1887

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Volume 55, Issue 7

Influence of colostrum deprivation and concurrent infection on the colonization and persistence of O157 : H7 in young lambs Free

Abstract

O157 : H7 and infections of man have been associated with direct contact with small ruminants. Colostrum protects neonates against gastrointestinal pathogens, and orphan lambs, which are common on petting farms, may be deprived of this protection. In a recent study, it was demonstrated that high shedding of O157 : H7 by an 8-week-old goat kid was associated with coincidental infection. Furthermore, both pathogens were co-located in the distal gastrointestinal tract. It was hypothesized that colostrum deprivation and pre-infection with predisposed young ruminants to colonization and increased shedding of O157 : H7. To test this, 21 lambs 5 weeks of age were divided into four groups as follows: (A) colostrum-deprived and inoculated with O157 : H7, (B) colostrum-deprived and inoculated with and then O157 : H7, (C) conventionally reared and inoculated with O157 : H7, (D) conventionally reared and inoculated with and then O157 : H7. was detected between 8 and 12 days post-inoculation in most of the infected lambs. At 24 h post-inoculation with O157 : H7, all lambs were shedding between 5×10 and 5×10 c.f.u. O157 : H7 per gram of faeces. O157 : H7 was shed in higher numbers in the groups pre-inoculated with , whether conventionally reared or colostrum-deprived. Interestingly, for the colostrum-deprived lambs on day 3, a significant difference in shedding of O157 : H7 was observed (=0.038), with the lambs inoculated with alone yielding higher counts than those pre-inoculated with . From day 15 onwards, shedding of O157 : H7 was highest from the colostrum-deprived -infected lambs, then (in descending order of shedding) the colostrum-deprived lambs, the conventionally reared lambs infected with , and the conventionally reared animals. In total, four animals were euthanized, two at 24 h and two at 96 h post inoculation with O157 : H7 (two conventionally reared and two colostrum-deprived). All animals euthanized were from groups pre-inoculated with prior to challenge with O157 : H7. On examination of tissues, in three of the four animals examined, multifocal attaching and effacing lesions were observed in the caecum, colon, rectum and at the recto-anal junction, and were confirmed by immunohistochemistry to be associated with O157 : H7.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): AE, attaching and effacing , GIT, gastrointestinal tract , HE, haematoxylin and eosin , IFAT, indirect fluorescent antibody test , IMS, immunomagnetic separation , mZN, modified Ziehl–Neelsen , p.i., post-infection , RAJ, recto-anal junction and VLA, Veterinary Laboratories Agency
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2006-07-01
2024-04-18
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References

  1. Altmann K., Mukkur T. K. 1983; Passive immunisation of neonatal lambs against infection with enteropathogenic Escherichia coli via colostrum of ewes immunised with crude and purified K99 pili. Res Vet Sci 35:234–239
     [Google Scholar]
  2. Angus K. W., Tzipori S., Gray E. W. 1982; Intestinal lesions in specific-pathogen-free lambs associated with a Cryptosporidium from calves with diarrhoea. Vet Pathol 19:67–78 [CrossRef]
     [Google Scholar]
  3. Bach S. J., Selinger L. J., Stanford K., McAllister T. A. 2005; Effect of supplementing corn- or barley-based feedlot diets with canola oil on faecal shedding of Escherichia coli O157 : H7 by steers. J Appl Microbiol 98:464–475 [CrossRef]
     [Google Scholar]
  4. Barker I. K., Carbonell P. L. 1974; Cryptosporidium agni spp. N. from lambs and Cryptosporidium bovis sp. N. from a calf with observations on the oocyst. Z Parasitenkd 44:289–298 [CrossRef]
     [Google Scholar]
  5. Best A., La Ragione R. M., Sayers A. R., Woodward M. J. 2005; Role for flagella but not intimin in the persistent infection of the gastro-intestinal tissues of specific pathogen free chicks by Stx-negative Escherichia coli O157 : H7. Infect Immun 73:1836–1846 [CrossRef]
     [Google Scholar]
  6. Boyce T. G., Swerdlow D. L., Griffin P. M. 1995; Escherichia coli O157 and the haemolytic uraemic syndrome. N Engl J Med 333:364–368 [CrossRef]
     [Google Scholar]
  7. Brown C. A., Harmon B. G., Zhao T., Doyle M. P. 1997; Experimental Escherichia coli O157 carriage in cattle. Appl Environ Microbiol 63:27–32
     [Google Scholar]
  8. Butler J. E. 1979; Immunologic aspects of breast feeding, anti-infectious activity of breast milk. Semin Perinatol 3:255–270
     [Google Scholar]
  9. Castro-Hermida J. A., Gonzalez-Losada Y., Freire-Santos F., Gonzalez-Warleta M., Mezo-Menendez M., Ares-Mazas E. 2002; Efficacy of beta-cyclodextrin against experimental cryptosporidiosis in neonatal lambs. J Parasitol 88:185–187
     [Google Scholar]
  10. Chapman P. A., Siddons C. A., Cerdan-Malo A. T., Harkin M. A. 1997; A 1-year study of Escherichia coli O157 in cattle, sheep, pigs and poultry. Epidemiol Infect 119:245–250 [CrossRef]
     [Google Scholar]
  11. Chapman P. A., Cornell J., Green C. 2000; Infection with verocytotoxin-producing Escherichia coli O157 : H7 during a visit to an inner city open farm. Epidemiol Infect 125:553–536
     [Google Scholar]
  12. Cookson A. L., Wales A. D., Roe J. M., Hayes C. M., Pearson G. R., Woodward M. J. 2002; Variation in the persistence of Escherichia coli O157 : H7 in experimentally inoculated 6-week-old conventional lambs. J Med Microbiol 51:1032–1040
     [Google Scholar]
  13. Cray W. C. Jr, Moon H. W. 1995; Experimental infection of calves and adult cattle with Escherichia coli O157 : H7. Appl Environ Microbiol 61:1586–1590
     [Google Scholar]
  14. Dean-Nystrom E. A., Bosworth B. T., Moon H. W. 1997; Pathogenesis of O157 : H7 Escherichia coli infection in neonatal calves. Adv Exp Med Biol 412:47–51
     [Google Scholar]
  15. Dean-Nystrom E. A., Bosworth B. T., O'Brien A. D., Moon H. W. 1999 Bovine infection with Escherichia coli O157 : H7. In E. coli O157 in Farm Animals Edited by Stewart C. S., Flint H. J. Wallingford, UK: CAB International;
     [Google Scholar]
  16. Dean-Nystrom E. A., Gansheroff L. J., Mills M., Moon H. W., O'Brien A. D. 2002; Vaccination of pregnant dams with intimin (O157) protects suckling piglets from Escherichia coli O157 : H7 infection. Infect Immun 70:2414–2418 [CrossRef]
     [Google Scholar]
  17. De Graff D. C., Vanopdenbosch E., Ortega-Mora L. M., Abbassi H., Peeters J. E. 1999; A review of the importance of cryptosporidiosis in farm animals. Int J Parasitol 29:1269–1287 [CrossRef]
     [Google Scholar]
  18. De la Fuente R., Luzon M., Ruiz-Santa-Quiteria J. A., Garcia A., Cid D., Orden J. A., Garcia S., Sanz R., Gomez-Baustista M. 1999; Cryptosporidium and concurrent infections with other major enteropathogens in 1 to 30 day old diarrheic dairy calves in central Spain. Vet Parasitol 80:179–185 [CrossRef]
     [Google Scholar]
  19. Elliott D. A., Clark D. P. 2000; Cryptosporidium parvum induces host cell actin accumulation at the host–parasite interface. Infect Immun 68:2315–2322 [CrossRef]
     [Google Scholar]
  20. Elliott D. A., Coleman D. J., Lane M. A., May R. C., Machesky L. M., Clark D. P. 2001; Cryptosporidium parvum infection requires host cell actin polymerization. Infect Immun 69:5940–5942 [CrossRef]
     [Google Scholar]
  21. Fegan N., Desmarchelier P. 1999; Shiga toxin-producing Escherichia coli in sheep and pre-slaughter lambs in eastern Australia. Lett Appl Microbiol 28:335–339 [CrossRef]
     [Google Scholar]
  22. Foreyt W. J. 1990; Coccidiosis and cryptosporidiosis in sheep and goats. Vet Clin North Am Food Animal Pract 6:655–670
     [Google Scholar]
  23. Griffin P. M., Tauxe R. V. 1991; The epidemiology of infections caused by Escherichia coli O157, other enterohaemorrhagic E. coli and the associated haemolytic uraemic syndrome. Epidemiol Rev 13:60–98
     [Google Scholar]
  24. Griffiths J. K. 1998; Human cryptosporidiosis: epidemiology, transmission, clinical disease, treatment, and diagnosis. Adv Parasitol 40:37–85 [CrossRef]
     [Google Scholar]
  25. Guerrant R. L. 1997; Cryptosporidiosis: an emerging highly infectious threat. Emerg Infect Dis 3:51–57 [CrossRef]
     [Google Scholar]
  26. Gunning R. F., Wales A. D., Pearson G. R., Done E., Cookson A. L., Woodward M. J. 2001; Attaching and effacing lesions in the intestines of two calves associated with natural infection with Escherichia coli O26 : H11. Vet Rec 148:780–782 [CrossRef]
     [Google Scholar]
  27. Hancock D. D., Besser T. E., Rice D. H., Herriott D. E., Tarr P. I. 1997; A longitudinal study of Escherichia coli O157 in fourteen cattle herds. Epidemiol Infect 118:193–195 [CrossRef]
     [Google Scholar]
  28. Henriksen S. A., Pohlenz J. F. 1981; Staining of cryptosporidia by a modified Ziehl–Neelsen technique. Acta Vet Scand 22:594–596
     [Google Scholar]
  29. Heuvelink A. E., Van Den Biggelaar F. L., De Boer E., Herbes R. G., Melchers W. J., Huis in't Veld J. H., Monnens L. A. 1998; Isolation and characterization of verocytotoxin-producing Escherichia coli O157 strains from Dutch cattle and sheep. J Clin Microbiol 36:878–882
     [Google Scholar]
  30. Heuvelink A. E., van Heerwaarden C., Zwartkruis-Nahuis J. T., van Oosterom R., Edink K., van Duynhoven Y. T., de Boer E. 2002; Escherichia coli O157 infection associated with a petting zoo. Epidemiol Infect 129:295–302
     [Google Scholar]
  31. Janke B. H., Francis D. H., Collins J. E., Libal M. C., Zeman D. H., Johnson D. D., Neiger R. D. 1990; Attaching and effacing Escherichia coli infection as a cause of diarrhea in young calves. J Am Vet Med Assoc 196:897–901
     [Google Scholar]
  32. Johnson E. H., Muirhead D. E., Windsor J. J., King G. J., Al-Busaidy R., Cornelius R. 1999; Atypical outbreak of caprine cryptosporidiosis in the Sultanate of Oman. Vet Rec 145:521–524 [CrossRef]
     [Google Scholar]
  33. Kaper J. B., Nataro J. P., Mobley H. L. 2004; Pathogenic Escherichia coli . Nat Rev Microbiol 2:123–140 [CrossRef]
     [Google Scholar]
  34. Karmali M. A., Steele B. T., Petric M., Lim C. 1983; Sporadic cases of haemolytic-uraemic syndrome associated with faecal cytotoxin producing Escherichia coli in stools. Lancet I:619–620
     [Google Scholar]
  35. Kelleher S. L., Lonnerdal B. 2001; Immunological activities associated with milk. Adv Nutr Res 10:39–65
     [Google Scholar]
  36. Knutton S., Baldwin T., Williams P. H., McNeish A. S. 1989; Actin accumulation at sites of bacterial adhesion to tissue culture cells: basis of a new diagnostic test for enteropathogenic and enterohaemorrhagic E. coli . Infect Immun 57:1290–1298
     [Google Scholar]
  37. Koudela B., Bokova A. 1997; The effect of cotrimoxazole on experimental Cryptosporidium parvum infection in kids. Vet Res 28:405–412
     [Google Scholar]
  38. Koudela B., Jiri V. 1997; Experimental cryptosporidiosis in kids. Vet Parasitol 71:273–281 [CrossRef]
     [Google Scholar]
  39. La Ragione R. M., Ahmed N. M. Y., Best A., Clifford D., Weyer U., Cooley W. A., Johnson L., Pearson G. R., Woodward M. J. 2005a; Colonisation of eight-week-old conventionally-reared goats by Escherichia coli O157 : H7 after oral inoculation. J Med Microbiol 54:485–492 [CrossRef]
     [Google Scholar]
  40. La Ragione R. M., Best A., Clifford D., Weyer U., Woodward M. J. 2005b; Failure to detect transmission of E. coli O157 : H7 from orally dosed nannies to suckling kids at foot. Vet Rec 157:659–661 [CrossRef]
     [Google Scholar]
  41. Locking M. E., O'Brien S. J., Reilly W. J., Wright E. M., Campbell D. M., Coia J. E., Browning L. M., Ramsay C. N. 2001; Risk factors for sporadic cases of Escherichia coli O157 infection: the importance of contact with animal excreta. Epidemiol Infect 127:215–220
     [Google Scholar]
  42. Logan E. F., Stenhouse A., Ormrod D. J. 1974; The role of colostral immunoglobulins in intestinal immunity to enteric colibacillosis in the calf. Res Vet Sci 17:290–301
     [Google Scholar]
  43. Meng J., Zhao S., Doyle M. P. 1998; Virulence genes of Shiga toxin-producing Escherichia coli isolated from food, animals and humans. Int J Food Microbiol 45:229–235 [CrossRef]
     [Google Scholar]
  44. Moon H. W., McClurkin A. W., Isaacson R. E., Pohlenz J., Skartvedt S. M., Gillette K. G., Baetz A. L. 1978; Pathogenic relationships of rotavirus, Escherichia coli , and other agents in mixed infections in calves. J Am Vet Med Assoc 173:577–583
     [Google Scholar]
  45. Morin M., Lariviee S., Lallier R., Begin M. E., Ethier R., Roy R. S., Tremblay A. 1980; Diarrhoea of newborn calves. II. Agents responsible for the disease on Quebec dairy farm. . Med Vet Quebec 10:60–65
     [Google Scholar]
  46. Munoz-Fernandez M., Alvarez M., Lanza I., Carmenes P. 1996; Role of enteric pathogens in the aetiology of neonatal diarrhoea in lambs and goat kids in Spain. Epidemiol Infect 117:203–211 [CrossRef]
     [Google Scholar]
  47. Naylor S. W., Low J. C., Besser T. E., Mahajan A., Gunn G. J., Pearce M. C., McKendrick I. J., Smith D. G., Gally D. L. 2003; Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157 : H7 in the bovine host. Infect Immun 71:1505–1512 [CrossRef]
     [Google Scholar]
  48. Noordeen F., Horaldagoda N. U., Faizal A. C. M., Rajapakse R. P. V. J., Razak M. A. A., Arulkanthan A. 2002; Infectivity of Cryptosporidium parvum isolated from asymptomatic adult goats to mice and goat kids. Vet Parasitol 103:217–225 [CrossRef]
     [Google Scholar]
  49. O'Donoghue P. J. 1995; Cryptosporidium and cryptosporidiosis in man and animals. Int J Parasitol 25:139–195 [CrossRef]
     [Google Scholar]
  50. Ortega-Mora L. M., Troncoso J. M., Rojo-Vazquez F. A., Gomez-Bautista M. 1993; Serum antibody response in lambs naturally and experimentally infected with Cryptosporidium parvum . Vet Parasitol 50:45–54 [CrossRef]
     [Google Scholar]
  51. Panciera R. J., Thomassen R. W., Garner F. M. 1971; Cryptosporidiosis in a calf. Vet Pathol 8:479–484
     [Google Scholar]
  52. Paton J. C., Paton A. W. 1998; Pathogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11:450–479
     [Google Scholar]
  53. Payne C. J., Petrovic M., Roberts R. J. & 9 other authors; 2003; Vero cytotoxin-producing Escherichia coli O157 gastroenteritis in farm visitors, North Wales. Emerg Infect Dis 9:526–530 [CrossRef]
     [Google Scholar]
  54. Pepin M., Russo P., Pardon P. 1997; Public health hazards from small ruminant meat products in Europe. Rev Sci Technol 16:415–425
     [Google Scholar]
  55. Pritchard G. C., Willshaw G. A., Bailey J. R., Carson T., Cheasty T. 2000; Verocytotoxin-producing Escherichia coli O157 on a farm open to the public: outbreak investigation and longitudinal bacteriological study. Vet Rec 147:259–264 [CrossRef]
     [Google Scholar]
  56. Reynolds D. J., Morgan J. H., Chanter N., Jones P. W., Bridger J. C., Debney T. G., Bunch K. L. 1986; Microbiology of calf diarrhoea in southern Britain. Vet Rec 119:34–39 [CrossRef]
     [Google Scholar]
  57. Riley L. W., Remis R. S., Helgerson S. D. & 9 other authors; 1983; Hemorrhagic colitis associated with a rare Escherichia coli serotype. N Engl J Med 308:681–685 [CrossRef]
     [Google Scholar]
  58. Rugsbjerg H., Nielsen E. M., Andersen J. S. 2003; Risk factors associated with faecal shedding of verocytotoxin-producing Escherichia coli O157 in eight known-infected Danish dairy herds. Prev Vet Med 58:101–113 [CrossRef]
     [Google Scholar]
  59. Shaner N. C., Sanger J. W., Sanger J. M. 2005; Actin and alpha-actinin dynamics in the adhesion and motility of EPEC and EHEC on host cells. Cell Motil Cytoskeleton 60:104–120 [CrossRef]
     [Google Scholar]
  60. Sheng H., Davis M. A., Knecht H. J., Hovde C. J. 2004; Rectal administration of Escherichia coli O157 : H7: novel model for colonization of ruminants. Appl Environ Microbiol 70:4588–4595 [CrossRef]
     [Google Scholar]
  61. Smith H. R., Scotland S. M. 1993; Isolation and identification methods for Escherichia coli O157 and other verocytotoxin producing strains. J Clin Pathol 46:10–17 [CrossRef]
     [Google Scholar]
  62. Swinbanks D. 1996; Japan shuns radishes after ‘possible link’ to E. coli . Nature 382:567–568
     [Google Scholar]
  63. Tzipori S., Angus K. W., Gray E. W., Campbell I., Allan F. 1981; Diarrhea in lambs experimentally infected with Cryptosporidium isolated from calves. Am J Vet Res 42:1400–1404
     [Google Scholar]
  64. Wales A. D., Clifton-Hadley F. A., Cookson A. L., Dibb-Fuller M. P., La Ragione R. M., Sprigings K. A., Pearson G. R., Woodward M. J. 2001a; Experimental infection of six-month old lambs with Escherichia coli O157 : H7. Vet Rec 148:630–631 [CrossRef]
     [Google Scholar]
  65. Wales A. D., Pearson G. R., Skuse A. M., Roe J. M., Hayes C. M., Cookson A. L., Woodward M. J. 2001b; Attaching and effacing lesions caused by Escherichia coli O157 : H7 in experimentally inoculated neonatal lambs. J Med Microbiol 50:752–758
     [Google Scholar]
  66. Wales A. D., Pearson G. R., Roe J. M., Hayes C. M., La Ragione R. M., Woodward M. J. 2005; Attaching-effacing lesions associated with Escherichia coli O157 : H7 and other bacteria in experimentally inoculated conventional neonatal goat kids. J Comp Pathol 132:185–194 [CrossRef]
     [Google Scholar]
  67. Woodward M. J., Best A., Sprigings K. A. & 7 other authors; 2003; Non-toxigenic Escherichia coli O157 : H7 strain NCTC12900 causes attaching-effacing lesions and eae dependent persistence in weaned sheep. Int J Med Microbiol 293:299–308 [CrossRef]
     [Google Scholar]
  68. Zhao T., Doyle M. P., Shere J., Garber L. 1995; Prevalence of enterohaemorrhagic Escherichia coli O157 : H7 in a survey of dairy herds. Appl Environ Microbiol 61:1290–1293
     [Google Scholar]
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Influence of colostrum deprivation and concurrent Cryptosporidium parvum infection on the colonization and persistence of Escherichia coli O157 : H7 in young lambs
J. Med. Microbiol. 55, 819 (2006); https://doi.org/10.1099/jmm.0.46469-0
/content/journal/jmm/10.1099/jmm.0.46469-0
/content/journal/jmm/10.1099/jmm.0.46469-0
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