Fate of Clostridium difficile during wastewater treatment and incidence in Southern Ontario watersheds

Journal of Applied Microbiology

Volumn 117, Issue 3, 2014, Pages 891-904

  Xu, C ^a   Weese, J S ^a   Flemming, C ^b   Odumeru, J ^b   Warriner, K ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b ONTARIO MINISTRY OF THE ENVIRONMENT   (Canada)

Author keywords

Anaerobic digester; Biosolids; Clostridium difficile; Community associated infections; Effluent; Sewage; Wastewater treatment

Indexed keywords

ANAEROBIC DIGESTION; BIOLOGICAL MATERIALS; BIOSOLIDS; EFFLUENT TREATMENT; ELECTROPHORESIS; RIVERS; SEDIMENTS; SEWAGE PUMPING PLANTS; SEWAGE TREATMENT PLANTS; WASTEWATER TREATMENT; WATER TREATMENT PLANTS;

ANAEROBIC DIGESTER; CLOSTRIDIUM DIFFICILE; COMMUNITY-ASSOCIATED INFECTION; DIGESTED SLUDGES; ONTARIO; RAW SEWAGE; RIVER SEDIMENTS; TREATED EFFLUENT; WASTE WATER TREATMENT PLANTS; WATER SOURCE;

EFFLUENTS;

ANOXIC CONDITIONS; BACTERIUM; EFFLUENT; ELECTROKINESIS; FLUVIAL DEPOSIT; GEL; SEWAGE TREATMENT; SLUDGE; SURVIVAL; WASTEWATER; WATERSHED;

ARTICLE; BACTERIUM ISOLATION; BIOSOLID; CANADA; CLOSTRIDIUM DIFFICILE; CLOSTRIDIUM PERFRINGENS; DNA FINGERPRINTING; EFFLUENT; INCIDENCE; NONHUMAN; PREVALENCE; PULSED FIELD GEL ELECTROPHORESIS; RIBOTYPING; RIVER; SEDIMENT; SEWAGE TREATMENT; SLUDGE DIGESTION; WASTE WATER MANAGEMENT; WASTE WATER TREATMENT PLANT; WATER SUPPLY; WATERSHED; CLASSIFICATION; ISOLATION AND PURIFICATION; MICROBIOLOGY; PEPTOCLOSTRIDIUM DIFFICILE; SEWAGE; WATER MANAGEMENT;

CANADA; ONTARIO [CANADA];

CLOSTRIDIUM DIFFICILE;

SEWAGE;

CLOSTRIDIUM DIFFICILE; ONTARIO; RIBOTYPING; RIVERS; SEWAGE; WATER PURIFICATION;

EID: 85027928308     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12575     Document Type: Article

References (40)

1. Barbut, F., Mastrantonio, P., Delmee, M., Brazier, J., Kuijper, E., Poxton, I. and European Study Group on Clostridium difficile (2007) Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates. Clin Microbiol Infect 13, 1048-1057.
2. Bartlett, J.G., Chang, W., Gurwith, M., Gorbach, S.L. and Onderdonk, A.B. (1978) Antibiotic-associated pseudomembranous colitis due to toxin-producing Clostridia. N Engl J Med 298, 531-534.
3. Bidet, P., Barbut, F., Lalande, V., Burghoffer, B. and Petit, J. (1999) Development of a new PCR-ribotyping method for Clostridium difficile based on ribosomal RNA gene sequencing. FEMS Microbiol Lett 175, 261-266.
4. Chauret, C., Springthorpe, S. and Sattar, S. (1999) Fate of Cryptosporidium oocysts, Giardia cysts, and microbial indicators during wastewater treatment and anaerobic sludge digestion. Can J Microbiol 45, 257-262.
5. Cohen, M.B. (2009) Clostridium difficile infections: emerging epidemiology and new treatments. J Pediatr Gastroenterol Nutr 48, 63-65.
6. Goorhuis, A., Bakker, D., Corver, J., Debast, S.B., Harmanus, C., Notermans, D.W., Bergwerff, A.A., Dekker, F.W. et al. (2008) Emergence of Clostridium difficile Infection due to a new hypervirulent strain, Polymerase Chain Reaction Ribotype 078. Clin Infect Dis 47, 1162-1170.
7. Hall, I.C. and O'Toole, E. (1935) Intestinal flora in new-born infants: with a description of a new pathogenic anaerobe, Bacillus difficilis. Am J Dis Child 49, 390-402.
8. Hawken, P., Weese, J.S., Friendship, R. and Warriner, K. (2013) Longitudinal study of Clostridium difficile and methicillin-Resistant Staphylococcus aureus associated with pigs from weaning through to the end of processing. J Food Prot 76, 624-630.
9. Hensgens, M.P.M., Keessen, E.C., Squire, M.M., Riley, T.V., Koene, M.G.J., Boer, E.d., Lipman, L.J.A., Kuijper, E.J. and European Society of Clinical Microbiology and Infectious Diseases Study Group for Clostridium difficile (ESGCD) (2012) Clostridium difficile infection in the community: a zoonotic disease? Clin Microbiol Infect 18, 635-645.
10. Hirschhorn, L.R., Trnka, Y., Onderdonk, A., Lee, M.T. and Platt, R. (1994) Epidemiology of community-acquired Clostridium difficile-associated diarrhea. J Infect Dis 169, 127-133.
11. Kato, H., Kato, N., Watanabe, K., Iwai, N., Nakamura, H., Yamamoto, T., Suzuki, K., Kim, S. et al. (1998) Identification of toxin A-Negative, toxin B-positive Clostridium difficile by PCR. J Clin Microbiol 36, 2178-2182.
12. Kato, H., Kato, N., Katow, S., Maegawa, T., Nakamura, S. and Lyerly, D.M. (1999) Deletions in the repeating sequences of the toxin A gene of toxin A-negative, toxin B-positive Clostridium difficile strains. FEMS Microbiol Lett 175, 197-203.
13. Keel, K., Brazier, J.S., Post, K., Weese, S.J. and Songer, G. (2007) Prevalence of PCR Ribotypes among Clostridium difficile isolates from pigs, calves, and other species. Am Soc Microbiol 45, 1963-1964.
14. Kutty, P.K., Woods, C.W., Sena, A.C., Benoit, S.R., Naggie, S., Frederick, J., Evans, S., Engel, J. et al. (2010) A multicenter study of Clostridium difficile infection-related colectomy risk factors for and estimated incidence of community-associated Clostridium difficile infection, North Carolina, USA. Emerg Infect Dis 16, 197-204.
15. McDonald, L.C., Owings, M. and Jernigan, D.B. (2006) Clostridium difficile Infection in Patients Discharged from US Short-stay Hospitals, 1996-2003. Emerg Infect Dis 12, 409-415.
16. Metcalf, D., Reid-Smith, R.J., Avery, B.P. and Weese, J.S. (2010a) Prevalence of Clostridium difficile in retail pork. Can Vet J 51, 873-876.
17. Metcalf, D.S., Costa, M.C., Dew, W.M.V. and Weese, J.S. (2010b) Clostridium difficile in vegetables. Can Lett Appl Microbiol 51, 600-602.
18. Metcalf, D., Avery, B.P., Janecko, N., Matic, N., Reid-Smith, R. and Weese, J.S. (2011) Clostridium difficile in seafood and fish. Anaerobe 17, 85-86.
19. Miller, M., Gravel, D., Mulvey, M., Taylor, G., Boyd, D., Simor, A., Gardam, M., McGeer, A. et al. (2010) Health care-associated Clostridium difficile infection in Canada: patient age and infecting strain type are highly predictive of severe outcome and mortality. Clin Infect Dis 90, 194-201.
20. Mulvey, M.R., Boyd, D.A., Gravel, D., Hutchinson, J., Kelly, S., McGeer, A., Moore, D., Simor, A. et al. (2010) Hypervirulent Clostridium difficile Strains in hospitalized patients, Canada. Emerg Infect Dis 16, 678-681.
21. Musher, D.M., Aslam, S., Logan, N., Nallacheru, S., Bhaila, I., Borchert, F. and Hamill, R.J. (2005) Relatively poor outcome after treatment of Clostridium difficile colitis with metronidazole. Clin Infect Dis 40, 1586-1590.
22. Norén, T., Åkerlund, T., Bäck, E., Sjöberg, L., Persson, I., Alriksson, I. and Burman, L.G. (2004) Molecular epidemiology of hospital-associated and community-acquired Clostridium difficile infection in a Swedish County. J Clin Microbiol 42, 3635-3643.
23. Otten, A.M., Reid-Smith, R.J., Fazil, A. and Weese, J.S. (2010) Disease transmission model for community-associated Clostridium difficile infection. Epidemiol Infect 138, 907-914.
24. Payment, P., Plante, R. and Cejka, P. (2001) Removal of indicator bacteria, human enteric viruses, Giardia cysts, and Cryptosporidium oocysts at a large wastewater primary treatment facility. Can J Microbiol 47, 188-193.
25. Pépin, J., Valiquette, L., Alary, M., Villemure, P., Pelletier, A., Forget, K., Pépin, K. and Chouinard, D. (2004) Clostridium difficile-associated diarrhea in a region of Quebec from 1991 to 2003: a changing pattern of disease severity. CMAJ 171, 466-472.
26. Plummer, S., Weaver, M.A., Harris, J.C., Dee, P. and Hunter, J. (2010) Clostridium difficile pilot study: effects of probiotic supplementation on the incidence of C. difficile diarrhoea. Int Microbiol 7, 59-62.
27. Redelings, M.D., Sorvillo, F. and Mascola, L. (2007) Increase in Clostridium difficile-related mortality rates, United States, 1999-2004. Emerg Infect Dis 13, 1417-1419.
28. Ricciardi, R., Rothenberger, D.A., Madoff, R.D. and Baxter, N.N. (2007) Increasing prevalence and severity of Clostridium difficile colitis in hospitalized patients in the United States. Am Med Assoc 142, 624-631.
29. Rodriguez-Palacios, A., Staempfli, H.R., Duffield, T. and Weese, J.S. (2007) Clostridium difficile in retail ground meat, Canada. Emerg Infect Dis 13, 485-487.
30. Rodriguez-Palacios, A., Reid-Smith, R.J., Staempfli, H.R., Daignault, D., Janecko, N., Avery, B.P., Martin, H., Thomspon, A.D. et al. (2009) Possible seasonality of Clostridium difficile in retail meat, Canada. Emerg Infect Dis 15, 802-805.
31. Romano, V., Pasquale, V., Krovacek, K., Mauri, F., Demarta, A. and Dumontet, S. (2012) Toxigenic Clostridium difficile PCR ribotypes from wastewater treatment plants in Southern Switzerland. Appl Environ Microbiol 78, 6643-6646.
32. Rupnik, M., Avesani, V., Janc, M., Eichel-Streiber, C. and Delmée, M. (1998) A novel toxinotyping scheme and correlation of toxinotypes with serogroups of isolates Clostridium difficile. J Clin Microbiol 36, 2240-2247.
33. Salf, N.A. and Brazier, J.S. (1996) The distribution of Clostridium difficile in the environment of South Wales. J Med Microbiol 45, 133-137.
34. Simango, C. (2006) Prevalence of Clostridium difficile in the environment in a rural community in Zimbabwe. Trans R Soc Trop Med Hyg 100, 1146-1150.
35. Spigaglia, P. and Mastrantonio, P. (2002) Molecular analysis of the pathogenicity locus and polymorphism in the putative negative regulator of toxin production (TcdC) among Clostridium difficile clinical isolates. J Clin Microbiol 40, 3470-3475.
36. Stubbs, S., Rupnik, M., Gibert, M., Brazier, J., Duerden, B. and Popoff, M. (2000) Production of actin-specific ADP-ribosyltransferase (binary toxin) by strains of Clostridium difficile. FEMS Microbiol Lett 186, 307-312.
37. Weese, J.S., Avery, B.P., Rousseau, J. and Reid-Smith, R.J. (2009) Detection and enumeration of Clostridium difficile Spores in retail beef and pork. Appl Environ Microbiol 75, 5009-5011.
38. Weese, J.S., Reid-Smith, R.J., Avery, B.P. and Rousseau, J. (2010c) Detection and characterization of Clostridium difficile in retail chicken. Lett Appl Microbiol 50, 362-365.
39. Weese, J.S., Rousseau, J., Deckert, A., Gow, S. and Reid-Smith, R. (2011) Clostridium difficile and methicillin-resistant Staphylococcus aureus shedding by slaughter-age pigs. BMC Vet Res 7, 1-7.
40. Zidaric, V., Beigot, S., Lapajne, S. and Rupnik, M. (2010) The occurrence and high diversity of Clostridium difficile genotypes in rivers. Anaerobe 16, 371-375.