1,874
Views
9
CrossRef citations to date
0
Altmetric
Research Article

A mouse-adapted CVA6 strain exhibits neurotropism and triggers systemic manifestations in a novel murine model

, , ORCID Icon, , , , , , , & show all
Pages 2248-2263 | Received 12 Apr 2022, Accepted 25 Aug 2022, Published online: 26 Sep 2022

References

  • Solomon T, Lewthwaite P, Perera D, et al. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis. 2010 Nov;10(11):778–790.
  • Mao Q, Wang Y, Yao X, et al. Coxsackievirus A16: epidemiology, diagnosis, and vaccine. Hum Vaccin Immunother. 2014;10(2):360–367.
  • Xing W, Liao Q, Viboud C, et al. Hand, foot, and mouth disease in China, 2008–2012: an epidemiological study. Lancet Infect Dis. 2014 Apr;14(4):308–318.
  • Hu L, Maimaiti H, Zhou L, et al. Changing serotypes of hand, foot and mouth disease in Shanghai, 2017-2019. Gut Pathog. 2022 Mar 21;14(1):12.
  • Kamau E, Nguyen D, Celma C, et al. Seroprevalence and virologic surveillance of Enterovirus 71 and Coxsackievirus A6, United Kingdom, 2006–2017. Emerg Infect Dis. 2021 Sep;27(9):2261–2268.
  • Cabrerizo M, Tarrago D, Munoz-Almagro C, et al. Molecular epidemiology of enterovirus 71, coxsackievirus A16 and A6 associated with hand, foot and mouth disease in Spain. Clin Microbiol Infect. 2014 Mar;20(3):O150–O156.
  • Kobayashi M, Makino T, Hanaoka N, et al. Clinical manifestations of coxsackievirus A6 infection associated with a major outbreak of hand, foot, and mouth disease in Japan. Jpn J Infect Dis. 2013;66(3):260–261.
  • Mirand A, Cohen R, Bisseux M, et al. A large-scale outbreak of hand, foot and mouth disease, France, as at 28 September 2021. Euro Surveill. 2021 Oct;26:43.
  • Gopalkrishna V, Patil PR, Patil GP, et al. Circulation of multiple enterovirus serotypes causing hand, foot and mouth disease in India. J Med Microbiol. 2012 Mar;61(Pt 3):420–425.
  • Han JF, Xu S, Zhang Y, et al. Hand, foot, and mouth disease outbreak caused by coxsackievirus A6, China, 2013. J Infect. 2014 Sep;69(3):303–305.
  • Lim CT, Jiang L, Ma S, et al. Basic reproduction number of coxsackievirus type A6 and A16 and enterovirus 71: estimates from outbreaks of hand, foot and mouth disease in Singapore, a tropical city-state. Epidemiol Infect. 2016 Apr;144(5):1028–1034.
  • Centers for Disease C, Prevention. Notes from the field: severe hand, foot, and mouth disease associated with coxsackievirus A6 – Alabama, Connecticut, California, and Nevada, November 2011-February 2012. MMWR Morb Mortal Wkly Rep. 2012 Mar 30;61(12):213–214.
  • Fonseca MC, Sarmiento L, Resik S, et al. Coxsackievirus A6 and enterovirus 71 causing hand, foot and mouth disease in Cuba, 2011–2013. Arch Virol. 2014 Sep;159(9):2451–2455.
  • Zhao TS, Du J, Sun DP, et al. A review and meta-analysis of the epidemiology and clinical presentation of coxsackievirus A6 causing hand-foot-mouth disease in China and global implications. Rev Med Virol. 2020 Mar;30(2):e2087.
  • Ramirez-Fort MK, Downing C, Doan HQ, et al. Coxsackievirus A6 associated hand, foot and mouth disease in adults: clinical presentation and review of the literature. J Clin Virol. 2014 Aug;60(4):381–386.
  • Guimbao J, Rodrigo P, Alberto MJ, et al. Onychomadesis outbreak linked to hand, foot, and mouth disease, Spain, July 2008. Euro Surveill. 2010 Sep 16;15:37.
  • Rao CD, Yergolkar P, Shankarappa KS. Antigenic diversity of enteroviruses associated with nonpolio acute flaccid paralysis, India, 2007–2009. Emerg Infect Dis. 2012 Nov;18(11):1833–1840.
  • Blomqvist S, Klemola P, Kaijalainen S, et al. Co-circulation of coxsackieviruses A6 and A10 in hand, foot and mouth disease outbreak in Finland. J Clin Virol. 2010 May;48(1):49–54.
  • Logotheti M, Pogka V, Horefti E, et al. Laboratory investigation and phylogenetic analysis of enteroviruses involved in an aseptic meningitis outbreak in Greece during the summer of 2007. J Clin Virol. 2009 Nov;46(3):270–274.
  • Jiang Z, Zhang Y, Lin H, et al. A 10-day-old murine model of coxsackievirus A6 infection for the evaluation of vaccines and antiviral drugs. Front Immunol. 2021;12:665197.
  • Ji W, Qin L, Tao L, et al. Neonatal murine model of coxsackievirus A2 infection for the evaluation of antiviral therapeutics and vaccination. Front Microbiol. 2021;12:658093.
  • Li CX, Zhang B, Feng Y, et al. Establishment and characterization of an oral gerbil model for a non-mouse-adapted enterovirus 71 strain. Virus Res. 2018 Aug 15;255:117–126.
  • Liao CC, Liou AT, Chang YS, et al. Immunodeficient mouse models with different disease profiles by in vivo infection with the same clinical isolate of enterovirus 71. J Virol. 2014 Nov;88(21):12485–12499.
  • Liu CC, Hwang CS, Yang WS, et al. Long-term immunogenicity studies of formalin-inactivated enterovirus 71 whole-virion vaccine in macaques. PLoS One. 2014;9(9):e106756.
  • Li JP, Liao Y, Zhang Y, et al. Experimental infection of tree shrews (Tupaia belangeri) with Coxsackie virus A16. Dongwuxue Yanjiu. 2014 Nov 18;35(6):485–491.
  • Jin Y, Sun T, Zhou G, et al. Pathogenesis study of Enterovirus 71 using a novel human SCARB2 knock-in mouse model. mSphere. 2021 Mar 10;6:2.
  • Yang L, Mao Q, Li S, et al. A neonatal mouse model for the evaluation of antibodies and vaccines against coxsackievirus A6. Antiviral Res. 2016 Oct;134:50–57.
  • Zhang Z, Dong Z, Wei Q, et al. A neonatal murine model of Coxsackievirus A6 infection for evaluation of antiviral and vaccine efficacy. J Virol. 2017 May 1;91:9.
  • Reed LJ, Muench H. A simple method of estimating fifty per cent endpoints12. Am J Epidemiol. 1938;27(3):493–497.
  • Ji W, Zhu P, Liang R, et al. Coxsackievirus A2 leads to heart injury in a neonatal mouse model. Viruses. 2021 Aug 11;13:8.
  • Perez-de-Puig I, Miro-Mur F, Ferrer-Ferrer M, et al. Neutrophil recruitment to the brain in mouse and human ischemic stroke. Acta Neuropathol. 2015 Feb;129(2):239–257.
  • Haubruck P, Colbath AC, Liu Y, et al. Flow cytometry analysis of immune cell subsets within the murine spleen, bone marrow, lymph nodes and synovial tissue in an osteoarthritis model. J Vis Exp. 2020 Apr 24;e61008.
  • Ai Y, Zhang W, Wu J, et al. Molecular epidemiology and clinical features of enteroviruses-associated hand, foot, and mouth disease and herpangina outbreak in Zunyi, China, 2019. Front Med (Lausanne). 2021;8:656699.
  • Jiang H, Zhang Z, Rao Q, et al. The epidemiological characteristics of enterovirus infection before and after the use of enterovirus 71 inactivated vaccine in Kunming, China. Emerg Microbes Infect. 2021 Dec;10(1):619–628.
  • Fujimoto T, Iizuka S, Enomoto M, et al. Hand, foot, and mouth disease caused by coxsackievirus A6, Japan, 2011. Emerg Infect Dis. 2012 Feb;18(2):337–339.
  • Wei SH, Huang YP, Liu MC, et al. An outbreak of coxsackievirus A6 hand, foot, and mouth disease associated with onychomadesis in Taiwan, 2010. BMC Infect Dis. 2011 Dec 14;11:346.
  • Nhan LNT, Khanh TH, Hong NTT, et al. Clinical, etiological and epidemiological investigations of hand, foot and mouth disease in southern Vietnam during 2015–2018. PLoS Negl Trop Dis. 2020 Aug;14(8):e0008544.
  • de Sousa IP, Giamberardino HI, Raboni SM, et al. Simultaneous enterovirus EV-D68 and CVA6 infections causing acute respiratory distress syndrome and hand, foot and mouth disease. Virol J. 2021 Apr 30;18(1):88.
  • Liu H, Zhang M, Feng C, et al. Characterization of Coxsackievirus A6 strains isolated from children with hand, foot, and mouth disease. Front Cell Infect Microbiol. 2021;11:700191.
  • Gonzalez G, Carr MJ, Kobayashi M, et al. Enterovirus-associated hand-foot and mouth disease and neurological complications in Japan and the rest of the world. Int J Mol Sci. 2019 Oct 20;20:20.
  • Jin Y, Li D, Sun T, et al. Pathological features of Enterovirus 71-associated brain and lung damage in mice based on quantitative proteomic analysis. Front Microbiol. 2021;12:663019.
  • Wang SM, Lei HY, Liu CC. Cytokine immunopathogenesis of enterovirus 71 brain stem encephalitis. Clin Dev Immunol. 2012: 876241.
  • Sun YS, Yang ZN, Xu F, et al. Global gene expression analysis of the brainstem in EV71- and CVA16-infected gerbils. Viruses. 2019 Dec 30;12:1.
  • Zhang W, Huang Z, Huang M, et al. Predicting severe enterovirus 71-infected hand, foot, and mouth disease: cytokines and chemokines. Mediators Inflamm. 2020; 9273241.
  • Xing J, Liu D, Shen S, et al. Pathologic studies of fatal encephalomyelitis in children caused by Enterovirus 71. Am J Clin Pathol. 2016 Jul;146(1):95–106.
  • Khong WX, Yan B, Yeo H, et al. A non-mouse-adapted enterovirus 71 (EV71) strain exhibits neurotropism, causing neurological manifestations in a novel mouse model of EV71 infection. J Virol. 2012 Feb;86(4):2121–2131.
  • Qian SS, Wei ZN, Jin WP, et al. Efficacy of a coxsackievirus A6 vaccine candidate in an actively immunized mouse model. Emerg Microbes Infect. 2021 Dec;10(1):763–773.
  • Ren R, Racaniello VR. Poliovirus spreads from muscle to the central nervous system by neural pathways. J Infect Dis. 1992 Oct;166(4):747–752.
  • Douche-Aourik F, Berlier W, Feasson L, et al. Detection of enterovirus in human skeletal muscle from patients with chronic inflammatory muscle disease or fibromyalgia and healthy subjects. J Med Virol. 2003 Dec;71(4):540–547.
  • Ong KC, Badmanathan M, Devi S, et al. Pathologic characterization of a murine model of human enterovirus 71 encephalomyelitis. J Neuropathol Exp Neurol. 2008 Jun;67(6):532–542.
  • Li JG, Qu D, Li Y, et al. Acute kidney injury in critically ill children infected with influenza A virus (H1N1) and enterovirus 71. Zhonghua Er Ke Za Zhi. 2011 Nov;49(11):839–842.
  • Wu TC, Wang YF, Lee YP, et al. Immunity to avirulent enterovirus 71 and coxsackie A16 virus protects against enterovirus 71 infection in mice. J Virol. 2007 Oct;81(19):10310–10315.
  • Lin YW, Chang KC, Kao CM, et al. Lymphocyte and antibody responses reduce enterovirus 71 lethality in mice by decreasing tissue viral loads. J Virol. 2009 Jul;83(13):6477–6483.
  • Li S, Cai C, Feng J, et al. Peripheral T lymphocyte subset imbalances in children with enterovirus 71-induced hand, foot and mouth disease. Virus Res. 2014 Feb 13;180:84–91.
  • Lin TY, Chang LY, Hsia SH, et al. The 1998 enterovirus 71 outbreak in Taiwan: pathogenesis and management. Clin Infect Dis. 2002 May 1;34(Suppl. 2):S52–S57.
  • Nolan MA, Craig ME, Lahra MM, et al. Survival after pulmonary edema due to enterovirus 71 encephalitis. Neurology. 2003 May 27;60(10):1651–1656.
  • Liu CC, Chow YH, Chong P, et al. Prospect and challenges for the development of multivalent vaccines against hand, foot and mouth diseases. Vaccine. 2014 Oct 29;32(47):6177–6182.