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 Psychologiihttps://orcid.org/0000-0002-0881-1401
Dominika Żarnecka
Uniwersytet Warszawski, Wydział Psychologiihttps://orcid.org/0000-0002-4026-3900
Emilia Łojek
Uniwersytet Warszawski, Wydział Psychologiihttps://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 testoweReferences
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
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