Persistence of Escherichia coli O157 and non-O157 strains in agricultural soils

Science of the Total Environment

Volumn 490, Issue , 2014, Pages 822-829

  Ma, Jincai ^a,b   Mark Ibekwe, A ^a   Crowley, David E ^b   Yang, Ching Hong ^c  

^a U S SALINITY LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

Contamination; Escherichia coli O157 and non O157; Fresh produce; Persistence; Preharvest; Soil

Indexed keywords

AGRICULTURE; CONTAMINATION; DATA PROCESSING; SOILS; STRAIN;

ENVIRONMENTAL FACTORS; ESCHERICHIA COLI O157; FRESH PRODUCE; NON-O157 SEROGROUPS; PEARSON CORRELATION ANALYSIS; PERSISTENCE; PREHARVEST; SHIGA TOXIN-PRODUCING ESCHERICHIA COLI;

ESCHERICHIA COLI;

NALIDIXIC ACID; RIFAMPICIN; SOIL;

BACTERIUM; ENVIRONMENTAL FACTOR; SOIL POLLUTION; SOIL QUALITY; SURVIVAL; TOXIN;

AGRICULTURAL LAND; AGRICULTURAL MANAGEMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM CONTAMINATION; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ESCHERICHIA COLI O157; MICROBIAL ACTIVITY; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; SOIL ANALYSIS; SOIL PROPERTY; STRAIN DIFFERENCE; SURVIVAL TIME; UNITED STATES; AGRICULTURE; CLASSIFICATION; ESCHERICHIA COLI; GROWTH, DEVELOPMENT AND AGING; MICROBIOLOGY; SOIL;

ARIZONA; CALIFORNIA; UNITED STATES;

AGRICULTURE; ARIZONA; ESCHERICHIA COLI; ESCHERICHIA COLI O157; SOIL; SOIL MICROBIOLOGY;

EID: 84901834506     PISSN: 00489697     EISSN: 18791026     Source Type: Journal    
DOI: 10.1016/j.scitotenv.2014.05.069     Document Type: Article

References (52)

1. Berger C.N., Sodha S.V., Shaw R.K., Griffin P.M., Pink D., Hand P., et al. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ Microbiol 2010, 12:2385-2397.
2. Besser R.E., Griffin P.M., Slutsker L. Escherichia coli O157:H7 gastroenteritis and the hemolytic uremic syndrome: an emerging infectious disease. Annu Rev Med 1999, 50:355-367.
3. Bettelheim K.A. The non-O157 shiga-toxigenic (verocytotoxigenic) Escherichia coli; under-rated pathogens. Crit Rev Microbiol 2007, 33:67-87.
4. Beutin L., Martin A. Outbreak of Shiga toxin-producing Escherichia coli (STEC) O104:H4 infection in Germany causes a paradigm shift with regard to human pathogenicity of STEC strains. J Food Prot 2012, 75:408-418.
5. Bolton D.J., Byrne C.M., Sheridan J.J., McDowell D.A., Blair I.S. The survival characteristics of a non-toxigenic strain of Escherichia coli O157: H7. J Appl Microbiol 1999, 86:407-411.
6. Bolton D.J., Monaghan A., Byrne B., Fanning S., Sweeney T., McDowell D.A. Incidence and survival of non-O157 verocytotoxigenic Escherichia coli in soil. J Appl Microbiol 2011, 111:484-490.
7. Brandl M.T. Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl Environ Microbiol 2008, 74:5285-5289.
8. Brooks J.T., Sowers E.G., Wells J.G., Greene K.D., Griffin P.M., Hoekstra R.M., et al. Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983-2002. J Infect Dis 2005, 192:1422-1429.
9. Caprioli A., Morabito S., Brugere H., Oswald E. Enterohaemorrhagic Escherichia coli: emerging issues on virulence and modes of transmission. Vet Res 2005, 36:289-311.
10. CDC Investigation update: multistate outbreak of human E. coli O145 infections linked to shredded romaine lettuce from a single processing facility. 2012 2010, CDC.
11. Chase-Topping M., Gally D., Low C., Matthews L., Woolhouse M. Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat Rev Microbiol 2008, 6:904-912.
12. Cooley M., Carychao D., Crawford-Miksza L., Jay M.T., Myers C., Rose C., et al. Incidence and tracking of Escherichia coli O157:H7 in a major produce production region in California. PLoS One 2007, 2:e1159.
13. Erikson M.C., Habteselassie M.Y., Liao J., Webb C.C., Mantripragada V., Davey L.E., et al. Examination of factors for use as potential predictors of humen enteric pathogen survival in soil. J Appl Microbiol 2013, 116:335-349.
14. Feng P., Dey M., Abe A., Takeda T. Isogenic strain of Escherichia coli O157:H7 that has lost both Shiga toxin 1 and 2 genes. Clin Diagn Lab Immunol 2001, 8:711-717.
15. Fey P.D., Wickert R.S., Rupp M.E., Safranek T.J., Hinrichs S.H. Prevalence of non-O157: H7 shiga toxin-producing Escherichia coli in diarrheal stool samples from Nebraska. Emerg Infect Dis 2000, 6:530-533.
16. Fields P.I., Blom K., Hughes H.J., Helsel L.O., Feng P., Swaminathan B. Molecular characterization of the gene encoding H antigen in Escherichia coli and development of a PCR-restriction fragment length polymorphism test for identification of E. coli O157:H7 and O157:NM. J Clin Microbiol 1997, 35:1066-1070.
17. Franz E., Semenov A.V., Termorshuizen A.J., de Vos O.J., Bokhorst J.G., van Bruggen A.H.C. Manure-amended soil characteristics affecting the survival of E. coli O157: H7 in 36 Dutch soils. Environ Microbiol 2008, 10:313-327.
18. Franz E., van Hoek A.H.A.M., Bouw E., Aarts H.J.M. Variability of Escherichia coli O157 strain survival in manure-amended soil in relation to strain origin, virulence profile, and carbon nutrition profile. Appl Environ Microbiol 2011, 77:8088-8096.
19. Fremaux B., Prigent-Combaret C., Delignette-Muller M.L., Mallen B., Dothal M., Gleizal A., et al. Persistence of Shiga toxin-producing Escherichia coli O26 in various manure-amended soil types. J Appl Microbiol 2008, 104:296-304.
20. Geeraerd A.H., Valdramidis V.P., Van Impe J.F. GInaFiT, a freeware tool to assess non-log-linear microbial survivor curves. Int J Food Microbiol 2005, 102:95-105.
21. Ibekwe A.M., Ma J. Effects of fumigants on microbial diversity and persistence of E. coli O15:H7 in contrasting soil microcosms. Sci Total Environ 2011, 409:3740-3748.
22. Ibekwe A.M., Grieve C.M., Yang C.H. Survival of Escherichia coli O157:H7 in soil and on lettuce after soil fumigation. Can J Microbiol 2007, 53:623-635.
23. Ito H., Terai A., Kurazono H., Takeda Y., Nishibuchi M. Cloning and nucleotide sequencing of Vero toxin 2 variant genes from Escherichia coli O91:H21 isolated from a patient with the hemolytic uremic syndrome. Microb Pathog 1990, 8:47-60.
24. Jiang X.P., Morgan J., Doyle M.P. Fate of Escherichia coli O157: H7 in manure-amended soil. Appl Environ Microbiol 2002, 68:2605-2609.
25. Johnson R.P., Clarke R.C., Wilson J.B., Read S.C., Rahn K., Renwick S.A., et al. Growing concerns and recent outbreaks involving non-O157:H7 serotypes of verotoxigenic Escherichia coli. J Food Prot 1996, 59:1112-1122.
26. Johnson K.E., Thorpe C.M., Sears C.L. The emerging clinical importance of non-O157 Shiga toxin - producing Escherichia coli. Clin Infect Dis 2006, 43:1587-1595.
27. Jones N.L., Day A.S., Jennings H.A., Sherman P.M. Helicobacter pylori induces gastric epithelial cell apoptosis in association with increased Fas receptor expression. Infect Immun 1999, 67:4237-4242.
28. Kaper J.B., Nataro J.P., Mobley H.L. Pathogenic Escherichia coli. Nat Rev Microbiol 2004, 2:123-140.
29. Kappeli U., Hachler H., Giezendanner N., Beutin L., Stephan R. Human infections with non-O157 Shiga toxin-producing Escherichia coli, Switzerland, 2000-2009. Emerg Infect Dis 2011, 17:180-185.
30. Karch H., Tarr P.I., Bielaszewska M. Enterohaemorrhagic Escherichia coli in human medicine. Int J Med Microbiol 2005, 295:405-418.
31. Klute A. Methods of soil analysis. Part 1: physical and mineralogical methods 9(1) 1996, American Society of Agronomy.
32. Kolter R., Siegele D.A., Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol 1993, 47:855-874.
33. Laing C.R., Zhang Y., Gilmour M.W., Allen V., Johnson R., Thomas J.E., et al. A comparison of Shiga-toxin 2 bacteriophage from classical enterohemorrhagic Escherichia coli serotypes and the German E. coli O104:H4 outbreak strain. PLoS One 2012, 7:e37362.
34. Louie M., Read S., Simor A.E., Holland J., Louie L., Ziebell K., et al. Application of multiplex PCR for detection of non-O157 verocytotoxin-producing Escherichia coli in bloody stools: identification of serogroups O26 and O111. J Clin Microbiol 1998, 36:3375-3377.
35. Lynch M.F., Tauxe R.V., Hedberg C.W. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol Infect 2009, 137:307-315.
36. Ma J., Ibekwe A.M., Yi X., Wang H., Yamazaki A., Crowley D.E., et al. Persistence of Escherichia coli O157:H7 and its mutants in soils. PLoS One 2011, 6:e23191.
37. Ma J., Ibekwe A.M., Crowley D.E., Yang C.H. Persistence of Escherichia coli O157:H7 in major leafy green producing soils. Environ Sci Technol 2012, 46:12154-12161.
38. Ma J., Ibekwe A.M., Wang H., Xu J., Leddy M., Yang C.H., et al. Assimilable organic carbon (AOC) in soil water extracts using Vibrio harveyi BB721 and its implication for microbial biomass. PLoS One 2012, 7:e28519.
39. Ma J., Ibekwe A.M., Yang C.H., Crowley D.E. Influence of bacterial communities based on 454-pyrosequencing on the survival of Escherichia coli O157:H7 in soils. FEMS Microbiol Ecol 2013, 84:542-554.
40. Mafart P., Couvert O., Gaillard S., Leguerinel I. On calculating sterility in thermal preservation methods: application of the Weibull frequency distribution model. Int J Food Microbiol 2002, 72:107-113.
41. Mathusa E.C., Chen Y., Enache E., Hontz L. Non-O157 Shiga toxin-producing Escherichia coli in foods. J Food Prot 2010, 73:1721-1736.
42. Paton J.C., Paton A.W. Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 1998, 11:450-479.
43. Perna N.T., Plunkett G., Burland V., Mau B., Glasner J.D., Rose D.J., et al. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 2001, 409:529-533.
44. Ribot E.M., Fair M.A., Gautom R., Cameron D.N., Hunter S.B., Swaminathan B., et al. Standardization of pulsed-field gel electrophoresis protocols for the subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog Dis 2006, 3:59-67.
45. Semenov A.V., van Bruggen A.H.C., van Overbeek L., Termorshuizen A.J., Semenov A.M. Influence of temperature fluctuations on Escherichia coli O157: H7 and Salmonella enterica serovar Typhimurium in cow manure. FEMS Microbiol Ecol 2007, 60:419-428.
46. Semenov A.V., Franz E., van Overbeek L., Termorshuizen A.J., van Bruggen A.H.C. Estimating the stability of Escherichia coli O157: H7 survival in manure-amended soils with different management histories. Environ Microbiol 2008, 10:1450-1459.
47. Solomon E.B., Potenski C.J., Matthews K.R. Effect of irrigation method on transmission to and persistence of Escherichia coli O157: H7 on lettuce. J Food Prot 2002, 65:673-676.
48. Tyler H.L., Triplett E.W. Plants as a habitat for beneficial and/or human pathogenic bacteria. Annu Rev Phytopathol 2008, 46:53-73.
49. Unc A., Gardner J., Springthorpe S. Recovery of Escherichia coli from soil after addition of sterile organic wastes. Appl Environ Microbiol 2006, 72:2287-2289.
50. van Elsas J.D., Semenov A.V., Costa R., Trevors J.T. Survival of Escherichia coli in the environment: fundamental and public health aspects. ISME J 2011, 5:173-183.
51. Vance E.D., Brookes P.C., Jenkinson D.S. An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 1987, 19:703-707.
52. Vital M., Stucki D., Egli T., Hammes F. Evaluating the growth potential of pathogenic bacteria in water. Appl Environ Microbiol 2010, 76:6477-6484.