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Applied and Environmental Microbiology, December 2008, p. 7447-7450, Vol. 74, No. 23
0099-2240/08/$08.00+0     doi:10.1128/AEM.01190-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

International Comparison of Clinical, Bovine, and Environmental Escherichia coli O157 Isolates on the Basis of Shiga Toxin-Encoding Bacteriophage Insertion Site Genotypes{triangledown}

Joshua H. Whitworth,1 Narelle Fegan,2 Jasmin Keller,2 Kari S. Gobius,2 James L. Bono,3 Douglas R. Call,1 Dale D. Hancock,4 and Thomas E. Besser1*

Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, Washington 99164-7040,1 Department of Veterinary Clinical Sciences, College of Veterinary Medicine, Washington State University, Pullman, Washington 99164-6610,4 Microbiology Group, Food Science Australia, P.O. Box 3312, Tingalpa DC, Queensland 4173, Australia,2 U.S. Meat Animal Research Center, Agricultural Research Service, U.S. Department of Agriculture, Clay Center, Nebraska 68933-01663

Received 28 May 2008/ Accepted 30 September 2008


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ABSTRACT
 
Escherichia coli O157:H7 genotypes in the bovine reservoir may differ in virulence. The proportion of clinical genotypes among cattle isolates was weakly (P = 0.054) related to the international incidence of E. coli O157:H7-associated hemolytic-uremic syndrome, varied among clinical isolates internationally, and also differed along the putative cattle-hamburger-clinical case transmission chain.


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INTRODUCTION
 
Infection with enterohemorrhagic Escherichia coli serotypes O157:H7 and O157:H– (EHEC-O157) may cause diarrhea, hemorrhagic colitis, and hemolytic uremic syndrome (HUS) (13, 24). Cattle are considered the principal reservoir of EHEC (18). EHEC-O157 typically produces Shiga toxins Stx1 and/or Stx2, encoded by lambdoid bacteriophages (23, 28, 34). In EHEC-O157 strains EDL933 and Sakai, Stx-encoding phages are inserted in yehV and wrbA (19, 40). Shaikh and Tarr (44), however, demonstrated insertion site diversity in Stx-encoding bacteriophages among clinical EHEC-O157 isolates, defining three predominant clinical genotypes (genotypes 1 to 3). Subsequently, the predominance of genotypes 1 to 3 among a larger set of U.S. human clinical isolates was confirmed; in contrast, considerable additional diversity of Stx-encoding bacteriophage insertion sites was demonstrated in isolates from the bovine reservoir (6). Since nonclinical genotypes represented almost half of the bovine isolates, broad exposure of the human population to these genotypes would be expected.

The frequency of reported EHEC-O157-associated disease varies markedly internationally. For example, the incidence of EHEC-O157 (infections/100,000 population annually) was reported as 4.1 (Scotland, 2004), 0.9 (United States, 2004), 0.87 (Japan, 2004), 0.13 and 1.6 (Germany, 2004 and 1997 to 2003, respectively), 0.11 (Republic of Korea, 2003), and 0.08 (Australia, 2004) (2, 9, 14, 15, 27, 31, 38). HUS, an uncommon sequel to EHEC-O157 infection, may be less under-reported due to its severity (32). The corresponding incidence of EHEC-O157-associated HUS was 0.41 (Scotland), 0.1 (United States), 0.002 to 0.20 (Germany), 0.05 (Republic of Korea), and 0.01 (Japan and Australia) (1, 2, 10, 14, 15, 20, 37).

To determine whether the proportion of EHEC-O157 genotypes in the bovine reservoirs influences the rates of the diverse international incidence of EHEC-O157 disease, we genotyped EHEC-O157 isolates obtained from cattle in several countries. Study isolates included non-sorbitol-fermenting, β-glucuronidase-negative EHEC-O157 isolates from cattle originating from different farms in geographically disseminated locations within the United States (1994 to 2002), Australia (1993 to 2003), Japan (1996 to 1997; provided by Masato Akiba, National Institute of Animal Health, Tsukuba, Ibaraki, Japan), Scotland (1999; provided by Barti Synge, Scottish Agricultural College, Inverness, United Kingdom), and Korea (1997; provided by B. Young).

Genotypes of EHEC-O157 isolates were determined by using a multiplexed variation of a PCR method previously described (6, 44). Multiplex 1 included stx1 (36), the right wrbA-bacteriophage junction, and the left yehV-bacteriophage junction. Multiplex 2 included stx2 (39), the left wrbA-bacteriophage junction, and the right yehV-bacteriophage junction. EHEC-O157 cells were grown overnight at 37°C in LB broth with shaking and diluted 1:10 with water for use as a whole-cell template. The 50-µl reaction mixtures included 2.5 U/µl Taq polymerase, 2 mM MgCl2, 0.4 mM deoxynucleoside triphosphates, 5 µl 10x buffer (Invitrogen, Carlsbad, CA), and 2 µl of the whole-cell template. Thermocycler (iCycler; Bio-Rad, Hercules, CA) parameters included one 95°C (5 min) cycle and 35 cycles at 94°C (30 s), 58°C (45 s), and 72°C (90 s), followed by a final 72°C (10 min) cycle. The assignment of genotypes was based on the presence or absence of the six PCR products (6). Controls included E. coli DH5{alpha} (negative control) and EDL933 (positive control).

No significant association was observed between the proportion of clinical genotypes among isolates from the international bovine reservoirs and the respective international incidences of EHEC-O157 disease (rs [Spearman's rho statistic] = 0.50, P = 0.39) (Table 1). In contrast, the correlation between the proportion of clinical genotypes in the bovine reservoirs and the respective international incidences of HUS approached statistical significance (rs = 0.87, P = 0.054). Isolates from Scottish cattle had the highest proportion of clinical genotypes 1 to 3 (56%) (Fig. 1), but the relative numbers of clinical genotypes in cattle isolates in the United States (38%), Korea (45%), Australia (37%), Japan (36%), and Scotland did not differ ({chi}2 = 5.1; 4 df; P = 0.28). Therefore, the effect of EHEC-O157 genotypes would appear to be limited to, at most, the more-severe disease manifestation of HUS. Even for HUS, the observed ~2-fold difference in the proportions of clinical genotypes in isolates from the bovine reservoir is far smaller than the 40-fold difference in the reported incidences of EHEC-O157-associated HUS, suggesting that other factors must account for most of the international differences. Such factors may include differences in the magnitudes of shedding of EHEC-O157 for specific genotypes or differing international prevalences of EHEC-O157 shedding by cattle. Reports of bovine prevalence vary widely, both within and between countries, in part as a result of different sampling, culture, and isolation methods used for EHEC-O157 detection (11, 12, 16, 21, 22, 30, 33, 35, 42, 43, 45). International comparisons of the prevalence of cattle infection, the magnitudes of cattle fecal shedding, and the frequency of contamination of human food and water sources using standardized methods and sampling frames, in conjunction with genotype determinations of the isolates in those sources, would be required to more accurately address the effects of the EHEC-O157 genotypes present in bovine reservoirs on the incidence of human disease.


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  		TABLE 1. Genotypes of Stx-encoding bacteriophage insertion sites from an international group of clinical, bovine, and environmental isolates of EHEC-O157


Figure 1
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  		FIG. 1. The proportion of bovine isolates with clinical genotypes (genotypes 1 to 3, unfilled bars) among isolates from cattle in the specified countries and the incidence (cases per 100,000 population, filled bars) of EHEC-O157 HUS are shown. Error bars indicate 95% confidence intervals.

Where available to us, we also analyzed clinical EHEC-O157 isolates to determine if the relative prevalences of clinical genotypes are similar internationally. Clinical isolates were obtained from the United States (2004 to 2005; Washington Department of Health), Japan (1995 to 1996; M. Akiba), Australia (1986 to 1999; R. Robins-Browne and D. Lightfoot, University of Melbourne, Parkville, Victoria, Australia), and Germany (DNA from both sorbitol-fermenting and non-sorbitol-fermenting isolates; Martina Bielaszewska, University of Münster, Münster, Germany). Since DNA from all of the sorbitol-fermenting, ß-glucuronidase-positive EHEC-O157 German isolates were negative for all Stx insertion site genotyping markers except stx2, consistent with its status as a distinct clade of EHEC-O157, the following analyses of genotypes were limited to isolates of the non-sorbitol-fermenting clade.

The proportions of clinical genotypes differed significantly among clinical isolates obtained from different countries ({chi}2 = 13.7; 3 df; P < 0.005), including 84% (United States), 76% (Germany), 60% (Japan), and 47% (Australia). With Bonferroni's correction, pairwise analyses demonstrated that the proportions of clinical genotypes among clinical isolates differed significantly between the United States and Australia only (P < 0.02).

Lastly, we compared genotypes of EHEC-O157 strate isolated from along the putative transmission chain from cattle, retail ground beef, clinically ill humans, and untreated sewage. Ground beef isolates were provided by Marcus Head, United States Department of Agriculture Food Safety and Inspection Service, Athens, Georgia. Additional isolates were obtained from untreated sewage at two municipal sewage treatment facilities in Washington State in 2006. The proportions of clinical genotypes were significantly higher among clinical isolates than from cattle or ground beef specimens (P < 0.01) (Fig. 2), but surprisingly different proportions of clinical genotypes were observed in isolates from cattle feces and from retail ground beef specimens ({chi}2 = 7.9; 1 df; P < 0.01) (Table 1 and Fig. 1 and 2), with relatively more genotype 3 isolates, and smaller amounts of genotype 5 and 6 isolates from ground beef than from cattle feces. These differences may be due to differential fitness among some genotypes, such as higher shedding levels in cattle feces, increased ability to survive processing and persist on hamburger and other food products, or other similar traits. Strain-specific differences in survival on beef or in media (3, 4, 5, 7, 41) have been reported, some in the opposite direction (4) from the tendency to explain the differences in genotypes reported here.


Figure 2
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  		FIG. 2. The proportion of clinical genotypes (genotypes 1 to 3) in human clinical isolates and isolates from retail ground beef and untreated municipal sewage in the specified countries. Error bars indicate 95% confidence intervals.

Differences in EHEC-O157 genotypes among clinical and bovine reservoir isolates have been previously reported, including those detected by Octamer Based Genomic Scanning (OBGS; lineage I versus lineage II), with the bacteriophage antiterminator allele Q933 (presence versus absence) and a polymorphism in tir (255 T versus A), and by phage typing (21/28 versus others from Scotland) (8, 17, 25, 26, 29, 31). Some of these genotypes may be correlated; for example, both Stx insertion typing and OBGS classify most Australian isolates into genotypes less associated with clinical disease (lineage II and nonclinical genotypes, respectively). The biologic basis of the differential representation of these genotypes in cattle and in human disease remains largely unexplained.

In summary, while the proportion of clinical genotypes in the bovine reservoir tended to correlate with the incidence of HUS in human populations, this tendency was too weak to provide a satisfying explanation for the magnitude of the differences in the international incidences of HUS and other EHEC-O157-related diseases. Assuming that the incidence estimates for EHEC-O157 disease are accurate, then other factors, such as the prevalence of EHEC-O157 in cattle, genotype-related differences in fecal shedding by cattle, survival in food products and environmental niches, and infectivity and virulence, as well as differences in food preparation practices and dietary composition, may contribute significantly to the differing international incidences of EHEC-O157 disease.


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ACKNOWLEDGMENTS
 
This project was funded by the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under contract number N01-AI-30055.

Liz Ossian provided excellent technical support for this work.


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FOOTNOTES
 
* Corresponding author. Mailing address: Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, P.O. Box 647040, Pullman, WA 99164-7040. Phone: (509) 335-6075. Fax: (509) 335-8529. E-mail: tbesser{at}vetmed.wsu.edu Back

{triangledown} Published ahead of print on 10 October 2008. Back


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REFERENCES
 
    1
  1. Anonymous. 2007. Enter-net annual report 2005. Surveillance of enteric pathogens in Europe and beyond. Enter-net surveillance hub, HPA, Centre for Infections, Colindale, London, United Kingdom. http://ecdc.europa.eu/en/files/pdf/Activities/ENTER_NET/annual_report2005.pdf.
    2. 2
  2. Anonymous. 2006. Enter-net annual report 2004. Surveillance of enteric pathogens in Europe and beyond. Enter-net surveillance hub, HPA, Centre for Infections, Colindale, London, United Kingdom. http://ecdc.europa.eu/documents/ENTER_NET/annual_report2004.pdf.
    3. 3
  3. Ansay, S. E., K. A. Darling, and C. W. Kaspar. 1999. Survival of Escherichia coli O157:H7 in ground-beef patties during storage at 2, –2, 15 and then –2 degrees C, and –20 degrees C. J. Food Prot. 62:1243-1247.[Medline]
    4. 4
  4. Avery, S. M., and S. Buncic. 2003. Escherichia coli O157 diversity with respect to survival during drying on concrete. J. Food Prot. 66:780-786.[Medline]
    5. 5
  5. Barkocy-Gallagher, G. A., D. H. Kang, and M. Koohmaraie. 2002. Fate of field-isolated Escherichia coli O157 in ground beef at different storage temperatures. J. Food Prot. 65:1106-1109.[Medline]
    6. 6
  6. Besser, T. E., N. Shaikh, N. J. Holt, P. I. Tarr, M. E. Konkel, P. Malik-Kale, C. W. Walsh, T. S. Whittam, and J. L. Bono. 2007. Greater diversity of Shiga toxin-encoding bacteriophage insertion sites among Escherichia coli O157:H7 isolates from cattle than in those from humans. Appl. Environ. Microbiol. 73:671-679.[Abstract/Free Full Text]
    7. 7
  7. Bollman, J., A. Ismond, and G. Blank. 2001. Survival of Escherichia coli O157:H7 in frozen foods: impact of the cold shock response. Int. J. Food Microbiol. 64:127-138.[CrossRef][Medline]
    8. 8
  8. Bono, J. L., J. E. Keen, M. L. Clawson, L. M. Durso, M. P. Heaton, and W. W. Laegreid. 2007. Association of Escherichia coli O157:H7 tir polymorphisms with human infection. BMC Infect. Dis. 7:98.[Medline]
    9. 9
  9. Centers for Disease Control and Prevention. 2005. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food—10 sites, United States, 2004. MMWR Morb. Mortal. Wkly. Rep. 54:352-356.[Medline]
    10. 10
  10. Centers for Disease Control and Prevention. 2006. Preliminary FoodNet data on the incidence of infection with pathogens transmitted commonly through food—10 States, United States, 2005. MMWR Morb. Mortal. Wkly. Rep. 55:392-395.[Medline]
    11. 11
  11. Cobbold, R., and P. Desmarchelier. 2000. A longitudinal study of Shiga-toxigenic Escherichia coli (STEC) prevalence in three Australian dairy herds. Vet. Microbiol. 71:125-137.[CrossRef][Medline]
    12. 12
  12. Dodson, K., and J. LeJeune. 2005. Escherichia coli O157:H7, Campylobacter jejuni, and Salmonella prevalence in cull dairy cows marketed in northeastern Ohio. J. Food Prot. 68:927-931.[Medline]
    13. 13
  13. Donnenberg, M. S., and T. S. Whittam. 2001. Pathogenesis and evolution of virulence in enteropathogenic and enterohemorrhagic Escherichia coli. J. Clin. Investig. 107:539-548.[Medline]
    14. 14
  14. Dreesman, J., and M. Pulz. 2004. The epidemiology of human enterohemorrhagic Escherichia coli infections in Lower Saxony. Dtsch. Tierarztl. Wochenschr. 111:317-320. (In German.)[Medline]
    15. 15
  15. Energy Information Administration. 2006. World population, 1980-2004. International Energy Annual 2004. Energy Information Administration, U.S. Department of Energy, Washington, DC. http://www.eia.doe.gov.
    16. 16
  16. Gunn, G. J., I. J. McKendrick, H. E. Ternent, F. Thomson-Carter, G. Foster, and B. A. Synge. 2007. An investigation of factors associated with the prevalence of verocytotoxin producing Escherichia coli O157 shedding in Scottish beef cattle. Vet. J. 174:554-564.[CrossRef][Medline]
    17. 17
  17. Halliday, J. E., M. E. Chase-Topping, M. C. Pearce, I. J. McKendrick, L. Allison, D. Fenlon, C. Low, D. J. Mellor, G. J. Gunn, and M. E. Woolhouse. 2006. Herd-level risk factors associated with the presence of Phage type 21/28 E. coli O157 on Scottish cattle farms. BMC Microbiol. 6:99.[CrossRef][Medline]
    18. 18
  18. Hancock, D., T. Besser, J. Lejeune, M. Davis, and D. Rice. 2001. The control of VTEC in the animal reservoir. Int. J. Food Microbiol. 66:71-78.[CrossRef][Medline]
    19. 19
  19. Hayashi, T., K. Makino, M. Ohnishi, K. Kurokawa, K. Ishii, K. Yokoyama, C. G. Han, E. Ohtsubo, K. Nakayama, T. Murata, M. Tanaka, T. Tobe, T. Iida, H. Takami, T. Honda, C. Sasakawa, N. Ogasawara, T. Yasunaga, S. Kuhara, T. Shiba, M. Hattori, and H. Shinagawa. 2001. Complete genome sequence of enterohemorrhagic Escherichia coli O157:H7 and genomic comparison with a laboratory strain K-12. DNA Res. 8:11-22.[Abstract]
    20. 20
  20. Hong, I. H., and J. H. Koo. 2001. Clinical characteristics and prognostic factors of hemolytic uremic syndrome in Korean children. Korean J. Nephrol. 20:486-492.
    21. 21
  21. Hussein, H. S., and L. M. Bollinger. 2005. Prevalence of Shiga toxin-producing Escherichia coli in beef cattle. J. Food Prot. 68:2224-2241.[Medline]
    22. 22
  22. Hussein, H. S., and T. Sakuma. 2005. Prevalence of Shiga toxin-producing Escherichia coli in dairy cattle and their products. J. Dairy Sci. 88:450-465.[Abstract/Free Full Text]
    23. 23
  23. Karch, H., H. Schmidt, C. Janetzki-Mittmann, J. Scheef, and M. Kroger. 1999. Shiga toxins even when different are encoded at identical positions in the genomes of related temperate bacteriophages. Mol. Gen. Genet. 262:600-607.[CrossRef][Medline]
    24. 24
  24. Karmali, M. A. 2004. Infection by Shiga toxin-producing Escherichia coli: an overview. Mol. Biotechnol. 26:117-122.[CrossRef][Medline]
    25. 25
  25. Khakhria, R., D. Duck, and H. Lior. 1990. Extended phage-typing scheme for Escherichia coli O157:H7. Epidemiol. Infect. 105:511-520.[Medline]
    26. 26
  26. Kim, J., J. Nietfeldt, J. Ju, J. Wise, N. Fegan, P. Desmarchelier, and A. K. Benson. 2001. Ancestral divergence, genome diversification, and phylogeographic variation in subpopulations of sorbitol-negative, β-glucuronidase-negative enterohemorrhagic Escherichia coli O157. J. Bacteriol. 183:6885-6897.[Abstract/Free Full Text]
    27. 27
  27. Korean Centers for Disease Control and Prevention. 2007. Communicable disease statistics. Korean Centers for Disease Control and Prevention, Seoul, Korea. http://www.cdc.go.kr.
    28. 28
  28. Law, D. 2000. Virulence factors of Escherichia coli O157 and other Shiga toxin-producing E. coli. J. Appl. Microbiol. 88:729-745.[CrossRef][Medline]
    29. 29
  29. Lejeune, J. T., S. T. Abedon, K. Takemura, N. P. Christie, and S. Sreevatsan. 2004. Human Escherichia coli O157:H7 genetic marker in isolates of bovine origin. Emerg. Infect. Dis. 10:1482-1485.[Medline]
    30. 30
  30. LeJeune, J. T., T. E. Besser, D. H. Rice, J. L. Berg, R. P. Stilborn, and D. D. Hancock. 2004. Longitudinal study of fecal shedding of Escherichia coli O157:H7 in feedlot cattle: predominance and persistence of specific clonal types despite massive cattle population turnover. Appl. Environ. Microbiol. 70:377-384.[Abstract/Free Full Text]
    31. 31
  31. Locking, M., L. Allison, L. Rae, K. Pollock, and M. Hanson. 2006. VTEC infections and livestock-related exposures in Scotland, 2004. Euro Surveill. 11(8):pii=2908. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2908.
    32. 32
  32. Mahon, B. E., P. M. Griffin, P. S. Mead, and R. V. Tauxe. 1997. Hemolytic uremic syndrome surveillance to monitor trends in infection with Escherichia coli O157:H7 and other shiga toxin-producing E. coli. Emerg. Infect. Dis. 3:409-412.[Medline]
    33. 33
  33. Meyer-Broseta, S., S. N. Bastian, P. D. Arne, O. Cerf, and M. Sanaa. 2001. Review of epidemiological surveys on the prevalence of contamination of healthy cattle with Escherichia coli serogroup O157:H7. Int. J. Hyg. Environ. Health 203:347-361.[CrossRef][Medline]
    34. 34
  34. O'Brien, A. D., J. W. Newland, S. F. Miller, R. K. Holmes, H. W. Smith, and S. B. Formal. 1984. Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226:694-696.[Abstract/Free Full Text]
    35. 35
  35. Ogden, I. D., M. MacRae, and N. J. Strachan. 2004. Is the prevalence and shedding concentrations of E. coli O157 in beef cattle in Scotland seasonal? FEMS Microbiol. Lett. 233:297-300.[CrossRef][Medline]
    36. 36
  36. Olsvik, O., E. Rimstad, E. Hornes, N. Strockbine, Y. Wasteson, A. Lund, and K. Wachsmuth. 1991. A nested PCR followed by magnetic separation of amplified fragments for detection of Escherichia coli Shiga-like toxin genes. Mol. Cell. Probes 5:429-435.[Medline]
    37. 37
  37. OzFoodNet Working Group. 2006. Burden and causes of foodborne disease in Australia: annual report of the OzFoodNet network, 2005. Commun. Dis. Intell. 30:278-300.[Medline]
    38. 38
  38. OzFoodNet Working Group. 2005. Reported foodborne illness and gastroenteritis in Australia: annual report of the OzFoodNet network, 2004. Commun. Dis. Intell. 29:164-190.
    39. 39
  39. Paton, A. W., and J. C. Paton. 1998. Detection and characterization of Shiga toxigenic Escherichia coli by using multiplex PCR assays for stx1, stx2, eaeA, enterohemorrhagic E. coli hlyA, rfbO111, and rfbO157. J. Clin. Microbiol. 36:598-602.[Abstract/Free Full Text]
    40. 40
  40. Perna, N. T., G. Plunkett III, V. Burland, B. Mau, J. D. Glasner, D. J. Rose, G. F. Mayhew, P. S. Evans, J. Gregor, H. A. Kirkpatrick, G. Posfai, J. Hackett, S. Klink, A. Boutin, Y. Shao, L. Miller, E. J. Grotbeck, N. W. Davis, A. Lim, E. T. Dimalanta, K. D. Potamousis, J. Apodaca, T. S. Anantharaman, J. Lin, G. Yen, D. C. Schwartz, R. A. Welch, and F. R. Blattner. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409:529-533.[CrossRef][Medline]
    41. 41
  41. Sage, J. R., and S. C. Ingham. 1998. Survival of Escherichia coli O157:H7 after freezing and thawing in ground beef patties. J. Food Prot. 61:1181-1183.[Medline]
    42. 42
  42. Sargeant, J. M., M. W. Sanderson, R. A. Smith, and D. D. Griffin. 2003. Escherichia coli O157 in feedlot cattle feces and water in four major feeder-cattle states in the USA. Prev. Vet. Med. 61:127-135.[CrossRef][Medline]
    43. 43
  43. Sekiya, J. 1997. Escherichia coli O157:H7 in livestock in Japan. Rev. Sci. Tech. 16:391-394.[Medline]
    44. 44
  44. Shaikh, N., and P. I. Tarr. 2003. Escherichia coli O157:H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J. Bacteriol. 185:3596-3605.[Abstract/Free Full Text]
    45. 45
  45. Woerner, D. R., J. R. Ransom, J. N. Sofos, G. A. Dewell, G. C. Smith, M. D. Salman, and K. E. Belk. 2006. Determining the prevalence of Escherichia coli O157 in cattle and beef from the feedlot to the cooler. J. Food Prot. 69:2824-2827.[Medline]

Applied and Environmental Microbiology, December 2008, p. 7447-7450, Vol. 74, No. 23
0099-2240/08/$08.00+0     doi:10.1128/AEM.01190-08
Copyright © 2008, American Society for Microbiology. All Rights Reserved.




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