Persistent viral RNA shedding of SARS-CoV-2 is associated with delirium incidence and six-month mortality in hospitalized COVID-19 patients.


Journal

GeroScience
ISSN: 2509-2723
Titre abrégé: Geroscience
Pays: Switzerland
ID NLM: 101686284

Informations de publication

Date de publication:
06 2022
Historique:
received: 22 01 2022
accepted: 17 03 2022
pubmed: 11 5 2022
medline: 24 6 2022
entrez: 10 5 2022
Statut: ppublish

Résumé

Persistent viral RNA shedding of SARS-CoV-2 following COVID-19 has increasingly been recognized, with limited understanding of its implications on outcomes in hospitalized COVID-19 patients. We retrospectively assessed for persistent viral shedding across Northwestern Medicine Healthcare (NMHC) patients between March and August 2020. We assessed for predictors of persistent viral shedding, in-hospital delirium, and six-month mortality using binary logistic regression. Of the 2,518 hospitalized patients with an RT-PCR-confirmed diagnosis of COVID-19, 959 underwent repeat SARS-CoV-2 RT-PCR at least fourteen days from initial positive testing. Of those, 405 (42.2%) patients were found to have persistent viral shedding. Persistent viral shedding was associated with male sex, increased BMI, diabetes mellitus, chronic kidney disease, and exposure to corticosteroids during initial COVID-19 hospitalization. Persistent viral shedding was independently associated with incidence of in-hospital delirium after adjusting for factors including severity of respiratory dysfunction (OR 2.45; 95% CI 1.75, 3.45). Even after adjusting for age, severity of respiratory dysfunction, and occurrence of in-hospital delirium, persistent viral shedding remained significantly associated with increased six-month mortality (OR 2.43; 95% CI 1.42, 4.29). Persistent viral shedding occurs frequently in hospitalized COVID-19 patients and is associated with in-hospital delirium and increased six-month mortality.

Sections du résumé

BACKGROUND
Persistent viral RNA shedding of SARS-CoV-2 following COVID-19 has increasingly been recognized, with limited understanding of its implications on outcomes in hospitalized COVID-19 patients.
METHODS
We retrospectively assessed for persistent viral shedding across Northwestern Medicine Healthcare (NMHC) patients between March and August 2020. We assessed for predictors of persistent viral shedding, in-hospital delirium, and six-month mortality using binary logistic regression.
RESULTS
Of the 2,518 hospitalized patients with an RT-PCR-confirmed diagnosis of COVID-19, 959 underwent repeat SARS-CoV-2 RT-PCR at least fourteen days from initial positive testing. Of those, 405 (42.2%) patients were found to have persistent viral shedding. Persistent viral shedding was associated with male sex, increased BMI, diabetes mellitus, chronic kidney disease, and exposure to corticosteroids during initial COVID-19 hospitalization. Persistent viral shedding was independently associated with incidence of in-hospital delirium after adjusting for factors including severity of respiratory dysfunction (OR 2.45; 95% CI 1.75, 3.45). Even after adjusting for age, severity of respiratory dysfunction, and occurrence of in-hospital delirium, persistent viral shedding remained significantly associated with increased six-month mortality (OR 2.43; 95% CI 1.42, 4.29).
CONCLUSIONS
Persistent viral shedding occurs frequently in hospitalized COVID-19 patients and is associated with in-hospital delirium and increased six-month mortality.

Identifiants

pubmed: 35538386
doi: 10.1007/s11357-022-00561-z
pii: 10.1007/s11357-022-00561-z
pmc: PMC9090540
doi:

Substances chimiques

RNA, Viral 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1241-1254

Subventions

Organisme : NINDS NIH HHS
ID : L30 NS098427
Pays : United States

Informations de copyright

© 2022. The Author(s), under exclusive licence to American Aging Association.

Références

Cucinotta D, Vanelli M. WHO Declares COVID-19 a Pandemic. Acta Biomed. 2020;91:157–60.
pubmed: 32191675 pmcid: 7569573
Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis. 2020;20:533–4.
pubmed: 32087114 pmcid: 7159018
Wu Z, McGoogan JM. Characteristics of and Important Lessons From the Coronavirus Disease 2019 (COVID-19) Outbreak in China: Summary of a Report of 72314 Cases From the Chinese Center for Disease Control and Prevention. JAMA. 2020;323:1239–42.
pubmed: 32091533
Paules CI, Marston HD, Fauci AS. Coronavirus Infections-More Than Just the Common Cold. JAMA. 2020;323:707–8.
pubmed: 31971553
Yang X, Yu Y, Xu J, Shu H, Xia J, Liu H, Wu Y, Zhang L, Yu Z, Fang M, Yu T, Wang Y, Pan S, Zou X, Yuan S, Shang Y. Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study. Lancet Respir Med. 2020;8:475–81.
pubmed: 32105632 pmcid: 7102538
Hanson KE, Caliendo AM, Arias CA, Hayden MK, Englund JA, Lee MJ, Loeb M, Patel R, El Alayli A, Altayar O, Patel P, Falck-Ytter Y, Lavergne V, Morgan RL, Murad MH, Sultan S, Bhimraj A and Mustafa RA. The Infectious Diseases Society of America Guidelines on the Diagnosis of COVID-19: Molecular Diagnostic Testing. Clin Infect Dis. 2021.
Widders A, Broom A, Broom J. SARS-CoV-2: The viral shedding vs infectivity dilemma. Infect Dis Health. 2020;25:210–5.
pubmed: 32473952 pmcid: 7237903
Joukar F, Yaghubi Kalurazi T, Khoshsorour M, Taramian S, Mahfoozi L, Balou HA, Jafarinezhad A, Pourkazemi A, Hesni E, Asgharnezhad M, Shenagari M, Jahanzad I, Naghipour M, Maroufizadeh S, Mansour-Ghanaei F. Persistence of SARS-CoV-2 RNA in the nasopharyngeal, blood, urine, and stool samples of patients with COVID-19: a hospital-based longitudinal study. Virol J. 2021;18:134.
pubmed: 34210325 pmcid: 8248752
Owusu D, Pomeroy MA, Lewis NM, Wadhwa A, Yousaf AR, Whitaker B, Dietrich E, Hall AJ, Chu V, Thornburg N, Christensen K, Kiphibane T, Willardson S, Westergaard R, Dasu T, Pray IW, Bhattacharyya S, Dunn A, Tate JE, Kirking HL, Matanock A and Household Transmission Study T. Persistent SARS-CoV-2 RNA Shedding without Evidence of Infectiousness: A Cohort Study of Individuals with COVID-19. J Infect Dis. 2021.
Bjorkman KK, Saldi TK, Lasda E, Bauer LC, Kovarik J, Gonzales PK, Fink MR, Tat KL, Hager CR, Davis JC, Ozeroff CD, Brisson GR, Larremore DB, Leinwand LA, McQueen MB and Parker R. Higher viral load drives infrequent SARS-CoV-2 transmission between asymptomatic residence hall roommates. J Infect Dis. 2021.
Wang Y, Guo Q, Yan Z, Zhou D, Zhang W, Zhou S, Li YP, Yuan J, Uyeki TM, Shen X, Wu W, Zhao H, Wu YF, Shang J, He Z, Yang Y, Zhao H, Hong Y, Zhang Z, Wu M, Wei T, Deng X, Deng Y, Cai LH, Lu W, Shu H, Zhang L, Luo H, Ing Zhou Y, Weng H, Song K, Yao L, Jiang M, Zhao B, Chi R, Guo B, Fu L, Yu L, Min H, Chen P, Chen S, Hong L, Mao W, Huang X, Gu L, Li H, Wang C, Cao B and Network CA-C. Factors Associated With Prolonged Viral Shedding in Patients With Avian Influenza A(H7N9) Virus Infection. J Infect Dis. 2018;217:1708–1717.
Paz-Bailey G, Rosenberg ES, Doyle K, Munoz-Jordan J, Santiago GA, Klein L, Perez-Padilla J, Medina FA, Waterman SH, Gubern CG, Alvarado LI, Sharp TM. Persistence of Zika Virus in Body Fluids - Final Report. N Engl J Med. 2018;379:1234–43.
pubmed: 28195756
Subissi L, Keita M, Mesfin S, Rezza G, Diallo B, Van Gucht S, Musa EO, Yoti Z, Keita S, Djingarey MH, Diallo AB, Fall IS. Ebola Virus Transmission Caused by Persistently Infected Survivors of the 2014–2016 Outbreak in West Africa. J Infect Dis. 2018;218:S287–91.
pubmed: 29920602 pmcid: 6249578
Brooks DG, Teyton L, Oldstone MB, McGavern DB. Intrinsic functional dysregulation of CD4 T cells occurs rapidly following persistent viral infection. J Virol. 2005;79:10514–27.
pubmed: 16051844 pmcid: 1182641
Zheng HY, Zhang M, Yang CX, Zhang N, Wang XC, Yang XP, Dong XQ, Zheng YT. Elevated exhaustion levels and reduced functional diversity of T cells in peripheral blood may predict severe progression in COVID-19 patients. Cell Mol Immunol. 2020;17:541–3.
pubmed: 32203186 pmcid: 7091621
van Kampen JJA, van de Vijver D, Fraaij PLA, Haagmans BL, Lamers MM, Okba N, van den Akker JPC, Endeman H, Gommers D, Cornelissen JJ, Hoek RAS, van der Eerden MM, Hesselink DA, Metselaar HJ, Verbon A, de Steenwinkel JEM, Aron GI, van Gorp ECM, van Boheemen S, Voermans JC, Boucher CAB, Molenkamp R, Koopmans MPG, Geurtsvankessel C, van der Eijk AA. Duration and key determinants of infectious virus shedding in hospitalized patients with coronavirus disease-2019 (COVID-19). Nat Commun. 2021;12:267.
pubmed: 33431879 pmcid: 7801729
Hu F, Chen F, Ou Z, Fan Q, Tan X, Wang Y, Pan Y, Ke B, Li L, Guan Y, Mo X, Wang J, Wang J, Luo C, Wen X, Li M, Ren P, Ke C, Li J, Lei C, Tang X, Li F. A compromised specific humoral immune response against the SARS-CoV-2 receptor-binding domain is related to viral persistence and periodic shedding in the gastrointestinal tract. Cell Mol Immunol. 2020;17:1119–25.
pubmed: 33037400
Xu K, Chen Y, Yuan J, Yi P, Ding C, Wu W, Li Y, Ni Q, Zou R, Li X, Xu M, Zhang Y, Zhao H, Zhang X, Yu L, Su J, Lang G, Liu J, Wu X, Guo Y, Tao J, Shi D, Yu L, Cao Q, Ruan B, Liu L, Wang Z, Xu Y, Liu Y, Sheng J, Li L. Factors Associated With Prolonged Viral RNA Shedding in Patients with Coronavirus Disease 2019 (COVID-19). Clin Infect Dis. 2020;71:799–806.
pubmed: 32271376
Liotta EM, Batra A, Clark JR, Shlobin NA, Hoffman SC, Orban ZS and Koralnik IJ. Frequent neurologic manifestations and encephalopathy-associated morbidity in Covid-19 patients. Ann Clin Transl Neurol. 2020.
Chou SH, Beghi E, Helbok R, Moro E, Sampson J, Altamirano V, Mainali S, Bassetti C, Suarez JI, McNett M, Consortium GC-N and Consortium E. Global Incidence of Neurological Manifestations Among Patients Hospitalized With COVID-19-A Report for the GCS-NeuroCOVID Consortium and the ENERGY Consortium. JAMA Netw Open. 2021;4:e2112131.
Centers for Disease Control and Prevention. COVID-19: When to Quarantine. https://www.cdc.gov/coronavirus/2019-ncov/your-health/quarantine-isolation.html . Accessed 11 Feb 2021.
Inouye SK, van Dyck CH, Alessi CA, Balkin S, Siegal AP and Horwitz RI. Clarifying confusion: the confusion assessment method. A new method for detection of delirium. Ann Intern Med. 1990;113:941–8.
Sessler CN, Gosnell MS, Grap MJ, Brophy GM, O’Neal PV, Keane KA, Tesoro EP, Elswick RK. The Richmond Agitation-Sedation Scale: validity and reliability in adult intensive care unit patients. Am J Respir Crit Care Med. 2002;166:1338–44.
pubmed: 12421743
Richardson S, Hirsch JS, Narasimhan M, Crawford JM, McGinn T, Davidson KW, the Northwell C-RC, Barnaby DP, Becker LB, Chelico JD, Cohen SL, Cookingham J, Coppa K, Diefenbach MA, Dominello AJ, Duer-Hefele J, Falzon L, Gitlin J, Hajizadeh N, Harvin TG, Hirschwerk DA, Kim EJ, Kozel ZM, Marrast LM, Mogavero JN, Osorio GA, Qiu M and Zanos TP. Presenting Characteristics, Comorbidities, and Outcomes Among 5700 Patients Hospitalized With COVID-19 in the New York City Area. JAMA. 2020;323:2052–2059.
Schreiber MP, Colantuoni E, Bienvenu OJ, Neufeld KJ, Chen KF, Shanholtz C, Mendez-Tellez PA, Needham DM. Corticosteroids and transition to delirium in patients with acute lung injury. Crit Care Med. 2014;42:1480–6.
pubmed: 24589640 pmcid: 4028387
Liotta EM, Batra A, Clark JR, Shlobin NA, Hoffman SC, Orban ZS, Koralnik IJ. Frequent neurologic manifestations and encephalopathy-associated morbidity in Covid-19 patients. Ann Clin Transl Neurol. 2020;7:2221–30.
pubmed: 33016619 pmcid: 7664279
Girard TD, Thompson JL, Pandharipande PP, Brummel NE, Jackson JC, Patel MB, Hughes CG, Chandrasekhar R, Pun BT, Boehm LM, Elstad MR, Goodman RB, Bernard GR, Dittus RS, Ely EW. Clinical phenotypes of delirium during critical illness and severity of subsequent long-term cognitive impairment: a prospective cohort study. Lancet Respir Med. 2018;6:213–22.
pubmed: 29508705 pmcid: 6709878
Baron RM, Kenny DA. The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. J Pers Soc Psychol. 1986;51:1173–82.
pubmed: 3806354
Clark JR, Batra A, Shlobin NA, Hoffman SC, Orban ZS, Koralnik IJ, Liotta EM. Acute-care hospital reencounters in COVID-19 patients. Geroscience. 2021.
Chen WJ, Yang JY, Lin JH, Fann CS, Osyetrov V, King CC, Chen YM, Chang HL, Kuo HW, Liao F, Ho MS. Nasopharyngeal shedding of severe acute respiratory syndrome-associated coronavirus is associated with genetic polymorphisms. Clin Infect Dis. 2006;42:1561–9.
pubmed: 16652313
Argyropoulos KV, Serrano A, Hu J, Black M, Feng X, Shen G, Call M, Kim MJ, Lytle A, Belovarac B, Vougiouklakis T, Lin LH, Moran U, Heguy A, Troxel A, Snuderl M, Osman I, Cotzia P, Jour G. Association of Initial Viral Load in Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) Patients with Outcome and Symptoms. Am J Pathol. 2020;190:1881–7.
pubmed: 32628931 pmcid: 7332909
Maltezou HC, Raftopoulos V, Vorou R, Papadima K, Mellou K, Spanakis N, Kossyvakis A, Gioula G, Exindari M, Froukala E, Martinez-Gonzalez B, Panayiotakopoulos G, Papa A, Mentis A, Tsakris A. Association Between Upper Respiratory Tract Viral Load, Comorbidities, Disease Severity, and Outcome of Patients With SARS-CoV-2 Infection. J Infect Dis. 2021;223:1132–8.
pubmed: 33388780
Cevik M, Tate M, Lloyd O, Maraolo AE, Schafers J, Ho A. SARS-CoV-2, SARS-CoV, and MERS-CoV viral load dynamics, duration of viral shedding, and infectiousness: a systematic review and meta-analysis. Lancet Microbe. 2021;2:e13–22.
pubmed: 33521734
Le Bert N, Tan AT, Kunasegaran K, Tham CYL, Hafezi M, Chia A, Chng MHY, Lin M, Tan N, Linster M, Chia WN, Chen MI, Wang LF, Ooi EE, Kalimuddin S, Tambyah PA, Low JG, Tan YJ, Bertoletti A. SARS-CoV-2-specific T cell immunity in cases of COVID-19 and SARS, and uninfected controls. Nature. 2020;584:457–62.
pubmed: 32668444
De Biasi S, Meschiari M, Gibellini L, Bellinazzi C, Borella R, Fidanza L, Gozzi L, Iannone A, Lo Tartaro D, Mattioli M, Paolini A, Menozzi M, Milic J, Franceschi G, Fantini R, Tonelli R, Sita M, Sarti M, Trenti T, Brugioni L, Cicchetti L, Facchinetti F, Pietrangelo A, Clini E, Girardis M, Guaraldi G, Mussini C, Cossarizza A. Marked T cell activation, senescence, exhaustion and skewing towards TH17 in patients with COVID-19 pneumonia. Nat Commun. 2020;11:3434.
pubmed: 32632085 pmcid: 7338513
Pomerantz RJ. Reservoirs of human immunodeficiency virus type 1: the main obstacles to viral eradication. Clin Infect Dis. 2002;34:91–7.
pubmed: 11731950
Nassal M. HBV cccDNA: viral persistence reservoir and key obstacle for a cure of chronic hepatitis B. Gut. 2015;64:1972–84.
pubmed: 26048673
Chertow D, Stein S, Ramelli S, Grazioli A, Chung J-Y, Singh M, Yinda CK, Winkler C, Dickey J, Ylaya K, Ko SH, Platt A, Burbelo P, Quezado M, Pittaluga S, Purcell M, Munster V, Belinky F, Ramos-Benitez M, Boritz E, Herr D, Rabin J, Saharia K, Madathil R, Tabatabai A, Soherwardi S, McCurdy M, Peterson K, Cohen J, de Wit E, Vannella K, Hewitt S and Kleiner D. SARS-CoV-2 infection and persistence throughout the human body and brain. 2021.
Goh D, Lim JCT, Fernández SB, Lee JN, Joseph CR, Neo ZW, Guerrero S, Lau MC, Sheng JYP. Persistence of residual SARS-CoV-2 viral antigen and RNA in tissues of patients with long COVID-19. 2022.
Davis DH, Kreisel SH, Muniz Terrera G, Hall AJ, Morandi A, Boustani M, Neufeld KJ, Lee HB, Maclullich AM, Brayne C. The epidemiology of delirium: challenges and opportunities for population studies. Am J Geriatr Psychiatry. 2013;21:1173–89.
pubmed: 23907068 pmcid: 3837358
Cerejeira J, Firmino H, Vaz-Serra A, Mukaetova-Ladinska EB. The neuroinflammatory hypothesis of delirium. Acta Neuropathol. 2010;119:737–54.
pubmed: 20309566
van Gool WA, van de Beek D, Eikelenboom P. Systemic infection and delirium: when cytokines and acetylcholine collide. Lancet. 2010;375:773–5.
pubmed: 20189029
Pandharipande PP, Girard TD, Jackson JC, Morandi A, Thompson JL, Pun BT, Brummel NE, Hughes CG, Vasilevskis EE, Shintani AK, Moons KG, Geevarghese SK, Canonico A, Hopkins RO, Bernard GR, Dittus RS, Ely EW and Investigators B-IS. Long-term cognitive impairment after critical illness. N Engl J Med. 2013;369:1306–16.
Davis DH, Muniz Terrera G, Keage H, Rahkonen T, Oinas M, Matthews FE, Cunningham C, Polvikoski T, Sulkava R, MacLullich AM, Brayne C. Delirium is a strong risk factor for dementia in the oldest-old: a population-based cohort study. Brain. 2012;135:2809–16.
pubmed: 22879644 pmcid: 3437024
Lee N, Chan PK, Hui DS, Rainer TH, Wong E, Choi KW, Lui GC, Wong BC, Wong RY, Lam WY, Chu IM, Lai RW, Cockram CS, Sung JJ. Viral loads and duration of viral shedding in adult patients hospitalized with influenza. J Infect Dis. 2009;200:492–500.
pubmed: 19591575
Group RC, Horby P, Lim WS, Emberson JR, Mafham M, Bell JL, Linsell L, Staplin N, Brightling C, Ustianowski A, Elmahi E, Prudon B, Green C, Felton T, Chadwick D, Rege K, Fegan C, Chappell LC, Faust SN, Jaki T, Jeffery K, Montgomery A, Rowan K, Juszczak E, Baillie JK, Haynes R, Landray MJ. Dexamethasone in Hospitalized Patients with Covid-19. N Engl J Med. 2021;384:693–704.
Ostergaard L. SARS CoV-2 related microvascular damage and symptoms during and after COVID-19: Consequences of capillary transit-time changes, tissue hypoxia and inflammation. Physiol Rep. 2021;9:e14726.
pubmed: 33523608 pmcid: 7849453
Ambrosino P, Calcaterra I, Molino A, Moretta P, Lupoli R, Spedicato GA, Papa A, Motta A, Maniscalco M and Di Minno MND. Persistent Endothelial Dysfunction in Post-Acute COVID-19 Syndrome: A Case-Control Study. Biomedicines. 2021;9.
Andrianto, Al-Farabi MJ, Nugraha RA, Marsudi BA and Azmi Y. Biomarkers of endothelial dysfunction and outcomes in coronavirus disease 2019 (COVID-19) patients: A systematic review and meta-analysis. Microvasc Res. 2021;138:104224.
Charfeddine S, Ibn Hadj Amor H, Jdidi J, Torjmen S, Kraiem S, Hammami R, Bahloul A, Kallel N, Moussa N, Touil I, Ghrab A, Elghoul J, Meddeb Z, Thabet Y, Kammoun S, Bouslama K, Milouchi S, Abdessalem S and Abid L. Long COVID 19 Syndrome: Is It Related to Microcirculation and Endothelial Dysfunction? Insights From TUN-EndCOV Study. Front Cardiovasc Med. 2021;8:745758.
Jud P, Gressenberger P, Muster V, Avian A, Meinitzer A, Strohmaier H, Sourij H, Raggam RB, Stradner MH, Demel U, Kessler HH, Eller K, Brodmann M. Evaluation of Endothelial Dysfunction and Inflammatory Vasculopathy After SARS-CoV-2 Infection-A Cross-Sectional Study. Front Cardiovasc Med. 2021;8:750887.
pubmed: 34722682 pmcid: 8549830
Mejia-Renteria H, Travieso A, Sagir A, Martinez-Gomez E, Carrascosa-Granada A, Toya T, Nunez-Gil IJ, Estrada V, Lerman A, Escaned J. In-vivo evidence of systemic endothelial vascular dysfunction in COVID-19. Int J Cardiol. 2021;345:153–5.
pubmed: 34706286 pmcid: 8542397
Mezoh G, Crowther NJ. Endothelial Dysfunction as a Primary Consequence of SARS-CoV-2 Infection. Adv Exp Med Biol. 2021;1321:33–43.
pubmed: 33656711
Moretta P, Maniscalco M, Papa A, Lanzillo A, Trojano L, Ambrosino P. Cognitive impairment and endothelial dysfunction in convalescent COVID-19 patients undergoing rehabilitation. Eur J Clin Invest. 2022;52:e13726.
pubmed: 34921559
Prasad M, Leon M, Lerman LO, Lerman A. Viral Endothelial Dysfunction: A Unifying Mechanism for COVID-19. Mayo Clin Proc. 2021;96:3099–108.
pubmed: 34863398
Ruhl L, Pink I, Kuhne JF, Beushausen K, Keil J, Christoph S, Sauer A, Boblitz L, Schmidt J, David S, Jack HM, Roth E, Cornberg M, Schulz TF, Welte T, Hoper MM, Falk CS. Endothelial dysfunction contributes to severe COVID-19 in combination with dysregulated lymphocyte responses and cytokine networks. Signal Transduct Target Ther. 2021;6:418.
pubmed: 34893580 pmcid: 8661333
Sabioni L, De Lorenzo A, Lamas C, Muccillo F, Castro-Faria-Neto HC, Estato V, Tibirica E. Systemic microvascular endothelial dysfunction and disease severity in COVID-19 patients: Evaluation by laser Doppler perfusion monitoring and cytokine/chemokine analysis. Microvasc Res. 2020;134:104119.
pubmed: 33278457 pmcid: 7710468
Sashindranath M, Nandurkar HH. Endothelial Dysfunction in the Brain: Setting the Stage for Stroke and Other Cerebrovascular Complications of COVID-19. Stroke. 2021;52:1895–904.
pubmed: 33794655 pmcid: 8078121
Seitz A, Ong P. Endothelial dysfunction in COVID-19: A potential predictor of long-COVID? Int J Cardiol. 2022;349:155–6.
pubmed: 34838682
Wagner JUG, Bojkova D, Shumliakivska M, Luxan G, Nicin L, Aslan GS, Milting H, Kandler JD, Dendorfer A, Heumueller AW, Fleming I, Bibli SI, Jakobi T, Dieterich C, Zeiher AM, Ciesek S, Cinatl J, Dimmeler S. Increased susceptibility of human endothelial cells to infections by SARS-CoV-2 variants. Basic Res Cardiol. 2021;116:42.
pubmed: 34224022 pmcid: 8256413
Balasubramanian P, Kiss T, Tarantini S, Nyul-Toth A, Ahire C, Yabluchanskiy A, Csipo T, Lipecz A, Tabak A, Institoris A, Csiszar A, Ungvari Z. Obesity-induced cognitive impairment in older adults: a microvascular perspective. Am J Physiol Heart Circ Physiol. 2021;320:H740–61.
pubmed: 33337961
Wilson JE, Mart MF, Cunningham C, Shehabi Y, Girard TD, MacLullich AMJ, Slooter AJC, Ely EW. Delirium. Nat Rev Dis Primers. 2020;6:90
Revello MG, Gerna G. Human cytomegalovirus tropism for endothelial/epithelial cells: scientific background and clinical implications. Rev Med Virol. 2010;20:136–55.
pubmed: 20084641
McNaughton CD, Adams NM, Johnson CH, Ward MJ, Lasko TA. Diurnal variation in SARS-CoV-2 PCR test results: Test accuracy may vary by time of day. medRxiv. 2021:2021.03.12.21253015.
Vena A, Taramasso L, Di Biagio A, Mikulska M, Dentone C, De Maria A, Magnasco L, Nicolini LA, Bruzzone B, Icardi G, Orsi A, Pelosi P, Ball L, Battaglini D, Brunetti I, Loconte M, Patroniti NA, Robba C, Bavastro M, Cerchiaro M, Giacobbe DR, Schiavetti I, Berruti M, Bassetti M and group Gs. Prevalence and Clinical Significance of Persistent Viral Shedding in Hospitalized Adult Patients with SARS-CoV-2 Infection: A Prospective Observational Study. Infect Dis Ther. 2021;10:387–398.
Yu F, Yan L, Wang N, Yang S, Wang L, Tang Y, Gao G, Wang S, Ma C, Xie R, Wang F, Tan C, Zhu L, Guo Y, Zhang F. Quantitative Detection and Viral Load Analysis of SARS-CoV-2 in Infected Patients. Clin Infect Dis. 2020;71:793–8.
pubmed: 32221523

Auteurs

Ayush Batra (A)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.
Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Jeffrey R Clark (JR)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Anthony K Kang (AK)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Sareen Ali (S)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Tulsi R Patel (TR)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Nathan A Shlobin (NA)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Steven C Hoffman (SC)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Patrick H Lim (PH)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Zachary S Orban (ZS)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Lavanya Visvabharathy (L)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Edith L Graham (EL)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

David P Sullivan (DP)

Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

William A Muller (WA)

Department of Pathology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Sherry H-Y Chou (SH)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Zoltán Ungvári (Z)

Vascular Cognitive Impairment and Neurodegeneration Program, Oklahoma Center for Geroscience and Healthy Brain Aging, Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
International Training Program in Geroscience, Doctoral School of Basic and Translational Medicine/Department of Public Health, Semmelweis University, Budapest, Hungary.
Department of Health Promotion Sciences, College of Public Health, University of Oklahoma Health Sciences Center, Oklahoma City, OK, USA.
The Peggy and Charles Stephenson Cancer Center, University of Oklahoma Health Sciences Center, Oklahoma City, OK, 73104, USA.

Igor J Koralnik (IJ)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA.

Eric M Liotta (EM)

Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL, USA. Eric.Liotta@northwestern.edu.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH