Skip to main content
SpringerLink
Log in

Premorbid functional reserve modulates the effect of rehabilitation in multiple sclerosis

  • Original Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

Background

Premorbid physically and intellectually enriching lifestyles have increasingly been recognized as able to mitigate the risk of disease-related disability in patients with multiple sclerosis (MS).

Objective

To explore if premorbid physical activity, cognitive reserve and trait personality act as proxies for functional reserve that contributes to rehabilitation outcome.

Methods

We recruited all patients previously enrolled in two pilot trials investigating the effect of home-based video game training in improving balance (Study 1) and attention (Study 2) for additional assessments with the Historical Leisure Activity Questionnaire (HLAQ; a proxy for premorbid physical activity), Cognitive Reserve Index Questionnaire (CRIQ), and Temperament and Character Inventory (TCI). Hierarchical logistic regression (HLR) analyses tested the association of HLAQ, CRIQ, and TCI with training effect on balance (static posturography) and on attention (Symbol Digit Modalities Test).

Results

We identified 94% (34/36) and 74% (26/35) of patients participating at the original Study 1 and Study 2, respectively. HLR analyses showed an exclusive “intra-modal” modulation of rehabilitation outcome by functional reserve, given that (1) larger training effect on balance was associated with higher HLAQ (OR = 2.03, p = 0.031); (2) larger training effect on attention was associated with higher CRIQ (OR = 1.27, p = 0.033). Furthermore, we found specific personality traits associated with (1) greater training effect on balance (self-directedness; OR = 1.40, p = 0.051) and lower training effect on attention (harm avoidance; OR = 0.66, p = 0.075).

Conclusion

We hypothesize that premorbid physical and intellectual activities not only act as a buffer for limiting the MS-related damage but also as functional reserve that can be retrieved by task-oriented training to promote recovery through rehabilitation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Cramer SC, Sur M, Dobkin BH, O'Brien C, Sanger TD, Trojanowski JQ, Rumsey JM, Hicks R, Cameron J, Chen D, Chen WG, Cohen LG, deCharms C, Duffy CJ, Eden GF, Fetz EE, Filart R, Freund M, Grant SJ, Haber S, Kalivas PW, Kolb B, Kramer AF, Lynch M, Mayberg HS, McQuillen P, Nitkin R, Pascual-Leone A, Reuter-Lorenz P, Schiff N, Sharma A, Shekim L, Stryker M, Sullivan EV, Vinogradov S (2011) Harnessing neuroplasticity for clinical applications. Brain J Neurol 134(Pt 6):1591–1609

    Article  Google Scholar 

  2. Kleim JA (2011) Neural plasticity and neurorehabilitation: teaching the new brain old tricks. J Commun Disord 44(5):521–528

    Article  PubMed  Google Scholar 

  3. Tomassini V, Matthews PM, Thompson AJ et al (2012) Neuroplasticity and functional recovery in multiple sclerosis. Nat Rev Neurol 8(11):635–646

    Article  PubMed  PubMed Central  Google Scholar 

  4. Barkhof F (2002) The clinico-radiological paradox in multiple sclerosis revisited. Curr Opin Neurol 15(3):239–245

    Article  PubMed  Google Scholar 

  5. Krieger SC, Sumowski J (2018) New insights into multiple sclerosis clinical course from the topographical model and functional reserve. Neurol Clin 36(1):13–25

    Article  PubMed  Google Scholar 

  6. Sumowski JF, Leavitt VM (2013) Cognitive reserve in multiple sclerosis. Mult Scler 19(9):1122–1127

    Article  PubMed  Google Scholar 

  7. Elmståhl S, Sommer M, Hagberg B (1996) A 3-year follow-up of stroke patients: relationships between activities of daily living and personality characteristics. Arch Gerontol Geriatr 22(3):233–244

    Article  PubMed  Google Scholar 

  8. Sela-Kaufman M, Rassovsky Y, Agranov E, Levi Y, Vakil E (2013) Premorbid personality characteristics and attachment style moderate the effect of injury severity on occupational outcome in traumatic brain injury: another aspect of reserve. J Clin Exp Neuropsychol 35(6):584–595

    Article  PubMed  Google Scholar 

  9. Prosperini L, Fortuna D, Giannì C, Leonardi L, Marchetti MR, Pozzilli C (2013) Home-based balance training using the Wii balance board: a randomized, crossover pilot study in multiple sclerosis. Neurorehabil Neural Repair 27(6):516–525

    Article  PubMed  Google Scholar 

  10. De Giglio L, De Luca F, Prosperini L et al (2015) A low-cost cognitive rehabilitation with a commercial video game improves sustained attention and executive functions in multiple sclerosis: a pilot study. Neurorehabil Neural Repair 29(5):453–461

    Article  PubMed  Google Scholar 

  11. Prosperini L, Fanelli F, Petsas N et al (2014) Multiple sclerosis: changes in microarchitecture of white matter tracts after training with a video game balance board. Radiology. 273(2):529–538

    Article  PubMed  Google Scholar 

  12. De Giglio L, Tona F, De Luca F et al (2016) Multiple sclerosis: changes in thalamic resting-state functional connectivity induced by a home-based cognitive rehabilitation program. Radiology. 280(1):202–211

    Article  PubMed  Google Scholar 

  13. Motl RW, Dlugonski D, Pilutti L, Sandroff B, McAuley E (2012) Premorbid physical activity predicts disability progression in relapsing-remitting multiple sclerosis. J Neurol Sci 323(1–2):123–127

    Article  PubMed  Google Scholar 

  14. Nucci M, Mapelli D, Mondini S (2012) Cognitive reserve index questionnaire (CRIq): a new instrument for measuring cognitive reserve. Aging Clin Exp Res 24(3):218–226

    PubMed  Google Scholar 

  15. Cloninger CR, Svrakic DM, Przybeck TR (1993) A psychobiological model of temperament and character. Arch Gen Psychiatry 50(12):975–990

    Article  CAS  PubMed  Google Scholar 

  16. Fossati A, Cloninger CR, Villa D, Borroni S, Grazioli F, Giarolli L, Battaglia M, Maffei C (2007) Reliability and validity of the Italian version of the temperament and character inventory-revised in an outpatient sample. Compr Psychiatry 48(4):380–387

    Article  PubMed  Google Scholar 

  17. Prosperini L, Coghe G, Pau M et al (2015) Minimal detectable change of postural sway detected at static posturography in multiple sclerosis. RIMS conference abstracts. Mult Scler 21(4):492–534

    Article  Google Scholar 

  18. Strober L, DeLuca J, Benedict RH, et al (2019) Symbol digit modalities test: a valid clinical trial endpoint for measuring cognition in multiple sclerosis. Mult Scler 25(13):1781–1790

  19. Santangelo G, Altieri M, Enzinger C, Gallo A, Trojano L (2019) Cognitive reserve and neuropsychological performance in multiple sclerosis: a meta-analysis. Neuropsychology. 33(3):379–390

    Article  PubMed  Google Scholar 

  20. Gazioglu S, Cakmak VA, Ozkorumak E, Usta NC, Ates C, Boz C (2014) Personality traits of patients with multiple sclerosis and their relationship with clinical characteristics. J Nerv Ment Dis 202(5):408–411

    Article  PubMed  Google Scholar 

  21. Fazekas C, Khalil M, Enzinger C, Matzer F, Fuchs S, Fazekas F (2013) No impact of adult attachment and temperament on clinical variability in patients with clinically isolated syndrome and early multiple sclerosis. Clin Neurol Neurosurg 115(3):293–297

    Article  PubMed  Google Scholar 

  22. Leavitt VM, Buyukturkoglu K, Inglese M (2017) Sumowski JF (2017) protective personality traits: high openness and low neuroticism linked to better memory in multiple sclerosis. Mult Scler 23(13):1786–1790

    Article  PubMed  PubMed Central  Google Scholar 

  23. Zarbo IR, Minacapelli E, Falautano M et al (2016) Personality traits predict perceived health-related quality of life in persons with multiple sclerosis. Mult Scler 22(4):551–558

    Article  PubMed  Google Scholar 

  24. Roy S, Drake A, Fuchs T, et al (2018) Longitudinal personality change associated with cognitive decline in multiple sclerosis. Mult Scler. https://doi.org/10.1177/1352458517753720

  25. Prosperini L, Piattella MC, Giannì C, Pantano P (2015) Functional and structural brain plasticity enhanced by motor and cognitive rehabilitation in multiple sclerosis. Neural Plast 2015:481574

    Article  PubMed  PubMed Central  Google Scholar 

  26. Sunwoo MK, Lee JE, Hong JY, Ye BS, Lee HS, Oh JS, Kim JS, Lee PH, Sohn YH (2017) Premorbid exercise engagement and motor reserve in Parkinson’s disease. Parkinsonism Relat Disord 34:49–53

    Article  PubMed  Google Scholar 

  27. Yamaguchi T, Yamamura O, Hamano T, Murakita K, Nakamoto Y (2018) Premorbid physical activity is modestly associated with gait independence after a stroke: an exploratory study. Eur Rev Aging Phys Act 15:18

    Article  PubMed  PubMed Central  Google Scholar 

  28. Karaahmet OZ, Umay E, Gurcay E, Serçe A, Gundogdu I, Cakci A (2018) The effect of premorbid features on post-stroke rehabilitation outcome. Iran J Neurol 17(1):38–46

    PubMed  PubMed Central  Google Scholar 

  29. Schneider EB, Sur S, Raymont V et al (2014) Functional recovery after moderate/severe traumatic brain injury: a role for cognitive reserve? Neurology. 82(18):1636–1642

    Article  PubMed  PubMed Central  Google Scholar 

  30. Jokinen H, Melkas S, Madureira S et al (2016) Cognitive reserve moderates long-term cognitive and functional outcome in cerebral small vessel disease. J Neurol Neurosurg Psychiatry 87(12):1296–1302

    Article  PubMed  Google Scholar 

  31. Cheng S-T (2016) Cognitive reserve and the prevention of dementia: the role of physical and cognitive activities. Curr Psychiatry Rep 18(9):85

    Article  PubMed  PubMed Central  Google Scholar 

  32. Steward KA, Kennedy R, Novack TA, Crowe M, Marson DC, Triebel KL (2018) The role of cognitive reserve in recovery from traumatic brain injury. J Head Trauma Rehabil 33(1):E18–E27

    Article  PubMed  PubMed Central  Google Scholar 

  33. 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(4):554–559

    PubMed  Google Scholar 

  34. Satz P, Cole MA, Hardy DJ, Rassovsky Y (2011) Brain and cognitive reserve: mediator(s) and construct validity, a critique. J Clin Exp Neuropsychol 33(1):121–130

    Article  PubMed  Google Scholar 

  35. Sumowski JF (2015) Cognitive reserve as a useful concept for early intervention research in multiple sclerosis. Front Neurol 6:176

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

Supported by FISM - Fondazione Italiana Sclerosi Multipla - cod. 2017/R/22 and financed or co-financed with the ‘5 per mille’ public funding.

Author information

Authors and Affiliations

  1. IRCCS Don Carlo Gnocchi Foundation, Piazzale Morandi 6, 20121, Milan, Italy

    Letizia Castelli

  2. S. Filippo Neri Hospital, Via G. Martinotti 20, 00135, Roma, Italy

    Laura De Giglio

  3. Department of Human Neuroscience, Sapienza University, viale dell’Università 30, 00185, Rome, Italy

    Laura De Giglio

  4. S. Camillo-Forlanini Hospital, C.ne Gianicolense 87, 00152, Rome, Italy

    Shalom Haggiag, Serena Ruggieri & Luca Prosperini

  5. Physical Therapy Unit, S. Andrea Hospital, Via di Grottarossa 1035, 00189, Rome, Italy

    Arianna Traini

  6. Department of Psychology, Sapienza University, Viale dell’Università 30, 00185, Rome, Italy

    Francesca De Luca

Authors
  1. Letizia Castelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laura De Giglio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shalom Haggiag
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Arianna Traini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francesca De Luca
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Serena Ruggieri
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luca Prosperini
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Luca Prosperini.

Ethics declarations

Conflict of interest

None related to this article.

Ethical standards

The present study was conducted after approval of the Local Ethics Committee. All data were gathered after informed consent was obtained from each participant, in accordance with specific national laws and the ethics standards laid down in the 1964 Declaration of Helsinki and its later amendments. In no way this study did interfere in the care received by patients. Anonymized data will be shared upon request by the corresponding author (LP).

Financial disclosures

LC: consulting fees from Almirall; LDG: travel grants from Biogen, Novartis, and Teva; LP: consulting fees from Biogen, Novartis and Roche; speaker honoraria from Biogen, Genzyme, Merck Serono, Novartis, and Teva; travel grants from Biogen, Genzyme, Novartis, and Teva; research grants from the Italian MS Society (Associazione Italiana Sclerosi Multipla) and Genzyme; SH, AT, FDL: none to declare.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Castelli, L., De Giglio, L., Haggiag, S. et al. Premorbid functional reserve modulates the effect of rehabilitation in multiple sclerosis. Neurol Sci 41, 1251–1257 (2020). https://doi.org/10.1007/s10072-019-04237-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-019-04237-z

Keywords

Search

Navigation