FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Animals (Basel) / The Healthy and Diseased Equine Endometrium: A Review of Mor...
Animals : an open access journal from MDPI2020; 10(4); 625; doi: 10.3390/ani10040625

The Healthy and Diseased Equine Endometrium: A Review of Morphological Features and Molecular Analyses.

Abstract: Mares are seasonally polyestric. The breeding season in spring and summer and the winter anestrus are flanked by transitional periods. Endometrial diseases are a frequent cause of subfertility and have an economic impact on the horse breeding industry. They include different forms of endometrosis, endometritis, glandular maldifferentiation, and angiosis. Except for suppurative endometritis, these are subclinical and can only be diagnosed by the microscopic examination of an endometrial biopsy. Endometrosis is characterized by periglandular fibrosis and nonsuppurative endometritis by stromal infiltration with lymphocytes and plasma cells. The pathogenesis of endometrosis and nonsuppurative endometritis is still undetermined. Some mares are predisposed to persistent endometritis; this has likely a multifactorial etiology. Glandular differentiation has to be interpreted under consideration of the season. The presence of endometrial diseases is associated with alterations in the expression of several intra- and extracellular molecular markers. Some of them may have potential to be used as diagnostic biomarkers for equine endometrial health and disease. The aim of this review is to provide an overview on pathomorphological findings of equine endometrial diseases, to outline data on analyses of cellular and molecular mechanisms, and to discuss the impact of these data on reproduction and treatment.
Get Full Text
Publication Date: 2020-04-05 PubMed ID: 32260515PubMed Central: PMC7222714DOI: 10.3390/ani10040625Google 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.
LinkedInCopy
  • Journal Article
  • Review

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.

The research provides a comprehensive review of the morphological features and molecular analyses related to healthy and disease conditions of a horse’s endometrium, with a focus on particular diseases impacting fertility and their potential causes, diagnostic markers, and impacts on reproduction and treatment.

Understanding the Equine Reproductive Cycle

  • The research initially sets the scene by discussing the nature of the equine reproductive cycle, stating that mares are seasonally polyestric, experiencing a breeding season in spring and summer, and winter anestrus surrounded by transitional periods.

Mares’ Endometrial Diseases and Economic Impact

  • The study emphasizes the high frequency of endometrial diseases among mares, leading to subfertility, and consequently causing an economic impact on the horse breeding industry.
  • These diseases include different forms of endometrosis, endometritis, glandular maldifferentiation, and angiosis. Importantly, except for suppurative endometritis, these diseases are subclinical and require microscopic examination of an endometrial biopsy for diagnosis.

Characteristics of Endometrosis and Nonsuppurative Endometritis

  • The research delves into specific diseases like endometrosis and nonsuppurative endometritis. Endometrosis is characterized by periglandular fibrosis, and nonsuppurative endometritis by infiltration of the stroma with lymphocytes and plasma cells.
  • However, the study acknowledges the current gap in understanding regarding the pathogenesis of endometrosis and nonsuppurative endometritis.

Equine Predisposition to Persistent Endometritis

  • Another aspect the research covers is the apparent predisposition of some mares to persistent endometritis, hypothesizing that it likely has a multifactorial etiology. This implies that persistent endometritis could be brought about by a combination of genetic, environmental, and lifestyle factors.

Glandular Differentiation and Seasonality

  • The researchers suggest that glandular differentiation should be interpreted in the context of the season. However, precise connections between seasonality and glandular differentiation are not further specified in the abstract.

Molecular Markers and Diagnostic Biomarkers

  • A major portion of the study explores the role of molecular markers in equine endometrial health and disease. The presence of endometrial diseases is associated with changes in the expression of several intra- and extracellular molecular markers.
  • Importantly, some of these molecular markers may have potential to serve as diagnostic biomarkers for equine endometrial health and disease, enhancing early detection and subsequent treatment of these conditions.

Review Aim

  • The abstract concludes by summarizing the aim of the review, which is primarily to provide an overview of pathomorphological findings of endometrial diseases, analyze cellular and molecular mechanisms, and discuss these data’s implications for reproduction and treatment.

Cite This Article

APA
Schöniger S, Schoon HA. (2020). The Healthy and Diseased Equine Endometrium: A Review of Morphological Features and Molecular Analyses. Animals (Basel), 10(4), 625. https://doi.org/10.3390/ani10040625

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 10
Issue: 4
PII: 625

Researcher Affiliations

Schöniger, Sandra
  • Targos Molecular Pathology GmbH, Germaniastrasse 7, 34119 Kassel, Germany.
Schoon, Heinz-Adolf
  • Institute of Veterinary Pathology, Faculty of Veterinary Medicine, Leipzig University, An den Tierkliniken 33, 04103 Leipzig, Germany.

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 102 references
  1. Kenney RM, Doig PA. Equine endometrial biopsy. 1986;pp. 723–729.
  2. Schoon H-A, Schoon D, Klug E. Uterusbiopsien als Hilfsmittel für Diagnose und Prognose von Fertilitätsstörungen der Stute. Pferdeheilkunde 1992;8:355–362.
    doi: 10.21836/PEM19920603google scholar: lookup
  3. Schoon H-A, Schoon D, Klug E. Die Endometriumbiopsie bei der Stute im klinisch-gynäkologischen Kontext. Pferdeheilkunde 1997;13:453–464.
    doi: 10.21836/PEM19970506google scholar: lookup
  4. Schoon D, Schoon H-A, Klug E. Angioses in the equine endometrium—Pathogenesis and clinical correlations. Pferdeheilkunde 1999;15:541–546.
    doi: 10.21836/PEM19990610google scholar: lookup
  5. Schoon H-A, Schoon D, Wiegandt I, Bartmann C-P, Aupperle H. “Endometrial maldifferentiation”—A clinically significant diagnosis in equine reproduction?. Pferdeheilkunde 1999;15:555–559.
    doi: 10.21836/PEM19990613google scholar: lookup
  6. Schoon HA, Wiegandt I, Schoon D, Aupperle H, Bartmann CP. Functional disturbances in the endometrium of barren mares: a histological and immunohistological study.. J Reprod Fertil Suppl 2000;(56):381-91.
    pubmed: 20681150
  7. Schoon H-A, Schoon D. The category I mare (Kenney and Doig 1986): Expected foaling rate 80–90%—Fact or fiction?. Pferdeheilkunde 2003;19:698–701.
    doi: 10.21836/PEM20030626google scholar: lookup
  8. Buczkowska J, Kozdrowski R, Nowak M, Raś A, Mrowiec J. Endometrosis--significance for horse reproduction, pathogenesis, diagnosis, and proposed therapeutic methods.. Pol J Vet Sci 2014;17(3):547-54.
    doi: 10.2478/pjvs-2014-0083pubmed: 25286671google scholar: lookup
  9. Killisch R, Böttcher D, Theuß T, Edzards H, Martinsson G, Einspanier A, Gottschalk J, Schoon HA. Seasonal or pathological findings? Morphofunctional characteristics of the equine endometrium during the autumn and spring transition.. Reprod Domest Anim 2017 Dec;52(6):1011-1018.
    doi: 10.1111/rda.13016pubmed: 28691249google scholar: lookup
  10. Katila T. Onset and duration of uterine inflammatory response of mares after insemination with fresh semen. Biol. Reprod. 1995;1:515–517.
    doi: 10.1093/biolreprod/52.monograph_series1.515google scholar: lookup
  11. 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
  12. LeBlanc MM, Causey RC. Clinical and subclinical endometritis in the mare: both threats to fertility.. Reprod Domest Anim 2009 Sep;44 Suppl 3:10-22.
    doi: 10.1111/j.1439-0531.2009.01485.xpubmed: 19660076google scholar: lookup
  13. Kilgenstein HJ, Schöniger S, Schoon D, Schoon HA. Microscopic examination of endometrial biopsies of retired sports mares: an explanation for the clinically observed subfertility?. Res Vet Sci 2015 Apr;99:171-9.
    doi: 10.1016/j.rvsc.2015.01.005pubmed: 25639692google scholar: lookup
  14. Mambelli LI, Mattos RC, Winter GH, Madeiro DS, Morais BP, Malschitzky E, Miglino MA, Kerkis A, Kerkis I. Changes in expression pattern of selected endometrial proteins following mesenchymal stem cells infusion in mares with endometrosis.. PLoS One 2014;9(6):e97889.
    doi: 10.1371/journal.pone.0097889pmc: PMC4046935pubmed: 24901368google scholar: lookup
  15. Aupperle H, Steiger K, Reischauer A, Schoon H-A. Ultrastructural and immunohistochemical characterization of the physiological and pathological inactivity of the equine endometrium. Pferdeheilkunde 2003;19:629–632.
    doi: 10.21836/PEM20030611google scholar: lookup
  16. Aupperle H, Schoon D, Schoon HA. Physiological and pathological expression of intermediate filaments in the equine endometrium.. Res Vet Sci 2004 Jun;76(3):249-55.
    doi: 10.1016/j.rvsc.2003.11.003pubmed: 15046960google scholar: lookup
  17. Schöniger S, Gräfe H, Schoon H-A. Beta-defensin is a component of the endometrial immune defence in the mare. Pferdeheilkunde 2013;29:335–346.
    doi: 10.21836/PEM20130307google scholar: lookup
  18. Huth N, Schöniger S, Sieme H, Bartmann C-P, Schoon H-A. Lymphocyte subpopulations in the equine endometrium: A methodical approach with diagnostic implications. Pferdeheilkunde 2014;30:4–14.
    doi: 10.21836/PEM20140101google scholar: lookup
  19. Rebordão MR, Galvão A, Szóstek A, Amaral A, Mateus L, Skarzynski DJ, Ferreira-Dias G. Physiopathologic mechanisms involved in mare endometrosis.. Reprod Domest Anim 2014 Oct;49 Suppl 4:82-7.
    doi: 10.1111/rda.12397pubmed: 25277436google scholar: lookup
  20. Klose K, Schoon H-A. Periglandular inflammatory cells in the endometrium of the mare—A physiological defence mechanisms which impacts on the development of endometrosis. Pferdeheilkunde 2016;32:15–23.
    doi: 10.21836/PEM20160102google scholar: lookup
  21. Schöniger S, Böttcher D, Theuß T, Gräfe H, Schoon H-A. New insights into the innate immune defences of the equine endometrium: In situ and in vitro expression pattern of beta-defensin. Pferdeheilkunde 2016;32:4–14.
    doi: 10.21836/PEM20160101google scholar: lookup
  22. Rudolph N, Schoon H-A, Schöniger S. Immunohistochemical characterization of immune cells in fixed equine endometrial tissue: A diagnostic relevant method. Pferdeheilkunde 2017;33:524–537.
    doi: 10.21836/PEM20170601google scholar: lookup
  23. Schöniger S, Gräfe H, Schoon HA. Expression of Toll-like receptors 2, 4 and 6 in different cell populations of the equine endometrium.. Vet Immunol Immunopathol 2017 Mar;185:7-13.
    doi: 10.1016/j.vetimm.2017.01.002pubmed: 28242004google scholar: lookup
  24. Schöniger S, Böttcher D, Theuß T, Schoon HA. Expression of Toll-like receptors 2, 4 and 6 in equine endometrial epithelial cells: A comparative in situ and in vitro study.. Res Vet Sci 2017 Jun;112:34-41.
    doi: 10.1016/j.rvsc.2017.01.004pubmed: 28119161google scholar: lookup
  25. Schöniger S, Gräfe H, Richter F, Schoon HA. Expression of indoleamine 2,3-dioxygenase 1 as transcript and protein in the healthy and diseased equine endometrium.. Res Vet Sci 2018 Jun;118:278-287.
    doi: 10.1016/j.rvsc.2018.03.001pubmed: 29547726google scholar: lookup
  26. Schöniger S, Gräfe H, Schoon H-A. Innate immunity mechanisms of the equine endometrium—Benefit or harm?. Pferdeheilkunde 2018;34:5–11.
    doi: 10.21836/PEM20180101google scholar: lookup
  27. Bischofberger L, Szewczyk K, Schoon H-A. Unequal glandular differentiation of the equine endometrium—A separate endometrial alteration?. Pferdeheilkunde 2019;35:304–315.
    doi: 10.21836/PEM20190401google scholar: lookup
  28. Minkwitz C, Schoon HA, Zhang Q, Schöniger S. Plasticity of endometrial epithelial and stromal cells-A new approach towards the pathogenesis of equine endometrosis.. Reprod Domest Anim 2019 Jun;54(6):835-845.
    doi: 10.1111/rda.13431pubmed: 30907027google scholar: lookup
  29. Moore RE, Kirwan J, Doherty MK, Whitfield PD. Biomarker discovery in animal health and disease: the application of post-genomic technologies.. Biomark Insights 2007 Jul 10;2:185-96.
    doi: 10.1177/117727190700200040pmc: PMC2717813pubmed: 19662203google scholar: lookup
  30. Califf RM. Biomarker definitions and their applications.. Exp Biol Med (Maywood) 2018 Feb;243(3):213-221.
    doi: 10.1177/1535370217750088pmc: PMC5813875pubmed: 29405771google scholar: lookup
  31. Taylor CR. Introduction to predictive biomarkers: Definitions and characteristics. 2019;pp. 3–18.
  32. Ricketts SW. The technique and clinical appication of endometrial biopsy in the mare.. Equine Vet J 1975 Apr;7(2):102-8.
    doi: 10.1111/j.2042-3306.1975.tb03243.xpubmed: 1140188google scholar: lookup
  33. Kenney RM. Cyclic and pathologic changes of the mare endometrium as detected by biopsy, with a note on early embryonic death.. J Am Vet Med Assoc 1978 Feb 1;172(3):241-62.
    pubmed: 621166
  34. Van Camp SD. Endometrial biopsy of the mare. A review and update.. Vet Clin North Am Equine Pract 1988 Aug;4(2):229-45.
    doi: 10.1016/S0749-0739(17)30639-9pubmed: 3044538google scholar: lookup
  35. Aurich C. Reproductive cycles of horses.. Anim Reprod Sci 2011 Apr;124(3-4):220-8.
    doi: 10.1016/j.anireprosci.2011.02.005pubmed: 21377299google scholar: lookup
  36. Brunckhorst D, Schoon H-A, Bader H, Sieme H. Morphologische, enzyme- and immunhistologische Charakteristika des endometrialen Zyklus der Stute. Fertilität 1991;7:44–51.
  37. Kilgenstein HJ. Die Subfertilität der Sportstute: Welchen Einblick gewährt die histopathologische Untersuchung von Endometriumbioptaten?. 2014.
  38. Strankmeyer O. Morphometrische Untersuchungen am Endometrium zyklischer und ovariektomierter hormonbehandelter Stuten: Entwicklung eines diagnostischen Verfahrens. 1993.
  39. Watson ED, Skolnik SB, Zanecosky HG. Progesterone and estrogen receptor distribution in the endometrium of the mare.. Theriogenology 1992 Oct;38(4):575-80.
    doi: 10.1016/0093-691X(92)90020-Rpubmed: 16727160google scholar: lookup
  40. Aupperle H, Ozgen SSchoon HA, Schoon D, Hoppen HO, Sieme H, Tannapfel A. Cyclical endometrial steroid hormone receptor expression and proliferation intensity in the mare.. Equine Vet J 2000 May;32(3):228-32.
    doi: 10.2746/042516400776563554pubmed: 10836478google scholar: lookup
  41. Hartt LS, Carling SJ, Joyce MM, Johnson GA, Vanderwall DK, Ott TL. Temporal and spatial associations of oestrogen receptor alpha and progesterone receptor in the endometrium of cyclic and early pregnant mares.. Reproduction 2005 Aug;130(2):241-50.
    doi: 10.1530/rep.1.00596pubmed: 16049162google scholar: lookup
  42. Silva ES, Scoggin KE, Canisso IF, Troedsson MH, Squires EL, Ball BA. Expression of receptors for ovarian steroids and prostaglandin E2 in the endometrium and myometrium of mares during estrus, diestrus and early pregnancy.. Anim Reprod Sci 2014 Dec 30;151(3-4):169-81.
    doi: 10.1016/j.anireprosci.2014.11.001pubmed: 25465360google scholar: lookup
  43. Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, Fitzgibbons PL, Francis G, Goldstein NS, Hayes M, Hicks DG, Lester S, Love R, Mangu PB, McShane L, Miller K, Osborne CK, Paik S, Perlmutter J, Rhodes A, Sasano H, Schwartz JN, Sweep FC, Taube S, Torlakovic EE, Valenstein P, Viale G, Visscher D, Wheeler T, Williams RB, Wittliff JL, Wolff AC. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version).. Arch Pathol Lab Med 2010 Jul;134(7):e48-72.
    pubmed: 20586616doi: 10.5858/134.7.e48google scholar: lookup
  44. Cooke PS, Buchanan DL, Young P, Setiawan T, Brody J, Korach KS, Taylor J, Lubahn DB, Cunha GR. Stromal estrogen receptors mediate mitogenic effects of estradiol on uterine epithelium.. Proc Natl Acad Sci U S A 1997 Jun 10;94(12):6535-40.
    doi: 10.1073/pnas.94.12.6535pmc: PMC21085pubmed: 9177253google scholar: lookup
  45. Kurita T, Lee KJ, Cooke PS, Lydon JP, Cunha GR. Paracrine regulation of epithelial progesterone receptor and lactoferrin by progesterone in the mouse uterus.. Biol Reprod 2000 Apr;62(4):831-8.
    doi: 10.1095/biolreprod62.4.831pubmed: 10727250google scholar: lookup
  46. Cunha GR, Cooke PS, Kurita T. Role of stromal-epithelial interactions in hormonal responses.. Arch Histol Cytol 2004 Dec;67(5):417-34.
    doi: 10.1679/aohc.67.417pubmed: 15781983google scholar: lookup
  47. Chung D, Gao F, Jegga AG, Das SK. Estrogen mediated epithelial proliferation in the uterus is directed by stromal Fgf10 and Bmp8a.. Mol Cell Endocrinol 2015 Jan 15;400:48-60.
    doi: 10.1016/j.mce.2014.11.002pmc: PMC4751583pubmed: 25451979google scholar: lookup
  48. Pierro E, Minici F, Alesiani O, Miceli F, Proto C, Screpanti I, Mancuso S, Lanzone A. Stromal-epithelial interactions modulate estrogen responsiveness in normal human endometrium.. Biol Reprod 2001 Mar;64(3):831-8.
    doi: 10.1095/biolreprod64.3.831pubmed: 11207198google scholar: lookup
  49. Crossett B, Suire S, Herrler A, Allen WR, Stewart F. Transfer of a uterine lipocalin from the endometrium of the mare to the developing equine conceptus.. Biol Reprod 1998 Sep;59(3):483-90.
    doi: 10.1095/biolreprod59.3.483pubmed: 9716544google scholar: lookup
  50. Stewart F, Gerstenberg C, Suire S, Allen WR. Immunolocalization of a novel protein (P19) in the endometrium of fertile and subfertile mares.. J Reprod Fertil Suppl 2000;(56):593-9.
    pubmed: 20681174
  51. Hoffmann C, Bazer FW, Klug J, Aupperle H, Ellenberger C, Özgen S, Schoon D, Schoon H-A. Immunohistochemical and histochemical identification of proteins and carbohydrates in the equine endometrium: Reaction patterns in the cycling mare. Pferdeheilkunde 2009;25:212–219.
    doi: 10.21836/PEM20090303google scholar: lookup
  52. Suire S, Stewart F, Beauchamp J, Kennedy MW. Uterocalin, a lipocalin provisioning the preattachment equine conceptus: fatty acid and retinol binding properties, and structural characterization.. Biochem J 2001 Jun 1;356(Pt 2):369-76.
    doi: 10.1042/bj3560369pmc: PMC1221847pubmed: 11368763google scholar: lookup
  53. Bramer SA, Macedo A, Klein C. Hexokinase 2 drives glycogen accumulation in equine endometrium at day 12 of diestrus and pregnancy.. Reprod Biol Endocrinol 2017 Jan 5;15(1):4.
    doi: 10.1186/s12958-016-0223-4pmc: PMC5217302pubmed: 28056994google scholar: lookup
  54. Grimm AL, Schoon HA, Schöniger S. Histopathological features of endometritis eosinophilica in mares.. Histol Histopathol 2017 Nov;32(11):1161-1173.
    pubmed: 28105630doi: 10.14670/hh-11-872google scholar: lookup
  55. Schulz S. Untersuchungen zu Vorkommen, Nachweis und Bedeutung von Mastzellen im Endometrium der Stute. 1997.
  56. Watson ED, Thomson SR. Lymphocyte subsets in the endometrium of genitally normal mares and mares susceptible to endometritis.. Equine Vet J 1996 Mar;28(2):106-10.
    doi: 10.1111/j.2042-3306.1996.tb01600.xpubmed: 8706640google scholar: lookup
  57. Waelchli RO, Winder NC. Mononuclear cell infiltration of the equine endometrium: immunohistochemical studies.. Equine Vet J 1991 Nov;23(6):470-4.
    doi: 10.1111/j.2042-3306.1991.tb03764.xpubmed: 1778168google scholar: lookup
  58. Schöniger S, Gräfe H, Richter F, Helmschrodt C, Schoon H-A. Expression of NOD1 and NOD2 transcripts in the healthy and diseased equine endometrium. Pferdeheilkunde 2017;33:216–222.
    doi: 10.21836/PEM20170301google scholar: lookup
  59. Christoffersen M, Woodward E, Bojesen AM, Jacobsen S, Petersen MR, Troedsson MH, Lehn-Jensen H. Inflammatory responses to induced infectious endometritis in mares resistant or susceptible to persistent endometritis.. BMC Vet Res 2012 Mar 29;8:41.
    doi: 10.1186/1746-6148-8-41pmc: PMC3368729pubmed: 22458733google scholar: lookup
  60. Woodward EM, Christoffersen M, Campos J, Betancourt A, Horohov D, Scoggin KE, Squires EL, Troedsson MH. Endometrial inflammatory markers of the early immune response in mares susceptible or resistant to persistent breeding-induced endometritis.. Reproduction 2013 Mar 1;145(3):289-96.
    doi: 10.1530/REP-12-0452pubmed: 23580950google scholar: lookup
  61. Constantine VS. A combined tissue stain for the selective staining of collagen, elastic fibers and acidic carbohydrates.. J Invest Dermatol 1969 Apr;52(4):353-6.
    doi: 10.1038/jid.1969.60pubmed: 4180701google scholar: lookup
  62. Ebert A, Schoon D, Schoon H-A. Age-related endometrial alterations in mares—biopsy findings of the last 20 years. 2014;pp. 230–232.
  63. Alimi Y, Iwanaga J, Loukas M, Tubbs RS. The Clinical Anatomy of Endometriosis: A Review.. Cureus 2018 Sep 25;10(9):e3361.
    doi: 10.7759/cureus.3361pmc: PMC6257623pubmed: 30510871google scholar: lookup
  64. Hoffmann C, Ellenberger C, Mattos RC, Aupperle H, Dhein S, Stief B, Schoon HA. The equine endometrosis: new insights into the pathogenesis.. Anim Reprod Sci 2009 Apr;111(2-4):261-78.
    doi: 10.1016/j.anireprosci.2008.03.019pubmed: 18468817google scholar: lookup
  65. Lehmann J, Ellenberger C, Hoffmann C, Bazer FW, Klug J, Allen WR, Sieme H, Schoon HA. Morpho-functional studies regarding the fertility prognosis of mares suffering from equine endometrosis.. Theriogenology 2011 Oct 15;76(7):1326-36.
    doi: 10.1016/j.theriogenology.2011.06.001pubmed: 21855986google scholar: lookup
  66. Hoffmann C, Bazer FW, Klug J, Aupperle H, Ellenberger C, Schoon HA. Immunohistochemical and histochemical identification of proteins and carbohydrates in the equine endometrium Expression patterns for mares suffering from endometrosis.. Theriogenology 2009 Jan 15;71(2):264-74.
    doi: 10.1016/j.theriogenology.2008.07.008pubmed: 18762329google scholar: lookup
  67. Rebordão MR, Amaral A, Lukasik K, Szóstek-Mioduchowska A, Pinto-Bravo P, Galvão A, Skarzynski DJ, Ferreira-Dias G. Constituents of neutrophil extracellular traps induce in vitro collagen formation in mare endometrium.. Theriogenology 2018 Jun;113:8-18.
    pubmed: 29452855doi: 10.1016/j.theriogenology.2018.02.001google scholar: lookup
  68. Szóstek-Mioduchowska AZ, Lukasik K, Skarzynski DJ, Okuda K. Effect of transforming growth factor -β1 on α-smooth muscle actin and collagen expression in equine endometrial fibroblasts.. Theriogenology 2019 Jan 15;124:9-17.
    doi: 10.1016/j.theriogenology.2018.10.005pubmed: 30321755google scholar: lookup
  69. Rebordão MR, Carneiro C, Alexandre-Pires G, Brito P, Pereira C, Nunes T, Galvão A, Leitão A, Vilela C, Ferreira-Dias G. Neutrophil extracellular traps formation by bacteria causing endometritis in the mare.. J Reprod Immunol 2014 Dec;106:41-9.
    pubmed: 25218891doi: 10.1016/j.jri.2014.08.003google scholar: lookup
  70. Woodward EM, Christoffersen M, Campos J, Horohov DW, Scoggin KE, Squires E, Troedsson MH. An investigation of uterine nitric oxide production in mares susceptible and resistant to persistent breeding-induced endometritis and the effects of immunomodulation.. Reprod Domest Anim 2013 Aug;48(4):554-61.
    doi: 10.1111/rda.12124pubmed: 23228000google scholar: lookup
  71. Kabisch J, Klose K, Schoon H-A. Endometrial biopsies of old mares—What to expect?!. Pferdeheilkunde 2019;35:211–219.
    doi: 10.21836/PEM20190302google scholar: lookup
  72. Wittenbrink MW, Hoelzle K, Hoelzle LE. What’s new in the bacteriology of the mare’s genital tract. Pferdeheilkunde 2008;24:53–55.
    doi: 10.21836/PEM20080111google scholar: lookup
  73. Petersen MR, Skive B, Christoffersen M, Lu K, Nielsen JM, Troedsson MH, Bojesen AM. Activation of persistent Streptococcus equi subspecies zooepidemicus in mares with subclinical endometritis.. Vet Microbiol 2015 Aug 31;179(1-2):119-25.
    doi: 10.1016/j.vetmic.2015.06.006pubmed: 26123371google scholar: lookup
  74. Christoffersen M, Troedsson M. Inflammation and fertility in the mare.. Reprod Domest Anim 2017 Aug;52 Suppl 3:14-20.
    doi: 10.1111/rda.13013pubmed: 28815848google scholar: lookup
  75. Tunón A-M, Katila T, Magnusson U, Nummijärvi A, Rodriguez-Martinez H. T-cell distribution in two different segments of the equine endometrium 6 and 48 hours after insemination.. Theriogenology 2000 Oct 1;54(6):835-41.
    doi: 10.1016/S0093-691X(00)00395-2pubmed: 11097038google scholar: lookup
  76. Slusher SH, Freeman KP, Roszel JF. Eosinophils in equine uterine cytology and histology specimens.. J Am Vet Med Assoc 1984 Mar 15;184(6):665-70.
    pubmed: 6539323
  77. Klug E, Bartmann CP, Schöning A, Schoon D, Schoon H-A. Auswirkung einer Progestagen-Langzeit-Applikation auf Sexualzyklus und Endometrium des Pferdes—Zwei Seiten einer therapeutischen Medaille. Pferdeheilkunde 1997;13:490–498.
    doi: 10.21836/PEM19970511google scholar: lookup
  78. Ellenberger C, Schoon D, Schoon H-A. Außergewöhnliche Befunde bei der Untersuchung von Uterusbiopsien der Stute. Pferdeheilkunde 2006;22:171–176.
    doi: 10.21836/PEM20060210google scholar: lookup
  79. Fumuso EA, Aguilar J, Giguère 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
  80. Häfner I, Schoon H-A, Schoon D, Aupperle H. Glanduläre Differenzierungsstörungen im Endometrium der Stute—Lichtmikroskopische und immunhistologische Untersuchungen. Pferdeheilkunde 2001;17:103–110.
    doi: 10.21836/PEM20010201google scholar: lookup
  81. Ellenberger C, Aupperle H, Bartmann C-P, Hoppen H-O, Schoon D, Schoon H-A. Endometrial maldifferentiation caused by ovarian disorders in the mare—morphological and immunohistochemical studies. Theriogenology 2002;58:499–502.
  82. Ellenberger C, Bartmann C-P, Klug E, Hoppen H-O, Hoffmann C, Bazer FW, Klug J, Allen WR, Schoon D, Schoon H-A. Immunohistochemical characterization of equine endometrial maldifferentiation with special emphasis on uterine secretory proteins. 2005;pp. 13–15.
  83. Grüninger B, Schoon HA, Schoon D, Menger S, Klug E. Incidence and morphology of endometrial angiopathies in mares in relationship to age and parity.. J Comp Pathol 1998 Oct;119(3):293-309.
    doi: 10.1016/S0021-9975(98)80051-0pubmed: 9807730google scholar: lookup
  84. Ludwig S, Schoon D, Aupperle H, von Reiswitz A, Schoon H-A. Angiopathies in the equine endometrial biopsy—A marker for extrauterine vascular lesions?. Pferdeheilkunde 2001;17:608–614.
    doi: 10.21836/PEM20010614google scholar: lookup
  85. Aupperle H, Hasenbein I, Ellenberger C, Ludwig S, Schoon D, Schoon H-A. Histopathological findings in ovarian vessels, in comparison to alterations in extraovarian, extrauterine and uterine vessels in the mare. Pferdeheilkunde 2003;19:589–594.
    doi: 10.21836/PEM20030603google scholar: lookup
  86. Agnew DW, MacLachlan NJ. Tumors of the genital system. 2016;pp. 689–722.
  87. Gunson DE, Gillette DM, Beech J, Orsini J. Endometrial adenocarcinoma in a mare.. Vet Pathol 1980 Nov;17(6):776-80.
    doi: 10.1177/030098588001700615pubmed: 7423833google scholar: lookup
  88. Chaffin MK, Fuentealba IC, Schmitz DG, Read WK. Endometrial adenocarcinoma in a mare.. Cornell Vet 1990 Jan;80(1):65-73.
    pubmed: 2403426
  89. Thompson R, Armién AG, Rasmussen JM, Wolf TM. Uterine adenocarcinoma in a Przewalski's wild horse (Equus ferus przewalskii).. J Zoo Wildl Med 2014 Jun;45(2):441-5.
    doi: 10.1638/2013-0200R1.1pubmed: 25000717google scholar: lookup
  90. Lopez C, Ciccarelli M, Gold JR, Tibary A. Uterine adenocarcinoma in Quarter horse mare. Equine Vet. Educ. 2017;30:640–644.
    doi: 10.1111/eve.12795google scholar: lookup
  91. Govaere J, Maes S, Saey V, Blancke W, Hoogewijs M, Deschauwer C, Smits K, Roels K, Vercauteren G, de Kruif A. Uterine fibrosarcoma in a Warmblood mare.. Reprod Domest Anim 2011 Jun;46(3):564-6.
    doi: 10.1111/j.1439-0531.2010.01694.xpubmed: 21545654google scholar: lookup
  92. Freeman SL, England GC, Bjornson S, Smith RK. Uterine T cell lymphoma in a mare, with multicentric involvement.. Vet Rec 1997 Oct 11;141(15):391-3.
    doi: 10.1136/vr.141.15.391pubmed: 9364708google scholar: lookup
  93. Canisso IF, Pinn TL, Gerdin JA, Ollivett TL, Buckles EL, Schweizer CM, Ainsworth DM. B-cell multicentric lymphoma as a probable cause of abortion in a Quarter horse broodmare.. Can Vet J 2013 Mar;54(3):288-91.
    pmc: PMC3573638pubmed: 23997268
  94. Claes A, Ball BA, Liu IKM, Vaughan B, Highland MA, Brown JA. Uterine B cell lymphoma in a mare. Equine Vet. Educ. 2015;27:e5–Ce8.
    doi: 10.1111/j.2042-3292.2012.00431.xgoogle scholar: lookup
  95. Yamini B, Borg L. Endometrial polyps and endometritis in a thoroughbred filly.. J Vet Diagn Invest 1994 Oct;6(4):496-8.
    doi: 10.1177/104063879400600419pubmed: 7858034google scholar: lookup
  96. Hamir AN, Hunt PR, Kenney RM. Hyperplastic endometrial polyps in a two-year-old filly.. Vet Pathol 1989 Mar;26(2):185-7.
    doi: 10.1177/030098588902600216pubmed: 2711576google scholar: lookup
  97. Allen WR, Stewart F. Equine placentation.. Reprod Fertil Dev 2001;13(7-8):623-34.
    doi: 10.1071/RD01063pubmed: 11999314google scholar: lookup
  98. Alghamdi A, Troedsson MH, Laschkewitsch T, Xue JL. Uterine secretion from mares with post-breeding endometritis alters sperm motion characteristics in vitro.. Theriogenology 2001 Mar 1;55(4):1019-28.
    doi: 10.1016/S0093-691X(01)00462-9pubmed: 11291908google scholar: lookup
  99. Troedsson MH, Desvousges A, Alghamdi AS, Dahms B, Dow CA, Hayna J, Valesco R, Collahan PT, Macpherson ML, Pozor M, Buhi WC. Components in seminal plasma regulating sperm transport and elimination.. Anim Reprod Sci 2005 Oct;89(1-4):171-86.
    doi: 10.1016/j.anireprosci.2005.07.005pubmed: 16102920google scholar: lookup
  100. Gilbert RO. The effects of endometritis on the establishment of pregnancy in cattle.. Reprod Fertil Dev 2011;24(1):252-7.
    doi: 10.1071/RD11915pubmed: 22394966google scholar: lookup
  101. Ferris RA, Frisbie DD, McCue PM. Use of mesenchymal stem cells or autologous conditioned serum to modulate the inflammatory response to spermatozoa in mares.. Theriogenology 2014 Jul 1;82(1):36-42.
    doi: 10.1016/j.theriogenology.2014.02.015pubmed: 24681213google scholar: lookup
  102. Rink BE, Amilon KR, Esteves CL, French HM, Watson E, Aurich C, Donadeu FX. Isolation and characterization of equine endometrial mesenchymal stromal cells.. Stem Cell Res Ther 2017 Jul 12;8(1):166.
    doi: 10.1186/s13287-017-0616-0pmc: PMC5506676pubmed: 28701175google scholar: lookup

Citations

This article has been cited 12 times.
  1. Hallman I, Karikoski N, Kareskoski M. The effects of obesity and insulin dysregulation on mare reproduction, pregnancy, and foal health: a review.. Front Vet Sci 2023;10:1180622.
    doi: 10.3389/fvets.2023.1180622pubmed: 37152686google scholar: lookup
  2. Mohamed RH, Yousef NA, Awad M, Mohamed RS, Ali F, Hussein HA, Wehrend A. The relationship between ovarian hormones and mast cell distribution in the ovaries of dromedary camel (Camelus dromedaries) during the follicular wave.. Vet World 2023 Feb;16(2):309-316.
    doi: 10.14202/vetworld.2023.309-316pubmed: 37041993google scholar: lookup
  3. Zdrojkowski Ł, Jasiński T, Ferreira-Dias G, Pawliński B, Domino M. The Role of NF-κB in Endometrial Diseases in Humans and Animals: A Review.. Int J Mol Sci 2023 Feb 2;24(3).
    doi: 10.3390/ijms24032901pubmed: 36769226google scholar: lookup
  4. Alpoim-Moreira J, Fernandes C, Pimenta J, Bliebernicht M, Rebordão MR, Castelo-Branco P, Szóstek-Mioduchowska A, Skarzynski DJ, Ferreira-Dias G. Metallopeptidades 2 and 9 genes epigenetically modulate equine endometrial fibrosis.. Front Vet Sci 2022;9:970003.
    doi: 10.3389/fvets.2022.970003pubmed: 36032279google scholar: lookup
  5. Jasiński T, Zdrojkowski Ł, Ferreira-Dias G, Kautz E, Juszczuk-Kubiak E, Domino M. Molecular Mechanism of Equine Endometrosis: The NF-κB-Dependent Pathway Underlies the Ovarian Steroid Receptors' Dysfunction.. Int J Mol Sci 2022 Jul 1;23(13).
    doi: 10.3390/ijms23137360pubmed: 35806363google scholar: lookup
  6. Smieszek A, Marcinkowska K, Pielok A, Sikora M, Valihrach L, Carnevale E, Marycz K. Obesity Affects the Proliferative Potential of Equine Endometrial Progenitor Cells and Modulates Their Molecular Phenotype Associated with Mitochondrial Metabolism.. Cells 2022 Apr 24;11(9).
    doi: 10.3390/cells11091437pubmed: 35563743google scholar: lookup
  7. Katila T, Ferreira-Dias G. Evolution of the Concepts of Endometrosis, Post Breeding Endometritis, and Susceptibility of Mares.. Animals (Basel) 2022 Mar 19;12(6).
    doi: 10.3390/ani12060779pubmed: 35327176google scholar: lookup
  8. Jasiński T, Zdrojkowski Ł, Kautz E, Juszczuk-Kubiak E, Ferreira-Dias G, Domino M. The NF-κB-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
  9. Westendorf J, Wobeser B, Epp T. IIB or not IIB, part 2: assessing inter-rater and intra-rater repeatability of the Kenney-Doig scale in equine endometrial biopsy evaluation.. J Vet Diagn Invest 2022 Mar;34(2):215-225.
    doi: 10.1177/10406387211062866pubmed: 34965793google scholar: lookup
  10. Westendorf J, Wobeser B, Epp T. IIB or not IIB, part 1: retrospective evaluation of Kenney-Doig categorization of equine endometrial biopsies at a veterinary diagnostic laboratory and comparison with published reports.. J Vet Diagn Invest 2022 Mar;34(2):206-214.
    doi: 10.1177/10406387211062207pubmed: 34841986google scholar: lookup
  11. Jasiński T, Zdrojkowski Ł, Kautz E, Juszczuk-Kubiak E, Ferreira-Dias G, Domino M. Equine Endometrosis Pathological Features: Are They Dependent on NF-κB Signaling Pathway?. Animals (Basel) 2021 Nov 4;11(11).
    doi: 10.3390/ani11113151pubmed: 34827882google scholar: lookup
  12. Amaral A, Fernandes C, Morazzo S, Rebordão MR, Szóstek-Mioduchowska A, Lukasik K, Gawronska-Kozak B, Telo da Gama L, Skarzynski DJ, Ferreira-Dias G. The Inhibition of Cathepsin G on Endometrial Explants With Endometrosis in the Mare.. Front Vet Sci 2020;7:582211.
    doi: 10.3389/fvets.2020.582211pubmed: 33195599google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.