1887

Abstract

Human enteroviruses (HEVs) are responsible for a wide spectrum of clinical diseases. Even though usually associated with non-specific febrile illness, they are the most common cause of viral meningitis and pose a serious public-health problem, especially during outbreaks. Rapid detection and identification of HEV serotypes in clinical specimens are important in appropriate patient management and epidemiological investigation. A 5 year study (2003–2007) of clinical specimens from patients with viral meningitis and/or symptoms of enteroviral infection was carried out in Cyprus to determine the underlying enteroviral aetiology. Reverse transcription, followed by a sequential PCR strategy targeting the 5′ non-coding region and VP1 region, was used for typing the isolated enteroviruses. The serotype of each isolate was determined by search of the VP1 amplicon sequence against GenBank. Clinical specimens from a total of 146 patients were diagnosed as enterovirus-positive. Twenty-two different serotypes were identified. The main strains identified were echovirus 18 and echovirus 30, followed by coxsackievirus B5, echovirus 9, echovirus 6, coxsackievirus A10 and coxsackievirus B2. However, rapid changes in serotype frequency and diversity were observed over time. Serotype distribution corresponded essentially with observations reported from other European countries in the same period. The present report demonstrates the epidemiology of enteroviruses in Cyprus from 2003 to 2007.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.029892-0
2011-10-01
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/jmm/60/10/1433.html?itemId=/content/journal/jmm/10.1099/jmm.0.029892-0&mimeType=html&fmt=ahah

References

  1. Antona D., Chomel J. J.with theEnterovirus Surveillance Laboratory Network 2005; Increase in viral meningitis cases reported in France, summer 2005. Euro Surveill 10:E050908–, 1[PubMed]
    [Google Scholar]
  2. Antona D., Lévêque N., Chomel J. J., Dubrou S., Lévy-Bruhl D., Lina B. 2007; Surveillance of enteroviruses in France, 2000–2004. Eur J Clin Microbiol Infect Dis 26:403–412 [View Article][PubMed]
    [Google Scholar]
  3. Archimbaud C., Chambon M., Bailly J. L., Petit I., Henquell C., Mirand A., Aublet-Cuvelier B., Ughetto S., Beytout J. et al. 2009; Impact of rapid enterovirus molecular diagnosis on the management of infants, children, and adults with aseptic meningitis. J Med Virol 81:42–48 [View Article][PubMed]
    [Google Scholar]
  4. Bahri O., Rezig D., Nejma-Oueslati B. B., Yahia A. B., Sassi J. B., Hogga N., Sadraoui A., Triki H. 2005; Enteroviruses in Tunisia: virological surveillance over 12 years (1992–2003). J Med Microbiol 54:63–69 [View Article][PubMed]
    [Google Scholar]
  5. Bailly J. L., Mirand A., Henquell C., Archimbaud C., Chambon M., Charbonné F., Traoré O., Peigue-Lafeuille H. 2009; Phylogeography of circulating populations of human echovirus 30 over 50 years: nucleotide polymorphism and signature of purifying selection in the VP1 capsid protein gene. Infect Genet Evol 9:699–708 [View Article][PubMed]
    [Google Scholar]
  6. Bolanaki E., Kottaridi C., Dedepsidis E., Kyriakopoulou Z., Pliaka V., Pratti A., Levidiotou-Stefanou S., Markoulatos P. 2008; Direct extraction and molecular characterization of enteroviruses genomes from human faecal samples. Mol Cell Probes 22:156–161 [View Article][PubMed]
    [Google Scholar]
  7. Brown B., Oberste M. S., Maher K., Pallansch M. A. 2003; Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J Virol 77:8973–8984 [View Article][PubMed]
    [Google Scholar]
  8. Brunel D., Lévêque N., Jacques J., Renois F., Motte J., Andréoletti L. 2008; Clinical and virological features of an aseptic meningitis outbreak in North-Eastern France, 2005. J Clin Virol 42:225–228 [View Article][PubMed]
    [Google Scholar]
  9. Cabrerizo M., Echevarria J. E., González I., de Miguel T., Trallero G. 2008; Molecular epidemiological study of HEV-B enteroviruses involved in the increase in meningitis cases occurred in Spain during 2006. J Med Virol 80:1018–1024 [View Article][PubMed]
    [Google Scholar]
  10. Caro V., Guillot S., Delpeyroux F., Crainic R. 2001; Molecular strategy for ‘serotyping’ of human enteroviruses. J Gen Virol 82:79–91[PubMed]
    [Google Scholar]
  11. Casas I., Palacios G. F., Trallero G., Cisterna D., Freire M. C., Tenorio A. 2001; Molecular characterization of human enteroviruses in clinical samples: comparison between VP2, VP1, and RNA polymerase regions using RT nested PCR assays and direct sequencing of products. J Med Virol 65:138–148 [View Article][PubMed]
    [Google Scholar]
  12. CDC 2003; Outbreaks of aseptic meningitis associated with echoviruses 9 and 30 and preliminary surveillance reports on enterovirus activity – United States, 2003. MMWR Morb Mortal Wkly Rep 52:761–764[PubMed]
    [Google Scholar]
  13. CDC 2006; Enterovirus surveillance – United States, 2002–2004. MMWR Morb Mortal Wkly Rep 55:153–156[PubMed]
    [Google Scholar]
  14. Chambon M., Archimbaud C., Bailly J. L., Henquell C., Regagnon C., Charbonné F., Peigue-Lafeuille H. 2001; Circulation of enteroviruses and persistence of meningitis cases in the winter of 1999–2000. J Med Virol 65:340–347 [View Article][PubMed]
    [Google Scholar]
  15. Drake J. W., Holland J. J. 1999; Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96:13910–13913 [View Article][PubMed]
    [Google Scholar]
  16. Eurosurveillance Weekly 2006; Enteroviral meningitis outbreak, Kosovo, July–September 2006. Euro Surveill 11:E060914–4[PubMed]
    [Google Scholar]
  17. Hyypiä T., Hovi T., Knowles N. J., Stanway G. 1997; Classification of enteroviruses based on molecular and biological properties. J Gen Virol 78:1–11[PubMed]
    [Google Scholar]
  18. Iturriza-Gómara M., Megson B., Gray J. 2006; Molecular detection and characterization of human enteroviruses directly from clinical samples using RT-PCR and DNA sequencing. J Med Virol 78:243–253 [View Article][PubMed]
    [Google Scholar]
  19. Kapusinszky B., Szomor K. N., Farkas A., Takács M., Berencsi G. 2010; Detection of non-polio enteroviruses in Hungary 2000–2008 and molecular epidemiology of enterovirus 71, coxsackievirus A16, and echovirus 30. Virus Genes 40:163–173 [View Article][PubMed]
    [Google Scholar]
  20. Khetsuriani N., Lamonte A., Oberste M. S., Pallansch M. 2006a; Neonatal enterovirus infections reported to the national enterovirus surveillance system in the United States, 1983–2003. Pediatr Infect Dis J 25:889–893 [View Article][PubMed]
    [Google Scholar]
  21. Khetsuriani N., Lamonte-Fowlkes A., Oberst S. , Pallansch M. A. 2006b; Enterovirus surveillance – United States, 1970–2005. MMWR Surveill Summ 55:1–20[PubMed]
    [Google Scholar]
  22. Leitch E. C., Harvala H., Robertson I., Ubillos I., Templeton K., Simmonds P. 2009; Direct identification of human enterovirus serotypes in cerebrospinal fluid by amplification and sequencing of the VP1 region. J Clin Virol 44:119–124 [View Article][PubMed]
    [Google Scholar]
  23. Lévêque N., Jacques J., Renois F., Antona D., Abely M., Chomel J. J., Andréoletti L. 2010; Phylogenetic analysis of echovirus 30 isolated during the 2005 outbreak in France reveals existence of multiple lineages and suggests frequent recombination events. J Clin Virol 48:137–141 [View Article][PubMed]
    [Google Scholar]
  24. Lukashev A. N., Ivanova O. E., Eremeeva T. P., Gmyl L. V. 2008; Analysis of echovirus 30 isolates from Russia and new independent states revealing frequent recombination and reemergence of ancient lineages. J Clin Microbiol 46:665–670 [View Article][PubMed]
    [Google Scholar]
  25. McWilliam Leitch E. C., Bendig J., Cabrerizo M., Cardosa J., Hyypiä T., Ivanova O. E., Kelly A., Kroes A. C., Lukashev A. et al. 2009; Transmission networks and population turnover of echovirus 30. J Virol 83:2109–2118 [View Article][PubMed]
    [Google Scholar]
  26. McWilliam Leitch E. C., Cabrerizo M., Cardosa J., Harvala H., Ivanova O. E., Kroes A. C., 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 [View Article][PubMed]
    [Google Scholar]
  27. Mirand A., Archimbaud C., Henquell C., Michel Y., Chambon M., Peigue-Lafeuille H., Bailly J. L. 2006; Prospective identification of HEV-B enteroviruses during the 2005 outbreak. J Med Virol 78:1624–1634 [View Article][PubMed]
    [Google Scholar]
  28. Mirand A., Henquell C., Archimbaud C., Peigue-Lafeuille H., Bailly J. L. 2007; Emergence of recent echovirus 30 lineages is marked by serial genetic recombination events. J Gen Virol 88:166–176 [View Article][PubMed]
    [Google Scholar]
  29. Mirand A., Henquell C., Archimbaud C., Chambon M., Charbonne F., Peigue-Lafeuille H., Bailly J. L. 2008; Prospective identification of enteroviruses involved in meningitis in 2006 through direct genotyping in cerebrospinal fluid. J Clin Microbiol 46:87–96 [View Article][PubMed]
    [Google Scholar]
  30. Morens D., Pallansch M. A. 1995; Epidemiology. In Human Enterovirus Infections pp. 3–24 Edited by Rotbart H. A. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  31. Muir P., Kämmerer U., Korn K., Mulders M. N., Pöyry T., Weissbrich B., Kandolf R., Cleator G. M., van Loon A. M.forThe European Union Concerted Action on Virus Meningitis and Encephalitis 1998; Molecular typing of enteroviruses: current status and future requirements. Clin Microbiol Rev 11:202–227[PubMed]
    [Google Scholar]
  32. Nix W. A., Oberste M. S., Pallansch M. A. 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 [View Article][PubMed]
    [Google Scholar]
  33. Norder H., Bjerregaard L., Magnius L. O. 2001; Homotypic echoviruses share aminoterminal VP1 sequence homology applicable for typing. J Med Virol 63:35–44 [View Article][PubMed]
    [Google Scholar]
  34. Oberste M. S., Maher K., Kilpatrick D. R., Pallansch M. A. 1999; Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 73:1941–1948[PubMed]
    [Google Scholar]
  35. Oberste M. S., Maher K., Flemister M. R., Marchetti G., Kilpatrick D. R., Pallansch M. A. 2000; Comparison of classic and molecular approaches for the identification of untypeable enteroviruses. J Clin Microbiol 38:1170–1174[PubMed]
    [Google Scholar]
  36. Oberste M. S., Nix W. A., Maher K., Pallansch M. A. 2003; Improved molecular identification of enteroviruses by RT-PCR and amplicon sequencing. J Clin Virol 26:375–377 [View Article][PubMed]
    [Google Scholar]
  37. Ortner B., Huang C. W., Schmid D., Mutz I., Wewalka G., Allerberger F., Yang J. Y., Huemer H. P. 2009; Epidemiology of enterovirus types causing neurological disease in Austria 1999–2007: detection of clusters of echovirus 30 and enterovirus 71 and analysis of prevalent genotypes. J Med Virol 81:317–324 [View Article][PubMed]
    [Google Scholar]
  38. Palacios G., Casas I., Tenorio A., Freire C. 2002; Molecular identification of enterovirus by analyzing a partial VP1 genomic region with different methods. J Clin Microbiol 40:182–192 [View Article][PubMed]
    [Google Scholar]
  39. Pallansch M. A., Oberste M. S. 2003; Coxsackievirus, echovirus, and other enteroviruses. In Infectious Diseases pp. 2047–2053 Edited by Gorbach S., Bartlett J. G., Blacklow N. R. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  40. Pallansch M. A., Roos R. P. 2001; Enteroviruses: polioviruses, coxsackieviruses, echoviruses, and newer enteroviruses. In Fields Virology, 4th edn. pp. 723–775 Edited by Knipe D. M., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Straus S. E. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  41. Perevoscikovs J., Lucenko I., Nikiforova R. 2006; Outbreak of enteroviral meningitis in Latvia, August–October 2006. Euro Surveill 11:E061005–2[PubMed]
    [Google Scholar]
  42. Richter J., Koptides D., Tryfonos C., Christodoulou C. 2006; Molecular typing of enteroviruses associated with viral meningitis in Cyprus, 2000–2002. J Med Microbiol 55:1035–1041 [View Article][PubMed]
    [Google Scholar]
  43. Richter J., Bashiardes S., Koptides D., Tryfonos C., Pissarides N., Stavrou N., Papageorgiou G. T., Christodoulou C. 2008; 2005 poliovirus eradication: poliovirus presence in Cyprus 2 years after. Water Sci Technol 58:647–651 [View Article][PubMed]
    [Google Scholar]
  44. Rotbart H. A. 1995; Meningitis and encephalitis. In Human Enterovirus Infections pp. 271–289 Edited by Rotbart H. A. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  45. Roth B., Enders M., Arents A., Pfitzner A., Terletskaia-Ladwig E. 2007; Epidemiologic aspects and laboratory features of enterovirus infections in Western Germany, 2000–2005. J Med Virol 79:956–962 [View Article][PubMed]
    [Google Scholar]
  46. Santti J., Hyypiä T., Kinnunen L., Salminen M. 1999; Evidence of recombination among enteroviruses. J Virol 73:8741–8749[PubMed]
    [Google Scholar]
  47. Simmonds P., Welch J. 2006; Frequency and dynamics of recombination within different species of human enteroviruses. J Virol 80:483–493 [View Article][PubMed]
    [Google Scholar]
  48. Stanway G., Brown F., Christian P., Hovi T., Hyypiä T., King A. M. Q., Knowles N. J., Lemon S. M., Minor P. D. et al. 2005; Family Picornaviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp. 757–778 Edited by Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. London: Elsevier/Academic Press;
    [Google Scholar]
  49. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  50. Tavakoli N. P., Wang H., Nattanmai S., Dupuis M., Fusco H., Hull R. 2008; Detection and typing of enteroviruses from CSF specimens from patients diagnosed with meningitis/encephalitis. J Clin Virol 43:207–211 [View Article][PubMed]
    [Google Scholar]
  51. Thoelen I., Lemey P., Van Der Donck I., Beuselinck K., Lindberg A. M., Van Ranst M. 2003; Molecular typing and epidemiology of enteroviruses identified from an outbreak of aseptic meningitis in Belgium during the summer of 2000. J Med Virol 70:420–429 [View Article][PubMed]
    [Google Scholar]
  52. Thoelen I., Moës E., Lemey P., Mostmans S., Wollants E., Lindberg A. M., Vandamme A. M., Van Ranst M. 2004; Analysis of the serotype and genotype correlation of VP1 and the 5′ noncoding region in an epidemiological survey of the human enterovirus B species. J Clin Microbiol 42:963–971 [View Article][PubMed]
    [Google Scholar]
  53. Trallero G., Avellon A., Otero A., De Miguel T., Pérez C., Rabella N., Rubio G., Echevarria J. E., Cabrerizo M. 2010; Enteroviruses in Spain over the decade 1998–2007: virological and epidemiological studies. J Clin Virol 47:170–176 [View Article][PubMed]
    [Google Scholar]
  54. Tsao K. C., Huang C. G., Huang Y. L., Chen F. C., Huang P. N., Huang Y. C., Lin T. Y., Shih S. R., Chang S. C. 2010; Epidemiologic features and virus isolation of enteroviruses in Northern Taiwan during 2000–2008. J Virol Methods 165:330–332 [View Article][PubMed]
    [Google Scholar]
  55. WHO 2003 Guidelines for Environmental Surveillance of Poliovirus Circulation Geneva: World Health Organization;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.029892-0
Loading
/content/journal/jmm/10.1099/jmm.0.029892-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error