Neuroinvasion, neurotropic, and neuroinflammatory events of SARS-CoV-2: understanding the neurological manifestations in COVID-19 patients

Yassine Yachou, Abdeslem El Idrissi, Vladimir Belapasov, Said Ait Benali, Yassine Yachou, Abdeslem El Idrissi, Vladimir Belapasov, Said Ait Benali

Abstract

Respiratory viruses are opportunistic pathogens that infect the upper respiratory tract in humans and cause severe illnesses, especially in vulnerable populations. Some viruses have neuroinvasive properties and activate the immune response in the brain. These immune events may be neuroprotective or they may cause long-term damage similar to what is seen in some neurodegenerative diseases. The new "Severe Acute Respiratory Syndrome Coronavirus 2" (SARS-CoV-2) is one of the Respiratory viruses causing highly acute lethal pneumonia coronavirus disease 2019 (COVID-19) with clinical similarities to those reported in "Severe Acute Respiratory Syndrome Coronavirus"(SARS-CoV) and the "Middle East Respiratory Syndrome Coronavirus"(MERS-CoV) including neurological manifestation. To examine the possible neurological damage induced by SARS-CoV-2, it is necessary to understand the immune reactions to viral infection in the brain, and their short- and long-term consequences. Considering the similarities between SARS-CoV and SARS-CoV-2, which will be discussed, cooperative homological and phylogenetical studies lead us to question if SARS-CoV-2 can have similar neuroinvasive capacities and neuroinflammatiory events that may lead to the same short- and long-term neuropathologies that SARS-CoV had shown in human and animal models. To explain the neurological manifestation caused by SARS-CoV-2, we will present a literature review of 765 COVID-19 patients, in which 18% had neurological symptoms and complications, including encephalopathy, encephalitis and cerebrovascular pathologies, acute myelitis, and Guillain-Barré syndrome. Clinical studies describe anosmia or partial loss of the sense of smell as the most frequent symptom in COVID19 patients, suggesting that olfactory dysfunction and the initial ultrarapid immune responses could be a prognostic factor.

Keywords: Acute and chronic neurological diseases; CNS infection; COVID-19; Encephalitis; Encephalopathy; Human coronavirus; Human respiratory virus; Neuroinvasion; Respiratory viral infection.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Immune control of viral infections
Fig. 2
Fig. 2
Several viruses spread to the CNS by infecting the neuron receptor in the nasal olfactory epithelium to reach the brain by axonal transport along the olfactory nerve
Fig. 3
Fig. 3
Some respiratory viruses spread from the lungs to the CNS through the vagus nerve
Fig. 4
Fig. 4
a Several viruses spread to the CNS by infecting the neuron receptor in the nasal olfactory epithelium to reach the brain by axonal transport along the olfactory nerve. b Some respiratory viruses spread from the lungs to the CNS through the vagus nerve

References

    1. Koyuncu OO, Hogue IB, Enquist LW. Virus infections in the nervous system. Cell Host Microbe. 2013;13:379–393. doi: 10.1016/j.chom.2013.03.010.
    1. Englund J, Feuchtinger T, Ljungman P. Viral infections in immunocompromised patients. Biol Blood Marrow Transplant. 2011;17:S2–S5. doi: 10.1016/j.bbmt.2010.11.008.
    1. Talbot HK, Falsey AR. The diagnosis of viral respiratory disease in older adults. Clin Infect Dis. 2010;50:747–751. doi: 10.1086/650486.
    1. Tregoning JS, Schwarze J. Respiratory viral infections in infants: causes, clinical symptoms, virology, and immunology. Clin Microbiol Rev. 2010;23:74–98. doi: 10.1128/cmr.00032-09.
    1. Saitgareeva AR, Bulygin KV, Gareev IF, Beylerli OA, Akhmadeeva LR (2020) The role of microglia in the development of neurodegeneration. Neurol Sci. 10.1007/s10072-020-04468-5
    1. Streit WJ. Microglial senescence: does the brain’s immune system have an expiration date? Trends Neurosci. 2006;29:506–510.
    1. Streit WJ, Mrak RE, Griffin WS. Microglia and neuroinflammation: a pathological perspective. J Neuroinflammation. 2004;1:14.
    1. von Bernhardi R. Glial cell dysregulation: a new perspective on Alzheimer Disease. Neurotox Res. 2007;12:215–232.
    1. Nakajima K, Tohyama Y, Kohsaka S, Kurihara T. Ability of rat microglia to uptake extracellular glutamate. Neurosci Lett. 2001;307:171–174.
    1. van den Pol AN. Viral infections in the developing and mature brain. Trends Neurosci. 2006;29:398–406.
    1. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med. 2004;10:1366–1373.
    1. Boulanger LM. Immune proteins in brain development and synaptic plasticity. Neuron. 2009;64:93–109.
    1. Deleidi M, Hallett PJ, Koprich JB, Chung CY, Isacson O. The Toll-like receptor-3 agonist polyinosinic:polycytidylic acid triggers nigrostriatal dopaminergic degeneration. J Neurosci. 2010;30:16091–16101.
    1. Chung CY, Koprich JB, Siddiqi H, Isacson O. Dynamic changes in presynaptic and axonal transport proteins combined with striatal neuroinflammation precede dopaminergic neuronal loss in a rat model of AAV alpha-synucleinopathy. J Neurosci. 2009;29:3365–3373.
    1. Centonze D, Muzio L, Rossi S, Cavasinni F, De Chiara V, Bergami A, Musella A, D’Amelio M, Cavallucci V, Martorana A, Bergamaschi A, Cencioni MT, Diamantini A, Butti E, Comi G, Bernardi G, Cecconi F, Battistini L, Furlan R, Martino G. Inflammation triggers synaptic alteration and degeneration in experimental autoimmune encephalomyelitis. J Neurosci. 2009;29:3442–3452.
    1. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R. Physical basis of cognitive alterations in Alzheimer’s disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol. 1991;30:572–580.
    1. Arkwright PD, Abinun M. Recently identified factors predisposing children to infectious diseases. Curr Opin Infect Dis. 2008;21:217–222.
    1. Bohmwald K, Espinoza JA, Gonzalez PA, Bueno SM, Riedel CA, Kalergis AM. Central nervous system alterations caused by infection with the human respiratory syncytial virus. Rev Med Virol. 2014;24:407–419.
    1. Halfhide CP, Flanagan BF, Brearey SP, Hunt JA, Fonceca AM, McNamara PS, Howarth D, Edwards S, Smyth RL. Respiratory syncytial virus binds and undergoes transcription in neutrophils from the blood and airways of infants with severe bronchiolitis. J Infect Dis. 2011;204:451–458.
    1. Mathieu C, Pohl C, Szecsi J, Trajkovic-Bodennec S, Devergnas S, Raoul H, Cosset FL, Gerlier D, Wild TF, Horvat B (2011) Nipah virus usesleukocytes for efficient dissemination within a host. J Virol 85:7863–7871
    1. Escaffre O, Borisevich V, Carmical JR, Prusak D, Prescott J, Feldmann H, Rockx B. Henipavirus pathogenesis in human respiratory epithelial cells. J Virol. 2013;87:3284–3294.
    1. Tse H, To KK, Wen X, Chen H, Chan KH, Tsoi HW, Li IW, Yuen KY. Clinical and virological factors associated with viremia in pandemic influenza A/H1N1/2009 virus infection. PLoS One. 2011;6:e22534.
    1. Imamura T, Suzuki A, Lupisan S, Kamigaki T, Okamoto M, Roy CN, Olveda R, Oshitani H. Detection of enterovirus 68 in serum from pediatric patients with pneumonia and their clinical outcomes. Influenza Other Respir Viruses. 2014;8:21–24.
    1. Berth SH, Leopold PL, Morfini GN. Virus-induced neuronal dysfunction and degeneration. Front Biosci. 2009;14:5239–5259.
    1. Mori I. Transolfactory neuroinvasion by viruses threatens the human brain. Acta Virol. 2015;59:338–349.
    1. Lochhead JJ, Thorne RG. Intranasal delivery of biologics to the central nervous system. Adv Drug Deliv Rev. 2012;64:614–628.
    1. Lochhead JJ, Kellohen KL, Ronaldson PT, Davis TP. Distribution of insulin in trigeminal nerve and brain after intranasal administration. Sci Rep. 2019;9:2621.
    1. Driessen AK, Farrell MJ, Mazzone SB, McGovern AE. Multiple neural circuits mediating airway sensations: recent advances in the neurobiology of the urge-to-cough. Respir Physiol Neurobiol. 2016;226:115–120.
    1. Goenka A, Michael BD, Ledger E, Hart IJ, Absoud M, Chow G, Lilleker J, Lunn M, McKee D, Peake D, Pysden K, Roberts M, Carrol ED, Lim M, Avula S, Solomon T, Kneen R. Neurological manifestations of influenza infection in children and adults: results of a national british surveillance study. Clin Infect Dis. 2014;58:775–784. doi: 10.1093/cid/cit922.
    1. Paksu MS, Aslan K, Kendirli T, Akyildiz BN, Yener N, Yildizdas RD, Davutoglu M, Yaman A, Isikay S, Sensoy G, Tasdemir HA. Neuroinfluenza: evaluation of seasonal influenza associated severe neurological complications in children (a multicenter study) Childs Nerv Syst. 2018;34:335–347. doi: 10.1007/s00381-017-3554-3.
    1. Popescu CP, Florescu SA, Lupulescu E, Zaharia M, Tardei G, Lazar M, Ceausu E, Ruta SM. Neurologic complications of influenza B virus infection in adults, Romania. Emerg Infect Dis. 2017;23:574–581. doi: 10.3201/eid2304.161317.
    1. Newland JG, Romero JR, Varman M, Drake C, Holst A, Safranek T, Subbarao K. Encephalitis associated with influenza B virus infection in 2 children and a review of the literature. Clin Infect Dis. 2003;36:e87–e95. doi: 10.1086/368184.
    1. Ottaviani D, Boso F, Tranquillini E, Gapeni I, Pedrotti G, Cozzio S, Guarrera GM, Giometto B. Early Guillain-Barré syndrome in coronavirus disease 2019 (COVID-19): a case report from an Italian COVID-hospital. Neurol Sci. 2020;41:1351–1354. doi: 10.1007/s10072-020-04449-8.
    1. Sivadon-Tardy V, Orlikowski D, Porcher R, Sharshar T, Durand MC, Enouf V, Rozenberg F, Caudie C, Annane D, van der Werf S, Lebon P, Raphaël JC, Gaillard JL, Gault E. Guillain-Barré syndrome and influenza virus infection. Clin Infect Dis. 2009;48(1):48–56. doi: 10.1086/594124.
    1. Chiu SS, Tse CYC, Lau YL, Peiris M. Influenza a infection is an important cause of febrile seizures. Pediatrics. 2001;108:E63. doi: 10.1542/peds.108.4.e63.
    1. Zeng H, Quinet S, Huang W, Gan Y, Han C, He Y, Wang Y. Clinical and MRI features of neurological complications after influenza A (H1N1) infection in critically ill children. Pediatr Radiol. 2013;43:1182–1189.
    1. Beraki S, Aronsson F, Karlsson H, Ogren SO, Kristensson K. Influenza a virus infection causes alterations in expression of synaptic regulatory genes combined with changes in cognitive and emotional behaviors in mice. Mol Psychiatry. 2005;10:299–308.
    1. Hosseini S, Wilk E, Michaelsen-Preusse K, Gerhauser I, Baumgartner W, Geffers R, Schughart K, Korte M. Long-term neuroinflammation induced by influenza a virus infection and the impact on hippocampal neuron morphology and function. J Neurosci. 2018;38:3060–3080.
    1. Matsuda K, Park CH, Sunden Y, Kimura T, Ochiai K, Kida H, Umemura T. The vagus nerve is one route of transneural invasion for intranasally inoculated influenza a virus in mice. Vet Pathol. 2004;41:101–107.
    1. Shinya K, Makino A, Hatta M, Watanabe S, Kim JH, Hatta Y, Gao P, Ozawa M, Le QM, Kawaoka Y. Subclinical brain injury caused by H5N1 influenza virus infection. J Virol. 2011;85:5202–5207.
    1. Jang H, Boltz D, Sturm-Ramirez K, Shepherd KR, Jiao Y, Webster R, Smeyne RJ. Highly pathogenic H5N1 influenza virus can enter the central nervous system and induce neuroinflammation and neurodegeneration. Proc Natl Acad Sci U S A. 2009;106:14063–14068.
    1. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (Eds) (2012) Classification and nomenclature of viruses. In: Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier: San Diego, 1326–1327
    1. Ksiazek TG, Erdman D, Goldsmith CS, Zaki SR, Peret T, Emery S, Tong S, Urbani C, Comer JA, Lim W, Rollin PE, Dowell SF, Ling AE, Humphrey CD, Shieh WJ, Guarner J, Paddock CD, Rota P, Fields B, DeRisi J, Yang JY, Cox N, Hughes JM, LeDuc J, Bellini WJ, Anderson LJ, SARS Working Group A novel coronavirus associated with severe acute respiratory syndrome. N Engl J Med. 2003;348:1953–1966.
    1. Sheahan TP, Sims AC, Leist SR, Schäfer A, Won J, Brown AJ, Montgomery SA, Hogg A, Babusis D, Clarke MO, Spahn JE, Bauer L, Sellers S, Porter D, Feng JY, Cihlar T, Jordan R, Denison MR, Baric RS. Comparative therapeutic efficacy of remdesivir and combination lopinavir, ritonavir, and interferon beta against MERS-CoV. Nat Commun. 2020;11:222.
    1. de Groot RJ, Baker SC, Baric RS, et al. Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group. J Virol. 2013;87:7790–7792.
    1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus ADME, Fouchier RAM. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814–1820.
    1. WHO novel coronavirus – China. Date: Jan 12, 2020 Date accessed: January 19, 2020
    1. Gerna G, Passarani N, Battaglia M, Rondanelli EG. Human enteric coronaviruses: antigenic relatedness to human coronavirus OC43 and possible etiologic role in viral gastroenteritis. J Infect Dis. 1985;151:796–803.
    1. Jevsnik M, Steyer A, Pokorn M, Mrvic T, Grosek S, Strle F, Lusa L, Petrovec M. The role of human coronaviruses in children hospitalized for acute bronchiolitis, acute gastroenteritis, and febrile seizures: a 2-year prospective study. PLoS One. 2016;11:e0155555.
    1. Raj VS, Osterhaus AD, Fouchier RA, Haagmans BL. MERS: emergence of a novel human coronavirus. Curr Opin Virol. 2014;5:58–62.
    1. Resta S, Luby JP, Rosenfeld CR, Siegel JD. Isolation and propagation of a human enteric coronavirus. Science. 1985;229:978–981.
    1. Riski H, Hovi T. Coronavirus infections of man associated with diseases other than the common cold. J Med Virol. 1980;6:259–265.
    1. Jiang G, Gong E, Zhang B, Zheng J, Gao Z, Zhong Y, Zou W, Zhan J, Wang S, Xie Z, Zhuang H, Wu B, Zhong H, Shao H, Fang W, Gao D, Pei F, Li X, He Z, Xu D, Shi X, Anderson VM, Leong AS-Y (2005) Multiple organ infection and the pathogenesis of SARS. J Exp Med 202(3):415–424
    1. Lau KK, Yu WC, Chu CM, Lau ST, Sheng B, Yuen KY. Possible central nervous system infection by SARS coronavirus. Emerg Infect Dis. 2004;10(2):342–344. doi: 10.3201/eid1002.030638.
    1. Yeh EA, Collins A, Cohen ME, Duffner PK, Faden H. Detection of coronavirus in the central nervous system of a child with acute disseminated encephalomyelitis. Pediatrics. 2004;113:e73–e76. doi: 10.1542/peds.113.1.e73.
    1. Zlateva KT, Van Ranst M. Detection of subgroup B respiratory syncytial virus in the cerebrospinal fluid of a patient with respiratory syncytial virus pneumonia. Pediatr Infect Dis J. 2004;23:1065–1066. doi: 10.1097/01.inf.0000143654.12493.c9.
    1. Arbour N, Day R, Newcombe J, Talbot PJ. Neuroinvasion by human respiratory coronaviruses. J Virol. 2000;74:8913–8921. doi: 10.1128/jvi.74.19.8913-8921.2000.
    1. Desforges M, Le Coupanec A, Brison É, Meessen-Pinard M, Talbot PJ. Neuroinvasive and neurotropic human respiratory coronaviruses: potential neurovirulent agents in humans. In: Adhikari R, Thapa S, editors. Infectious Diseases and Nanomedicine I. India: Springer; 2014. pp. 75–96.
    1. Burks JS, DeVald BL, Jankovsky LD, Gerdes JC. Two coronaviruses isolated from central nervous system tissue of two multiple sclerosis patients. Science. 1980;209:933–934. doi: 10.1126/science.7403860.
    1. Hung ECW, Chim SSC, Chan PKS, Tong YK, Ng EKO, Chiu RWK, Leung CB, Sung JJY, Tam JS, Lo YMD. Detection of SARS coronavirus RNA in the cerebrospinal fluid of a patient with severe acute respiratory syndrome. Clin Chem. 2003;49:2108–2109. doi: 10.1373/clinchem.2003.025437.
    1. Ding YQ, He L, Zhang QL, Huang ZX, Che XY, Hou JL, 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. 2004;203:622–630. doi: 10.1002/path.1560.
    1. Li Z, He W, Lan Y, Zhao K, Lv X, Lu H, Ding N, Zhang J, Shi J, Shan C, Gao F. The evidence of porcine hemagglutinating encephalomyelitis virus induced nonsuppurative encephalitis as the cause of death in piglets. Peer J. 2016;4:e2443.
    1. Chen C, Zhang XR, Ju ZY, He WF. Advances in the research of cytokine storm mechanism induced by Corona Virus Disease 2019 and the corresponding immunotherapies. Zhonghua Shao Shang Za Zhi. 2020;36:E005.
    1. Mengeling WL, Boothe AD, Ritchie AE (1972) Characteristics of a coronavirus (strain 67N) of pigs. Am J Vet Res 33(2):297–308
    1. Andries K, Pensaert MB (1980) Virus isolated and immunofluorescence in different organs of pigs infected with hemagglutinating encephalomyelitis virus. Am J Vet Res 41:215–218
    1. Gialluisi A, de Gaetano G, Iacoviello L. New challenges from Covid-19 pandemic: an unexpected opportunity to enlighten the link between viral infections and brain disorders? Neurol Sci. 2020;41:1349–1350. doi: 10.1007/s10072-020-04444-z.
    1. Niazkar HR, Zibaee B, Nasimi A, Bahri N (2020) The neurological manifestations of COVID-19: a review article. Neurol Sci. 10.1007/s10072-020-04486-3
    1. Lu R, Zhao X, Li J, Niu P, Yang B, Wu H, Wang W, Song H, Huang B, Zhu N, Bi Y, Ma X, Zhan F, Wang L, Hu T, Zhou H, Hu Z, Zhou W, Zhao L, Chen J, Meng Y, Wang J, Lin Y, Yuan J, Xie Z, Ma J, Liu WJ, Wang D, Xu W, Holmes EC, Gao GF, Wu G, Chen W, Shi W, Tan W. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 2020;395(10224):565–574. doi: 10.1016/S0140-6736(20)30251-8.
    1. Tsai LK, Hsieh ST, Chang YC. Neurological manifestations in severe acute respiratory syndrome. Acta Neurol Taiwanica. 2005;14(3):113–119.
    1. Xu J, Zhong S, Liu J, Li L, Li Y, Wu X, Li Z, Deng P, Zhang J, Zhong N, Ding Y, Jiang Y. Detection of severe acute respiratory syndrome coronavirus in the brain: potential role of the chemokine mig in pathogenesis. Clin Infect Dis. 2005;41(8):1089–1096. doi: 10.1086/444461.
    1. McCray PB, Jr, Pewe L, Wohlford-Lenane C, Hickey M, Manzel L, Shi L, Netland J, Jia HP, Halabi C, Sigmund CD, Meyerholz DK, Kirby P, Look DC, Perlman S. Lethal infection of K18-hACE2 mice infected with severe acute respiratory syndrome coronavirus. J Virol. 2007;81(2):813–821. doi: 10.1128/JVI.02012-06.
    1. Wu A, Peng Y, Huang B, Ding X, Wang X, Niu P, Meng J, Zhu Z, Zhang Z, Wang J, Sheng J, Quan L, Xia Z, Tan W, Cheng G, Jiang T. Genome composition and divergence of the novel coronavirus (2019-nCoV) originating in China. Cell Host Microbe. 2020;27(3):325–328.
    1. Xu J, Zhao S, Teng T, et al. Systematic comparison of two animal-to-human transmitted human coronaviruses: SARS-CoV-2 and SARS-CoV. Viruses. 2020;12(2):244. doi: 10.3390/v12020244.
    1. Gralinski LE, Menachery VD. Return of the coronavirus: 2019-nCoV. Viruses. 2020;12:135. doi: 10.3390/v12020135.
    1. Mao L, Jin H, Wang M, et al (2020) Neurologic manifestations of hospitalized patients with coronavirus disease 2019 in Wuhan, China. JAMA Neurol. 77(6):683–690. 10.1001/jamaneurol.2020.1127
    1. Wang W, Xu Y, Gao R, Lu R, Han K, Wu G, Tan W. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 2020;323(18):1843–1844. doi: 10.1001/jama.2020.3786.
    1. Yang J. Prevalence of comorbidities in the novel Wuhan coronavirus (COVID-19) infection: a systematic review and meta-analysis. Int J Infect Dis. 2020;94:91–95.
    1. Xiang P, Xu XM, Gao LL, Wang HZ, Xiong HF, Li RH et al. First case of 2019 novel coronavirus disease with encephalitis ChinaXiv, T202003 (2020), p. 00015
    1. Altwairqi RG, Aljuaid SM, Alqahtani AS. Effect of tonsillectomy on humeral and cellular immunity: a systematic review of published studies from 2009 to 2019. Eur Arch Otorhinolaryngol. 2020;277(1):1–7. doi: 10.1007/s00405-019-05672-6.
    1. Olender T, Keydar I, Pinto JM, Tatarskyy P, Alkelai A, Chien M-S, Fishilevich S, Restrepo D, Matsunami H, Gilad Y, Lancet D. The human olfactory transcriptome. BMC Genomics. 2016;17:619.
    1. Kangeswaran N, Demond M, Nagel M. Deep sequencing of the murine olfactory receptor transcriptome. PLoS One. 2015;10(1):e0113170.
    1. Saraiva LR, Ibarra-Soria X, Khan M, Omura M, Scialdone A, Mombaerts P, Marioni JC, Logan DW. Hierarchical deconstruction of mouse olfactory sensory neurons: from whole mucosa to single-cell RNA-seq. Sci Rep. 2015;5:18178.
    1. Sepahi A, Kraus A, Casadei E, Johnston CA, Galindo-Villegas J, Kelly C, Garcia-Moreno D, Munoz P, Mulero V, Huertas M, Salinas I. Olfactory sensory neurons mediate ultrarapid antiviral immune responses in a TrkA-dependent manner. Proc Natl Acad Sci U S A. 2019;116(25):12428–12436.
    1. Baker E, Lui F (2020) Neuroanatomy, vagal nerve nuclei (Nucleus Vagus). In: StatPearls. StatPearls Publishing, Treasure Island (FL)
    1. Ikeda K, Kawakami K, Onimaru H, Okada Y, Yokota S, Koshiya N, Oku Y, Iizuka M, Koizumi H. The respiratory control mechanisms in the brainstem and spinal cord: integrative views of the neuroanatomy and neurophysiology. J Physiol Sci. 2017;67(1):45–62. doi: 10.1007/s12576-016-0475-y.
    1. Arbour N, Cote G, Lachance C, Tardieu M, Cashman NR, Talbot PJ. Acute and persistent infection of human neural cell lines by human coronavirus OC43. J Virol. 1999;73:3338–3350.
    1. Jacomy H, Fragoso G, Almazan G, Mushynski WE, Talbot PJ. Human coronavirus OC43 infection induces chronic encephalitis leading to disabilities in BALB/C mice. Virology. 2006;349:335–346.
    1. Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM. Impaired learning resulting from respiratory syncytial virus infection. Proc Natl Acad Sci U S A. 2013;110:9112–9117.
    1. Espinoza JA, Bohmwald K, Cespedes PF, Gomez RS, Riquelme SA, Cortes CM, Valenzuela JA, Sandoval RA, Pancetti FC, Bueno SM, Riedel CA, Kalergis AM. Impaired learning resulting from respiratory syncytial virusinfection. Proc Natl Acad Sci U S A. 2013;110:9112–9117.
    1. Jurgens HA, Amancherla K, Johnson RW. Influenza infection induces neuroinflammation, alters hippocampal neuron morphology, and impairs cognition in adult mice. J Neurosci. 2012;32:3958–3968.
    1. Vasek MJ, Garber C, Dorsey D, Durrant DM, Bollman B, Soung A, Yu J, Perez-Torres C, Frouin A, Wilton DK, Funk K, DeMasters BK, Jiang X, Bowen JR, Mennerick S, Robinson JK, Garbow JR, Tyler KL, Suthar MS, Schmidt RE, Stevens B, Klein RS. A complement-microglial axis drives synapse loss during virus-induced memory impairment. Nature. 2016;534:538–543.
    1. Poyiadji N, Shahin G, Noujaim D, Stone M, Patel S, Griffith B (2020) COVID-19-associated Acute Hemorrhagic Necrotizing Encephalopathy: CT and MRI Features [published online ahead of print, 2020 Mar 31]. Radiology. 201187. 10.1148/radiol.2020201187
    1. Mizuguchi M, Yamanouchi H, Ichiyama T, Shiomi M. Acute encephalopathy associated with influenza and other viral infections. Acta Neurol Scand Suppl. 2007;186:45–56.
    1. Elkind MS. Why now? Moving from stroke risk factors to stroke triggers. Curr Opin Neurol. 2007;20(1):51–57.
    1. Warren-Gash C, Blackburn R, Whitaker H, McMenamin J, Hayward AC (2018) Laboratory-confirmed respiratory infections as triggers for acute myocardial infarction and stroke: a self-controlled case series analysis of national linked datasets from Scotland. Eur Respir J 51(3):1701794. 10.1183/13993003.01794-2017
    1. Muhammad S, Haasbach E, Kotchourko M, Strigli A, Krenz A, Ridder DA, et al. Influenza virus infection aggravates stroke outcome. Stroke. 2011;42(3):783–791.
    1. Mehta P, McAuley DF, Brown M, Sanchez E, Tattersall RS, Manson JJ. COVID-19: consider cytokine storm syndromes and immunosuppression [published online ahead of print, 2020 Mar 16] Lancet. 2020;S0140-6736(20):30628.
    1. Zhou F. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020;395(10229):1054–1062.
    1. Guo J. Coronavirus disease 2019 (COVID-19) and cardiovascular disease: a viewpoint on the potential influence of angiotensin-converting enzyme inhibitors/angiotensin receptor blockers on onset and severity of severe acute respiratory syndrome coronavirus 2 infection. J Am Heart Assoc. 2020;9(7):e016219.
    1. Padroni M. Guillain-Barre syndrome following COVID-19: new infection, old complication? J Neurol. 2020;267:1877–1879.
    1. El Otmani H, El Moutawakil B, Rafai MA et al (2020) Covid-19 and Guillain-Barré syndrome: More than a coincidence!. Rev Neurol (Paris). 176(6):518–519. 10.1016/j.neurol.2020.04.007
    1. Cusick MF, Libbey JE, Fujinami RS. Multiple sclerosis: autoimmunity and viruses. Curr Opin Rheumatol. 2013;25:496–501.
    1. Gilden DH. Infectious causes of multiple sclerosis. Lancet Neurol. 2005;4:195–202.
    1. Kurtzke JF. Epidemiologic evidence for multiple sclerosis as an infection. Clin Microbiol Rev. 1993;6:382–427.
    1. Saberi A, Akhondzadeh S, Kazemi S. Infectious agents and different course of multiple sclerosis: a systematic review. Acta Neurol Belg. 2018;118:361–377.
    1. Smatti MK, Cyprian FS, Nasrallah GK, Al Thani AA, Almishal RO, Yassine HM. Viruses and autoimmunity: a review on the potential interaction and molecular mechanisms. Viruses. 2019;11:762.
    1. Tanaka R, Iwasaki Y, Koprowski H. Intracisternal virus-like particles in brain of a multiple sclerosis patient. J Neurol Sci. 1976;28(1):121–126.
    1. Salmi A, Ziola B, Hovi T, Reunanen M. Antibodies to coronaviruses OC43 and 229E in multiple sclerosis patients. Neurology. 1982;32:292–295.
    1. Murray RS, Brown B, Brian D, Cabirac GF. Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol. 1992;31:525–533.
    1. Murray RS, Brown B, Brian D, Cabirac GF. Detection of coronavirus RNA and antigen in multiple sclerosis brain. Ann Neurol. 1992;31:525–533.
    1. Sorensen O, Coulter-Mackie MB, Puchalski S, Dales S. In vivo and in vitro models of demyelinating disease. IX. Progression of JHM virus infection in the central nervous system of the rat during overt and asymptomatic phases. Virology. 1984;137:347–357.
    1. Cristallo A, Gambaro F, Biamonti G, Ferrante P, Battaglia M, Cereda PM. Human coronavirus polyadenylated RNA sequences in cerebrospinal fluid from multiple sclerosis patients. Microbiologica. 1997;2:105–114.
    1. Oleszak EL, Chang JR, Friedman H, Katsetos CD, Platsoucas CD. Theiler’s virus infection: a model for multiple sclerosis. Clin Microbiol Rev. 2004;17(1):174–207. doi: 10.1128/cmr.17.1.174-207.2004.
    1. Weber T, Major EO. Progressive multifocal leukoencephalopathy: molecular biology, pathogenesis and clinical impact. Intervirology. 1997;40:98–111.
    1. Sun N, Grzybicki D, Castro F, Murphy S, Perlman S. Activation of astrocytes in the spinal cord of mice chronically infected with a neurotropic coronavirus. Virology. 1995;213:482–493.
    1. Lane TE, Asensio VC, Yu N, Paoletti AD, Campbell IL, Buchmeier MJ. Dynamic regulation of α- and β-chemokine expression in the central nervous system during mouse hepatitis virus-induced demyelinating disease. J Immunol. 1998;160:970–978.
    1. Rima BK, Duprex WP. Molecular mechanisms of measles virus persistence. Virus Res. 2005;111(2):132–147.
    1. Roberts MT. AIDS-associated progressive multifocal leukoencephalopathy: current management strategies. CNS Drugs. 2005;19(8):671–682.
    1. Sweet TM, Del Valle L, Khalili K. Molecular biology and immunoregulation of human neurotropic JC virus in CNS. J Cell Physiol. 2002;191(3):249–256.
    1. Gonzalez-Scarano F, Baltuch G. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci. 1999;22:219–240.
    1. Hovelmeyer N, Hao Z, Kranidioti K, Kassiotis G, Buch T, Frommer F, von Hoch L, Kramer D, Minichiello L, Kollias G, Lassmann H, Waisman A. Apoptosis of oligodendrocytes via Fas and TNF-R1 is a key event in the induction of experimental autoimmune encephalomyelitis. J Immunol. 2005;175(9):5875–5884.
    1. McLarnon JG, Michikawa M, Kim SU. Effects of tumor necrosis factor on inward potassium current and cell morphology in cultured human oligodendrocytes. Glia. 1993;9(2):120–126.
    1. Miller SD, Vanderlugt CL, Begolka WS, Pao W, Neville KL, Yauch RL, Kim BS. Epitope spreading leads to myelin-specific autoimmune responses in SJL mice chronically infected with Theiler’s virus. J Neuro-Oncol. 1997;3(Suppl 1):S62–S65.
    1. Butler N, Pewe L, Trandem K, Perlman S. Murine encephalitis caused by HCoV-OC43, a human coronavirus with broad species specificity, is partly immune-mediated. Virology. 2006;347:410–421.
    1. Moriguchi T. A first case of meningitis/encephalitis associated with SARS-Coronavirus-2. Int J Infect Dis. 2020;94:55–58.
    1. Yu WB, Tang GD, Zhang L, Corlett RT (2020) Decoding the evolution and transmissions of the novel pneumonia coronavirus (SARS-CoV-2) using whole genomic data. ChinaXiv. 10.12074/202002.00033
    1. Chan JF-W, Kok K-H, Zheng Z, Chu H, To KK-W, Yuan S, Yuen K-Y (2020) Genomic characterization of the 2019 novel human-pathogenic coronavirus isolated from a patient with atypical pneumonia after visiting Wuhan. Emerg Microbes Infect 9(1):221–236. 10.1080/22221751.2020.1719902
    1. Sedaghat Z, Karimi N (2020) Guillain Barre syndrome associated with COVID-19 infection: A case report. J Clin Neurosci 76:233–235
    1. Zhao H, Shen D, Zhou H, Liu J, Chen S (2020) Guillain-Barré syndrome associated with SARS-CoV-2 infection: causality or coincidence? Lancet Neurol 19(5):383–384
    1. Dobbs M (2011) Toxic Encephalopathy. Semin Neurol 31(02):184–193
    1. Yu F, Du L, Ojcius DM, Pan C, Jiang S (2020) Measures for diagnosing and treating infections by a novel coronavirus responsible for a pneumonia outbreak originating in Wuhan, China. Microbes Infect 22:74–79. 10.1016/j.micinf.2020.01.003
    1. Chan JF-W, Yuan S, Kok K-H, To KK-W, Chu H, Yang J, Xing F, Liu J, Yip CC-Y, Poon RW-S, Tsoi H-W, Lo SK-F, Chan K-H, Poon VK-M, Chan W-M, Ip JD, Cai J-P, Cheng VC-C, Chen H, Hui CK-M, Yuen K-Y (2020) A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster. Lancet 395(10223):514–523
    1. Huang C, Wang Y, Li X, Ren L, Zhao J, Hu Y et al (2020) Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395(10223):497–506
    1. Zhang G, Hu C, Luo L, Fang F, Chen Y, Li J et al (2020) Clinical features and short-term outcomes of 221 patients with COVID-19 in Wuhan, China. J Clin Virol 104364

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