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Effect of Escherichia coli infection of the bovine uterus from the whole animal to the cell*

Published online by Cambridge University Press:  01 August 2008

E. J. Williams ,
S. Herath ,
G. C. W. England ,
H. Dobson ,
C. E. Bryant  and
I. M. Sheldon
E. J. Williams*
Affiliation:
Department of Veterinary Clinical Sciences, Royal Veterinary College, Royal College Street, London, NW1 0TU, UK
S. Herath
Affiliation:
Department of Veterinary Clinical Sciences, Royal Veterinary College, Royal College Street, London, NW1 0TU, UK
G. C. W. England
Affiliation:
The School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington Campus, Sutton Bonington, Leicestershire, LE12 5RD, UK
H. Dobson
Affiliation:
Department of Veterinary Clinical Science and Animal Husbandry, Faculty of Veterinary Science, University of Liverpool, Leahurst, Neston, CH64 7TE, UK
C. E. Bryant
Affiliation:
Centre for Veterinary Science, Department of Clinical Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK
I. M. Sheldon
Affiliation:
Department of Veterinary Clinical Sciences, Royal Veterinary College, Royal College Street, London, NW1 0TU, UK
*
E-mail: erin.williams@ucd.ie
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Abstract

Following parturition, contamination of the uterine lumen by bacteria is ubiquitous, and uterine health is impaired in cattle because infection persists in 10% to 15% of animals as endometritis. Endometritis causes infertility for the duration of infection, and subfertility persists even after apparent successful resolution of the disease. Escherichia coli is the pathogenic bacterium most frequently isolated from the post partum uterus, and is associated with increased concentrations of peripheral plasma acute phase proteins and fetid vaginal mucus. The presence of E. coli is also associated with slower growth of the first post partum dominant follicle and perturbed oestradiol secretion. Furthermore, in animals that ovulate the first dominant follicle, the corpus luteum is smaller and secretes less progesterone. The endotoxin lipopolysaccharide (LPS), which is released from E.coli, can pass from the uterine lumen to the peripheral circulation and LPS concentrations are increased in cows with uterine infection. Infusion of E. coli LPS into the uterine lumen suppresses the pre-ovulatory luteinising hormone surge and disrupts ovulation in heifers. In vitro, endometrial explants produce prostaglandins in response to LPS. Addition of LPS or E. coli to stromal or epithelial cells increases cyclooxygenase-2 mRNA expression, and stimulates the production of prostaglandin E2 and prostaglandin F2α . Furthermore, uterine and ovarian cells express mRNA of the molecules required for recognition of LPS, Toll-like receptor-4 and CD14. In summary, E. coli is a common cause of infertility involving the perturbation of the hypothalamus, pituitary and ovary in dairy cows.

Keywords

uterusovaryinfectionE. coliimmunity
Type
Full Paper
Information
animal , Volume 2 , Issue 8 , August 2008 , pp. 1153 - 1157
Copyright
Copyright © The Animal Consortium 2008

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Footnotes

*

This invited paper was presented at BSAS meeting ‘Fertility in Dairy Cows – bridging the gaps’ 30-31 August 2007, Liverpool Hope University.

References

Akira, S, Takeda, K 2004. Toll-like receptor signalling. Nature Reviews Immunology 4, 499–511.Google Scholar
Akira, S, Uematsu, S, Takeuchi, O 2006. Pathogen recognition and innate immunity. Cell 124, 783–801.Google Scholar
Battaglia, DF, Krasa, HB, Padmanabhan, V, Viguie, C, Karsch, FJ 2000. Endocrine alterations that underlie endotoxin-induced disruption of the follicular phase in ewes. Biology of Reproduction 62, 45–53.Google Scholar
Baumann, H, Gauldie, J 1994. The acute phase response. Immunology Today 15, 74–80.Google Scholar
Beutler, B 2003. Innate immune responses to microbial poisons: discovery and function of the Toll-like receptors. Annual Review of Pharmacology and Toxicology 43, 609–628.Google Scholar
Beutler, B 2004. Innate immunity: an overview. Molecular Immunology 40, 845–859.Google Scholar
Bonnett, B, Martin, SW, Gannon, VP, Miller, RB, Etherington, WG 1991. Endometrial biopsy in Holstein-Friesian dairy cows III: bacteriological analysis and correlations with histological findings. Canadian Journal of Veterinary Research 55, 168–173.Google Scholar
Borsberry, S, Dobson, H 1989. Periparturient diseases and their effect on reproductive performance in five dairy herds. The Veterinary Record 124, 217–219.Google Scholar
Dhaliwal, GS, Murray, RD, Woldehiwet, Z 2001. Some aspects of immunology of the bovine uterus related to treatments for endometritis. Animal Reproduction Science 67, 135–152.CrossRefGoogle ScholarPubMed
Donofrio, G, Herath, S, Sartori, C, Cavirani, S, Flammini, C, Sheldon, IM 2007. Bovine herpesvirus 4 (BoHV-4) is tropic for bovine endometrial cells and modulates endocrine function. Reproduction 134, 183–197.Google Scholar
Elliott, L, McMahon, KJ, Gier, HT, Marion, GB 1968. Uterus of the cow after parturition: bacterial content. American Journal of Veterinary Research 29, 77–81.Google ScholarPubMed
Farin, PW, Ball, L, Olson, JD, Mortimer, RG, Jones, RL, Admey, WS, McChesney, AE 1989. Effect of Actinomyces pyogenes and Gram-negative bacteria on the development of bovine pyometra. Theriogenology 31, 979–989.Google Scholar
Griffin, JFT, Hartigan, PJ, Nunn, WR 1974. Non-specific uterine infection and bovine fertility I: infection patterns and endometritis during the first seven weeks postpartum. Theriogenology 1, 91–106.CrossRefGoogle Scholar
Herath, S, Fischer, DP, Werling, D, Williams, EJ, Lilly, ST, Dobson, H, Bryant, CE, Sheldon, IM 2006. Expression and function of Toll-like receptor 4 in the endometrial cells of the uterus. Endocrinology 147, 562–570.CrossRefGoogle ScholarPubMed
Herath, S, Williams, EJ, Lilly, SR, Gilbert, RO, Dobson, H, Bryant, CE, Sheldon, IM 2007. Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 134, 683–693.Google Scholar
Hirata, T, Osuga, Y, Hirota, Y, Koga, K, Yoshino, O, Harada, M, Morimoto, C, Yano, T, Nishii, O, Tsutsumi, O, Taketani, Y 2005. Evidence for the presence of toll-like receptor 4 system in the human endometrium. Journal of Clinical Endocrinology and Metabolism 90, 548–556.Google Scholar
Hussain, AMD, Daniel, RCW, O’Boyle, D 1990. Postpartum uterine flora following normal and abnormal puerperium in cows. Theriogenology 34, 291–302.CrossRefGoogle ScholarPubMed
Huszenicza, G, Fodor, M, Gacs, M, Kulcsar, M, Dohmen, MJW, Vamos, M 1999. Uterine bacteriology, resumption of cyclic ovarian activity and fertility in postpartum cows kept in large-scale dairy herds. Reproduction in Domestic Animals 34, 237–245.Google Scholar
Laven, RA, Biggadike, HJ, Proven, MJ, Halfacre, S, Tickle, LR 2000. Changes in vaginal microbiology associated with the use of progesterone-releasing intravaginal devices. The Veterinary Record 146, 760–762.CrossRefGoogle ScholarPubMed
LeBlanc, SJ, Duffield, TF, Leslie, KE, Bateman, KG, Keefe, GP, Walton, JS, Johnson, WH 2002a. Defining and diagnosing postpartum clinical endometritis and its impact on reproductive performance in dairy cows. Journal of Dairy Science 85, 2223–2236.Google Scholar
LeBlanc, SJD, Duffield, TF, Leslie, KE, Bateman, KG, Keefe, GP, Walton, JS, Johnson, WH 2002b. The effect of treatment of clinical endometritis on reproductive performance in dairy cows. Journal of Dairy Science 85, 2237–2249.Google Scholar
Mateus, L, Lopes da Costa, LL, Bernardo, F, Silva, JR 2002. Influence of puerperal uterine infection on uterine involution and postpartum ovarian activity in dairy cows. Reproduction in Domestic Animals 37, 31–35.Google Scholar
Mateus, L, Lopes da Costa, LL, Diniz, P, Ziecik, AJ 2003. Relationship between endotoxin and prostaglandin (PGE2 and PGFM) concentrations and ovarian function in dairy cows with puerperal endometritis. Animal Reproduction Science 76, 143–154.Google Scholar
Miller, AN, Williams, EJ, Sibley, K, Herath, S, Lane, EA, Fishwick, J, Nash, DM, Rycroft, AN, Dobson, H, Bryant, CE, Sheldon, IM 2007. The effects of Arcanobacterium pyogenes on endometrial function in vitro, and on uterine and ovarian function in vivo. Theriogenology 68, 972–980.Google Scholar
Noakes, DE, Till, D, Smith, GR 1989. Bovine uterine flora postpartum: a comparison of swabbing and biopsy. The Veterinary Record 124, 563–564.CrossRefGoogle Scholar
Olson, JD, Ball, L, Mortimer, RG, Farin, PW, Adney, WS, Huffman, EM 1984. Aspects of bacteriology and endocrinology of cows with pyometra and retained fetal membranes. American Journal of Veterinary Research 45, 2251–2255.Google Scholar
Opsomer, G, Grohn, YT, Hertl, J, Coryn, M, Deluyker, H, de Kruif, A 2000. Risk factors for postpartum ovarian dysfunction in high producing dairy cows in Belgium: a field study. Theriogenology 53, 841–857.Google Scholar
Peter, AT, Bosu, WT, DeDecker, RJ 1989. Suppression of preovulatory luteinising hormone surges in heifers after intrauterine infusions of E. coli endotoxin. American Journal of Veterinary Research 50, 368–373.Google Scholar
Pioli, PA, Amiel, E, Schaefer, TM, Connolly, JE, Wira, CR, Guyre, PM 2004. Differential expression of Toll-like receptors 2 and 4 in tissues of the human female reproductive tract. Infection and Immunity 72, 5799–5806.CrossRefGoogle ScholarPubMed
Poyser, NL 1995. The control of prostaglandin production by the endometrium in relation to luteolysis and menstruation. Prostaglandins Leukotrienes and Essential Fatty Acids 53, 147–195.Google Scholar
Ruder, CA, Sasser, RG, Williams, RJ, Ely, JK, Bull, RC, Butler, JE 1981. Uterine infections in the postpartum cow. II. Possible synergistic effect of Fusobacterium necrophorum and Corynebacterium pyogenes. Theriogenology 15, 573–580.Google Scholar
Schaefer, TM, Fahey, JV, Wright, JA, Wira, CR 2005. Innate immunity in the human female reproductive tract: Antiviral response of uterine epithelial cells to the TLR3 agonist Poly(I:C). Journal of Immunology 174, 992–1002.CrossRefGoogle Scholar
Sheldon, IM, Dobson, H 1999. Postpartum uterine recovery and its influence on ovarian activity – a preliminary report. Cattle Practice 7, 409–410.Google Scholar
Sheldon, IM, Noakes, DE, Rycroft, A, Dobson, H 2001. Acute phase protein response to postpartum uterine bacterial contamination in cattle. The Veterinary Record 148, 172–175.Google Scholar
Sheldon, IM, Noakes, DE, Rycroft, AN, Pfeiffer, DU, Dobson, H 2002. Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction 123, 837–845.Google Scholar
Sheldon, IM, Dobson, H 2004. Postpartum uterine health in cattle. Animal Reproduction Science 82–83, 295–306.Google Scholar
Suzuki, C, Yoshioka, K, Iwamura, S, Hirose, H 2001. Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers. Domestic Animal Endocrinology 20, 267–278.Google Scholar
Williams, CY, Harris, TG, Battaglia, DF, Viquie, C, Karsch, FJ 2001. Endotoxin inhibits pituitary responsiveness to gonadotropin-releasing hormone. Endocrinology 142, 1915–1922.CrossRefGoogle ScholarPubMed
Williams, EJ, Fischer, DP, Pfeiffer, DU, England, GE, Noakes, DE, Dobson, H, Sheldon, IM 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63, 102–117.Google Scholar
Williams, EJ, Fischer, DP, Noakes, DE, England, GE, Rycroft, A, Dobson, H, Sheldon, IM 2007. Uterine infection perturbs ovarian function in the postpartum dairy cow. Theriogenology 68, 549–559.Google Scholar
Xiao, E, Xia-Zhang, L, Barth, A, Zhu, J, Ferrin, M 1998. Stress and the menstrual cycle: relevance of cycle quality in the short and long-term response to a 5-day endotoxin challenge during the follicular phase in the rhesus monkey. Journal of Clinical Endocrinology and Metabolism 83, 2454–2460.Google Scholar
Young, SL, Lyddon, TD, Jorgenson, RL, Misfeldt, ML 2004. Expression of Toll-like receptors in human endometrial epithelial cells and cell lines. American Journal of Reproductive Immunology 52, 67–73.Google Scholar