Ann Rehabil Med.  2019 Aug;43(4):445-457. 10.5535/arm.2019.43.4.445.

Effects of Combined Upper Limb Robotic Therapy in Patients With Tetraplegic Spinal Cord Injury

• Jung JH
• Lee HJ
• Cho DY
• Lim JE
• Lee BS
• Kwon SH
• Kim HY
• Lee SJ

• KMID: 2457753
• DOI: http://doi.org/10.5535/arm.2019.43.4.445

Abstract

OBJECTIVE
To confirm the effects of combined upper limb robotic therapy (RT) as compared to conventional occupational therapy (OT) in tetraplegic spinal cord injury (SCI) patients and to suggest the optimized treatment guidelines of combined upper limb RT.
METHODS
After subject recruitment and screening for eligibility, the baseline evaluation for outcome measures were performed. We evaluated the Graded and Redefined Assessment of Strength, Sensibility, and Prehension (GRASSP), the American Spinal Injury Association upper extremity motor score, grip and pinch strength, and the Spinal Cord Independence Measurement III (SCIM-III). In this study, the pre-tested participants were divided randomly into the RT and OT group. The utilized interventions included combined upper limb RT using ArmeoPower and Amadeo (RT group), or conventional OT (OT group) in addition to daily inpatient rehabilitation program. The participants underwent 40 minutes×3 sessions×5 weeks of interventions.
RESULTS
A total of 30 tetraplegic SCI patients completed entire study program. After 5 weeks of intervention, both groups demonstrated increases in GRASSP-strength and SCIM-III. The manual muscle test scores of elbow flexion, elbow extension, 2-5th metacarpophalangeal extension, and SCIM-III subscores of bathing-upper, dressing-upper, and grooming as well as the GRASSP-qualitative prehension score were noted to have been significantly increased in the RT group as evaluated. The OT group showed improvements in the GRASSP-quantitative prehension score and some items in grip and pinch strength. There was no significant difference between the two groups in almost all measurements except for the SCIM-III bathing-upper subscore.
CONCLUSION
Combined upper limb RT demonstrated beneficial effects on the upper limb motor function in patients with tetraplegic SCI, which were comparable with conventional OT.

Keyword

Spinal cord injuries; Upper extremity; Robotics; Rehabilitation

MeSH Terms

Animals
Elbow
Grooming
Hand Strength
Humans
Inpatients
Mass Screening
Occupational Therapy
Outcome Assessment (Health Care)
Pinch Strength
Rehabilitation
Robotics
Spinal Cord Injuries*
Spinal Cord*
Spinal Injuries
Upper Extremity*

Figure

• 

  Fig. 1. (A) ArmeoPower, a rehabilitation exoskeleton that mainly trains proximal upper limb including shoulder, elbow, and wrist. (B) The patient training proximal upper limb with ArmeoPower.

• 

  Fig. 2. (A) Amadeo, a rehabilitation exoskeleton that trains distal upper limb including hand and fingers. (B) The patient training distal upper limb with Amadeo.

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  Fig. 3. Flow chart of subject recruitment. RT, combining upper limb robotic therapy with conventional occupational therapy; OT, only conventional occupational therapy.

Reference

1. Kang Y, Ding H, Zhou H, Wei Z, Liu L, Pan D, et al. Epidemiology of worldwide spinal cord injury: a literature review. J Neurorestoratol. 2017; 6:1–9.

2. Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2004; 21:1371–83.

3. Snoek GJ, IJzerman MJ, Post MW, Stiggelbout AM, Roach MJ, Zilvold G. Choice-based evaluation for the improvement of upper-extremity function compared with other impairments in tetraplegia. Arch Phys Med Rehabil. 2005; 86:1623–30.

4. Foy T, Perritt G, Thimmaiah D, Heisler L, Offutt JL, Cantoni K, et al. The SCIRehab project : treatment time spent in SCI rehabilitation: occupational therapy treatment time during inpatient spinal cord injury rehabilitation. J Spinal Cord Med. 2011; 34:162–75.

5. Ozelie R, Gassaway J, Buchman E, Thimmaiah D, Heisler L, Cantoni K, et al. Relationship of occupational therapy inpatient rehabilitation interventions and patient characteristics to outcomes following spinal cord injury: the SCIRehab project. J Spinal Cord Med. 2012; 35:527–46.

6. Behrman AL, Bowden MG, Nair PM. Neuroplasticity after spinal cord injury and training: an emerging paradigm shift in rehabilitation and walking recovery. Phys Ther. 2006; 86:1406–25.

7. Cano-de-la-Cuerda R, Molero-Sanchez A, Carratala-Tejada M, Alguacil-Diego IM, Molina-Rueda F, Miangolarra-Page JC, et al. Theories and control models and motor learning: clinical applications in neurorehabilitation. Neurologia. 2015; 30:32–41.

8. Lynskey JV, Belanger A, Jung R. Activity-dependent plasticity in spinal cord injury. J Rehabil Res Dev. 2008; 45:229–40.

9. Onifer SM, Smith GM, Fouad K. Plasticity after spinal cord injury: relevance to recovery and approaches to facilitate it. Neurotherapeutics. 2011; 8:283–93.

10. Quel de Oliveira C, Refshauge K, Middleton J, de Jong L, Davis GM. Effects of activity-based therapy interventions on mobility, independence, and quality of life for people with spinal cord injuries: a systematic review and meta-analysis. J Neurotrauma. 2017; 34:1726–43.

11. Francisco GE, Yozbatiran N, Berliner J, O’Malley MK, Pehlivan AU, Kadivar Z, et al. Robot-assisted training of arm and hand movement shows functional improvements for incomplete cervical spinal cord injury. Am J Phys Med Rehabil. 2017; 96(10 Suppl 1):S171–S177.

12. Godfrey SB, Holley RJ, Lum PS. Clinical effects of using HEXORR (Hand Exoskeleton Rehabilitation Robot) for movement therapy in stroke rehabilitation. Am J Phys Med Rehabil. 2013; 92:947–58.

13. Sale P, Mazzoleni S, Lombardi V, Galafate D, Massimiani MP, Posteraro F, et al. Recovery of hand function with robot-assisted therapy in acute stroke patients: a randomized-controlled trial. Int J Rehabil Res. 2014; 37:236–42.

14. Takahashi K, Domen K, Sakamoto T, Toshima M, Otaka Y, Seto M, et al. Efficacy of upper extremity robotic therapy in subacute poststroke hemiplegia: an exploratory randomized trial. Stroke. 2016; 47:1385–8.

15. Klamroth-Marganska V, Blanco J, Campen K, Curt A, Dietz V, Ettlin T, et al. Three-dimensional, task-specific robot therapy of the arm after stroke: a multicentre, parallel-group randomised trial. Lancet Neurol. 2014; 13:159–66.

16. Zariffa J, Kapadia N, Kramer JL, Taylor P, Alizadeh-Meghrazi M, Zivanovic V, et al. Feasibility and efficacy of upper limb robotic rehabilitation in a subacute cervical spinal cord injury population. Spinal Cord. 2012; 50:220–6.

17. Cortes M, Elder J, Rykman A, Murray L, Avedissian M, Stampas A, et al. Improved motor performance in chronic spinal cord injury following upper-limb robotic training. NeuroRehabilitation. 2013; 33:57–65.

18. Fitle KD, Pehlivan AU, O’Malley MK. A robotic exoskeleton for rehabilitation and assessment of the upper limb following incomplete spinal cord injury. In : Proceedings of 2015 IEEE International Conference on Robotics and Automation (ICRA); 2015 May 26-30; Seattle, WA. p. 4960–6.

19. Kadivar Z, Sullivan JL, Eng DP, Pehlivan AU, O’Malley MK, Yozbatiran N, et al. Robotic training and kinematic analysis of arm and hand after incomplete spinal cord injury: a case study. IEEE Int Conf Rehabil Robot. 2011; 2011:5975429.

20. Zariffa J, Kapadia N, Kramer JL, Taylor P, Alizadeh-Meghrazi M, Zivanovic V, et al. Relationship between clinical assessments of function and measurements from an upper-limb robotic rehabilitation device in cervical spinal cord injury. IEEE Trans Neural Syst Rehabil Eng. 2012; 20:341–50.

21. Zariffa J, Kapadia N, Kramer JL, Taylor P, Alizadeh-Meghrazi M, Zivanovic V, et al. Effect of a robotic rehabilitation device on upper limb function in a subacute cervical spinal cord injury population. IEEE Int Conf Rehabil Robot. 2011; 2011:5975400.

22. Kalsi-Ryan S, Beaton D, Curt A, Duff S, Popovic MR, Rudhe C, et al. The Graded Redefined Assessment of Strength Sensibility and Prehension: reliability and validity. J Neurotrauma. 2012; 29:905–14.

23. Kalsi-Ryan S, Beaton D, Ahn H, Askes H, Drew B, Curt A, et al. Responsiveness, sensitivity, and minimally detectable difference of the Graded and Redefined Assessment of Strength, Sensibility, and Prehension, Version 1.0. J Neurotrauma. 2016; 33:307–14.

24. Frullo JM, Elinger J, Pehlivan AU, Fitle K, Nedley K, Francisco GE, et al. Effects of assist-as-needed upper extremity robotic therapy after incomplete spinal cord injury: a parallel-group controlled trial. Front Neurorobot. 2017; 11:26.

25. Lu Z, Tong KY, Shin H, Stampas A, Zhou P. Robotic hand-assisted training for spinal cord injury driven by myoelectric pattern recognition: a case report. Am J Phys Med Rehabil. 2017; 96(10 Suppl 1):S146–S149.

26. Steeves JD, Lammertse DP, Kramer JL, Kleitman N, Kalsi-Ryan S, Jones L, et al. Outcome measures for acute/subacute cervical sensorimotor complete (AISA) spinal cord injury during a phase 2 clinical trial. Top Spinal Cord Inj Rehabil. 2012; 18:1–14.

27. Zariffa J, Curt A, Verrier MC, Fehlings MG, Kalsi-Ryan S; GRASSP Cross-Sectional Study Team and Ontario GRASSP Longitudinal Study Team. Predicting task performance from upper extremity impairment measures after cervical spinal cord injury. Spinal Cord. 2016; 54:1145–51.

28. Steeves JD, Lammertse D, Curt A, Fawcett JW, Tuszynski MH, Ditunno JF, et al. Guidelines for the conduct of clinical trials for spinal cord injury (SCI) as developed by the ICCP panel: clinical trial outcome measures. Spinal Cord. 2007; 45:206–21.

29. Anderson K, Aito S, Atkins M, Biering-Sorensen F, Charlifue S, Curt A, et al. Functional recovery measures for spinal cord injury: an evidence-based review for clinical practice and research. J Spinal Cord Med. 2008; 31:133–44.

30. Itzkovich M, Gelernter I, Biering-Sorensen F, Weeks C, Laramee MT, Craven BC, et al. The Spinal Cord Independence Measure (SCIM) version III: reliability and validity in a multi-center international study. Disabil Rehabil. 2007; 29:1926–33.

31. Lu X, Battistuzzo CR, Zoghi M, Galea MP. Effects of training on upper limb function after cervical spinal cord injury: a systematic review. Clin Rehabil. 2015; 29:3–13.

32. Kloosterman MG, Snoek GJ, Jannink MJ. Systematic review of the effects of exercise therapy on the upper extremity of patients with spinal-cord injury. Spinal Cord. 2009; 47:196–203.

33. Dunn JA, Sinnott KA, Rothwell AG, Mohammed KD, Simcock JW. Tendon transfer surgery for people with tetraplegia: an overview. Arch Phys Med Rehabil. 2016; 97(6 Suppl):S75–80.

34. Fox IK, Novak CB, Krauss EM, Hoben GM, Zaidman CM, Ruvinskaya R, et al. The use of nerve transfers to restore upper extremity function in cervical spinal cord injury. PM R. 2018; 10:1173–1184. e2.

35. Choi H, Seo KC, Kim TU, Lee SJ, Hyun JK. Repetitive transcranial magnetic stimulation enhances recovery in central cord syndrome patients. Ann Rehabil Med. 2019; 43:62–73.

36. Lum PS, Burgar CG, Shor PC, Majmundar M, Van der Loos M. Robot-assisted movement training compared with conventional therapy techniques for the rehabilitation of upper-limb motor function after stroke. Arch Phys Med Rehabil. 2002; 83:952–9.

37. Lee KW, Kim SB, Lee JH, Lee SJ, Kim JW. Effect of robot-assisted game training on upper extremity function in stroke patients. Ann Rehabil Med. 2017; 41:539–46.

38. Hesse S, Heß A, Werner C C, Kabbert N, Buschfort R. Effect on arm function and cost of robot-assisted group therapy in subacute patients with stroke and a moderately to severely affected arm: a randomized controlled trial. Clin Rehabil. 2014; 28:637–47.

39. Orihuela-Espina F, Roldan GF, Sanchez-Villavicencio I, Palafox L, Leder R, Sucar LE, et al. Robot training for hand motor recovery in subacute stroke patients: a randomized controlled trial. J Hand Ther. 2016; 29:51–7.

40. Beekhuizen KS, Field-Fote EC. Massed practice versus massed practice with stimulation: effects on upper extremity function and cortical plasticity in individuals with incomplete cervical spinal cord injury. Neurorehabil Neural Repair. 2005; 19:33–45.