Generic placeholder image

Cardiovascular & Hematological Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5257
ISSN (Online): 1875-6182

Review Article

Coagulopathy and Brain Injury Pathogenesis in Post-Covid-19 Syndrome

Author(s): Basheer Abdullah Marzoog*

Volume 20, Issue 3, 2022

Published on: 22 June, 2022

Page: [178 - 188] Pages: 11

DOI: 10.2174/1871525720666220405124021

Price: $65

Abstract

The post-COVID neurological syndrome has been coined, which describes the functional and structural sequelae of coronavirus infection disease-19 (COVID-19) in the brain. Mild/severe manifestations of the post-COVID neurological syndrome have been identified in approximately 33.00% of COVID-19 survivors. The presence of neurological complications after COVID allowed neuropathologists to investigate in-depth the role of viral infection in neurons. The pathophysiology of the post-COVID neurological syndrome involved the development of a systematic response, including coagulopathy characterized by the formation of microthrombi. Coagulopathy, an old term for a new disease, describes the discrepancy between pro-coagulant and anticoagulant systems due to overexpression of pro-coagulant substances and or their receptors in addition to suppression of the anticoagulant molecules and or their receptors. Vascular endothelial cells and hepatocytes play a central role in the regulation of hemostasis that is disrupted during the acute phase response (APR) of coronavirus-19 (COVID-19). Currently, coagulopathy and inflammation are termed together since both form a complementary system, indicated by the elevation of inflammatory biomarkers (APR) and fibrinolysis biomarkers (D-dimer/fibrin). The later events of the post-COVID neurological syndrome are primarily induced by coagulopathy and direct viral tropism. Therefore, the paper introduces the hypothesis of coagulopathy induced post-COVID neurological syndrome.

Keywords: Homeostasis & hemostasis, COVID-19 & SARS-CoV2, coagulopathy, endothelial dysfunction, pathogenesis & pathophysiology, post-COVID syndrome, neurology.

Graphical Abstract

[1]
Wijeratne, T.; Crewther, S. Post-COVID 19 Neurological Syndrome (PCNS); a novel syndrome with challenges for the global neurology community. J. Neurol. Sci., 2020, 419, 117179.
[2]
Wijeratne, T.; Crewther, S. COVID-19 and long-term neurological problems: Challenges ahead with post-COVID-19 neurological syndrome. Aust. J. Gen. Pract., 2021, 12, 50.
[http://dx.doi.org/10.31128/AJGP-COVID-43]
[3]
Taquet, M.; Geddes, J.R.; Husain, M.; Luciano, S.; Harrison, P.J. 6-month neurological and psychiatric outcomes in 236 379 survivors of COVID-19: A retrospective cohort study using electronic health records. Lancet Psychiatry, 2021, 8(5), 416-427.
[http://dx.doi.org/10.1016/S2215-0366(21)00084-5] [PMID: 33836148]
[4]
Iadecola, C.; Anrather, J.; Kamel, H. Effects of COVID-19 on the nervous system. Cell, 2020, 183(1), 16-27.e1.
[http://dx.doi.org/10.1016/j.cell.2020.08.028] [PMID: 32882182]
[5]
Pun, B.T.; Badenes, R.; Heras La Calle, G.; Orun, O.M.; Chen, W.; Raman, R.; Simpson, B.K.; Wilson-Linville, S.; Hinojal Olmedillo, B.; Vallejo de la Cueva, A.; van der Jagt, M.; Navarro Casado, R.; Leal Sanz, P.; Orhun, G.; Ferrer Gómez, C.; Núñez Vázquez, K.; Piñeiro Otero, P.; Taccone, F.S.; Gallego Curto, E.; Caricato, A.; Woien, H.; Lacave, G.; O’Neal, H.R., Jr; Peterson, S.J.; Brummel, N.E.; Girard, T.D.; Ely, E.W.; Pandharipande, P.P. COVID-19 Intensive Care International Study Group. Prevalence and risk factors for delirium in critically ill patients with COVID-19 (COVID-D): A multicentre cohort study. Lancet Respir. Med., 2021, 9(3), 239-250.
[http://dx.doi.org/10.1016/S2213-2600(20)30552-X] [PMID: 33428871]
[6]
Camargo-Martínez, W.; Lozada-Martínez, I.; Escobar-Collazos, A.; Navarro-Coronado, A.; Moscote-Salazar, L.; Pacheco-Hernández, A.; Janjua, T.; Bosque-Varela, P. Post-COVID 19 neurological syndrome: Implications for sequelae’s treatment. J. Clin. Neurosci., 2021, 88, 219-225.
[http://dx.doi.org/10.1016/j.jocn.2021.04.001] [PMID: 33992187]
[7]
Nuzzo, D.; Vasto, S.; Scalisi, L.; Cottone, S.; Cambula, G.; Rizzo, M.; Giacomazza, D.; Picone, P. Post-acute COVID-19 neurological syndrome: A new medical challenge. J. Clin. Med., 2021, 10(9), 1947.
[http://dx.doi.org/10.3390/jcm10091947] [PMID: 34062770]
[8]
Avula, A.; Nalleballe, K.; Narula, N. COVID-19 presenting as stroke. Brain Behav. Immun., 2020, 87, 115-119.
[9]
Saiegh, F.; Ghosh, R.; Leibold, A. Status of SARS-CoV-2 in cerebrospinal fluid of patients with COVID-19 and stroke. J. Neurol. Neurosurg. Psychiatry, 2020, 91(8), 846-848.
[http://dx.doi.org/10.1136/jnnp-2020-323522]
[10]
Giri, P.; Hong, G.; Lam, H. COVID encephalopathy in the setting of multiple bilateral acute cerebral vascular infarcts. Chest, 2020, 158, A890.
[http://dx.doi.org/10.1016/j.chest.2020.08.828]
[11]
Harapan, B.N.; Yoo, H.J. Neurological symptoms, manifestations, and complications associated with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease 19 (COVID-19). J. Neurol., 2021, 268(9), 3059-3071.
[http://dx.doi.org/10.1007/s00415-021-10406-y] [PMID: 33486564]
[12]
Hallal-Peche, F.; Aguilera-Vergara, M.; Guzmán-Méndez, M.; González-Mendoza, C.; Armas-Zurita, R.; Garzón-Pulido, T.; Moreno-Jiménez, C.; Villar Royo-Martínez, M. Utilidad y valor pronóstico del electroencefalograma en la COVID-19 y la encefalopatía: Patrones electroencefalográficos en una serie de casos. Rev. Neurol., 2020, 71(12), 431-437.
[http://dx.doi.org/10.33588/rn.7112.2020236] [PMID: 33319345]
[13]
Vollono, C.; Rollo, E.; Romozzi, M.; Frisullo, G.; Servidei, S.; Borghetti, A.; Calabresi, P. Focal status epilepticus as unique clinical feature of COVID-19: A case report. Seizure, 2020, 78, 109-112.
[http://dx.doi.org/10.1016/j.seizure.2020.04.009] [PMID: 32344366]
[14]
Panda, P.K.; Sharawat, I.K.; Panda, P. Neurological complications of SARS-CoV-2 infection in children: A systematic review and meta-analysis. J. Trop. Pediatr., 2021, 67(3), fmaa070.
[http://dx.doi.org/10.1093/tropej/fmaa070] [PMID: 32910826]
[15]
Wang, Z.; Yang, Y.; Liang, X.; Gao, B.; Liu, M.; Li, W.; Chen, Z.; Wang, Z. COVID-19 Associated ischemic stroke and hemorrhagic stroke: Incidence, potential pathological mechanism, and management. Front. Neurol., 2020, 11, 571996.
[http://dx.doi.org/10.3389/fneur.2020.571996] [PMID: 33193019]
[16]
Liotta, E.M.; Batra, A.; Clark, J.R.; Shlobin, N.A.; Hoffman, S.C.; Orban, Z.S.; Koralnik, I.J. Frequent neurologic manifestations and encephalopathy-associated morbidity in Covid-19 patients. Ann. Clin. Transl. Neurol., 2020, 7(11), 2221-2230.
[http://dx.doi.org/10.1002/acn3.51210] [PMID: 33016619]
[17]
Needham, E.; Newcombe, V.; Michell, A. Mononeuritis multiplex: An unexpectedly frequent feature of severe COVID-19. J. Neurol., 2020, 268(8), 2685-2689.
[http://dx.doi.org/10.1007/s00415-020-10321-8] [PMID: 33244712]
[18]
El Aidaoui, K.; Ait Benhamou, R.; Hazim, A.; Haoudar, A.; El Kettani, C. COVID-19: A potential cause of non-convulsive status epilepticus. Cureus, 2021, 13(5), e15041.
[http://dx.doi.org/10.7759/cureus.15041] [PMID: 34150392]
[19]
Lazarte-Rantes, C.; Guevara-Castañón, J.; Romero, L.; Guillén-Pinto, D. Acute necrotizing encephalopathy associated with SARS-CoV-2 exposure in a pediatric patient. Cureus, 2021, 13(5), e15018.
[http://dx.doi.org/10.7759/cureus.15018] [PMID: 34017667]
[20]
Wijeratne, T.; Gillard Crewther, S.; Sales, C.; Karimi, L. COVID-19 Pathophysiology predicts that ischemic stroke occurrence is an expectation, not an exception-a systematic review. Front. Neurol., 2021, 11, 607221.
[http://dx.doi.org/10.3389/fneur.2020.607221] [PMID: 33584506]
[21]
Sharifian-Dorche, M.; Huot, P.; Osherov, M.; Wen, D.; Saveriano, A.; Giacomini, P.S.; Antel, J.P.; Mowla, A. Neurological complications of coronavirus infection; a comparative review and lessons learned during the COVID-19 pandemic. J. Neurol. Sci., 2020, 417, 117085.
[http://dx.doi.org/10.1016/j.jns.2020.117085] [PMID: 32871412]
[22]
Beyrouti, R.; Adams, M.; Benjamin, L. Characteristics of ischaemic stroke associated with COVID-19. J. Neurol. Neurosurg. Psychiatry, 2020, 91(8), 889-891.
[http://dx.doi.org/10.1136/jnnp-2020-323586]
[23]
Showers, C.R.; Nuovo, G.J.; Lakhanpal, A.; Siegel, C.H.; Aizer, J.; Elreda, L.; Halevi, A.; Lai, A.R.; Erkan, D.; Magro, C.M.A. Covid-19 patient with complement-mediated coagulopathy and severe thrombosis. Pathobiology, 2021, 88(1), 28-36.
[http://dx.doi.org/10.1159/000512503] [PMID: 33137805]
[24]
Grillet, F.; Behr, J.; Calame, P.; Aubry, S.; Delabrousse, E. Acute pulmonary embolism associated with COVID-19 pneumonia detected with pulmonary CT angiography. Radiology, 2020, 296(3), E186-E188.
[http://dx.doi.org/10.1148/radiol.2020201544] [PMID: 32324103]
[25]
Poissy, J.; Goutay, J.; Caplan, M.; Parmentier, E.; Duburcq, T.; Lassalle, F.; Jeanpierre, E.; Rauch, A.; Labreuche, J.; Susen, S. Lille ICU Haemostasis COVID-19 Group. Pulmonary embolism in patients with COVID-19: Awareness of an increased prevalence. Circulation, 2020, 142(2), 184-186.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.120.047430] [PMID: 32330083]
[26]
Léonard-Lorant, I.; Delabranche, X.; Séverac, F.; Helms, J.; Pauzet, C.; Collange, O.; Schneider, F.; Labani, A.; Bilbault, P.; Molière, S.; Leyendecker, P.; Roy, C.; Ohana, M. Acute pulmonary embolism in patients with COVID-19 at CT angiography and relationship to d-dimer levels. Radiology, 2020, 296(3), E189-E191.
[http://dx.doi.org/10.1148/radiol.2020201561] [PMID: 32324102]
[27]
Poyiadji, N.; Cormier, P.; Patel, P.Y.; Hadied, M.O.; Bhargava, P.; Khanna, K.; Nadig, J.; Keimig, T.; Spizarny, D.; Reeser, N.; Klochko, C.; Peterson, E.L.; Song, T. Acute pulmonary embolism and COVID-19. Radiology, 2020, 297(3), E335-E338.
[http://dx.doi.org/10.1148/radiol.2020201955] [PMID: 32407256]
[28]
Si-Mohamed, S.; Chebib, N.; Sigovan, M.; Zumbihl, L.; Turquier, S.; Boccalini, S.; Boussel, L.; Mornex, J.F.; Cottin, V.; Douek, P. In vivo demonstration of pulmonary microvascular involvement in COVID-19 using dual-energy computed tomography. Eur. Respir. J., 2020, 56(4), 2002608.
[http://dx.doi.org/10.1183/13993003.02608-2020] [PMID: 32943402]
[29]
Vyas, V.; Kanagalingam, G.; Yadava, S.; Gambhir, H.S.; Costanza, M.; Chaudhuri, D. Bilateral pulmonary artery thrombectomy with saddle embolism and COVID-19 infection. Proc. Bayl. Univ. Med. Cent., 2020, 33(4), 666-667.
[http://dx.doi.org/10.1080/08998280.2020.1799133] [PMID: 33100564]
[30]
Hammer, M.M.; Hunsaker, A.R.; Gooptu, M.; Hatabu, H. Frequency of pulmonary embolism in patients with COVID-19. JACC Cardiovasc. Imaging, 2020, 13(11), 2478-2479.
[http://dx.doi.org/10.1016/j.jcmg.2020.09.006] [PMID: 33153537]
[31]
Giusti, B.; Gori, A.M.; Alessi, M.; Rogolino, A.; Lotti, E.; Poli, D.; Sticchi, E.; Bartoloni, A.; Morettini, A.; Nozzoli, C.; Peris, A.; Pieralli, F.; Poggesi, L.; Marchionni, N.; Marcucci, R. Sars-CoV-2 induced coagulopathy and prognosis in hospitalized patients: A snapshot from Italy. Thromb. Haemost., 2020, 120(8), 1233-1236.
[http://dx.doi.org/10.1055/s-0040-1712918] [PMID: 32455440]
[32]
Tang, N.; Li, D.; Wang, X. Abnormal coagulation parameters are associated with poor prognosis in patients with novel coronavirus pneumonia. J. Thromb. Haemost., 2020, 18, 844-847.
[http://dx.doi.org/10.1111/jth.14768]
[33]
Klok, F.A.; Kruip, M.J.H.A.; van der Meer, N.J.M.; Arbous, M.S.; Gommers, D.A.M.P.J.; Kant, K.M.; Kaptein, F.H.J.; van Paassen, J.; Stals, M.A.M.; Huisman, M.V.; Endeman, H. Incidence of thrombotic complications in critically ill ICU patients with COVID-19. Thromb. Res., 2020, 191, 145-147.
[http://dx.doi.org/10.1016/j.thromres.2020.04.013] [PMID: 32291094]
[34]
Middeldorp, S.; Coppens, M.; van Haaps, T.F.; Foppen, M.; Vlaar, A.P.; Müller, M.C.A.; Bouman, C.C.S.; Beenen, L.F.M.; Kootte, R.S.; Heijmans, J.; Smits, L.P.; Bonta, P.I.; van Es, N. Incidence of venous thromboembolism in hospitalized patients with COVID-19. J. Thromb. Haemost., 2020, 18(8), 1995-2002.
[http://dx.doi.org/10.1111/jth.14888] [PMID: 32369666]
[35]
Helms, J.; Tacquard, C.; Severac, F.; Leonard-Lorant, I.; Ohana, M.; Delabranche, X.; Merdji, H.; Clere-Jehl, R.; Schenck, M.; Fagot Gandet, F.; Fafi-Kremer, S.; Castelain, V.; Schneider, F.; Grunebaum, L.; Anglés-Cano, E.; Sattler, L.; Mertes, P.M.; Meziani, F. High risk of thrombosis in patients with severe SARS-CoV-2 infection: A multicenter prospective cohort study. Intensive Care Med., 2020, 46(6), 1089-1098.
[http://dx.doi.org/10.1007/s00134-020-06062-x] [PMID: 32367170]
[36]
Ventura-Díaz, S.; Quintana-Pérez, J.V.; Gil-Boronat, A.; Herrero-Huertas, M.; Gorospe-Sarasúa, L.; Montilla, J.; Acosta-Batlle, J.; Blázquez-Sánchez, J.; Vicente-Bártulos, A. A higher D-dimer threshold for predicting pulmonary embolism in patients with COVID-19: A retrospective study. Emerg. Radiol., 2020, 27(6), 679-689.
[http://dx.doi.org/10.1007/s10140-020-01859-1] [PMID: 33025219]
[37]
Wichmann, D.; Sperhake, J.P.; Lütgehetmann, M.; Steurer, S.; Edler, C.; Heinemann, A.; Heinrich, F.; Mushumba, H.; Kniep, I.; Schröder, A.S.; Burdelski, C.; de Heer, G.; Nierhaus, A.; Frings, D.; Pfefferle, S.; Becker, H.; Bredereke-Wiedling, H.; de Weerth, A.; Paschen, H.R.; Sheikhzadeh-Eggers, S.; Stang, A.; Schmiedel, S.; Bokemeyer, C.; Addo, M.M.; Aepfelbacher, M.; Püschel, K.; Kluge, S. Autopsy findings and venous thromboembolism in patients with COVID-19: A prospective cohort study. Ann. Intern. Med., 2020, 173(4), 268-277.
[http://dx.doi.org/10.7326/M20-2003] [PMID: 32374815]
[38]
Malas, M.B.; Naazie, I.N.; Elsayed, N.; Mathlouthi, A.; Marmor, R.; Clary, B. Thromboembolism risk of COVID-19 is high and associated with a higher risk of mortality: A systematic review and meta-analysis. EClinicalMedicine, 2020, 29, 100639.
[http://dx.doi.org/10.1016/j.eclinm.2020.100639] [PMID: 33251499]
[39]
Huang, C.; Wang, Y.; Li, X. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet, 2020, 395, 497-506.
[40]
Guan, W.J.; Ni, Z.Y.; Hu, Y.; Liang, W.H.; Ou, C.Q.; He, J.X.; Liu, L.; Shan, H.; Lei, C.L.; Hui, D.S.C.; Du, B.; Li, L.J.; Zeng, G.; Yuen, K.Y.; Chen, R.C.; Tang, C.L.; Wang, T.; Chen, P.Y.; Xiang, J.; Li, S.Y.; Wang, J.L.; Liang, Z.J.; Peng, Y.X.; Wei, L.; Liu, Y.; Hu, Y.H.; Peng, P.; Wang, J.M.; Liu, J.Y.; Chen, Z.; Li, G.; Zheng, Z.J.; Qiu, S.Q.; Luo, J.; Ye, C.J.; Zhu, S.Y.; Zhong, N.S. China Medical Treatment Expert Group for Covid-19. Clinical characteristics of coronavirus disease 2019 in China. N. Engl. J. Med., 2020, 382(18), 1708-1720.
[http://dx.doi.org/10.1056/NEJMoa2002032] [PMID: 32109013]
[41]
Sakka, M.; Connors, J.M.; Hékimian, G.; Martin-Toutain, I.; Crichi, B.; Colmegna, I.; Bonnefont-Rousselot, D.; Farge, D.; Frere, C. Association between D-Dimer levels and mortality in patients with coronavirus disease 2019 (COVID-19): A systematic review and pooled analysis. J. Med. Vasc., 2020, 45(5), 268-274.
[http://dx.doi.org/10.1016/j.jdmv.2020.05.003] [PMID: 32862984]
[42]
Lazzeri, C.; Bonizzoli, M.; Franci, A.; Socci, F.; Peris, A. Pulmonary embolism and screening for concomitant proximal deep vein thrombosis in noncritically ill hospitalized patients with coronavirus disease 2019. Intern. Emerg. Med., 2020, 15(6), 1081-1083.
[http://dx.doi.org/10.1007/s11739-020-02460-7] [PMID: 32729026]
[43]
Pieralli, F.; Pomero, F.; Giampieri, M.; Marcucci, R.; Prisco, D.; Luise, F.; Mancini, A.; Milia, A.; Sammicheli, L.; Tassinari, I.; Caldi, F.; Innocenti, F.; Faraone, A.; Beltrame, C.; Pini, R.; Ungar, A.; Fortini, A. Incidence of deep vein thrombosis through an ultrasound surveillance protocol in patients with COVID-19 pneumonia in non-ICU setting: A multicenter prospective study. PLoS One, 2021, 16(5), e0251966.
[http://dx.doi.org/10.1371/journal.pone.0251966] [PMID: 34015018]
[44]
Santoliquido, A.; Porfidia, A.; Nesci, A.; De Matteis, G.; Marrone, G.; Porceddu, E.; Cammà, G.; Giarretta, I.; Fantoni, M.; Landi, F.; Gasbarrini, A.; Pola, R.; D’Alfonso, M.E.; Lo Monaco, M.R. Gemelli Against COVID-19 Group. Incidence of deep vein thrombosis among non-ICU patients hospitalized for COVID-19 despite pharmacological thromboprophylaxis. J. Thromb. Haemost., 2020, 18(9), 2358-2363.
[http://dx.doi.org/10.1111/jth.14992] [PMID: 32633068]
[45]
Parekh, Y.H.; Altomare, N.J.; McDonnell, E.P.; Blaser, M.J.; Parikh, P.D. Recurrence of upper extremity deep vein thrombosis secondary to COVID-19. Viruses, 2021, 13(5), 878.
[http://dx.doi.org/10.3390/v13050878] [PMID: 34064763]
[46]
Zhang, Y.; Xiao, M.; Zhang, S.; Xia, P.; Cao, W.; Jiang, W.; Chen, H.; Ding, X.; Zhao, H.; Zhang, H.; Wang, C.; Zhao, J.; Sun, X.; Tian, R.; Wu, W.; Wu, D.; Ma, J.; Chen, Y.; Zhang, D.; Xie, J.; Yan, X.; Zhou, X.; Liu, Z.; Wang, J.; Du, B.; Qin, Y.; Gao, P.; Qin, X.; Xu, Y.; Zhang, W.; Li, T.; Zhang, F.; Zhao, Y.; Li, Y.; Zhang, S. Coagulopathy and antiphospholipid antibodies in patients with Covid-19. N. Engl. J. Med., 2020, 382(17), e38.
[http://dx.doi.org/10.1056/NEJMc2007575] [PMID: 32268022]
[47]
Bowles, L.; Platton, S.; Yartey, N.; Dave, M.; Lee, K.; Hart, D.P.; MacDonald, V.; Green, L.; Sivapalaratnam, S.; Pasi, K.J.; MacCallum, P. Lupus anticoagulant and abnormal coagulation tests in patients with covid-19. N. Engl. J. Med., 2020, 383(3), 288-290.
[http://dx.doi.org/10.1056/NEJMc2013656] [PMID: 32369280]
[48]
Harzallah, I.; Debliquis, A.; Drénou, B. Lupus anticoagulant is frequent in patients with Covid-19. J. Thromb. Haemost., 2020, 18(8), 2064-2065.
[http://dx.doi.org/10.1111/jth.14867] [PMID: 32324958]
[49]
Hossri, S.; Shadi, M.; Hamarsha, Z.; Schneider, R.; El-Sayegh, D. Clinically significant anticardiolipin antibodies associated with COVID-19. J. Crit. Care, 2020, 59, 32-34.
[http://dx.doi.org/10.1016/j.jcrc.2020.05.017] [PMID: 32512349]
[50]
Zuo, Y.; Estes, S.; Ali, R. Prothrombotic antiphospholipid antibodies in COVID-19. medRxiv, 2020, 2020.06.15.20131607.
[http://dx.doi.org/10.1101/2020.06.15.20131607]
[51]
Marzoog, B.A.; Vlasova, T.I. Membrane lipids under norm and pathology. Eur. J. Clin. Exp. Med., 2021, 19, 59-75.
[http://dx.doi.org/10.15584/ejcem.2021.1.9]
[52]
Marzoog, B.A.; Vlasova, T.I. Anticoagulant status under COVID 19: The potential pathophysiological mechanism. J. Appl. Hematol, 2021.
[http://dx.doi.org/10.4103/joah.joah_154_21]
[53]
Popkin, B.M.; Du, S.; Green, W.D.; Beck, M.A.; Algaith, T.; Herbst, C.H.; Alsukait, R.F.; Alluhidan, M.; Alazemi, N.; Shekar, M. Individuals with obesity and COVID-19: A global perspective on the epidemiology and biological relationships. Obes. Rev., 2020, 21(11), e13128.
[http://dx.doi.org/10.1111/obr.13128] [PMID: 32845580]
[54]
Jambusaria, A.; Hong, Z.; Zhang, L.; Srivastava, S.; Jana, A.; Toth, P.T.; Dai, Y.; Malik, A.B.; Rehman, J. Endothelial heterogeneity across distinct vascular beds during homeostasis and inflammation. eLife, 2020, 9, e51413.
[http://dx.doi.org/10.7554/eLife.51413] [PMID: 31944177]
[55]
Gris, J-C.C.; Perez-Martin, A.; Quéré, I.; Sotto, A. COVID-19 associated coagulopathy: The crowning glory of thrombo-inflammation concept. Anaesth. Crit. Care Pain Med., 2020, 39(3), 381-382.
[http://dx.doi.org/10.1016/j.accpm.2020.04.013] [PMID: 32418867]
[56]
Hultström, M.; Fromell, K.; Larsson, A. Elevated angiopoietin-2 inhibits thrombomodulin-mediated anticoagulation in critically ill COVID-19 patients. medRxiv, 2021, 2021.01.13.21249429.
[http://dx.doi.org/10.1101/2021.01.13.21249429]
[57]
Ferreira, C.N.; Sousa, M de O.; Dusse, L.M.S. A cell-based model of coagulation and its implications. Rev. Bras. Hematol. Hemoter., 2010, 32, 416-421.
[http://dx.doi.org/10.1590/S1516-84842010000500016]
[58]
Ranucci, M.; Ballotta, A.; Di Dedda, U.; Baryshnikova, E.; Dei Poli, M.; Resta, M.; Falco, M.; Albano, G.; Menicanti, L. The procoagulant pattern of patients with COVID-19 acute respiratory distress syndrome. J. Thromb. Haemost., 2020, 18(7), 1747-1751.
[http://dx.doi.org/10.1111/jth.14854] [PMID: 32302448]
[59]
Fried, J.A.; Ramasubbu, K.; Bhatt, R.; Topkara, V.K.; Clerkin, K.J.; Horn, E.; Rabbani, L.; Brodie, D.; Jain, S.S.; Kirtane, A.J.; Masoumi, A.; Takeda, K.; Kumaraiah, D.; Burkhoff, D.; Leon, M.; Schwartz, A.; Uriel, N.; Sayer, G. The variety of cardiovascular presentations of COVID-19. Circulation, 2020, 141(23), 1930-1936.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.120.047164] [PMID: 32243205]
[60]
Pedersen, S.F.; Ho, Y.C. SARS-CoV-2: A storm is raging. J. Clin. Invest., 2020, 130(5), 2202-2205.
[http://dx.doi.org/10.1172/JCI137647] [PMID: 32217834]
[61]
Morgul, E.; Bener, A.; Atak, M.; Akyel, S.; Aktaş, S.; Bhugra, D.; Ventriglio, A.; Jordan, T.R. COVID-19 pandemic and psychological fatigue in Turkey. Int. J. Soc. Psychiatry, 2021, 67(2), 128-135.
[http://dx.doi.org/10.1177/0020764020941889] [PMID: 32650681]
[62]
Huang, C.; Huang, L.; Wang, Y.; Li, X.; Ren, L.; Gu, X.; Kang, L.; Guo, L.; Liu, M.; Zhou, X.; Luo, J.; Huang, Z.; Tu, S.; Zhao, Y.; Chen, L.; Xu, D.; Li, Y.; Li, C.; Peng, L.; Li, Y.; Xie, W.; Cui, D.; Shang, L.; Fan, G.; Xu, J.; Wang, G.; Wang, Y.; Zhong, J.; Wang, C.; Wang, J.; Zhang, D.; Cao, B. 6-month consequences of COVID-19 in patients discharged from hospital: A cohort study. Lancet, 2021, 397(10270), 220-232.
[http://dx.doi.org/10.1016/S0140-6736(20)32656-8] [PMID: 33428867]
[63]
Espíndola, O.M.; Brandão, C.O.; Gomes, Y.C.P.; Siqueira, M.; Soares, C.N.; Lima, M.A.S.D.; Leite, A.C.C.B.; Torezani, G.; Araujo, A.Q.C.; Silva, M.T.T. Cerebrospinal fluid findings in neurological diseases associated with COVID-19 and insights into mechanisms of disease development. Int. J. Infect. Dis., 2021, 102, 155-162.
[http://dx.doi.org/10.1016/j.ijid.2020.10.044] [PMID: 33127503]
[64]
Cantuti-Castelvetri, L.; Ojha, R.; Pedro, L.D.; Djannatian, M.; Franz, J.; Kuivanen, S.; van der Meer, F.; Kallio, K.; Kaya, T.; Anastasina, M.; Smura, T.; Levanov, L.; Szirovicza, L.; Tobi, A.; Kallio-Kokko, H.; Österlund, P.; Joensuu, M.; Meunier, F.A.; Butcher, S.J.; Winkler, M.S.; Mollenhauer, B.; Helenius, A.; Gokce, O.; Teesalu, T.; Hepojoki, J.; Vapalahti, O.; Stadelmann, C.; Balistreri, G.; Simons, M. Neuropilin-1 facilitates SARS-CoV-2 cell entry and infectivity. Science, 2020, 370(6518), 856-860.
[http://dx.doi.org/10.1126/science.abd2985] [PMID: 33082293]
[65]
Baig, A.M.; Khaleeq, A.; Ali, U.; Syeda, H. Evidence of the COVID-19 virus targeting the CNS: Tissue distribution, host-virus interaction, and proposed neurotropic mechanisms. ACS Chem. Neurosci., 2020, 11(7), 995-998.
[http://dx.doi.org/10.1021/acschemneuro.0c00122] [PMID: 32167747]
[66]
Webb, S.; Wallace, V.C.J.; Martin-Lopez, D.; Yogarajah, M. Guillain-Barré syndrome following COVID-19: A newly emerging post-infectious complication. BMJ Case Rep., 2020, 13(6), e236182.
[http://dx.doi.org/10.1136/bcr-2020-236182] [PMID: 32540883]
[67]
Farzi, M.A.; Ayromlou, H.; Jahanbakhsh, N.; Bavil, P.H.; Janzadeh, A.; Shayan, F.K. Guillain-Barré syndrome in a patient infected with SARS-CoV-2, a case report. J. Neuroimmunol., 2020, 346, 577294.
[http://dx.doi.org/10.1016/j.jneuroim.2020.577294] [PMID: 32590125]
[68]
Khalifa, M.; Zakaria, F.; Ragab, Y.; Saad, A.; Bamaga, A.; Emad, Y.; Rasker, J.J. Guillain-Barré syndrome associated with severe acute respiratory syndrome coronavirus 2 detection and coronavirus disease 2019 in a child. J. Pediatric Infect. Dis. Soc., 2020, 9(4), 510-513.
[http://dx.doi.org/10.1093/jpids/piaa086] [PMID: 32652520]
[69]
Coen, M.; Jeanson, G.; Culebras Almeida, L.A.; Hübers, A.; Stierlin, F.; Najjar, I.; Ongaro, M.; Moulin, K.; Makrygianni, M.; Leemann, B.; Kronig, I.; Bertrand, J.; Reny, J.L.; Schibler, M.; Serratrice, J. Guillain-Barré syndrome as a complication of SARS-CoV-2 infection. Brain Behav. Immun., 2020, 87, 111-112.
[http://dx.doi.org/10.1016/j.bbi.2020.04.074] [PMID: 32360440]
[70]
Frank, C.H.M.; Almeida, T.V.R.; Marques, E.A. Guillain–barré syndrome associated with SARS-CoV-2 infection in a pediatric patient. J. Trop. Pediatr., 2021, 67(3), fmaa044.
[http://dx.doi.org/10.1093/tropej/fmaa044] [PMID: 32653906]
[71]
Lyons, S.; O’Kelly, B.; Woods, S.; Rowan, C.; Brady, D.; Sheehan, G.; Smyth, S. Seizure with CSF lymphocytosis as a presenting feature of COVID-19 in an otherwise healthy young man. Seizure, 2020, 80, 113-114.
[http://dx.doi.org/10.1016/j.seizure.2020.06.010] [PMID: 32563170]
[72]
Carroll, E.; Neumann, H.; Aguero-Rosenfeld, M.E.; Lighter, J.; Czeisler, B.M.; Melmed, K.; Lewis, A. Post-COVID-19 inflammatory syndrome manifesting as refractory status epilepticus. Epilepsia, 2020, 61(10), e135-e139.
[http://dx.doi.org/10.1111/epi.16683] [PMID: 32944946]
[73]
Elgamasy, S.; Kamel, M.G.; Ghozy, S.; Khalil, A.; Morra, M.E.; Islam, S.M.S. First case of focal epilepsy associated with SARS-coronavirus-2. J. Med. Virol., 2020, 92(10), 2238-2242.
[http://dx.doi.org/10.1002/jmv.26113] [PMID: 32484990]
[74]
Sousa, L.P.; Pinho, V.; Teixeira, M.M. Harnessing inflammation resolving-based therapeutic agents to treat pulmonary viral infections: What can the future offer to COVID-19? Br. J. Pharmacol., 2020, 177(17), 3898-3904.
[http://dx.doi.org/10.1111/bph.15164] [PMID: 32557557]
[75]
Cyprian, F.; Sohail, M.U.; Abdelhafez, I.; Salman, S.; Attique, Z.; Kamareddine, L.; Al-Asmakh, M. SARS-CoV-2 and immune-microbiome interactions: Lessons from respiratory viral infections. Int. J. Infect. Dis., 2021, 105, 540-550.
[http://dx.doi.org/10.1016/j.ijid.2021.02.071] [PMID: 33610778]
[76]
Andrianto; Al-Farabi, MJ; Nugraha, RA Biomarkers of endothelial dysfunction and outcomes in coronavirus disease 2019 (COVID-19) patients: A systematic review and meta-analysis. Microvasc. Res., 2021, 138, 104224.
[77]
Padda, I.; Khehra, N.; Jaferi, U.; Parmar, M.S. The neurological complexities and prognosis of COVID-19. SN Compr. Clin. Med., 2020, 2, 1-12.
[http://dx.doi.org/10.1007/s42399-020-00527-2] [PMID: 33015552]
[78]
Burlacu, A.; Artene, B.; Crisan-Dabija, R.; Popa, I.V.; Covic, A. Is thrombophilic genetic profile responsible for an acute ischemic stroke in a COVID-19 male patient? Clin. Appl. Thromb. Hemost., 2020, 26, 1076029620967107.
[http://dx.doi.org/10.1177/1076029620967107] [PMID: 33054360]
[79]
Kurushina, O.V.; Barulin, A.E. Effects of covid-19 on the central nervous system. Zhurnal Nevrologii i Psihiatrii imeni S.S. Korsakova, 2021, 121, 92-97.
[80]
Monroy-Gómez, J.; Torres-Fernández, O. Effects of the severe acute respiratory syndrome coronavirus (SARS-CoV) and the Middle East respiratory syndrome coronavirus (MERS-CoV) on the nervous system. What can we expect from SARS -CoV-2? Biomédica, 2020, 40(Suppl. 2), 173-179.
[PMID: 33152201]
[81]
Ellul, M.A.; Benjamin, L.; Singh, B.; Lant, S.; Michael, B.D.; Easton, A.; Kneen, R.; Defres, S.; Sejvar, J.; Solomon, T. Neurological associations of COVID-19. Lancet Neurol., 2020, 19(9), 767-783.
[http://dx.doi.org/10.1016/S1474-4422(20)30221-0] [PMID: 32622375]
[82]
Wijeratne, T.; Wijeratne, C. Clinical utility of serial systemic immune inflammation indices (SSIIi) in the context of post covid-19 neurological syndrome (PCNS). J. Neurol. Sci., 2021, 423, 117356.
[http://dx.doi.org/10.1016/j.jns.2021.117356] [PMID: 33636659]
[83]
Nuzzo, D.; Picone, P. Potential neurological effects of severe COVID-19 infection. Neurosci. Res., 2020, 158, 1-5.
[http://dx.doi.org/10.1016/j.neures.2020.06.009] [PMID: 32628969]
[84]
Lou, J.J.; Movassaghi, M.; Gordy, D. Neuropathology of COVID-19 (neuro-COVID): clinicopathological update. Free Neuropathol., 2021, 2, 2.
[http://dx.doi.org/10.17879/freeneuropathology-2021-2993]
[85]
Xu, X.W.; Wu, X.X.; Jiang, X.G.; Xu, K.J.; Ying, L.J.; Ma, C.L.; Li, S.B.; Wang, H.Y.; Zhang, S.; Gao, H.N.; Sheng, J.F.; Cai, H.L.; Qiu, Y.Q.; Li, L.J. Clinical findings in a group of patients infected with the 2019 novel coronavirus (SARS-Cov-2) outside of Wuhan, China: Retrospective case series. BMJ, 2020, 368, m606.
[http://dx.doi.org/10.1136/bmj.m606] [PMID: 32075786]
[86]
Cao, J.; Tu, W.J.; Cheng, W.; Yu, L.; Liu, Y.K.; Hu, X.; Liu, Q. Clinical features and short-term outcomes of 102 patients with coronavirus disease 2019 in Wuhan, China. Clin. Infect. Dis., 2020, 71(15), 748-755.
[http://dx.doi.org/10.1093/cid/ciaa243] [PMID: 32239127]
[87]
Wang, D.; Hu, B.; Hu, C.; Zhu, F.; Liu, X.; Zhang, J.; Wang, B.; Xiang, H.; Cheng, Z.; Xiong, Y.; Zhao, Y.; Li, Y.; Wang, X.; Peng, Z. Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA, 2020, 323(11), 1061-1069.
[http://dx.doi.org/10.1001/jama.2020.1585] [PMID: 32031570]
[88]
Wang, Z.; Yang, B.; Li, Q.; Wen, L.; Zhang, R. Clinical features of 69 cases with coronavirus disease 2019 in Wuhan, China. Clin. Infect. Dis., 2020, 71(15), 769-777.
[http://dx.doi.org/10.1093/cid/ciaa272] [PMID: 32176772]
[89]
Hessami, A.; Shamshirian, A.; Heydari, K. Cardiovascular diseases burden in COVID-19: Systematic review and meta-analysis. Am. J. Emerg. Med., 2021, 46, 382-391.
[http://dx.doi.org/10.1016/j.ajem.2020.10.022] [PMID: 33268238]
[90]
Fath, A.R.; Aglan, A.; Varkoly, K.S.; Eldaly, A.S.; Beladi, R.N.; Forlemu, A.; Mihyawi, N.; Solsi, A.; Israr, S.; Lucas, A.R. Distinct coagulopathy with myocardial injury and pulmonary embolism in COVID-19. J. Investig. Med. High Impact Case Rep., 2021, 9, 23247096211019559.
[http://dx.doi.org/10.1177/23247096211019559] [PMID: 34036814]
[91]
Mohammadi Arbati, M.; Molseghi, M.H. COVID-19 Presenting as acute necrotizing pancreatitis. J. Investig. Med. High Impact Case Rep., 2021, 9, 23247096211009393.
[http://dx.doi.org/10.1177/23247096211009393] [PMID: 33847153]
[92]
Arévalos, V.; Ortega-Paz, L.; Rodríguez-Arias, J.J.; Calvo, M.; Castrillo, L.; Salazar, A.; Roque, M.; Dantas, A.P.; Sabaté, M.; Brugaletta, S. Myocardial injury in COVID-19 patients: Association with inflammation, coagulopathy and in-hospital prognosis. J. Clin. Med., 2021, 10(10), 2096.
[http://dx.doi.org/10.3390/jcm10102096] [PMID: 34068127]
[93]
Mukherjee, A.; Ghosh, R.; Furment, M.M. Case report: COVID-19 associated renal infarction and ascending aortic thrombosis. Am. J. Trop. Med. Hyg., 2020, 103(5), 1989-1992.
[http://dx.doi.org/10.4269/ajtmh.20-0869] [PMID: 32918409]
[94]
Post, A.; den Deurwaarder, E.S.G.; Bakker, S.J.L.; de Haas, R.J.; van Meurs, M.; Gansevoort, R.T.; Berger, S.P. Kidney infarction in patients with COVID-19. Am. J. Kidney Dis., 2020, 76(3), 431-435.
[http://dx.doi.org/10.1053/j.ajkd.2020.05.004] [PMID: 32479921]
[95]
Añazco, P.H.; Balta, F.M.; Córdova-Cueva, L. Bilateral renal infarction in a patient with severe COVID-19 infection. J. Bras. Nefrol., 2021, 43(1), 127-131.
[http://dx.doi.org/10.1590/2175-8239-jbn-2020-0156] [PMID: 33460428]
[96]
Murray, N.P.; Fuentealba, C.; Reyes, E.; Salazar, A. Renal infarction associated with asymptomatic Covid-19 infection. Hematol. Transfus. Cell Ther., 2021, 43(3), 353-356.
[http://dx.doi.org/10.1016/j.htct.2021.03.008] [PMID: 34027306]
[97]
Kundal, S.V.; Emeasoba, E.U.; Harris, C. Aortic thrombosis and renal infarction in a young female with patent foramen ovale and COVID-19 antibody. Clin. Case Rep., 2021, 9, 345-349.
[98]
Huang, Z.; Huang, P.; Du, B.; Kong, L.; Zhang, W.; Zhang, Y.; Dong, J. Prevalence and clinical outcomes of cardiac injury in patients with COVID-19: A systematic review and meta-analysis. Nutr. Metab. Cardiovasc. Dis., 2021, 31(1), 2-13.
[http://dx.doi.org/10.1016/j.numecd.2020.09.004] [PMID: 33229199]
[99]
Kaafarani, H.M.A.; El Moheb, M.; Hwabejire, J.O.; Naar, L.; Christensen, M.A.; Breen, K.; Gaitanidis, A.; Alser, O.; Mashbari, H.; Bankhead-Kendall, B.; Mokhtari, A.; Maurer, L.; Kapoen, C.; Langeveld, K.; El Hechi, M.W.; Lee, J.; Mendoza, A.E.; Saillant, N.N.; Parks, J.; Fawley, J.; King, D.R.; Fagenholz, P.J.; Velmahos, G.C. Gastrointestinal complications in critically ill patients with COVID-19. Ann. Surg., 2020, 272(2), e61-e62.
[http://dx.doi.org/10.1097/SLA.0000000000004004] [PMID: 32675498]
[100]
Xiao, F.; Tang, M.; Zheng, X.; Liu, Y.; Li, X.; Shan, H. Evidence for gastrointestinal infection of SARS-CoV-2. Gastroenterology, 2020, 158(6), 1831-1833.e3.
[http://dx.doi.org/10.1053/j.gastro.2020.02.055] [PMID: 32142773]
[101]
Ignat, M.; Philouze, G.; Aussenac-Belle, L.; Faucher, V.; Collange, O.; Mutter, D.; Pessaux, P. Small bowel ischemia and SARS-CoV-2 infection: An underdiagnosed distinct clinical entity. Surgery (United States), 2020, 168(1), 14-16.
[http://dx.doi.org/10.1016/j.surg.2020.04.035] [PMID: 32473831]
[102]
Gartland, R.M.; Velmahos, G.C. Bowel necrosis in the setting of COVID-19. J. Gastrointest. Surg., 2020, 24(12), 2888-2889.
[http://dx.doi.org/10.1007/s11605-020-04632-4] [PMID: 32363540]
[103]
Bhayana, R.; Som, A.; Li, M.D.; Carey, D.E.; Anderson, M.A.; Blake, M.A.; Catalano, O.; Gee, M.S.; Hahn, P.F.; Harisinghani, M.; Kilcoyne, A.; Lee, S.I.; Mojtahed, A.; Pandharipande, P.V.; Pierce, T.T.; Rosman, D.A.; Saini, S.; Samir, A.E.; Simeone, J.F.; Gervais, D.A.; Velmahos, G.; Misdraji, J.; Kambadakone, A. Abdominal imaging findings in COVID-19: Preliminary observations. Radiology, 2020, 297(1), E207-E215.
[http://dx.doi.org/10.1148/radiol.2020201908] [PMID: 32391742]
[104]
Page, V.; McKenzie, C. Sedation in the intensive care unit. Curr. Anesthesiol. Rep., 2021, 11(2), 92-100.
[http://dx.doi.org/10.1007/s40140-021-00446-5] [PMID: 33935593]
[105]
Najjar, S.; Najjar, A.; Chong, D.J.; Pramanik, B.K.; Kirsch, C.; Kuzniecky, R.I.; Pacia, S.V.; Azhar, S. Central nervous system complications associated with SARS-CoV-2 infection: Integrative concepts of pathophysiology and case reports. J. Neuroinflammation, 2020, 17(1), 231.
[http://dx.doi.org/10.1186/s12974-020-01896-0] [PMID: 32758257]
[106]
Spence, J.D.; de Freitas, G.R.; Pettigrew, L.C. Mechanisms of stroke in COVID-19. Cerebrovasc. Dis., 2020, 49(4), 451-458.
[107]
Gupta, A.; Madhavan, M.V.; Sehgal, K.; Nair, N.; Mahajan, S.; Sehrawat, T.S.; Bikdeli, B.; Ahluwalia, N.; Ausiello, J.C.; Wan, E.Y.; Freedberg, D.E.; Kirtane, A.J.; Parikh, S.A.; Maurer, M.S.; Nordvig, A.S.; Accili, D.; Bathon, J.M.; Mohan, S.; Bauer, K.A.; Leon, M.B.; Krumholz, H.M.; Uriel, N.; Mehra, M.R.; Elkind, M.S.V.; Stone, G.W.; Schwartz, A.; Ho, D.D.; Bilezikian, J.P.; Landry, D.W. Extrapulmonary manifestations of COVID-19. Nat. Med., 2020, 26(7), 1017-1032.
[http://dx.doi.org/10.1038/s41591-020-0968-3] [PMID: 32651579]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy