Hostname: page-component-7c8c6479df-fqc5m Total loading time: 0 Render date: 2024-03-29T10:08:45.174Z Has data issue: false hasContentIssue false

Neurocognitive Outcome Following Recovery from Severe Acute Respiratory Syndrome – Coronavirus-1 (SARS-CoV-1)

Published online by Cambridge University Press:  07 September 2021

Farena S. Pinnock*
Affiliation:
Neuropsychology & Cognitive Health, Baycrest Health Sciences, Toronto, ON, Canada
Jill B. Rich
Affiliation:
Neuropsychology & Cognitive Health, Baycrest Health Sciences, Toronto, ON, Canada Department of Psychology, York University, Toronto, ON, Canada
Brandon Vasquez
Affiliation:
Neuropsychology & Cognitive Health, Baycrest Health Sciences, Toronto, ON, Canada Department of Occupational Science & Occupational Therapy, University of Toronto, Toronto, ON, Canada
Melanie Wiegand
Affiliation:
Department of Psychology, York University, Toronto, ON, Canada
John Patcai
Affiliation:
Department of Medicine, University of Toronto, Toronto, ON, Canada Department of Medicine, McMaster University, Hamilton, ON, Canada
Angela K. Troyer
Affiliation:
Neuropsychology & Cognitive Health, Baycrest Health Sciences, Toronto, ON, Canada Department of Psychology, University of Toronto, Toronto, ON, Canada
Kelly J. Murphy
Affiliation:
Neuropsychology & Cognitive Health, Baycrest Health Sciences, Toronto, ON, Canada Department of Psychology, University of Toronto, Toronto, ON, Canada
*
*Correspondence and reprint requests to: Farena Pinnock, PhD, Neuropsychology & Cognitive Health, Baycrest Health Sciences, 3560 Bathurst St, North York, ONM6A 2E1, Canada. Email: fpinnock@baycrest.org

Abstract

Objective:

Severe acute respiratory syndrome (SARS) is a highly contagious viral respiratory illness associated with hypoxia and dyspnea. Many of those who contracted and recovered from SARS during the 2002–2003 outbreak reported persistent physical, psychological, and cognitive difficulties. Here, we investigated the residual influences of SARS on cognition for a subset of healthcare professionals who recovered and were referred for neuropsychological evaluation through their workplace insurance.

Method:

Twenty-eight healthcare professionals were evaluated on neuropsychological and mood functioning approximately 1.5 years post-recovery from a severe respiratory illness. Test scores were compared with age-matched normative data, and correlations were examined between mood, self-report memory scales, subjective complaints (e.g., poor concentration, pain, fatigue), illness severity (i.e., length of hospitalization, oxygen use during hospital stay), and cognitive performance.

Results:

Participants performed within age expectations on the majority of cognitive measures including overall memory ability. Although processing speed was generally within normal limits, 43% showed significant speed–accuracy trade-offs favoring accuracy over maintaining speed. Deficits were observed on measures of complex attention, such as working memory and the ability to sustain attention under conditions of distraction. Participants endorsed poorer memory ability than same-age peers on a meta-memory measure and mild to moderate depression and anxiety symptoms. Objective test performance was largely uncorrelated with self-reports, mood, or illness severity, except for moderate correlations between complex attention and participants’ subjective ratings of Everyday Task-Oriented Memory.

Conclusions:

These findings demonstrate specific long-term cognitive deficits associated with SARS and provide further evidence of the cognitive effects of hypoxic illnesses.

Type
Research Article
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adhikari, N.K., Tansey, C.M., McAndrews, M.P., Matté, A., Pinto, R., Cheung, A.M., … Herridge, M.S. (2011). Self-reported depressive symptoms and memory complaints in survivors five years after ARDS. Chest, 140(6), 14841493. https://doi.org/10.1378/chest.11-1667 CrossRefGoogle ScholarPubMed
Beck, A.T. & Steer, R.A. (1993). Beck Anxiety Inventory manual. San Antonio: The Psychological Corporation.Google Scholar
Beck, A.T., Steer, R.A., & Brown, G.K. (1996). Beck Depression Inventory-II . San Antonio: The Psychological Corporation, 78, 490498.Google Scholar
Bohmwald, K., Gálvez, N.M.S., Ríos, M., & Kalergis, A.M. (2018). Neurologic alterations due to respiratory virus infections. In Frontiers in Cellular Neuroscience (Vol. 12). Frontiers Media S.A. https://doi.org/10.3389/fncel.2018.00386 CrossRefGoogle Scholar
Burmester, B., Leathem, J., & Merrick, P. (2016). Subjective cognitive complaints and objective cognitive function in aging: A systematic review and meta-analysis of recent cross-sectional findings. Neuropsychology Review, 26(4), 376393.CrossRefGoogle ScholarPubMed
Butler, D. (2015). South Korean MERS outbreak is not a global threat. Nature. https://www.nature.com/news/south-korean-mers-outbreak-is-not-a-global-threat-1.17709. Accessed 5 Jul 2016.Google Scholar
Centers for Disease Control and Prevention (2003). Public Health Guidance for Community-Level Preparedness and Response to Severe Acute Respiratory Syndrome (SARS) Draft–October 2003.Google Scholar
Chan, J.C.K. (2005). Recovery pathway of post-SARS patients. Thorax, 60, 361.CrossRefGoogle ScholarPubMed
Chen, J., Wu, J., Hao, S., Yang, M., Lu, X., Chen, X., & Li, L. (2017). Long term outcomes in survivors of epidemic Influenza A (H7N9) virus infection. Scientific Reports, 7(1), 18. https://doi.org/10.1038/s41598-017-17497-6 CrossRefGoogle ScholarPubMed
Chen, T.B., Lin, C.Y., Lin, K.N., Yeh, Y.C., Chen, W.T., Wang, K.S., & Wang, P.N. (2014). Culture qualitatively but not quantitatively influences performance in the Boston Naming Test in a Chinese-speaking population. Dementia and Geriatric Cognitive Disorders Extra, 4, 8694.CrossRefGoogle ScholarPubMed
Cole, W.R. & Bailie, J.M. (2016). Neurocognitive and psychiatric symptoms following mild traumatic brain injury. In Laskowitz, D. & Grant, G. (Eds.), Translational Research in Traumatic Brain Injury (Chapter 19). Boca Raton: CRC Press/Taylor and Francis Group.Google ScholarPubMed
Crook, T.H., & Larrabee, G.J. (1990). A self-rating scale for evaluating memory in everyday life. Psychology and Aging, 5, 4857.CrossRefGoogle Scholar
Delis, D.C., Kaplan, E., & Kramer, J.H. (2001). Delis-Kaplan executive function system (D-KEFS). San Antonio: Psychological Corporation.Google Scholar
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (1987). California Verbal Learning Test (CVLT). San Antonio: The Psychological Corporation.Google Scholar
Gardner, P.J. & Moallef, P. (2015). Psychological impact on SARS survivors: Critical review of the English language literature. Canadian Psychology, 56, 123135.CrossRefGoogle Scholar
Greenberg, G.D., Watson, R.K., & Deptula, D. (1987). Neuropsychological dysfunction in sleep apnea. Sleep, 10, 254–62.CrossRefGoogle ScholarPubMed
Gronwall, D.M. (1977). Paced auditory serial-addition task: a measure of recovery from concussion. Perceptual and Motor Skills, 44, 367373.CrossRefGoogle ScholarPubMed
Henri-Bhargava, A., Stuss, D.T., & Freedman, M. (2018). Clinical assessment of prefrontal lobe functions. CONTINUUM: Lifelong Learning in Neurology, 24(3), 704726.Google ScholarPubMed
Herridge, M.S., Cheung, A.M., Tansey, C.M., Matte-Martyn, A., Diaz-Granados, N., Al-Saidi, F., … Slutsky, A.S. (2003). One-year outcomes in survivors of the acute respiratory distress syndrome. The New England Journal of Medicine, 348, 683693.CrossRefGoogle ScholarPubMed
Higgins, D.M., Martin, A.M., Baker, D.G., Vasterling, J.J., & Risbrough, V. (2018). The relationship between chronic pain and neurocognitive function: a systematic review. The Clinical Journal of Pain, 34(3), 262.CrossRefGoogle ScholarPubMed
Hilgenfeld, R. & Peiris, M. (2013). From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses. Antiviral Research, 100, 286295.CrossRefGoogle ScholarPubMed
Hopkins, R.O., Larson-Lohr, V., Weaver, L.K., & Bigler, E.D. (1998). Neuropsychological impairments following hantavirus pulmonary syndrome. Journal of the International Neuropsychological Society, 4, 190196.CrossRefGoogle ScholarPubMed
Hopkins, R.O., Weaver, L.K., Collingridge, D., Parkinson, R.B., Chan, K.J., & Orme, J.F. (2005) Two-year cognitive, emotional, and quality-of-life outcomes in acute respiratory distress syndrome. American Journal of Respiratory and Critical Care Medicine, 171, 340347.CrossRefGoogle ScholarPubMed
Irani, F., Barbone, J.M., Beausoleil, J., & Gerald, L. (2017). Is asthma associated with cognitive impairments? A meta-analytic review. Journal of Clinical and Experimental Neuropsychology, 24, 14.Google Scholar
Kamps, B.S. & Hoffman, C. (2004). SARS Reference. http://www.sarsreference.com. Accessed 4 Jan 2016.Google Scholar
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). The Boston Naming Test. Philadelphia: Lea & Febiger.Google Scholar
Kim, J. S. (2016). Post-stroke mood and emotional disturbances: pharmacological therapy based on mechanisms. Journal Stroke, 18, 244.CrossRefGoogle Scholar
Kwek, S.K., Chew, W.M., Ong, K.C., Ng, A.W.K., Lee, L.S.U., Kaw, G., & Leow, M.K.S. (2006). Quality of life and psychological status in survivors of severe acute respiratory syndrome at 3 months postdischarge. Journal of Psychosomatic Research, 60, 513519.CrossRefGoogle ScholarPubMed
Lam, M.H.B., Wing, Y.K., Yu, M.W.M., Leung, C.M., Ma, R.C., Kong, A.P., … Lam, S.P. (2009) Mental morbidities and chronic fatigue in severe acute respiratory syndrome survivors: long-term follow-up. Archives of Internal Medicine, 169, 21422147.CrossRefGoogle ScholarPubMed
Lezak, M.D. (2012). Neuropathology for Neuropsychologists. In Neuropsychological assessment (Fifth edition). New York: Oxford University Press.Google Scholar
Luyt, C.E., Combes, A., Becquemin, M.H., Beigelman-Aubry, C., Hatem, S., Brun, A.L., … Chastre, J. (2012). Long-term outcomes of pandemic 2009 influenza A(H1N1)-associated severe ARDS. Chest, 142(3), 583592. https://doi.org/10.1378/chest.11-2196 CrossRefGoogle ScholarPubMed
Mak, I.W.C., Chu, C.M., Pan, P.C., Yiu, M.G.C., & Chan, V.L. (2009). Long-term psychiatric morbidities among SARS survivors. General Hospital Psychiatry, 31(4), 318326. https://doi.org/10.1016/j.genhosppsych.2009.03.001 CrossRefGoogle ScholarPubMed
Mariën, P., Mampaey, E., Vervaet, A., Saerens, J., & De Deyn, P.P. (1998). Normative data for the Boston Naming Test in native Dutch-speaking Belgian elderly. Brain and language, 65(3), 447467.CrossRefGoogle ScholarPubMed
Marshall, M. (2020). The lasting misery of coronavirus long-haulers. Nature, 585(7825), 339341.CrossRefGoogle ScholarPubMed
Maunder, R.G., Lancee, W.J., Balderson, K.E., Bennett, J.P., Borgundvaag, B., Evans, S., … Wasylenki, D.A. (2006). Long-term psychological and occupational effects of providing hospital healthcare during SARS outbreak. Emerging Infectious Diseases, 12, 19241932.CrossRefGoogle ScholarPubMed
McMorris, T., Hale, B.J., Barwood, M., Costello, J., & Corbett, J. (2017). Effect of acute hypoxia on cognition: A systematic review and meta-regression analysis. Neuroscience & Biobehavioral Reviews, 74, 225232.CrossRefGoogle ScholarPubMed
Mikkelsen, M.E., Christie, J.D., Lanken, P.N., Biester, R.C., Thompson, B.T., Bellamy, S.L., … Angus, D.C. (2012). The adult respiratory distress syndrome cognitive outcomes study: long-term neuropsychological function in survivors of acute lung injury. American Journal of Respiratory and Critical Care Medicine, 185, 13071315.CrossRefGoogle ScholarPubMed
Moallef, P., Lueke, N.A., Gardner, P.J., & Patcai, J. (2021). Chronic PTSD and other psychological sequelae in a group of frontline healthcare workers who contracted and survived SARS. Canadian Journal of Behavioural Science/Revue Canadienne des Sciences du Comportement.CrossRefGoogle Scholar
Moldofsky, H., & Patcai, J. (2011). Chronic widespread musculoskeletal pain, fatigue, depression and disordered sleep in chronic post-SARS syndrome; A case-controlled study. BMC Neurology, 11, 37.CrossRefGoogle ScholarPubMed
Muller, M.P., Richardson, S.E., McGeer, A., Dresser, L., Raboud, J., Mazzulli, T., … Louie, M. (2006). Early diagnosis of SARS: lessons from the Toronto SARS outbreak. European Journal of Clinical Microbiology and Infectious Diseases, 25, 230237.CrossRefGoogle ScholarPubMed
Naylor, D., Basrur, S., Bergeron, M.G., Brunham, R.C., Butler-Jones, D., & Dafoe, G. (2003). Chapter 2 - SARS in Canada: Anatomy of an Outbreak. In National Advisory Committee on SARS and Public Health. Learning from SARS: renewal of public health in Canada (pp. 2342). Ottawa: Health Canada. http://www.phac-aspc.gc.ca/publicat/sars-sras/naylor/. Accessed 5 Jul 2016.Google Scholar
Negrini, F., Ferrario, I., Mazziotti, D., Berchicci, M., Bonazzi, M., de Sire, A., … Zapparoli, L. (2020). Neuropsychological features of severe hospitalized COVID-19 patients at clinical stability and clues for post-acute rehabilitation. Archives of Physical Medicine and Rehabilitation. https://doi.org/10.1016/j.apmr.2020.09.376 CrossRefGoogle Scholar
Ngai, J.C., Ko, F.W., Ng, S.S., To, K.W., Tong, M., & Hui, D.S. (2010). The long-term impact of severe acute respiratory syndrome on pulmonary function, exercise capacity and health status. Respirology, 15, 543550.CrossRefGoogle ScholarPubMed
O’Farrell, E., MacKenzie, J., & Collins, B. (2013). Clearing the air: a review of our current understanding of “chemo fog”. Current Oncology Reports, 15, 260269.CrossRefGoogle ScholarPubMed
Ownsworth, T. & McKenna, K. (2004). Investigation of factors related to employment outcome following traumatic brain injury: A critical review and conceptual model. Disability and Rehabilitation, 26(13), 765784.CrossRefGoogle ScholarPubMed
Rabinovitz, B., Jaywant, A., & Fridman, C. B. (2020). Neuropsychological functioning in severe acute respiratory disorders caused by the coronavirus: implications for the current COVID-19 pandemic. Clinical Neuropsychologist. https://doi.org/10.1080/13854046.2020.1803408 CrossRefGoogle Scholar
Riordan, P., Stika, M., Goldberg, J., & Drzewiecki, M. (2020). COVID-19 and clinical neuropsychology: A review of neuropsychological literature on acute and chronic pulmonary disease. In Clinical Neuropsychologist. Routledge. https://doi.org/10.1080/13854046.2020.1810325 Google Scholar
Ritchie, K., Chan, D., & Watermeyer, T. (2020). The cognitive consequences of the COVID-19 epidemic: collateral damage? Brain Communications, 2(2). https://doi.org/10.1093/braincomms/fcaa069 CrossRefGoogle Scholar
Roberts, P.M. & Doucet, N. (2011). Performance of French-speaking Quebec adults on the Boston Naming Test. Canadian Journal of Speech-Language Pathology & Audiology, 35(3), 254–267.Google Scholar
Robertson, I.H., Ward, T., Ridgeway, V., & Nimmo-Smith, I. (1994). The Test of Everyday Attention (TEA). San Antonio: Psychological Corporation.Google Scholar
Rock, P.L., Roiser, J.P., Riedel, W.J., & Blackwell, A.D. (2014). Cognitive impairment in depression: a systematic review and meta-analysis. Psychological Medicine, 44(10), 2029.CrossRefGoogle ScholarPubMed
Rogers, J.P., Chesney, E., Oliver, D., Pollak, T.A., McGuire, P., Fusar-Poli, P., … David, A.S. (2020). Psychiatric and neuropsychiatric presentations associated with severe coronavirus infections: a systematic review and meta-analysis with comparison to the COVID-19 pandemic. The Lancet Psychiatry, 7(7), 611627. https://doi.org/10.1016/S2215-0366(20)30203-0 CrossRefGoogle ScholarPubMed
Rosenzweig, I., Glasser, M., Polsek, D., Leschziner, G.D., Williams, S.C., & Morrell, M.J. (2015). Sleep apnoea and the brain: a complex relationship. The Lancet Respiratory Medicine, 3(5), 404414.CrossRefGoogle ScholarPubMed
Ruff, R.M., Niemann, H., Allen, C.C., Farrow, C.E., & Wylie, T. (1992). The Ruff 2 and 7 selective attention test: a neuropsychological application. Perceptual and Motor Skills, 75, Suppl 3, 13111319.CrossRefGoogle ScholarPubMed
Schou, L., Østergaard, B., Rasmussen, L.S., Rydahl-Hansen, S., & Phanareth, K. (2012). Cognitive dysfunction in patients with chronic obstructive pulmonary disease–a systematic review. Respiratory Medicine, 106, 10711081.CrossRefGoogle ScholarPubMed
Schultz, I.Z., Sepehry, A.A., & Greer, S.C. (2018). Anoxia-Hypoxia in Forensic Neuropsychological Assessment: Cognitive Impact of Pulmonary Injuries, Respiratory Distress, Cerebral Blood Hypoperfusion, and Major Surgeries. Psychological Injury and Law, 11, 118.CrossRefGoogle Scholar
Schwartz, E.S., Erdodi, L., Rodriguez, N., Ghosh, J.J., Curtain, J.R., Flashman, L.A., & Roth, R.M. (2016). CVLT-II forced choice recognition trial as an embedded validity indicator: A systematic review of the evidence. Journal of the International Neuropsychological Society: JINS, 22(8), 851.CrossRefGoogle Scholar
Sforza, E. & Roche, F. (2012). Sleep apnea syndrome and cognition. Frontiers in Neurology, 3, 87. doi 10.3389/fneur.2012.00087 CrossRefGoogle ScholarPubMed
Sheng, B., Cheng, S.K.W., Lau, K.K., Li, H.L., & Chan, E.L.Y. (2005). The effects of disease severity, use of corticosteroids and social factors on neuropsychiatric complaints in severe acute respiratory syndrome (SARS) patients at acute and convalescent phases. European Psychiatry, 20, 236242.CrossRefGoogle ScholarPubMed
Stern, R.A., Singer, E.A., Duke, L.M., Singer, N.G., Morey, C.E., Daughtrey, E.W., & Kaplan, E. (1994). The Boston qualitative scoring system for the Rey-Osterrieth Complex Figure: Description and interrater reliability. The Clinical Neuropsychologist, 8, 309322.CrossRefGoogle Scholar
Stranks, E.K. & Crowe, S.F. (2016). The cognitive effects of obstructive sleep apnea: an updated meta-analysis. Archives of Clinical Neuropsychology, 31, 186193.Google ScholarPubMed
Stuss, D.T. (2006). Frontal lobes and attention: processes and networks, fractionation and integration. Journal of the International Neuropsychological Society: JINS, 12(2), 261.CrossRefGoogle Scholar
Stuss, D.T. (2011). Functions of the frontal lobes: relation to executive functions. Journal of the International Neuropsychological Society: JINS, 17(5), 759.CrossRefGoogle ScholarPubMed
Stuss, D.T., Peterkin, I., Guzman, D.A., Guzman, C., & Troyer, A.K. (1997). Chronic obstructive pulmonary disease: effects of hypoxia on neurological and neuropsychological measures. Journal of Clinical and Experimental Neuropsychology, 19(4), 515524.CrossRefGoogle ScholarPubMed
Suhr, J.A. (2003). Neuropsychological impairment in fibromyalgia: relation to depression, fatigue, and pain. Journal of Psychosomatic Research, 55, 321329.CrossRefGoogle Scholar
Tallberg, I.M. (2005). The Boston naming test in Swedish: normative data. Brain and Language, 94(1), 1931.CrossRefGoogle ScholarPubMed
Thakur, N., Blanc, P.D., Julian, L.J., Yelin, E.H., Katz, P.P., Sidney, S., … Eisner, M.D. (2010). COPD and cognitive impairment: the role of hypoxemia and oxygen therapy. International Journal of Chronic Obstructive Pulmonary Disease, 5, 263269.Google ScholarPubMed
Troyer, A.K., & Murphy, K.J. (2007). Memory for intentions in amnestic mild cognitive impairment: Time-and event-based prospective memory. Journal of the International Neuropsychological Society 13, 365369.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). Wechsler Memory Scale (WMS-III). San Antonio: Psychological Corporation.Google Scholar
Wechsler, D. (1999). Wechsler Abbreviated Scale of Intelligence. San Antonio: Psychological Corporation.Google Scholar
Wing, Y., & Leung, C.M. (2012). Mental health impact of severe acute respiratory syndrome: a prospective study. Hong Kong Medical Journal, 18, 2427.Google ScholarPubMed
World Health Organization (2013). Novel coronavirus infection - update (Middle East respiratory syndrome- coronavirus). http://www.who.int/csr/don/2013_05_23_ncov/en. Accessed 19 Sept 2016.Google Scholar
World Health Organization (2015). Summary of probable SARS cases with onset of illness from 1 November 2002 to 31 July 2003. https://www.who.int/publications/m/item/summary-of-probable-sars-cases-with-onset-of-illness-from-1-november-2002-to-31-july-2003. Accessed 5 Jul 2016.Google Scholar
Wu, P., Fang, Y., Guan, Z., Fan, B., Kong, J., Yao, Z., … Hoven, C.W. (2009). The psychological impact of the SARS epidemic on hospital employees in China: Exposure, risk perception, and altruistic acceptance of risk. The Canadian Journal of Psychiatry, 54, 302311.CrossRefGoogle ScholarPubMed
Zakzanis, K.K., Leach, L., & Kaplan, E. (1998). On the nature and pattern of neurocognitive function in major depressive disorder. Neuropsychiatry, Neuropsychology, & Behavioral Neurology, 11(3), 111119.Google ScholarPubMed
Zhou, H., Lu, S., Chen, J., Wei, N., Wang, D., Lyu, H., … Hu, S. (2020). The landscape of cognitive function in recovered COVID-19 patients. Journal of Psychiatric Research, 129, 98102. https://doi.org/10.1016/j.jpsychires.2020.06.022 CrossRefGoogle ScholarPubMed