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Molecular epidemiology of coxsackievirus type B1

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Abstract

Coxsackievirus type B1 (CVB1) has emerged globally as the predominant enterovirus serotype and is associated with epidemics of meningitis and chronic diseases. In this report, the phylogeny of CVB1 was studied based on the VP1 sequences of 11 North African isolates and 81 published sequences. All CVB1 isolates segregated into four distinct genogroups and 10 genotypes. Most of the identified genotypes of circulating CVB1 strains appear to have a strict geographical specificity. The North African strains were of a single genotype and probably evolved distinctly. Using a relaxed molecular clock model and three different population models (constant population, exponential growth and Bayesian skyline demographic models) in coalescent analysis using the BEAST program, the substitution rate in CVB1 varied between 6.95 × 10−3 and 7.37 × 10−3 substitutions/site/year in the VP1 region. This study permits better identification of circulating CVB1, which has become one of the most predominant enterovirus serotypes in humans.

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References

  1. Pallansch M, Roos R (2007) Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In: Knipe DM, Howley PM (eds) Fields virology, 5th edn. Lippincott Williams and Wilkins, Philadelphia, pp 839–894

    Google Scholar 

  2. Laitinen OH, Honkanen H, Pakkanen O, Oikarinen S, Hankaniemi MM, Huhtala H, Ruokoranta T, Lecouturier V, André P, Harju R, Virtanen SM, Lehtonen J, Almond JW, Simell T, Simell O, Ilonen J, Veijola R, Knip M, Hyöty H (2014) Coxsackievirus B1 is associated with induction of β-cell autoimmunity that portends type 1 diabetes. Diabetes 63(2):446–455. doi:10.2337/db13-0619

    Article  CAS  PubMed  Google Scholar 

  3. Oikarinen S, Tauriainen S, Hober D, Lucas B, Vazeou A, Sioofy-Khojine A, Bozas E, Muir P, Honkanen H, Ilonen J, Knip M, Keskinen P, Saha MT, Huhtala H, Stanway G, Bartsocas C, Ludvigsson J, Taylor K, Hyöty H (2014) Virus antibody survey in different European populations indicates risk association between coxsackievirus B1 and type 1 diabetes. Diabetes 63(2):655–662. doi:10.2337/db13-0620

    Article  CAS  PubMed  Google Scholar 

  4. Kim H, Kang B, Hwang S, Hong J, Chung J, Kim S, Jeong YS, Kim K, Cheon DS (2013) Molecular characteristics of human coxsackievirus B1 infection in Korea, 2008–2009. J Med Virol 85(1):110–115. doi:10.1002/jmv.23359

    Article  CAS  PubMed  Google Scholar 

  5. Khetsuriani N, Lamonte A, Oberste MS, Pallansch M (2006) Neonatal enterovirus infections reported to the National Enterovirus Surveillance system in the United States, 1983–2003. Pediatr Infect Dis J 25:889–893

    Article  PubMed  Google Scholar 

  6. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA, Centers for Disease Control and Prevention (2006) Enterovirus surveillance—United States, 1970–2005. MMWR Surveill Summ 55:1–20

    PubMed  Google Scholar 

  7. Centers for Disease Control and Prevention (CDC) (2008) Increased detections and severe neonatal disease associated with coxsackievirus b1 infection—United States, 2007. MMWR 57:553–556

    Google Scholar 

  8. Wikswo ME, Khetsuriani N, Fowlkes AL, Zheng X, Peñaranda S, Verma N, Shulman ST, Sircar K, Robinson CC, Schmidt T, Schnurr D, Oberste MS (2009) Increased activity of Coxsackievirus B1 strains associated with severe disease among young infants in the United States, 2007–2008. Clin Infect Dis 49(5):e44–e51. doi:10.1086/605090

    Article  PubMed  Google Scholar 

  9. Zhang L, Yan J, Ojcius DM, Lv H, Miao Z, Chen Y, Zhang Y, Yan J (2013) Novel and predominant pathogen responsible for the enterovirus-associated encephalitis in eastern China. PLoS One 8(12):e85023. doi:10.1371/journal.pone.0085023

    Article  PubMed Central  PubMed  Google Scholar 

  10. Muir P, Kammerer U, Korn K, Mulders MN, Poÿry T, Weissbrich B, Kandolf R, Cleator GM, Van Loon AM (1998) Molecular typing of enteroviruses: current status and future requirements. Clin Microbiol Rev 11(1):202–227

    PubMed Central  CAS  PubMed  Google Scholar 

  11. Nix WA, Oberste MS, Pallansch MA (2006) Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 44:2698–2704. doi:10.1128/JCM.00542-06

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Oberste MS, Maher K, Flemister MR (2000) Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol 38:1170–1174

    PubMed Central  CAS  PubMed  Google Scholar 

  13. Ishiko H, Takeda N, Miyamura K, Kato N, Tanimura M, Lin KH, Yin-Murphy M, Tam JS, Mu GF, Yamazaki S (1992) Phylogenetic analysis of a coxsackievirus A24 variant: the most recent worldwide pandemic was caused by progenies of a virus prevalent around 1981. Virology 187:748–759

    Article  CAS  PubMed  Google Scholar 

  14. Hughes MS, Hoey EM, Coyle PV (1993) A nucleotide sequence comparison of coxsackievirus B4 isolates from aquatic samples and clinical specimens. Epidemiol Infect 110:389–398

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Takeda N, Tanimura M, Miyamura K (1994) Molecular evolution of the major capsid protein VP1 of enterovirus 70. J Virol 68:854–862

    PubMed Central  CAS  PubMed  Google Scholar 

  16. Brown BA, Oberste MS, Alexander JP Jr, Kennett ML, Pallansch MA (1999) Molecular epidemiology and evolution of enterovirus 71 strains isolated from 1970 to 1998. J Virol 73:9969–9975

    PubMed Central  CAS  PubMed  Google Scholar 

  17. Santti J, Harvala H, Kinnunen L, Hyypia T (2000) Molecular epidemiology and evolution of coxsackievirus A9. J Gen Virol 81:1361–1372

    Article  CAS  PubMed  Google Scholar 

  18. Wang JR, Tsai HP, Huang SW, Kuo PH, Kiang D, Liu CC (2002) Laboratory diagnosis and genetic analysis of an echovirus 30- associated outbreak of aseptic meningitis in Taiwan in 2001. J Clin Microbiol 40:4439–4444

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Bailly JL, Brosson D, Archimbaud C, Chambon M, Henquell C, Peigue-Lafeuille H (2002) Genetic diversity of echovirus 30 during a meningitis outbreak, demonstrated by direct molecular typing from cerebrospinal fluid. J Med Virol 68(4):558–567

    Article  CAS  PubMed  Google Scholar 

  20. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Drummond AJ, Rambaut A (2007) BEAST: bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214

    Article  PubMed Central  PubMed  Google Scholar 

  22. Mulders MN, Salminen M, Kalkkinen N, Hovi T (2000) Molecular epidemiology of coxsackievirus B4 and disclosure of the correct VP1/2A (pro) cleavage site: evidence for high genomic diversity and long-term endemicity of distinct genotypes. J Gen Virol 81(Pt3):803–812

    Article  CAS  PubMed  Google Scholar 

  23. McWilliam Leitch EC, Cabrerizo M, Cardos J, Harvala H, Ivanova OE, Kroes AC, Lukashev A, Muir P, Odoom J et al (2010) Evolutionary dynamics and temporal/geographical correlates of recombination in the human enterovirus echovirus types 9, 11, and 30. J Virol 84:9292–9300. doi:10.1128/JVI.00783-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  24. Oberste MS, Maher K, Kennett ML, Campbell JJ, Carpenter MS, Schnurr D, Pallansch MA (1999) Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J Clin Microbiol 37:3928–3933

    PubMed Central  CAS  PubMed  Google Scholar 

  25. Oberste MS, Nix WA, Kilpatrick DR, Flemister MR, Pallansch MA (2003) Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East. Virus Res 91:241–248

    Article  CAS  PubMed  Google Scholar 

  26. Fares W, Rezig D, Seghier M, Ben Yahia A, Touzi H, Triki H (2011) Phylogenetic analysis of complete VP1 sequences of echoviruses 11 and 6: high genetic diversity and circulation of genotypes with a wide geographical and temporal range. J Med Microbiol 60(Pt7):1017–1025. doi:10.1099/jmm.0.028795-0

    Article  PubMed  Google Scholar 

  27. Fares W, Rezig D, Yahia AB, Touzi H, Meddeb Z, Triki H (2012) Genetic variability of type 3 echoviruses. Ann Biol Clin 70(2):189–198. doi:10.1684/abc.2012.0688

    CAS  Google Scholar 

  28. Rezig D, Fares W, Seghier M, Yahia AB, Touzi H, Triki H (2011) Update on molecular characterization of coxsackievirus B5 strains. J Med Virol 83(7):1247–1254. doi:10.1002/jmv.22084

    Article  CAS  PubMed  Google Scholar 

  29. Tian X, Zhang Y, Gu S, Fan Y, Sun Q, Zhang B, Yan S, Xu W, Ma X, Wang W (2014) New coxsackievirus B4 genotype circulating in Inner Mongolia Autonomous Region, China. PLoS One 9(3):e90379. doi:10.1371/journal.pone.0090379

    Article  PubMed Central  PubMed  Google Scholar 

  30. Tao Z, Wang H, Li Y, Liu G, Xu A, Lin X, Song L, Ji F, Wang S, Cui N, Song Y (2014) Molecular epidemiology of human enterovirus associated with aseptic meningitis in Shandong Province, China, 2006–2012. PLoS One 9(2):e89766. doi:10.1371/journal.pone.0089766

    Article  PubMed Central  PubMed  Google Scholar 

  31. Rao CD, Yergolkar P, Shankarappa KS (2012) Antigenic diversity of enteroviruses associated with nonpolio acute flaccid paralysis, India, 2007–2009. Emerg Infect Dis 18(11):1833–1840. doi:10.3201/eid1811.111457

    Article  PubMed Central  PubMed  Google Scholar 

  32. Bahri O, Rezig D, Nejma-Oueslati BB, Yahia AB, Sassi JB, Hogga N, Sadraoui A, Triki H (2005) Enteroviruses in Tunisia: virological surveillance over 12 years (1992–2003). J Med Microbiol 54(Pt1):63–69

    Article  CAS  PubMed  Google Scholar 

  33. McWilliam Leitch EC, Cabrerizo M, Cardosa J, Harvala H, Ivanova OE, Koike S, Kroes AC, Lukashev A, Perera D, Roivainen M, Susi P, Trallero G, Evans DJ, Simmonds P (2012) The association of recombination events in the founding and emergence of subgenogroup evolutionary lineages of human enterovirus 71. J Virol 86(5):2676–2685. doi:10.1128/JVI.06065-11

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Bailly JL, Mirand A, Henquell C, Archimbaud C, Chambon M, Regagnon C, Charbonné F, Peigue-Lafeuille H (2011) Repeated genomic transfers from echovirus 30 to echovirus 6 lineages indicate co-divergence between co-circulating populations of the two human enterovirus serotypes. Infect Genet Evol 11(2):276–289. doi:10.1016/j.meegid.2010.06.019

    Article  CAS  PubMed  Google Scholar 

  35. Tao Z, Wang H, Li Y, Xu A, Zhang Y, Song L, Yoshida H, Xu Q, Yang J, Zhang Y, Liu Y, Feng L, Xu W (2011) Cocirculation of two transmission lineages of echovirus 6 in Jinan, China, as revealed by environmental surveillance and sequence analysis. Appl Environ Microbiol 77(11):3786–3792. doi:10.1128/AEM.03044-10

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Smura T, Kakkola L, Blomqvist S, Klemola P, Parsons A, Kallio-Kokko H, Savolainen-Kopra C, Kainov DE, Roivainen M (2013) Molecular evolution and epidemiology of echovirus 6 in Finland. Infect Genet Evol 16:234–247. doi:10.1016/j.meegid.2013.02.011

    Article  CAS  PubMed  Google Scholar 

  37. Cabrerizo M, Trallero G, Simmonds P (2014) Recombination and evolutionary dynamics of human echovirus 6. J Med Virol 86(5):857–864. doi:10.1002/jmv.23741

    Article  PubMed  Google Scholar 

  38. Chu PY, Lu PL, Tsai YL, Hsi E, Yao CY, Chen YH, Hsu LC, Wang SY, Wu HS, Lin YY, Su HJ, Lin KH (2011) Spatiotemporal phylogenetic analysis and molecular characterization of coxsackievirus A4. Infect Genet Evol 11(6):1426–1435. doi:10.1016/j.meegid.2011.05.010

    Article  CAS  PubMed  Google Scholar 

  39. Kyriakopoulou Z, Bletsa M, Tsakogiannis D, Dimitriou TG, Amoutzias GD, Gartzonika C, Levidiotou-Stefanou S, Markoulatos P (2015) Molecular epidemiology and evolutionary dynamics of Echovirus 3 serotype. Infect Genet Evol 32:305–312. doi:10.1016/j.meegid.2015.03.008

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Tunisian Ministry for High Education and Scientific Research, grant number LR11-IPT09. We acknowledge the collaboration and expertise of Dr. Kais Ghedira from the Bioinformatics and Mathematical Modelling Group-Laboratory of Medical Parasitology, Biotechnologies and Biomolecules, LR11-IPT06, Pasteur Institute of Tunis, Tunisia.

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Correspondence to Dorra Rezig.

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Abdelkhalek, I., Seghier, M., Yahia, A.B. et al. Molecular epidemiology of coxsackievirus type B1. Arch Virol 160, 2815–2821 (2015). https://doi.org/10.1007/s00705-015-2561-5

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  • DOI: https://doi.org/10.1007/s00705-015-2561-5

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