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Theriogenology2011; 76(7); 1326-1336; doi: 10.1016/j.theriogenology.2011.06.001

Morpho-functional studies regarding the fertility prognosis of mares suffering from equine endometrosis.

Abstract: The aim of the present study was to characterize the morpho-functional features of endometrosis in barren and foaling mares, using both conventional histopathological and immunohistochemical methods. Endometrial biopsy samples were collected during the physiological breeding season from 159 estrous, clinically healthy mares (mean age 12 years), and the quality and degree of endometrosis was histomorphologically defined. The mares were bred and those that foaled were put in the foaling group whereas those that did not foal were placed in the barren group. Foaling mares were then compared with barren mares. Sixty-four percent (101/159) of uterine samples showed varying degrees of endometrosis and were used for this study. The sample population consisted of 51 barren and 50 foaling mares suffering from endometrosis. Expression of steroid hormone receptors (estrogen receptor, progesterone receptor) and endometrial protein secretion patterns (uteroglobin [UG], uterocalin [UC], calbindin(D9k) [CAL], uteroferrin [UF]) was evaluated by immunohistochemistry (barren mares N = 51, foaling mares N = 31). In comparison with unaffected glands, fibrotic glands generally showed a cycle-asynchronous, partially patchy protein expression pattern which is interpreted as a sign of endometrial maldifferentiation within fibrotic areas. In barren mares (N = 51) more than half of biopsy samples (27/51) showed a destructive mostly moderate (20/27) type of endometrosis. In affected glands, staining for UG (17/21) was decreased (P < 0.001). Foaling mares (N = 50) frequently showed a mild, nondestructive endometrosis (35/50). Compared with barren mares, foaling mares had statistically (P < 0.05) more often a cycle-synchronous or increased UG expression pattern within fibrotic glands. Obvious deviations of either UG or UC rarely occurred. Within fibrotic foci, UF often demonstrated a cycle-synchronous or more intense expression pattern in both foaling (28/31) and barren mares (41/51), compared with healthy glands. Mares of both groups showed a cycle-asynchronous staining for estrogen receptor and progesterone receptor in the stromal cells in areas of periglandular fibrosis and the glandular epithelia. These findings indicate that affected areas become independent of the uterine control mechanisms and exhibit specific differentiation dynamics. Immunohistochemical investigations showed that the secretory patterns differ between barren and foaling mares. The findings in this study should be considered as a useful addition to the "classical" Kenney categorization.
Copyright © 2011 Elsevier Inc. All rights reserved.
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Publication Date: 2011-08-23 PubMed ID: 21855986DOI: 10.1016/j.theriogenology.2011.06.001Google Scholar: Lookup
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Summary

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The study investigates the characteristics and implications of endometrosis—a common uterine condition—in mares (female horses), particularly concerning their ability to conceive and give birth to offspring. The researchers utilized histopathological and immunohistochemical techniques on collected endometrial biopsy samples from 159 mares, and analyzed the correlation between the level and type of endometrosis with the mares’ fertility outcome.

Study Method and Population Breakdown

  • The study comprised of first collecting endometrial biopsy samples from 159 estrous (in heat, and therefore ready to conceive), clinically healthy mares within the normal breeding seasons.
  • The mares, which had an average age of 12 years, were categorized based on their ability to foal (give birth) after being bred. Those that gave birth were put in the ‘foaling mares’ group while those who didn’t were classified as ‘barren mares’.
  • The researchers detected endometrosis of varying degrees in 101 of these samples, which were subsequently used for further analysis.
  • The final population for this study involved 51 barren and 50 foaling mares with endometrosis.

Fertility Markers and Their Expression

  • The study also assessed the expression of steroid hormone receptors (specifically estrogen and progesterone receptors) and different endometrial protein secretion patterns, including uteroglobin (UG), uterocalin (UC), calbindin(D9k) (CAL), and uteroferrin (UF) among others. These markers were analyzed by conducting immunohistochemistry on biopsy samples from both barren mares and foaling mares.
  • Fibrotic (scarred or damaged) glands generally showed inconsistent protein expression patterns, possibly indicating endometrial malformation within fibrotic areas. The barren mares’ biopsy samples more than often exhibited a moderate type of destructive endometrosis. The researchers noticed decreased staining for UG in affected glands.
  • Conversely, the foaling mares majorly displayed a milder, nondestructive type of endometrosis. Compared to barren mares, these foaling mares had statistically more frequent or higher UG expression levels within fibrotic glands. Other significant deviations regarding UG or UC were seldom found.

Findings and Relevance to Fertility

  • Both barren and foaling mares exhibited inconsistent staining for estrogen and progesterone receptors in their stromal (connective tissue) cells and glandular epithelia (layers of cells forming the gland’s interior). This shows an independence of the affected areas from uterine control mechanisms, hinting at specific differentiation dynamics within.
  • The immunohistochemistry results demonstrated that secretory patterns varied between barren and foaling mares, hinting this may be a significant factor when investigating or predicting a mare’s fertility state in relation to endometrosis.
  • In conclusion, these findings should be considered as a valuable addition to the traditional Kenney categorization for assessing equine fertility.

Cite This Article

APA
Lehmann J, Ellenberger C, Hoffmann C, Bazer FW, Klug J, Allen WR, Sieme H, Schoon HA. (2011). Morpho-functional studies regarding the fertility prognosis of mares suffering from equine endometrosis. Theriogenology, 76(7), 1326-1336. https://doi.org/10.1016/j.theriogenology.2011.06.001

Publication

Theriogenology
ISSN: 1879-3231
NlmUniqueID: 0421510
Country: United States
Language: English
Volume: 76
Issue: 7
Pages: 1326-1336

Researcher Affiliations

Lehmann, J
  • University of Leipzig, Faculty of Veterinary Medicine, Institute of Pathology, Leipzig, Germany. equinevet@gmx.de
Ellenberger, C
    Hoffmann, C
      Bazer, F W
        Klug, J
          Allen, W R
            Sieme, H
              Schoon, H-A

                MeSH Terms

                • Animals
                • Calbindins
                • Endometriosis / pathology
                • Endometriosis / veterinary
                • Endometrium / metabolism
                • Endometrium / pathology
                • Female
                • Horse Diseases / pathology
                • Horses
                • Immunohistochemistry
                • Infertility, Female / complications
                • Infertility, Female / epidemiology
                • Infertility, Female / veterinary
                • Receptors, Estrogen / metabolism
                • Receptors, Progesterone / metabolism
                • S100 Calcium Binding Protein G / metabolism
                • Uteroglobin / metabolism

                Citations

                This article has been cited 21 times.
                1. Wójtowicz A, Sadowska A, Myszczyński K, Molcan T, Kaczmarek MM, Szóstek-Mioduchowska A. Interleukin-4 changes the transcriptome, ECM-associated components and function of mare endometrial fibroblast: Insights from healthy and fibrotic cells. Cell Tissue Res 2026 Feb 23;403(2).
                  doi: 10.1007/s00441-026-04049-6pubmed: 41729313google scholar: lookup
                2. Sadowska A, Molcan T, Słyszewska M, Skarzynski DJ, Ferreira-Dias G, Szóstek-Mioduchowska A. Transcriptomic Insights into Tumor Necrosis Factor α's Role in the Fibrosis-Related Processes of Equine Endometrial Fibroblasts. Int J Mol Sci 2025 Nov 24;26(23).
                  doi: 10.3390/ijms262311344pubmed: 41373504google scholar: lookup
                3. Wójtowicz A, Sadowska A, Molcan T, Słyszewska M, Drzewiecka EM, Tobolski D, Ferreira-Dias G, Szóstek-Mioduchowska A. Th1 and Th2 cells in equine endometrosis and their interactions with endometrial fibroblasts. Sci Rep 2025 Oct 16;15(1):36263.
                  doi: 10.1038/s41598-025-20152-0pubmed: 41102323google scholar: lookup
                4. Drzewiecka EM, Molcan T, Sadowska A, Piotrowska-Tomala K, Słyszewska M, Dias GF, Skarżyński DJ, Szóstek-Mioduchowska A. The myometrial transcriptome changes in mares with endometrosis. Sci Rep 2025 Jan 25;15(1):3173.
                  doi: 10.1038/s41598-025-86742-0pubmed: 39863666google scholar: lookup
                5. Amaral A, Sadowska A, Cerveira-Pinto M, Kordowitzki P, Skarzynski D, Ferreira-Dias G, Szóstek-Mioduchowska A. Ovarian steroids modulate mRNA expression of ECM associated genes and collagen deposition induced by TGF β1 in equine endometrium in vitro. Sci Rep 2025 Jan 2;15(1):538.
                  doi: 10.1038/s41598-024-84250-1pubmed: 39747561google scholar: lookup
                6. Piotrowska-Tomala KK, Szóstek-Mioduchowska AZ, Drzewiecka EM, Jonczyk AW, Wójtowicz A, Wrobel MH, Ferreira-Dias G, Skarzynski DJ. Prostaglandin pathways in equine myometrium regulations: endometrosis progression. Front Vet Sci 2024;11:1479508.
                  doi: 10.3389/fvets.2024.1479508pubmed: 39735588google scholar: lookup
                7. Zdrojkowski Ł, Pawliński B, Skierbiszewska K, Jasiński T, Domino M. Assessment of Connective Tissue in the Equine Uterus and Cervix: Review of Clinical Impact and Staining Options. Animals (Basel) 2024 Jan 3;14(1).
                  doi: 10.3390/ani14010156pubmed: 38200887google scholar: lookup
                8. Szóstek-Mioduchowska A, Wójtowicz A, Sadowska A, Moza Jalali B, Słyszewska M, Łukasik K, Gurgul A, Szmatoła T, Bugno-Poniewierska M, Ferreira-Dias G, Skarzynski DJ. Transcriptomic profiling of mare endometrium at different stages of endometrosis. Sci Rep 2023 Sep 27;13(1):16263.
                  doi: 10.1038/s41598-023-43359-5pubmed: 37758834google scholar: lookup
                9. Alpoim-Moreira J, Szóstek-Mioduchowska A, Słyszewska M, Rebordão MR, Skarzynski DJ, Ferreira-Dias G. 5-Aza-2'-Deoxycytidine (5-Aza-dC, Decitabine) Inhibits Collagen Type I and III Expression in TGF-β1-Treated Equine Endometrial Fibroblasts. Animals (Basel) 2023 Mar 30;13(7).
                  doi: 10.3390/ani13071212pubmed: 37048467google scholar: lookup
                10. 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
                11. 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
                12. 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
                13. 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
                14. Amaral A, Fernandes C, Szóstek-Mioduchowska A, Lukasik K, Rebordão 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
                15. Bukowska J, Szóstek-Mioduchowska AZ, Kopcewicz M, Walendzik K, Machcińska S, Gawrońska-Kozak B. Adipose-Derived Stromal/Stem Cells from Large Animal Models: from Basic to Applied Science. Stem Cell Rev Rep 2021 Jun;17(3):719-738.
                  doi: 10.1007/s12015-020-10049-ypubmed: 33025392google scholar: lookup
                16. Szóstek-Mioduchowska A, Leciejewska N, Zelmańska B, Staszkiewicz-Chodor J, Ferreira-Dias G, Skarzynski D. Lysophosphatidic acid as a regulator of endometrial connective tissue growth factor and prostaglandin secretion during estrous cycle and endometrosis in the mare. BMC Vet Res 2020 Sep 17;16(1):343.
                  doi: 10.1186/s12917-020-02562-6pubmed: 32943074google scholar: lookup
                17. Schöniger 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
                18. Szóstek-Mioduchowska A, Słowińska M, Pacewicz J, Skarzynski DJ, Okuda K. Matrix metallopeptidase expression and modulation by transforming growth factor-β1 in equine endometrosis. Sci Rep 2020 Jan 24;10(1):1119.
                  doi: 10.1038/s41598-020-58109-0pubmed: 31980722google scholar: lookup
                19. 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
                20. Hanada M, Maeda Y, Oikawa MA. Histopathological characteristics of endometrosis in thoroughbred mares in Japan: results from 50 necropsy cases. J Equine Sci 2014;25(2):45-52.
                  doi: 10.1294/jes.25.45pubmed: 25013358google scholar: lookup
                21. 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.0097889pubmed: 24901368google scholar: lookup
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