Dynamics of Changes in the Level of Cognitive Functioning Among Patients After SARS-CoV-2 Infection ‒ A Proposal for Remote Neuropsychological Assessment in a Longitudinal Study
Ewa Malinowska
University of Warsaw, Faculty of Psychologyhttps://orcid.org/0000-0002-0881-1401
Dominika Żarnecka
University of Warsaw, Faculty of Psychologyhttps://orcid.org/0000-0002-4026-3900
Emilia Łojek
University of Warsaw, Faculty of Psychologyhttps://orcid.org/0000-0002-0809-5601
NeuroCovid Research Team
based at the the Faculty of Psychology of the University of WarsawAbstrakt
Study purpose: The aim of this longitudinal study was to assess the cognitive functioning of people who had COVID-19, to determine the dynamics of changes observed in this area over a period of 3‒4 months, to compare the patients' results with those of a control group, and to verify the usefulness of a new method of remote neuropsychological assessment.
Method: A longitudinal study was conducted using the Brief Test of Adult Cognition by Telephone (BTACT) neuropsychological assessment tool, which was translated into Polish for the purpose of the study. The study included subjects following SARS-CoV-2 infection (COVID(+) group) and control subjects (COVID(‒) group). Cognitive functions in both groups were assessed twice, 3‒4 months apart. The study was conducted from July 2020 to January 2022.
Results: Data comparisons were performed using mixed ANOVA with repeated measures. Compared to the COVID(‒) group, the COVID(+) group scored significantly lower on the first and second measurements of the Backward Digit Span Test and on the first measurement of the Number Series Test. Additionally, an improvement was observed in COVID(+) group scores in the second measurement compared to the first measurement in: Rey Auditory-Verbal Learning Test (RAVLT) in both the immediate and delayed recall condition; the Backward Digit Span Test, the Number Series Test and 30 Seconds and Counting Task (30-SACT).
Conclusions: The obtained results show an impairment in working memory functions and inductive reasoning in COVID(+) subjects compared to COVID(‒) subjects. In addition, the study indicates the usefulness of BTACT in tracking the changes in cognitive functioning over time in individuals following SARS-CoV-2 infection. Tests to assess working memory (Rey Auditory-Verbal Learning Test (RAVLT), Backward Digit Span Test) and a test of inductive reasoning (Number Series Test) appear to be particularly useful in monitoring the mentioned changes.
Słowa kluczowe:
COVID-19, long-COVID, cognitive functions, neuropsychological assessment, remote testing methodsBibliografia
Adjaye-Gbewonyo, D., Vahratian, A., Perrine, C. G., & Bertolli, J. (2023). Long COVID in Adults: United States. 2022. NCHS Data Brief, 480, 1–8. https://dx.doi.org/10.15620/cdc:132417
Crossref
Google Scholar
Almeria, M., Cejudo, J. C., Sotoca, J., Deus, J., & Krupinski, J. (2020). Cognitive profile following COVID-19 infection: Clinical predictors leading to neuropsychological impairment. Brain, Behavior, & Immunity – Health, 9, article 100163. https://doi.org/10.1016/j.bbih.2020.100163
Crossref
Google Scholar
Atkins, A. S., Kraus, M. S., Welch, M., Yuan, Z., Stevens, H., Welsh-Bohmer, K. A., & Keefe, R. S. (2022). Remote self-administration of digital cognitive tests using the Brief Assessment of Cognition: Feasibility, reliability, and sensitivity to subjective cognitive decline. Frontiers in Psychiatry, 13, article 910896. https://doi.org/10.3389/fpsyt.2022.910896
Crossref
Google Scholar
Barcellos, L. F., Horton, M., Shao, X., Bellesis, K. H., Chinn, T., Waubant, E., Bakshi, N., Marcus, J., Benedict, R. H., & Schaefer, C. (2021). A validation study for remote testing of cognitive function in multiple sclerosis. Multiple Sclerosis Journal, 27(5), 795–798. https://doi.org/10.1177/1352458520937385
Crossref
Google Scholar
Biagianti, B., Di Liberto, A., Nicolò Edoardo, A., Lisi, I., Nobilia, L., de Ferrabonc, G. D, Zanier, E. R., Stocchetti, N., & Brambilla, P. (2022). Cognitive assessment in SARS-CoV-2 patients: A systematic review. Frontiers in Aging Neuroscience, 14, article 909661. https://doi.org/10.3389/fnagi.2022.909661
Crossref
Google Scholar
Bianchetti, A., Ferrara, N., Padovani, A., Scarpini, E., Trabucchi, M., & Maggi, S. (2019). Timely Detection of Mild Cognitive Impairment in Italy: An Expert Opinion. Journal of Alzheimer's Disease, 68(4), 1401–1414. https://doi.org/10.3233/JAD-181253
Crossref
Google Scholar
Bloch, A., Maril, S., & Kavé, G. (2021). How, when, and for whom: decisions regarding remote neuropsychological assessment during the 2020 COVID-19 pandemic. Israel Journal of Health Policy Research, 10(1), article 31. https://doi.org/10.1186/s13584-021-00465-x
Crossref
Google Scholar
Boldrini, M., Canoll, P. D., & Klein, R. S. (2021). How COVID-19 Affects the Brain. JAMA Psychiatry, 78(6), 682–683. https://doi.org/10.1001/jamapsychiatry.2021.0500
Crossref
Google Scholar
Borkowski, J. G., Benton, A. L., & Spreen, O. (1967). Word fluency and brain damage. Neuropsychologia, 5(2), 135–140. https://doi.org/10.1016/0028-3932(67)90015-2
Crossref
Google Scholar
Brearly, T. W., Shura, R. D., Martindale, S. L., Lazowski, R. A., Luxton, D. D., Shenal, B. V., & Rowland, J. A. (2017). Neuropsychological Test Administration by Videoconference: A Systematic Review and Meta-Analysis. Neuropsychology Review, 27(2), 174–186. https://doi.org/10.1007/s11065-017-9349-1
Crossref
Google Scholar
Carlew, A. R., Fatima, H., Livingstone, J. R., Reese, C., Lacritz, L., Pendergrass, C., Bailey, K. C., Presley, C., Mokhtari, B., & Cullum, C. M. (2020). Cognitive Assessment via Telephone: A Scoping Review of Instruments. Archives of Clinical Neuropsychology, 35(8), 1215–1233. https://doi.org/10.1093/arclin/acaa096
Crossref
Google Scholar
Crook, H., Raza, S., Nowell, J., Young, M., & Edison, P. (2021). Long covid-mechanisms, risk factors, and management. British Medical Journal, 374, article n1648. https://doi.org/10.1136/bmj.n1648
Crossref
Google Scholar
Cysique, L. A., Łojek, E., Ching-Kong Cheung, T., Cullen, B., Egbert, A. R., Evans, J., Garolera, M., Gawron, N., Gouse, H., Hansen, K., Holas, P., Hyniewska, S., Malinowska, E., Marcopulos, B. A., Merkley, T. L., Muñoz-Moreno, J. A., Ramsden, C., Salas, C., Sikkes, S. A. M., … the NeuroCOVID International Neuropsychology Taskforce. (2021). Assessment of neurocognitive functions, olfaction, taste, mental, and psychosocial health and COVID-19 in adults: Recommendations for harmonization of research and implications for clinical practice. Journal of International Neuropsychological Society, 28(6), 642–660. https://doi.org/10.1017/S1355617721000862
Crossref
Google Scholar
Davis, H. E., McCorkell, L., Vogel, J. M., & Topol, E. J. (2023). Author Correction: Long COVID: major findings, mechanisms and recommendations. Nature Reviews. Microbiology, 21(6), 133–146. https://doi.org/10.1038/s41579-023-00896-0
Crossref
Google Scholar
Del Brutto, O. H., Wu, S., Mera, R. M., Costa, A. F., Recalde, B. Y., & Issa, N. P. (2021). Cognitive decline among individuals with history of mild symptomatic SARS-CoV-2 infection: A longitudinal prospective study nested to a population cohort. European Journal of Neurology, 28(10), 3245–3253. https://doi.org/10.1111/ene.14775
Crossref
Google Scholar
Egbert, A. R., Cankurtaran, S., & Karpiak, S. (2020). Brain abnormalities in COVID-19 acute/subacute phase: A rapid systematic review. Brain, Behavior, and Immunity, 89, 543–554. https://doi.org/10.1016/j.bbi.2020.07.014
Crossref
Google Scholar
Frontera, J. A., Yang, D., Lewis, A., Patel, P., Medicherla, C., Arena, V., Fang, T., Andino, A., Snyder, T., Madhavan, M., Gratch, D., Fuchs, B., Dessy, A., Canizares, M., Jauregui, R., Thomas, B., Bauman, K., Olivera, A., Bhagat, D., … Galetta, S. (2021). A prospective study of long-term outcomes among hospitalized COVID-19 patients with and without neurological complications. Journal of the Neurological Sciences, 426, article 117486. https://doi.org/10.1016/j.jns.2021.117486
Crossref
Google Scholar
Helms, J., Kremer, S., Merdji, H., Clere-Jehl, R., Schenck, M., Kummerlen, C., Collange, O., Boulay, C., Fafi-Kremer, S., Ohana, M., Anheim, M., & Meziani, F. (2020). Neurologic Features in Severe SARS-CoV-2 Infection. The New England Journal of Medicine, 382(23), 2268–2270. https://doi.org/10.1056/NEJMc2008597
Crossref
Google Scholar
Heneka, M. T., Golenbock, D., Latz, E., Morgan, D., & Brown, R. (2020). Immediate and long-term consequences of COVID-19 infections for the development of neurological disease. Alzheimer's Research & Therapy, 12(1), article 69. https://doi.org/10.1186/s13195-020-00640-3
Crossref
Google Scholar
Klein, J., Wood, J., Jaycox, J. R., Dhodapkar, R. M., Lu, P., Gehlhausen, J. R., Tabachnikova, A., Greene, K., Tabacof, L., Malik, A. A., Silva Monteiro, V., Silva, J., Kamath, K., Zhang, M., Dhal, A., Ott, I. M., Valle, G., Peña-Hernández, M., Mao, T., … Iwasaki, A. (2023). Distinguishing features of long COVID identified through immune profiling. Nature, 623(7985), 139–148. https://doi.org/10.1038/s41586-023-06651-y
Crossref
Google Scholar
Lachman, M. E., Agrigoroaei, S., Tun, P. A., & Weaver, S. L. (2014). Monitoring cognitive functioning: psychometric properties of the brief test of adult cognition by telephone. Assessment, 21(4), 404–417. https://doi.org/10.1177/1073191113508807
Crossref
Google Scholar
Lee, M. H., Perl, D. P., Steiner, J., Pasternack, N., Li, W., Maric, D., Safavi, F., Horkayne-Szakaly, I., Jones, R., Stram, M. N., Moncur, J. T., Hefti, M., Folkerth, R. D., & Nath, A. (2022). Neurovascular injury with complement activation and inflammation in COVID-19. Brain: A Journal of Neurology, 145(7), 2555–2568. https://doi.org/10.1093/brain/awac151
Crossref
Google Scholar
Malinowska, W., Żarnecka, D., Wyszomirska, J., Hyniewska, S., Filon, M., Łojek, E., Zespół Badawczy NeuroCovid Wydziału Psychologii Uniwersytetu Warszawskiego. (2022). Nowe wyzwania dla neuropsychologii klinicznej: studia przypadku osób zakażonych wirusem SARS-CoV-2 [New challenges for clinical neuropsychology: Case studies of people infected with SARS-C]. In M. Gambin & B. Zawadzki (Eds.), Pandemia COVID-19. Perspektywa psychologiczna [COVID-19 pandemic: A psychological perspective] (pp. 205–232). Wydawnictwo Liberi Libri. https://doi.org/10.47943/lib.9788363487607.rozdzial07
Crossref
Google Scholar
Michael, B. D., Dunai, C., Needham, E. J., Tharmaratnam, K., Williams, R., Huang, Y., Boardman, S. A., Clark, J. J., Sharma, P., Subramaniam, K., Wood, G. K., Collie, C., Digby, R., Ren, A., Norton, E., Leibowitz, M., Ebrahimi, S., Fower, A., Fox, H., Tato, E., … Menon, D. K. (2023). Para-infectious brain injury in COVID-19 persists at follow-up despite attenuated cytokine and autoantibody responses. Nature Communications, 14, article 8487. https://doi.org/10.1038/s41467-023-42320-4
Crossref
Google Scholar
Michael, B., Wood, G., Sargent, B., Ahmad, Z., Tharmaratnam, K., Dunai, C., Egbe, F., Martin, N., Facer, B., Pendered, S., Rogers, H., Hübel, Ch., van Wamelen, D., Bethlehem, R., Giunchiglia, V., Hellyer, P., Trender, W., Kalsi, G., Needham, E., ... Leek, C. (2024). Post-COVID cognitive deficits at one year are global and associated with elevated brain injury markers and grey matter volume reduction: national prospective study. Research Square, 14, article 8487. https://doi.org/10.21203/rs.3.rs-3818580/v1
Crossref
Google Scholar
Moreno-Pérez, O., Merino, E., Leon-Ramirez, J. M., Andres, M., Ramos, J. M., Arenas-Jiménez, J., Asensio, S., Sanchez, R., Ruiz-Torregrosa, P., Galan, I., Scholz, A., Amo, A., González-delaAleja, P., Boix, V., Gil, J., & COVID19-ALC research group. (2021). Post-acute COVID-19 syndrome. Incidence and risk factors: A Mediterranean cohort study. The Journal of Infection, 82(3), 378–383. https://doi.org/10.1016/j.jinf.2021.01.004
Crossref
Google Scholar
Ortelli, P., Ferrazzoli, D., Sebastianelli, L., Engl, M., Romanello, R., Nardone, R., Bonini, I., Koch, G., Saltuari, L., Quartarone, A., Oliviero, A., Kofler, M., & Versace, V. (2021). Neuropsychological and neurophysiological correlates of fatigue in post-acute patients with neurological manifestations of COVID-19: Insights into a challenging symptom. Journal of the Neurological Sciences, 420, article 117271. https://doi.org/10.1016/j.jns.2020.117271
Crossref
Google Scholar
Parlar, M. E., Spilka, M. J., Wong Gonzalez, D., Ballantyne, E. C., Dool, C., Gojmerac, C., King, J., McNeely, H., & MacKillop, E. (2020). “You can't touch this”: Delivery of inpatient neuropsychological assessment in the era of COVID-19 and beyond. The Clinical Neuropsychologist, 34(7–8), 1395–1410. https://doi.org/10.1080/13854046.2020.1810324
Crossref
Google Scholar
Raman, B., Cassar, M. P., Tunnicliffe, E. M., Filippini, N., Griffanti, L., Alfaro-Almagro, F., Okell, T., Sheerin, F., Xie, C., Mahmod, M., Mózes, F. E., Lewandowski, A. J., Ohuma, E. O., Holdsworth, D., Lamlum, H., Woodman, M. J., Krasopoulos, C., Mills, R., McConnell, F. A. K., … Neubauer, S. (2021). Medium-term effects of SARS-CoV-2 infection on multiple vital organs, exercise capacity, cognition, quality of life and mental health, post-hospital discharge. eClinicalMedicine, 31, article 100683. https://doi.org/10.1016/j.eclinm.2020.100683
Crossref
Google Scholar
Rapp, S. R., Legault, C., Espeland, M. A., Resnick, S. M., Hogan, P. E., Coker, L. H., Dailey, M., Shumaker, S. A., & CAT Study Group. (2012). Validation of a Cognitive Assessment Battery Administered over the Telephone. Journal of the American Geriatrics Society, 60(9), 1616–1623. https://doi.org/10.1111/j.1532-5415.2012.04111.x
Crossref
Google Scholar
Rasika, S., Nogueiras, R., Schwaninger, M., & Prevot, V. (2024). Seeing through the fog: a neuroendocrine explanation for post-COVID cognitive deficits. Nature Reviews Endocrinology, 20(4), 189‒190. https://doi.org/10.1038/s41574-024-00955-3
Crossref
Google Scholar
Rey, A. (1964). L'examen clinique en psychologie. Presses Universitaries De France. Google Scholar
Salthouse, T. A., & Prill, K. A. (1987). Inferences about age impairments in inferential reasoning. Psychology and Aging, 2(1), 43–51. https://doi.org/10.1037/0882-7974.2.1.43
Crossref
Google Scholar
Savarraj, J. P. J., Burkett, A. B., Hinds, S. N., Paz, A. S., Assing, A., Juneja, S., Colpo, G. D., Torres, L. F., Cho, S. M., Gusdon, A. M., McCullough, L. D., & Choi, H. A. (2021). Pain and Other Neurological Symptoms Are Present at 3 Months After Hospitalization in COVID-19 Patients. Frontiers in Pain Research, 16(2), article 737961. https://doi.org/10.3389/fpain.2021.737961
Crossref
Google Scholar
Schaie, K. W. (1996). Intellectual development in adulthood: The Seattle Longitudinal Study. Cambridge University Press. Google Scholar
Smith, P. J., Need, A. C., Cirulli, E. T., Chiba-Falek, O., & Attix, D. K. (2013). A comparison of the Cambridge Automated Neuropsychological Test Battery (CANTAB) with "traditional" neuropsychological testing instruments. Journal of Clinical and Experimental Neuropsychology, 35(3), 319–328. https://doi.org/10.1080/13803395.2013.771618
Crossref
Google Scholar
Sozzi, M., Algeri, L., Corsano, M., Crivelli, D., Daga, M. A., Fumagalli, F., Gemignani, P., Granieri, M. C., Inzaghi, M. G., Pala, F., Turati, S., & Balconi, M. (2020). Neuropsychology in the Times of COVID-19. The Role of the Psychologist in Taking Charge of Patients With Alterations of Cognitive Functions. Frontiers in Neurology, 11, article 573207. https://doi.org/10.3389/fneur.2020.573207
Crossref
Google Scholar
Sumpter, R., Camsey, E., Meldrum, S., Alford, M., Campbell, I., Bois, C., O'Connell, S., & Flood, J. (2023). Remote neuropsychological assessment: Acceptability and feasibility of direct-to-home teleneuropsychology methodology during the COVID-19 pandemic. The Clinical Neuropsychologist, 37(2), 432–47. https://doi.org/10.1080/13854046.2022.2056922
Crossref
Google Scholar
Takakura, Y., Otsuki, M., Takagi, R., & Houkin, K. (2023). A validation study for wide-range remote assessment of cognitive functions in the healthy older Japanese population: a pilot randomised crossover trial. BMC Geriatrics, 23, article 575. https://doi.org/10.1186/s12877-023-04275-5
Crossref
Google Scholar
Tomasoni, D., Bai, F., Castoldi, R., Barbanotti, D., Falcinella, C., Mulè, G., Mondatore, D., Tavelli, A., Vegni, E., Marchetti, G., & d'Arminio Monforte, A. (2021). Anxiety and depression symptoms after virological clearance of COVID-19: A cross-sectional study in Milan, Italy. Journal of Medical Virology, 93(2), 1175–1179. https://doi.org/10.1002/jmv.26459
Crossref
Google Scholar
Webb, S. S., Kontou, E., & Demeyere, N. (2022). The COVID-19 pandemic altered the modality, but not the frequency, of formal cognitive assessment. Disability and Rehabilitation, 44(21), 6365–6373. https://doi.org/10.1080/09638288.2021.1963855
Crossref
Google Scholar
Wechsler, D. (1997). Wechsler Adult Intelligence Scale-III (WAIS-III) manual. The Psychological Corporation.
Crossref
Google Scholar
Whiteside, D. M., Oleynick, V., Holker, E., Waldron, E. J., Porter, J., & Kasprzak, M. (2021). Neurocognitive deficits in severe COVID-19 infection: Case series and proposed model. The Clinical Neuropsychologist, 35(4), 799–818. https://doi.org/10.1080/13854046.2021.1874056
Crossref
Google Scholar
WHO (World Health Organization). (2023). Clinical management of COVID-19: living guideline. Reference number: WHO/2019-nCoV/clinical/2023.2. https://www.who.int/publications/i/item/WHO-2019-nCoV-clinical-2023.2 Google Scholar
WHO (World Health Organization) Data. WHO COVID-19 dashboard. https://data.who.int/dashboards/covid19/cases?n=c Google Scholar
Woo, M. S., Malsy, J., Pöttgen, J., Seddiq Zai, S., Ufer, F., Hadjilaou, A., Schmiedel, S., Addo, M. M., Gerloff, C., Heesen, C., Schulze Zur Wiesch, J., & Friese, M. A. (2020). Frequent neurocognitive deficits after recovery from mild COVID-19. Brain Communications, 2(2), article fcaa205. https://doi.org/10.1093/braincomms/fcaa205
Crossref
Google Scholar
Yong, S. J. (2021). Persistent Brainstem Dysfunction in Long-COVID: A Hypothesis. ACS Chemical Neuroscience, 12(4), 573–580. https://doi.org/10.1021/acschemneuro.0c00793
Crossref
Google Scholar
Zhao, S., Martin, E. M., Reuken, P. A., Scholcz, A., Ganse-Dumrath, A., Srowig, A., Utech, I., Kozik, V., Radscheidt, M., Brodoehl, S., Stallmach, A., Schwab, M., Fraser, E., Finke, K., & Husain, M. (2024). Long COVID is associated with severe cognitive slowing: a multicentre cross-sectional study. eClinicalMedicine, 68, article 102434. https://doi.org/10.1016/j.eclinm.2024.102434
Crossref
Google Scholar
based at the the Faculty of Psychology of the University of Warsaw
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