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Open Access 26-02-2024 | Alzheimer's Disease | Review

Virtual Reality and Serious Videogame-Based Instruments for Assessing Spatial Navigation in Alzheimer’s Disease: A Systematic Review of Psychometric Properties

Authors: Juan Pablo Sánchez-Escudero, Ana María Galvis-Herrera, David Sánchez-Trujillo, Laura Cristina Torres-López, Cole J. Kennedy, Daniel Camilo Aguirre-Acevedo, Mauricio A. Garcia-Barrera, Natalia Trujillo

Published in: Neuropsychology Review

Abstract

Over the past decade, research using virtual reality and serious game-based instruments for assessing spatial navigation and spatial memory in at-risk and AD populations has risen. We systematically reviewed the literature since 2012 to identify and evaluate the methodological quality and risk of bias in the analyses of the psychometric properties of VRSG-based instruments. The search was conducted primarily in July–December 2022 and updated in November 2023 in eight major databases. The quality of instrument development and study design were analyzed in all studies. Measurement properties were defined and analyzed according to COSMIN guidelines. A total of 1078 unique records were screened, and following selection criteria, thirty-seven studies were analyzed. From these studies, 30 instruments were identified. Construct and criterion validity were the most reported measurement properties, while structural validity and internal consistency evidence were the least reported. Nineteen studies were deemed very good in construct validity, whereas 11 studies reporting diagnostic accuracy were deemed very good in quality. Limitations regarding theoretical framework and research design requirements were found in most of the studies. VRSG-based instruments are valuable additions to the current diagnostic toolkit for AD. Further research is required to establish the psychometric performance and clinical utility of VRSG-based instruments, particularly the instrument development, content validity, and diagnostic accuracy for preclinical AD screening scenarios. This review provides a straightforward synthesis of the state of the art of VRSG-based instruments and suggests future directions for research.

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Abma, I. L., Rovers, M., & Van Der Wees, P. J. (2016). Appraising convergent validity of patient-reported outcome measures in systematic reviews: Constructing hypotheses and interpreting outcomes. BMC Research Notes, 9(226), 1–5. https://doi.org/10.1186/s13104-016-2034-2CrossRef

Allison, S. L., Fagan, A. M., Morris, J. C., & Head, D. (2016). Spatial navigation in preclinical Alzheimer’s disease Samantha. Journal of Alzheimer’s Disease, 52(1), 77–90. https://doi.org/10.3233/JAD-150855CrossRefPubMed

Allison, S. L., Rodebaugh, T. L., Johnston, C., Fagan, A. M., Morris, J. C., & Head, D. (2019). Developing a spatial navigation screening tool sensitive to the preclinical Alzheimer disease continuum. Archives of Clinical Neuropsychology, 34(7), 1138–1155. https://doi.org/10.1093/arclin/acz019CrossRefPubMedPubMedCentral

Alsbury-Nealy, K., Wang, H., Howarth, C., Gordienko, A., Schlichting, M. L., & Duncan, K. D. (2021). OpenMaze: An open-source toolbox for creating virtual navigation experiments. Behavior Research Methods, 54(3), 1374–1387. https://doi.org/10.3758/s13428-021-01664-9CrossRefPubMed

Alzheimer’s Association. (2023). 2023 Alzheimer’s disease facts and figures, 19(4), 1598–1695. https://doi.org/10.1002/alz.13016CrossRef

Bayahya, A. Y., Alhalabi, W., & Alamri, S. H. (2021). Smart health system to detect dementia disorders using virtual reality. Healthcare (Switzerland), 9(7), 810. https://doi.org/10.3390/healthcare9070810CrossRef

Bellassen, V., Iglói, K., de Souza, L. C., Dubois, B., & Rondi-Reig, L. (2012). Temporal order memory assessed during spatiotemporal navigation as a behavioral cognitive marker for differential Alzheimer’s disease diagnosis. Journal of Neuroscience, 32(6), 1942–1952. https://doi.org/10.1523/JNEUROSCI.4556-11.2012CrossRefPubMed

Ben-sadoun, G., Manera, V., Alvarez, J., Sacco, G., Robert, P., Kuljiš, R. O., & García-betances, R. I. (2018). Recommendations for the design of serious games in neurodegenerative diseases. Frontiers in Aging Neuroscience, 10(February), 1–7. https://doi.org/10.3389/fnagi.2018.00013CrossRef

Bierbrauer, A., Kunz, L., Gomes, C. A., Luhmann, M., Deuker, L., Getzmann, S., Wascher, E., Gajewski, P. D., Hengstler, J. G., Fernandez-Alvarez, M., Atienza, M., Cammisuli, D. M., Bonatti, F., Pruneti, C., Percesepe, A., Bellaali, Y., Hanseeuw, B., Strange, B. A., Cantero, J. L., & Axmacher, N. (2020). Unmasking selective path integration deficits in Alzheimer’s disease risk carriers. Science Advances, 6(35). https://doi.org/10.1126/sciadv.aba1394

Bird, C. M., & Burgess, N. (2009). Spatial memory: Assessment in animals. In L. R. Squire (Ed.), Encyclopedia of Neuroscience (pp. 187–194). Elsevier. https://doi.org/10.1016/B978-008045046-9.00288-6

Boot, W. R. (2015). Video games as tools to achieve insight into cognitive processes. Frontiers in Psychology, 6(1), 1–3. https://doi.org/10.3389/fpsyg.2015.00003

Bossuyt, P. M., Reitsma, J. B., Bruns, D. E., Gatsonis, C. A., Glasziou, P. P., Irwig, L. M., Moher, D., Rennie, D., de Vet, H. C., Lijmer, J. G., & Standards for Reporting of Diagnostic Accuracy,. (2003). The STARD statement for reporting studies of diagnostic accuracy: Explanation and elaboration. Annals of Internal Medicine, 138(1), W1–W12. https://doi.org/10.7326/0003-4819-138-1-200301070-00012-w1CrossRefPubMed

Burgess, N. (2006). Spatial memory: How egocentric and allocentric combine. Trends in Cognitive Sciences, 10(12), 551–557. https://doi.org/10.1016/j.tics.2006.10.005CrossRefPubMed

Burgess, N., Spiers, H. J., & Paleologou, E. (2004). Orientational manoeuvres in the dark: Dissociating allocentric and egocentric influences on spatial memory. Cognition, 94(2), 149–166. https://doi.org/10.1016/j.cognition.2004.01.001CrossRefPubMed

Caffò, A. O., De Caro, M. F., Picucci, L., Notarnicola, A., Settanni, A., Livrea, P., Lancioni, G. E., & Bosco, A. (2012). Reorientation deficits are associated with amnestic mild cognitive impairment. American Journal of Alzheimer’s Disease and Other Dementias, 27(5), 321–330. https://doi.org/10.1177/1533317512452035CrossRefPubMed

Caffò, A. O., Lopez, A., Spano, G., Serino, S., Cipresso, P., Stasolla, F., Savino, M., Lancioni, G. E., Riva, G., & Bosco, A. (2018). Spatial reorientation decline in aging: The combination of geometry and landmarks. Aging and Mental Health, 22(10), 1372–1383. https://doi.org/10.1080/13607863.2017.1354973CrossRefPubMed

Campbell, Z., Zakzanis, K. K., Jovanovski, D., Joordens, S., Mraz, R., & Graham, S. J. (2009). Utilizing virtual reality to improve the ecological validity of clinical neuropsychology: An fMRI case study elucidating the neural basis of planning by comparing the Tower of London with a three-dimensional navigation task. Applied Neuropsychology, 16(4), 295–306. https://doi.org/10.1080/09084280903297891CrossRefPubMed

Carter, R., & Woldstad, J. (1985). Repeated measurements of spatial ability with the Manikin test. HUMAN FACTORS, 27(2), 209–219. https://doi.org/10.1177/001872088502700208CrossRefPubMed

Castegnaro, A., Howett, D., Li, A., Harding, E., Chan, D., Burgess, N., & King, J. (2022). Assessing mild cognitive impairment using object-location memory in immersive virtual environments. Hippocampus, 32(9), 660–678. https://doi.org/10.1002/hipo.23458CrossRefPubMedPubMedCentral

Chan, J. Y. C., Yau, S. T. Y., Kwok, T. C. Y., & Tsoi, K. K. F. (2021). Diagnostic performance of digital cognitive tests for the identification of MCI and dementia: A systematic review. Ageing Research Reviews, 72, 101506. https://doi.org/10.1016/j.arr.2021.101506CrossRefPubMed

Cipresso, P., Giglioli, I. A. C., Raya, M. A., & Riva, G. (2018). The past, present, and future of virtual and augmented reality research: A network and cluster analysis of the literature. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2018.02086CrossRefPubMedPubMedCentral

Cogné, M., Taillade, M., N’Kaoua, B., Tarruella, A., Klinger, E., Larrue, F., Sauzéon, H., Joseph, P. A., & Sorita, E. (2017). The contribution of virtual reality to the diagnosis of spatial navigation disorders and to the study of the role of navigational aids: A systematic literature review. Annals of Physical and Rehabilitation Medicine, 60(3), 164–176. https://doi.org/10.1016/j.rehab.2015.12.004CrossRefPubMed

Colmant, L., Bierbrauer, A., Bellaali, Y., Kunz, L., Van Dongen, J., Sleegers, K., Axmacher, N., Lefèvre, P., & Hanseeuw, B. (2023). Dissociating effects of aging and genetic risk of sporadic Alzheimer’s disease on path integration. Neurobiology of Aging, 131, 170–181. https://doi.org/10.1016/j.neurobiolaging.2023.07.025CrossRefPubMed

Colombo, D., Serino, S., Tuena, C., Pedroli, E., Dakanalis, A., Cipresso, P., & Riva, G. (2017). Egocentric and allocentric spatial reference frames in aging: A systematic review. Neuroscience and Biobehavioral Reviews, 80, 605–621. https://doi.org/10.1016/j.neubiorev.2017.07.012CrossRefPubMed

Coughlan, G., Coutrot, A., Khondoker, M., Minihane, A. M., Spiers, H., & Hornberger, M. (2019). Toward personalized cognitive diagnostics of at-genetic-risk Alzheimer’s disease. Proceedings of the National Academy of Sciences of the United States of America, 116(19), 9285–9292. https://doi.org/10.1073/pnas.1901600116ADSCrossRefPubMedPubMedCentral

Coughlan, G., Laczó, J., Hort, J., Minihane, A. M., & Hornberger, M. (2018). Spatial navigation deficits — Overlooked cognitive marker for preclinical Alzheimer disease? Nature Reviews Neurology, 14(8), 496–506. https://doi.org/10.1038/s41582-018-0031-xCrossRefPubMed

Coughlan, G., Puthusseryppady, V., Lowry, E., Gillings, R., Spiers, H., Minihane, A. M., & Hornberger, M. (2020). Test-retest reliability of spatial navigation in adults at-risk of Alzheimer’s disease. PLoS ONE, 15(9), e0239077. https://doi.org/10.1371/journal.pone.0239077CrossRefPubMedPubMedCentral

Coutrot, A., Silva, R., Manley, E., de Cothi, W., Sami, S., Bohbot, V. D., Wiener, J. M., Hölscher, C., Dalton, R. C., Hornberger, M., & Spiers, H. J. (2018). Global determinants of navigation ability. Current Biology, 28(17), 2861-2866.e4. https://doi.org/10.1016/j.cub.2018.06.009CrossRefPubMed

Da Costa, R. Q. M., Pompeu, J. E., Moretto, E., Silva, J. M., Dos Santos, M. D., Nitrini, R., & Brucki, S. M. D. (2022). Two immersive virtual reality tasks for the assessment of spatial orientation in older adults with and without cognitive impairment: Concurrent validity, group comparison, and accuracy results. Journal of the International Neuropsychological Society, 28(5), 460–472. https://doi.org/10.1017/S1355617721000655CrossRefPubMed

Davis, R., & Sikorskii, A. (2020). Eye tracking analysis of visual cues during wayfinding in early stage Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 49(1), 91–97. https://doi.org/10.1159/000506859CrossRefPubMed

delCacho-Tena, A., Christ, B. R., Arango-Lasprilla, J. C., Perrin, P. B., Rivera, D., & Olabarrieta-Landa, L. (2023). Normative data estimation in neuropsychological tests: A systematic review. Archives of Clinical Neuropsychology: The Official Journal of the National Academy of Neuropsychologists, 00, 1–16. https://doi.org/10.1093/arclin/acad084CrossRef

Deterding, S., Dixon, D., Khaled, R., & Nacke, L. (2011). From game design elements to gamefulness: Defining “gamification.” Proceedings of the 15th International Academic MindTrek Conference: Envisioning Future Media Environments, MindTrek 2011, 9–15. https://doi.org/10.1145/2181037.2181040

Diersch, N., & Wolbers, T. (2019). The potential of virtual reality for spatial navigation research across the adult lifespan. Journal of Experimental Biology, 222(Suppl_1). https://doi.org/10.1242/jeb.187252

Eichenbaum, H., & Cohen, N. J. (2014). Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron, 83(4), 764–770. https://doi.org/10.1016/j.neuron.2014.07.032CrossRefPubMedPubMedCentral

Epstein, R. A., Patai, E. Z., Julian, J. B., & Spiers, H. J. (2017). The cognitive map in humans: Spatial navigation and beyond. Nature Neuroscience, 20(11), 1504–1513. https://doi.org/10.1038/nn.4656CrossRefPubMedPubMedCentral

Fernandez-Baizan, C., Arias, J. L., & Mendez, M. (2020a). Spatial memory assessment reveals age-related differences in egocentric and allocentric memory performance. Behavioural Brain Research, 388, 112646. https://doi.org/10.1016/j.bbr.2020.112646CrossRefPubMed

Fernandez-Baizan, C., Diaz-Caceres, E., Arias, J. L., & Mendez, M. (2019). Egocentric and allocentric spatial memory in healthy aging: Performance on real-world tasks. Brazilian Journal of Medical and Biological Research, 52(4), 1–7. https://doi.org/10.1590/1414-431x20198041CrossRef

Fernandez-Baizan, C., Nuñez, P., Arias, J. L., & Mendez, M. (2020b). Egocentric and allocentric spatial memory in typically developed children: Is spatial memory associated with visuospatial skills, behavior, and cortisol? Brain and Behavior, 10(5), 1–14. https://doi.org/10.1002/brb3.1532CrossRef

Fuller, J. T., Cronin-golomb, A., Gatchel, J. R., Norton, D. J., Guzmán-vélez, E., Jacobs, H. I. L., Pardilla-delgado, E., Artola, A., Baena, A., Bocanegra, Y., Kosik, K., Chen, K., Tariot, P. N., Sperling, R. A., Reiman, E. M., Lopera, F., & Quiroz, Y. T. (2019). Biological and cognitive markers of presinilin1 e280a autosomal dominant Alzheimer’s disease: A comprehensive review of the Colombian kindred. The Journal of Prevention of Alzheimer´s Disease - JPAD, 6(2), 112–120. https://doi.org/10.14283/jpad.2019.6.BiologicalCrossRef

Gazova, I., Vlcek, K., Laczó, J., Nedelska, Z., Hyncicova, E., Mokrisova, I., Sheardova, K., & Hort, J. (2012). Spatial navigation—A unique window into physiological and pathological aging. Frontiers in Aging Neuroscience. https://doi.org/10.3389/fnagi.2012.00016CrossRefPubMedPubMedCentral

Gellersen, H. M., Coughlan, G., Hornberger, M., & Simons, J. S. (2021). Memory precision of object-location binding is unimpaired in APOE ϵ4-carriers with spatial navigation deficits. Brain Communications, 3(2). https://doi.org/10.1093/braincomms/fcab087

Goodroe, S. C., Starnes, J., & Brown, T. I. (2018). The complex nature of hippocampal-striatal interactions in spatial navigation. Frontiers in Human Neuroscience, 12, 250. https://doi.org/10.3389/fnhum.2018.00250CrossRefPubMedPubMedCentral

Hirtle, S. C. (2013). Models of spatial cognition. In D. Waller, & L. Nadel (Eds.), Handbook of spatial cognition (pp. 211–226). American Psychological Association.

Iachini, T., Iavarone, A., Senese, V. P., Ruotolo, F., & Ruggiero, G. (2009). Visuospatial Memory in Healthy Elderly AD and MCI: A Review., 2(1), 43–59. https://doi.org/10.2174/1874609810902010043CrossRef

Jack, C. R., Bennett, D. A., Blennow, K., Carrillo, M. C., Dunn, B., Budd Haeberlein, S., Holtzman, D. M., Jagust, W., Jessen, F., Karlawish, J., Liu, E., Molinuevo, J. L., Montine, T. J., Phelps, C. H., Rankin, K. P., Rowe, C. C., Scheltens, P., Siemers, E., Snyder, H. M., & Sperling, R. A. (2018). NIA-AA research framework: Toward a biological definition of Alzheimer’s disease. Alzheimer’s Dementia, 14(4), 535–562. https://doi.org/10.1016/j.jalz.2018.02.018.NIA-AACrossRefPubMed

Jacobs, L. F. (2003). Memory, spatial. In M. J. Aminoff, & R. B. Daroff (Eds.), Encyclopedia of the neurological sciences (pp. 86–90). Academic Press. https://doi.org/10.1016/B0-12-226870-9/01375-7

Kessels, R. P. C., Overbeek, A., & Bouman, Z. (2015). Assessment of verbal and visuospatial working memory in mild cognitive impairment and Alzheimer’s dementia. Dementia & Neuropsychologia, 9(3), 301–305. https://doi.org/10.1590/1980-57642015DN93000014CrossRef

Kessels, R. P. C., Van Den Berg, E., Ruis, C., & Brands, A. M. A. (2008). The backward span of the Corsi block-tapping task and its association with the WAIS-III digit span. Assessment, 15(4), 426–434. https://doi.org/10.1177/1073191108315611CrossRefPubMed

Kessels, R. P. C., Van Zandvoort, M. J. E., Postma, A., Jaap, L., De Haan, E. H. F., Kessels, R. P. C., Van Zandvoort, M. J. E., Postma, A., Jaap, L., Kessels, R. P. C., & Postma, A. (2010). The Corsi block-tapping task : Standardization and normative data. Applied Neuropsychology, 4282(7), 252–258. https://doi.org/10.1207/S15324826AN0704CrossRef

Knottnerus, J. A., & Buntinx, F. (2009). The evidence base of clinical diagnosis: Theory and methods of diagnostic research: Second edition. In The evidence base of clinical diagnosis: Theory and methods of diagnostic research: Second edition. https://doi.org/10.1002/9781444300574CrossRef

Kohn, M. A., Carpenter, C. R., & Newman, T. B. (2013). Understanding the direction of bias in studies of diagnostic test accuracy. Academic Emergency Medicine, 20(11), 1194–1206. https://doi.org/10.1111/acem.12255CrossRefPubMed

Kolarik, B., & Ekstrom, A. (2015). The neural underpinnings of spatial memory and navigation. In A. W. Toga (Ed.), Brain Mapping (pp. 507–514). Academic Press. https://doi.org/10.1016/B978-0-12-397025-1.00277-3

Konishi, K., Joober, R., Poirier, J., MacDonald, K., Chakravarty, M., Patel, R., Breitner, J., & Bohbot, V. D. (2018). Healthy versus entorhinal cortical atrophy identification in asymptomatic APOE4 carriers at risk for Alzheimer’s disease. Journal of Alzheimer’s Disease, 61(4), 1493–1507. https://doi.org/10.3233/JAD-170540CrossRefPubMedPubMedCentral

Krohn, S., Tromp, J., Quinque, E. M., Belger, J., Klotzsche, F., Rekers, S., Chojecki, P., de Mooij, J., Akbal, M., McCall, C., Villringer, A., Gaebler, M., Finke, C., & Thöne-Otto, A. (2020). Multidimensional evaluation of virtual reality paradigms in clinical neuropsychology: Application of the VR-Check framework. Journal of Medical Internet Research, 22(4), e16724. https://doi.org/10.2196/16724CrossRefPubMedPubMedCentral

Kunz, L., Brandt, A., Reinacher, P. C., Staresina, B. P., Reifenstein, E. T., Weidemann, C. T., Herweg, N. A., Patel, A., Tsitsiklis, M., Kempter, R., Kahana, M. J., Schulze-Bonhage, A., & Jacobs, J. (2021). A neural code for egocentric spatial maps in the human medial temporal lobe. Neuron, 109(17), 2781-2796.e10. https://doi.org/10.1016/j.neuron.2021.06.019CrossRefPubMedPubMedCentral

Kunz, L., Navarro Schröder, T., Lee, H., Montag, C., Lachmann, B., Sariyska, R., Reuter, M., Stirnberg, R., Stöcker, T., Messing-Floeter, P. C., Fell, J., Doeller, C. F., & Axmacher, N. (2015). Reduced grid-cell-like representations in adults at genetic risk for Alzheimer’s disease. Science, 350(6259), 430–433. https://doi.org/10.1126/science.aad1171ADSCrossRefPubMed

Laczó, J., Andel, R., Vyhnalek, M., Vlcek, K., Magerova, H., Varjassyova, A., Nedelska, Z., Gazova, I., Bojar, M., Sheardova, K., & Hort, J. (2012). From Morris water maze to computer tests in the prediction of Alzheimer’s disease. Neurodegenerative Diseases, 10(1–4), 153–157. https://doi.org/10.1159/000333121CrossRefPubMed

Laczó, J., Andel, R., Vyhnalek, M., Vlcek, K., Nedelska, Z., Matoska, V., Gazova, I., Mokrisova, I., Sheardova, K., & Hort, J. (2014). APOE and spatial navigation in Amnestic MCI: Results from a computer-based test. Neuropsychology, 28(5), 676–684. https://doi.org/10.1037/neu0000072CrossRefPubMed

Laczó, J., Parizkova, M., & Moffat, S. D. (2018). Spatial navigation, aging and Alzheimer’s disease. Aging, 10(11), 3050–3051. https://doi.org/10.18632/aging.101634CrossRefPubMedPubMedCentral

Laczó, M., Martinkovic, L., Lerch, O., Wiener, J. M., Kalinova, J., Matuskova, V., Nedelska, Z., Vyhnalek, M., Hort, J., & Laczó, J. (2022). Different profiles of spatial navigation deficits in Alzheimer’s disease biomarker-positive versus biomarker-negative older adults with amnestic mild cognitive impairment. Frontiers in Aging Neuroscience. https://doi.org/10.3389/fnagi.2022.886778CrossRefPubMedPubMedCentral

Laczó, M., Wiener, J. M., Kalinova, J., Matuskova, V., Vyhnalek, M., Hort, J., & Laczó, J. (2021). Spatial Navigation and Visuospatial Strategies in Typical and Atypical Aging. https://doi.org/10.3390/brainsciCrossRef

Latendorf, A., Runde, L. M., Salminen, T., & Steinert, A. (2021). Digitization of neuropsychological diagnostics: A pilot study to compare three paper-based and digitized cognitive assessments. Aging Clinical and Experimental Research, 33(6), 1585–1597. https://doi.org/10.1007/s40520-020-01668-zCrossRefPubMed

Lee, J., Kho, S., Yoo, H. B., Park, S., & Choi, J. (2014). Spatial memory impairments in amnestic mild cognitive impairment in a virtual radial arm maze. Neuropsychiatric Disease and Treatment, 10, 653–660. https://doi.org/10.2147/NDT.S58185CrossRefPubMedPubMedCentral

Lesk, V. E., Wan Shamsuddin, S. N., Walters, E. R., & Ugail, H. (2014). Using a virtual environment to assess cognition in the elderly. Virtual Reality, 18(4), 271–279. https://doi.org/10.1007/s10055-014-0252-2CrossRef

Lester, A. W., Moffat, S. D., Wiener, J. M., Barnes, C. A., & Wolbers, T. (2017). The aging navigational system. Neuron, 95(5), 1019–1035. https://doi.org/10.1016/j.neuron.2017.06.037CrossRefPubMedPubMedCentral

Levine, T. F., Allison, S. L., Stojanovic, M., Fagan, A. M., Morris, J. C., & Head, D. (2020). Spatial navigation ability predicts progression of dementia symptomatology. Alzheimer’s and Dementia, 16(3), 491–500. https://doi.org/10.1002/alz.12031CrossRefPubMed

Levy, B., Tsoy, E., & Gable, S. (2016). Developing cognitive markers of Alzheimer’s disease for primary care: Implications for behavioral and global prevention. Journal of Alzheimer’s Disease, 54(4), 1259–1272. https://doi.org/10.3233/JAD-160309CrossRefPubMed

Lewis, J. R. (2018). Measuring perceived usability: The CSUQ, SUS, and UMUX. International Journal of Human-Computer Interaction, 34(12), 1148–1156. https://doi.org/10.1080/10447318.2017.1418805CrossRef

Liu, Y., Chen, Y., & Chu, H. (2015). A unification of models for meta-analysis of diagnostic accuracy studies without a gold standard. Biometrics, 71(2), 538–547. https://doi.org/10.1111/biom.12264MathSciNetCrossRefPubMed

Lizio, R. (2020). Classification of Alzheimer’s disease dementia (ADD) by using features derived from resting‐state electroencephalography (rsEEG). Alzheimer’s & Dementia, 16(S4). https://doi.org/10.1002/alz.045816

Manera, V., Ben-sadoun, G., Aalbers, T., Agopyan, H., Askenazy, F., Benoit, M., Bensamoun, D., Bourgeois, J., Bredin, J., Bremond, F., Crispim-junior, C., & David, R. (2017). Recommendations for the use of serious games in neurodegenerative disorders: 2016 Delphi panel. Frontiers in Psychology, 8(July), 1–10. https://doi.org/10.3389/fpsyg.2017.01243CrossRef

Meneghini, R., & Packer, A. L. (2007). Is there science beyond English? EMBO Reports, 8(2), 112–116. https://doi.org/10.1038/sj.embor.7400906CrossRefPubMedPubMedCentral

Migo, E. M., O’Daly, O., Mitterschiffthaler, M., Antonova, E., Dawson, G. R., Dourish, C. T., Craig, K. J., Simmons, A., Wilcock, G. K., McCulloch, E., Jackson, S. H. D., Kopelman, M. D., Williams, S. C. R., & Morris, R. G. (2016). Investigating virtual reality navigation in amnestic mild cognitive impairment using fMRI. Neuropsychology, Development, and Cognition. Section B, Aging, Neuropsychology and Cognition, 23(2), 196–217. https://doi.org/10.1080/13825585.2015.1073218CrossRefPubMed

Mitolo, M., Gardini, S., Fasano, F., Crisi, G., & Pelosi, A. (2013). visuospatial memory and neuroimaging correlates in mild cognitive impairment. Journal o, 35, 75–90. https://doi.org/10.3233/JAD-121288CrossRef

Mohammadi, A., Kargar, M., & Hesami, E. (2018). Using virtual reality to distinguish subjects with multiple- but not single-domain amnestic mild cognitive impairment from normal elderly subjects. Psychogeriatrics, 18(2), 132–142. https://doi.org/10.1111/psyg.12301CrossRefPubMed

Mokkink, L. B., Prinsen, C. A. C., Patrick, D. L., Alonso, J., Bouter, L. M., de Vet, H. C. W., & Terwee, C. B. (2019). COSMIN study design checklist for patient-reported outcome measurement instruments. Department of Epidemiology and Biostatistics Amsterdam Public Health Research Institute Amsterdam University Medical Centers, Location VUmc, July, 1–32. Retrieved October 11, 2022, from www.cosmin.nl

Mokkink, L. B., de Vet, H. C. W., Prinsen, C. A. C., Patrick, D. L., Alonso, J., Bouter, L. M., & Terwee, C. B. (2018). COSMIN risk of bias checklist for systematic reviews of patient-reported outcome measures. Quality of Life Research: An International Journal of Quality of Life Aspects of Treatment, Care and Rehabilitation, 27(5), 1171–1179. https://doi.org/10.1007/s11136-017-1765-4CrossRefPubMed

Molina da Costa, R. Q., Pompeu, J. E., Pereire de Viveiro, L. A., & Dozzi Brucki, S. M. (2020). Spatial orientation tasks show moderate to high accuracy for the diagnosis of mild cognitive impairment: A systematic literature review. Arquivos De Neuro-Psiquiatria, 78, 713–723. https://doi.org/10.1590/0004-282X20200043CrossRef

Morganti, F., Stefanini, S., & Riva, G. (2013). From allo- to egocentric spatial ability in early Alzheimer’s disease: A study with virtual reality spatial tasks. Cognitive Neuroscience, 4(3–4), 171–180. https://doi.org/10.1080/17588928.2013.854762CrossRefPubMed

Morrison, G. E., Simone, C. M., Ng, N. F., Hardy, J. L., & Morrison, G. E. (2015). Reliability and validity of the NeuroCognitive Performance Test, a web-based neuropsychological assessment. Frontiers in psychology, 6(November), 1–15. https://doi.org/10.3389/fpsyg.2015.01652CrossRef

Motes, M. A., Finlay, G. A., & Kozhevnikov, M. (2006). Scene recognition following locomotion around a scene. Perception, 35(11), 1507–1520. https://doi.org/10.1068/p5459CrossRefPubMed

Moussavi, Z., Kimura, K., & Lithgow, B. (2022). Egocentric spatial orientation differences between Alzheimer’s disease at early stages and mild cognitive impairment: A diagnostic aid. Medical and Biological Engineering and Computing, 60(2), 501–509. https://doi.org/10.1007/s11517-021-02478-9CrossRefPubMed

Nedelska, Z., Andel, R., Laczó, J., Vlcek, K., Horinek, D., Lisy, J., Sheardova, K., Bureš, J., & Hort, J. (2012). Spatial navigation impairment is proportional to right hippocampal volume. Proceedings of the National Academy of Sciences of the United States of America, 109(7), 2590–2594. https://doi.org/10.1073/pnas.1121588109ADSCrossRefPubMedPubMedCentral

Nguyen, K. V., Tansan, M., & Newcombe, N. S. (2023). Studying the development of navigation using virtual environments. Journal of Cognition and Development, 24(1), 1–16. https://doi.org/10.1080/15248372.2022.2133123CrossRefPubMed

Noel-Storr, A. H., McCleery, J. M., Richard, E., Ritchie, C. W., Flicker, L., Cullum, S. J., Davis, D., Quinn, T. J., Hyde, C., Rutjes, A. W. S., Smailagic, N., Marcus, S., Black, S., Blennow, K., Brayne, C., Fiorivanti, M., Johnson, J. K., Köpke, S., Schneider, L. S., ... & McShane, R. (2014). Reporting standards for studies of diagnostic test accuracy in dementia: The STARDdem Initiative. Neurology, 83(4), 364–373. https://doi.org/10.1212/WNL.0000000000000621CrossRefPubMedPubMedCentral

O’Keefee, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Clarendon Press.

Ouzzani, M., Hammady, H., Fedorowicz, Z., & Elmagarmid, A. (2016). Rayyan-a web and mobile app for systematic reviews. Systematic Reviews, 5(1), 1–10. https://doi.org/10.1186/s13643-016-0384-4CrossRef

Pan, Z., Cheok, A. D., Yang, H., Zhu, J., & Shi, J. (2006). Virtual reality and mixed reality for virtual learning environments. Computers and Graphics (pergamon), 30(1), 20–28. https://doi.org/10.1016/j.cag.2005.10.004CrossRef

Parizkova, M., Lerch, O., Moffat, S. D., Andel, R., Mazancova, A. F., Nedelska, Z., Vyhnalek, M., Hort, J., & Laczó, J. (2018). The effect of Alzheimer’s disease on spatial navigation strategies. Neurobiology of Aging, 64, 107–115. https://doi.org/10.1016/j.neurobiolaging.2017.12.019CrossRefPubMed

Park, J. H. (2022). Can the virtual reality-based spatial memory test better discriminate mild cognitive impairment than neuropsychological assessment? International Journal of Environmental Research and Public Health, 19(16). https://doi.org/10.3390/ijerph19169950

Pepe, M. S. (2003). The statistical evaluation of medical tests for classification and prediction (Oxford Sta). Oxford University Press.CrossRef

Pieper, D., & Puljak, L. (2021). Language restrictions in systematic reviews should not be imposed in the search strategy but in the eligibility criteria if necessary. Journal of Clinical Epidemiology, 132, 146–147. https://doi.org/10.1016/j.jclinepi.2020.12.027CrossRefPubMed

Pink, D., Ilkel, E., Chandreswaran, V., Moser, D., Getzmann, S., Patrick, G., Axmacher, N., & Zhang, H. (2023). Modeling the impact of genotype, age, sex, and continuous navigation on pathway integration performance. BioRxiv. https://doi.org/10.1101/2023.09.11.556925CrossRefPubMedPubMedCentral

Plaza-Rosales, I., Brunetti, E., Montefusco-Siegmund, R., Madariaga, S., Hafelin, R., Ponce, D. P., Behrens, M. I., Maldonado, P. E., & Paula-Lima, A. (2023). Visual-spatial processing impairment in the occipital-frontal connectivity network at early stages of Alzheimer’s disease. Frontiers in Aging Neuroscience. https://doi.org/10.3389/fnagi.2023.1097577CrossRefPubMedPubMedCentral

Poos, J. M., van der Ham, I. J. M., Leeuwis, A. E., Pijnenburg, Y. A. L., van der Flier, W. M., & Postma, A. (2021). Short digital spatial memory test detects impairment in Alzheimer’s disease and mild cognitive impairment. Brain Sciences, 11(10), 1350. https://doi.org/10.3390/brainsci11101350CrossRefPubMedPubMedCentral

Potashman, M., Pang, M., Tahir, M., Shahraz, S., Dichter, S., Perneczky, R., & Nolte, S. (2023). Psychometric properties of the Alzheimer’s Disease Cooperative Study – Activities of Daily Living for Mild Cognitive Impairment (ADCS-MCI-ADL) scale: A post hoc analysis of the ADCS ADC-008 trial. BMC Geriatrics, 23(1). https://doi.org/10.1186/s12877-022-03527-0

Prinsen, C. A. C., Mokkink, L. B., Bouter, L. M., Alonso, J., Patrick, D. L., de Vet, H. C. W., & Terwee, C. B. (2018). COSMIN guideline for systematic reviews of patient-reported outcome measures. Quality of Life Research : An International Journal of Quality of Life Aspects of Treatment, Care and Rehabilitation, 27(5), 1147–1157. https://doi.org/10.1007/s11136-018-1798-3CrossRefPubMed

Puthusseryppady, V., Morrissey, S., Spiers, H., Patel, M., & Hornberger, M. (2022). Predicting real world spatial disorientation in Alzheimer’s disease patients using virtual reality navigation tests. Scientific Reports, 12(1). https://doi.org/10.1038/s41598-022-17634-w

Ribordy, F., Jabès, A., Banta, P., & Lavenex, P. (2013). Development of allocentric spatial memory abilities in children from 18 months to 5 years of age. Cognitive Psychology, 66(1), 1–29. https://doi.org/10.1016/j.cogpsych.2012.08.001CrossRefPubMed

Ritchie, K., Carrière, I., Howett, D., Su, L., Hornberger, M., O’Brien, J. T., Ritchie, C. W., & Chan, D. (2018). Allocentric and egocentric spatial processing in middle-aged adults at high risk of late-onset Alzheimer’s disease: The PREVENT dementia study. Journal of Alzheimer’s Disease, 65(3), 885–896. https://doi.org/10.3233/JAD-180432CrossRefPubMed

Ruggiero, G., Iavarone, A., & Iachini, T. (2018). Allocentric to egocentric spatial switching: Impairment in aMCI and Alzheimer’s disease patients? Current Alzheimer Research, 15, 229–236. https://doi.org/10.2174/1567205014666171030114821CrossRefPubMed

Sabbagh, M. N., & Blennow, K. (2019). Peripheral biomarkers for Alzheimer’s disease: Update and progress. Neurology and Therapy, 8(S2), 33–36. https://doi.org/10.1007/s40120-019-00171-6CrossRefPubMedPubMedCentral

Sacco, G., Ben-Sadoun, G., Bourgeois, J., Fabre, R., Manera, V., & Robert, P. (2019). Comparison between a paper-pencil version and computerized version for the realization of a neuropsychological test: The example of the trail making test. Journal of Alzheimer’s Disease, 68(4), 1657–1666. https://doi.org/10.3233/JAD-180396CrossRefPubMed

Sackett, D. L., & Haynes, R. B. (2002). The architecture of diagnostic research. BMJ, 324(7336), 539–541. https://doi.org/10.1136/bmj.324.7336.539CrossRefPubMedPubMedCentral

Sauro, J., & Lewis, J. R. (2012). Quantifying the user experience: Practical statistics for user research. Elsevier Inc.

Schöberl, F., Pradhan, C., Irving, S., Buerger, K., Xiong, G., Kugler, G., Kohlbecher, S., Engmann, J., Werner, P., Brendel, M., Schneider, E., Perneczky, R., Jahn, K., la Fougère, C., Bartenstein, P., Brandt, T., Dieterich, M., & Zwergal, A. (2020). Real-space navigation testing differentiates between amyloid-positive and -negative aMCI. Neurology, 94(8), e861–e873. https://doi.org/10.1212/WNL.0000000000008758CrossRefPubMed

Sepulveda-Falla, D., Glatzel, M., & Lopera, F. (2012). Phenotypic profile of early-onset familial Alzheimer’s disease caused by presenilin-1 E280A mutation. Journal of Alzheimer’s Disease, 32(1), 1–12. https://doi.org/10.3233/JAD-2012-120907CrossRefPubMed

Serino, S., Morganti, F., Colombo, D., & Riva, G. (2018). The contribution of allocentric impairments to the cognitive decline in Alzheimer’s disease. Lecture Notes of the Institute for Computer Sciences, Social-Informatics and Telecommunications Engineering, LNICST, 253, 84–91. https://doi.org/10.1007/978-3-030-01093-5_11CrossRef

Serino, S., Morganti, F., Di Stefano, F., & Riva, G. (2015). Detecting early egocentric and allocentric impairments deficits in Alzheimer’s disease: An experimental study with virtual reality. Frontiers in Aging Neuroscience, 7, 1–10. https://doi.org/10.3389/fnagi.2015.00088CrossRef

Sijtsma, K. (2009). On the use, the misuse, and the very limited usefulness of Cronbach’s alpha. Psychometrika, 74(1), 107–120. https://doi.org/10.1007/s11336-008-9101-0MathSciNetCrossRefPubMed

Silva, J. M. D., dos Santos, M. D., da Costa, R. Q. M., Moretto, E. G., de Viveiro, L. A. P., de Lopes, R. D., Brucki, S. M. D., & Pompeu, J. E. (2023). Applicability of an immersive virtual reality system to assess egocentric orientation of older adults. Arquivos De Neuro-Psiquiatria, 81(01), 019–026. https://doi.org/10.1055/s-0042-1759762CrossRef

Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., Iwatsubo, T., Jack, C. R., Kaye, J., Montine, T. J., Park, D. C., Reiman, E. M., Rowe, C. C., Siemers, E., Stern, Y., Yaffe, K., Carrillo, M. C., Thies, B., Morrison-bogorad, M., ... & Phelps, C. H. (2011). Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’ s disease. Alzheimer’s & Dementia, 7(3), 280–292. https://doi.org/10.1016/j.jalz.2011.03.003CrossRef

Sperling, R., Mormino, E., & Johnson, K. (2014). The evolution of preclinical Alzheimer’s disease: Implications for prevention trials. Neuron, 84(3), 608–622. https://doi.org/10.1016/j.neuron.2014.10.038CrossRefPubMedPubMedCentral

Tarnanas, I., Laskaris, N., & Tsolaki, M. (2012). On the comparison of VR-responses, as performance measures in prospective memory, with auditory P300 responses in MCI detection. Studies in Health Technology and Informatics, 181, 156–161.PubMed

Tarnanas, I., Papagiannopoulos, S., Kazis, D., Wiederhold, M., Widerhold, B., Vuillermot, S., & Tsolaki, M. (2015). Reliability of a novel serious game using dual-task gait profiles to early characterize aMCI. Frontiers in Aging Neuroscience. https://doi.org/10.3389/fnagi.2015.00050CrossRefPubMedPubMedCentral

Terwee, C. B., Prinsen, C. A. C., Chiarotto, A., Westerman, M. J., Patrick, D. L., Alonso, J., Bouter, L. M., de Vet, H. C. W., & Mokkink, L. B. (2018). COSMIN methodology for evaluating the content validity of patient-reported outcome measures: A Delphi study. Quality of Life Research: An International Journal of Quality of Life Aspects of Treatment, Care and Rehabilitation, 27(5), 1159–1170. https://doi.org/10.1007/s11136-018-1829-0CrossRefPubMed

Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55(4), 189–208. https://doi.org/10.1037/h0061626CrossRefPubMed

Tong, T., Chignell, M., Lam, P., Tierney, M. C., & Lee, J. (2014). Designing serious games for cognitive assessment of the elderly. Proceedings of the International Symposium on Human Factors and Ergonomics in Health Care, 3(1), 28–35. https://doi.org/10.1177/2327857914031004CrossRef

Tong, T., Chignell, M., Tierney, M. C., Lee, J., & Tong, T. (2016). A serious game for clinical assessment of cognitive status: Validation study. JMIR Serious Games, 4(1), 1–14. https://doi.org/10.2196/games.5006CrossRef

Tuena, C., Mancuso, V., Stramba-Badiale, C., Pedroli, E., Stramba-Badiale, M., Riva, G., & Repetto, C. (2021). Egocentric and allocentric spatial memory in mild cognitive impairment with real-world and virtual navigation tasks: A systematic review. Journal of Alzheimer’s Disease, 79(1), 95–116. https://doi.org/10.3233/JAD-201017CrossRefPubMedPubMedCentral

Vasilyeva, M. (2005). Spatial cognition and perception. In K. Kempf-Leonard (Ed.), Encyclopedia of social measurement (Vol. 3, pp. 591–597). Elsevier Academic Press.

Vasser, M., Kängsepp, M., Magomedkerimov, M., Kilvits, K., Stafinjak, V., Kivisik, T., Vicente, R., & Aru, J. (2017). VREX: An open-source toolbox for creating 3D virtual reality experiments. BMC Psychology, 5(1), 4. https://doi.org/10.1186/s40359-017-0173-4CrossRefPubMedPubMedCentral

Ventura, M., Shute, V., Wright, T., & Zhao, W. (2013). An investigation of the validity of the virtual spatial navigation assessment. Frontiers in Psychology. https://doi.org/10.3389/fpsyg.2013.00852CrossRefPubMedPubMedCentral

Vingerhoets, G., Lannoo, E., & Bauwens, S. (1996). Analysis of the money road-map test performance in normal and brain-damaged subjects. Archives of Clinical Neuropsychology, 11(1), 9. https://doi.org/10.1016/0887-6177(95)00055-0CrossRef

Vlcek, K., & Laczó, J. (2014). Neural correlates of spatial navigation changes in mild cognitive impairment and Alzheimer’s disease. Frontiers in Behavioral Neuroscience, 8, 1–6. https://doi.org/10.3389/fnbeh.2014.00089CrossRef

Wiener, J. M., Carroll, D., Moeller, S., Bibi, I., Ivanova, D., Allen, P., & Wolbers, T. (2020). A novel virtual-reality-based route-learning test suite: Assessing the effects of cognitive aging on navigation. Behavior Research Methods, 52(2), 630–640. https://doi.org/10.3758/s13428-019-01264-8CrossRefPubMed

Winters, M., & Weir, A. (2017). Grey matters; on the importance of publication bias in systematic reviews. British Journal of Sports Medicine, 51(6), 488–489. https://doi.org/10.1136/bjsports-2016-096679CrossRefPubMed

Zen, D., Byagowi, A., Garcia, M., Kelly, D., Lithgow, B., & Moussavi, Z. (2013, November). The perceived orientation in people with and without Alzheimer's. In 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER) (pp. 460–463). IEEE. https://doi.org/10.1109/ner.2013.6695971

Zheng, J. M., Chan, K. W., & Gibson, I. (1998). Virtual reality. IEEE Potentials, 17(2), 20–23. https://doi.org/10.1109/45.666641CrossRef

Zucchella, C., Sinforiani, E., Tassorelli, C., Cavallini, E., Tost-Pardell, D., Grau, S., Pazzi, S., Puricelli, S., Bernini, S., Bottiroli, S., Vecchi, T., Sandrini, G., & Nappi, G. (2014). Serious games for screening pre-dementia conditions: From virtuality to reality? A pilot project. Functional Neurology, 29(3), 153–158. https://doi.org/10.11138/FNeur/2014.29.3.153CrossRefPubMed

Title: Virtual Reality and Serious Videogame-Based Instruments for Assessing Spatial Navigation in Alzheimer’s Disease: A Systematic Review of Psychometric Properties
Authors: Juan Pablo Sánchez-Escudero
Ana María Galvis-Herrera
David Sánchez-Trujillo
Laura Cristina Torres-López
Cole J. Kennedy
Daniel Camilo Aguirre-Acevedo
Mauricio A. Garcia-Barrera
Natalia Trujillo
Publication date: 26-02-2024
Publisher: Springer US
Keywords: Alzheimer's Disease
Alzheimer's Disease
Mild Neurocognitive Disorder
Published in: Neuropsychology Review
Print ISSN: 1040-7308
Electronic ISSN: 1573-6660
DOI: https://doi.org/10.1007/s11065-024-09633-7

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Virtual Reality and Serious Videogame-Based Instruments for Assessing Spatial Navigation in Alzheimer’s Disease: A Systematic Review of Psychometric Properties

Abstract

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Abstract

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