Sporadic isolation of Sabin-like polioviruses and high-level detection of non-polio enteroviruses during sewage surveillance in seven Italian cities, after several years of inactivated poliovirus vaccination

Applied and Environmental Microbiology

Volumn 80, Issue 15, 2014, Pages 4491-4501

  Battistone, A ^a   Buttinelli, G ^a   Fiore, S ^a   Amato, C ^a   Bonomo, P ^a   Patti, A M ^b   Vulcano, A ^b   Barbi, M ^c   Binda, S ^c   Pellegrinelli, L ^c   Tanzi, M L ^d   Affanni, P ^d   Castiglia, P ^e   Germinario, C ^f   Mercurio, P ^g   Cicala, A ^g   Triassi, M ^h   Pennino, F ^h   Fiore, L ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF PARMA   (Italy)

^e UNIVERSITY OF SASSARI   (Italy)

^f UNIVERSITY OF BARI   (Italy)

^g AMAP SpA   (Italy)

^h UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

D REGION; SEWAGE; VACCINES; VIRUSES;

CLINICAL STRAINS; ENVIRONMENTAL STRAIN; ENZYME LINKED IMMUNOSORBENT ASSAY; MOLECULAR APPROACH; MUTATION RATES; NON-CODING REGION; POTENTIAL RISKS; SEQUENCE IDENTITY;

MONITORING;

ORAL POLIOMYELITIS VACCINE; POLIOMYELITIS VACCINE; SEWAGE; VIRUS PROTEIN;

CITY; CLASSIFICATION; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; ENVIRONMENTAL MONITORING; GENETICS; HUMAN; ISOLATION AND PURIFICATION; ITALY; MOLECULAR GENETICS; PHYLOGENY; POLIOMYELITIS; POLIOMYELITIS VIRUS; SENTINEL SURVEILLANCE; SEWAGE; VACCINATION; VIROLOGY;

CITIES; ENTEROVIRUS; ENTEROVIRUS INFECTIONS; ENVIRONMENTAL MONITORING; HUMANS; ITALY; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLIOMYELITIS; POLIOVIRUS; POLIOVIRUS VACCINE, INACTIVATED; POLIOVIRUS VACCINE, ORAL; SENTINEL SURVEILLANCE; SEWAGE; VACCINATION; VIRAL PROTEINS;

EID: 84904893426     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00108-14     Document Type: Article

References (89)

1. Patti AM, Martini V, Calvani A, Vulcano A, Zotti C, Sudano L, Gasparini R, Barbi M, Brusaferro S, Carraro V, Simeoni J, Poli A, Tanzi ML, Bonanni P, Battaglia MA, Carducci AL, D'Errico M, Iorio AM, Vallone S, Grasso GM, Triassi M. 2008. La sorveglianza della poliomielite in Italia: stato immunitario della popolazione di età 0-14 anni. Ann. Ig. 20(Suppl 3):15-22.
2. de Gourville E, Duintjer Tebbens RJ, Sangrujee N, Pallansch MA, Thompson KM. 2006. Global surveillance and the value of information: the case of the global polio laboratory network. Risk Anal. 26:1557-1569. http://dx.doi.org/10.1111/j.1539-6924.2006.00845.x.
3. Pallansch MA, Sandhu HS. 2006. The eradication of polio-progress and challenges. N. Engl. J. Med. 355:2508-2511. http://dx.doi.org/10.1056/NEJMp068200.
4. Aylward B, Yamada T. 2011. The polio endgame. N. Engl. J. Med. 364: 2273-2275. http://dx.doi.org/10.1056/NEJMp1104329.
5. Fiore L, Novello F, Grandolfo ME. 1996. Eradicazione della poliomielite e sorveglianza delle paralisi flaccide in Italia, p 43. In Rapporti ISTISAN 96/22. Istituto Superiore di Sanità, Rome, Italy.
6. Fiore L, Novello F, Simeoni P, Amato C, Vellucci L, De Stefano D, Grandolfo ME, Luzzi I. 1999. Surveillance of acute flaccid paralysis in Italy: 1996-1997. AFP Study Group. Acute flaccid paralysis. Eur. J. Epidemiol. 15:757-763.
7. Ministry of Health Italy. 2007. Attività per l'eradicazione globale della poliomielite. Stato della sorveglianza della paralisi flaccida acuta e del contenimento di laboratorio dei Poliovirus selvaggi in Italia nell'anno 2007. 0001451-P-13/01/2009. Ministry of Health Italy, Rome, Italy.
8. Novello F, Lombardi F, Amato C, Santoro R, Fiore L, Grandolfo ME, Pasquini P. 1987. Paralytic poliomyelitis in Italy (1981-85). Eur. J. Epidemiol. 3:54-60. http://dx.doi.org/10.1007/BF00145073.
9. WHO. 2003. Recommended standards for surveillance of selected vaccine preventable diseases: vaccines and biologicals, p 31-34. WHO/V&B/03.01. WHO, Geneva, Switzerland.
10. Hird TR, Grassly NC. 2012. Systematic review of mucosal immunity induced by oral and inactivated poliovirus vaccines against virus shedding following oral poliovirus challenge. PLoS Pathog. 8:e1002599. http://dx.doi.org/10.1371/journal.ppat.1002599.
11. Alexander JP, Ehresmann K, Seward J, Wax G, Harriman K, Fuller S, Cebelinski EA, Chen Q, Jorba J, Kew OM, Pallansch MA, Oberste MS, Schleiss M, Davis JP, Warshawsky B, Squires S, Hull HF; Vaccine-Derived Poliovirus Investigations Group. 2009. Transmission of imported vaccine-derived poliovirus in an undervaccinated community in Minnesota. J. Infect. Dis. 199:391-397. http://dx.doi.org/10.1086/596052.
12. Anis E, Kopel E, Singer SR, Kaliner E, Moerman L, Moran-Gilad J, Sofer D, Manor Y, Shulman LM, Mendelson E, Gdalevich M, Lev B, Gamzu R, Grotto I. 2013. Insidious reintroduction of wild poliovirus into Israel, 2013. Euro Surveill. 18:pii=20586. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20586.
13. Roivainen M, Blomqvist S, Al-Hello H, Paananen A, Delpeyroux F, Kuusi M, Hovi T. 2010. Highly divergent neurovirulent vaccine-derived polioviruses of all three serotypes are recurrently detected in Finnish sewage. Euro Surveill. 15:pii=19566. http://www.eurosurveillance.org/View Article.aspx?ArticleId=19566.
14. Zurbriggen S, Tobler K, Abril C, Diedrich S, Ackermann M, Pallansch MA, Metzler A. 2008. Isolation of Sabin-like polioviruses from wastewater in a country using inactivated polio vaccine. Appl. Environ. Microbiol. 74:5608-5614. http://dx.doi.org/10.1128/AEM.02764-07.
15. Dedepsidis E, Kyriakopoulou Z, Pliaka V, Kottaridi C, Bolanaki E, Levidiotou-Stefanou S, Komiotis D, Markoulatos P. 2007. Retrospective characterization of a vaccine-derived poliovirus type 1 isolate from sewage in Greece. Appl. Environ. Microbiol. 73:6697-6704. http://dx.doi.org/10.1128/AEM.00535-07.
16. Hovi T, Blomqvist S, Nasr E, Burns CC, Sarjakoski T, Ahmed N, Savolainen C, Roivainen M, Stenvik M, Laine P, Barakat I, Wahdan MH, Kamel FA, Asghar H, Pallansch MA, Kew OM, Gary HE, Jr, deGourville EM, El Bassioni L. 2005. Environmental surveillance of wild poliovirus circulation in Egypt-balancing between detection sensitivity and workload. J. Virol. Methods 126:127-134. http://dx.doi.org/10.1016/j.jviromet.2005.02.002.
17. El Bassioni L, Barakat I, Nasr E, de Gourville EM, Hovi T, Blomqvist S, Burns C, Stenvik M, Gary H, Kew OM, Pallansch MA, Wahdan MH. 2003. Prolonged detection of indigenous wild polioviruses in sewage from communities in Egypt. Am. J. Epidemiol. 158:807-815. http://dx.doi.org/10.1093/aje/kwg202.
18. Chowdhary R, Dhole TN. 2008. Interrupting wild poliovirus transmission using oral poliovirus vaccine: environmental surveillance in highrisks area of India. J. Med. Virol. 80:1477-1488. http://dx.doi.org/10.1002/jmv.21230.
19. Shulman LM, Manor Y, Sofer D, Handsher R, Swartz T, Delpeyroux F, Mendelson E. 2006. Neurovirulent vaccine-derived polioviruses in sewage from highly immune populations. PLoS One 1:e69. http://dx.doi.org/10.1371/journal.pone.0000069.
20. Tapparel C, Siegrist F, Petty TJ, Kaiser L. 2013. Picornavirus and enterovirus diversity with associated human diseases. Infect. Genet. Evol. 14:282-293. http://dx.doi.org/10.1016/j.meegid.2012.10.016.
21. Palacios G, Oberste MS. 2005. Enteroviruses as agents of emerging infectious diseases. J. Neurovirol. 11:424-433. http://dx.doi.org/10.1080/13550280591002531.
22. Yajima T. 2011. Viral myocarditis: potential defense mechanisms within the cardiomyocyte against virus infection. Future Microbiol. 6:551-566. http://dx.doi.org/10.2217/fmb.11.40.
23. Rhoades RE, Tabor-Godwin JM, Tsueng G, Feuer R. 2011. Enterovirus infections of the central nervous system. Virology 411:288-305. http://dx.doi.org/10.1016/j.virol.2010.12.014.
24. Hober D, Sane F, Jaïdane H, Riedweg K, Goffard A, Desailloud R. 2012. Immunology in the clinic review series; focus on type 1 diabetes and viruses: role of antibodies enhancing the infection with Coxsackievirus-B in the pathogenesis of type 1 diabetes. Clin. Exp. Immunol. 168:47-51. http://dx.doi.org/10.1111/j.1365-2249.2011.04559.x.
25. Pianetti A, Baffone W, Citterio B, Casaroli A, Bruscolini F, Salvaggio L. 2000. Presence of enteroviruses and reoviruses in the waters of the Italian coast of the Adriatic Sea. Epidemiol. Infect. 125:455-462. http://dx.doi.org/10.1017/S0950268899004604.
26. Rajtar B, Majek M, Polański L, Polz-Dacewicz M. 2008. Enteroviruses in water environment-a potential threat to public health. Ann. Agric. Environ. Med. 15:199-203.
27. Steele M, Odumeru J. 2004. Irrigation water as source of foodborne pathogens on fruit and vegetables. J. Food Prot. 67:2839-2849.
28. Muñoz I, Tomàs N, Mas J, García-Reyes JF, Molina-Díaz A, Fernández-Alba AR. 2010. Potential chemical and microbiological risks on human health from urban wastewater reuse in agriculture. Case study of wastewater effluents in Spain. J. Environ. Sci. Health B 45:300-309. http://dx.doi.org/10.1080/03601231003704648.
29. Viau E, Bibby K, Paez-Rubio T, Peccia J. 2011. Toward a consensus view on the infectious risks associated with land application of sewage sludge. Environ. Sci. Technol. 45:5459-5469. http://dx.doi.org/10.1021/es200566f.
30. Simmons FJ, Xagoraraki I. 2011. Release of infectious human enteric viruses by full-scale wastewater utilities. Water Res. 45:3590-3598. http://dx.doi.org/10.1016/j.watres.2011.04.001.
31. Francy DS, Stelzer EA, Bushon RN, Brady AM, Williston AG, Riddell KR, Borchardt MA, Spencer SK, Gellner TM. 2012. Comparative effectiveness of membrane bioreactors, conventional secondary treatment, and chlorine and UV disinfection to remove microorganisms from municipal wastewaters. Water Res. 46:4164-4178. http://dx.doi.org/10.1016/j.watres.2012.04.044.
32. Petrinca AR, Donia D, Pierangeli A, Gabrieli R, Degener AM, Bonanni E, Diaco L, Cecchini G, Anastasi P, Divizia M. 2009. Presence and environmental circulation of enteric viruses in three different wastewater treatment plants. J. Appl. Microbiol. 106:1608-1617. http://dx.doi.org/10.1111/j.1365-2672.2008.04128.x.
33. Pellegrinelli L, Binda S, Chiaramonte I, Primache V, Fiore L, Battistone A, Fiore S, Gambino M, Bubba L, Barbi M. 2013. Detection and distribution of culturable human enteroviruses through environmental surveillance in Milan, Italy. J. Appl. Microbiol. 115:1231-1239. http://dx.doi.org/10.1111/jam.12321.
34. Cesari C, Colucci ME, Veronesi L, Giordano R, Paganuzzi F, Affanni P, Bracchi MT, Capobianco E, Ferrari G, Tanzi ML. 2010. Detection of enteroviruses from urban sewage in Parma. Acta Biomed. 81:40-46.
35. WHO. 2003. Guidelines for environmental surveillance of poliovirus circulation. WHO/V&B/03.03. WHO, Geneva, Switzerland.
36. WHO. 2004. Polio laboratory manual. WHO/IVB/04.10. WHO, Geneva, Switzerland.
37. Kilpatrick DR, Iber JC, Chen Q, Ching K, Yang SJ, De L, Mandelbaum MD, Emery B, Campagnoli R, Burns CC, Kew O. 2011. Poliovirus serotype-specific VP1 sequencing primers. J. Virol. Methods 174:128-130. http://dx.doi.org/10.1016/j.jviromet.2011.03.020.
38. Di Lonardo A, Buttinelli G, Amato C, Novello F, Ridolfi B, Fiore L. 2002. Rapid methods for identification of poliovirus isolates and determination of polio neutralizing antibody titers in human sera. J. Virol. Methods 101:189-196. http://dx.doi.org/10.1016/S0166-0934(01)00437-2.
39. Kew OM, Mulders MN, Lipskaya GY, da Silva EE, Pallansch MA. 1995. Molecular epidemiology of polioviruses. Semin. Virol. 6:401-414. http://dx.doi.org/10.1016/S1044-5773(05)80017-4.
40. Zoll GJ, Melchers WJG, Kopecka H, Jambroes G, Van der Poel HJA, Galama JMD. 1992. General primer-mediated polymerase chain reaction for detection of enteroviruses: application for diagnostic routine and persistent infections. J. Clin. Microbiol. 30:160-165.
41. Guillot S, Caro V, Cuervo N, Korotkova E, Combiescu M, Persu A, Aubert-Combiescu A, Delpeyroux F, Crainic R. 2000. Natural genetic exchanges between vaccine and wild poliovirus strains in humans. J. Virol. 74:8434-8443. http://dx.doi.org/10.1128/JVI.74.18.8434-8443.2000.
42. 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. http://dx.doi.org/10.1128/JCM.00542-06.
43. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739. http://dx.doi.org/10.1093/molbev/msr121.
44. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
45. Pianetti A, Baffone W, Citterio B, Casaroli A, Bruscolini F, Salvaggio L. 2000. Presence of enteroviruses and reoviruses in the waters of the Italian coast of the Adriatic Sea. Epidemiol. Infect. 125:455-462. http://dx.doi.org/10.1017/S0950268899004604.
46. Danovaro R, Armeni M, Corinaldesi C, Mei ML. 2003. Viruses and marine pollution. Mar. Pollut. Bull. 46:301-304. http://dx.doi.org/10.1016/S0025-326X(02)00461-7.
47. De Donno A, Liaci D, Bagordo F, Guido M, Carducci A. 2005. Evaluation of viral and bacterial contamination of coastal seawater. Ig. Sanità Pubbl. 61:585-600. (In Italian.)
48. Masciopinto C, La Mantia R, Carducci A, Casini B, Calvario A, Jatta E. 2007. Unsafe tap water in households supplied from groundwater in the Salento region of southern Italy. J. Water Health 5:129-148. http://dx.doi.org/10.2166/wh.2006.054.
49. Muscillo M, La Rosa G, Marianelli C, Zaniratti S, Capobianchi MR, Cantiani L, Carducci A. 2001. A new RT-PCR method for the identification of reoviruses in seawater samples. Water Res. 35:548-556. http://dx.doi.org/10.1016/S0043-1354(00)00282-7.
50. Verani M, Casini B, Battistini R, Pizzi F, Rovini E, Carducci A. 2006. One-year monthly monitoring of Torque teno virus (TTV) in river water in Italy. Water Sci. Technol. 54:191-195.
51. Donia D, Dell'Amico MC, Petrinca AR, Martinucci I, Mazzei M, Tolari F, Divizia M. 2012. Presence of hepatitis E RNA in mussels used as biomonitors of viral marine pollution. J. Virol. Methods 186:198-202. http://dx.doi.org/10.1016/j.jviromet.2012.06.007.
52. Battistone A, Buttinelli G, Bonomo P, Fiore S, Amato C, Mercurio P, Cicala A, Simeoni J, Foppa A, Triassi M, Pennino F, Fiore L. 26 November 2013. Detection of enteroviruses in influent and effluent flow samples from wastewater treatment plants in Italy. Food Environ. Virol. http://dx.doi.org/10.1007/s12560-013-9132-2.
53. Zheng H, Lu J, Zhang Y, Yoshida H, Guo X, Liu L, Li H, Zeng H, Fang L, Mo Y, Yi L, Chosa T, Xu W, Ke C. 2013. Prevalence of nonpolio enteroviruses in the sewage of Guangzhou City, China, from 2009 to 2012. Appl. Environ. Microbiol. 79:7679-7683. http://dx.doi.org/10.1128/AEM.02058-13.
54. Klement C, Kissova R, Lengyelova V, Stipalova D, Sobotova Z, Galama JM, Bopegamage S. 2013. Human enterovirus surveillance in the Slovak Republic from 2001 to 2011. Epidemiol. Infect. 141:2658-2662. http://dx.doi.org/10.1017/S0950268813000563.
55. Shukla D, Kumar A, Srivastava S, Idris MZ, Dhole TN. 2013. Environmental surveillance of enterovirus in Northern India using an integrated shell vial culture with a semi-nested RT PCR and partial sequencing of the VP1 gene. J. Med. Virol. 85:505-511. http://dx.doi.org/10.1002/jmv.23441.
56. Costán-Longares A, Mocé-Llivina L, Avellón A, Jofre J, Lucena F. 2008. Occurrence and distribution of culturable enteroviruses in wastewater and surface waters of north-eastern Spain. J. Appl. Microbiol. 105:1945-1955. http://dx.doi.org/10.1111/j.1365-2672.2008.03954.x.
57. Wieczorek M, Kuryk L, Witek A, Diuwe A, Litwińska B. 2013. The detection of enteroviruses in sewage using Caco-2 cells. Pol. J. Microbiol. 62:97-100.
58. Kargar M, Sadeghipour S, Nategh R. 2009. Environmental surveillance of non-polio enteroviruses in Iran. Virol. J. 6:149. http://dx.doi.org/10.1186/1743-422X-6-149.
59. Ruggeri FM, Fiore L. 2012. Vaccine preventable viral diseases and risks associated with waterborne transmission. Ann. Ist. Super. Sanita 48:460-472. http://dx.doi.org/10.4415/ANN_12_04_12.
60. Savolainen-Kopra C, Samoilovich E, Kahelin H, Hiekka AK, Hovi T, Roivainen M. 2009. Comparison of poliovirus recombinants: accumulation of point mutations provides further advantages. J. Gen. Virol. 90: 1859-1868. http://dx.doi.org/10.1099/vir.0.010942-0.
61. Avellón A, Cabrerizo M, de Miguel T, Pérez-Breña P, Tenorio A, Pérez JL, de Aragón MV, Trallero G. 2008. Paralysis case and contact spread of recombinant vaccine-derived poliovirus, Spain. Emerg. Infect. Dis. 14: 1807-1809. http://dx.doi.org/10.3201/eid1411.080517.
62. Haddad-Boubaker S, Ould-Mohamed-Abdallah MV, Ben-Yahia A, Triki H. 2010. Genetic recombination in vaccine poliovirus: comparative study in strains excreted in course of vaccination by oral poliovirus vaccine and circulating strains. Pathol. Biol. (Paris) 58:420-425. (In French.) http://dx.doi.org/10.1016/j.patbio.2009.01.004.
63. Benyesh-Melnick M, Melnick JL, Rawls WE, Wimberly I, Oro JB, Ben-Porath E, Rennick V. 1967. Studies of the immunogenicity, communicability, and genetic stability of oral polio vaccine administered in the winter. Am. J. Epidemiol. 86:112-136.
64. Alexander JP, Gary HE, Pallansch MA. 1997. Duration of poliovirus excretion and its implications for acute flaccid paralysis surveillance: a review of the literature. J. Infect. Dis. 175(Suppl 1):S176-S182. http://dx.doi.org/10.1093/infdis/175.1.176.
65. Huang QS, Greening G, Baker MG, Grimwood K, Hewitt J, Hulston D, van Duin L, Fitzsimons A, Garrett N, Graham D, Lennon D, Shimizu H, Miyamura T, Pallansch MA. 2005.Persistence of oral polio vaccine virus after its removal from the immunisation schedule in New Zealand. Lancet 366:394-396. http://dx.doi.org/10.1016/S0140-6736(05)66386-6.
66. 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.
67. van der Sanden SM, Koopmans MP, van der Avoort HG. 2013. Detection of human enteroviruses and parechoviruses as part of the national enterovirus surveillance in the Netherlands, 1996-2011. Eur. J. Clin. Microbiol. Infect. Dis. 32:1525-1531. http://dx.doi.org/10.1007/s10096-013-1906-9.
68. Fox JP. 1964. Epidemiological aspects of coxsackie and echo virus infections in tropical areas. Am. J. Public Health Nations Health 54:1134-1142. http://dx.doi.org/10.2105/AJPH.54.7.1134.
69. Parlamento Italiano. 1999. Pubblicato nella Gazzetta Ufficiale n. 246 del 20 ottobre 2000-Supplemento Ordinario n. 172. http://www.camera.it/parlam/leggi/deleghe/99152dl.htm. Parlamento Italiano, Rome, Italy.
70. Hot D, Legeay O, Jacques J, Gantzer C, Caudrelier Y, Guyard K, Lange M, Andréoletti L. 2003. Detection of somatic phages, infectious enteroviruses and enterovirus genomes as indicators of human enteric viral pollution in surface water. Water Res. 37:4703-4710. http://dx.doi.org/10.1016/S0043-1354(03)00439-1.
71. Bosch A. 1995. The survival of enteric viruses in the water environment. Microbiologia 11:393-396.
72. Bosch A. 1998. Humanentroviruses in water environment: a minireview. Int. Microbiol. 1:191-196.
73. Rzezutka A, Cook N. 2004. Survival of human enteric viruses in the environment and food. FEMS Microbiol. Rev. 28:441-453. http://dx.doi.org/10.1016/j.femsre.2004.02.001.
74. Antona D, Lévêque N, Chomel JJ, Dubrou S, Lévy-Bruhl D, Lina B. 2007. Surveillance of enterovirus in France, 2000-2004. Eur. J. Clin. Microbiol. Infect. Dis. 26:403-412. http://dx.doi.org/10.1007/s10096-007-0306-4.
75. Klemola P, Kaijalainen S, Ylipaasto P, Roivainen M. 2008. Diabetogenic effects of the most prevalent enteroviruses in Finnish sewage. Ann. N. Y. Acad. Sci. 1150:210-212. http://dx.doi.org/10.1196/annals.1447.012.
76. Groneck P, Jahn P, Schuler-Lüttmann S, Beyrer K. 2011. Neonatal enterovirus meningitis: transmission via parents during rooming-in and current epidemiology in Germany. Z. Geburtshilfe Neonatol. 215:1-5. (In German.). http://dx.doi.org/10.1055/s-0030-1255024.
77. Ramelli GP, Simonetti GD, Gorgievski-Hrisoho M, Aebi C, Bianchetti MG. 2004. Outbreak of coxsackie B5 virus meningitis in a Scout camp. Pediatr. Infect. Dis. J. 23:86-87.
78. Rezig D, Fares W, Seghier M, Yahia AB, Touzi H, Triki H. 2011. Update on molecular characterization of coxsackievirus B5 strains. J. Med. Virol. 83:1247-1254. http://dx.doi.org/10.1002/jmv.22084.
79. Nairn C, Clements GB. 1999. A study of enterovirus isolations in Glasgow from 1977 to 1997. J. Med. Virol. 58:304-312.
80. Trallero G, Avellon A, Otero A, De Miguel T, Pérez C, Rabella N, Rubio G, Echevarria JE, Cabrerizo M. 2010. Enterovirus in Spain over the decade 1998-2007: virological and epidemiological studies. J. Clin. Virol. 47:170-176. http://dx.doi.org/10.1016/j.jcv.2009.11.013.
81. Lukashev AN, Ivanova OE, Eremeeva TP, Gmyl LV. 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. http://dx.doi.org/10.1128/JCM.02386-06.
82. Cabrerizo M, Echevarria JE, González I, de Miguel T. 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. http://dx.doi.org/10.1002/jmv.21197.
83. Lévêquea N, Jacquesa J, Renoisa F, Antona D, Abelyd M, Chomele JJ, Andréolettia 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. http://dx.doi.org/10.1016/j.jcv.2010.03.011.
84. Milia MG, Cerutti F, Gregori G, Burdino E, Allice T, Ruggiero T, Proia M, De Rosa G, Enrico E, Lipani F, Di Perri G, Ghisetti V. 2013. Recent outbreak of aseptic meningitis in Italy due to echovirus 30 and phylogenetic relationship with other European circulating strains. J. Clin. Virol. 58:579-583. http://dx.doi.org/10.1016/j.jcv.2013.08.023.
85. Savolainen-Kopra C, Paananen A, Blomqvist S, Klemola P, Simonen ML, Lappalainen M, Vuorinen T, Kuusi M, Lemey P, Roivainen M. 2011. A large Finnish echovirus 30 outbreak was preceded by silent circulation of the same genotype. Virus Genes 42:28-36. http://dx.doi.org/10.1007/s11262-010-0536-x.
86. Prim N, Rodríguez G, Margall N, Del Cuerpo M, Trallero G, Rabella N. 2013. Combining cell lines to optimize isolation of human enterovirus from clinical specimens: report of 25 years of experience. J. Med. Virol. 85:116-120. http://dx.doi.org/10.1002/jmv.23426.
87. Rodríguez RA, Gundy PM, Gerba CP. 2008. Comparison of BGM and PLC/PRC/5 cell lines for total culturable viral assay of treated sewage. Appl. Environ. Microbiol. 74:2583-2587. http://dx.doi.org/10.1128/AEM.00626-07.
88. Combelas N, Holmblat B, Joffret ML, Colbère-Garapin F, Delpeyroux F. 2011. Recombination between poliovirus and coxsackie A viruses of species C: a model of viral genetic plasticity and emergence. Viruses 3:1460-1484. http://dx.doi.org/10.3390/v3081460.
89. Norder H, Bjerregaard L, Magnius L, Lina B, Aymard M, Chomel JJ. 2003. Sequencing of "untypeable" enteroviruses reveals new types, EV-77 and EV-78, within human enterovirus type B and substitutions in the BC loop of the VP1 protein for known types. J. Gen. Virol. 84:827-836. http://dx.doi.org/10.1099/vir.0.18647-0.