BMC veterinary research2012; 8; 41; doi: 10.1186/1746-6148-8-41

Inflammatory responses to induced infectious endometritis in mares resistant or susceptible to persistent endometritis.

Abstract: The objective of the study was to evaluate the gene expression of inflammatory cytokines (interleukin [IL]-1β, IL-6, IL-8, IL-10, tumor necrosis factor [TNF]-α, IL-1 receptor antagonist [ra] and serum amyloid A (SAA) in endometrial tissue and circulating leukocytes in response to uterine inoculation of 105 colony forming units (CFU) Escherichia coli in mares. Before inoculation, mares were classified as resistant or susceptible to persistent endometritis based on their uterine inflammatory response to infusion of 109 killed spermatozoa and histological assessment of the endometrial quality. Endometrial biopsies were obtained 3, 12, 24 and 72 hours (h) after bacterial inoculation and blood samples were obtained during the 7 day period post bacterial inoculation. Expression levels of cytokines and SAA were determined by quantitative real-time reverse transcriptase PCR (qRT-PCR). Results: Compared to levels in a control biopsy (obtained in the subsequent estrous), resistant mares showed an up-regulation of IL-1β, IL-6, IL-8 and TNF-α at 3 h after E. coli inoculation, while susceptible mares showed increased gene expression of IL-6 and IL-1ra. Susceptible mares had a significant lower gene expression of TNF-α,IL-6 and increased expression of IL-1ra 3 h after E. coli inoculation compared to resistant mares. Susceptible mares showed a sustained and prolonged inflammatory response with increased gene expression levels of IL-1β, IL-8, IL-1ra and IL-1β:IL-1ra ratio throughout the entire study period (72 h), whereas levels in resistant mares returned to estrous control levels by 12 hours. Endometrial mRNA transcripts of IL-1β and IL-1ra were significantly higher in mares with heavy uterine bacterial growth compared to mares with no/mild growth.All blood parameters were unaffected by intrauterine E. coli infusion, except for a lower gene expression of IL-10 at 168 h and an increased expression of IL-1ra at 48 h observed in susceptible mares compared to resistant mares. Conclusions: The current investigation suggests that endometrial mRNA transcripts of pro-inflammatory cytokines in response to endometritis are finely regulated in resistant mares, with initial high expression levels followed by normalization within a short period of time. Susceptible mares had a prolonged expression of pro-inflammatory cytokines, supporting the hypothesis that an unbalanced endometrial gene expression of inflammatory cytokines might play an important role in the pathogenesis of persistent endometritis.
Publication Date: 2012-03-29 PubMed ID: 22458733PubMed Central: PMC3368729DOI: 10.1186/1746-6148-8-41Google Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
  • Journal Article
  • Research Support
  • Non-U.S. Gov't

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This study investigates how the gene expression of certain inflammatory proteins changes in response to artificially induced uterine infections in mares. Differences between mares that are resistant and those susceptible to chronic uterine inflammation were analyzed to better understand the role of these inflammatory proteins in the persistence of uterine inflammation.

Research Methodology

  • The researchers divided the mares into two groups based on their resilience to chronic uterine inflammation. This was determined through their inflammatory response to a large number of killed sperm cells and a histological examination of their uterine tissue.
  • They induced a uterine infection in each mare by inoculating them with 105 CFU Escherichia coli and collected endometrial biopsies at 3, 12, 24 and 72 hours after the inoculation process.
  • Blood samples were taken over the course of 7 days following the E. coli inoculation.
  • They utilised real-time reverse transcriptase PCR, a method used to measure gene expression levels, to determine the levels of inflammatory cytokines and serum amyloid A (a protein associated with inflammation) in the endometrial tissue and circulating blood cells.

Results

  • Resistant mares displayed an increase in the gene expression of certain inflammatory cytokines within the first 3 hours of infection. This increase subsided and returned to normal levels by 12 hours.
  • Susceptible mares also evidenced an increased gene expression of some inflammatory cytokines, but this response was sustained, and their levels remained elevated throughout the 72-hour study period.
  • Endometrial mRNA levels of specific pro-inflammatory cytokines were significantly higher in mares with heavy uterine bacterial growth as compared to mares with no or mild growth.
  • The majority of blood parameters remained unaffected by the intrauterine E. coli infection, with a few exceptions manifested differently in resistant and susceptible mares.

Conclusion

  • The study indicates that the manner in which the gene expression of pro-inflammatory cytokines is regulated is crucial in the body’s response to uterine infections. The early spike in levels, followed by normalization in resistant mares, suggests a well-balanced inflammatory response.
  • Susceptible mares, on the other hand, show prolonged inflammation due to an extended period of elevated inflammatory protein levels. This supports the theory that an imbalance in the gene expression of inflammatory proteins can contribute significantly to the progression of chronic uterine inflammation.

Cite This Article

APA
Christoffersen M, Woodward E, Bojesen AM, Jacobsen S, Petersen MR, Troedsson MH, Lehn-Jensen H. (2012). Inflammatory responses to induced infectious endometritis in mares resistant or susceptible to persistent endometritis. BMC Vet Res, 8, 41. https://doi.org/10.1186/1746-6148-8-41

Publication

ISSN: 1746-6148
NlmUniqueID: 101249759
Country: England
Language: English
Volume: 8
Pages: 41

Researcher Affiliations

Christoffersen, Mette
  • Department of Large Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, Dyrlaegevej 68, Frederiksberg, Copenhagen DK-1870, Denmark. metc@life.ku.dk
Woodward, Elizabeth
    Bojesen, Anders M
      Jacobsen, Stine
        Petersen, Morten R
          Troedsson, Mats Ht
            Lehn-Jensen, Henrik

              MeSH Terms

              • Animals
              • Biopsy / veterinary
              • Cytokines / genetics
              • Cytokines / immunology
              • Endometritis / genetics
              • Endometritis / immunology
              • Endometritis / veterinary
              • Female
              • Gene Expression Profiling / veterinary
              • Gene Expression Regulation
              • Horse Diseases / genetics
              • Horse Diseases / immunology
              • Horses
              • Inflammation / genetics
              • Inflammation / immunology
              • Inflammation / veterinary
              • Least-Squares Analysis
              • RNA, Messenger / chemistry
              • RNA, Messenger / genetics
              • Reverse Transcriptase Polymerase Chain Reaction / veterinary

              References

              This article includes 67 references
              1. Dimock W, Edwards P. Pathology and bacteriology of the reproductive organs of mares in relation to sterility. Kentucky Agricultural Experiment Station Bulletin (Research Bulletin) 1928;286:157u2013237.
              2. Wingfield Digby NJ, Ricketts SW. Results of concurrent bacteriological and cytological examinations of the endometrium of mares in routine stud farm practice 1978-1981.. J Reprod Fertil Suppl 1982;32:181-5.
                pubmed: 6962852
              3. Adams GP, Kastelic JP, Bergfelt DR, Ginther OJ. Effect of uterine inflammation and ultrasonically-detected uterine pathology on fertility in the mare.. J Reprod Fertil Suppl 1987;35:445-54.
                pubmed: 3316644
              4. Hughes J, Loy R. Investigations on the effect of intrauterine inoculations of Streptococcus zooepidemicus in the mare. Proc 15th Ann Conv Am Assoc Eq Pract. 1969. pp. 289u2013292.
              5. Peterson FB, McFeely RA, David JSE. Studies on the pathogenesis of endometritis in the mare. Proc 15th Ann Conv Am Assoc Eq Pract. 1969. pp. 279u2013287.
              6. Troedsson MH. Breeding-induced endometritis in mares.. Vet Clin North Am Equine Pract 2006 Dec;22(3):705-12.
                doi: 10.1016/j.cveq.2006.07.003pubmed: 17129798google scholar: lookup
              7. Kotilainen T, Huhtinen M, Katila T. Sperm-induced leukocytosis in the equine uterus.. Theriogenology 1994 Feb 2;41(3):629-36.
                doi: 10.1016/0093-691X(94)90173-Gpubmed: 16727418google scholar: lookup
              8. Troedsson MHT, Crabo BG, Ibrahim N, Scott M, Ing M. Mating-induced endometritis: mechanisms, clinical importance and consequences [abstract] Proc Am Assoc Equine Pract. 1994;41:11u201312.
              9. Christoffersen M, Baagoe CD, Jacobsen S, Bojesen AM, Petersen MR, Lehn-Jensen H. Evaluation of the systemic acute phase response and endometrial gene expression of serum amyloid A and pro- and anti-inflammatory cytokines in mares with experimentally induced endometritis.. Vet Immunol Immunopathol 2010 Nov 15;138(1-2):95-105.
                doi: 10.1016/j.vetimm.2010.07.011pubmed: 20728224google scholar: lookup
              10. Nash DM, Sheldon IM, Herath S, Lane EA. Markers of the uterine innate immune response of the mare.. Anim Reprod Sci 2010 May;119(1-2):31-9.
              11. Fumuso E, Giguu00e8re S, Wade J, Rogan D, Videla-Dorna I, Bowden RA. Endometrial IL-1beta, IL-6 and TNF-alpha, mRNA expression in mares resistant or susceptible to post-breeding endometritis. Effects of estrous cycle, artificial insemination and immunomodulation.. Vet Immunol Immunopathol 2003 Nov 15;96(1-2):31-41.
                doi: 10.1016/S0165-2427(03)00137-5pubmed: 14522132google scholar: lookup
              12. Fumuso EA, Aguilar J, Giguu00e8re S, Rivulgo M, Wade J, Rogan D. Immune parameters in mares resistant and susceptible to persistent post-breeding endometritis: effects of immunomodulation.. Vet Immunol Immunopathol 2007 Jul 15;118(1-2):30-9.
                doi: 10.1016/j.vetimm.2007.04.009pubmed: 17559943google scholar: lookup
              13. Troedsson MHT. Proc Soc Theriogenology. San Antonio, TX; 1995. Uterine response to semen deposition in the mare; pp. 130u2013135.
              14. Asbury AC. Uterine defense mechanisms in the mare: The use of intrauterine plasma in the management of endometritis.. Theriogenology 1984 Feb;21(2):387-93.
                pubmed: 16725888doi: 10.1016/0093-691x(84)90423-0google scholar: lookup
              15. Widders PR, Stokes CR, David JS, Bourne FJ. Quantitation of the immunoglobulins in reproductive tract secretions of the mare.. Res Vet Sci 1984 Nov;37(3):324-30.
                pubmed: 6522826
              16. Evans MJ, Hamer JM, Gason LM, Graham CS, Asbury AC, Irvine CH. Clearance of bacteria and non-antigenic markers following intra-uterine inoculation into maiden mares: Effect of steroid hormone environment.. Theriogenology 1986 Jul;26(1):37-50.
                doi: 10.1016/0093-691X(86)90110-Xpubmed: 16726168google scholar: lookup
              17. Troedsson MH, Liu IK. Uterine clearance of non-antigenic markers (51Cr) in response to a bacterial challenge in mares potentially susceptible and resistant to chronic uterine infections.. J Reprod Fertil Suppl 1991;44:283-8.
                pubmed: 1795272
              18. Troedsson MH, Liu IK, Ing M, Pascoe J, Thurmond M. Multiple site electromyography recordings of uterine activity following an intrauterine bacterial challenge in mares susceptible and resistant to chronic uterine infection.. J Reprod Fertil 1993 Nov;99(2):307-13.
                doi: 10.1530/jrf.0.0990307pubmed: 8107011google scholar: lookup
              19. Battut I, Colchen S, Fieni F, Tainturier D, Bruyas JF. Success rates when attempting to nonsurgically collect equine embryos at 144, 156 or 168 hours after ovulation.. Equine Vet J Suppl 1997 Dec;(25):60-2.
              20. Orsi NM, Tribe RM. Cytokine networks and the regulation of uterine function in pregnancy and parturition.. J Neuroendocrinol 2008 Apr;20(4):462-9.
              21. Kenney RM, Doig PA. In: Current therapy in Theriogenology: Diagnosis, Treatment, and Prevention of Reproductive Diseases in Small and Large Animals. Marrow D, Marrow D, editor. Vol. 2. Philadelphia: W.B. Saunders; 1986. Equine Endometrial Biopsy; pp. 723u2013729.
              22. Troedsson MHT, Alghamdi AM, Matissen J. Equine seminal plasma protects the fertility of spermatozoa in an inflamed uterine environment. Theriogenology. 2002;58(2-4):453u2013456.
              23. Nielsen JM. Endometritis in the mare: a diagnostic study comparing cultures from swab and biopsy.. Theriogenology 2005 Aug;64(3):510-8.
              24. Jacobsen S, Kjelgaard-Hansen M, Hagbard Petersen H, Jensen AL. Evaluation of a commercially available human serum amyloid A (SAA) turbidometric immunoassay for determination of equine SAA concentrations.. Vet J 2006 Sep;172(2):315-9.
                doi: 10.1016/j.tvjl.2005.04.021pubmed: 15950503google scholar: lookup
              25. Berg LC, Jacobsen S, Dybdahl-Thomsen P. In: Proceedings of the 6th European Colloquium on Acute Phase Proterins. Jacobsen S, Kjelgaard-Hansen M, editor. Copenhagen, Denmark: Samfundslitteratur; 2006. Local production of serum amyloid A in equine articular cartilage and cultured chondrocytes.
              26. Iqbal J, Bird JL, Hollander AP, Bayliss MT. Effect of matrix depleting agents on the expression of chondrocyte metabolism by equine chondrocytes.. Res Vet Sci 2004 Dec;77(3):249-56.
                doi: 10.1016/j.rvsc.2004.04.005pubmed: 15276777google scholar: lookup
              27. Quinlivan M, Nelly M, Prendergast M, Breathnach C, Horohov D, Arkins S, Chiang YW, Chu HJ, Ng T, Cullinane A. Pro-inflammatory and antiviral cytokine expression in vaccinated and unvaccinated horses exposed to equine influenza virus.. Vaccine 2007 Oct 10;25(41):7056-64.
                doi: 10.1016/j.vaccine.2007.07.059pubmed: 17825959google scholar: lookup
              28. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.. Genome Biol 2002 Jun 18;3(7):RESEARCH0034.
              29. Robinson TL, Sutherland IA, Sutherland J. Validation of candidate bovine reference genes for use with real-time PCR.. Vet Immunol Immunopathol 2007 Jan 15;115(1-2):160-5.
                doi: 10.1016/j.vetimm.2006.09.012pubmed: 17074403google scholar: lookup
              30. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.. Methods 2001 Dec;25(4):402-8.
                doi: 10.1006/meth.2001.1262pubmed: 11846609google scholar: lookup
              31. Palm F, Walter I, Budik S, Kolodziejek J, Nowotny N, Aurich C. Influence of different semen extenders and seminal plasma on PMN migration and on expression of IL-1beta, IL-6, TNF-alpha and COX-2 mRNA in the equine endometrium.. Theriogenology 2008 Sep 15;70(5):843-51.
              32. Dinarello CA. Interleukin-1 and interleukin-1 antagonism.. Blood 1991 Apr 15;77(8):1627-52.
                pubmed: 1826616
              33. Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection.. J Immunol 2008 May 1;180(9):5771-7.
                pubmed: 18424693doi: 10.4049/jimmunol.180.9.5771google scholar: lookup
              34. Arend WP, Guthridge CJ. Biological role of interleukin 1 receptor antagonist isoforms.. Ann Rheum Dis 2000 Nov;59 Suppl 1(Suppl 1):i60-4.
                doi: 10.1136/ard.59.suppl_1.i60pmc: PMC1766634pubmed: 11053091google scholar: lookup
              35. Couper KN, Blount DG, Riley EM. IL-10: the master regulator of immunity to infection.. J Immunol 2008 May 1;180(9):5771-7.
                pubmed: 18424693doi: 10.4049/jimmunol.180.9.5771google scholar: lookup
              36. Steel DM, Whitehead AS. The major acute phase reactants: C-reactive protein, serum amyloid P component and serum amyloid A protein.. Immunol Today 1994 Feb;15(2):81-8.
                doi: 10.1016/0167-5699(94)90138-4pubmed: 8155266google scholar: lookup
              37. Raynes JG, Eagling S, McAdam KP. Acute-phase protein synthesis in human hepatoma cells: differential regulation of serum amyloid A (SAA) and haptoglobin by interleukin-1 and interleukin-6.. Clin Exp Immunol 1991 Mar;83(3):488-91.
              38. Herath S, Fischer DP, Werling D, Williams EJ, Lilly ST, Dobson H, Bryant CE, Sheldon IM. Expression and function of Toll-like receptor 4 in the endometrial cells of the uterus.. Endocrinology 2006 Jan;147(1):562-70.
                pmc: PMC2738982pubmed: 16223858doi: 10.1210/en.2005-1113google scholar: lookup
              39. Herath S, Lilly ST, Santos NR, Gilbert RO, Goetze L, Bryant CE, White JO, Cronin J, Sheldon IM. Expression of genes associated with immunity in the endometrium of cattle with disparate postpartum uterine disease and fertility.. Reprod Biol Endocrinol 2009 May 29;7:55.
                doi: 10.1186/1477-7827-7-1pmc: PMC2702306pubmed: 19476661google scholar: lookup
              40. Gabler C, Drillich M, Fischer C, Holder C, Heuwieser W, Einspanier R. Endometrial expression of selected transcripts involved in prostaglandin synthesis in cows with endometritis.. Theriogenology 2009 Apr 1;71(6):993-1004.
              41. LeBlanc MM, Neuwirth L, Asbury AC, Tran T, Mauragis D, Klapstein E. Scintigraphic measurement of uterine clearance in normal mares and mares with recurrent endometritis.. Equine Vet J 1994 Mar;26(2):109-13.
              42. Troedsson MH. Uterine clearance and resistance to persistent endometritis in the mare.. Theriogenology 1999 Aug;52(3):461-71.
                doi: 10.1016/S0093-691X(99)00143-0pubmed: 10734380google scholar: lookup
              43. Baggiolini M, Walz A, Kunkel SL. Neutrophil-activating peptide-1/interleukin 8, a novel cytokine that activates neutrophils.. J Clin Invest 1989 Oct;84(4):1045-9.
                doi: 10.1172/JCI114265pmc: PMC329758pubmed: 2677047google scholar: lookup
              44. Troedsson MHT, Liu IKM, Ing M, Pascoe J. Smooth muscle electrical activity in the oviduct and the effect of oxytocin, PGF2u03b1 and PGE2 on the myometrium and the oviduct of the cycling mare. Biol Reprod Mono. 1995;1:439u2013452.
              45. Tizard I. In: Veterinary Immunology -An introduction. Tizard I, editor. Vol. 8. St. Louis: Saunders Elsevier; 2009. Neutrophils and their products; pp. 28u201340.
              46. Troedsson MH, Liu IK, Thurmond M. Function of uterine and blood-derived polymorphonuclear neutrophils in mares susceptible and resistant to chronic uterine infection: phagocytosis and chemotaxis.. Biol Reprod 1993 Sep;49(3):507-14.
                doi: 10.1095/biolreprod49.3.507pubmed: 8399843google scholar: lookup
              47. Casini-Raggi V, Kam L, Chong YJ, Fiocchi C, Pizarro TT, Cominelli F. Mucosal imbalance of IL-1 and IL-1 receptor antagonist in inflammatory bowel disease. A novel mechanism of chronic intestinal inflammation.. J Immunol 1995 Mar 1;154(5):2434-40.
                pubmed: 7868909
              48. Hinrichs K, Cummings MR, Sertich PL, Kenney RM. Clinical significance of aerobic bacterial flora of the uterus, vagina, vestibule, and clitoral fossa of clinically normal mares.. J Am Vet Med Assoc 1988 Jul 1;193(1):72-5.
                pubmed: 3417532
              49. Nikolakopoulos E, Watson ED. Uterine contractility is necessary for the clearance of intrauterine fluid but not bacteria after bacterial infusion in the mare.. Theriogenology 1999 Aug;52(3):413-23.
                doi: 10.1016/S0093-691X(99)00139-9pubmed: 10734376google scholar: lookup
              50. BROOME AW, WINTER AJ, McNUTT SH, CASIDA LE. Variations in uterine response to experimental infection due to the hormonal state of the ovaries. II. The mobilization of leukocytes and their importance in uterine bactericidal activity.. Am J Vet Res 1960 Jul;21:675-81.
                pubmed: 13804803
              51. Petersen MR, Nielsen JM, Lehm-Jensen H, Bojesen AM. Streptococcus equi subspecies zooepidemicus resides deep in the chronically infected endometrium of mares. Clin Theriogenology. 2009;1:393u2013409.
              52. Gu00fcvenc K, Reilas T, Katila T. Effect of insemination dose and site on uterine inflammatory response of mares.. Theriogenology 2005 Jun;63(9):2504-12.
              53. Watson ED, Stokes CR, Bourne FJ. Effect of exogenous ovarian steroids on the uterine luminal prostaglandins in ovariectomised mares with experimental endometritis.. Res Vet Sci 1988 May;44(3):361-5.
                pubmed: 3165540
              54. Cadario ME, Thatcher MJ, LeBlanc MM. Relationship between prostaglandin and uterine clearance of radiocolloid in the mare. Biol Reprod Mono. 1995;1:495u2013500.
              55. Alghamdi AS, Foster DN, Carlson CS, Troedsson MH. Nitric oxide levels and nitric oxide synthase expression in uterine samples from mares susceptible and resistant to persistent breeding-induced endometritis.. Am J Reprod Immunol 2005 May;53(5):230-7.
              56. Li D, Liu Y, Li Y, Lv Y, Pei X, Guo D. Significance of nitric oxide concentration in plasma and uterine secretes with puerperal endometritis in dairy cows.. Vet Res Commun 2010 Apr;34(4):315-21.
                doi: 10.1007/s11259-010-9355-8pubmed: 20414720google scholar: lookup
              57. Yallampalli C, Garfield RE, Byam-Smith M. Nitric oxide inhibits uterine contractility during pregnancy but not during delivery.. Endocrinology 1993 Oct;133(4):1899-902.
                doi: 10.1210/en.133.4.1899pubmed: 8404632google scholar: lookup
              58. Troedsson MH, deMoraes MJ, Liu IK. Correlations between histologic endometrial lesions in mares and clinical response to intrauterine exposure with Streptococcus zooepidemicus.. Am J Vet Res 1993 Apr;54(4):570-2.
                pubmed: 8484576
              59. Boosman R, Niewold TA, Mutsaers CW, Gruys E. Serum amyloid A concentrations in cows given endotoxin as an acute-phase stimulant.. Am J Vet Res 1989 Oct;50(10):1690-4.
                pubmed: 2508514
              60. Hirvonen J, Eklund K, Teppo AM, Huszenicza G, Kulcsar M, Saloniemi H, Pyu00f6ru00e4lu00e4 S. Acute phase response in dairy cows with experimentally induced Escherichia coli mastitis.. Acta Vet Scand 1999;40(1):35-46.
                pmc: PMC8043231pubmed: 10418194doi: 10.1186/BF03547039google scholar: lookup
              61. Dabrowski R, Wawron W, Kostro K. Changes in CRP, SAA and haptoglobin produced in response to ovariohysterectomy in healthy bitches and those with pyometra.. Theriogenology 2007 Jan 15;67(2):321-7.
              62. Sheldon IM, Noakes DE, Rycroft A, Dobson H. Acute phase protein responses to uterine bacterial contamination in cattle after calving.. Vet Rec 2001 Feb 10;148(6):172-5.
                doi: 10.1136/vr.148.6.172pubmed: 11258722google scholar: lookup
              63. Huzzey JM, Duffield TF, LeBlanc SJ, Veira DM, Weary DM, von Keyserlingk MA. Short communication: Haptoglobin as an early indicator of metritis.. J Dairy Sci 2009 Feb;92(2):621-5.
                doi: 10.3168/jds.2008-1526pubmed: 19164673google scholar: lookup
              64. Jacobsen S, Andersen PH, Toelboell T, Heegaard PM. Dose dependency and individual variability of the lipopolysaccharide-induced bovine acute phase protein response.. J Dairy Sci 2004 Oct;87(10):3330-9.
              65. Regassa F, Noakes DE. Acute phase protein response of ewes and the release of PGFM in relation to uterine involution and the presence of intrauterine bacteria.. Vet Rec 1999 May 1;144(18):502-6.
                doi: 10.1136/vr.144.18.502pubmed: 10358889google scholar: lookup
              66. Hunt JS, Miller L, Roby KF, Huang J, Platt JS, DeBrot BL. Female steroid hormones regulate production of pro-inflammatory molecules in uterine leukocytes.. J Reprod Immunol 1997 Nov 15;35(2):87-99.
                doi: 10.1016/S0165-0378(97)00060-0pubmed: 9421794google scholar: lookup
              67. Pycock J. In: Arthur's Veterinary Reproduction and Obstetrics. Noakes DE, Parkinson TJ, England GCW, editor. Vol. 8. Philadelphia: Saunders; 2001. Infertility in the mare; pp. 577u2013621.

              Citations

              This article has been cited 27 times.
              1. Lange-Consiglio A, Gaspari G, Funghi F, Capra E, Cretich M, Frigerio R, Bosi G, Cremonesi F. Amniotic Mesenchymal-Derived Extracellular Vesicles and Their Role in the Prevention of Persistent Post-Breeding Induced Endometritis.. Int J Mol Sci 2023 Mar 8;24(6).
                doi: 10.3390/ijms24065166pubmed: 36982240google scholar: lookup
              2. Balcu00e3o VM, Belline BG, Silva EC, Almeida PFFB, Baldo Du00c2, Amorim LRP, Oliveira Ju00fanior JM, Vila MMDC, Del Fiol FS. Isolation and Molecular Characterization of Two Novel Lytic Bacteriophages for the Biocontrol of Escherichia coli in Uterine Infections: In Vitro and Ex Vivo Preliminary Studies in Veterinary Medicine.. Pharmaceutics 2022 Oct 30;14(11).
                doi: 10.3390/pharmaceutics14112344pubmed: 36365162google scholar: lookup
              3. Li J, Zhu Y, Mi J, Zhao Y, Holyoak GR, Yi Z, Wu R, Wang Z, Zeng S. Endometrial and vaginal microbiome in donkeys with and without clinical endometritis.. Front Microbiol 2022;13:884574.
                doi: 10.3389/fmicb.2022.884574pubmed: 35979491google scholar: lookup
              4. Jasiu0144ski T, Zdrojkowski u0141, Kautz E, Juszczuk-Kubiak E, Ferreira-Dias G, Domino M. The NF-u03baB-signalling pathway in mare's endometrium infiltrated with the inflammatory cells.. Reprod Domest Anim 2022 Jun;57(6):598-610.
                doi: 10.1111/rda.14099pubmed: 35182075google scholar: lookup
              5. Ibrahim S, Hedia M, Taqi MO, Derbala MK, Mahmoud KGM, Ahmed Y, Sosa AS, Saber YHA, Hasanain MH, Nawito MF, Seidel GE. Extracellular vesicles in low volume uterine lavage and serum: novel and promising biomarker for endometritis in Arabian mares.. BMC Vet Res 2022 Jan 18;18(1):42.
                doi: 10.1186/s12917-022-03137-3pubmed: 35042518google scholar: lookup
              6. Satuu00e9 K, Calvo A, Muu00f1oz A, Fazio E, Medica P. Interrelationship between reproductive hormones and acute phase proteins during estrous cycle and pregnancy in Spanish purebred broodmares.. Vet Anim Sci 2021 Dec;14:100212.
                doi: 10.1016/j.vas.2021.100212pubmed: 34765800google scholar: lookup
              7. Amaral A, Fernandes C, Szu00f3stek-Mioduchowska A, Lukasik K, Rebordu00e3o MR, Pinto-Bravo P, Skarzynski DJ, Ferreira-Dias G. The Inhibitory Effect of Noscapine on the In Vitro Cathepsin G-Induced Collagen Expression in Equine Endometrium.. Life (Basel) 2021 Oct 19;11(10).
                doi: 10.3390/life11101107pubmed: 34685478google scholar: lookup
              8. Rebordu00e3o MR, Amaral A, Fernandes C, Silva E, Lukasik K, Szu00f3stek-Mioduchowska A, Pinto-Bravo P, Galvu00e3o A, Skarzynski DJ, Ferreira-Dias G. Enzymes Present in Neutrophil Extracellular Traps May Stimulate the Fibrogenic PGF(2u03b1) Pathway in the Mare Endometrium.. Animals (Basel) 2021 Sep 6;11(9).
                doi: 10.3390/ani11092615pubmed: 34573581google scholar: lookup
              9. Ibrahim S, Hedia M, Taqi MO, Derbala MK, Mahmoud KGM, Ahmed Y, Ismail S, El-Belely M. Alterations in the Expression Profile of Serum miR-155, miR-223, miR-17, miR-200a, miR-205, as well as Levels of Interleukin 6, and Prostaglandins during Endometritis in Arabian Mares.. Vet Sci 2021 Jun 4;8(6).
                doi: 10.3390/vetsci8060098pubmed: 34199703google scholar: lookup
              10. Weber KS, Wagener K, Blanco M, Bauersachs S, Bollwein H. A comparative analysis of the intrauterine transcriptome in fertile and subfertile mares using cytobrush sampling.. BMC Genomics 2021 May 22;22(1):377.
                doi: 10.1186/s12864-021-07701-3pubmed: 34022808google scholar: lookup
              11. Segabinazzi LGTM, Canisso IF, Podico G, Cunha LL, Novello G, Rosser MF, Loux SC, Lima FS, Alvarenga MA. Intrauterine Blood Plasma Platelet-Therapy Mitigates Persistent Breeding-Induced Endometritis, Reduces Uterine Infections, and Improves Embryo Recovery in Mares.. Antibiotics (Basel) 2021 Apr 23;10(5).
                doi: 10.3390/antibiotics10050490pubmed: 33922743google scholar: lookup
              12. Wojtysiak K, Ryszka W, Stefaniak T, Kru00f3l J, Kozdrowski R. Changes in the Secretion of Anti-Inflammatory Cytokines and Acute-Phase Proteins in the Uterus after Artificial Insemination in the Mare.. Animals (Basel) 2020 Dec 19;10(12).
                doi: 10.3390/ani10122438pubmed: 33352707google scholar: lookup
              13. Schu00f6niger S, Schoon HA. The Healthy and Diseased Equine Endometrium: A Review of Morphological Features and Molecular Analyses.. Animals (Basel) 2020 Apr 5;10(4).
                doi: 10.3390/ani10040625pubmed: 32260515google scholar: lookup
              14. Canisso IF, Segabinazzi LGTM, Fedorka CE. Persistent Breeding-Induced Endometritis in Mares - a Multifaceted Challenge: From Clinical Aspects to Immunopathogenesis and Pathobiology.. Int J Mol Sci 2020 Feb 20;21(4).
                doi: 10.3390/ijms21041432pubmed: 32093296google scholar: lookup
              15. Long A, Nolen-Walston R. Equine Inflammatory Markers in the Twenty-First Century: A Focus on Serum Amyloid A.. Vet Clin North Am Equine Pract 2020 Apr;36(1):147-160.
                doi: 10.1016/j.cveq.2019.12.005pubmed: 32007299google scholar: lookup
              16. Chiba A, Ujiie Y, Aoki T. Relationship between the presence of intrauterine fluid and cervical bacteria in heavy draft mares before and after mating.. J Equine Sci 2019;30(4):75-79.
                doi: 10.1294/jes.30.75pubmed: 31871408google scholar: lookup
              17. Crociati M, Capomaccio S, Mandara MT, Stradaioli G, Sylla L, Monaci M, Cappelli K. Different expression of Defensin-B gene in the endometrium of mares of different age during the breeding season.. BMC Vet Res 2019 Dec 21;15(1):465.
                doi: 10.1186/s12917-019-2215-zpubmed: 31864349google scholar: lookup
              18. Zhu H, Li W, Wang Z, Chen J, Ding M, Han L. TREM-1 deficiency attenuates the inflammatory responses in LPS-induced murine endometritis.. Microb Biotechnol 2019 Nov;12(6):1337-1345.
                doi: 10.1111/1751-7915.13467pubmed: 31365951google scholar: lookup
              19. Witkowska-Piu0142aszewicz OD, u017bmigrodzka M, Winnicka A, Miu015bkiewicz A, Strzelec K, Cywiu0144ska A. Serum amyloid A in equine health and disease.. Equine Vet J 2019 May;51(3):293-298.
                doi: 10.1111/evj.13062pubmed: 30565319google scholar: lookup
              20. Zhang W, Lu X, Wang W, Ding Z, Fu Y, Zhou X, Zhang N, Cao Y. Inhibitory Effects of Emodin, Thymol, and Astragalin on Leptospira interrogans-Induced Inflammatory Response in the Uterine and Endometrium Epithelial Cells of Mice.. Inflammation 2017 Apr;40(2):666-675.
                doi: 10.1007/s10753-017-0513-9pubmed: 28210912google scholar: lookup
              21. Marth CD, Firestone SM, Glenton LY, Browning GF, Young ND, Krekeler N. Oestrous cycle-dependent equine uterine immune response to induced infectious endometritis.. Vet Res 2016 Nov 8;47(1):110.
                doi: 10.1186/s13567-016-0398-xpubmed: 27825391google scholar: lookup
              22. Sikora M, Kru00f3l J, Nowak M, Stefaniak T, Aubertsson G, Kozdrowski R. The usefulness of uterine lavage and acute phase protein levels as a diagnostic tool for subclinical endometritis in Icelandic mares.. Acta Vet Scand 2016 Sep 7;58(1):50.
                doi: 10.1186/s13028-016-0233-4pubmed: 27604098google scholar: lookup
              23. Ru00fctten S, Schusser GF, Abraham G, Schru00f6dl W. Release kinetics of tumor necrosis factor-u03b1 and interleukin-1 receptor antagonist in the equine whole blood.. BMC Vet Res 2016 Jun 17;12(1):117.
                doi: 10.1186/s12917-016-0742-4pubmed: 27316332google scholar: lookup
              24. Vinther AM, Heegaard PM, Skovgaard K, Buhl R, Andreassen SM, Andersen PH. Characterization and differentiation of equine experimental local and early systemic inflammation by expression responses of inflammation-related genes in peripheral blood leukocytes.. BMC Vet Res 2016 Jun 1;12:83.
                doi: 10.1186/s12917-016-0706-8pubmed: 27250718google scholar: lookup
              25. Siemieniuch MJ, Szu00f3stek AZ, Gajos K, Kozdrowski R, Nowak M, Okuda K. Type of Inflammation Differentially Affects Expression of Interleukin 1u03b2 and 6, Tumor Necrosis Factor-u03b1 and Toll-Like Receptors in Subclinical Endometritis in Mares.. PLoS One 2016;11(5):e0154934.
                doi: 10.1371/journal.pone.0154934pubmed: 27152525google scholar: lookup
              26. Marth CD, Young ND, Glenton LY, Noden DM, Browning GF, Krekeler N. Deep sequencing of the uterine immune response to bacteria during the equine oestrous cycle.. BMC Genomics 2015 Nov 14;16:934.
                doi: 10.1186/s12864-015-2139-3pubmed: 26572250google scholar: lookup
              27. Akbar H, Cardoso FC, Meier S, Burke C, McDougall S, Mitchell M, Walker C, Rodriguez-Zas SL, Everts RE, Lewin HA, Roche JR, Loor JJ. Postpartal subclinical endometritis alters transcriptome profiles in liver and adipose tissue of dairy cows.. Bioinform Biol Insights 2014;8:45-63.
                doi: 10.4137/BBI.S13735pubmed: 24578603google scholar: lookup