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Improving motor performance in Parkinson’s disease: a preliminary study on the promising use of the computer assisted virtual reality environment (CAREN)

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Abstract

Background

Parkinson’s disease (PD) is a neurodegenerative disorder characterized by various motor symptoms including balance and gait impairment. Several studies have shown that physiotherapy, cueing techniques, treadmill training, and cognitive movement strategies are useful in improving balance and gait in patients with PD. Devices employing virtual reality (VR) have been shown to be promising in neurorehabilitation as they can provide the patients with multisensory stimulation creating a realistic environment and improve the motivation and the adhesion of patients to the rehabilitation program. This preliminary study is aimed at testing the efficacy and feasibility of gait training based on the computer-assisted virtual reality environment (CAREN) in a sample of PD.

Methods

In this preliminary study, 22 outpatients affected by PD who attended the Behavioral and Robotic Neurorehab Laboratory of the IRCCS Neurolesi between August 2017 and October 2018 were enrolled. All PD patients underwent 20 conventional physiotherapy sessions followed by 3-month of rest. Then, the patients were provided with 20 sessions of CAREN training. Gait and balance performances were rated before, after each training protocol, and 3 months later. Gait analysis was also performed before and after CAREN training.

Results

All patients completed both of the rehabilitation trainings without any adverse event. All considered scales improved significantly at the end of both rehabilitation treatments. However, patients presented with a greater clinical improvement after the CAREN training, compared with conventional physiotherapy. In particular, patients walked faster and with more stability, with wider, longer steps.

Conclusions

Even though further neurophysiological details are required to identify the patients who may benefit from CAREN training, our findings suggest that this innovative device is an effective and feasible tool to train balance and gait in patients with PD.

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References

  1. Shulman LM (2010) Understanding disability in Parkinson's disease. Mov Disord 25(Suppl 1):S131–S135

    Article  Google Scholar 

  2. McNeely ME, Duncan RP, Earhart GM (2012) Medication improves balance and complex gait performance in Parkinson disease. Gait Posture 36(1):144–148

    Article  Google Scholar 

  3. Burleigh-Jacobs A, Horak FB, Nutt JG, Obeso JA (1997) Step initiation in Parkinson's disease: influence of levodopa and external sensory triggers. Mov Disord 12(2):206–215

    Article  CAS  Google Scholar 

  4. Wood BH, Bilclough JA, Bowron A, Walker RW (2002) Incidence and prediction of falls in Parkinson's disease: a prospective multidisciplinary study. J Neurol Neurosurg Psychiatry 72(6):721–725

    Article  CAS  Google Scholar 

  5. Bloem BR, Hausdorff JM, Visser JE, Giladi N (2004) Falls and freezing of gait in Parkinson's disease: a review of two interconnected, episodic phenomena. Mov Disord 19(8):871–884

    Article  Google Scholar 

  6. Bonnet AM, Loria Y, Saint-Hilaire MH, Lhermitte F, Agid Y (1987) Does long-term aggravation of Parkinson's disease result from nondopaminergic lesions? Neurology. 37(9):1539–1542

    Article  CAS  Google Scholar 

  7. Frazzitta G, Bertotti G, Uccellini D, Boveri N, Rovescala R, Pezzoli G, Maestri R (2013) Short- and long-term efficacy of intensive rehabilitation treatment on balance and gait in parkinsonian patients: a preliminary study with a 1-year followup. Parkinsons Dis. 2013:583278

    PubMed  PubMed Central  Google Scholar 

  8. Frazzitta G, Maestri R, Uccellini D, Bertotti G, Abelli P (2009) Rehabilitation treatment of gait in patients with Parkinson's disease with freezing: a comparison between two physical therapy protocols using visual and auditory cues with or without treadmill training. Mov Disord 24(8):1139–1143

    Article  Google Scholar 

  9. Frazzitta G, Maestri R, Bertotti G, Riboldazzi G, Boveri N, Perini M, Uccellini D, Turla M, Comi C, Pezzoli G, Ghilardi MF (2015) Intensive rehabilitation treatment in early Parkinson's disease: a randomized pilot study with a 2-year follow-up. Neurorehabil Neural Repair 29(2):123–131

    Article  Google Scholar 

  10. Papagno C, Trojano L (2018) Cognitive and behavioral disorders in Parkinson's disease: an update. I: cognitive impairments. Neurol Sci 39(2):215–223

    Article  Google Scholar 

  11. Tachibana H (2013) Cognitive impairment in Parkinson's disease. Seishin Shinkeigaku Zasshi 115(11):1142–1149

    PubMed  Google Scholar 

  12. Maggio MG, Russo M, Cuzzola MF, Destro M, La Rosa G, Molonia F, Bramanti P, Lombardo G, De Luca R, Calabrò RS (2019) Virtual reality in multiple sclerosis rehabilitation: A review on cognitive and motor outcomes. J Clin Neurosci pii:S0967–5868(19)30185–7

  13. Maggio MG, Maresca G, Scarcella I, Latella D, De Domenico C, Destro M, De Luca R, Calabro RS (2019) Virtual reality-based cognitive rehabilitation in progressive supranuclear palsy. Psychogeriatrics. https://doi.org/10.1111/psyg.12431

  14. De Luca R, Portaro S, Le Cause M, De Domenico C, Maggio MG, Cristina Ferrera M, Giuffrè G, Bramanti A, Calabrò RS (2019) Cognitive rehabilitation using immersive virtual reality at young age: a case report on traumatic brain injury. Appl Neuropsychol Child 6:1–6

    Google Scholar 

  15. Albiol-Pérez S, Gil-Gómez JA, Muñoz-Tomás MT, Gil-Gómez H et al (2017) The effect of balance training on postural control in patients with Parkinson's disease using a virtual rehabilitation system. Methods Inf Med 56(2):138–144

    Article  Google Scholar 

  16. Laver KE, George S, Thomas S, Deutsch JE, Crotty M (2015) Virtual reality for stroke rehabilitation. Cochrane Database Syst Rev 12:CD008349

    Google Scholar 

  17. Kalron A, Fonkatz I, Frid L, Baransi H, Achiron A (2016) The effect of balance training on postural control in people with multiple sclerosis using the CAREN virtual reality system: a pilot randomized controlled trial. J Neuroeng Rehabil 13:13

    Article  Google Scholar 

  18. Sessoms PH, Gottshall KR, Collins JD, Markham AE, Service KA, Reini SA (2015) Improvements in gait speed and weight shift of persons with traumatic brain injury and vestibular dysfunction using a virtual reality computer-assisted rehabilitation environment. Mil Med 180(3 Suppl):143–149

    Article  Google Scholar 

  19. Freitag F, Brucki SMD, Barbosa AF, Chen J, Souza CO, Valente DF, Chien HF, Bedeschi C, Voos MC (2019) Is virtual reality beneficial for dual-task gait training in patients with Parkinson's disease? A systematic review. Dement Neuropsychol 13(3):259–267

    Article  Google Scholar 

  20. Cano Porras D, Sharon H, Inzelberg R, Ziv-Ner Y, Zeilig G, Plotnik M (2019) Advanced virtual reality-based rehabilitation of balance and gait in clinical practice. Ther Adv Chronic Dis 10:2040622319868379

    Article  Google Scholar 

  21. Mehrholz J, Kugler J, Storch A, Pohl M, Elsner B, Hirsch K (2015) Treadmill training for patients with Parkinson's disease. Cochrane Database Syst Rev 8:CD007830

    Google Scholar 

  22. Maggio MG, Maresca G, De Luca R, Stagnitti MC, Porcari B, Ferrera MC, Galletti F, Casella C, Manuli A, Calabrò RS (2019) The growing use of virtual reality in cognitive rehabilitation: fact, fake or vision? A Scoping Review. J Natl Med Assoc pii: S0027–9684(18)30346–8

  23. Santos P, Machado T, Santos L, Ribeiro N, Melo A (2019) Efficacy of the Nintendo Wii combination with conventional exercises in the rehabilitation of individuals with Parkinson's disease: a randomized clinical trial. NeuroRehabilitation. https://doi.org/10.3233/NRE-192771

  24. Kastavelis D, Mukherjee M, Decker LM, Stergiou N (2010) The effect of virtual reality on gait variability. Biomech Res Build 14(3):239–256

    Google Scholar 

  25. Zimmerli L, Duschau-Wicke A, Riener R, Mayr A, Lünenburger L (2009) Virtual reality and gait rehabilitation augmented feedback for the Lokomat. Virtual Rehabilitation International Conference:150–153

  26. Doniger GM, Beeri MS, Bahar-Fuchs A et al (2018) Virtual reality-based cognitive-motor training for middle-aged adults at high Alzheimer's disease risk: a randomized controlled trial. Alzheimers Dement (NY) 4:118–129

    Google Scholar 

  27. Cheung KL, Tunik E, Adamovich SV, Boyd LA (2014) Neuroplasticity and virtual reality. In: Keshner E, Levin M (eds) Weiss P. Virtual reality for physical and motor rehabilitation. Virtual Reality Technologies for Health and Clinical Applications, Springer, New York, NY, pp 5–24

    Google Scholar 

  28. Nieuwboer A, Kwakkel G, Rochester L et al (2007) Cueing training in the home improves gait-related mobility in Parkinson's disease: the RESCUE trial. J Neurol Neurosurg Psychiatry 78:134–140

    Article  CAS  Google Scholar 

  29. Siegert RJ, Taylor KD, Weatherall M, Abernethy DA (2006) Is implicit sequence learning impaired in Parkinson's disease? A meta-analysis. Neuropsychology 20:490–495

    Article  Google Scholar 

  30. Vakil E, Kahan S, Huberman M, Osimani A (2000) Motor and non-motor sequence learning in patients with basal ganglia lesions: the case of serial reaction time (SRT). Neuropsychologia 38:1–10

    Article  CAS  Google Scholar 

  31. Calabrò RS, Naro A, Filoni S, Pullia M, Billeri L, Tomasello P, Portaro S, Di Lorenzo G, Tomaino C, Bramanti P (2019) Walking to your right music: a randomized controlled trial on the novel use of treadmill plus music in Parkinson's disease. J Neuroeng Rehabil. 16(1):68

    Article  Google Scholar 

  32. Allen NE, Schwarzel AK, Canning CG (2013) Recurrent falls in Parkinson's disease: a systematic review. Parkinsons Dis 2013:906274

    PubMed  PubMed Central  Google Scholar 

  33. Bloem BR, Grimbergen YA, Cramer M, Willemsen M, Zwinderman AH (2001) Prospective assessment of falls in Parkinson’s disease. J Neurol 248:950–958

    Article  CAS  Google Scholar 

  34. Stolze H, Klebe S, Zechlin C, Baecker C, Friege L, Deuschl G (2004) Falls in frequent neurological diseases--prevalence, risk factors and aetiology. J Neurol 251(1):79–84

    Article  Google Scholar 

  35. Rahman S, Griffin HJ, Quinn NP, Jahanshahi M (2008) Quality of life in Parkinson's disease: the relative importance of the symptoms. Mov Disord 23(10):1428–1434

    Article  Google Scholar 

  36. Koay L, Rose J, Abdelhafiz AH (2018) Factors that lead to hospitalisation in patients with Parkinson disease-a systematic review. Int J Clin Pract 72(1)

  37. Karadsheh MS, Rodriguez EK, Harris MB, Zurakowski D, Lucas R, Weaver MJ (2015) Mortality and revision surgery are increased in patients with Parkinson's disease and fractures of the femoral neck. Clin Orthop Relat Res 473(10):3272–3279

    Article  Google Scholar 

  38. Calabrò RS, De Cola MC, Leo A, Reitano S, Balletta T, Trombetta G, Naro A, Russo M, Bertè F, De Luca R, Bramanti P (2015) Robotic neurorehabilitation in patients with chronic stroke: psychological well-being beyond motor improvement. Int J Rehabil Res 38(3):219–225

    Article  Google Scholar 

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Authors and Affiliations

  1. IRCCS Centro Neurolesi Bonino Pulejo, via Palermo, S.S. 113, C.da Casazza, 98124, Messina, Italy

    Rocco Salvatore Calabrò, Antonino Naro, Vincenzo Cimino, Antonio Buda, Giuseppe Paladina, Giuseppe Di Lorenzo, Alfredo Manuli, Demetrio Milardi, Placido Bramanti & Alessia Bramanti

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  1. Rocco Salvatore Calabrò
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  2. Antonino Naro
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  3. Vincenzo Cimino
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  4. Antonio Buda
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  5. Giuseppe Paladina
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  6. Giuseppe Di Lorenzo
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  7. Alfredo Manuli
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  10. Alessia Bramanti
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Correspondence to Rocco Salvatore Calabrò.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The local Ethics Committee of the IRCCS Centro Neurolesi Bonino Pulejo (Messina, Italy) approved the study.

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Calabrò, R.S., Naro, A., Cimino, V. et al. Improving motor performance in Parkinson’s disease: a preliminary study on the promising use of the computer assisted virtual reality environment (CAREN). Neurol Sci 41, 933–941 (2020). https://doi.org/10.1007/s10072-019-04194-7

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