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) / Collagen Type III as a Possible Blood Biomarker of Fibrosis ...
Animals : an open access journal from MDPI2022; 12(14); 1854; doi: 10.3390/ani12141854

Collagen Type III as a Possible Blood Biomarker of Fibrosis in Equine Endometrium.

Abstract: Collagen pathological deposition in equine endometrium (endometrosis) is responsible for infertility. Kenney and Doig's endometrial biopsy histopathological classification is the gold standard method for endometrosis evaluation, whereby blood biomarkers identification would be less invasive and could provide additional information regarding endometrosis diagnosis and fertility prognosis. This study aimed to identify blood biomarkers for endometrosis diagnosis (42 mares were used in experiment 1), and fertility assessment (50 mares were used in experiment 2). Reproductive examination, endometrial biopsy histopathological classification (Kenney and Doig) and blood collection were performed. Endometrium and serum collagen type I (COL1) and type III (COL3), and hydroxyproline concentrations were measured (ELISA). Serum COL3 cut-off value of 60.9 ng/mL allowed healthy endometria (category I) differentiation from endometria with degenerative/fibrotic lesions (categories IIA, IIB or III) with 100% specificity and 75.9% sensitivity. This cut-off value enabled category I + IIA differentiation from IIB + III (76% specificity, 81% sensitivity), and category III differentiation from others (65% specificity, 92.3% sensitivity). COL1 and hydroxyproline were not valid as blood biomarkers. Serum COL3 cut-off value of 146 ng/mL differentiated fertile from infertile mares (82.4% specificity, 55.6% sensitivity), and was not correlated with mares' age. Only COL3 may prove useful as a diagnostic aid in mares with endometrial fibrosis and as a fertility indicator.
Get Full Text
Publication Date: 2022-07-21 PubMed ID: 35883401PubMed Central: PMC9311888DOI: 10.3390/ani12141854Google 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

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 explores the use of Collagen Type III as a potential blood biomarker for diagnosing fibrosis in the endometrium of horses, a condition known to cause infertility. This study suggests that testing for this collagen could provide a less invasive method to diagnose fibrosis and assess fertility in mares.

Objective of the Study

  • The main objective of this study was to identify blood biomarkers that could be used for the diagnosis of endometrosis (fibrosis in the equine endometrium) and to assess the fertility of mares.
  • The study aimed to provide a less invasive method of diagnosis and fertility assessment, compared to the current gold standard method – the Kenney and Doig endometrial biopsy histopathological classification.

Methodology of the Study

  • The study was conducted in two separate experiments. Experiment 1 focused on endometrosis diagnosis and used a sample of 42 mares, while experiment 2 evaluated the fertility of 50 mares.
  • Each mare underwent a reproductive examination, endometrial biopsy histopathological classification, and a blood collection.
  • The researchers measured the concentrations of Collagen type I and Collagen type III, as well as hydroxyproline in both the endometrium and the serum of the mares.

Results and Findings of the Study

  • The study found that a serum Collagen Type III (COL3) cut-off value of 60.9 ng/mL could effectively differentiate healthy endometria from those with degenerative or fibrotic lesions.
  • This cut-off value also made it possible to distinguish between the different severity categories of endometrial condition.
  • However, neither Collagen Type I (COL1) nor hydroxyproline were found to be valid blood biomarkers for endometrosis diagnosis.
  • Furthermore, a serum COL3 cut-off value of 146 ng/mL could differentiate fertile from infertile mares with notable specificity and sensitivity.
  • These findings held true regardless of the age of the mares.

Conclusions of the Study

  • Based on the results of this study, the researchers propose that Collagen Type III could be a useful diagnostic aid for endometrial fibrosis in mares.
  • Coupled with its ability to serve as an indicator of fertility, Collagen Type III may provide an effective, less invasive alternative to the current standard method of diagnosis.

Cite This Article

APA
Alpoim-Moreira J, Fernandes C, Rebordão MR, Costa AL, Bliebernicht M, Nunes T, Szóstek-Mioduchowska A, Skarzynski DJ, Ferreira-Dias G. (2022). Collagen Type III as a Possible Blood Biomarker of Fibrosis in Equine Endometrium. Animals (Basel), 12(14), 1854. https://doi.org/10.3390/ani12141854

Publication

Animals : an open access journal from MDPI
ISSN: 2076-2615
NlmUniqueID: 101635614
Country: Switzerland
Language: English
Volume: 12
Issue: 14
PII: 1854

Researcher Affiliations

Alpoim-Moreira, Joana
  • CIISA-Center for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
  • Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 1300-477 Lisbon, Portugal.
Fernandes, Carina
  • CIISA-Center for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
  • Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 1300-477 Lisbon, Portugal.
Rebordão, Maria Rosa
  • CIISA-Center for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
  • Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 1300-477 Lisbon, Portugal.
  • Polytechnic of Coimbra, Coimbra Agriculture School, Bencanta, 3045-601 Coimbra, Portugal.
Costa, Ana Luísa
  • Embriovet-Prestação de Serviços Veterinários Lda., 2125-348 Muge, Portugal.
Bliebernicht, Miguel
  • Embriovet-Prestação de Serviços Veterinários Lda., 2125-348 Muge, Portugal.
Nunes, Telmo
  • CIISA-Center for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
  • Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 1300-477 Lisbon, Portugal.
Szóstek-Mioduchowska, Anna
  • Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-748 Olsztyn, Poland.
Skarzynski, Dariusz J
  • Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, 10-748 Olsztyn, Poland.
Ferreira-Dias, Graça
  • CIISA-Center for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal.
  • Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 1300-477 Lisbon, Portugal.

Grant Funding

  • UID/CVT/00276/2020; PTDC-CVT-REP-4202-2014; LA/0059/2020/AL4AnimalS / Fundau00e7u00e3o para a Ciu00eancia e Tecnologia
  • Bilateral Polish-Portugal project under NAWA and FCT agreement (2019-2020). / Fundau00e7u00e3o para a Ciu00eancia e Tecnologia (Portugal) and NAWA (Poland)
  • OPUS19 nr 2020/37/B/NZ9/03355 / National Science Center (Poland)

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 55 references
  1. . Proceedings of the John P. Hughes International Workshop on Equine Endometritis. Davis, California, August 1992.. Equine Vet J 1993 May;25(3):184-93.
    pubmed: 8508744doi: 10.1111/j.2042-3306.1993.tb02940.xgoogle scholar: lookup
  2. Schoon HA, 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 HA, Schoon D, Klug E. Die Endometriumbiopsie bei der Stute im klinisch-gynäkologischen Kontext.. Pferdeheilkun-de 1997;13:453–464.
    doi: 10.21836/PEM19970506google scholar: lookup
  4. Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE. Developmental biology of uterine glands.. Biol Reprod 2001 Nov;65(5):1311-23.
    doi: 10.1095/biolreprod65.5.1311pubmed: 11673245google scholar: lookup
  5. Schoon HA, Schoon D. The category I mare (Kenney and Doig 1986): Expected foaling rate 80–90%-Fact or fiction?. Pferde-heilkunde 2003;19:698–701.
    doi: 10.21836/PEM20030626google scholar: lookup
  6. Ebert A, Schoon D, Schoon HA. Age-related endometrial alterations in mares-biopsy findings of the last 20 years.. In: Rackwitz R., Pees M., Aschenbach J.R., Gäbel G., editors. Leipziger Blaue Hefte, 7th Leipzig Veterinary Congress, 8th International Conference on Equine Reproductive Medicine. Volume 2. Lehmanns Media GmbH; Berlin, Germany: 2014. pp. 230–232.
  7. Ricketts SW, Alonso S. The effect of age and parity on the development of equine chronic endometrial disease.. Equine Vet J 1991 May;23(3):189-92.
    doi: 10.1111/j.2042-3306.1991.tb02752.xpubmed: 1884699google scholar: lookup
  8. 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
  9. Aresu L, Benali S, Giannuzzi D, Mantovani R, Castagnaro M, Falomo ME. The role of inflammation and matrix metalloproteinases in equine endometriosis.. J Vet Sci 2012 Jun;13(2):171-7.
    doi: 10.4142/jvs.2012.13.2.171pmc: PMC3386342pubmed: 22705739google scholar: lookup
  10. Raila G. Zur Pathogenese der Endometrose der Stute. Morphologisch-Funktionelle Untersuchungen.. Ph.D. Thesis. University of Leipzig; Leipzig, Germany: 2020.
  11. Evans TJ, Miller MA, Ganjam VK, Niswender KD, Ellersieck MR, Krause WJ, Youngquist RS. Morphometric analysis of endometrial periglandular fibrosis in mares.. Am J Vet Res 1998 Oct;59(10):1209-14.
    pubmed: 9781449
  12. Walter I, Handler J, Reifinger M, Aurich C. Association of endometriosis in horses with differentiation of periglandular myofibroblasts and changes of extracellular matrix proteins.. Reproduction 2001 Apr;121(4):581-6.
    doi: 10.1530/rep.0.1210581pubmed: 11277878google scholar: lookup
  13. 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
  14. Guyot C, Lepreux S, Combe C, Doudnikoff E, Bioulac-Sage P, Balabaud C, Desmoulière A. Hepatic fibrosis and cirrhosis: the (myo)fibroblastic cell subpopulations involved.. Int J Biochem Cell Biol 2006 Feb;38(2):135-51.
    doi: 10.1016/j.biocel.2005.08.021pubmed: 16257564google scholar: lookup
  15. Masseno APB. Avaliação da Fibrose Endometrial e dos Miofibroblastos na Endometroses Ativa e Inativa das Éguas.. Ph.D. Thesis. Faculdade de Medicina Veterinária e Zootecnia, Universidade Estadual Paulista; Botucatu, Brazil: 2012.
  16. Martinez-Hernandez A. Repair, regeneration and fibrosis.. In: Rubin E., Faber J.L., editors. Pathology. 3rd ed. Lippincot-Raven; Philadelphia, PA, USA: 1999.
  17. Bochsler PN, Slauson DO. Inflammation and repair of tissue.. In: Slauson D.O., Cooper B.J., editors. Mechanisms of Disease: A Textbook of Comparative General Pathology. 3rd ed. Mosby; St. Louis, MO, USA: 2002. pp. 140–245.
  18. 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
  19. Kenney RM, Doig PA. Equine endometrial biopsy.. In: Morrow D.A., editor. Current Therapy in Theriogenology 2: Diagnosis, Treatment, and Prevention of Reproductive Diseases in Small and Large Animals. 2nd ed. Saunders WB; Philadelphia, PA, USA: 1986. pp. 723–729.
  20. Flores JM, Rodriguez A, Sanchez J, Gomez-Cuetara C, Ramiro F. Endometrosis in Mares: Incidence of Histopathological Alterations.. Reprod. Dom. Anim. 1995;30:61–65.
    doi: 10.1111/j.1439-0531.1995.tb00606.xgoogle scholar: lookup
  21. Ricketts SW, Barrelet A. A retrospective review of the histopathological features seen in a series of 4241 endometrial biopsy samples collected from UK Thoroughbred mares over a 25 year period.. Pferdeheilkunde 1997;13:525–530.
    doi: 10.21836/PEM19970517google scholar: lookup
  22. Katkiewicz M, Witkowski M, Zajac S. Endometrial biopsy of mares: Visualization of healthy and diseased structure.. Med. Weter. 2007;63:463–466.
  23. Zajac S, Katkiewicz M, Witkowski M, Boryczko Z, Pawlak M. Endometrosis in mares.. Med. Weter. 2008;64:257–261.
  24. Schlafer DH. Equine endometrial biopsy: enhancement of clinical value by more extensive histopathology and application of new diagnostic techniques?. Theriogenology 2007 Aug;68(3):413-22.
    doi: 10.1016/j.theriogenology.2007.04.040pubmed: 17560641google scholar: lookup
  25. Snider TA, Sepoy C, Holyoak GR. Equine endometrial biopsy reviewed: observation, interpretation, and application of histopathologic data.. Theriogenology 2011 Jun;75(9):1567-81.
    doi: 10.1016/j.theriogenology.2010.12.013pubmed: 21356552google scholar: lookup
  26. 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.25.45pmc: PMC4090358pubmed: 25013358google scholar: lookup
  27. Luo Y, Oseini A, Gagnon R, Charles ED, Sidik K, Vincent R, Collen R, Idowu M, Contos MJ, Mirshahi F, Daita K, Asgharpour A, Siddiqui MS, Jarai G, Rosen G, Christian R, Sanyal AJ. An Evaluation of the Collagen Fragments Related to Fibrogenesis and Fibrolysis in Nonalcoholic Steatohepatitis.. Sci Rep 2018 Aug 17;8(1):12414.
    doi: 10.1038/s41598-018-30457-ypmc: PMC6098042pubmed: 30120271google scholar: lookup
  28. Frisbie DD, Ray CS, Ionescu M, Poole AR, Chapman PL, McIlwraith CW. Measurement of synovial fluid and serum concentrations of the 846 epitope of chondroitin sulfate and of carboxy propeptides of type II procollagen for diagnosis of osteochondral fragmentation in horses.. Am J Vet Res 1999 Mar;60(3):306-9.
    pubmed: 10188811
  29. Laverty S, Ionescu M, Marcoux M, Bouré L, Doizé B, Poole AR. Alterations in cartilage type-II procollagen and aggrecan contents in synovial fluid in equine osteochondrosis.. J Orthop Res 2000 May;18(3):399-405.
    doi: 10.1002/jor.1100180311pubmed: 10937626google scholar: lookup
  30. Billinghurst RC, Brama PA, van Weeren PR, Knowlton MS, McIlwraith CW. Evaluation of serum concentrations of biomarkers of skeletal metabolism and results of radiography as indicators of severity of osteochondrosis in foals.. Am J Vet Res 2004 Feb;65(2):143-50.
    doi: 10.2460/ajvr.2004.65.143pubmed: 14974569google scholar: lookup
  31. Frisbie DD, Al-Sobayil F, Billinghurst RC, Kawcak CE, McIlwraith CW. Changes in synovial fluid and serum biomarkers with exercise and early osteoarthritis in horses.. Osteoarthritis Cartilage 2008 Oct;16(10):1196-204.
    doi: 10.1016/j.joca.2008.03.008pubmed: 18442931google scholar: lookup
  32. Gressner OA, Weiskirchen R, Gressner AM. Biomarkers of hepatic fibrosis, fibrogenesis and genetic pre-disposition pending between fiction and reality.. J Cell Mol Med 2007 Sep-Oct;11(5):1031-51.
    doi: 10.1111/j.1582-4934.2007.00092.xpmc: PMC4401271pubmed: 17979881google scholar: lookup
  33. Karsdal MA, Daniels SJ, Holm Nielsen S, Bager C, Rasmussen DGK, Loomba R, Surabattula R, Villesen IF, Luo Y, Shevell D, Gudmann NS, Nielsen MJ, George J, Christian R, Leeming DJ, Schuppan D. Collagen biology and non-invasive biomarkers of liver fibrosis.. Liver Int 2020 Apr;40(4):736-750.
    doi: 10.1111/liv.14390pubmed: 31997561google scholar: lookup
  34. Bruckner P. Suprastructures of extracellular matrices: paradigms of functions controlled by aggregates rather than molecules.. Cell Tissue Res 2010 Jan;339(1):7-18.
    doi: 10.1007/s00441-009-0864-0pubmed: 19756756google scholar: lookup
  35. Karsdal MA, Woodworth T, Henriksen K, Maksymowych WP, Genant H, Vergnaud P, Christiansen C, Schubert T, Qvist P, Schett G, Platt A, Bay-Jensen AC. Biochemical markers of ongoing joint damage in rheumatoid arthritis--current and future applications, limitations and opportunities.. Arthritis Res Ther 2011 Apr 28;13(2):215.
    doi: 10.1186/ar3280pmc: PMC3132026pubmed: 21539724google scholar: lookup
  36. Neto da Silva AC, Costa AL, Teixeira A, Alpoim-Moreira J, Fernandes C, Fradinho MJ, Rebordão MR, Silva E, Ferreira da Silva J, Bliebernicht M, Alexandre-Pires G, Ferreira-Dias G. Collagen and Microvascularization in Placentas From Young and Older Mares.. Front Vet Sci 2021;8:772658.
    doi: 10.3389/fvets.2021.772658pmc: PMC8764314pubmed: 35059454google scholar: lookup
  37. Rosenberg WM, Voelker M, Thiel R, Becka M, Burt A, Schuppan D, Hubscher S, Roskams T, Pinzani M, Arthur MJ. Serum markers detect the presence of liver fibrosis: a cohort study.. Gastroenterology 2004 Dec;127(6):1704-13.
    doi: 10.1053/j.gastro.2004.08.052pubmed: 15578508google scholar: lookup
  38. Tanwar S, Trembling PM, Hogan BJ, Srivastava A, Parkes J, Harris S, Grant P, Nastouli E, Ocker M, Wehr K, Herold C, Neureiter D, Schuppan D, Rosenberg WM. Noninvasive markers of liver fibrosis: on-treatment changes of serum markers predict the outcome of antifibrotic therapy.. Eur J Gastroenterol Hepatol 2017 Mar;29(3):289-296.
    doi: 10.1097/MEG.0000000000000789pubmed: 27906753google scholar: lookup
  39. Metschl S, Reutersberg B, Maegdefessel L, Eckstein H, Pelisek J. Collagen Type I and III in Serum of Patients with Abdominal Aortic Aneurysm: Potential Biomarker of Risk Stratification?. Arterioscler. Thromb. Vasc. Biol. 2019;39:A255.
  40. Ong KL, Chung RWS, Hui N, Festin K, Lundberg AK, Rye KA, Jonasson L, Kristenson M. Usefulness of Certain Protein Biomarkers for Prediction of Coronary Heart Disease.. Am J Cardiol 2020 Feb 15;125(4):542-548.
    doi: 10.1016/j.amjcard.2019.11.016pubmed: 31812227google scholar: lookup
  41. Zannad F, Rossignol P, Iraqi W. Extracellular matrix fibrotic markers in heart failure.. Heart Fail Rev 2010 Jul;15(4):319-29.
    doi: 10.1007/s10741-009-9143-0pubmed: 19404737google scholar: lookup
  42. Ix JH, Biggs ML, Mukamal K, Djousse L, Siscovick D, Tracy R, Katz R, Delaney JA, Chaves P, Rifkin DE, Hughes-Austin JM, Garimella PS, Sarnak MJ, Shlipak MG, Kizer JR. Urine Collagen Fragments and CKD Progression-The Cardiovascular Health Study.. J Am Soc Nephrol 2015 Oct;26(10):2494-503.
    doi: 10.1681/ASN.2014070696pmc: PMC4587692pubmed: 25655067google scholar: lookup
  43. Soylemezoglu O, Wild G, Dalley AJ, MacNeil S, Milford-Ward A, Brown CB, el Nahas AM. Urinary and serum type III collagen: markers of renal fibrosis.. Nephrol Dial Transplant 1997 Sep;12(9):1883-9.
    doi: 10.1093/ndt/12.9.1883pubmed: 9306339google scholar: lookup
  44. Lunelli D, Cirio SM, Leite SC, Camargo CE, Kozicki LE. Collagen types in relation to expression of estradiol and pro-gesterone receptors in equine endometrial fibrosis.. Adv. Biosci. Biotechnol. 2013;4:599–605.
    doi: 10.4236/abb.2013.44078google scholar: lookup
  45. Liu X, Wu H, Byrne M, Krane S, Jaenisch R. Type III collagen is crucial for collagen I fibrillogenesis and for normal cardiovascular development.. Proc Natl Acad Sci U S A 1997 Mar 4;94(5):1852-6.
    doi: 10.1073/pnas.94.5.1852pmc: PMC20006pubmed: 9050868google scholar: lookup
  46. Kuivaniemi H, Tromp G. Type III collagen (COL3A1): Gene and protein structure, tissue distribution, and associated diseases.. Gene 2019 Jul 30;707:151-171.
    doi: 10.1016/j.gene.2019.05.003pmc: PMC6579750pubmed: 31075413google scholar: lookup
  47. Miller EJ, Gay S. The collagens: an overview and update.. Methods Enzymol 1987;144:3-41.
    doi: 10.1016/0076-6879(87)44170-0pubmed: 3306286google scholar: lookup
  48. Badid C, Vincent M, McGregor B, Melin M, Hadj-Aissa A, Veysseyre C, Hartmann DJ, Desmouliere A, Laville M. Mycophenolate mofetil reduces myofibroblast infiltration and collagen III deposition in rat remnant kidney.. Kidney Int 2000 Jul;58(1):51-61.
    doi: 10.1046/j.1523-1755.2000.00140.xpubmed: 10886549google scholar: lookup
  49. Nielsen MJ, Veidal SS, Karsdal MA, Ørsnes-Leeming DJ, Vainer B, Gardner SD, Hamatake R, Goodman ZD, Schuppan D, Patel K. Plasma Pro-C3 (N-terminal type III collagen propeptide) predicts fibrosis progression in patients with chronic hepatitis C.. Liver Int 2015 Feb;35(2):429-37.
    doi: 10.1111/liv.12700pubmed: 25308921google scholar: lookup
  50. Leeming DJ, Dolman G, Nielsen MJ, Karsdal MA, Patel K, Irving W, Guha IN. True collagen type III formation (Pro-C3) is predictive of outcome in HCV patients with advanced liver fibrosis with in the trent study.. J. Hepatol. 2016;64:S719–S720.
    doi: 10.1016/S0168-8278(16)01390-8google scholar: lookup
  51. Gressner OA, Weiskirchen R, Gressner AM. Biomarkers of liver fibrosis: clinical translation of molecular pathogenesis or based on liver-dependent malfunction tests.. Clin Chim Acta 2007 Jun;381(2):107-13.
    doi: 10.1016/j.cca.2007.02.038pubmed: 17399697google scholar: lookup
  52. Carnevale EM, Ginther OJ. Relationships of age to uterine function and reproductive efficiency in mares.. Theriogenology 1992 May;37(5):1101-15.
    doi: 10.1016/0093-691X(92)90108-4pubmed: 16727108google scholar: lookup
  53. Rebordão MR, Amaral A, Lukasik K, Szóstek-Mioduchowska A, Pinto-Bravo P, Galvão A, Skarzynski DJ, Ferreira-Dias G. Impairment of the antifibrotic prostaglandin E(2) pathway may influence neutrophil extracellular traps-induced fibrosis in the mare endometrium.. Domest Anim Endocrinol 2019 Apr;67:1-10.
    doi: 10.1016/j.domaniend.2018.10.004pubmed: 30522057google scholar: lookup
  54. Pinto-Bravo P, Rebordão MR, Amaral A, Fernandes C, Cuello C, Parrilla I, Martínez E, Roberto da Costa RP, Skarzynski DJ, Ferreira-Dias G. Is mare endometrosis linked to oviduct fibrosis?. Pferdeheilkunde Equine Med. 2018;34:43–46.
    doi: 10.21836/PEM20180107google scholar: lookup
  55. Price JS, Jackson B, Eastell R, Goodship AE, Blumsohn A, Wright I, Stoneham S, Lanyon LE, Russell RG. Age related changes in biochemical markers of bone metabolism in horses.. Equine Vet J 1995 May;27(3):201-7.
    doi: 10.1111/j.2042-3306.1995.tb03063.xpubmed: 7556047google scholar: lookup

Citations

This article has been cited 6 times.
  1. 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
  2. Zhou Z, Guo J, Du X, Li H, Xie N, Liu C, He H, Yang L, Cui L, Fu C. Weakly supervised deep multi-instance learning for classification of endometrial lesions on hematoxylin and eosin-stained whole-slide images. PLoS One 2026;21(1):e0340186.
    doi: 10.1371/journal.pone.0340186pubmed: 41481616google scholar: lookup
  3. Sabzpoosh M, Hoveizi E, Gooraninejad S. Isolation and differentiation of endometrial mesenchymal stem cells from Arabian mares. In Vitro Cell Dev Biol Anim 2025 Dec;61(10):1187-1192.
    doi: 10.1007/s11626-025-01103-5pubmed: 41288937google scholar: lookup
  4. Méndez-Pérez L, Wong YS, Ibáñez BO, Martinez-Hormaza I, Rodríguez-Álvarez L, Castro FO. Bidirectional Interaction Between PGE(2)-Preconditioned Mesenchymal Stem Cells and Myofibroblasts Mediates Anti-Fibrotic Effects: A Proteomic Investigation into Equine Endometrial Fibrosis Reversal. Proteomes 2025 Sep 8;13(3).
    doi: 10.3390/proteomes13030041pubmed: 40981201google scholar: lookup
  5. Ferreira-Dias GM, Alpoim-Moreira J, Szóstek-Mioduchowska A, Rebordão MR, Skarzynski DJ. The path to fertility: Current approaches to mare endometritis and endometrosis. Anim Reprod 2024;21(3):e20240070.
    doi: 10.1590/1984-3143-AR2024-0070pubmed: 39286368google scholar: lookup
  6. 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
Subscribe to our newsletter
Join 99,357 horse owners like you who receive our email updates on horse health and nutrition.