Changes in the Secretion of Anti-Inflammatory Cytokines and Acute-Phase Proteins in the Uterus after Artificial Insemination in the Mare

Simple Summary Semen deposition into the uterus during mating or artificial insemination induces a rapid inflammatory response, and, in susceptible mares, persistent endometritis can develop. Cytokines are mediators involved in the regulation of the inflammatory process, and acute phase proteins are the most sensitive indicators of the inflammatory process. Therefore, the aim of this research was to determine the secretion of anti-inflammatory cytokines and acute-phase proteins in the uterus before and after artificial insemination in the mare. The obtained results indicate that the status of the mare before artificial insemination has little effect on the response measured shortly after artificial insemination. The presence of intrauterine fluid during estrus is not connected with the inflammation parameters investigated in this study at 7 h post artificial insemination. Detailed examination of the mare’s reproductive tract before and after artificial insemination guarantees high fertility. Abstract The objective of the study was to evaluate the concentrations of interleukin-1 receptor antagonist (IL-1RA), interleukin-10 (IL-10), serum amyloid A (SAA) and haptoglobin (Hp) in uterine lavage fluid before and after artificial insemination (AI). Based on ultrasound examination, mares were divided into: Group 1 (n = 9), no fluid was detected in the uterus during estrus and 7 h after AI; Group 2 (n = 8), no fluid was detected in the uterus during estrus but 7 h after AI fluid was detected in the uterus; Group 3 (n = 8), fluid was detected in the uterus during estrus and also 7 h after AI. In all groups of mares, a significant increase in polymorphonuclear cells (PMN) and a significant increase in IL-1RA and SAA were recorded 7 h after AI. The obtained results show that, regardless of the status of the mare before AI, the endometrial response characterized by PMN influx, and SAA, Hp, IL-1RA and IL-10 production, is similar. The presence of intrauterine fluid during estrus is not connected with PMN influx but can impact uterine IL-1RA production at this time.

[1]  A. Winnicka,et al.  Serum amyloid A in equine health and disease , 2019, Equine veterinary journal.

[2]  E. Scholtz,et al.  Endometrial nitric oxide synthase activity in mares susceptible or resistant to persistent breeding‐induced endometritis and the effect of a specific iNOS inhibitor in vitro , 2018, Reproduction in domestic animals = Zuchthygiene.

[3]  E. Scholtz,et al.  Dose-dependent inhibition of uterine contractility by nitric oxide: A potential mechanism underlying persistent breeding-induced endometritis in the mare. , 2017, Theriogenology.

[4]  K. Okuda,et al.  Type of Inflammation Differentially Affects Expression of Interleukin 1β and 6, Tumor Necrosis Factor-α and Toll-Like Receptors in Subclinical Endometritis in Mares , 2016, PloS one.

[5]  M. Yeste,et al.  Effects on the equine endometrium of cervical occlusion after insemination. , 2016, Theriogenology.

[6]  J. Król,et al.  The usefulness of uterine lavage and acute phase protein levels as a diagnostic tool for subclinical endometritis in Icelandic mares , 2015, Acta Veterinaria Scandinavica.

[7]  M. Christoffersen,et al.  Risk factors associated with uterine fluid after breeding caused by Streptococcus zooepidemicus. , 2015, Theriogenology.

[8]  J. Ziętek,et al.  The concentrations of inflammatory cytokines and acute-phase proteins in the peripheral blood and uterine washings in cows with pyometra. , 2015, Reproduction in domestic animals = Zuchthygiene.

[9]  K. Kostro,et al.  Inflammatory cytokine and acute phase protein concentrations in the peripheral blood and uterine washings of cows with subclinical endometritis in the late postpartum period , 2015, Veterinary Research Communications.

[10]  M. Nowak,et al.  Effects of cycle stage and sampling procedure on interpretation of endometrial cytology in mares. , 2015, Animal reproduction science.

[11]  J. Jeong,et al.  Inflammatory cytokine concentrations in uterine flush and serum samples from dairy cows with clinical or subclinical endometritis. , 2014, Theriogenology.

[12]  T. Orro,et al.  Influence of the uterine inflammatory response after insemination with frozen-thawed semen on serum concentrations of acute phase proteins in mares. , 2014, Animal reproduction science.

[13]  C. Cray,et al.  Haptoglobin Quantitation in Serum Samples from Clinically Normal and Clinically Abnormal Horses , 2014 .

[14]  A. Szóstek,et al.  Impairment of the Interleukin System in Equine Endometrium During the Course of Endometrosis1 , 2013, Biology of reproduction.

[15]  M. Troedsson,et al.  Equine Breeding-Induced Endometritis: A Review , 2013 .

[16]  M. Christoffersen,et al.  An investigation of uterine nitric oxide production in mares susceptible and resistant to persistent breeding-induced endometritis and the effects of immunomodulation. , 2013, Reproduction in domestic animals = Zuchthygiene.

[17]  K. Scoggin,et al.  Endometrial inflammatory markers of the early immune response in mares susceptible or resistant to persistent breeding-induced endometritis. , 2013, Reproduction.

[18]  K. Meade,et al.  Endometrial epithelial cells are potent producers of tracheal antimicrobial peptide and serum amyloid A3 gene expression in response to E. coli stimulation. , 2013, Veterinary immunology and immunopathology.

[19]  M. Christoffersen,et al.  Susceptibility to persistent breeding-induced endometritis in the mare: relationship to endometrial biopsy score and age, and variations between seasons. , 2012, Theriogenology.

[20]  T. Katila,et al.  Post-mating inflammatory responses of the uterus. , 2012, Reproduction in domestic animals = Zuchthygiene.

[21]  S. Jacobsen,et al.  Inflammatory responses to induced infectious endometritis in mares resistant or susceptible to persistent endometritis , 2012, BMC Veterinary Research.

[22]  I. C. Bustamante-Filho,et al.  Is the presence of uterine fluid a reliable indicator of endometrial inflammation , 2012 .

[23]  O. Paciello,et al.  Comparison of the cytobrush, cottonswab, and low-volume uterine flush techniques to evaluate endometrial cytology for diagnosing endometritis in chronically infertile mares. , 2012, Theriogenology.

[24]  K. Kostro,et al.  Serum levels of acute phase proteins: SAA, Hp and progesterone (P4) in mares with early embryonic death. , 2011, Reproduction in domestic animals = Zuchthygiene.

[25]  Christoffersen Mette,et al.  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. , 2010 .

[26]  I. M. Sheldon,et al.  Markers of the uterine innate immune response of the mare. , 2010, Animal reproduction science.

[27]  S. Jacobsen,et al.  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. , 2010, Veterinary immunology and immunopathology.

[28]  Luis Serrano,et al.  Correlation of mRNA and protein in complex biological samples , 2009, FEBS letters.

[29]  C. Cray,et al.  Acute phase response in animals: a review. , 2009, Comparative medicine.

[30]  E. Marcotte,et al.  Global signatures of protein and mRNA expression levelsw , 2009 .

[31]  G. Dolci,et al.  The use of dexamethasone administered to mares at breeding time in the modulation of persistent mating induced endometritis. , 2008, Theriogenology.

[32]  C. Aurich,et al.  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. , 2008, Theriogenology.

[33]  A. Stromberg,et al.  Use of a low-volume uterine flush for diagnosing endometritis in chronically infertile mares. , 2007, Theriogenology.

[34]  D. Rogan,et al.  Immune parameters in mares resistant and susceptible to persistent post-breeding endometritis: effects of immunomodulation. , 2007, Veterinary immunology and immunopathology.

[35]  D. Foster,et al.  Nitric Oxide Levels and Nitric Oxide Synthase Expression in Uterine Samples from Mares Susceptible and Resistant to Persistent Breeding‐induced Endometritis , 2005, American journal of reproductive immunology.

[36]  D. Rogan,et al.  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. , 2003, Veterinary immunology and immunopathology.

[37]  D. Varner,et al.  A practical method for recognizing mares susceptible to post-breeding endometritis. , 2003 .

[38]  R. MacKay Inflammation in horses. , 2000, The Veterinary clinics of North America. Equine practice.

[39]  R. Badolato,et al.  Serum amyloid A is an activator of PMN antimicrobial functions: induction of degranulation, phagocytosis, and enhancement of anti‐Candida activity , 2000, Journal of leukocyte biology.

[40]  M. Troedsson,et al.  Uterine clearance and resistance to persistent endometritis in the mare. , 1999, Theriogenology.

[41]  S. Edwards,et al.  Acute phase proteins in cattle: discrimination between acute and chronic inflammation , 1999, Veterinary Record.

[42]  T. Stefaniak,et al.  Cross reactivities among some mammalian haptoglobins studied by a monoclonal antibody. , 1998, Comparative biochemistry and physiology. Part B, Biochemistry & molecular biology.

[43]  T. Katila,et al.  Intrauterine Fluid Accumulation in Oestrous Mares , 1997, Acta Veterinaria Scandinavica.

[44]  S. Brackenridge,et al.  The human/horse bond and client bereavement in equine practice. 1 , 1996 .

[45]  T. Katila Onset and Duration of Uterine Inflammatory Response of Mares after Insemination with Fresh Semen , 1995 .

[46]  L. Neuwirth,et al.  Scintigraphic measurement of uterine clearance in normal mares and mares with recurrent endometritis. , 1994, Equine veterinary journal.

[47]  G. E. Jones,et al.  Adaptation of the guaiacol (peroxidase) test for haptoglobins to a microtitration plate system. , 1984, Research in veterinary science.