Effectiveness of an Innovative Cognitive Treatment and Telerehabilitation on Subjects With Mild Cognitive Impairment: A Multicenter, Randomized, Active-Controlled Study

Rosa Manenti, Elena Gobbi, Francesca Baglio, Ambra Macis, Clarissa Ferrari, Ilaria Pagnoni, Federica Rossetto, Sonia Di Tella, Federica Alemanno, Vincenzo Cimino, Giuliano Binetti, Sandro Iannaccone, Placido Bramanti, Stefano F Cappa, Maria Cotelli, Rosa Manenti, Elena Gobbi, Francesca Baglio, Ambra Macis, Clarissa Ferrari, Ilaria Pagnoni, Federica Rossetto, Sonia Di Tella, Federica Alemanno, Vincenzo Cimino, Giuliano Binetti, Sandro Iannaccone, Placido Bramanti, Stefano F Cappa, Maria Cotelli

Abstract

Background: In recent years, the potential usefulness of cognitive training procedures in normal aging and mild cognitive impairment (MCI) have received increased attention.

Objective: The main aim of this study was to evaluate the efficacy of the face-to-face cognitive virtual reality rehabilitation system (VRRS) and to compare it to that of face-to-face cognitive treatment as usual for individuals with MCI. Moreover, we assessed the possibility of prolonging the effects of treatment with a telerehabilitation system.

Methods: A total of 49 subjects with MCI were assigned to 1 of 3 study groups in a randomized controlled trial design: (a) those who received face-to-face cognitive VRRS (12 sessions of individualized cognitive rehabilitation over 4 weeks) followed by telerehabilitation (36 sessions of home-based cognitive VRRS training, three sessions for week); (b) those who received face-to-face cognitive VRRS followed by at-home unstructured cognitive stimulation (36 sessions of home-based unstructured cognitive stimulation, three sessions for week); and (c) those who received face-to-face cognitive treatment as usual (12 sessions of face-to-face cognitive treatment as usual).

Results: An improvement in memory, language and visuo-constructional abilities was observed after the end of face-to-face VRRS treatment compared to face-to-face treatment as usual. The application of home-based cognitive VRRS telerehabilitation seems to induce more maintenance of the obtained gains than home-based unstructured stimulation.

Discussion: The present study provides preliminary evidence in support of individualized VRRS treatment and telerehabilitation delivery for cognitive rehabilitation and should pave the way for future studies aiming at identifying optimal cognitive treatment protocols in subjects with MCI.

Clinical trial registration: www.ClinicalTrials.gov, identifier NCT03486704.

Keywords: cognitive; dementia; home; mild cognitive impairment; telerehabilitation.

Copyright © 2020 Manenti, Gobbi, Baglio, Macis, Ferrari, Pagnoni, Rossetto, Di Tella, Alemanno, Cimino, Binetti, Iannaccone, Bramanti, Cappa and Cotelli.

Figures

FIGURE 1
FIGURE 1
Flow chart showing study subject enrollment and sample processing.
FIGURE 2
FIGURE 2
Effects of Face to Face cognitive VRRS (clinic-VRRS) vs. Face to Face cognitive treatment as Usual (clinic-TAU) on neuropsychological assessment. Asterisks indicate statistical significance.
FIGURE 3
FIGURE 3
Effects of home-based cognitive telerehabilitation (Tele@H-VRRS) vs. home-based unstructured cognitive stimulation (Tele@H-UCS) vs. no treatment on computerized cognitive tasks. Asterisks indicate statistical significance.

References

    1. American Psychiatric Association (2014). DSM-5: Manuale Diagnostico e Statistico dei Disturbi Mentali. Milan: Raffaello Cortina editore.
    1. Antonietti A., Gandolla M., Rossini M., Molteni F., Pedrocchi A., Consortium A. (2016). “Interference between cognitive and motor recovery in elderly dementia patients through a holistic tele-rehabilitation platform,” in International Conference on Wireless Mobile Communication and Healthcare, Vol. 192 eds Perego P., Andreoni G., Rizzo G. (Cham: Springer; ), 359–366. 10.1007/978-3-319-58877-3_45
    1. Astell A. J. (2019). Technology and dementia: the future is now. Dement. Geriatr. Cogn. Disord. 47 129–130. 10.1159/000497799
    1. Bangor A., Kortum P., Miller J. (2009). Determining what individual SUS scores mean: adding an adjective rating scale. J. Usability Stud. 4 114–123.
    1. Bangor A., Kortum P. T., Miller J. T. (2008). An empirical evaluation of the system usability scale. Int. J. Hum. Comput. Interact. 24 574–594. 10.1080/10447310802205776
    1. Basso A., Capitani E., Laiacona M. (1987). Raven’s coloured progressive matrices: normative values on 305 adult normal controls. Funct. Neurol. 2 189–194.
    1. Belleville S. (2008). Cognitive training for persons with mild cognitive impairment. Int. Psychogeriatr. 20 57–66. 10.1017/s104161020700631x
    1. Bender R., Lange S. (2001). Adjusting for multiple testing—when and how? J. Clin. Epidemiol. 54 343–349. 10.1016/s0895-4356(00)00314-0
    1. Bharucha A. J., Anand V., Forlizzi J., Dew M. A., Reynolds C. F., III, Stevens S., et al. (2009). Intelligent assistive technology applications to dementia care: current capabilities, limitations, and future challenges. Am. J. Geriatr. Psychiatry 17 88–104. 10.1097/jgp.0b013e318187dde5
    1. Bianchetti A., Cornali C., Ranieri P., Trabucchi M. (2017). Quality of life in patients with mild dementia. Validation of the Italian version of the quality of life Alzheimer’s disease (QoL-AD) scale. J. Ital. Soc. Gerontol. Geriatr. 65:137.
    1. Binetti G., Mega M. S., Magni E., Padovani A., Rozzini L., Bianchetti A., et al. (1998). Behavioral disorders in Alzheimer disease: a transcultural perspective. Arch. Neurol. 55 539–544. 10.1001/archneur.55.4.539
    1. Boutron I., Altman D. G., Moher D., Schulz K. F., Ravaud P., Group C. N. (2017). CONSORT statement for randomized trials of nonpharmacologic treatments: a 2017 update and a CONSORT extension for nonpharmacologic trial abstracts. Ann. Intern. Med. 167 40–47. 10.7326/m17-0046
    1. Boutron I., Moher D., Altman D. G., Schulz K. F., Ravaud P., Group C. (2008). Extending the CONSORT statement to randomized trials of nonpharmacologic treatment: explanation and elaboration. Ann. Intern. Med. 148 295–309. 10.7326/0003-4819-148-4-200802190-00008
    1. Brennan D., Georgeadis A., Baron C. (2002). Telerehabilitation tools for the provision of remote speech-language treatment. Top. Stroke Rehabil. 8 71–78. 10.1310/u7kv-dy7u-q6qp-lvbp
    1. Brennan D. M., Mawson S., Brownsell S. (2009). Telerehabilitation: enabling the remote delivery of healthcare, rehabilitation, and self management. Stud. Health Technol. Inform. 145 231–248.
    1. Brennan D. M., Tindall L., Theodoros D., Brown J., Campbell M., Christiana D., et al. (2011). A blueprint for telerehabilitation guidelines–October 2010. Telemed. J. E Health 17 662–665. 10.1089/tmj.2011.0036
    1. Brooke J. (1996). SUS-A quick and dirty usability scale. Usability Eval. Ind. 189 4–7.
    1. Brown G. C. (2015). Living too long: the current focus of medical research on increasing the quantity, rather than the quality, of life is damaging our health and harming the economy. EMBO Rep. 16 137–141. 10.15252/embr.201439518
    1. Burdea G., Polistico K., Krishnamoorthy A., House G., Rethage D., Hundal J., et al. (2015). Feasibility study of the BrightBrainerTM integrative cognitive rehabilitation system for elderly with dementia. Disabil. Rehabil. Assist. Technol. 10 421–432. 10.3109/17483107.2014.900575
    1. Burton R. L., O’Connell M. E. (2018). Telehealth rehabilitation for cognitive impairment: randomized controlled feasibility trial. JMIR Res. Protoc. 7:e43. 10.2196/resprot.9420
    1. Caffarra P., Vezzadini G., Dieci F., Zonato F., Venneri A. (2002). Rey-Osterrieth complex figure: normative values in an Italian population sample. Neurol. Sci. 22 443–447. 10.1007/s100720200003
    1. Calabria M., Manenti R., Rosini S., Zanetti O., Miniussi C., Cotelli M. (2011). Objective and subjective memory impairment in elderly adults: a revised version of the everyday memory questionnaire. Aging Clin. Exp. Res. 23 67–73. 10.1007/bf03324954
    1. Carlesimo G. A., Caltagirone C., Gainotti G. (1996). The mental deterioration battery: normative data, diagnostic reliability and qualitative analyses of cognitive impairment. The group for the standardization of the mental deterioration battery. Eur. Neurol. 36 378–384. 10.1159/000117297
    1. Cherney L. R., van Vuuren S. (2012). Telerehabilitation, virtual therapists, and acquired neurologic speech and language disorders. Semin. Speech Lang. 33 243–257. 10.1055/s-0032-1320044
    1. Cotelli M., Manenti R., Brambilla M., Gobbi E., Ferrari C., Binetti G., et al. (2019). Cognitive telerehabilitation in mild cognitive impairment, Alzheimer’s disease and frontotemporal dementia: a systematic review. J. Telemed. Telecare 25 67–79. 10.1177/1357633x17740390
    1. Cummings J. L., Mega M., Gray K., Rosenberg-Thompson S., Carusi D. A., Gornbein J. (1994). The neuropsychiatric inventory: comprehensive assessment of psychopathology in dementia. Neurology 44 2308–2314. 10.1212/wnl.44.12.2308
    1. Di Tella S., Pagliari C., Blasi V., Mendozzi L., Rovaris M., Baglio F. (2019). Integrated telerehabilitation approach in multiple sclerosis: a systematic review and meta-analysis. J. Telemed. Telecare 26 385–399. 10.1177/1357633x19850381
    1. Dodakian L., Mckenzie A. L., Le V., See J., Pearson-Fuhrhop K., Burke Quinlan E., et al. (2017). A home-based telerehabilitation program for patients with stroke. Neurorehabil. Neural Repair 31 923–933. 10.1177/1545968317733818
    1. Espay A. J., Bonato P., Nahab F. B., Maetzler W., Dean J. M., Klucken J., et al. (2016). Technology in Parkinson’s disease: challenges and opportunities. Mov. Disord. 31 1272–1282.
    1. Fetta J., Starkweather A., Gill J. M. (2017). Computer-based cognitive rehabilitation interventions for traumatic brain injury: a critical review of the literature. J. Neurosci. Nurs. 49 235–240. 10.1097/jnn.0000000000000298
    1. Folstein M. F., Folstein S. E., Mchugh P. R. (1975). “Mini-mental state”: a practical method for grading the cognitive state of patients for the clinician. J. Psychiatr. Res. 12 189–198.
    1. Forducey P. G., Ruwe W. D., Dawson S. J., Scheideman-Miller C., Mcdonald N. B., Hantla M. R. (2003). Using telerehabilitation to promote TBI recovery and transfer of knowledge. NeuroRehabilitation 18 103–111. 10.3233/nre-2003-18203
    1. Frasson P., Ghiretti R., Catricalà E., Pomati S., Marcone A., Parisi L., et al. (2011). Free and cued selective reminding test: an Italian normative study. Neurol. Sci. 32 1057–1062. 10.1007/s10072-011-0607-3
    1. Fratiglioni L., De Ronchi D., Aguero-Torres H. (1999). Worldwide prevalence and incidence of dementia. Drugs Aging 15 365–375. 10.2165/00002512-199915050-00004
    1. Giovagnoli A. R., Del Pesce M., Mascheroni S., Simoncelli M., Laiacona M., Capitani E. (1996). Trail making test: normative values from 287 normal adult controls. Ital. J. Neurol. Sci. 17 305–309. 10.1007/bf01997792
    1. Gooding A. L., Choi J., Fiszdon J. M., Wilkins K., Kirwin P. D., Van Dyck C. H., et al. (2016). Comparing three methods of computerised cognitive training for older adults with subclinical cognitive decline. Neuropsychol. Rehabil. 26 810–821. 10.1080/09602011.2015.1118389
    1. Hailey D., Roine R., Ohinmaa A., Dennett L. (2011). Evidence of benefit from telerehabilitation in routine care: a systematic review. J. Telemed. Telecare 17 281–287. 10.1258/jtt.2011.101208
    1. Hong Y. J., Jang E. H., Hwang J., Roh J. H., Lee J. H. (2015). The efficacy of cognitive intervention programs for mild cognitive impairment: a systematic review. Curr. Alzheimer Res. 12 527–542. 10.2174/1567205012666150530201636
    1. Isernia S., Pagliari C., Jonsdottir J., Castiglioni C., Gindri P., Gramigna C., et al. (2019). Efficiency and patient-reported outcome measures from clinic to home: the human empowerment aging and disability program for digital-health rehabilitation. Front. Neurol. 10:1206. 10.3389/fneur.2019.01206
    1. Janoutova J., Sery O., Hosak L., Janout V. (2015). Is mild cognitive impairment a precursor of Alzheimer’s disease? Short review. Cent. Eur. J. Public Health 23 365–367. 10.21101/cejph.a4414
    1. Jelcic N., Agostini M., Meneghello F., Busse C., Parise S., Galano A., et al. (2014). Feasibility and efficacy of cognitive telerehabilitation in early Alzheimer’s disease: a pilot study. Clin. Interv. Aging 9 1605–1611. 10.2147/cia.s68145
    1. Kairy D., Lehoux P., Vincent C., Visintin M. (2009). A systematic review of clinical outcomes, clinical process, healthcare utilization and costs associated with telerehabilitation. Disabil. Rehabil. 31 427–447. 10.1080/09638280802062553
    1. Katz S. (1983). Assessing self-maintenance: activities of daily living, mobility, and instrumental activities of daily living. J. Am. Geriatr. Soc. 31 721–727. 10.1111/j.1532-5415.1983.tb03391.x
    1. Kidd P. M. (2008). Alzheimer’s disease, amnestic mild cognitive impairment, and age-associated memory impairment: current understanding and progress toward integrative prevention. Altern. Med. Rev. 13 85–115.
    1. Lampit A., Hallock H., Moss R., Kwok S., Rosser M., Lukjanenko M., et al. (2014). The Timecourse of global cognitive gains from supervised computer-assisted cognitive training: a randomised, active-controlled trial in elderly with multiple dementia risk factors can computerized cognitive training reverse the diagnosis of HIV-associated neurocognitive disorder? A research protocol. J. Prev. Alzheimers Dis. 1 33–39.
    1. Lawton M., Brody E. (1988). Instrumental activities of daily living (IADL) scale-self-rated version. Psychopharmacol. Bull. 24 789–791.
    1. Lezak M., Howieson D., Bigler E., Tranel D. (2012). Neuropsychological Assessment, 5th Edn Oxford: Oxford University Press.
    1. Li B. Y., Wang Y., Tang H. D., Chen S. D. (2017). The role of cognitive activity in cognition protection: from Bedside to Bench. Transl. Neurodegener. 6:7.
    1. Li H., Li J., Li N., Li B., Wang P., Zhou T. (2011). Cognitive intervention for persons with mild cognitive impairment: a meta-analysis. Ageing Res. Rev. 10 285–296. 10.1016/j.arr.2010.11.003
    1. Li R., Zhu X., Yin S., Niu Y., Zheng Z., Huang X., et al. (2014). Multimodal intervention in older adults improves resting-state functional connectivity between the medial prefrontal cortex and medial temporal lobe. Front. Aging Neurosci. 6:39. 10.3389/fnagi.2014.00039
    1. Liao Y. Y., Chen I. H., Lin Y. J., Chen Y., Hsu W. C. (2019). Effects of virtual reality-based physical and cognitive training on executive function and dual-task gait performance in older adults with mild cognitive impairment: a randomized control trial. Front. Aging Neurosci. 11:162. 10.3389/fnagi.2019.00162
    1. Linden M., Hawley C., Blackwood B., Evans J., Anderson V., O’rourke C. (2016). Technological aids for the rehabilitation of memory and executive functioning in children and adolescents with acquired brain injury. Cochrane Database Syst. Rev. 7:CD011020.
    1. Livingston G., Sommerlad A., Orgeta V., Costafreda S. G., Huntley J., Ames D., et al. (2017). Dementia prevention, intervention, and care. Lancet 390 2673–2734.
    1. Mashima P. A., Doarn C. R. (2008). Overview of telehealth activities in speech-language pathology. Telemed. J. E Health 14 1101–1117. 10.1089/tmj.2008.0080
    1. Matamala-Gomez M., Maisto M., Montana J. I., Mavrodiev P. A., Baglio F., Rossetto F., et al. (2020). The role of engagement in teleneurorehabilitation: a systematic review. Front. Neurol. 11:354. 10.3389/fneur.2020.00354
    1. McCue M., Fairman A., Pramuka M. (2010). Enhancing quality of life through telerehabilitation. Phys. Med. Rehabil. Clin. N. Am. 21 195–205. 10.1016/j.pmr.2009.07.005
    1. Medalia A., Freilich B. (2008). The neuropsychological educational approach to cognitive remediation (NEAR) model: practice principles and outcome studies. Am. J. Psychiatr. Rehabil. 11 123–143. 10.1080/15487760801963660
    1. Miceli G., Laudanna A., Burani C., Capasso R. (1994). Batteria per l’Analisi dei Deficit Afasici (BADA), CEPSAG. Rome: Universita Cattolica del Sacro Cuore.
    1. Moreno A., Wall K. J., Thangavelu K., Craven L., Ward E., Dissanayaka N. N. (2019). A systematic review of the use of virtual reality and its effects on cognition in individuals with neurocognitive disorders. Alzheimers Dement. 5 834–850. 10.1016/j.trci.2019.09.016
    1. Morris J. C. (1997). Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. Int. Psychogeriatr. 9(Suppl. 1), 173–176; discussion 177–178.
    1. Moyle W. (2019). The promise of technology in the future of dementia care. Nat. Rev. Neurol. 15 353–359. 10.1038/s41582-019-0188-y
    1. Novelli G., Papagno C., Capitani E., Laiacona M. (1986). Tre test clinici di ricerca e produzione lessicale. Taratura su sogetti normali. Arch. Psicol. Neurol. Psichiatr. 47 477–506.
    1. 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.
    1. Peres S. C., Pham T., Phillips R. (2013). “Validation of the system usability scale (SUS) SUS in the wild,” in Proceedings of the Human Factors and Ergonomics Society Annual Meeting (Los Angeles, CA: SAGE Publications; ), 192–196. 10.1177/1541931213571043
    1. Peretti A., Amenta F., Tayebati S. K., Nittari G., Mahdi S. S. (2017). Telerehabilitation: review of the state-of-the-art and areas of application. JMIR Rehabil. Assist. Technol. 4:e7. 10.2196/rehab.7511
    1. Petersen R. C. (2004). Mild cognitive impairment as a diagnostic entity. J. Intern. Med. 256 183–194. 10.1111/j.1365-2796.2004.01388.x
    1. Petersen R. C. (2011). Clinical practice. Mild cognitive impairment. N. Engl. J. Med. 364 2227–2234.
    1. Petersen R. C., Caracciolo B., Brayne C., Gauthier S., Jelic V., Fratiglioni L. (2014). Mild cognitive impairment: a concept in evolution. J. Intern. Med. 275 214–228.
    1. Petersen R. C., Smith G. E., Waring S. C., Ivnik R. J., Tangalos E. G., Kokmen E. (1999). Mild cognitive impairment: clinical characterization and outcome. Arch. Neurol. 56 303–308. 10.1001/archneur.56.3.303
    1. Pitt R., Theodoros D., Hill A. J., Russell T. (2019). The impact of the telerehabilitation group aphasia intervention and networking programme on communication, participation, and quality of life in people with aphasia. Int. J. Speech Lang. Pathol. 21 513–523. 10.1080/17549507.2018.1488990
    1. Poon P., Hui E., Dai D., Kwok T., Woo J. (2005). Cognitive intervention for community-dwelling older persons with memory problems: telemedicine versus face-to-face treatment. Int. J. Geriatr. Psychiatry 20 285–286. 10.1002/gps.1282
    1. Proschan M. A., Follmann D. A. (1995). Multiple comparisons with control in a single experiment versus separate experiments: why do we feel differently? Am. Stat. 49 144–149. 10.2307/2684628
    1. R Core Team (2013). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.
    1. Realdon O., Rossetto F., Nalin M., Baroni I., Cabinio M., Fioravanti R., et al. (2016). Technology-enhanced multi-domain at home continuum of care program with respect to usual care for people with cognitive impairment: the ability-TelerehABILITation study protocol for a randomized controlled trial. BMC Psychiatry 16:425. 10.1186/s12888-016-1132-y
    1. Rosen M. J. (2004). Telerehabilitation. Telemed. J. E Health 10 115–117.
    1. Sherman D. S., Mauser J., Nuno M., Sherzai D. (2017). The efficacy of cognitive intervention in mild cognitive impairment (MCI): a meta-analysis of outcomes on neuropsychological measures. Neuropsychol. Rev. 27 440–484. 10.1007/s11065-017-9363-3
    1. Shulman K. I., Pushkar Gold D., Cohen C. A., Zucchero C. A. (1993). Clock-drawing and dementia in the community: a longitudinal study. Int. J. Geriatr. Psychiatry 8 487–496. 10.1002/gps.930080606
    1. Siciliano M., Chiorri C., Battini V., Sant’elia V., Altieri M., Trojano L., et al. (2019). Regression-based normative data and equivalent scores for Trail Making Test (TMT): an updated Italian normative study. Neurol. Sci. 40 469–477. 10.1007/s10072-018-3673-y
    1. Solana J., Cáceres C., García-Molina A., Opisso E., Roig T., Tormos J. M., et al. (2015). Improving brain injury cognitive rehabilitation by personalized telerehabilitation services: guttmann neuropersonal trainer. IEEE J. Biomed. Health Inform. 19 124–131. 10.1109/jbhi.2014.2354537
    1. Sunderland A., Watts K., Baddeley A. D., Harris J. E. (1986). Subjective memory assessment and test performance in elderly adults. J. Gerontol. 41 376–384. 10.1093/geronj/41.3.376
    1. Topol E. (2019). The Topol Review: Preparing the Healthcare Workforce to Deliver the Digital Future. London: Health Education England.
    1. Tuena C., Pedroli E., Trimarchi P. D., Gallucci A., Chiappini M., Goulene K., et al. (2020). Usability issues of clinical and research applications of virtual reality in older people: a systematic review. Front. Hum. Neurosci. 14:93. 10.3389/fnhum.2020.00093
    1. Vance D. E., Fazeli P. L., Azuero A., Wadley V. G., Jensen M., Raper J. L. (2018). Can computerized cognitive training reverse the diagnosis of HIV-associated neurocognitive disorder? A research protocol. Res. Nurs. Health 41 11–18. 10.1002/nur.21841
    1. Vannini P., Amariglio R., Hanseeuw B., Johnson K. A., Mclaren D. G., Chhatwal J., et al. (2017). Memory self-awareness in the preclinical and prodromal stages of Alzheimer’s disease. Neuropsychologia 99 343–349. 10.1016/j.neuropsychologia.2017.04.002
    1. Vermeij A., Claassen J. A., Dautzenberg P. L., Kessels R. P. (2016). Transfer and maintenance effects of online working-memory training in normal ageing and mild cognitive impairment. Neuropsychol. Rehabil. 26 783–809. 10.1080/09602011.2015.1048694
    1. Yao S., Liu Y., Zheng X., Zhang Y., Cui S., Tang C., et al. (2020). Do nonpharmacological interventions prevent cognitive decline? a systematic review and meta-analysis. Transl. Psychiatry 10:19.
    1. Yesavage J. A., Brink T. L., Rose T. L., Lum O., Huang V., Adey M., et al. (1982). Development and validation of a geriatric depression screening scale: a preliminary report. J. Psychiatr. Res. 17 37–49. 10.1016/0022-3956(82)90033-4
    1. Zampolini M., Todeschini E., Bernabeu Guitart M., Hermens H., Ilsbroukx S., Macellari V., et al. (2008). Tele-rehabilitation: present and future. Ann. Ist. Super. Sanita 44 125–134.

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