. Rehabil. 13:98, 2016.

    PubMed  PubMed Central  Google Scholar 

  4. Borggraefe, I., J. S. Schaefer, M. Klaiber, E. Dabrowski, C. Ammann-Reiffer, B. Knecht, S. Berweck, F. Heinen, and A. Meyer-Heim. Robotic-assisted treadmill therapy improves walking and standing performance in children and adolescents with cerebral palsy. Eur. J. Paediatr. Neurol. 14:496–502, 2010.

    PubMed  Google Scholar 

  5. Brown, J. K., J. Rodda, E. G. Walsh, and G. W. Wright. Neurophysiology of lower-limb function in hemiplegic children. Dev. Med. Child Neurol. 33:1037–1047, 2008.

    Google Scholar 

  6. Burdea, G. C., D. Cioi, A. Kale, W. E. Janes, S. A. Ross, and J. R. Engsberg. Robotics and gaming to improve ankle strength, motor control, and function in children with cerebral palsy: a case study series. IEEE Trans. Neural Syst. Rehabil. Eng. 21:165–173, 2013.

    PubMed  Google Scholar 

  7. Clark, B. C., J. R. Pierce, T. M. Manini, and L. L. Ploutz-Snyder. Effect of prolonged unweighting of human skeletal muscle on neuromotor force control. Eur. J. Appl. Physiol. 100:53–62, 2007.

    PubMed  Google Scholar 

  8. Colborne, G. R., F. V. Wright, and S. Naumann. Feedback of triceps surae EMG in gait of children with cerebral palsy: a controlled study. Arch. Phys. Med. Rehabil. 75:40–45, 1994.

    CAS  PubMed  Google Scholar 

  9. Dallmeijer, A. J., R. Baker, K. J. Dodd, and N. F. Taylor. Association between isometric muscle strength and gait joint kinetics in adolescents and young adults with cerebral palsy. Gait Posture 33:326–332, 2011.

    CAS  PubMed  Google Scholar 

  10. Davids, J. R., D. J. Oeffinger, A. M. Bagley, M. Sison-Williamson, and G. Gorton. Relationship of Strength, Weight, Age, and Function in Ambulatory Children With Cerebral Palsy. J. Pediatr. Orthop. 35:523–529, 2015.

    PubMed  Google Scholar 

  11. de Mello Monteiro, C. B., T. Massetti, T. D. da Silva, J. van der Kamp, L. C. de Abreu, C. Leone, and G. J. P. Savelsbergh. Transfer of motor learning from virtual to natural environments in individuals with cerebral palsy. Res. Dev. Disabil. 35:2430–2437, 2014.

    PubMed  Google Scholar 

  12. Delp, S. L., F. C. Anderson, A. S. Arnold, P. Loan, A. Habib, C. T. John, E. Guendelman, and D. G. Thelen. OpenSim: open-source software to create and analyze dynamic simulations of movement. IEEE Trans. Biomed. Eng. 54:1940–1950, 2007.

    PubMed  Google Scholar 

  13. Drużbicki, 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 thearapy in children with cerebral palsy. J. Rehabil. Med. 45:358–363, 2013.

    PubMed  Google Scholar 

  14. Dursun, E., N. Dursun, and D. Alican. Effects of biofeedback treatment on gait in children with cerebral palsy. Disabil. Rehabil. 26:116–120, 2004.

    PubMed  Google Scholar 

  15. Eek, M. N., and E. Beckung. Walking ability is related to muscle strength in children with cerebral palsy. Gait Posture 28:366–371, 2008.

    PubMed  Google Scholar 

  16. Gage, J. R., and T. F. Novacheck. An update on the treatment of gait problems in cerebral palsy. J. Pediatr. Orthop. B 10:265–274, 2001.

    CAS  PubMed  Google Scholar 

  17. Gage, J. R., M. H. Schwartz, S. E. Koop, and T. F. Novacheck. The Identification and Treatment of Gait Problems in Cerebral Palsy. London: Mac Keith Press, 2009.

    Google Scholar 

  18. Gasparri, G. M., J. Luque, and Z. F. Lerner. Proportional joint-moment control for instantaneously adaptive ankle exoskeleton assistance. IEEE Trans. Neural Syst. Rehabil. Eng. 27:751–759, 2019.

    PubMed  Google Scholar 

  19. Ghasemi, A., and S. Zahediasl. Normality tests for statistical analysis: a guide for non-statisticians. Int. J. Endocrinol. Metab. 10:486–489, 2012.

    PubMed  PubMed Central  Google Scholar 

  20. Jezernik, S., G. Colombo, T. Keller, H. Frueh, and M. Morari. Robotic orthosis lokomat: a rehabilitation and research tool. Neuromodulation Technol. Neural Interface 6:108–115, 2003.

    Google Scholar 

  21. Kang, J., D. Martelli, V. Vashista, I. Martinez-Hernandez, H. Kim, and S. K. Agrawal. Robot-driven downward pelvic pull to improve crouch gait in children with cerebral palsy. Sci. Robot. 2:2634, 2017.

    Google Scholar 

  22. Lachenbruch, P. A., and J. Cohen. Statistical power analysis for the behavioral sciences. J. Am. Stat. Assoc. 1989. https://doi.org/10.2307/2290095.

    Article  Google Scholar 

  23. Leonard, C. T., H. Hirschfeld, and H. Forssberg. The development of independent walking in children with cerebral palsy. Dev. Med. Child Neurol. 33:567–577, 2008.

    Google Scholar 

  24. Leonard, C. T., T. Moritani, H. Hirschfeld, and H. Forssberg. Deficits in reciprocal inhibition of children with cerebral palsy as revealed by H reflex testing. Dev. Med. Child Neurol. 32:974–984, 2008.

    Google Scholar 

  25. Lerner, Z. F., M. S. DeMers, S. L. Delp, and R. C. Browning. How tibiofemoral alignment and contact locations affect predictions of medial and lateral tibiofemoral contact forces. J. Biomech. 48:644–650, 2015.

    PubMed  PubMed Central  Google Scholar 

  26. Lerner, Z. F., T. A. Harvey, and J. L. Lawson. a battery-powered ankle exoskeleton improves gait mechanics in a feasibility study of individuals with cerebral palsy. Ann. Biomed. Eng. 2019. https://doi.org/10.1007/s10439-019-02237-w.

    Article  PubMed  Google Scholar 

  27. Lotze, M., C. Braun, N. Birbaumer, S. Anders, and L. G. Cohen. Motor learning elicited by voluntary drive. Brain 126:866–872, 2003.

    PubMed  Google Scholar 

  28. McGowan, C. P., R. R. Neptune, D. J. Clark, and S. A. Kautz. Modular control of human walking: adaptations to altered mechanical demands. J. Biomech. 43:412–419, 2010.

    PubMed  Google Scholar 

  29. 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.

    CAS  PubMed  Google Scholar 

  30. Mukaka, M. M. Statistics corner: a guide to appropriate use of correlation coefficient in medical research. Malawi Med. J. 24:69–71, 2012.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Novak, I., S. Mcintyre, C. Morgan, L. Campbell, L. Dark, N. Morton, E. Stumbles, S.-A. Wilson, and S. Goldsmith. A systematic review of interventions for children with cerebral palsy: state of the evidence. Dev. Med. Child Neurol. 55:885–910, 2013.

    PubMed  Google Scholar 

  32. Olney, S. J., H. A. MacPhail, D. M. Hedden, and W. F. Boyce. Work and power in hemiplegic cerebral palsy gait. Phys. Ther. 70:431–438, 1990.

    CAS  PubMed  Google Scholar 

  33. Reid, L. B., S. E. Rose, and R. N. Boyd. Rehabilitation and neuroplasticity in children with unilateral cerebral palsy. Nat. Rev. Neurol. 11:390–400, 2015.

    PubMed  Google Scholar 

  34. Rose, J., J. G. Gamble, A. Burgos, J. Medeiros, and W. L. Haskell. Energy expenditure index of walking for normal children and for children with cerebral palsy. Dev. Med. Child Neurol. 32:333–340, 1990.

    CAS  PubMed  Google Scholar 

  35. Rossignol, S., R. Dubuc, and J.-P. Gossard. Dynamic sensorimotor interactions in locomotion. Physiol. Rev. 86:89–154, 2006.

    PubMed  Google Scholar 

  36. Schmidt, R. A., and T. D. Lee. Motor Control and Learning: A Behavioral Emphasis. Champaign: Human Kinetics, 2011.

    Google Scholar 

  37. Scholtes, V. A., J. G. Becher, A. Comuth, H. Dekkers, L. Van Dijk, and A. J. Dallmeijer. Effectiveness of functional progressive resistance exercise strength training on muscle strength and mobility in children with cerebral palsy: a randomized controlled trial. Dev. Med. Child Neurol. 52:e107–e113, 2010.

    PubMed  Google Scholar 

  38. Scholtes, V. A., J. G. Becher, Y. J. Janssen-Potten, H. Dekkers, L. Smallenbroek, and A. J. Dallmeijer. Effectiveness of functional progressive resistance exercise training on walking ability in children with cerebral palsy: a randomized controlled trial. Res. Dev. Disabil. 33:181–188, 2012.

    PubMed  Google Scholar 

  39. Schroeder, A. S., M. Homburg, B. Warken, H. Auffermann, I. Koerte, S. Berweck, K. Jahn, F. Heinen, and I. Borggraefe. 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. 18:502–510, 2014.

    CAS  PubMed  Google Scholar 

  40. Sutherland, D. H., L. Cooper, and D. Daniel. The role of the ankle plantar flexors in normal walking. J. Bone Joint Surg. Am. 62:354–363, 1980.

    CAS  PubMed  Google Scholar 

  41. Taylor, N. F., K. J. Dodd, R. J. Baker, K. Willoughby, P. Thomason, and H. K. Graham. Progressive resistance training and mobility-related function in young people with cerebral palsy: a randomized controlled trial. Dev. Med. Child Neurol. 55:806–812, 2013.

    PubMed  Google Scholar 

  42. Unnithan, V. B., J. J. Dowling, G. Frost, and O. Bar-Or. Role of cocontraction in the O2 cost of walking in children with cerebral palsy. Med. Sci. Sports Exerc. 28:1498–1504, 1996.

    CAS  PubMed  Google Scholar 

  43. Verschuren, O., L. Ada, D. B. Maltais, J. W. Gorter, A. Scianni, and M. Ketelaar. Muscle strengthening in children and adolescents with spastic cerebral palsy: considerations for future resistance training protocols. Phys. Ther. 91:1130–1139, 2011.

    PubMed  Google Scholar 

  44. Wiley, M. E., and D. L. Damiano. Lower-extremity strength profiles in spastic cerebral palsy. Dev. Med. Child Neurol. 40:100–107, 1998.

    CAS  PubMed  Google Scholar 

  45. Winstein, C., R. Lewthwaite, S. R. Blanton, L. B. Wolf, and L. Wishart. Infusing motor learning research into neurorehabilitation practice: a historical perspective with case exemplar from the accelerated skill acquisition program. J. Neurol. Phys. Ther. 38:190–200, 2014.

    PubMed  PubMed Central  Google Scholar 

  46. Winters, T. F., J. R. Gage, and R. Hicks. Gait patterns in spastic hemiplegia in children and young adults. J. Bone Joint Surg. Am. 69:437–441, 1987.

    PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Nushka Remec, P.T., Emily Frank, R.N., Elizabeth Orum, and Jennifer Lawson for their assistance with data collection and processing. Research reported in this publication was supported in part by the Eunice Kennedy Shriver National Institute Of Child Health & Human Development of the National Institutes of Health under Award Number R03HD094583. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. This work was also supported in part by The University of Arizona College of Medicine – Phoenix MD/PhD Program.

Conflicts of interest

ZFL is a named inventor on a pending utility patent application that describes the exoskeleton utilized in the study. ZFL is a co-founder of a company seeking to commercialize the device.

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Correspondence to Zachary F. Lerner.

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Associate Editor Eric M. Darling oversaw the review of this article.

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Conner, B.C., Luque, J. & Lerner, Z.F. Adaptive Ankle Resistance from a Wearable Robotic Device to Improve Muscle Recruitment in Cerebral Palsy. Ann Biomed Eng 48, 1309–1321 (2020). https://doi.org/10.1007/s10439-020-02454-8

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