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Parkinson’s disease and virtual reality rehabilitation: cognitive reserve influences the walking and balance outcome

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Abstract

Introduction

Parkinson’s disease (PD) is a neurodegenerative pathology characterized by motor and non-motor symptoms that often lead to several impairments. Many studies show the efficacy of different rehabilitation protocols aimed to improve balance and gait functions in PD patients. However, multiple factors may influence rehabilitation outcome. Recently, it has been observed as the cognitive reserve (CR) may influence the rehabilitation outcome, helping to address the patient toward technological or conventional rehabilitation. Our study investigated how CR may affect motor rehabilitation outcomes in PD patients who undergo virtual reality (VR) rehabilitation, aimed at improving walking and balance.

Materials and methods

Thirty patients affected by idiopathic PD were enrolled. Patients underwent 12 sessions VR training, over 6 weeks (45 min). Six-Minute Walk Test (6MWT) and Berg Balance Scale (BBS) were used to assess walking and balance, respectively. CR was assessed by Cognitive Reserve Index questionnaire (CRIq).

Results

Significant correlations between CR and change from baseline in walking and balance measures were found, with a significant positive correlation between CRIq and 6MWT (r=0.50, p=0.01) and between CRIq and BBS (r=0.41, p=0.04).

Discussion

Our results showed that PD patients with higher CR treated with VR improved significantly more in their balance and walking distance than those with lower CR. The current study suggests that VR when aimed to improve balance and walking in PD patients is more effective in patients with higher CR.

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References

  1. Mak MK, Wong-Yu IS, Shen X, Chung CL (2017) Long-term effects of exercise and physical therapy in people with Parkinson disease. Nat Rev Neurol 13:689–703

    Article  Google Scholar 

  2. Shen X, Wong-Yu IS, Mak MK (2016) Effects of exercise on falls, balance, and gait ability in Parkinson’s disease: a meta-analysis. Neurorehabil Neural Repair 30:512–527

    Article  Google Scholar 

  3. Collomb-Clerc A, Welter ML (2015) Effects of deep brain stimulation on balance and gait in patients with Parkinson’s disease: a systematic neurophysiological review. Neurophysiol Clin 45:371–388

    Article  CAS  Google Scholar 

  4. Hackney ME, Earhart GM (2009) Health-related quality of life and alternative forms of exercise in Parkinson disease. Parkinsonism Relat Disord 15:644–648

    Article  Google Scholar 

  5. Vetrano DL, Villani ER, Grande G, Giovannini S, Cipriani MC, Manes-Gravina E, Bernabei R, onder G (2018) Association of polypharmacy with 1-year trajectories of cognitive and physical function in nursing home residents: results from a multicenter European Study. J Am Med Dir Assoc 19:710–713

    Article  Google Scholar 

  6. Giovannini S, van der Roest HGHG, Carfì A et al (2018) Polypharmacy in home care in Europe: cross-sectional data from the IBenC study. Drugs Aging 35:145–152

    Article  Google Scholar 

  7. Tomlinson CL, Patel S, Meek C et al (2012) Physiotherapy versus placebo or no intervention in Parkinson’s disease. Cochrane Database Syst Rev 11:CD002817

    Google Scholar 

  8. Ahlskog JE (2011) Does vigorous exercise have a neuroprotective effect in Parkinson disease? Neurology 77:288–294

    Article  Google Scholar 

  9. Kurt EE, Büyükturan B, Büyükturan Ö, Erdem HR, Tuncay F (2018) Effects of Ai Chi on balance, quality of life, functional mobility, and motor impairment in patients with Parkinson’s disease. Disabil Rehabil 40:791–797

    Article  Google Scholar 

  10. Sturkenboom IH, Nijhuis-van der Sanden MW, Graff MJ (2016) A process evaluation of a home-based occupational therapy intervention for Parkinson’s patients and their caregivers performed alongside a randomized controlled trial. Clin Rehabil 30:1186–1199

    Article  Google Scholar 

  11. Song R, Grabowska W, Park M, Osypiuk K, Vergara-Diaz GP, Bonato P, Hausdorff JM, Fox M, Sudarsky LR, Macklin E, Wayne PM (2017) The impact of Tai Chi and Qigong mind-body exercises on motor and non-motor function and quality of life in Parkinson’s disease: a systematic review and meta-analysis. Parkinsonism Relat Disord 41:3–13

    Article  CAS  Google Scholar 

  12. Wang B, Shen M, Wang YX, He ZW, Chi SQ, Yang ZH (2019) Effect of virtual reality on balance and gait ability in patients with Parkinson’s disease: a systematic review and meta-analysis. Clin Rehabil 33:1130–1138. https://doi.org/10.1177/0269215519843174

    Article  PubMed  Google Scholar 

  13. Lina C, Guoen C, Huidan W, Yingqing W, Ying C, Xiaochun C, Qinyong Y (2020) The effect of virtual reality on the ability to perform activities of daily living, balance during gait and motor function in Parkinson’s disease patients-- a systematic review and meta-analysis. Am J Phys Med Rehabil 99:917–924. https://doi.org/10.1097/PHM.0000000000001447

    Article  PubMed  Google Scholar 

  14. Pazzaglia C, Imbimbo I, Tranchita E, Minganti C, Ricciardi D, Lo Monaco R, Parisi A, Padua L (2020) Comparison of virtual reality rehabilitation and conventional rehabilitation in Parkinson’s disease: a randomised controlled trial. Physiother (United Kingdom) 106:36–42. https://doi.org/10.1016/j.physio.2019.12.007

    Article  CAS  Google Scholar 

  15. Vetrano DL, Collamati A, Magnavita N, Sowa A, Topinkova E, Finne-Soveri H, van der Roest HG, Tobiasz-Adamczyk B, Giovannini S, Ricciardi W, Bernabei R, onder G, Poscia A (2018) Health determinants and survival in nursing home residents in Europe: results from the SHELTER study. Maturitas 107:19–25

    Article  Google Scholar 

  16. Fortune DG, Walsh RS, Richards HL (2016) Cognitive reserve and preinjury educational attainment: effects on outcome of community-based rehabilitation for longer-term individuals with acquired brain injury. Int J Rehabil Res 39:234–239

    Article  Google Scholar 

  17. Stern Y (2009) Cognitive reserve. Neuropsychologia 7:2015–2028

    Article  Google Scholar 

  18. Stern Y (2002) What is cognitive reserve? Theory of research application of the reserve concept. J Int Neuropsychol Soc 8:448–460

    Article  Google Scholar 

  19. Koerts J, Tucha L, Lange KW, Tucha O (2013) The influence of cognitive reserve on cognition in Parkinson’s disease. J Neural Transm 120:593–596

    Article  Google Scholar 

  20. Perneczky R, Drzezga A, Boecker H, Ceballos-Baumann AO, Granert O, Förstl H, Kurz A, Häussermann P (2008) Activities of daily living, cerebral glucose metabolism, and cognitive reserve in Lewy body and Parkinson’s disease. Dement Geriatr Cogn Disord 26:475–481

    Article  CAS  Google Scholar 

  21. Hindle JV, Martyr A, Clare L (2014) Cognitive reserve in Parkinson’s disease: a systematic review and meta-analysis. Parkinsonism Relat Disord 20:1–7

    Article  Google Scholar 

  22. Piccinini G, Imbimbo I, Ricciardi D, Coraci D, Santilli C, Lo Monaco MR, Loreti C, Vulpiani MC, Silveri MC, Padua L (2018) The impact of cognitive reserve on the effectiveness of balance rehabilitation in Parkinson’s disease. Eur J Phys Rehabil Med 54:554–559

    Article  Google Scholar 

  23. Padua L, Imbimbo I, Aprile I, Loreti C, Germanotta M, Coraci D, Piccinini G, Pazzaglia C, Santilli C, Cruciani A, Carrozza MC, the FDG Robotic Rehabilitation Group, Pecchioli C, Loreti S, Lattanzi S, Cortellini L, Papadopoulou D, Liberti G, Panzera F, Mitrione P, Ruzzi D, Rinaldi G, Insalaco S, de Santis F, Spinelli P, Marsan S, Bastoni I, Pellegrino A, Petitti T, Montesano A, Castagna A, Grosso C, Ammenti P, Cattaneo D, Azzinnaro L, Barbieri D, Cassani S, Corrini C, Meotti M, Parelli R, Spedicato A, Zocchi M, Loffi M, Manenti D, Negri L, Gramatica F, Gower V, Galeri S, Noro F, Medici L, Garattini R, Bariselli F, Luli M, Ricca M, Negrini S, Diverio M, Giannini E, Gabrielli A, Deidda B, Gnetti B, Beatini P, Callegari S, Cabano B, Converti F, Pizzi A, Falsini C, Romanelli A, de Luca G, Vannetti F, Simoncini E, Martini M, Peccini E, Cecchi F, Avila L, Gabrielli MA, Barilli M, Bertocchi E, Giannarelli G, Lerda E, Vasoli M, Rossi P, Marsili V, Tognoli B, Bertolini A, Vastola G, Speranza G, Colella M, Mosca R, Competiello G, Chiusano A, Della Vecchia A, Soriano P, Pagliarulo M, Remollino V, Langone E, Santarsiero R, Magliulo M, Araneo G, Galantucci L, Lioi N, Marrazzo F, Larocca S, Calia R, Benevento S, Toscano O, Lategana M (2020) Cognitive reserve as a useful variable to address robotic or conventional upper limb rehabilitation treatment after stroke: a multicentre study of the Fondazione Don Carlo Gnocchi. Eur J Neurol 27:392–398. https://doi.org/10.1111/ene.14090

    Article  CAS  PubMed  Google Scholar 

  24. Hoehn MM, Yahr MD (1967) Parkinsonism: onset, progression, and mortality. Neurology 17:427–442. https://doi.org/10.1212/wnl.17.5.427

    Article  CAS  PubMed  Google Scholar 

  25. Magni E, Binetti G, Bianchetti A, Rozzini R, Trabucchi M (1996) Mini-mental state examination: a normative study in Italian elderly population. Eur J Neurol 3:198–202

    Article  CAS  Google Scholar 

  26. Nucci M, Mapelli D, Mondini S (2012) Cognitive Reserve Index questionnaire (CRIq): a new instrument for measuring cognitive reserve. Aging Clin Exp Res 24:218–226

    PubMed  Google Scholar 

  27. Antonini A, Abbruzzese G, Ferini-Strambi L et al (2013) Validation of the Italian version of the Movement Disorder Society--Unified Parkinson’s Disease Rating Scale. Neurol Sci 34:683–687

    Article  Google Scholar 

  28. All H, Issues A, Nov N et al (2013) ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med 284:111–117. https://doi.org/10.1164/rccm.166/1/111

    Article  Google Scholar 

  29. Vanhoutte EK, Faber CG, Van Nes SI et al (2012) Modifying the Medical Research Council grading system through Rasch analyses. Brain 135:1639–1649. https://doi.org/10.1093/brain/awr318

    Article  PubMed  Google Scholar 

  30. Aprile I, Iacovelli C, Iuvone L et al (2016) Use of a virtual-technological sailing program to prepare children with disabilities for a real sailing course: effects on balance and quality of life. J Child Neurol 31(8):1074–1080. 1–7. https://doi.org/10.1177/088307381663875610.1177/0883073816638756

    Article  PubMed  Google Scholar 

  31. Wang WQ, Pi YL, Chen BL et al (2016) Cognitive motor intervention for gait and balance in Parkinson’s disease: systematic review and meta-analysis. Clin Rehabil 30:134–144

    Article  Google Scholar 

  32. Caetano MJD, Lord SR, Allen NE, Brodie MA, Song J, Paul SS, Canning CG, Menant JC (2018) Stepping reaction time and gait adaptability are significantly impaired in people with Parkinson’s disease: Implications for fall risk. Parkinsonism Relat Disord 47:32–38

    Article  Google Scholar 

  33. Beghi E, Gervasoni E, Pupillo E, Bianchi E, Montesano A, Aprile I, Agostini M, Rovaris M, Cattaneo D, Iacobone G, Jonsdottir J, Rodanò A, Romi S, Russo R, Tettamanzi F, Cruciani A, Imbimbo I, Polli A, Turolla A (2018) Prediction of falls in subjects suffering from Parkinson disease, multiple sclerosis, and stroke. Arch Phys Med Rehabil 99:641–651

    Article  Google Scholar 

  34. Ritondi L, Aprile I, Padua L (2010) Five ws on falls in disability patients. Inj Prev 16:285–286. https://doi.org/10.1136/ip.2010.028084

    Article  Google Scholar 

  35. Schlick C, Ernst A, Bötzel K (2016) Visual cues combined with treadmill training to improve gait performance in Parkinson’s disease: a pilot randomized controlled trial. Clin Rehabil 30:463–471

    Article  Google Scholar 

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Acknowledgements

We would like to thank Dr. Lisa Hobson-Webb for language editing, and Barbara Di Bianco and Cristina Gargano for their technical support.

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Correspondence to Daniele Coraci.

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The study was approved by the local ethical committee.

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The authors declare no competing interests.

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Informed consent was obtained from all individual participants included in the study.

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During data collection, Claudia Santilli, Augusto Fusco, and Luca Padua were affiliated to IRCCS Fondazione Don Carlo Gnocchi IRCCS, Milan, Italy.

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Imbimbo, I., Coraci, D., Santilli, C. et al. Parkinson’s disease and virtual reality rehabilitation: cognitive reserve influences the walking and balance outcome. Neurol Sci 42, 4615–4621 (2021). https://doi.org/10.1007/s10072-021-05123-3

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