Low prevalence of rotavirus and high prevalence of norovirus in hospital and community wastewater after introduction of rotavirus vaccine in Nicaragua

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Bucardo, Filemón ^a,b   Lindgren, Per Eric ^b   Svensson, Lennart ^b   Nordgren, Johan ^b  

^a UNIVERSITY OF LEÓN   (Spain)

^b LINKÖPING UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ROTAVIRUS VACCINE; VIRUS VACCINE;

ARTICLE; CONTROLLED STUDY; DIARRHEA; GENE SEQUENCE; GENOTYPE; HOSPITAL WASTE; HUMAN; NICARAGUA; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; NUCLEOTIDE SEQUENCE; PREVALENCE; ROTAVIRUS; ROTAVIRUS INFECTION; SEQUENCE ANALYSIS; VACCINATION; VIRUS INFECTION; VIRUS TRANSMISSION; WASTE WATER; ADULT; ANIMAL; CATTLE; CLASSIFICATION; DEMOGRAPHY; GENETICS; HOSPITAL; IMMUNIZATION; IMMUNOLOGY; ISOLATION AND PURIFICATION; MALE; MICROBIOLOGY; SEASON; SEWAGE; STATISTICS;

BOVINAE; NOROVIRUS; ROTAVIRUS;

ADULT; ANIMALS; CATTLE; GENOTYPE; HOSPITALS; HUMANS; IMMUNIZATION SCHEDULE; MALE; NICARAGUA; NOROVIRUS; RESIDENCE CHARACTERISTICS; ROTAVIRUS; SEASONS; VACCINATION; VIRAL VACCINES; WASTE DISPOSAL, FLUID; WATER MICROBIOLOGY;

EID: 80053928144     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025962     Document Type: Article

References (54)

1. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, et al. (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14: 1224-1231.
2. Parashar UD, Gibson CJ, Bresse JS, Glass RI, (2006) Rotavirus and severe childhood diarrhea. Emerg Infect Dis 12: 304-306.
3. Parashar UD, Burton A, Lanata C, Boschi-Pinto C, Shibuya K, et al. (2009) Global mortality associated with rotavirus disease among children in 2004. J Infect Dis 200 (Suppl 1): S9-S15.
4. Iturriza Gomara M, Wong C, Blome S, Desselberger U, Gray J, (2002) Molecular characterization of VP6 genes of human rotavirus isolates: correlation of genogroups with subgroups and evidence of independent segregation. J Virol 76: 6596-6601.
5. Nordgren J, Bucardo F, Svensson L, Lindgren PE, (2010) Novel light-upon-extension real-time PCR assay for simultaneous detection, quantification, and genogrouping of group A rotavirus. J Clin Microbiol 48: 1859-1865.
6. Duclos P, Okwo-Bele JM, Salisbury D, (2011) Establishing global policy recommendations: the role of the Strategic Advisory Group of Experts on immunization. Expert Rev Vaccines 10: 163-173.
7. Ramani S, Sankaran P, Arumugam R, Sarkar R, Banerjee I, et al. (2010) Comparison of viral load and duration of virus shedding in symptomatic and asymptomatic neonatal rotavirus infections. J Med Virol 82: 1803-1807.
8. Bucardo F, Nordgren J, Carlsson B, Kindberg E, Paniagua M, et al. (2010) Asymptomatic norovirus infections in Nicaraguan children and its association with viral properties and histo-blood group antigens. Pediatr Infect Dis J 29: 934-939.
9. Bucardo F, Nordgren J, Carlsson B, Paniagua M, Lindgren PE, et al. (2008) Pediatric norovirus diarrhea in Nicaragua. J Clin Microbiol 46: 2573-2580.
10. Arraj A, Bohatier J, Aumeran C, Bailly JL, Laveran H, et al. (2008) An epidemiological study of enteric viruses in sewage with molecular characterization by RT-PCR and sequence analysis. J Water Health 6: 351-358.
11. Barril PA, Giordano MO, Isa MB, Masachessi G, Ferreyra LJ, et al. (2010) Correlation between rotavirus A genotypes detected in hospitalized children and sewage samples in 2006, Cordoba, Argentina. J Med Virol 82: 1277-1281.
12. Nordgren J, Matussek A, Mattsson A, Svensson L, Lindgren PE, (2009) Prevalence of norovirus and factors influencing virus concentrations during one year in a full-scale wastewater treatment plant. Water Res 43: 1117-1125.
13. Myrmel M, Berg EM, Grinde B, Rimstad E, (2006) Enteric viruses in inlet and outlet samples from sewage treatment plants. J Water Health 4: 197-209.
14. Kamel AH, Ali MA, El-Nady HG, Aho S, Pothier P, et al. (2010) Evidence of the co-circulation of enteric viruses in sewage and in the population of Greater Cairo. J Appl Microbiol 108: 1620-1629.
15. Laverick MA, Wyn-Jones AP, Carter MJ, (2004) Quantitative RT-PCR for the enumeration of noroviruses (Norwalk-like viruses) in water and sewage. Lett Appl Microbiol 39: 127-136.
16. Lodder WJ, de Roda Husman AM, (2005) Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl Environ Microbiol 71: 1453-1461.
17. Kremer JR, Langlet J, Skraber S, Weicherding P, Weber B, et al. (2011) Genetic diversity of noroviruses from outbreaks, sporadic cases and wastewater in Luxembourg 2008-2009. Clin Microbiol Infect 17: 1173-1176.
18. Iwai M, Hasegawa S, Obara M, Nakamura K, Horimoto E, et al. (2009) Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyama, Japan (2006 to 2008). Appl Environ Microbiol 75: 1264-1270.
19. Orozco M, Vasquez J, Pedreira C, De Oliveira LH, Amador JJ, et al. (2009) Uptake of rotavirus vaccine and national trends of acute gastroenteritis among children in Nicaragua. J Infect Dis 200 (Suppl 1): S125-130.
20. Becker-Dreps S, Paniagua M, Dominik R, Cao H, Shah NK, et al. (2011) Changes in childhood diarrhea incidence in nicaragua following 3 years of universal infant rotavirus immunization. Pediatr Infect Dis J 30: 243-247.
21. Bucardo F, Karlsson B, Nordgren J, Paniagua M, Gonzalez A, et al. (2007) Mutated G4P[8] rotavirus associated with a nationwide outbreak of gastroenteritis in Nicaragua in 2005. J Clin Microbiol 45: 990-997.
22. Nordgren J, Bucardo F, Dienus O, Svensson L, Lindgren PE, (2008) Novel light-upon-extension real-time PCR assays for detection and quantification of genogroup I and II noroviruses in clinical specimens. J Clin Microbiol 46: 164-170.
23. Swedish Environmental Protection Agency (2008) Guidance to the Swedish Environmental Protection Agency's regulation for environmental reports (Vägledning om Naturvårdsverkets föreskrifter om miljörapport).
24. Iturriza-Gomara M, Kang G, Gray J, (2004) Rotavirus genotyping: keeping up with an evolving population of human rotaviruses. J Clin Virol 31: 259-265.
25. Kojima S, Kageyama T, Fukushi S, Hoshino FB, Shinohara M, et al. (2002) Genogroup-specific PCR primers for detection of Norwalk-like viruses. J Virol Methods 100: 107-114.
26. He XQ, Cheng L, Zhang DY, Xie XM, Wang DH, et al. (2011) One-year monthly survey of rotavirus, astrovirus and norovirus in three sewage treatment plants in Beijing, China and associated health risk assessment. Water Sci Technol 63: 191-198.
27. Sdiri-Loulizi K, Hassine M, Aouni Z, Gharbi-Khelifi H, Chouchane S, et al. (2010) Detection and molecular characterization of enteric viruses in environmental samples in Monastir, Tunisia between January 2003 and April 2007. J Appl Microbiol 109: 1093-1104.
28. Hamza IA, Jurzik L, Stang A, Sure K, Uberla K, et al. (2009) Detection of human viruses in rivers of a densly-populated area in Germany using a virus adsorption elution method optimized for PCR analyses. Water Res 43: 2657-2668.
29. Prado T, Silva DM, Guilayn WC, Rose TL, Gaspar AM, et al. (2011) Quantification and molecular characterization of enteric viruses detected in effluents from two hospital wastewater treatment plants. Water Res 45: 1287-1297.
30. Mast TC, Khawaja S, Espinoza F, Paniagua M, Palacio Del Carmen L, et al. (2011) Case-control Study of the Effectiveness of Vaccination With Pentavalent Rotavirus Vaccine in Nicaragua. Pediatr Infect Dis J 30.
31. Espinoza F, Bucardo F, Paniagua M, Svensson L, Hallander HO, et al. (2006) Shifts of rotavirus g and p types in Nicaragua-2001-2003. Pediatr Infect Dis J 25: 1078-1080.
32. Tate JE, Panozzo CA, Payne DC, Patel MM, Cortese MM, et al. (2009) Decline and change in seasonality of US rotavirus activity after the introduction of rotavirus vaccine. Pediatrics 124: 465-471.
33. Fumian TM, Leite JP, Castello AA, Gaggero A, Caillou MS, et al. (2010) Detection of rotavirus A in sewage samples using multiplex qPCR and an evaluation of the ultracentrifugation and adsorption-elution methods for virus concentration. J Virol Methods 170: 42-46.
34. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, et al. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5: 607-625.
35. Boccia D, Tozzi AE, Cotter B, Rizzo C, Russo T, et al. (2002) Waterborne outbreak of Norwalk-like virus gastroenteritis at a tourist resort, Italy. Emerg Infect Dis 8: 563-568.
36. Cashman O, Lennon G, Sleator RD, Power E, Fanning S, et al. (2010) Changing profile of the bovine rotavirus G6 population in the south of Ireland from 2002 to 2009. Vet Microbiol 146: 238-244.
37. Alkan F, Ozkul A, Oguzoglu TC, Timurkan MO, Caliskan E, et al. (2010) Distribution of G (VP7) and P (VP4) genotypes of group A bovine rotaviruses from Turkish calves with diarrhea, 1997-2008. Vet Microbiol 141: 231-237.
38. Matthijnssens J, Joelsson DB, Warakomski DJ, Zhou T, Mathis PK, et al. (2010) Molecular and biological characterization of the 5 human-bovine rotavirus (WC3)-based reassortant strains of the pentavalent rotavirus vaccine, RotaTeq. Virology 403: 111-127.
39. Payne DC, Edwards KM, Bowen MD, Keckley E, Peters J, et al. (2010) Sibling transmission of vaccine-derived rotavirus (RotaTeq) associated with rotavirus gastroenteritis. Pediatrics 125: e438-441.
40. Vesikari T, Matson DO, Dennehy P, Van Damme P, Santosham M, et al. (2006) Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med 354: 23-33.
41. Yen C, Jakob K, Esona MD, Peckham X, Rausch J, et al. (2011) Detection of fecal shedding of rotavirus vaccine in infants following their first dose of pentavalent rotavirus vaccine. Vaccine 29: 4151-4155.
42. Banyai K, Esona MD, Mijatovic S, Kerin TK, Pedreira C, et al. (2009) Zoonotic bovine rotavirus strain in a diarrheic child, Nicaragua. J Clin Virol 46: 391-393.
43. Patel M, Pedreira C, De Oliveira LH, Tate J, Orozco M, et al. (2009) Association between pentavalent rotavirus vaccine and severe rotavirus diarrhea among children in Nicaragua. JAMA 301: 2243-2251.
44. Bourdett-Stanziola L, Ortega-Barria E, Espinoza F, Bucardo F, Jimenez C, et al. (2010) Rotavirus genotypes in Costa Rica, Nicaragua, Honduras and the Dominican Republic. Intervirology 53: 390-393.
45. Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Banyai K, et al. (2009) Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 4: 1303-1316.
46. Tang B, Gilbert JM, Matsui SM, Greenberg HB, (1997) Comparison of the rotavirus gene 6 from different species by sequence analysis and localization of subgroup-specific epitopes using site-directed mutagenesis. Virology 237: 89-96.
47. Kitajima M, Oka T, Haramoto E, Takeda N, Katayama K, et al. (2010) Seasonal distribution and genetic diversity of genogroups I, II, and IV noroviruses in the Tamagawa River, Japan. Environ Sci Technol 44: 7116-7122.
48. da Silva AK, Le Saux JC, Parnaudeau S, Pommepuy M, Elimelech M, et al. (2007) Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl Environ Microbiol 73: 7891-7897.
49. Nordgren J, Kindberg E, Lindgren PE, Matussek A, Svensson L, (2010) Norovirus gastroenteritis outbreak with a secretor-independent susceptibility pattern, Sweden. Emerg Infect Dis 16: 81-87.
50. Lysen M, Thorhagen M, Brytting M, Hjertqvist M, Andersson Y, et al. (2009) Genetic diversity among food-borne and waterborne norovirus strains causing outbreaks in Sweden. J Clin Microbiol 47: 2411-2418.
51. CDC, (2007) Norovirus outbreak associated with ill food-service workers-Michigan, January-February 2006. MMWR Morbidity and mortality weekly report 56: 1212-1216.
52. Siebenga JJ, Vennema H, Zheng DP, Vinje J, Lee BE, et al. (2009) Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001-2007. J Infect Dis 200: 802-812.
53. Gallimore CI, Iturriza-Gomara M, Xerry J, Adigwe J, Gray JJ, (2007) Inter-seasonal diversity of norovirus genotypes: emergence and selection of virus variants. Arch Virol 152: 1295-1303.
54. Aw TG, Gin KY, Ean Oon LL, Chen EX, Woo CH, (2009) Prevalence and genotypes of human noroviruses in tropical urban surface waters and clinical samples in Singapore. Appl Environ Microbiol 75: 4984-4992.