Salmonella serotype diversity and seasonality in urban and rural streams

Journal of Applied Microbiology

Volumn 114, Issue 3, 2013, Pages 907-922

  Thomas, J L ^a,b   Slawson, R M ^b   Taylor, W D ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b WILFRID LAURIER UNIVERSITY   (Canada)

Author keywords

Diversity; Microbial contamination; Pulsed field gel electrophoresis; Salmonella; Water quality

Indexed keywords

ELECTROPHORESIS; RESERVOIRS (WATER); RIVER POLLUTION; RIVERS; RURAL AREAS; SALMONELLA; WATERSHEDS;

AGRICULTURAL STREAMS; DIVERSITY; GENETICS DIVERSITIES; HEALTH SIGNIFICANCES; HEIDELBERG; MICROBIAL CONTAMINATION; PULSED FIELD GEL ELECTROPHORESIS; SEASONALITY; SEROTYPES; URBAN AND RURAL;

WATER QUALITY;

BACTERIUM; DISEASE TRANSMISSION; ELECTROKINESIS; GENETIC VARIATION; LABORATORY METHOD; LOW TEMPERATURE; MICROBIAL COMMUNITY; PATHOGEN; PUBLIC HEALTH; RURAL AREA; SEASONALITY; STREAM; URBAN AREA; WATER QUALITY; WATERSHED;

ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; GENETIC VARIABILITY; LOW TEMPERATURE; MICROBIAL DIVERSITY; NONHUMAN; PREVALENCE; RURAL AREA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA HEIDELBERG; SALMONELLA TYPHIMURIUM; SEASONAL VARIATION; SEROTYPE; STREAM (RIVER); URBAN AREA; WATERSHED;

CANADA; GRAND RIVER [ONTARIO]; ONTARIO [CANADA];

ANIMALIA; BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR HEIDELBERG; SALMONELLA TYPHIMURIUM DT104;

EID: 84873989763     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12079     Document Type: Article

References (57)

1. American Public Health Association (APHA), American Water Works Association (AWWA) and Water Environment Federation (WeF) (2005) Standard Methods for the Examination of Water and Wastewater, 21st edn. Washington, DC: United Book Press Inc.
2. Arvanitidou, M., Kanellou, K. and Vagiona, D.G. (2005) Diversity of Salmonella spp. and fungi in northern Greek rivers and their correlation to fecal pollution indicators. Environ Res 99, 278-284.
3. Baggesen, D.L., Sandvang, D. and Aarestrup, F.M. (2000) Characterization of Salmonella enterica serovar Typhimurium DT104 isolated from Denmark and comparison with isolates from Europe and the United States. J Clin Microbiol 38, 1581-1586.
4. Baudart, J., Lemarchand, K., Brisabois, A. and Lebaron, P. (2000) Diversity of Salmonella strains isolated from the aquatic environment as determined by serotyping and amplification of the ribosomal DNA spacer regions. Appl Environ Microbiol 66, 1544-1552.
5. Branham, L.A., Carr, M.A., Scott, C.B. and Callaway, T.R. (2005) E. coli O157 and Salmonella spp. in white-tailed deer and livestock. Curr Issues Intest Microbiol 6, 25-29.
6. Byappanahalli, M.N., Shively, D.A., Nevers, M.B., Sadowsky, M.J. and Whitman, R.L. (2003) Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiol Ecol 46, 203-211.
7. Carter, M.E. and Quinn, P.J. (2000) Salmonella infections in dogs and cats. In Salmonella in Domestic Animals ed. Wray, C. and Wray, A. pp. 231-244. New York: CABI Publishing.
8. Catalao Dionisio, L.P., Joao, M., Soares Ferreiro, V., Leonor Fidalgo, M., Esther Garcia Rosado, M. and Borrego, J.J. (2000) Occurrence of Salmonella spp in estuarine and coastal waters of Portugal. Antonie Van Leeuwenhoek 78, 99-106.
9. Centers for Disease Control and Prevention (CDC) (2007) Salmonella Surveillance: Annual Summary, 2005. Atlanta, Georgia: US Department of Health and Human Services.
10. Centers for Disease Control and Prevention (CDC) (2009a) Surveillance for foodborne disease outbreaks - United States, 2006. MMWR Morb Mortal Wkly Rep 58, 609-615.
11. Centers for Disease Control and Prevention (CDC) (2009b) One-Day (24-28 h) Standardized Laboratory Protocol for Molecular Subtyping of Escherichia coli O157:H7, Salmonella serotypes, and Shigella sonnei by Pulsed Field Gel Electrophoresis (PFGE). PulseNet USA PFGE Manual. Atlanta, GA: US Department of Health and Human Services.
12. Centers for Disease Control and Prevention (CDC) (2011) Surveillance for waterborne disease outbreaks associated with drinking water - United States, 2007-2008. Morb Mortal Wkly Rep 60, 38-75.
13. Chambers, D.L. and Hulse, A.C. (2006) Salmonella serovars in the Herpetofauna of Indiana County, Pennsylvania. Appl Environ Microbiol 72, 3771-3773.
14. Cooke, F.J., Brown, D.J., Fookes, M., Pickard, D., Ivens, A., Wain, J., Roberts, M., Kingsley, R.A. et al. (2008) Characterization of the genomes of a diverse collection of Salmonella enterica serovar Typhimurium definitive Phage Type 104. J Bacteriol 190, 8155-8162.
15. Denno, D.M., Keene, W.E., Hutter, C.M., Koepsell, J.K., Patnode, M., Flodin-Hursh, D., Stewart, L.K., Duchin, J.S. et al. (2009) Tri-county comprehensive assessment of risk factors for sporadic reportable bacterial enteric infection in children. J Infect Dis 199, 467-476.
16. Dolejska, M., Bierosova, B., Kohoutova, L., Literak, I. and Cizek, A. (2009) Antibiotic-resistant Salmonella and Escherichia coli isolates with integrons and extended-spectrum beta-lactamases in surface water and sympatric black-headed gulls. J Appl Microbiol 106, 1941-1950.
17. Dorner, S.M., Huck, P.M., Slawson, R.M., Gaulin, T. and Anderson, W.B. (2004) Assessing levels of pathogenic contamination in a heavily impacted river used as a drinking-water source. J Toxicol Environ Health A 67, 1813-1823.
18. Dorner, S.M., Anderson, W.B., Gaulin, T., Candon, H.L., Slawson, R.M., Payment, P. and Huck, P.M. (2007) Pathogen and indicator variability in a heavily impacted watershed. J Water Health 5, 241-257.
19. Edge, T.A., El-Shaarawi, A., Gannon, V., Jokinen, C., Kent, R., Khan, I.U.H., Koning, W., Lapen, D. et al. (2012) Investigation of an Escherichia coli environmental benchmark for waterborne pathogens in agricultural watersheds in Canada. J Environ Qual 41, 21-30.
20. Ford, M.W., Odoi, A., Majowicz, S.E., Michel, P., Middleton, D., Ciebin, B., Doré, K., McEwen, S.A. et al. (2003) A descriptive study of human Salmonella serotype Typhimurium infections reported in Ontario from 1990 to 1997. Can J Infect Dis 14, 267-273.
21. Frech, G., Kehrenberg, C. and Schwarz, S. (2003) Resistance phenotypes and genotypes of multiresistant Salmonella enterica subsp. enterica serovar Typhimurium var. Copenhagen isolates from animal sources. J Antimicrob Chemother 51, 180-182.
22. Gannon, V.P.J., Graham, T.A., Read, S., Ziebell, K., Muckle, A., Mori, J., Thomas, J., Selinger, B. et al. (2004) Bacterial pathogens in rural water supplies in southern Alberta, Canada. J Toxicol Environ Health A 67, 1643-1653.
23. Gorski, L., Parker, C.T., Liang, A., Cooley, M.B., Jay-Russell, M.T., Gordus, A.G., Atwill, E.R. and Mandrell, R.E. (2011) Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl Environ Microbiol 77, 2734-2748.
24. Government of Canada (2005) Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS), 2003. Guelph, ON: Public Health Agency of Canada.
25. Government of Canada (2006) Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS), 2004. Guelph, ON: Public Health Agency of Canada.
26. Government of Canada (2007) Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS), 2005. Guelph, ON: Public Health Agency of Canada.
27. Grand River Conservation Authority (GRCA) (2010) The Grand. A Watershed Report. Available at: www.grandriver.ca [Accessed 2 December 2010].
28. Guerin, M.T., Martin, S.W., Darlington, G.A. and Rajic, A. (2005) A temporal study of Salmonella serovars in animals in Alberta between 1990 and 2001. Can J Vet Res 69, 88-99.
29. Guerri, M.L., Aladuena, A., Echeita, A. and Rotger, R. (2004) Detection of integrons and antibiotic-resistance genes in Salmonella enterica serovar Typhimurium isolates with resistance to ampicillin and variable susceptibility to amoxicillin-clavulanate. Int J Antimicrob Agents 24, 327-333.
30. Haley, B.J., Cole, D.J. and Lipp, E.K. (2009) Distribution, diversity, and seasonality of waterborne salmonellae in a rural watershed. Appl Environ Microbiol 75, 1248-1255.
31. Hall, A.J. and Saito, E.K. (2008) Avian wildlife mortality events due to salmonellosis in the United States, 1985-2004. J Wildl Dis 44, 585-593.
32. Health Canada (2003) Canadian Integrated Surveillance Report: Salmonella, Campylobacter, pathogenic E. coli and Shigella, from 1996-1999. Canada Communicable Disease Report. Vol. 2951. March 2003.
33. Johnson, D.C., Enriquez, C.E., Pepper, I.L., Davis, T.L., Gerba, C.P. and Rose, J.B. (1997) Survival of Giardia, Cryptosporidium, Poliovirus, and Salmonella in Marine Waters. Water Sci Technol 35, 261-268.
34. Johnson, J.Y.M., Thomas, J.E., Graham, T.A., Townshend, I., Byrne, J., Selinger, L.B. and Gannon, V.P.J. (2003) Prevalence of Escherichia coli O157:H7 and Salmonella spp. in surface waters of southern Alberta and its relation to manure sources. Can J Microbiol 49, 326-335.
35. Kon, T., Weir, S., Howell, E.T., Lee, H. and Tervors, J.T. (2007) Genetic relatedness of Escherichia coli Isolates in interstitial water from a Lake Huron (Canada) beach. Appl Environ Microbiol 73, 1961-1967.
36. Martinez-Urtaza, J., Liebana, E., Garcia-Migura, L., Perez-Pineiro, P. and Saco, M. (2004a) Characterization of Salmonella enterica serovar Typhimurium from marine environments in coastal waters of Galicia (Spain). Appl Environ Microbiol 70, 4030-4034.
37. Martinez-Urtaza, J., Saco, M., de Novoa, J., Perez-Pineiro, P., Peiteado, J., Lozano-Leon, A. and Garcia-Martin, O. (2004b) Influence of environmental factors and human activity on the presence of Salmonella serovars in a marine environment. Appl Environ Microbiol 70, 2089-2097.
38. Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V. (1999) Food-related illness and death in the United States. Emerg Infect Dis 5, 607-625.
39. Nesse, L.L., Refsum, T., Heir, E., Nordby, K. and Vardund, T. (2005) Molecular epidemiology of Salmonella spp. isolated from gulls, fish-meal factories, feed factories, animals and humans in Norway based on pulsed field gel electrophoresis. Epidemiol Infect 133, 53-58.
40. Patchanee, P., Molla, B., White, N., Line, D.E. and Gebreyes, W.A. (2010) Tracking Salmonella contamination in various watersheds and phenotypic and genotypic diversity. Foodborne Pathog Dis 7, 1113-1120.
41. Polo, F., Figueras, M., Inza, I., Sala, J., Fleisher, J. and Guarro, J. (1999) Prevalence of Salmonella serotypes in environmental waters and their relationships with indicator organisms. Antonie Van Leeuwenhoek 75, 285-292.
42. Public Health Agency of Canada (PHAC) (2007a) National Integrated Enteric Pathogen Surveillance Program (C-EnterNet) Annual Report, 2005-2006. ON: Guelph.
43. Public Health Agency of Canada (PHAC) (2007b) National Integrated Enteric Pathogen Surveillance Program (C-EnterNet) Annual Report, 2006. ON: Guelph.
44. Public Health Agency of Canada (PHAC) (2007c) Laboratory Surveillance Data for Enteric Pathogens in Canada. Annual Summary 2006. Winnipeg, Manitoba, Canada: Ministry of Public Works and Government Services, National Microbiology Laboratory.
45. Ribot, E., Fair, M., Gautom, R., Cameron, D., Hunter, S., Swaminathan, B. and Barrett, T. (2006) Standardization of pulsed-field gel electrophoresis protocols for subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 3, 59-67.
46. Setti, I., Rodriguez-Castro, A., Pata, M.P., Cadarso-Suarez, C., Yacoubi, B., Bensmael, L., Moukrim, A. and Martinez-Urtaza, J. (2009) Characteristics and dynamics of Salmonella contamination along the coast of Agadir, Morocco. Appl Environ Microbiol 75, 7700-7709.
47. Simental, L. and Martinez-Urtaza, J. (2008) Climate patterns governing the presence and permanence of Salmonellae in coastal areas of Bahia de Todos Santos, Mexico. Appl Environ Microbiol 74, 5918-5924.
48. Thomas, M.K., Majowicz, S.E., Sockett, P.N., Fazil, A., Pollari, F., Doré, K., Flint, J.A. and Edge, V.A. (2006) Estimated numbers of community cases of illness due to Salmonella, Campylobacter and verotoxigenic Escherichia coli: pathogen specific community rates. Can J Infect Dis Med Microbiol 17, 229-234.
49. United States Environmental Protection Agency (USEPA) (2009a) Review of Published Studies to Characterize Relative Risk from Different Sources of Fecal Contamination in Recreational Water. EPA 822-R-09-001. Washington, DC: Health and Ecological Criteria Division, Office of Water.
50. United States Environmental Protection Agency (USEPA) (2009b) Drinking Water Contaminant Candidate List 3 - final. EPA-HQ-OW-2007-1189 FRL-8963-6. Final Regist 74, 51850-51860.
51. United States Environmental Protection Agency (USEPA) (2009c) Review of Zoonotic Pathogens in Ambient Waters. EPA 822-R-09-002. Washington, DC: Health and Ecological Criteria Division, Office of Water.
52. Voetsch, A.C., Van Gilder, T.J., Angulo, F.J., Farley, M.M., Shallow, S., Marcus, R., Cieslak, P.R., Deneen, V.C. et al. (2004) FoodNet estimate of the burden of illness caused by non-typhoidal Salmonella infections in the United States. Clin Infect Dis 38, S127-S134.
53. Whitman, R.L. and Nevers, M.B. (2003) Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Appl Environ Microbiol 69, 5555-5562.
54. Wilkes, G., Edge, T., Gannon, V., Jokinen, C., Lyautey, E., Medeiros, D., Neumann, N., Ruecker, N. et al. (2009) Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Res 43, 2209-2223.
55. Winfield, M.D. and Groisman, E.A. (2003) Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl Environ Microbiol 69, 3687-3694.
56. Wright, R. (1989) The survival patterns of selected faecal bacteria in tropical fresh waters. Epidemiol Infect 103, 603-611.
57. Zhao, S., Fedorka-Cray, P.J., Frienman, S., McDermott, P.F., Walker, R.D., Qaiyumi, S., Foley, S.L., Hubert, S.K. et al. (2005) Characterization of Salmonella Typhimurium of animal origin obtained from the national antimicrobial resistance monitoring system. Foodborne Pathog Dis 2, 169-181.