Assessment of F-RNA coliphage as a potential indicator of enteric virus contamination of hog carcasses

Journal of Food Protection

Volumn 75, Issue 8, 2012, Pages 1492-1500

  Jones, T H ^a   Johns, M W ^a  

^a LACOMBE RESEARCH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HEPATITIS E VIRUS; SUIDAE;

EID: 84864480083     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-11-547     Document Type: Article

References (46)

1. Anonymous. 1995. Water quality. Detection and enumeration of bacteriophages. Part Enumeration of F-specific RNA bacteriophages. ISO 10705-1. International Organization for Standardization, Geneva.
2. Bollback, J. P., and J. P. Huelsenbeck. 2001. Phylogeny, genome evolution, and host specificity of single stranded RNA bacteriophage (family Leviviridae). J. Mol. Evol. 52:117-128.
3. Bouwknegt, M., F. Lodder-Verschoor, W. M. H. van der Poel, S. A. Rutjes, and A. M. de Roda Husman. 2007. Hepatitis E virus RNA in commercial porcine livers in the Netherlands. J. Food Prot. 70:2889-2895.
4. Bryant, J., D. A. Brereton, and C. O. Gill. 2003. Implementation of a validated HACCP system for the control of microbiological contamination of pig carcasses at a small abattoir. Can. Vet. J. 44: 51-55.
5. Calci, K. R., W. Burkhardt III, W. D. Watkins, and S. R. Rippey. 1998. Occurrence of male-specific bacteriophage in feral and domestic animal wastes, human feces, and human associated waters. Appl. Environ. Microbiol. 64:5027-5029.
6. Cole, D., S. C. Long, and M. D. Sobsey. 2003. Evaluation of FzRNA and DNA coliphages as source-specific indicators of fecal contamination in surface waters. Appl. Environ. Microbiol. 69:6507-6514.
7. Dastjerdi, A. M., J. Green, C. I. Gallimore, D. W. G. Brown, and J. C. Bridger. 1999. The bovine Newbury agent-2 is genetically more closely related to human SRSBs than to animal caliciviruses. Virology 254:1-5.
8. Dawson, D. J., A. Paish, L. M. Staffel, I. J. Seymour, and H. Appleton. 2005. Survival of viruses on fresh produce, using MS2 as a surrogate for norovirus. J. Appl. Microbiol. 98:203-209.
9. Doré, W. J., K. Henshilwood, and D. N. Lees. 2000. Evaluation of Fspecific RNA bacteriophage as a candidate human enteric virus indicator for bivalve molluscan shellfish. Appl. Environ. Microbiol. 66:1280-1285.
10. Entis, P., and P. Boleszczuk. 1990. Direct enumeration of coliforms and Escherichia coli by hydrophobic grid membrane filter in 24 h using MUG. J. Food Prot. 53:948-952.
11. Farkas, T., S. Nakajima, M. Sugieda, X. Deng, W. Zhong, and X. Jiang. 2005. Seroprevalence of noroviruses in swine. J. Clin. Microbiol. 43:657-661.
12. Farrah, S. R. 2006. Bacterial indicators of viruses, p. 189-204. In S. M. Goyal (ed.), Viruses in foods. Springer, New York.
13. Feagins, A. R., T. Opriessnig, D. K. Guenette, P. G. Halbur, and X. J. Meng. 2007. Detection and characterization of infectious hepatitis E virus from commercial pig livers sold in local grocery stores in the USA. J. Gen. Virol. 88:912-917.
14. Fernández-Barredo, S., C. Galiana, A. García, S. Vega, M. T. Gómez, and M. T. Pérez-Gracia. 2006. Detection of hepatitis E virus shedding in feces of pigs at different stages of production using reverse transcription-polymerase chain reaction. J. Vet. Diagn. Invest. 18: 462-465.
15. Formiga-Cruz, M., A. K. Allard, A. C. Conden-Hansson, K. Henshilwood, B. E. Hernroth, J. Jofre, D. N. Lees, F. Lucena, M. Papapetropoulou, R. E. Rangdale, A. Tsibouxi, A. Vantarakis, and R. Girones. 2003. Evaluation of potential indicators of viral contamination in shellfish and their applicability to diverse geographical areas. Appl. Environ. Microbiol. 69:1556-1563.
16. Furuse, K. 1987. Distribution of coliphages in the environment: general considerations, p. 87-124. In S. G. Goyal, C. P. Gerba, and G. Bitton (ed.), Phage ecology. Wiley, New York.
17. Gill, C. O., and T. Jones. 1997. Assessment of the hygienic characteristics of a process for dressing pasteurized pig carcasses. Food Microbiol. 14:81-91.
18. Grabow, W. O. K. 2001. Bacteriophages: update on applications as models for viruses in water. Water S. A. 27:251-268.
19. Havelaar, A. H., W. M. Hogeboom, and R. Pot. 1984. F-specific RNA bacteriophages in sewage: methodology and occurrence. Water Sci. Technol. 17:645-655.
20. Havelaar, A. H., W. M. Pot-Hogeboom, K. Furuse, and R. Pot. 1990. F-specific RNA bacteriophages and sensitive host strains in faeces and wastewater of human and animal origin. J. Appl. Bacteriol. 69:30-37.
21. Hsu, F. C., Y. C. Shieh, and M. D. Sobsey. 2002. Enteric bacteriophages as potential fecal indicators in ground beef and poultry meat. J. Food Prot. 65:93-99.
22. Huang, F. F., G. Haqshenas, D. K. Guenette, P. G. Halbur, S. K. Schommer, F. W. Pierson, T. E. Toth, and X. J. Meng. 2002. Detection by reverse transcription-PCR and genetic characterization of field isolates of swine hepatitis E virus from pigs in different geographic regions of the United States. J. Clin. Microbiol. 40:1326-1332.
23. Jones, T. H., J. Brassard, M. W. Johns, and M.-J. Gagné. 2009. The effect of pre-treatment and sonication of centrifugal ultrafiltration devices on virus recovery. J. Virol. Methods 161:199-204.
24. Jones, T. H., A. Houde, E. Poitras, P. Ward, and M. W. Johns. 2009. Development and evaluation of a multiplexed real-time TaqMan RTPCR assay with internal amplification control for detection of F-specific RNA coliphage genogroups I and IV. Food Environ. Virol. 1:57-65.
25. Jothikumar, N., T. L. Cromeans, B. H. Robertson, X. J. Meng, and V. R. Hill. 2006. A broadly reactive one-step real time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J. Virol. Methods 131:65-71.
26. Kennedy, J. E., Jr., C. I. Wei, and J. L. Oblinger. 1986. Distribution of coliphages in foods. J. Food Prot. 49:944-951.
27. Leblanc, D., P. Ward, M.-J. Gagné, E. Poitras, P. Müller, Y.-L. Trottier, C. Simard, and A. Houde. 2007. Presence of hepatitis E virus in a naturally infected swine herd from nursery to slaughter. Int. J. Food Microbiol. 117:160-166.
28. Lee, J. E., M. Y. Lim, S. Y. Kim, S. Lee, H. Lee, H. M. Oh, H. G. Hur, and G. P. Ko. 2009. Molecular characterization of bacteriophages for microbial source tracking in Korea. Appl. Environ. Microbiol. 75:7107-7114.
29. Liu, B. L., P. R. Lambden, H. Günther, P. Otto, M. Elschner, and I. N. Clarke. 1999. Molecular characterization of a bovine-like enteric calicivirus: relationship to the Norwalk-like viruses. J. Virol. 73:819-825.
30. Matsuda, H., K. Okada, K. Takahashi, and S. Mishiro. 2003. Severe hepatitis E virus infection after ingestion of uncooked liver from a wild boar. J. Infect. Dis. 188:944.
31. Mattison, K., J. Brassard, M.-J. Gagné, P. Ward, A. Houde, L. Lessard, C. Simard, A. Shukla, F. Pagotto, T. H. Jones, and Y.-L. Trottier. 2009. The feline calicivirus as a sample process control for the detection of food and waterborne RNA viruses. Int. J. Food Microbiol. 132:73-77.
32. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Bresee, C. Shapiro, P. M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
33. Ogorzaly, L., and C. Gantzer. 2006. Development of real-time RTPCR methods for specific detection of F-specific RNA bacteriophage genogroups: application to urban raw wastewater. J. Virol. Methods 138:131-139.
34. Pillai, S. D. 2006. Bacteriophages as fecal indicator organisms, p. 205-222. In S. M. Goyal (ed.), Viruses in foods. Springer, New York.
35. Schaper, M., J. Jofre, M. Uys, and W. O. K. Grabow. 2002. Distribution of genotypes of F-specific RNA bacteriophages in human and non-human sources of faecal pollution in South Africa and Spain. J. Appl. Microbiol. 92:657-667.
36. Scott, T. M., J. B. Rose, T. M. Jenkins, S. R. Farrah, and J. Lukasik. 2002. Microbial source tracking: current methodology and future directions. Appl. Environ. Microbiol. 68:5796-5803.
37. Smith, J. L. 2001. Areview of hepatitis E virus. J. Food Prot. 64:572-586.
38. Sobsey, M. D., D. A. Battigelli, G. A. Shin, and S. Newland. 1998. RT-PCR amplification detects inactivated viruses in water and wastewater. Water Sci. Technol. 38:91-94.
39. Sundram, A., N. Jumanlal, and M. M. Ehlers. 2006. Genotyping of FRNA coliphages isolated from wastewater and river water samples. Water S. A. 32:65-70.
40. Tei, S., N. Kitajima, K. Takahashi, and S. Mishiro. 2003. Zoonotic transmission of hepatitis E virus from deer to human beings. Lancet 362:371-373.
41. van Der Poel, W. H., J. Vinjé, R. van Der Heide, M. I. Herrera, A. Vivo, and M. P. Koopmans. 2000. Norwalk-like calicivirus genes in farm animals. Emerg. Infect. Dis. 6:36-41.
42. Vinjé, J., S. J. G. Oudejans, J. R. Stewart, M. D. Sobsey, and S. C. Long. 2004. Molecular detection and genotyping of male-specific coliphages by reverse transcription-PCR and reverse line blot hybridization. Appl. Environ. Microbiol. 70:5996-6004.
43. Wang, Q. H., M. G. Han, S. Cheetham, M. Souza, J. A. Funk, and L. J. Saif. 2005. Porcine noroviruses related to human noroviruses. Emerg. Infect. Dis. 11:1874-1881.
44. Ward, P., E. Poitras, D. Leblanc, A. Letellier, J. Brassard, D. Plante, and A. Houde. 2009. Comparative analysis of different Taqman realtime RT-PCR assays for the detection of swine hepatitis E virus and integration of feline calicivirus as internal control. J. Appl. Microbiol. 106:1360-1369.
45. Woody, M. A., and D. O. Cliver. 1995. Effects of temperature and host cell growth phase on replication of F-specific RNA coliphage Qb. Appl. Environ. Microbiol. 61:1520-1526.
46. Yazaki, Y., H. Mizuo, M. Takahashi, T. Nishizawa, N. Sasaki, Y. Gotanda, and H. Okamoto. 2003. Sporadic acute or fulminant hepatitis E in Hokkaido, Japan, may be food-borne, as suggested by the presence of hepatitis E virus in pig liver as food. J. Gen. Virol. 84: 2351-2357.