Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 30, pp 30497–30507 | Cite as

Quantification of human adenovirus and norovirus in river water in the north-east of France

  • Maryse Iris Sedji
  • Mihayl Varbanov
  • Marie Meo
  • Marius Colin
  • Laurence Mathieu
  • Isabelle Bertrand
Research Article
  • 110 Downloads

Abstract

Human adenoviruses (HAdVs) are a major cause of infection and have been proposed as viral indicators of water quality. Human noroviruses (NoV) are the main cause of viral acute gastroenteritis. Quantitative data on the environmental prevalence of both viruses are needed. The genomes of HAdVs enteric adenovirus type 41 (HAdV41) and noroviruses of genogroups I and II (NoV GGI and GGII) were quantified over a 6-month period in a river located in north-eastern France. The samples were collected downstream from the discharge of a wastewater treatment plant. The viruses were concentrated using a glass wool method and the viral genomes were quantified using digital droplet PCR (ddPCR). All river water samples (15/15) were positive for the genomes of HAdVs, HAdV41, NoV GGI and NoV GGII. Concentrations of HAdVs, HAdV41 and NoV GII genomes were similar and HAdV41 represented ~ 80% of HAdVs. Infectious HAdVs were quantified in these samples using an integrated cell culture-quantitative PCR method (ICC-qPCR); they were detected in 93% (14/15) and quantified in 53% (8/15) of the samples. Thus, infectious HAdVs represented 0.3 to 12.2% of total HAdV particles detected by ddPCR. Infectious HAdV41 particles were found in 73% (11/15) of the samples. This common presence of pathogenic enteric viruses underlines the impact of wastewater discharge on quality of surface waters and may constitute a threat for human health. The relative abundance of genome of HAdV41 underlines the need for studies focusing on the specific detection of its infectious forms along water cycle.

Keywords

Adenovirus type 41 Norovirus River water Genome Infectivity ICC-qPCR Quantification 

Notes

Acknowledgements

The authors thank Leslie Ogorzaly for her contribution in the quantification of HAdV41 genome, Romain Rivet for his excellent technical assistance in ddPCR assays and Coline Wietrich for her contribution to the ddPCR analyses.

Funding information

The present work was financially supported by the Institut Jean Barriol (CNRS and Université de Lorraine). Complementary financial support was obtained from Zone Atelier Moselle (ZAM).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

11356_2018_3045_Fig5_ESM.png (1.1 mb)
Figure 1

Sampling point in the river Meurthe in the metropolitan area of Nancy. Black arrow = discharge of treated wastewater in the river. Red star = sampling point in the river (PNG 1163 kb)

11356_2018_3045_MOESM1_ESM.docx (19 kb)
ESM 1 (DOCX 19 kb)

References

  1. Bertrand I, Schijven JF, Sánchez G, Wyn-Jones P, Ottoson J, Morin T, Muscillo M, Verani M, Nasser A, de Roda Husman AM, Myrmel M, Sellwood J, Cook N, Gantzer C (2012) The impact of temperature on the inactivation of enteric viruses in food and water: a review. J Appl Microbiol 112:1059–1057CrossRefGoogle Scholar
  2. Bofill-Mas S, Albinana-Gimenez N, Clemente-Casares P, Hundesa A, Rodriguez-Manzano J, Allard A, Calvo M, Girones R (2006) Quantification and stability of human adenoviruses and polyomavirus JCPyV in wastewater matrices. Appl Environ Microbiol 72:7894–7896CrossRefGoogle Scholar
  3. Bofill-Mas S, Calgua B, Clemente-Casares P, La Rosa G, Iaconelli M, Muscillo M, Rutjes S, de Roda Husman AM, Grunert A, Gräber I, Verani M, Carducci A, Calvo M, Wyn-Jones P, Girones R (2010) Quantification of human adenoviruses in European recreational waters. Food Environ Virol 2:101–109CrossRefGoogle Scholar
  4. Bofill-Mas S, Rusiñol M, Fernandez-Cassi X, Carratalà A, Hundesa A, Girones R (2013) Quantification of human and animal viruses to differentiate the origin of the fecal contamination present in environmental samples. Biomed Res Int:192089Google Scholar
  5. Brié A, Razafimahefa R, Loutreul J, Robert A, Gantzer C, Boudaud N, Bertrand I (2017) The effect of heat and free chlorine treatments on the surface properties of murine norovirus. Food Environ Virol 9:149–115CrossRefGoogle Scholar
  6. Calgua B, Fumian T, Rusiñol M, Rodriguez-Manzano J, Mbayed VA, Bofill-Mas S, Miagostovich M, Girones R (2013) Detection and quantification of classic and emerging viruses by skimmed-milk flocculation and PCR in river water from two geographical areas. Water Res 47:2797–2810CrossRefGoogle Scholar
  7. Corsi SR, Borchardt MA, Spencer SK, Hughes PE, Baldwin AK (2014) Human and bovine viruses in the Milwaukee River watershed: hydrologically relevant representation and relations with environmental variables. Sci Total Environ 490:849–860CrossRefGoogle Scholar
  8. Farkas K, Cooper DM, McDonald JE, Malham SK, de Rougemont A, Jones DL (2018) Seasonal and spatial dynamics of enteric viruses in wastewater and in riverine and estuarine receiving waters. Sci Total Environ 634:1174–1183CrossRefGoogle Scholar
  9. Fongaro G, Nascimento MA, Rigotto C, Ritterbusch G, da Silva AD, Esteves PA, Barardi CR (2013) Evaluation and molecular characterization of human adenovirus in drinking water supplies: viral integrity and viability assays. Virol J 10:166CrossRefGoogle Scholar
  10. Fongaro G, Padilha J, Schissi CD, Nascimento MA, Bampi GB, Viancelli A, Barardi CR (2015) Human and animal enteric virus in groundwater from deep wells, and recreational and network water. Environ Sci Pollut Res Int 22:20060–20066CrossRefGoogle Scholar
  11. Garcia LA, Viancelli A, Rigotto C, Pilotto MR, Esteves PA, Kunz A, Barardi CR (2012) Surveillance of human and swine adenovirus, human norovirus and swine circovirus in water samples in Santa Catarina, Brazil. J Water Health 10:445–452CrossRefGoogle Scholar
  12. Gassilloud B, Schwartzbrod L, Gantzer C (2003) Presence of viral genomes in mineral water: a sufficient condition to assume infectious risk? Appl Environ Microbiol 69:3965–3969CrossRefGoogle Scholar
  13. Gerba CP, Betancourt WQ (2017) Viral aggregation: impact on virus behavior in the environment. Environ Sci Technol 51:7318–7325CrossRefGoogle Scholar
  14. Gerrity D, Ryu H, Crittenden J, Abbaszadegan M (2008) UV inactivation of adenovirus type 4 measured by integrated cell culture qPCR. J Environ Sci Health A Tox Hazard Subst Environ Eng 43:1628–1638CrossRefGoogle Scholar
  15. Girones R, Ferrús MA, Alonso JL, Rodriguez-Manzano J, Calgua B, Corrêa Ade A, Hundesa A, Carratala A, Bofill-Mas S (2010) Molecular detection of pathogens in water—the pros and cons of molecular techniques. Water Res 44:4325–4339CrossRefGoogle Scholar
  16. Greening GE, Hewitt J, Lewis GD (2002) Evaluation of integrated cell culture-PCR (C-PCR) for virological analysis of environmental samples. J Appl Microbiol 93:745–750CrossRefGoogle Scholar
  17. Hamza IA, Jurzik L, Stang A, Sure K, Uberla K, Wilhelm M (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 43:2657–2668CrossRefGoogle Scholar
  18. Haramoto E, Katayama H, Oguma K, Ohgaki S (2007) Quantitative analysis of human enteric adenoviruses in aquatic environments. J Appl Microbiol 103:2153–2159CrossRefGoogle Scholar
  19. Hernroth BE, Conden-Hansson AC, Rehnstam-Holm AS, Girones R, Allard AK (2002) Environmental factors influencing human viral pathogens and their potential indicator organisms in the blue mussel, Mytilus edulis: the first Scandinavian report. Appl Environ Microbiol 68:4523–4533CrossRefGoogle Scholar
  20. Iaconelli M, Muscillo M, Della Libera S, Fratini M, Meucci L, De Ceglia M, Giacosa D, La Rosa G (2017a) One-year surveillance of human enteric viruses in raw and treated wastewaters, downstream river waters, and drinking waters. Food Environ Virol 9:79–88CrossRefGoogle Scholar
  21. Iaconelli M, Valdazo-González B, Equestre M, Ciccaglione AR, Marcantonio C, Della Libera S, La Rosa G (2017b) Molecular characterization of human adenoviruses in urban wastewaters using next generation and sanger sequencing. Water Res 121:240–247CrossRefGoogle Scholar
  22. Ibrahim C, Hassen A, Pothier P, Mejri S, Hammami S (2018) Molecular detection and genotypic characterization of enteric adenoviruses in a hospital wastewater. Environ Sci Pollut Res Int 25:10977–10987CrossRefGoogle Scholar
  23. International Organization for Standardization (2013) ISO/TS 152616–1:2013. Microbiology of the food chain—horizontal method for determination of hepatitis A virus and norovirus using real-time RT-PCR—part 1: method for quantification. https://www.iso.org/standard/65681.html
  24. Jones TH, Brassard J, Topp E, Wilkes G, Lapen DR (2017) Waterborne viruses and F-specific coliphages in mixed-use watersheds: microbial associations, host specificities, and affinities with environmental/land use factors. Appl Environ Microbiol 83Google Scholar
  25. Kishida N, Morita H, Haramoto E, Asami M, Akiba M (2012) One-year weekly survey of noroviruses and enteric adenoviruses in the Tone River water in Tokyo metropolitan area, Japan. Water Res 46:2905–2910CrossRefGoogle Scholar
  26. Ko G, Cromeans TL, Sobsey MD (2003) Detection of infectious adenovirus in cell culture by mRNA reverse transcription-PCR. Appl Environ Microbiol 69:7377–7384CrossRefGoogle Scholar
  27. Kosulin K, Geiger E, Vécsei A, Huber WD, Rauch M, Brenner E, Wrba F, Hammer K, Innerhofer A, Pötschger U, Lawitschka A, Matthes-Leodolter S, Fritsch G, Lion T (2016) Persistence and reactivation of human adenoviruses in the gastrointestinal tract. Clin Microbiol Infect 22:381.e1–381.e8CrossRefGoogle Scholar
  28. La Rosa G, Pourshaban M, Iaconelli M, Muscillo M (2010) Quantitative real-time PCR of enteric viruses in influent and effluent samples from wastewater treatment plants in Italy. Ann Ist Super Sanita 46:266–273Google Scholar
  29. La Rosa G, Sanseverino I, Della Libera S, Iaconelli M, Ferrero VEV, Barra Caracciolo A, Lettieri T (2017) The impact of anthropogenic pressure on the virological quality of water from the Tiber River, Italy. Lett Appl Microbiol 65:298–305CrossRefGoogle Scholar
  30. Lee C, Lee SH, Han E, Kim SJ (2004) Use of cell culture-PCR assay based on combination of A549 and BGMK cell lines and molecular identification as a tool to monitor infectious adenoviruses and enteroviruses in river water. Appl Environ Microbiol 70:6695–6705CrossRefGoogle Scholar
  31. Lee SH, Lee C, Lee KW, Cho HB, Kim SJ (2005) The simultaneous detection of both enteroviruses and adenoviruses in environmental water samples including tap water with an integrated cell culture-multiplex-nested PCR procedure. J Appl Microbiol 98:1020–1029CrossRefGoogle Scholar
  32. Leifels M, Hamza IA, Krieger M, Wilhelm M, Mackowiak M, Jurzik L (2016) From lab to lake—evaluation of current molecular methods for the detection of infectious enteric viruses in complex water matrices in an urban area. PLoS One 11:e0167105CrossRefGoogle Scholar
  33. Li F, Feng L, Liu Y, Zhen X, Chen L (2009) An integrated cell culture and quantitative polymerase chain reaction technique for determining titers of functional and infectious adenoviruses. Anal Biochem 391:157–159CrossRefGoogle Scholar
  34. Mackowiak M, Leifels M, Hamza IA, Jurzik L, Wingender J (2018) Distribution of Escherichia coli, coliphages and enteric viruses in water, epilithic biofilms and sediments of an urban river in Germany. Sci Total Environ 626:650–659CrossRefGoogle Scholar
  35. Mena KD, Gerba CP (2009) Waterborne adenovirus. Rev Environ Contam Toxicol 198:133–167Google Scholar
  36. Ogorzaly L, Tissier A, Bertrand I, Maul A, Gantzer C (2009) Relationship between F-specific RNA phage genogroups, faecal pollution indicators and human adenoviruses in river water. Water Res 43:1257–1264CrossRefGoogle Scholar
  37. Ogorzaly L, Bertrand I, Paris M, Maul A, Gantzer C (2010) Occurrence, survival, and persistence of human adenoviruses and F-specific RNA phages in raw groundwater. Appl Environ Microbiol 76:8019–8025CrossRefGoogle Scholar
  38. Ogorzaly L, Cauchie HM, Penny C, Perrin A, Gantzer C, Bertrand I (2013) Two-day detection of infectious enteric and non-enteric adenoviruses by improved ICC-qPCR. Appl Microbiol Biotechnol 97:4159–4166CrossRefGoogle Scholar
  39. Ogorzaly L, Walczak C, Galloux M, Etienne S, Gassilloud B, Cauchie HM (2015) Human adenovirus diversity in water samples using a next-generation amplicon sequencing approach. Food Environ Virol 7:112–121CrossRefGoogle Scholar
  40. Prevost B, Lucas FS, Goncalves A, Richard F, Moulin L, Wurtzer S (2015) Large scale survey of enteric viruses in river and waste water underlines the health status of the local population. Environ Int 79:42–50CrossRefGoogle Scholar
  41. Prevost B, Goulet M, Lucas FS, Joyeux M, Moulin L, Wurtzer S (2016) Viral persistence in surface and drinking water: suitability of PCR pre-treatment with intercalating dyes. Water Res 91:68–76CrossRefGoogle Scholar
  42. Rames E, Roiko A, Stratton H, Macdonald J (2016) Technical aspects of using human adenovirus as a viral water quality indicator. Water Res 96:308–326CrossRefGoogle Scholar
  43. Rodríguez RA, Polston PM, Wu MJ, Wu J, Sobsey MD (2013) An improved infectivity assay combining cell culture with real-time PCR for rapid quantification of human adenoviruses 41 and semi-quantification of human adenovirus in sewage. Water Res 47:3183–3191CrossRefGoogle Scholar
  44. Rodríguez-Lázaro D, Cook N, Ruggeri FM, Sellwood J, Nasser A, Nascimento MS, D'Agostino M, Santos R, Saiz JC, Rzeżutka A, Bosch A, Gironés R, Carducci A, Muscillo M, Kovač K, Diez-Valcarce M, Vantarakis A, von Bonsdorff CH, de Roda Husman AM, Hernández M, van der Poel WH (2012) Virus hazards from food, water and other contaminated environments. FEMS Microbiol Rev 36:786–814CrossRefGoogle Scholar
  45. Rusiñol M, Fernandez-Cassi X, Timoneda N, Carratalà A, Abril JF, Silvera C, Figueras MJ, Gelati E, Rodó X, Kay D, Wyn-Jones P, Bofill-Mas S, Girones R (2015) Evidence of viral dissemination and seasonality in a Mediterranean river catchment: implications for water pollution management. J Environ Manage 159:58–67CrossRefGoogle Scholar
  46. Ryu H, Cashdollar JL, Fout GS, Schrantz KA, Hayes S (2015) Applicability of integrated cell culture quantitative PCR (ICC-qPCR) for the detection of infectious adenovirus type 2 in UV disinfection studies. J Environ Sci Health A Tox Hazard Subst Environ Eng 50:777–787CrossRefGoogle Scholar
  47. Shih YJ, Tao CW, Tsai HC, Huang WC, Huang TY, Chen JS, Chiu YC, Hsu TK, Hsu BM (2017) First detection of enteric adenoviruses genotype 41 in recreation spring areas of Taiwan. Environ Sci Pollut Res Int In PressGoogle Scholar
  48. Siqueira-Silva J, Yeda FP, Favier AL, Mezin P, Silva ML, Barrella KM, Mehnert DU, Fender P, Hársi CM (2009) Infection kinetics of human adenovirus serotype 41 in HEK 293 cells. Mem Inst Oswaldo Cruz 104:736–744CrossRefGoogle Scholar
  49. Timm C, Luther S, Jurzik L, Hamza IA, Kistemann T (2016) Applying QMRA and DALY to assess health risks from river bathing. Int J Hyg Environ Health 9:681–692CrossRefGoogle Scholar
  50. Vieira CB, de Abreu Corrêa A, de Jesus MS, Luz SL, Wyn-Jones P, Kay D, Vargha M, Miagostovich MP (2016) Viruses surveillance under different season scenarios of the negro river basin, Amazonia, Brazil. Food Environ Virol 8:57–69CrossRefGoogle Scholar
  51. Wyn-Jones AP, Carducci A, Cook N, D'Agostino M, Divizia M, Fleischer J, Gantzer C, Gawler A, Girones R, Höller C, de Roda Husman AM, Kay D, Kozyra I, López-Pila J, Muscillo M, Nascimento MS, Papageorgiou G, Rutjes S, Sellwood J, Szewzyk R, Wyer M (2011) Surveillance of adenoviruses and noroviruses in European recreational waters. Water Res 45:1025–1038CrossRefGoogle Scholar
  52. Xagoraraki I, Kuo DH, Wong K, Wong M, Rose JB (2007) Occurrence of human adenoviruses at two recreational beaches of the great lakes. Appl Environ Microbiol 73:7874–7881CrossRefGoogle Scholar
  53. Ye XY, Ming X, Zhang YL, Xiao WQ, Huang XN, Cao YG, Gu KD (2012) Real-time PCR detection of enteric viruses in source water and treated drinking water in Wuhan, China. Curr Microbiol 65:244–253CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Université de Lorraine, CNRS, LCPME (Laboratoire de Chimie Physique et Microbiologie pour les Matériaux et l’Environnement)NancyFrance
  2. 2.Université de Lorraine, CNRS, L2CM (Laboratoire Lorrain de Chimie Moléculaire)NancyFrance
  3. 3.EPHE, PSL Research University, LCPMENancyFrance

Personalised recommendations