The dynamics of change of cognitive functioning in patients after SARS-CoV-2 infection – proposal of a remote neuropsychological assessment in a longitudinal study

Ewa Malinowska

Uniwersytet Warszawski, Wydział Psychologii
https://orcid.org/0000-0002-0881-1401

Dominika Żarnecka

Uniwersytet Warszawski, Wydział Psychologii
https://orcid.org/0000-0002-4026-3900

Emilia Łojek

Uniwersytet Warszawski, Wydział Psychologii
https://orcid.org/0000-0002-0809-5601

Zespół Badawczy NeuroCovid Wydziału Psychologii Uniwersytetu Warszawskiego




Abstract

Cel: Celem przeprowadzonego badania podłużnego była ocena funkcjonowania poznawczego osób, które chorowały na COVID-19, określenie dynamiki zmian obserwowanych w tym zakresie na przestrzeni 3‒4 miesięcy, porównanie wyników pacjentów z wynikami grupy kontrolnej oraz weryfikacja przydatności nowej metody zdalnej oceny neuropsychologicznej.

Metoda: Przeprowadzono badanie podłużne z wykorzystaniem narzędzia do telefonicznej oceny neuropsychologicznej Brief Test of Adult Cognition by Telephone (BTACT), które na potrzeby badania przetłumaczono na język polski. Badanie objęło osoby po infekcji SARS-CoV-2 (grupa COVID(+) oraz osoby z grupy kontrolnej (COVID(‒). Obie grupy zostały przebadane dwukrotnie, w odstępie 3‒4 miesięcy. Badanie prowadzono od lipca 2020 do stycznia 2022 roku.

Wyniki: Przeprowadzono porównania danych z wykorzystaniem analizy wariancji dla pomiarów powtarzanych w schemacie mieszanym. W porównaniu z grupą COVID(‒) grupa COVID(+) uzyskała istotnie niższe wyniki w pierwszym i w drugim pomiarze Testu powtarzania liczb wspak oraz w pierwszym pomiarze w Teście ciągu liczb. Dodatkowo zaobserwowano poprawę w wynikach uzyskiwanych przez grupę COVID(+) w drugim pomiarze w porównaniu z pierwszym pomiarem w: Teście 15 słów Reya, zarówno w warunku natychmiastowego, jak i odroczonego odtworzenia; Teście powtarzania liczb wspak, Teście ciągu liczb oraz w Teście liczenia wspak.

Konkluzja: Uzyskane wyniki wskazują na obniżenie funkcji pamięci roboczej oraz wnioskowania indukcyjnego u osób z grupy COVID(+) w porównaniu z grupą COVID(‒). Dodatkowo przeprowadzone badanie wskazuje na przydatność BTACT w śledzeniu zmiany poziomu funkcjonowania poznawczego w czasie u osób po infekcji SARS-CoV-2. Szczególnie pomocne w monitorowaniu wspomnianych zmian wydają się testy służące ocenie pamięci operacyjnej (Test 15 słów Reya, Test powtarzania liczb wspak) oraz test wnioskowania indukcyjnego (Test ciągu liczb).


Keywords:

COVID-19, long-COVID, funkcje poznawcze, ocena neuropsychologiczna, zdalne metody testowe


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   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, artykuł 100163. https://doi.org/10.1016/j.bbih.2020.100163   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, artykuł 910896. https://doi.org/10.3389/fpsyt.2022.910896   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   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, artykuł 909661. https://doi.org/10.3389/fnagi.2022.909661   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   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), artykuł 31. https://doi.org/10.1186/s13584-021-00465-x   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   Google Scholar

Borkowski, J. G., Benton, A. L., Spreen, O. (1967). Word fluency and brain damage. Neuropsychologia, 5, 135–140. https://doi.org/10.1016/0028-3932(67)90015-2   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   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   Google Scholar

Crook, H., Raza, S., Nowell, J., Young, M., Edison, P. (2021). Long covid-mechanisms, risk factors, and management. British Medical Journal, 374, artykuł n1648. https://doi.org/10.1136/bmj.n1648   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   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   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   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   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, artykuł 117486. https://doi.org/10.1016/j.jns.2021.117486   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   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), artykuł 69. https://doi.org/10.1186/s13195-020-00640-3   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   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   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   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. W: M. Gambin i B. Zawadzki (red.), Pandemia COVID-19. Perspektywa psychologiczna (s. 205–232). Wydawnictwo Liberi Libri. https://doi.org/10.47943/lib.9788363487607.rozdzial07   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, artykuł 8487. https://doi.org/10.1038/s41467-023-42320-4   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. https://doi.org/10.21203/rs.3.rs-3818580/v1   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   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, artykuł 117271. https://doi.org/10.1016/j.jns.2020.117271   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   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, artykuł 100683. https://doi.org/10.1016/j.eclinm.2020.100683   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   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   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   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), artykuł 737961. https://doi.org/10.3389/fpain.2021.737961   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   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, artykuł 573207. https://doi.org/10.3389/fneur.2020.573207   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   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, artykuł 575. https://doi.org/10.1186/s12877-023-04275-5   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   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   Google Scholar

Wechsler, D. (1997). Wechsler Adult Intelligence Scale-III (WAIS-III) manual. The Psychological Corporation.   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   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), artykuł fcaa205. https://doi.org/10.1093/braincomms/fcaa205   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   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, artykuł 102434. https://doi.org/10.1016/j.eclinm.2024.102434   Google Scholar


Published
2024-06-27

Cited by

Malinowska, E., Żarnecka, D., Łojek, E., & Zespół Badawczy NeuroCovid Wydziału Psychologii Uniwersytetu Warszawskiego. (2024). The dynamics of change of cognitive functioning in patients after SARS-CoV-2 infection – proposal of a remote neuropsychological assessment in a longitudinal study. The Review of Psychology, 67(1), 27–43. https://doi.org/10.31648/przegldpsychologiczny.9509

Ewa Malinowska 
Uniwersytet Warszawski, Wydział Psychologii
https://orcid.org/0000-0002-0881-1401
Dominika Żarnecka 
Uniwersytet Warszawski, Wydział Psychologii
https://orcid.org/0000-0002-4026-3900
Emilia Łojek 
Uniwersytet Warszawski, Wydział Psychologii
https://orcid.org/0000-0002-0809-5601
Zespół Badawczy NeuroCovid Wydziału Psychologii Uniwersytetu Warszawskiego