Neurological Complications of COVID-19: Unraveling the Pathophysiological Underpinnings and Therapeutic Implications
Ashutosh Vashisht, Vishakha Vashisht, Harmanpreet Singh, Pankaj Ahluwalia, Ashis K Mondal, Colin Williams, Jaspreet Farmaha, Jana Woodall, Ravindra Kolhe
Viruses, doi:10.3390/v16081183
Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the causative agent of coronavirus disease (COVID-19), induced a global pandemic with a diverse array of clinical manifestations. While the acute phase of the pandemic may be waning, the intricacies of COVID-19 s impact on neurological health remain a crucial area of investigation. Early recognition of the spectrum of COVID-19 symptoms, ranging from mild fever and cough to life-threatening respiratory distress and multi-organ failure, underscored the significance of neurological complications, including anosmia, seizures, stroke, disorientation, encephalopathy, and paralysis. Notably, patients requiring intensive care unit (ICU) admission due to neurological challenges or due to them exhibiting neurological abnormalities in the ICU have shown increased mortality rates. COVID-19 can lead to a range of neurological complications such as anosmia, stroke, paralysis, cranial nerve deficits, encephalopathy, delirium, meningitis, seizures, etc., in affected patients. This review elucidates the burgeoning landscape of neurological sequelae associated with SARS-CoV-2 infection and explores the underlying neurobiological mechanisms driving these diverse manifestations. A meticulous examination of potential neuroinvasion routes by SARS-CoV-2 underscores the intricate interplay between the virus and the nervous system. Moreover, we dissect the diverse neurological manifestations emphasizing the necessity of a multifaceted approach to understanding the disease's neurological footprint. In addition to elucidating the pathophysiological underpinnings, this review surveys current therapeutic modalities and delineates prospective avenues for neuro-COVID research. By integrating epidemiological, clinical, and diagnostic parameters, we endeavor to foster a comprehensive analysis of the nexus between COVID-19 and neurological health, thereby laying the groundwork for targeted therapeutic interventions and long-term management strategies.
Author Contributions: Conceptualization, A.V. and R.K.; Formal analysis, A.V., V.V., H.S. and P.A.; Writing-original draft preparation, A.V., V.V., H.S. and P.A.; Writing-review and editing, A.K.M., C.W., J.F. and J.W.; Supervision, R.K. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding.
Conflicts of Interest: The authors declare no conflicts of interest. Viruses 2024, 16, 1183
References
Aggarwal, Garcia-Telles, Aggarwal, Lavie, Lippi et al., Clinical features, laboratory characteristics, and outcomes of patients hospitalized with coronavirus disease 2019 (COVID-19): Early report from the United States, Diagnosis,
doi:10.1515/dx-2020-0046Aladawi, Elfil, Abu-Esheh, Jazar, Armouti et al., Guillain Barre syndrome as a complication of COVID-19: A systematic review, Can. J. Neurol. Sci,
doi:10.1017/cjn.2021.102Aleem, Akbar Samad, Vaqar, Emerging Variants of SARS-CoV-2 and Novel Therapeutics against Coronavirus (COVID-19)
Barros-Aragão, Pinto, Carregari, Rezende, Pinheiro et al., Changes in neuroinflammatory biomarkers correlate with disease severity and neuroimaging alterations in patients with COVID-19 neurological complications, Brain Behav. Immun. Health,
doi:10.1016/j.bbih.2024.100805Beacon, Su, Lakowski, Delcuve, Davie, SARS-CoV-2 multifaceted interaction with the human host. Part II: Innate immunity response, immunopathology, and epigenetics, IUBMB Life,
doi:10.1002/iub.2379Beltrán-Corbellini, Chico-García, Martínez-Poles, Rodríguez-Jorge, Natera-Villalba et al., Acute-onset smell and taste disorders in the context of COVID-19: A pilot multicentre polymerase chain reaction based case-control study, Eur. J. Neurol,
doi:10.1111/ene.14273Beretta, Cristillo, Camera, Morotti Colleoni, Pellitteri et al., Incidence and long-term functional outcome of neurologic disorders in hospitalized patients with COVID-19 infected with pre-omicron variants, Neurology,
doi:10.1212/WNL.0000000000207534Bergmann, Lane, Stohlman, Coronavirus infection of the central nervous system: Host-virus stand-off, Nat. Rev. Microbiol,
doi:10.1038/nrmicro1343Biswas, Das Sarma, Effect of microtubule disruption on neuronal spread and replication of demyelinating and nondemyelinating strains of mouse hepatitis virus in vitro, J. Virol,
doi:10.1128/JVI.02545-13Bost, Giladi, Liu, Bendjelal, Xu et al., Host-viral infection maps reveal signatures of severe COVID-19 patients, Cell,
doi:10.1016/j.cell.2020.05.006Boucher, Desforges, Duquette, Talbot, Long-term human coronavirus-myelin cross-reactive T-cell clones derived from multiple sclerosis patients, Clin. Immunol,
doi:10.1016/j.clim.2007.02.002Bryce, Grimes, Pujadas, Ahuja, Beasley et al., Pathophysiology of SARS-CoV-2: Targeting of endothelial cells renders a complex disease with thrombotic microangiopathy and aberrant immune response. The Mount Sinai COVID-19 autopsy experience, medRxiv,
doi:10.1101/2020.05.18.20099960Cabirac, Soike, Butunoi, Hoel, Johnson et al., Coronavirus JHM OMP1 pathogenesis in owl monkey CNS and coronavirus infection of owl monkey CNS via peripheral routes
Cantuti-Castelvetri, Ojha, Pedro, Djannatian, Franz et al., Neuropilin-1 facilitates SARS-CoV-2 cell entry and provides a possible pathway into the central nervous system, bioRxiv,
doi:10.1101/2020.06.07.137802Chakraborty, Bhattacharya, Sharma, Present variants of concern and variants of interest of severe acute respiratory syndrome coronavirus 2: Their significant mutations in S-glycoprotein, infectivity, re-infectivity, immune escape and vaccines activity, Rev. Med. Virol,
doi:10.1002/rmv.2270Chen, Wang, Yu, Howard, French et al., The spatial and cell-type distribution of SARS-CoV-2 receptor ACE2 in the human and mouse brains, Front. Neurol,
doi:10.3389/fneur.2020.573095Chen, Wu, Chen, Yan, Yang et al., Clinical characteristics of 113 deceased patients with coronavirus disease 2019: Retrospective study, BMJ,
doi:10.1136/bmj.m1091Cuenca-Zaldivar, Monroy Acevedo, Fernández-Carnero, Sánchez-Romero, Villafañe et al., Effects of a Multicomponent Exercise Program on Improving Frailty in Post-COVID-19 Older Adults after Intensive Care Units: A Single-Group Retrospective Cohort Study, Biology,
doi:10.3390/biology11071084De Melo, Perraud, Alvarez, Vieites-Prado, Kim et al., Neuroinvasion and anosmia are independent phenomena upon infection with SARS-CoV-2 and its variants, Nat. Commun,
doi:10.1038/s41467-023-40228-7Ding, He, Zhang, Huang, Che et al., Organ distribution of severe acute respiratory syndrome (SARS) associated coronavirus (SARS-CoV) in SARS patients: Implications for pathogenesis and virus transmission pathways, J. Pathol. A J. Pathol. Soc. Great Br. Irel,
doi:10.1002/path.1560Engelhardt, Vajkoczy, Weller, The movers and shapers in immune privilege of the CNS, Nat. Immunol,
doi:10.1038/ni.3666Erickson, Banks, Neuroimmune axes of the blood-brain barriers and blood-brain interfaces: Bases for physiological regulation, disease states, and pharmacological interventions, Pharmacol. Rev,
doi:10.1124/pr.117.014647Escalard, Maïer, Redjem, Delvoye, Hébert et al., Treatment of acute ischemic stroke due to large vessel occlusion with COVID-19: Experience from Paris, Stroke,
doi:10.1161/STROKEAHA.120.030574Favas, Dev, Chaurasia, Chakravarty, Mishra et al., Neurological manifestations of COVID-19: A systematic review and meta-analysis of proportions, Neurol. Sci,
doi:10.1007/s10072-020-04801-yFenrich, Mrdenovic, Balog, Tomic, Zjalic et al., SARS-CoV-2 dissemination through peripheral nerves explains multiple organ injury, Front. Cell. Neurosci,
doi:10.3389/fncel.2020.00229Franke, Ferse, Kreye, Reincke, Sanchez-Sendin et al., High frequency of cerebrospinal fluid autoantibodies in COVID-19 patients with neurological symptoms, Brain Behav. Immun,
doi:10.1016/j.bbi.2020.12.022Ganji, Reddy, Impact of COVID-19 on mitochondrial-based immunity in aging and age-related diseases, Front. Aging Neurosci,
doi:10.3389/fnagi.2020.614650Ggarcia, Barreras, Lewis, Pinilla, Sokoll et al., Cerebrospinal fluid in COVID-19 neurological complications: No cytokine storm or neuroinflammation, medRxiv,
doi:10.1101/2021.01.10.20249014Glezer, Rivest, Oncostatin M is a novel glucocorticoid-dependent neuroinflammatory factor that enhances oligodendrocyte precursor cell activity in demyelinated sites, Brain Behav. Immun,
doi:10.1016/j.bbi.2010.01.005Gowrisankar, Clark, Angiotensin II regulation of angiotensin-converting enzymes in spontaneously hypertensive rat primary astrocyte cultures, J. Neurochem,
doi:10.1111/jnc.13641Gu, Gong, Zhang, Zheng, Gao et al., Multiple organ infection and the pathogenesis of SARS, J. Exp. Med,
doi:10.1084/jem.20050828Hamming, Timens, Bulthuis, Lely, Navis et al., Tissue distribution of ACE2 protein, the functional receptor for SARS coronavirus. A first step in understanding SARS pathogenesis, J. Pathol. A J. Pathol. Soc. Great Br. Irel,
doi:10.1002/path.1570He, Mäe, Sun, Muhl, Nahar et al., Pericytespecific vascular expression of SARS-CoV-2 receptor ACE2-implications for microvascular inflammation and hypercoagulopathy in COVID-19 patients, bioRxiv,
doi:10.1101/2020.05.11.088500Helms, Kremer, Merdji, Clere-Jehl, Schenck et al., Neurologic features in severe SARS-CoV-2 infection, N. Engl. J. Med,
doi:10.1056/NEJMc2008597Jacomy, Fragoso, Almazan, Mushynski, Talbot, Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/C mice, Virology,
doi:10.1016/j.virol.2006.01.049Kantonen, Mahzabin, Mäyränpää, Tynninen, Paetau et al., Neuropathologic features of four autopsied COVID-19 patients, Brain Pathol,
doi:10.1111/bpa.12889Kaur, Ling, The circumventricular organs, Histol. Histopathol
Kim, Heo, Kim, Song, Park et al., Neurological complications during treatment of Middle East respiratory syndrome, J. Clin. Neurol,
doi:10.3988/jcn.2017.13.3.227Kim, Kwon, Kam, Panicker, Karuppagounder et al., Transneuronal propagation of pathologic α-synuclein from the gut to the brain models Parkinson's disease, Neuron,
doi:10.1016/j.neuron.2019.05.035Lechien, Chiesa-Estomba, De Siati, Horoi, Le Bon et al., Olfactory and gustatory dysfunctions as a clinical presentation of mild-to-moderate forms of the coronavirus disease (COVID-19): A multicenter European study, Eur. Arch. Oto-Rhino Laryngol,
doi:10.1007/s00405-020-05965-1Li, Bai, Hirano, Hayashida, Taniguchi et al., Neurotropic virus tracing suggests a membranous-coating-mediated mechanism for transsynaptic communication, J. Comp. Neurol,
doi:10.1002/cne.23171Li, Li, Wang, Zhou, Chang et al., Acute cerebrovascular disease following COVID-19: A single center, retrospective, observational study, Stroke Vasc. Neurol,
doi:10.1136/svn-2020-000431Li, Liu, Yang, Han, Mi et al., Neurological manifestations of patients with COVID-19: Potential routes of SARS-CoV-2 neuroinvasion from the periphery to the brain, Front. Med,
doi:10.1007/s11684-020-0786-5Liotta, Batra, Clark, Shlobin, Hoffman et al., Frequent neurologic manifestations and encephalopathy-associated morbidity in COVID-19 patients, Ann. Clin. Transl. Neurol,
doi:10.1002/acn3.51210Liu, Jin, Xiao, Zhong, Li, Inhibition of CD147 improves oligodendrogenesis and promotes white matter integrity and functional recovery in mice after ischemic stroke, Brain Behav. Immun,
doi:10.1016/j.bbi.2019.07.027Mao, Jin, Wang, Hu, Chen et al., Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China, JAMA Neurol,
doi:10.1001/jamaneurol.2020.1127Massion, Howa, Zhu, Kim, Halasa et al., Sex differences in COVID-19 symptom severity and trajectories among ambulatory adults, Influenza Other Respir. Viruses,
doi:10.1111/irv.13235Matsuda, Park, Sunden, Kimura, Ochiai et al., The vagus nerve is one route of transneural invasion for intranasally inoculated influenza a virus in mice, Vet. Pathol,
doi:10.1354/vp.41-2-101Merad, Martin, Pathological inflammation in patients with COVID-19: A key role for monocytes and macrophages, Nat. Rev. Immunol,
doi:10.1038/s41577-020-0331-4Mesci, Macia, Saleh, Martin-Sancho, Yin et al., Sofosbuvir protects human brain organoids against SARS-CoV-2, bioRxiv,
doi:10.1101/2020.05.30.125856Moein, Hashemian, Mansourafshar, Khorram-Tousi, Tabarsi et al., Smell dysfunction: A biomarker for COVID-19, Int. Forum Allergy Rhinol,
doi:10.1002/alr.22587Moriguchi, Harii, Goto, Harada, Sugawara et al., A first case of meningitis/encephalitis associated with SARS-Coronavirus-2, Int. J. Infect. Dis,
doi:10.1016/j.ijid.2020.03.062Nampoothiri, Sauve, Ternier, Fernandois, Coelho et al., The hypothalamus as a hub for putative SARS-CoV-2 brain infection, bioRxiv,
doi:10.1101/2020.06.08.139329Nyberg, Ferguson, Nash, Webster, Flaxman et al., Comparative analysis of the risks of hospitalisation and death associated with SARS-CoV-2 omicron (B. 1.1. 529) and delta (B. 1.617. 2) variants in England: A cohort study, Lancet,
doi:10.1016/S0140-6736(22)00462-7O'brien, Forleo-Neto, Sarkar, Isa, Hou et al., Effect of subcutaneous casirivimab and imdevimab antibody combination vs placebo on development of symptomatic COVID-19 in early asymptomatic SARS-CoV-2 infection: A randomized clinical trial, JAMA,
doi:10.1001/jama.2021.24939Oxley, Mocco, Majidi, Kellner, Shoirah et al., Large-vessel stroke as a presenting feature of COVID-19 in the young, N. Engl. J. Med,
doi:10.1056/NEJMc2009787Paniz-Mondolfi, Bryce, Grimes, Gordon, Reidy et al., Central nervous system involvement by severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), J. Med. Virol,
doi:10.1002/jmv.25915Papatsiros, Stylianaki, Papakonstantinou, Papaioannou, Christodoulopoulos, Case report of transmissible gastroenteritis coronavirus infection associated with small intestine and brain lesions in piglets, Viral Immunol,
doi:10.1089/vim.2018.0095Paterson, Brown, Benjamin, Nortley, Wiethoff et al., The emerging spectrum of COVID-19 neurology: Clinical, radiological and laboratory findings, Brain,
doi:10.1093/brain/awaa240Pei, Wang, Zhang, Luo, Zhou, Association of frailty status with adverse clinical outcomes in patients with COVID-19: Protocol for a systematic review and dose-response meta-analysis, BMJ Open,
doi:10.1136/bmjopen-2020-046980Proust, Queval, Harvey, Adams, Bennett et al., Differential effects of SARS-CoV-2 variants on central nervous system cells and blood-brain barrier functions, J. Neuroinflamm,
doi:10.1186/s12974-023-02861-3Puntambekar, Hinton, Yin, Savarin, Bergmann et al., Interleukin-10 is a critical regulator of white matter lesion containment following viral induced demyelination, Glia,
doi:10.1002/glia.22880Ramani, Müller, Ostermann, Gabriel, Abida-Islam et al., SARS-CoV-2 targets neurons of 3D human brain organoids, EMBO J,
doi:10.15252/embj.2020106230Reichard, Kashani, Boire, Constantopoulos, Guo et al., Neuropathology of COVID-19: A spectrum of vascular and acute disseminated encephalomyelitis (ADEM)-like pathology, Acta Neuropathol,
doi:10.1007/s00401-020-02166-2Rogers, Chesney, Oliver, Pollak, Mcguire et al., Psychiatric and neuropsychiatric presentations associated with severe coronavirus infections: A systematic review and meta-analysis with comparison to the COVID-19 pandemic, Lancet Psychiatry,
doi:10.1016/S2215-0366(20)30203-0Samudyata, Oliveira, Malwade, Rufino De Sousa, Goparaju et al., SARS-CoV-2 promotes microglial synapse elimination in human brain organoids, Mol. Psychiatry,
doi:10.1038/s41380-022-01786-2Sanchis-Gomar, Lavie, Perez-Quilis, Henry, Lippi, Angiotensin-converting enzyme 2 and antihypertensives (angiotensin receptor blockers and angiotensin-converting enzyme inhibitors) in coronavirus disease 2019, Mayo Clin. Proc,
doi:10.1016/j.mayocp.2020.03.026Schaller, Hirschbühl, Burkhardt, Braun, Trepel et al., Postmortem examination of patients with COVID-19, JAMA,
doi:10.1001/jama.2020.8907Scheepers, Everatt, Amoako, Mnguni, Ismail et al., The continuous evolution of SARS-CoV-2 in South Africa: A new lineage with rapid accumulation of mutations of concern and global detection, medRxiv,
doi:10.1101/2021.08.20.21262342Siow, Lee, Zhang, Saffari, Ng, Encephalitis as neurological complication of COVID-19: A systematic review and meta-analysis of incidence, outcomes, and predictors, Eur. J. Neurol,
doi:10.1111/ene.14913Solomon, Normandin, Bhattacharyya, Mukerji, Keller et al., Neuropathological features of COVID-19, N. Engl. J. Med,
doi:10.1056/NEJMc2019373Song, Zhang, Israelow, Lu-Culligan, Sprado et al., Neuroinvasive potential of SARS-CoV-2 revealed in a human brain, J. Exp. Med,
doi:10.1084/jem.20202135Spinato, Fabbris, Polesel, Cazzador, Borsetto et al., Alterations in smell or taste in mildly symptomatic outpatients with SARS-CoV-2 infection, JAMA,
doi:10.1001/jama.2020.6771Srikantha, Mohajeri, The possible role of the microbiota-gut-brain-axis in autism spectrum disorder, Int. J. Mol. Sci,
doi:10.3390/ijms20092115Streinu-Cercel, Săndulescu, Preotescu, Kim, Kim et al., -controlled trial in outpatients with mild-to-moderate coronavirus disease 2019
Sudo, Pinto, Barros-Aragão, Bramati, Marins et al., Cognitive, behavioral, neuroimaging and inflammatory biomarkers after hospitalization for COVID-19 in Brazil, Brain Behav. Immun,
doi:10.1016/j.bbi.2023.10.020Synowiec, Szczepa Ński, Barreto-Duran, Lie, Pyrc, Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2): A systemic infection, Clin. Microbiol. Rev,
doi:10.1128/CMR.00133-20Tang, Kido, Shi, Mccafferty, Ford et al., Blood markers show neural consequences of longCOVID-19, Cells,
doi:10.3390/cells13060478Ttaquet, Sillett, Zhu, Mendel, Camplisson et al., Neurological and psychiatric risk trajectories after SARS-CoV-2 infection: An analysis of 2-year retrospective cohort studies including 1,284,437 patients, Lancet Psychiatry,
doi:10.1016/S2215-0366(22)00260-7Vashisht, Ahluwalia, Mondal, Singh, Sahajpal et al., Immune Factors Drive Expression of SARS-CoV-2 Receptor Genes Amid Sexual Disparity, Viruses,
doi:10.3390/v15030657Wang, Chen, Zhou, Lian, Zhang et al., SARS-CoV-2 invades host cells via a novel route: CD147-spike protein, bioRxiv,
doi:10.1101/2020.03.14.988345Wang, Mandigo, Yim, Meyers, Lavine, Stroke and mechanical thrombectomy in patients with COVID-19: Technical observations and patient characteristics, J. Neurointerventional Surg,
doi:10.1136/neurintsurg-2020-016220Wang, Xu, Musich, Lin, Mitochondrial dysfunction in neurodegenerative diseases and the potential countermeasure, CNS Neurosci. Ther,
doi:10.1111/cns.13116Williams, Martins, Shah, Hill, Coiras et al., Cytokine Deficiencies in Patients with Long-COVID, J. Clin. Cell. Immunol
Yang, Zheng, Gou, Pu, Chen et al., Prevalence of comorbidities and its effects in patients infected with SARS-CoV-2: A systematic review and meta-analysis, Int. J. Infect. Dis,
doi:10.1016/j.ijid.2020.03.017Zheng, Fan, Yu, Feng, Lou et al., Viral load dynamics and disease severity in patients infected with SARS-CoV-2 in Zhejiang province, China, January-March 2020: Retrospective cohort study, BMJ,
doi:10.1136/bmj.m1443Zieli Ńska-Turek, Turek, Lyson, Gajewski, Dorobek, Inflammatory proteins as strong predictors of death in COVID-19 patients with coexisting neurological diseases, medRxiv,
doi:10.1101/2024.02.27.24303438Zuckerkandl, Linus, Evolutionary divergence and convergence in proteins
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'journal-title': 'Clin. Microbiol. Rev.'},
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'article-title': 'Present variants of concern and variants of interest of severe acute '
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'S-glycoprotein, infectivity, re-infectivity, immune escape and vaccines '
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'author': 'Chakraborty',
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'Mahlangu, B., Wibmer, C.K., Wilkinson, E., Tegally, H., and San, J.E. '
'(2021). The continuous evolution of SARS-CoV-2 in South Africa: A new '
'lineage with rapid accumulation of mutations of concern and global '
'detection. medRxiv.'},
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'first-page': '683',
'DOI': '10.1001/jamaneurol.2020.1127',
'article-title': 'Neurologic manifestations of hospitalized patients with coronavirus '
'disease 2019 in Wuhan, China',
'volume': '77',
'author': 'Mao',
'year': '2020',
'journal-title': 'JAMA Neurol.'},
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'doi-asserted-by': 'crossref',
'first-page': '1',
'DOI': '10.1007/s11684-020-0786-5',
'article-title': 'Neurological manifestations of patients with COVID-19: Potential routes '
'of SARS-CoV-2 neuroinvasion from the periphery to the brain',
'volume': '14',
'author': 'Li',
'year': '2020',
'journal-title': 'Front. Med.'},
{ 'key': 'ref_6',
'doi-asserted-by': 'crossref',
'first-page': 'm1091',
'DOI': '10.1136/bmj.m1091',
'article-title': 'Clinical characteristics of 113 deceased patients with coronavirus '
'disease 2019: Retrospective study',
'volume': '368',
'author': 'Chen',
'year': '2020',
'journal-title': 'BMJ'},
{ 'key': 'ref_7',
'doi-asserted-by': 'crossref',
'first-page': '811',
'DOI': '10.1001/jamapsychiatry.2022.1616',
'article-title': 'Bridging Knowledge Gaps in the Diagnosis and Management of '
'Neuropsychiatric Sequelae of COVID-19',
'volume': '79',
'author': 'Frontera',
'year': '2022',
'journal-title': 'JAMA Psychiatry'},
{ 'key': 'ref_8',
'doi-asserted-by': 'crossref',
'first-page': '611',
'DOI': '10.1016/S2215-0366(20)30203-0',
'article-title': 'Psychiatric and neuropsychiatric presentations associated with severe '
'coronavirus infections: A systematic review and meta-analysis with '
'comparison to the COVID-19 pandemic',
'volume': '7',
'author': 'Rogers',
'year': '2020',
'journal-title': 'Lancet Psychiatry'},
{ 'key': 'ref_9',
'doi-asserted-by': 'crossref',
'first-page': '378',
'DOI': '10.5603/PJNNS.a2020.0050',
'article-title': 'Neurological manifestations of SARS-CoV-2—A systematic review',
'volume': '54',
'author': 'Domitrz',
'year': '2020',
'journal-title': 'Neurol. I Neurochir. Pol.'},
{ 'key': 'ref_10',
'doi-asserted-by': 'crossref',
'unstructured': 'He, L., Mäe, M.A., Sun, Y., Muhl, L., Nahar, K., Liébanas, E.V., '
'Fagerlund, M.J., Oldner, A., Liu, J., and Genové, G. (2020). '
'Pericyte-specific vascular expression of SARS-CoV-2 receptor '
'ACE2–implications for microvascular inflammation and hypercoagulopathy '
'in COVID-19 patients. bioRxiv.',
'DOI': '10.1101/2020.05.11.088500'},
{ 'key': 'ref_11',
'doi-asserted-by': 'crossref',
'unstructured': 'Chen, R., Wang, K., Yu, J., Howard, D., French, L., Chen, Z., Wen, C., '
'and Xu, Z. (2021). The spatial and cell-type distribution of SARS-CoV-2 '
'receptor ACE2 in the human and mouse brains. Front. Neurol., 11.',
'DOI': '10.3389/fneur.2020.573095'},
{ 'key': 'ref_12',
'doi-asserted-by': 'crossref',
'unstructured': 'Wang, K., Chen, W., Zhou, Y.S., Lian, J.Q., Zhang, Z., Du, P., Gong, L., '
'Zhang, Y., Cui, H.Y., and Geng, J.J. (2020). SARS-CoV-2 invades host '
'cells via a novel route: CD147-spike protein. bioRxiv.',
'DOI': '10.1101/2020.03.14.988345'},
{ 'key': 'ref_13',
'doi-asserted-by': 'crossref',
'unstructured': 'Cantuti-Castelvetri, L., Ojha, R., Pedro, L.D., Djannatian, M., Franz, '
'J., Kuivanen, S., Kallio, K., Kaya, T., Anastasina, M., and Smura, T. '
'(2020). Neuropilin-1 facilitates SARS-CoV-2 cell entry and provides a '
'possible pathway into the central nervous system. bioRxiv.',
'DOI': '10.1101/2020.06.07.137802'},
{ 'key': 'ref_14',
'doi-asserted-by': 'crossref',
'first-page': '699',
'DOI': '10.1002/jmv.25915',
'article-title': 'Central nervous system involvement by severe acute respiratory syndrome '
'coronavirus-2 (SARS-CoV-2)',
'volume': '92',
'author': 'Bryce',
'year': '2020',
'journal-title': 'J. Med. Virol.'},
{ 'key': 'ref_15',
'first-page': '622',
'article-title': 'Organ distribution of severe acute respiratory syndrome (SARS) '
'associated coronavirus (SARS-CoV) in SARS patients: Implications for '
'pathogenesis and virus transmission pathways',
'volume': '203',
'author': 'Ding',
'year': '2004',
'journal-title': 'J. Pathol. A J. Pathol. Soc. Great Br. Irel.'},
{ 'key': 'ref_16',
'doi-asserted-by': 'crossref',
'first-page': '415',
'DOI': '10.1084/jem.20050828',
'article-title': 'Multiple organ infection and the pathogenesis of SARS',
'volume': '202',
'author': 'Gu',
'year': '2005',
'journal-title': 'J. Exp. Med.'},
{ 'key': 'ref_17',
'doi-asserted-by': 'crossref',
'first-page': '74',
'DOI': '10.1111/jnc.13641',
'article-title': 'Angiotensin II regulation of angiotensin-converting enzymes in '
'spontaneously hypertensive rat primary astrocyte cultures',
'volume': '138',
'author': 'Gowrisankar',
'year': '2016',
'journal-title': 'J. Neurochem.'},
{ 'key': 'ref_18',
'first-page': '631',
'article-title': 'Tissue distribution of ACE2 protein, the functional receptor for SARS '
'coronavirus. A first step in understanding SARS pathogenesis',
'volume': '203',
'author': 'Hamming',
'year': '2004',
'journal-title': 'J. Pathol. A J. Pathol. Soc. Great Br. Irel.'},
{ 'key': 'ref_19',
'doi-asserted-by': 'crossref',
'unstructured': 'Mesci, P., Macia, A., Saleh, A., Martin-Sancho, L., Yin, X., Snethlage, '
'C., Avansini, S., Chanda, S.K., and Muotri, A. (2020). Sofosbuvir '
'protects human brain organoids against SARS-CoV-2. bioRxiv.',
'DOI': '10.1101/2020.05.30.125856'},
{ 'key': 'ref_20',
'doi-asserted-by': 'crossref',
'first-page': 'e106230',
'DOI': '10.15252/embj.2020106230',
'article-title': 'SARS-CoV-2 targets neurons of 3D human brain organoids',
'volume': '39',
'author': 'Ramani',
'year': '2020',
'journal-title': 'EMBO J.'},
{ 'key': 'ref_21',
'doi-asserted-by': 'crossref',
'first-page': 'e20202135',
'DOI': '10.1084/jem.20202135',
'article-title': 'Neuroinvasive potential of SARS-CoV-2 revealed in a human brain',
'volume': '218',
'author': 'Song',
'year': '2021',
'journal-title': 'J. Exp. Med.'},
{ 'key': 'ref_22',
'doi-asserted-by': 'crossref',
'first-page': '55',
'DOI': '10.1016/j.ijid.2020.03.062',
'article-title': 'A first case of meningitis/encephalitis associated with '
'SARS-Coronavirus-2',
'volume': '94',
'author': 'Moriguchi',
'year': '2020',
'journal-title': 'Int. J. Infect. Dis.'},
{ 'key': 'ref_23',
'doi-asserted-by': 'crossref',
'first-page': '2518',
'DOI': '10.1001/jama.2020.8907',
'article-title': 'Postmortem examination of patients with COVID-19',
'volume': '323',
'author': 'Schaller',
'year': '2020',
'journal-title': 'JAMA'},
{ 'key': 'ref_24',
'doi-asserted-by': 'crossref',
'unstructured': 'Cabirac, G.F., Soike, K.F., Butunoi, C., Hoel, K., Johnson, S., Cai, '
'G.Y., and Murray, R.S. (1994). Coronavirus JHM OMP1 pathogenesis in owl '
'monkey CNS and coronavirus infection of owl monkey CNS via peripheral '
'routes. Coronaviruses, Springer.',
'DOI': '10.1007/978-1-4615-2996-5_53'},
{ 'key': 'ref_25',
'first-page': '1843',
'article-title': 'Detection of SARS-CoV-2 in different types of clinical specimens',
'volume': '323',
'author': 'Wang',
'year': '2020',
'journal-title': 'JAMA'},
{ 'key': 'ref_26',
'doi-asserted-by': 'crossref',
'first-page': 'm1443',
'DOI': '10.1136/bmj.m1443',
'article-title': 'Viral load dynamics and disease severity in patients infected with '
'SARS-CoV-2 in Zhejiang province, China, January-March 2020: '
'Retrospective cohort study',
'volume': '369',
'author': 'Zheng',
'year': '2020',
'journal-title': 'BMJ'},
{ 'key': 'ref_27',
'unstructured': 'Bryce, C., Grimes, Z., Pujadas, E., Ahuja, S., Beasley, M.B., Albrecht, '
'R., Hernandez, T., Stock, A., Zhao, Z., and Rasheed, M.A. (2020). '
'Pathophysiology of SARS-CoV-2: Targeting of endothelial cells renders a '
'complex disease with thrombotic microangiopathy and aberrant immune '
'response. The Mount Sinai COVID-19 autopsy experience. medRxiv.'},
{ 'key': 'ref_28',
'doi-asserted-by': 'crossref',
'first-page': '278',
'DOI': '10.1124/pr.117.014647',
'article-title': 'Neuroimmune axes of the blood–brain barriers and blood–brain '
'interfaces: Bases for physiological regulation, disease states, and '
'pharmacological interventions',
'volume': '70',
'author': 'Erickson',
'year': '2018',
'journal-title': 'Pharmacol. Rev.'},
{ 'key': 'ref_29',
'doi-asserted-by': 'crossref',
'first-page': '389',
'DOI': '10.1038/s41577-020-0343-0',
'article-title': 'COVID-19: The vasculature unleashed',
'volume': '20',
'author': 'Teuwen',
'year': '2020',
'journal-title': 'Nat. Rev. Immunol.'},
{ 'key': 'ref_30',
'doi-asserted-by': 'crossref',
'first-page': '1012',
'DOI': '10.1111/bpa.12889',
'article-title': 'Neuropathologic features of four autopsied COVID-19 patients',
'volume': '30',
'author': 'Kantonen',
'year': '2020',
'journal-title': 'Brain Pathol.'},
{ 'key': 'ref_31',
'doi-asserted-by': 'crossref',
'first-page': '1',
'DOI': '10.1007/s00401-020-02166-2',
'article-title': 'Neuropathology of COVID-19: A spectrum of vascular and acute '
'disseminated encephalomyelitis (ADEM)-like pathology',
'volume': '140',
'author': 'Reichard',
'year': '2020',
'journal-title': 'Acta Neuropathol.'},
{ 'key': 'ref_32',
'doi-asserted-by': 'crossref',
'first-page': '989',
'DOI': '10.1056/NEJMc2019373',
'article-title': 'Neuropathological features of COVID-19',
'volume': '383',
'author': 'Solomon',
'year': '2020',
'journal-title': 'N. Engl. J. Med.'},
{ 'key': 'ref_33',
'first-page': '879',
'article-title': 'The circumventricular organs',
'volume': '32',
'author': 'Kaur',
'year': '2017',
'journal-title': 'Histol. Histopathol.'},
{ 'key': 'ref_34',
'doi-asserted-by': 'crossref',
'unstructured': 'Nampoothiri, S., Sauve, F., Ternier, G., Fernandois, D., Coelho, C., '
'Imbernon, M., Deligia, E., Perbet, R., Florent, V., and Baroncini, M. '
'(2020). The hypothalamus as a hub for putative SARS-CoV-2 brain '
'infection. bioRxiv.',
'DOI': '10.1101/2020.06.08.139329'},
{ 'key': 'ref_35',
'doi-asserted-by': 'crossref',
'first-page': '121',
'DOI': '10.1038/nrmicro1343',
'article-title': 'Coronavirus infection of the central nervous system: Host–virus '
'stand-off',
'volume': '4',
'author': 'Bergmann',
'year': '2006',
'journal-title': 'Nat. Rev. Microbiol.'},
{ 'key': 'ref_36',
'doi-asserted-by': 'crossref',
'first-page': '123',
'DOI': '10.1038/ni.3666',
'article-title': 'The movers and shapers in immune privilege of the CNS',
'volume': '18',
'author': 'Engelhardt',
'year': '2017',
'journal-title': 'Nat. Immunol.'},
{ 'key': 'ref_37',
'doi-asserted-by': 'crossref',
'first-page': '355',
'DOI': '10.1038/s41577-020-0331-4',
'article-title': 'Pathological inflammation in patients with COVID-19: A key role for '
'monocytes and macrophages',
'volume': '20',
'author': 'Merad',
'year': '2020',
'journal-title': 'Nat. Rev. Immunol.'},
{ 'key': 'ref_38',
'doi-asserted-by': 'crossref',
'unstructured': 'Feng, Z., Diao, B., Wang, R., Wang, G., Wang, C., Tan, Y., Liu, L., '
'Wang, C., Liu, Y., and Liu, Y. (2020). The novel severe acute '
'respiratory syndrome coronavirus 2 (SARS-CoV-2) directly decimates human '
'spleens and lymph nodes. medRxiv.',
'DOI': '10.1101/2020.03.27.20045427'},
{ 'key': 'ref_39',
'doi-asserted-by': 'crossref',
'first-page': '1475',
'DOI': '10.1016/j.cell.2020.05.006',
'article-title': 'Host-viral infection maps reveal signatures of severe COVID-19 patients',
'volume': '181',
'author': 'Bost',
'year': '2020',
'journal-title': 'Cell'},
{ 'key': 'ref_40',
'doi-asserted-by': 'crossref',
'first-page': '203',
'DOI': '10.1002/cne.23171',
'article-title': 'Neurotropic virus tracing suggests a membranous-coating-mediated '
'mechanism for transsynaptic communication',
'volume': '521',
'author': 'Li',
'year': '2013',
'journal-title': 'J. Comp. Neurol.'},
{ 'key': 'ref_41',
'doi-asserted-by': 'crossref',
'first-page': '3043',
'DOI': '10.1128/JVI.02545-13',
'article-title': 'Effect of microtubule disruption on neuronal spread and replication of '
'demyelinating and nondemyelinating strains of mouse hepatitis virus in '
'vitro',
'volume': '88',
'author': 'Biswas',
'year': '2014',
'journal-title': 'J. Virol.'},
{ 'key': 'ref_42',
'doi-asserted-by': 'crossref',
'first-page': '101',
'DOI': '10.1354/vp.41-2-101',
'article-title': 'The vagus nerve is one route of transneural invasion for intranasally '
'inoculated influenza a virus in mice',
'volume': '41',
'author': 'Matsuda',
'year': '2004',
'journal-title': 'Vet. Pathol.'},
{ 'key': 'ref_43',
'doi-asserted-by': 'crossref',
'unstructured': 'Fenrich, M., Mrdenovic, S., Balog, M., Tomic, S., Zjalic, M., Roncevic, '
'A., Mandic, D., Debeljak, Z., and Heffer, M. (2020). SARS-CoV-2 '
'dissemination through peripheral nerves explains multiple organ injury. '
'Front. Cell. Neurosci., 14.',
'DOI': '10.3389/fncel.2020.00229'},
{ 'key': 'ref_44',
'doi-asserted-by': 'crossref',
'first-page': '63',
'DOI': '10.1089/vim.2018.0095',
'article-title': 'Case report of transmissible gastroenteritis coronavirus infection '
'associated with small intestine and brain lesions in piglets',
'volume': '32',
'author': 'Papatsiros',
'year': '2019',
'journal-title': 'Viral Immunol.'},
{ 'key': 'ref_45',
'doi-asserted-by': 'crossref',
'first-page': '1222',
'DOI': '10.1016/j.mayocp.2020.03.026',
'article-title': 'Angiotensin-converting enzyme 2 and antihypertensives (angiotensin '
'receptor blockers and angiotensin-converting enzyme inhibitors) in '
'coronavirus disease 2019',
'volume': '95',
'author': 'Lavie',
'year': '2020',
'journal-title': 'Mayo Clin. Proc.'},
{ 'key': 'ref_46',
'doi-asserted-by': 'crossref',
'unstructured': 'Zuckerkandl, E., and Linus, P. (1965). Evolutionary divergence and '
'convergence in proteins. Evolving Genes and Proteins, Academic Press.',
'DOI': '10.1016/B978-1-4832-2734-4.50017-6'},
{ 'key': 'ref_47',
'doi-asserted-by': 'crossref',
'first-page': '2331',
'DOI': '10.1002/iub.2379',
'article-title': 'SARS-CoV-2 multifaceted interaction with the human host. Part II: '
'Innate immunity response, immunopathology, and epigenetics',
'volume': '72',
'author': 'Beacon',
'year': '2020',
'journal-title': 'IUBMB Life'},
{ 'key': 'ref_48',
'doi-asserted-by': 'crossref',
'first-page': '807',
'DOI': '10.4103/aian.AIAN_1296_20',
'article-title': 'Acute ataxia and myoclonus in COVID-19: A case series',
'volume': '24',
'author': 'Sundar',
'year': '2021',
'journal-title': 'Ann. Indian Acad. Neurol.'},
{ 'key': 'ref_49',
'doi-asserted-by': 'crossref',
'first-page': '2268',
'DOI': '10.1056/NEJMc2008597',
'article-title': 'Neurologic features in severe SARS-CoV-2 infection',
'volume': '382',
'author': 'Helms',
'year': '2020',
'journal-title': 'N. Engl. J. Med.'},
{ 'key': 'ref_50',
'doi-asserted-by': 'crossref',
'first-page': '2221',
'DOI': '10.1002/acn3.51210',
'article-title': 'Frequent neurologic manifestations and encephalopathy-associated '
'morbidity in COVID-19 patients',
'volume': '7',
'author': 'Liotta',
'year': '2020',
'journal-title': 'Ann. Clin. Transl. Neurol.'},
{ 'key': 'ref_51',
'doi-asserted-by': 'crossref',
'first-page': '434',
'DOI': '10.1016/S2468-1253(20)30083-2',
'article-title': 'Prolonged presence of SARS-CoV-2 viral RNA in fecal samples',
'volume': '5',
'author': 'Wu',
'year': '2020',
'journal-title': 'Lancet Gastroenterol. Hepatol.'},
{ 'key': 'ref_52',
'unstructured': 'Aleem, A., Akbar Samad, A.B., and Vaqar, S. (2023). Emerging Variants of '
'SARS-CoV-2 and Novel Therapeutics against Coronavirus (COVID-19). '
'StatPearls, StatPearls Publishing.'},
{ 'key': 'ref_53',
'doi-asserted-by': 'crossref',
'first-page': 'e892',
'DOI': '10.1212/WNL.0000000000207534',
'article-title': 'Incidence and long-term functional outcome of neurologic disorders in '
'hospitalized patients with COVID-19 infected with pre-omicron variants',
'volume': '101',
'author': 'Beretta',
'year': '2023',
'journal-title': 'Neurology'},
{ 'key': 'ref_54',
'doi-asserted-by': 'crossref',
'first-page': '4485',
'DOI': '10.1038/s41467-023-40228-7',
'article-title': 'Neuroinvasion and anosmia are independent phenomena upon infection with '
'SARS-CoV-2 and its variants',
'volume': '14',
'author': 'Perraud',
'year': '2023',
'journal-title': 'Nat. Commun.'},
{ 'key': 'ref_55',
'doi-asserted-by': 'crossref',
'first-page': '815',
'DOI': '10.1016/S2215-0366(22)00260-7',
'article-title': 'Neurological and psychiatric risk trajectories after SARS-CoV-2 '
'infection: An analysis of 2-year retrospective cohort studies including '
'1,284,437 patients',
'volume': '9',
'author': 'TTaquet',
'year': '2022',
'journal-title': 'Lancet Psychiatry'},
{ 'key': 'ref_56',
'doi-asserted-by': 'crossref',
'first-page': '184',
'DOI': '10.1186/s12974-023-02861-3',
'article-title': 'Differential effects of SARS-CoV-2 variants on central nervous system '
'cells and blood–brain barrier functions',
'volume': '20',
'author': 'Proust',
'year': '2023',
'journal-title': 'J. Neuroinflamm.'},
{ 'key': 'ref_57',
'doi-asserted-by': 'crossref',
'first-page': '1303',
'DOI': '10.1016/S0140-6736(22)00462-7',
'article-title': 'Comparative analysis of the risks of hospitalisation and death '
'associated with SARS-CoV-2 omicron (B. 1.1. 529) and delta (B. 1.617. '
'2) variants in England: A cohort study',
'volume': '399',
'author': 'Nyberg',
'year': '2022',
'journal-title': 'Lancet'},
{ 'key': 'ref_58',
'doi-asserted-by': 'crossref',
'first-page': '3104',
'DOI': '10.1093/brain/awaa240',
'article-title': 'The emerging spectrum of COVID-19 neurology: Clinical, radiological and '
'laboratory findings',
'volume': '143',
'author': 'Paterson',
'year': '2020',
'journal-title': 'Brain'},
{ 'key': 'ref_59',
'doi-asserted-by': 'crossref',
'first-page': '2251',
'DOI': '10.1007/s00405-020-05965-1',
'article-title': 'Olfactory and gustatory dysfunctions as a clinical presentation of '
'mild-to-moderate forms of the coronavirus disease (COVID-19): A '
'multicenter European study',
'volume': '277',
'author': 'Lechien',
'year': '2020',
'journal-title': 'Eur. Arch. Oto-Rhino Laryngol.'},
{ 'key': 'ref_60',
'doi-asserted-by': 'crossref',
'first-page': '91',
'DOI': '10.1515/dx-2020-0046',
'article-title': 'Clinical features, laboratory characteristics, and outcomes of patients '
'hospitalized with coronavirus disease 2019 (COVID-19): Early report '
'from the United States',
'volume': '7',
'author': 'Aggarwal',
'year': '2020',
'journal-title': 'Diagnosis'},
{ 'key': 'ref_61',
'doi-asserted-by': 'crossref',
'first-page': 'e13235',
'DOI': '10.1111/irv.13235',
'article-title': 'Sex differences in COVID-19 symptom severity and trajectories among '
'ambulatory adults',
'volume': '17',
'author': 'Massion',
'year': '2023',
'journal-title': 'Influenza Other Respir. Viruses'},
{ 'key': 'ref_62',
'doi-asserted-by': 'crossref',
'unstructured': 'Vashisht, A., Ahluwalia, P., Mondal, A.K., Singh, H., Sahajpal, N.S., '
'Fulzele, S., Kota, V., Gahlay, G.K., and Kolhe, R. (2023). Immune '
'Factors Drive Expression of SARS-CoV-2 Receptor Genes Amid Sexual '
'Disparity. Viruses, 15.',
'DOI': '10.3390/v15030657'},
{ 'key': 'ref_63',
'doi-asserted-by': 'crossref',
'first-page': '2089',
'DOI': '10.1001/jama.2020.6771',
'article-title': 'Alterations in smell or taste in mildly symptomatic outpatients with '
'SARS-CoV-2 infection',
'volume': '323',
'author': 'Spinato',
'year': '2020',
'journal-title': 'JAMA'},
{ 'key': 'ref_64',
'doi-asserted-by': 'crossref',
'first-page': '1738',
'DOI': '10.1111/ene.14273',
'article-title': 'Acute-onset smell and taste disorders in the context of COVID-19: A '
'pilot multicentre polymerase chain reaction based case–control study',
'volume': '27',
'author': 'Monreal',
'year': '2020',
'journal-title': 'Eur. J. Neurol.'},
{ 'key': 'ref_65',
'doi-asserted-by': 'crossref',
'first-page': '944',
'DOI': '10.1002/alr.22587',
'article-title': 'Smell dysfunction: A biomarker for COVID-19',
'volume': '10',
'author': 'Moein',
'year': '2020',
'journal-title': 'Int. Forum Allergy Rhinol.'},
{ 'key': 'ref_66',
'doi-asserted-by': 'crossref',
'first-page': 'e60',
'DOI': '10.1056/NEJMc2009787',
'article-title': 'Large-vessel stroke as a presenting feature of COVID-19 in the young',
'volume': '382',
'author': 'Oxley',
'year': '2020',
'journal-title': 'N. Engl. J. Med.'},
{ 'key': 'ref_67',
'doi-asserted-by': 'crossref',
'first-page': '401',
'DOI': '10.4103/ijmr.IJMR_957_20',
'article-title': 'Clinical management of COVID-19',
'volume': '151',
'author': 'Varghese',
'year': '2020',
'journal-title': 'Indian J. Med. Res.'},
{ 'key': 'ref_68',
'doi-asserted-by': 'crossref',
'first-page': '3437',
'DOI': '10.1007/s10072-020-04801-y',
'article-title': 'Neurological manifestations of COVID-19: A systematic review and '
'meta-analysis of proportions',
'volume': '41',
'author': 'Favas',
'year': '2020',
'journal-title': 'Neurol. Sci.'},
{ 'key': 'ref_69',
'doi-asserted-by': 'crossref',
'first-page': '279',
'DOI': '10.1136/svn-2020-000431',
'article-title': 'Acute cerebrovascular disease following COVID-19: A single center, '
'retrospective, observational study',
'volume': '5',
'author': 'Li',
'year': '2020',
'journal-title': 'Stroke Vasc. Neurol.'},
{ 'key': 'ref_70',
'doi-asserted-by': 'crossref',
'first-page': '639',
'DOI': '10.1038/s41586-021-03207-w',
'article-title': 'Evolution of antibody immunity to SARS-CoV-2',
'volume': '591',
'author': 'Gaebler',
'year': '2021',
'journal-title': 'Nature'},
{ 'key': 'ref_71',
'doi-asserted-by': 'crossref',
'first-page': '227',
'DOI': '10.3988/jcn.2017.13.3.227',
'article-title': 'Neurological complications during treatment of Middle East respiratory '
'syndrome',
'volume': '13',
'author': 'Kim',
'year': '2017',
'journal-title': 'J. Clin. Neurol.'},
{ 'key': 'ref_72',
'doi-asserted-by': 'crossref',
'first-page': '1669',
'DOI': '10.1001/archneur.61.11.1669',
'article-title': 'Neuromuscular disorders in severe acute respiratory syndrome',
'volume': '61',
'author': 'Tsai',
'year': '2004',
'journal-title': 'Arch. Neurol.'},
{ 'key': 'ref_73',
'doi-asserted-by': 'crossref',
'first-page': '335',
'DOI': '10.1016/j.virol.2006.01.049',
'article-title': 'Human coronavirus OC43 infection induces chronic encephalitis leading '
'to disabilities in BALB/C mice',
'volume': '349',
'author': 'Jacomy',
'year': '2006',
'journal-title': 'Virology'},
{ 'key': 'ref_74',
'doi-asserted-by': 'crossref',
'first-page': '1',
'DOI': '10.1186/s12985-017-0719-3',
'article-title': 'Multiple sclerosis: An example of pathogenic viral interaction?',
'volume': '14',
'author': 'Fierz',
'year': '2017',
'journal-title': 'Virol. J.'},
{ 'key': 'ref_75',
'doi-asserted-by': 'crossref',
'first-page': '369',
'DOI': '10.1146/annurev-pathol-020117-043952',
'article-title': 'Type I interferons in autoimmune disease',
'volume': '14',
'author': 'Crow',
'year': '2019',
'journal-title': 'Annu. Rev. Pathol. Mech. Dis.'},
{ 'key': 'ref_76',
'doi-asserted-by': 'crossref',
'first-page': '8913',
'DOI': '10.1128/JVI.74.19.8913-8921.2000',
'article-title': 'Neuroinvasion by human respiratory coronaviruses',
'volume': '74',
'author': 'Arbour',
'year': '2000',
'journal-title': 'J. Virol.'},
{ 'key': 'ref_77',
'doi-asserted-by': 'crossref',
'first-page': '258',
'DOI': '10.1016/j.clim.2007.02.002',
'article-title': 'Long-term human coronavirus-myelin cross-reactive T-cell clones derived '
'from multiple sclerosis patients',
'volume': '123',
'author': 'Boucher',
'year': '2007',
'journal-title': 'Clin. Immunol.'},
{ 'key': 'ref_78',
'doi-asserted-by': 'crossref',
'first-page': '627',
'DOI': '10.1016/j.neuron.2019.05.035',
'article-title': 'Transneuronal propagation of pathologic α-synuclein from the gut to the '
'brain models Parkinson’s disease',
'volume': '103',
'author': 'Kim',
'year': '2019',
'journal-title': 'Neuron'},
{ 'key': 'ref_79',
'doi-asserted-by': 'crossref',
'unstructured': 'Srikantha, P., and Mohajeri, M.H. (2019). The possible role of the '
'microbiota-gut-brain-axis in autism spectrum disorder. Int. J. Mol. '
'Sci., 20.',
'DOI': '10.3390/ijms20092115'},
{ 'key': 'ref_80',
'doi-asserted-by': 'crossref',
'first-page': '1130',
'DOI': '10.1038/s43587-022-00321-w',
'article-title': 'Severe COVID-19 induces molecular signatures of aging in the human '
'brain',
'volume': '2',
'author': 'Mavrikaki',
'year': '2022',
'journal-title': 'Nat. Aging'},
{ 'key': 'ref_81',
'doi-asserted-by': 'crossref',
'first-page': '3939',
'DOI': '10.1038/s41380-022-01786-2',
'article-title': 'SARS-CoV-2 promotes microglial synapse elimination in human brain '
'organoids',
'volume': '27',
'author': 'Samudyata',
'year': '2022',
'journal-title': 'Mol. Psychiatry'},
{ 'key': 'ref_82',
'doi-asserted-by': 'crossref',
'first-page': '816',
'DOI': '10.1111/cns.13116',
'article-title': 'Mitochondrial dysfunction in neurodegenerative diseases and the '
'potential countermeasure',
'volume': '25',
'author': 'Wang',
'year': '2019',
'journal-title': 'CNS Neurosci. Ther.'},
{ 'key': 'ref_83',
'doi-asserted-by': 'crossref',
'unstructured': 'Ganji, R., and Reddy, P.H. (2021). Impact of COVID-19 on '
'mitochondrial-based immunity in aging and age-related diseases. Front. '
'Aging Neurosci., 12.',
'DOI': '10.3389/fnagi.2020.614650'},
{ 'key': 'ref_84',
'doi-asserted-by': 'crossref',
'first-page': '91',
'DOI': '10.1016/j.ijid.2020.03.017',
'article-title': 'Prevalence of comorbidities and its effects in patients infected with '
'SARS-CoV-2: A systematic review and meta-analysis',
'volume': '94',
'author': 'Yang',
'year': '2020',
'journal-title': 'Int. J. Infect. Dis.'},
{ 'key': 'ref_85',
'doi-asserted-by': 'crossref',
'first-page': 'e046980',
'DOI': '10.1136/bmjopen-2020-046980',
'article-title': 'Association of frailty status with adverse clinical outcomes in '
'patients with COVID-19: Protocol for a systematic review and '
'dose–response meta-analysis',
'volume': '11',
'author': 'Pei',
'year': '2021',
'journal-title': 'BMJ Open'},
{ 'key': 'ref_86',
'first-page': '672',
'article-title': 'Cytokine Deficiencies in Patients with Long-COVID',
'volume': '13',
'author': 'Williams',
'year': '2022',
'journal-title': 'J. Clin. Cell. Immunol.'},
{ 'key': 'ref_87',
'doi-asserted-by': 'crossref',
'first-page': '415',
'DOI': '10.1016/j.bbi.2020.12.022',
'article-title': 'High frequency of cerebrospinal fluid autoantibodies in COVID-19 '
'patients with neurological symptoms',
'volume': '93',
'author': 'Franke',
'year': '2021',
'journal-title': 'Brain Behav. Immun.'},
{ 'key': 'ref_88',
'doi-asserted-by': 'crossref',
'unstructured': 'GGarcia, M.A., Barreras, P.V., Lewis, A., Pinilla, G., Sokoll, L.J., '
'Kickler, T., Mostafa, H., Caturegli, M., Moghekar, A., and Fitzgerald, '
'K.C. (2021). Cerebrospinal fluid in COVID-19 neurological complications: '
'No cytokine storm or neuroinflammation. medRxiv.',
'DOI': '10.1101/2021.01.10.20249014'},
{ 'key': 'ref_89',
'doi-asserted-by': 'crossref',
'first-page': '100805',
'DOI': '10.1016/j.bbih.2024.100805',
'article-title': 'Changes in neuroinflammatory biomarkers correlate with disease severity '
'and neuroimaging alterations in patients with COVID-19 neurological '
'complications',
'volume': '39',
'author': 'Pinto',
'year': '2024',
'journal-title': 'Brain Behav. Immun. Health'},
{ 'key': 'ref_90',
'doi-asserted-by': 'crossref',
'first-page': 'e219',
'DOI': '10.1161/STROKEAHA.120.030995',
'article-title': 'Acute cerebrovascular events in hospitalized COVID-19 patients',
'volume': '51',
'author': 'Rothstein',
'year': '2020',
'journal-title': 'Stroke'},
{ 'key': 'ref_91',
'doi-asserted-by': 'crossref',
'unstructured': 'Tang, N., Kido, T., Shi, J., McCafferty, E., Ford, J.M., Dal Bon, K., '
'and Pulliam, L. (2024). Blood markers show neural consequences of '
'longCOVID-19. Cells, 13.',
'DOI': '10.20944/preprints202402.0892.v1'},
{ 'key': 'ref_92',
'doi-asserted-by': 'crossref',
'unstructured': 'Zielińska-Turek, J., Turek, G., Lyson, T., Gajewski, J., Ząbek, M., and '
'Dorobek, M. (2024). Inflammatory proteins as strong predictors of death '
'in COVID-19 patients with coexisting neurological diseases. medRxiv.',
'DOI': '10.1101/2024.02.27.24303438'},
{ 'key': 'ref_93',
'doi-asserted-by': 'crossref',
'first-page': '434',
'DOI': '10.1016/j.bbi.2023.10.020',
'article-title': 'Cognitive, behavioral, neuroimaging and inflammatory biomarkers after '
'hospitalization for COVID-19 in Brazil',
'volume': '115',
'author': 'Sudo',
'year': '2024',
'journal-title': 'Brain Behav. Immun.'},
{ 'key': 'ref_94',
'doi-asserted-by': 'crossref',
'first-page': '648',
'DOI': '10.1136/neurintsurg-2020-016220',
'article-title': 'Stroke and mechanical thrombectomy in patients with COVID-19: Technical '
'observations and patient characteristics',
'volume': '12',
'author': 'Wang',
'year': '2020',
'journal-title': 'J. Neurointerventional Surg.'},
{ 'key': 'ref_95',
'doi-asserted-by': 'crossref',
'first-page': '2540',
'DOI': '10.1161/STROKEAHA.120.030574',
'article-title': 'Treatment of acute ischemic stroke due to large vessel occlusion with '
'COVID-19: Experience from Paris',
'volume': '51',
'author': 'Escalard',
'year': '2020',
'journal-title': 'Stroke'},
{ 'key': 'ref_96',
'doi-asserted-by': 'crossref',
'first-page': '3491',
'DOI': '10.1111/ene.14913',
'article-title': 'Encephalitis as neurological complication of COVID-19: A systematic '
'review and meta-analysis of incidence, outcomes, and predictors',
'volume': '28',
'author': 'Siow',
'year': '2021',
'journal-title': 'Eur. J. Neurol.'},
{ 'key': 'ref_97',
'doi-asserted-by': 'crossref',
'first-page': '38',
'DOI': '10.1017/cjn.2021.102',
'article-title': 'Guillain Barre syndrome as a complication of COVID-19: A systematic '
'review',
'volume': '49',
'author': 'Aladawi',
'year': '2022',
'journal-title': 'Can. J. Neurol. Sci.'},
{ 'key': 'ref_98',
'doi-asserted-by': 'crossref',
'first-page': '2106',
'DOI': '10.1002/glia.22880',
'article-title': 'Interleukin-10 is a critical regulator of white matter lesion '
'containment following viral induced demyelination',
'volume': '63',
'author': 'Puntambekar',
'year': '2015',
'journal-title': 'Glia'},
{ 'key': 'ref_99',
'doi-asserted-by': 'crossref',
'first-page': '695',
'DOI': '10.1016/j.bbi.2010.01.005',
'article-title': 'Oncostatin M is a novel glucocorticoid-dependent neuroinflammatory '
'factor that enhances oligodendrocyte precursor cell activity in '
'demyelinated sites',
'volume': '24',
'author': 'Glezer',
'year': '2010',
'journal-title': 'Brain Behav. Immun.'},
{ 'key': 'ref_100',
'doi-asserted-by': 'crossref',
'first-page': '13',
'DOI': '10.1016/j.bbi.2019.07.027',
'article-title': 'Inhibition of CD147 improves oligodendrogenesis and promotes white '
'matter integrity and functional recovery in mice after ischemic stroke',
'volume': '82',
'author': 'Liu',
'year': '2019',
'journal-title': 'Brain Behav. Immun.'},
{ 'key': 'ref_101',
'doi-asserted-by': 'crossref',
'first-page': '309',
'DOI': '10.2165/00002018-200932040-00005',
'article-title': 'Vaccines and guillain-barre syndrome',
'volume': '32',
'author': 'Haber',
'year': '2009',
'journal-title': 'Drug Saf.'},
{ 'key': 'ref_102',
'doi-asserted-by': 'crossref',
'first-page': '432',
'DOI': '10.1001/jama.2021.24939',
'article-title': 'Effect of subcutaneous casirivimab and imdevimab antibody combination '
'vs placebo on development of symptomatic COVID-19 in early asymptomatic '
'SARS-CoV-2 infection: A randomized clinical trial',
'volume': '327',
'author': 'Sarkar',
'year': '2022',
'journal-title': 'JAMA'},
{ 'key': 'ref_103',
'doi-asserted-by': 'crossref',
'first-page': 'ofac053',
'DOI': '10.1093/ofid/ofac053',
'article-title': 'Efficacy and safety of regdanvimab (CT-P59): A phase 2/3 randomized, '
'double-blind, placebo-controlled trial in outpatients with '
'mild-to-moderate coronavirus disease 2019',
'volume': 'Volume 9',
'author': 'Preotescu',
'year': '2022',
'journal-title': 'Open Forum Infectious Diseases'},
{ 'key': 'ref_104',
'doi-asserted-by': 'crossref',
'unstructured': 'Cuenca-Zaldivar, J.N., Monroy Acevedo, Á., Fernández-Carnero, J., '
'Sánchez-Romero, E.A., Villafañe, J.H., and Barragán Carballar, C. '
'(2022). Effects of a Multicomponent Exercise Program on Improving '
'Frailty in Post-COVID-19 Older Adults after Intensive Care Units: A '
'Single-Group Retrospective Cohort Study. Biology, 11.',
'DOI': '10.3390/biology11071084'}],
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