Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T09:58:02.781Z Has data issue: false hasContentIssue false

Post-acute sequelae of SARS-CoV-2 infection: relationship of central nervous system manifestations with physical disability and systemic inflammation

Published online by Cambridge University Press:  06 May 2022

Geraldo F. Busatto*
Affiliation:
Departamento e Instituto de Psiquiatria, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil Diretoria Executiva dos LIMs, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Adriana Ladeira de Araujo
Affiliation:
Diretoria Executiva dos LIMs, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
João Mauricio Castaldelli-Maia
Affiliation:
Departamento e Instituto de Psiquiatria, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil Departamento de Neurociências, Centro Universitário da Faculdade de Medicina do ABC, São Paulo, SP, Brasil
Rodolfo Furlan Damiano
Affiliation:
Departamento e Instituto de Psiquiatria, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Marta Imamura
Affiliation:
Departamento de Medicina Legal, Etica Medica e Medicina Social e do Trabalho, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Bruno F. Guedes
Affiliation:
Departamento de Neurologia, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Fabio de Rezende Pinna
Affiliation:
Departamento de Oftalmologia e Otorrinolaringologia, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Marcio Valente Yamada Sawamura
Affiliation:
Departamento de Radiologia, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Márcio C. Mancini
Affiliation:
Unidade de Obesidade e Síndrome Metabólica, Disciplina de Endocrinologia e Metabologia, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Katia R. da Silva
Affiliation:
Instituto do Coração (InCor) do Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Michelle L. Garcia
Affiliation:
Divisão de Pneumologia, Instituto do Coração, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brasil
Nairo Sumita
Affiliation:
Departamento de Patologia Clínica, LIM/03 – Laboratório de Medicina Laboratorial, Hospital das Clínicas, Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brasil
Andre Russowsky Brunoni
Affiliation:
Departamento de Clínica Médica, LIM/27 – Laboratório de Neurociências, Hospital das Clínicas, Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brasil
Alberto J. da Silva Duarte
Affiliation:
Departamento de Dermatologia, Laboratório de Dermatologia e Imunodeficiências, LIM-56, Faculdade de Medicina e Instituto de Medicina Tropical de São Paulo, São Paulo, SP, Brasil
Emmanuel A. Burdmann
Affiliation:
Departamento de Clínica Médica, LIM/12 – Laboratório de Pesquisa Básica em Doenças Renais, Disciplina de Nefrologia, Hospital das Clínicas, Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brasil
Esper G. Kallas
Affiliation:
Departamento de Moléstias Infecciosas e Parasitárias, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brasil
Giovanni G. Cerri
Affiliation:
Departamento de Radiologia, Faculdade de Medicina, LIM/44, Laboratório de Ressonância Magnética em Neurorradiologia Hospital das Clínicas, Faculdade de Medicina da Universidade de São Paulo, São Paulo, SP, Brasil
Ricardo Nitrini
Affiliation:
Departamento de Neurologia, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Ricardo F. Bento
Affiliation:
Departamento de Oftalmologia e Otorrinolaringologia, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil Divisão de Otorrinolaringologia, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Vanderson Geraldo Rocha
Affiliation:
Serviço de Hematologia, Hemoterapia e Terapia Celular, Divisão de Clínica Médica I do ICHC, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Heraldo Possolo de Souza
Affiliation:
Departamento de Clínica Médica, Disciplina de Emergências Clínicas, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Euripedes C. Miguel
Affiliation:
Departamento e Instituto de Psiquiatria, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Carlos R. R. de Carvalho
Affiliation:
Divisão de Pneumologia, Instituto do Coração, Hospital das Clinicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo, São Paulo, SP, Brasil
Orestes V. Forlenza
Affiliation:
Departamento e Instituto de Psiquiatria, Laboratório de Neurociências – LIM-27, Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
Linamara Rizzo Batistella
Affiliation:
Departamento de Medicina Legal, Etica Medica e Medicina Social e do Trabalho, Faculdade de Medicina da Universidade de São Paulo HCFMUSP, São Paulo, SP, Brasil
*
Author for correspondence: Geraldo F. Busatto, E-mail: [email protected]

Abstract

Background

Despite the multitude of clinical manifestations of post-acute sequelae of SARS-CoV-2 infection (PASC), studies applying statistical methods to directly investigate patterns of symptom co-occurrence and their biological correlates are scarce.

Methods

We assessed 30 symptoms pertaining to different organ systems in 749 adults (age = 55 ± 14 years; 47% female) during in-person visits conducted at 6–11 months after hospitalization due to coronavirus disease 2019 (COVID-19), including six psychiatric and cognitive manifestations. Symptom co-occurrence was initially investigated using exploratory factor analysis (EFA), and latent variable modeling was then conducted using Item Response Theory (IRT). We investigated associations of latent variable severity with objective indices of persistent physical disability, pulmonary and kidney dysfunction, and C-reactive protein and D-dimer blood levels, measured at the same follow-up assessment.

Results

The EFA extracted one factor, explaining 64.8% of variance; loadings were positive for all symptoms, and above 0.35 for 16 of them. The latent trait generated using IRT placed fatigue, psychiatric, and cognitive manifestations as the most discriminative symptoms (coefficients > 1.5, p < 0.001). Latent trait severity was associated with decreased body weight and poorer physical performance (coefficients > 0.240; p ⩽ 0.003), and elevated blood levels of C-reactive protein (coefficient = 0.378; 95% CI 0.215–0.541; p < 0.001) and D-dimer (coefficient = 0.412; 95% CI 0.123–0.702; p = 0.005). Results were similar after excluding subjects with pro-inflammatory comorbidities.

Conclusions

Different symptoms that persist for several months after moderate or severe COVID-19 may unite within one latent trait of PASC. This trait is dominated by fatigue and psychiatric symptoms, and is associated with objective signs of physical disability and persistent systemic inflammation.

Type
Original Article
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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.)

Footnotes

*

Equal contribution

**

The HCFMUSP COVID-19 Study Group is Eloisa Bonfá, Edivaldo M. Utiyama, Aluisio C. Segurado, Beatriz Perondi, Anna Miethke-Morais, Amanda C. Montal, Leila Harima, Solange R.G.Fusco, Marjorie F. Silva, Marcelo C. Rocha, Izabel Marcilio, Izabel Cristina Rios, Fabiane Yumi Ogihara Kawano, Maria Amélia de Jesus, Carolina Carmo, Clarice Tanaka, Julio F. M. Marchini, Juliana C Ferreira, Anna Sara Levin, Maura Salaroli Oliveira, Thaís Guimarães, Carolina dos Santos Lázari, Ester Sabino, Marcello M. C. Magri, Tarcisio E. P. Barros-Filho, Maria Cristina Peres Braido Francisco, Silvia Figueiredo Costa

This article has been updated since its original publication. A correction notice detailing the changes can be found here: https://doi.org/10.1017/S0033291722001799

References

Abel, K. M., Carr, M. J., Ashcroft, D. M., Chalder, T., Chew-Graham, C. A., Hope, H., … Pierce, M. (2021). Association of SARS-CoV-2 infection with psychological distress, psychotropic prescribing, fatigue, and sleep problems among UK primary care patients. JAMA Network Open, 4(11), e2134803. https://doi.org/10.1001/jamanetworkopen.2021.34803.CrossRefGoogle ScholarPubMed
Afari, N., & Buchwald, D. (2003). Chronic fatigue syndrome: A review. American Journal of Psychiatry, 160(2), 221236. https://doi.org/10.1176/appi.ajp.160.2.221.CrossRefGoogle ScholarPubMed
Ahmad, T., Pencina, M. J., Schulte, P. J., O'Brien, E., Whellan, D. J., Piña, I. L., … Felker, G. M. (2014). Clinical implications of chronic heart failure phenotypes defined by cluster analysis. Journal of the American College of Cardiology, 64(17), 17651774. https://doi.org/10.1016/j.jacc.2014.07.979.CrossRefGoogle ScholarPubMed
Aktas, A., Walsh, D., & Rybicki, L. (2010). Symptom clusters: Myth or reality? Palliative Medicine, 24(4), 373385. https://doi.org/10.1177/0269216310367842.CrossRefGoogle ScholarPubMed
Al-Aly, Z., Xie, Y., & Bowe, B. (2021). High-dimensional characterization of post-acute sequelae of COVID-19. Nature, 594, 259264. https://doi.org/10.1038/s41586-021-03553-9.CrossRefGoogle ScholarPubMed
Antonelli, M., Penfold, R. S., Merino, J., Sudre, C. H., Molteni, E., Berry, S., … Steves, C. J. (2022). Risk factors and disease profile of post-vaccination SARS-CoV-2 infection in UK users of the COVID symptom study app: A prospective, community-based, nested, case-control study. The Lancet Infectious Diseases, 22(1), 4355. https://doi.org/10.1016/S1473-3099(21)00460-6.CrossRefGoogle ScholarPubMed
Associação Brasileira de Empresas de Pesquisa (ABEP). (2020). Critério de Classificação Econômica no Brasil. São Paulo, SP: Associação Brasileira de Empresas de Pesquisa. Retrieved from https://www.abep.org/criterio-brasil (Accessed 16 August 2021).Google Scholar
Bastien, C. H., Vallières, A., & Morin, C. M. (2001). Validation of the insomnia severity index as an outcome measure for insomnia research. Sleep Medicine, 2(4), 297307. https://doi.org/10.1016/s1389-9457(00)00065-4.CrossRefGoogle ScholarPubMed
Becker, J. H., Lin, J. J., Doernberg, M., Stone, K., Navis, A., Festa, J. R., & Wisnivesky, J. P. (2021). Assessment of cognitive function in patients after COVID-19 infection. JAMA Network Open, 4(10), e2130645. https://doi.org/10.1001/jamanetworkopen.2021.30645.CrossRefGoogle ScholarPubMed
Bell, M. L., Catalfamo, C. J., Farland, L. V., Ernst, K. C., Jacobs, E. T., Klimentidis, Y. C., … Pogreba-Brown, K. (2021). Post-acute sequelae of COVID-19 in a non-hospitalized cohort: Results from the Arizona CoVHORT. PLoS ONE, 16(8), e0254347. https://doi.org/10.1371/journal.pone.0254347.CrossRefGoogle Scholar
Bestall, J. C., Paul, E. A., Garrod, R., Garnham, R., Jones, P. W., & Wedzicha, J. A. (1999). Usefulness of the medical research council (MRC) dyspnoea scale as a measure of disability in patients with chronic obstructive pulmonary disease. Thorax, 54(7), 581586. https://dx.doi.org/10.1136/thx.54.7.581.CrossRefGoogle ScholarPubMed
Blomberg, B., Mohn, K. G. I., Brokstad, K. A., Zhou, F., Linchausen, D. W., Hansen, B. A., … Langeland, N. (2021). Long COVID in a prospective cohort of home-isolated patients. Nature Medicine, 27, 16071613. https://doi.org/10.1038/s41591-021-01433-3.CrossRefGoogle Scholar
Bohannon, R. W. (2015). Muscle strength: Clinical and prognostic value of hand-grip dynamometry. Current Opinion in Clinical Nutrition and Metabolic Care, 18(5), 465470. doi:10.1097/MCO.0000000000000202.CrossRefGoogle ScholarPubMed
Boldrini, M., Canoll, P. D., & Klein, R. S. (2021). How COVID-19 affects the brain. JAMA Psychiatry, 78(6), 682683. https://doi.org/10.1001/jamapsychiatry.2021.0500.CrossRefGoogle ScholarPubMed
Boonstra, A. M., Preuper, H. R. S., Balk, G. A., & Stewart, R. E. (2014). Cut-off points for mild, moderate, and severe pain on the visual analogue scale for pain in patients with chronic musculoskeletal pain. Pain, 155(12), 25452550. https://doi.org/10.1016/j.pain.2014.09.014.CrossRefGoogle ScholarPubMed
Bornstein, S. R., Voit-Bak, K., Donate, T., Rodionov, R. N., Gainetdinov, R. R., Tselmin, S., … Straube, R. (2021). Chronic post-COVID-19 syndrome and chronic fatigue syndrome: Is there a role for extracorporeal apheresis? Molecular Psychiatry, 27(1), 3437. https://doi.org/10.1038/s41380-021-01148-4.CrossRefGoogle Scholar
Bourmistrova, N. W., Solomon, T., Braude, P., Strawbridge, R., & Carter, B. (2021). Long-term effects of COVID-19 on mental health: A systematic review. Journal of Affective Disorders, 299, 118125. https://doi.org/10.1016/j.jad.2021.11.031.CrossRefGoogle ScholarPubMed
Brandão Neto, D., Fornazieri, M. A., Dib, C., Di Francesco, R. C., Doty, R. L., Voegels, R. L., & Pinna, F. R. (2021). Chemosensory dysfunction in COVID-19: Prevalences, recovery rates, and clinical associations on a large Brazilian sample. Otolaryngology Head and Neck Surgery, 164(3), 512518. https://doi.org/10.1177/0194599820954825.CrossRefGoogle ScholarPubMed
Busatto, G. F., de Araújo, A. L., Duarte, A., Levin, A. S., Guedes, B. F., Kallas, E. G., … HCFMUSP Covid-19 Study Group. (2021). Post-acute sequelae of SARS-CoV-2 infection (PASC): A protocol for a multidisciplinary prospective observational evaluation of a cohort of patients surviving hospitalisation in Sao Paulo, Brazil. British Medical Journal Open, 11(6), e051706. https://doi.org/10.1136/bmjopen-2021-051706.Google ScholarPubMed
Committee on the Diagnostic Criteria for Myalgic Encephalomyelitis/Chronic Fatigue Syndrome, Board on the Health of Select Populations, & Institute of Medicine. (2015). Beyond myalgic encephalomyelitis/chronic fatigue syndrome: Redefining an illness. Washington, DC: National Academies Press (US).Google Scholar
Damiano, R. F., Guimarães, C. M. J., Cincoto, A. V., Rocca, C. C. A., Serafim, A. P., Bacchi, P., … Forlenza, O. V. (2022). Post-COVID psychiatric and cognitive morbidity: Preliminary findings from a Brazilian cohort study. General Hospital Psychiatry, 75, 3845. https://doi.org/10.1016/j.genhosppsych.2022.01.002.CrossRefGoogle ScholarPubMed
David, A. S. (2021). Long COVID: Research must guide future management. British Medical Journal, 17(375), n3109. https://doi.org/10.1136/bmj.n3109.CrossRefGoogle Scholar
Davis, H. E., Assaf, G. S., McCorkell, L., Wei, H., Low, R. J., Re'em, Y., … Akrami, A. (2021). Characterizing long COVID in an international cohort: 7 months of symptoms and their impact. EClinicalMedicine, 38, 101019. https://doi.org/10.1016/j.eclinm.2021.101019.CrossRefGoogle Scholar
Desmond, H. E., Lindner, C., Troost, J. P., Held, Z., Callaway, A., Oh, G. J., … Massengill, S. F. (2021). Association between psychiatric disorders and glomerular disease. Glomerular Diseases, 1, 118128. https://doi.org/10.1159/000516359.CrossRefGoogle Scholar
Evans, R. A., McAuley, H., Harrison, E. M., Shikotra, A., Singapuri, A., Sereno, M., … PHOSP-COVID Collaborative Group. (2021). Physical, cognitive, and mental health impacts of COVID-19 after hospitalisation (PHOSP-COVID): A UK multicentre, prospective cohort study. The Lancet Respiratory Medicine, 9(11), 12751287. https://doi.org/10.1016/S2213-2600(21)00383-0.CrossRefGoogle ScholarPubMed
Hampshire, A., Trender, W., Chamberlain, S. R., Jolly, A. E., Grant, J. E., Patrick, F., … Mehta, M. A. (2021). Cognitive deficits in people who have recovered from COVID-19. EClinicalMedicine, 39, 101044. https://doi.org/10.1016/j.eclinm.2021.101044.CrossRefGoogle ScholarPubMed
Harris, P. A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N., & Conde, J. G. (2009). Research electronic data capture (REDCap) – a metadata-driven methodology and workflow process for providing translational research informatics support. Journal of Biomedical Informatics, 42(2), 377381. doi:10.1016/j.jbi.2008.08.010.CrossRefGoogle ScholarPubMed
Hays, R. D., Morales, L. S., & Reise, S. P. (2000). Item response theory and health outcomes measurement in the 21st century. Medical Care, 38(9 Suppl. II), II28II42. https://doi.org/10.1097/00005650-200009002-00007.CrossRefGoogle ScholarPubMed
Heightman, M., Prashar, J., Hillman, T. E., Marks, M., Livingston, R., Ridsdale, H. A., … Banerjee, A. (2021). Post-COVID-19 assessment in a specialist clinical service: A 12-month, single-centre, prospective study in 1325 individuals. British Medical Journal Open Respiratory Research, 8(1), e001041. https://doi.org/10.1136/bmjresp-2021-001041.CrossRefGoogle Scholar
Huang, C., Huang, L., Wang, Y., Li, X., Ren, L., Gu, X., … Cao, B. (2021a). 6-month Consequences of COVID-19 in patients discharged from hospital: A cohort study. The Lancet, 397(10270), 220232. https://doi.org/10.1016/S0140-6736(20)32656-8.CrossRefGoogle Scholar
Huang, C., Wang, Y., Li, X., Ren, L., Zhao, J., Hu, Y., … Cao, B. (2020). Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. The Lancet, 395(10223), 497506. https://doi.org/10.1016/S0140-6736(20)30183-5.CrossRefGoogle ScholarPubMed
Huang, L., Yao, Q., Gu, X., Wang, Q., Ren, L., Wang, Y., … Cao, B. (2021b). 1-year outcomes in hospital survivors with COVID-19: A longitudinal cohort study. The Lancet, 398(10302), 747758. https://doi.org/10.1016/S0140-6736(21)01755-4.CrossRefGoogle Scholar
Ismael, F., Bizario, J. C. S., Battagin, T., Zaramella, B., Leal, F. E., Torales, J., … Castaldelli-Maia, J. M. (2021). Post-infection depressive, anxiety and post-traumatic stress symptoms: A prospective cohort study in patients with mild COVID-19. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 111, 110341. https://doi.org/10.1016/j.pnpbp.2021.110341.CrossRefGoogle ScholarPubMed
Krueger, R. F., Nichol, P. E., Hicks, B. M., Markon, K. E., Patrick, C. J., Iacono, W. G., & McGue, M. (2004). Using latent trait modeling to conceptualize an alcohol problems continuum. Psychological Assessment, 16(2), 107119. https://doi.org/10.1037/1040-3590.16.2.107.CrossRefGoogle ScholarPubMed
Levey, A. S., Stevens, L. A., Schmid, C. H., Zhang, Y. L., Castro, A. F., 3rd, Feldman, H. I., … CKD-EPI (Chronic Kidney Disease Epidemiology Collaboration). (2009). A new equation to estimate glomerular filtration rate. Annals of Internal Medicine, 150(9), 604612. https://doi.org/10.7326/0003-4819-150-9-200905050-00006.CrossRefGoogle ScholarPubMed
Lewis, G., Pelosi, A. J., Araya, R., & Dunn, G. (1992). Measuring psychiatric disorder in the community: A standardized assessment for use by lay interviewers. Psychological Medicine, 22(2), 465486. https://doi.org/10.1017/s0033291700030415.CrossRefGoogle ScholarPubMed
Litmanovich, D. E., Chung, M., Kirkbride, R. R., Kicska, G., & Kanne, J. P. (2020). Review of chest radiograph findings of COVID-19 pneumonia and suggested reporting language. Journal of Thoracic Imaging, 35(6), 354360. https://doi.org/10.1097/RTI.0000000000000541.Google ScholarPubMed
Lopez-Leon, S., Wegman-Ostrosky, T., Perelman, C., Sepulveda, R., Rebolledo, P. A., Cuapio, A., & Villapol, S. (2021). More than 50 long-term effects of COVID-19: A systematic review and meta-analysis. Scientific Reports, 11(1), 16144. https://doi.org/10.1038/s41598-021-95565-8.CrossRefGoogle ScholarPubMed
Mackay, A. (2021). A paradigm for post-COVID-19 fatigue syndrome analogous to ME/CFS. Frontiers in Neurology, 12, 701419. https://doi.org/10.3389/fneur.2021.701419.CrossRefGoogle ScholarPubMed
Manca, R., De Marco, M., Ince, P. G., & Venneri, A. (2021). Heterogeneity in regional damage detected by neuroimaging and neuropathological studies in older adults With COVID-19: A cognitive-neuroscience systematic review to inform the long-term impact of the virus on neurocognitive trajectories. Frontiers in Aging Neuroscience, 13, 646908. https://doi.org/10.3389/fnagi.2021.646908.CrossRefGoogle ScholarPubMed
Mandal, S., Barnett, J., Brill, S. E., Brown, J. S., Denneny, E. K., Hare, S. S., … Hurst, J. R. (2021). Long-COVID: A cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19. Thorax, 76(4), 396398. https://doi.org/10.1136/thoraxjnl-2020-215818.CrossRefGoogle ScholarPubMed
Mazza, M. G., De Lorenzo, R., Conte, C., Poletti, S., Vai, B., Bollettini, I., … Benedetti, F. (2020). Anxiety and depression in COVID-19 survivors: Role of inflammatory and clinical predictors. Brain, Behavior, and Immunity, 89, 594600. https://doi.org/10.1016/j.bbi.2020.07.037.CrossRefGoogle ScholarPubMed
Mazza, M. G., Palladini, M., De Lorenzo, R., Magnaghi, C., Poletti, S., Furlan, R., … Benedetti, F. (2021). Persistent psychopathology and neurocognitive impairment in COVID-19 survivors: Effect of inflammatory biomarkers at three-month follow-up. Brain, Behavior, and Immunity, 94, 138147. https://doi.org/10.1016/j.bbi.2021.02.021.CrossRefGoogle ScholarPubMed
Menges, D., Ballouz, T., Anagnostopoulos, A., Aschmann, H. E., Domenghino, A., Fehr, J. S., & Puhan, M. A. (2021). Burden of post-COVID-19 syndrome and implications for healthcare service planning: A population-based cohort study. PLoS ONE, 16(7), e0254523. https://doi.org/10.1371/journal.pone.0254523.CrossRefGoogle ScholarPubMed
Michopoulos, V., Powers, A., Gillespie, C. F., Ressler, K. J., & Jovanovic, T. (2017). Inflammation in fear-and anxiety-based disorders: PTSD, GAD, and beyond. Neuropsychopharmacology, 42(1), 254270. https://doi.org/10.1038/npp.2016.146.CrossRefGoogle ScholarPubMed
Montoya, J. G., Holmes, T. H., Anderson, J. N., Maecker, H. T., Rosenberg-Hasson, Y., Valencia, I. J., … Davis, M. M. (2017). Cytokine signature associated with disease severity in chronic fatigue syndrome patients. Proceedings of the National Academy of Sciences of the USA, 114(34), E7150E7158. https://doi.org/10.1073/pnas.1710519114.CrossRefGoogle ScholarPubMed
Writing Committee for the COMEBAC Study Group, Morin, L., Savale, L., Pham, T., Colle, R., Figueiredo, S., … Monnet, X. (2021). Four-month clinical status of a cohort of patients after hospitalization for COVID-19. JAMA, 325(15), 15251534. https://doi.org/10.1001/jama.2021.3331.Google ScholarPubMed
Morris, G., Anderson, G., Galecki, P., Berk, M., & Maes, M. (2013). A narrative review on the similarities and dissimilarities between myalgic encephalomyelitis/chronic fatigue syndrome (ME/CFS) and sickness behavior. BMC Medicine, 11, 64. https://doi.org/10.1186/1741-7015-11-64.CrossRefGoogle ScholarPubMed
Nalbandian, A., Sehgal, K., Gupta, A., Madhavan, M. V., McGroder, C., Stevens, J. S., … Wan, E. Y. (2021). Post-acute COVID-19 syndrome. Nature Medicine, 27(4), 601615. https://doi.org/10.1038/s41591-021-01283-z.CrossRefGoogle ScholarPubMed
Nasserie, T., Hittle, M., & Goodman, S. N. (2021). Assessment of the frequency and variety of persistent symptoms among patients With COVID-19: A systematic review. JAMA Network Open, 4(5), e2111417. https://doi.org/10.1001/jamanetworkopen.2021.11417.CrossRefGoogle ScholarPubMed
Pariante, C. M. (2017). Why are depressed patients inflamed? A reflection on 20 years of research on depression, glucocorticoid resistance and inflammation. European Neuropsychopharmacology, 27(6), 554559. https://doi.org/10.1016/j.euroneuro.2017.04.001.CrossRefGoogle ScholarPubMed
Pasini, E., Corsetti, G., Romano, C., Scarabelli, T. M., Chen-Scarabelli, C., Saravolatz, L., & Dioguardi, F. S. (2021). Serum metabolic profile in patients with long-COVID (PASC) syndrome: Clinical implications. Frontiers in Medicine, 8, 714426. https://doi.org/10.3389/fmed.2021.714426.CrossRefGoogle ScholarPubMed
Penfield, R. D., & Camilli, G. (2007). Differential item functioning and item bias. In Rao, C. R. & Sinharay, S. (Eds.), Handbook of statistics: Psychometrics (pp. 125167). Amsterdam: Elsevier. https://doi.org/10.1016/S0169-7161(06)26005-X.Google Scholar
Pereira, C. A., Sato, T., & Rodrigues, S. C. (2007). New reference values for forced spirometry in white adults in Brazil. Jornal Brasileiro de Pneumologia, 33(4), 397406. https://doi.org/10.1590/s1806-37132007000400008.CrossRefGoogle ScholarPubMed
Perrin, R., Riste, L., Hann, M., Walther, A., Mukherjee, A., & Heald, A. (2020). Into the looking glass: Post-viral syndrome post COVID-19. Medical Hypotheses, 144, 110055. https://doi.org/10.1016/j.mehy.2020.110055.CrossRefGoogle ScholarPubMed
Phillips, S., & Williams, M. A. (2021). Confronting our next national health disaster – Long-Haul COVID. The New England Journal of Medicine, 385(7), 577579. https://doi.org/10.1056/NEJMp2109285.CrossRefGoogle ScholarPubMed
Pirker-Kees, A., Platho-Elwischger, K., Hafner, S., Redlich, K., & Baumgartner, C. (2021). Hyposmia is associated with reduced cognitive function in COVID-19: First preliminary results. Dementia and Geriatric Cognitive Disorders, 50(1), 6873. https://doi.org/10.1159/000515575.CrossRefGoogle ScholarPubMed
Saha, T. D., Compton, W. M., Pulay, A. J., Stinson, F. S., Ruan, W. J., Smith, S. M., & Grant, B. F. (2010). Dimensionality of DSM-IV nicotine dependence in a national sample: An item response theory application. Drug and Alcohol Dependence, 108(1–2), 2128. https://doi.org/10.1016/j.drugalcdep.2009.11.012.CrossRefGoogle Scholar
Sankowski, R., Mader, S., & Valdés-Ferrer, S. I. (2015). Systemic inflammation and the brain: Novel roles of genetic, molecular, and environmental cues as drivers of neurodegeneration. Frontiers in Cellular Neuroscience, 9, 28. https://doi.org/10.3389/fncel.2015.00028.CrossRefGoogle ScholarPubMed
Sasannejad, C., Ely, E. W., & Lahiri, S. (2019). Long-term cognitive impairment after acute respiratory distress syndrome: A review of clinical impact and pathophysiological mechanisms. Critical Care, 23(1), 352. https://doi.org/10.1186/s13054-019-2626-z.CrossRefGoogle ScholarPubMed
Sonnweber, T., Boehm, A., Sahanic, S., Pizzini, A., Aichner, M., Sonnweber, B., … Weiss, G. (2020). Persisting alterations of iron homeostasis in COVID-19 are associated with non-resolving lung pathologies and poor patients’ performance: A prospective observational cohort study. Respiratory Research, 21(1), 276. https://doi.org/10.1186/s12931-020-01546-2.CrossRefGoogle ScholarPubMed
Søraas, A., , R., Kalleberg, K. T., Støer, N. C., Ellingjord-Dale, M., & Landrø, N. I. (2021). Self-reported memory problems 8 months after COVID-19 infection. JAMA Network Open, 4(7), e2118717. https://doi.org/10.1001/jamanetworkopen.2021.18717.CrossRefGoogle ScholarPubMed
Strassmann, A., Steurer-Stey, C., Lana, K. D., Zoller, M., Turk, A. J., Suter, P., & Puhan, M. A. (2013). Population-based reference values for the 1-min sit-to-stand test. International Journal of Public Health, 58(6), 949953. https://doi.org/10.1007/s00038-013-0504-z.CrossRefGoogle ScholarPubMed
Sudre, C. H., Murray, B., Varsavsky, T., Graham, M. S., Penfold, R. S., Bowyer, R. C., … Steves, C. J. (2021). Attributes and predictors of long COVID. Nature Medicine, 27(4), 626631. https://doi.org/10.1038/s41591-021-01292-y.CrossRefGoogle ScholarPubMed
Taquet, M., Geddes, J. R., Husain, M., Luciano, S., & Harrison, P. J. (2021). 6-month neurological and psychiatric outcomes in 236 379 survivors of COVID-19: A retrospective cohort study using electronic health records. The Lancet Psychiatry, 8(5), 416427. https://doi.org/10.1016/S2215-0366(21)00084-5.CrossRefGoogle ScholarPubMed
Townsend, L., Dowds, J., O'Brien, K., Sheill, G., Dyer, A. H., O'Kelly, B., … Bannan, C. (2021a). Persistent poor health after COVID-19 is not associated with respiratory complications or initial disease severity. Annals of the American Thoracic Society, 18(6), 9971003. https://doi.org/10.1513/AnnalsATS.202009-1175OC.CrossRefGoogle Scholar
Townsend, L., Dyer, A. H., Jones, K., Dunne, J., Mooney, A., Gaffney, F., … Conlon, N. (2020). Persistent fatigue following SARS-CoV-2 infection is common and independent of severity of initial infection. PLoS ONE, 15(11), e0240784. https://doi.org/10.1371/journal.pone.0240784.CrossRefGoogle ScholarPubMed
Townsend, L., Fogarty, H., Dyer, A., Martin-Loeches, I., Bannan, C., Nadarajan, P., … O'Donnell, J. S. (2021b). Prolonged elevation of D-dimer levels in convalescent COVID-19 patients is independent of the acute phase response. Journal of Thrombosis and Haemostasis, 19(4), 10641070. https://doi.org/10.1111/jth.15267.CrossRefGoogle Scholar
Vale, F., Balieiro, A. P. Jr, & Silva-Filho, J. H. (2012). Memory complaint scale (MCS). proposed tool for active systematic search. Dementia & Neuropsychologia, 6(4), 212218. https://doi.org/10.1590/S1980-57642012DN06040004.CrossRefGoogle ScholarPubMed
Vianna, L. C., Oliveira, R. B., & Araújo, C. G. (2007). Age-related decline in handgrip strength differs according to gender. Journal of Strength and Conditioning Research, 21(4), 13101314. https://doi.org/10.1519/R-23156.1.Google Scholar
Weathers, F. W., Litz, B. T., Herman, D. S., Huska, J. A., & Keane, T. M. (1993). The PTSD Checklist (PCL): Reliability, validity, and diagnostic utility. San Antonio, TX: Paper presented at the 9th Annual Meeting of the International Society for Traumatic Stress Studies (ISTSS). Retrieved from https://www.researchgate.net/publication/291448760_The_PTSD_Checklist_PCL_Reliability_validity_and_diagnostic_utilityGoogle Scholar
Webster, K., Cella, D., & Yost, K. (2003). The functional assessment of chronic illness therapy (FACIT) measurement system: Properties, applications, and interpretation. Health and Quality of Life Outcomes, 1, 79. https://doi.org/10.1186/1477-7525-1-79.CrossRefGoogle Scholar
WHO. (1982). WHO protocol: Epidemiologic studies of neurologic disorders (1982). Geneva: WHO. Retrieved from https://apps.who.int/iris/bitstream/handle/10665/72410/a82497.pdf?sequence=1&isAllowed=y.Google Scholar
WHO Working Group on the Clinical Characterisation and Management of COVID-19 infection. (2020). A minimal common outcome measure set for COVID-19 clinical research. The Lancet Infectious Diseases, 20(8), e192e197. https://doi.org/10.1016/S1473-3099(20)30483-7.CrossRefGoogle Scholar
Zigmond, A. S., & Snalth, R. P. (1983). The hospital anxiety and depression scale. Acta Psychiatrica Scandinavica, 67(6), 361370. https://doi.org/10.1111/j.1600-0447.1983.tb09716.x.CrossRefGoogle ScholarPubMed
Supplementary material: File

Busatto et al. supplementary material

Busatto et al. supplementary material

Download Busatto et al. supplementary material(File)
File 92 KB