{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,16]],"date-time":"2026-02-16T19:50:57Z","timestamp":1771271457874,"version":"3.50.1"},"reference-count":43,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2021,12,8]],"date-time":"2021-12-08T00:00:00Z","timestamp":1638921600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003030","name":"Ag\u00e8ncia de gesti\u00f3 d'Ajuts Universitaris i de Recerca","doi-asserted-by":"publisher","award":["2006 BP-A 10017"],"award-info":[{"award-number":["2006 BP-A 10017"]}],"id":[{"id":"10.13039\/501100003030","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100007404","name":"Finnish Foundation of Veterinary Research","doi-asserted-by":"publisher","award":["not provided"],"award-info":[{"award-number":["not provided"]}],"id":[{"id":"10.13039\/501100007404","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Intrauterine devices (IUDs) are used in mares to suppress oestrous behaviour, but the underlying mechanism is yet to be elucidated. The presence of an embryo or an IUD prevents cyclooxygenase-2 (COX-2) and, subsequently, prostaglandin (PG) release and luteolysis. However, inflammation may also be involved. Endometrial inflammatory markers in uterine lavage fluid were measured on Day 10 (EXP 1, n = 25) and Day 15 (EXP 2, n = 27) after ovulation in inseminated mares, non-pregnant or pregnant, and in mares in which a small plastic sphere had been inserted into the uterus 4 (EXP 1) or 3 days (EXP 2) after ovulation. Uterine lavage fluid samples were analysed for nitric oxide (NO), prostaglandin E2 (PGE2) (only EXP 1), prostaglandin F2\u03b1 (PGF2\u03b1), inhibin A and cytokines, and blood samples for progesterone and oestradiol. On Day 10, the concentration of PGF2\u03b1 was lower (p &lt; 0.05) in the IUD group than in pregnant mares. The concentration of the modulatory cytokine IL-10 was significantly higher in the IUD group in comparison to non-pregnant mares, and inhibin A was significantly higher in IUD mares than in the pregnant counterparts on Day 15. The results suggest that the presence of IUD causes endometrial inflammation which is at a resolution stage on Day 15.<\/jats:p>","DOI":"10.3390\/ani11123493","type":"journal-article","created":{"date-parts":[[2021,12,9]],"date-time":"2021-12-09T21:52:32Z","timestamp":1639086752000},"page":"3493","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Inflammatory Markers in Uterine Lavage Fluids of Pregnant, Non-Pregnant, and Intrauterine Device Implanted Mares on Days 10 and 15 Post Ovulation"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9557-4888","authenticated-orcid":false,"given":"Maria Montserrat","family":"Rivera del Alamo","sequence":"first","affiliation":[{"name":"Department of Animal Medicine and Surgery, Faculty of Veterinary Medicine, Autonomous University of Barcelona, 08193 Bellaterra, Spain"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2548-7700","authenticated-orcid":false,"given":"Tiina","family":"Reilas","sequence":"additional","affiliation":[{"name":"Natural Resources Institute Finland (Luke), 31600 Jokioinen, Finland"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2476-8818","authenticated-orcid":false,"given":"Karolina","family":"Lukasik","sequence":"additional","affiliation":[{"name":"Institute of Animal Reproduction and Food Research, PAS, 10-748 Olsztyn, Poland"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7990-3071","authenticated-orcid":false,"given":"Antonio M.","family":"Galv\u00e3o","sequence":"additional","affiliation":[{"name":"Institute of Animal Reproduction and Food Research, PAS, 10-748 Olsztyn, Poland"},{"name":"Centre for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477 Lisbon, Portugal"},{"name":"Epigenetics Programme, The Babraham Institute, Cambridge CB22 3AT, UK"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2209-340X","authenticated-orcid":false,"given":"Marc","family":"Yeste","sequence":"additional","affiliation":[{"name":"Unit of Cell Biology, Department of Biology, Faculty of Sciences, University of Girona, 17003 Girona, Spain"}]},{"given":"Terttu","family":"Katila","sequence":"additional","affiliation":[{"name":"Department of Production Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, 59511 Saari, Finland"}]}],"member":"1968","published-online":{"date-parts":[[2021,12,8]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"266","DOI":"10.1053\/jevs.2003.75","article-title":"Use of an intra-uterine glass ball protocol to extend luteal function in mares","volume":"23","author":"Nie","year":"2003","journal-title":"J. Eq. Vet. Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"94","DOI":"10.1016\/j.anireprosci.2007.06.010","article-title":"Mechanisms behind intrauterine device-induced luteal persistence in mares","volume":"107","author":"Reilas","year":"2008","journal-title":"An. Reprod. Sci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/j.tvjl.2009.07.013","article-title":"The effect of intra-uterine devices on the reproductive physiology and behavior of pony mares","volume":"186","author":"Argo","year":"2010","journal-title":"Vet. J."},{"key":"ref_4","first-page":"181","article-title":"Prostaglandin release patterns in the mare: Physiological, patho-physiological and therapeutic responses","volume":"27","author":"Neely","year":"1979","journal-title":"J. Reprod. Fertil. Suppl."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1095\/biolreprod.103.020800","article-title":"Expression of key prostaglandin synthases in equine endometrium during late diestrus and early pregnancy","volume":"70","author":"Boerboom","year":"2004","journal-title":"Biol. Reprod."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1016\/j.anireprosci.2018.11.004","article-title":"Cyclooxygenase-2 is inhibited in prolonged luteal maintenance induced by intrauterine devices in mares","volume":"199","author":"Reilas","year":"2018","journal-title":"Anim. Reprod. Sci."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"603","DOI":"10.1016\/0093-691X(83)90180-2","article-title":"Mobility of the early equine conceptus","volume":"19","author":"Ginther","year":"1983","journal-title":"Theriogenology"},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Klohonatz, K.M., Nulton, L.C., Hess, A.M., Bouma, G.J., and Bruemmer, J.E. (2019). The role of embryo contact and focal adhesions during maternal recognition of pregnancy. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0213322"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"629","DOI":"10.1016\/0093-691X(95)00243-2","article-title":"Fertility control using intrauterine devices: An alternative for population control in wild horses","volume":"44","author":"Daels","year":"1995","journal-title":"Theriogenology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1111\/rda.12651","article-title":"Effects of intrauterine devices in mares: A histomorphological and immunohistochemical evaluation of the endometrium","volume":"51","author":"Klein","year":"2016","journal-title":"Reprod. Domest. Anim."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.theriogenology.2021.02.001","article-title":"Effects of intrauterine devices on proteins in the uterine lavage fluid of mares","volume":"165","author":"Katila","year":"2021","journal-title":"Theriogenology"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1530\/jrf.0.1160315","article-title":"Oxytocin administration prolongs luteal function in cyclic mares","volume":"116","author":"Stout","year":"1999","journal-title":"J. Reprod. Fertil."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1530\/rep.0.1230261","article-title":"Prostaglandin E2 and F2\u03b1 production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares","volume":"123","author":"Stout","year":"2002","journal-title":"Reproduction"},{"key":"ref_14","first-page":"S58","article-title":"Intrauterine administration of plant oils inhibits luteolysis in the mare","volume":"121S","author":"Wilsher","year":"2010","journal-title":"An. Reprod. Sci."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"515","DOI":"10.2746\/042516405775314844","article-title":"Effect of seminal plasma on uterine inflammation, contractility and pregnancy rates in mares","volume":"37","author":"Portus","year":"2005","journal-title":"Eq. Vet. J."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1046\/j.1439-0531.2002.00315.x","article-title":"Proteins and enzymes in uterine lavage fluid of postpartum and nonparturient mares","volume":"37","author":"Reilas","year":"2002","journal-title":"Reprod. Dom. An."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1111\/j.2042-3306.1997.tb05102.x","article-title":"Success rates when attempting to nonsurgically collect equine embryos at 144, 156 or 168 h after ovulation","volume":"29","author":"Battut","year":"1997","journal-title":"Equine Vet. J. Suppl."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"872","DOI":"10.1095\/biolreprod.110.088732","article-title":"Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse","volume":"84","author":"Klein","year":"2011","journal-title":"Biol. Reprod."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"874","DOI":"10.1095\/biolreprod.110.085233","article-title":"Microarray analysis of equine endometrium at days 8 and 12 of pregnancy","volume":"83","author":"Merkl","year":"2010","journal-title":"Biol. Reprod."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1111\/j.2042-3306.1987.tb02574.x","article-title":"Concentrations of uterine luminal prostaglandins in mares with acute and persistent endometritis","volume":"19","author":"Watson","year":"1987","journal-title":"Equine Vet. J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1111\/rda.13013","article-title":"Inflammation and fertility in the mare","volume":"52","author":"Christoffersen","year":"2017","journal-title":"Reprod. Dom. Anim."},{"key":"ref_22","first-page":"335","article-title":"Effect of pregnancy and collection technique on prostaglandin F in the uterine lumen of Pony mares","volume":"32","author":"Berglund","year":"1982","journal-title":"J. Reprod. Fertil. Suppl."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1095\/biolreprod25.3.581","article-title":"Prostaglandin F2alpha in the equine endometrium: Steroid modulation and production capacities during the estrous cycle and early pregnancy","volume":"25","author":"Vernon","year":"1981","journal-title":"Biol. Reprod."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"120","DOI":"10.1016\/j.jevs.2013.10.081","article-title":"Auto-paracrine action of prostaglandins E2 and F2\u03b1 in equine corpus luteum","volume":"34","author":"Lukasik","year":"2014","journal-title":"J. Eq. Vet. Sci."},{"key":"ref_25","first-page":"RE12","article-title":"Signal transduction and mechanical stress","volume":"31","year":"2004","journal-title":"Sci. STKE"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1177\/1933719114542023","article-title":"Mechanical signaling in reproductive tissues: Mechanisms and importance","volume":"21","author":"Jorge","year":"2014","journal-title":"Reprod. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1071\/RD08015","article-title":"Actions of nitric oxide donor on prostaglandin production and angiogenic activity in the equine endometrium","volume":"20","author":"Costa","year":"2008","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1111\/j.1600-0897.2005.00270.x","article-title":"Nitric oxide levels and nitric oxide synthase expression in uterine samples from mares susceptible and resistant to persistent breeding-induced endometritis","volume":"53","author":"Alghamdi","year":"2005","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"554","DOI":"10.1111\/rda.12124","article-title":"An investigation of uterine nitric oxide production in mares susceptible and resistant to persistent breeding-induced endometritis and the effects of immunomodulation","volume":"48","author":"Woodward","year":"2013","journal-title":"Reprod. Dom. Anim."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3473","DOI":"10.1073\/pnas.92.8.3473","article-title":"Lipocrotin 1 mediates the inhibition by dexamethasone of the induction by endotoxin of nitric oxide synthase in the rat","volume":"92","author":"Wu","year":"1995","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.repbio.2016.01.003","article-title":"Our understanding of the pathophysiology of equine endometritis with an emphasis on breeding-induced endometritis","volume":"16","author":"Troedsson","year":"2016","journal-title":"Reprod. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"641","DOI":"10.1016\/j.cyto.2011.08.040","article-title":"Macrophage colony stimulating factor and monocyte chemoattractant protein 2 are elevated in intrinsic asthmatics","volume":"56","author":"Dajani","year":"2011","journal-title":"Cytokine"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"528","DOI":"10.1165\/ajrcmb.21.4.3660","article-title":"Expression of monocytes chemotactic protein (MCP)-1, MCP-2, and MCP-3 by human airway smooth-muscle cells. Modulation by corticosteroids and T-helper 2 cytokines","volume":"21","author":"Pype","year":"1999","journal-title":"Am. J. Resp. Cell Mol. Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1144","DOI":"10.1210\/jc.2004-1089","article-title":"Mechanical stretch stimulated interleukin-8 production in endometrial stromal cells: Possible implications in endometrium-related events","volume":"90","author":"Harada","year":"2005","journal-title":"J. Clin. Endorinol. Metab."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1111\/j.1600-065X.2008.00706.x","article-title":"Interleukin-10: New perspectives on an old cytokine","volume":"226","author":"Mosser","year":"2008","journal-title":"Immunol. Rev."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.vetimm.2010.07.011","article-title":"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","volume":"138","author":"Mette","year":"2010","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2485","DOI":"10.1007\/s11033-018-04579-5","article-title":"Expression of interleukins 6 and 10 and population of inflammatory cells in the equine endometrium: Diagnostic implications","volume":"46","author":"Consalter","year":"2019","journal-title":"Mol. Biol. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1007\/s00011-003-1235-z","article-title":"Annexin 1: More than an anti-phopholipase protein","volume":"53","author":"Parente","year":"2004","journal-title":"Inflamm. Res."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"8239258","DOI":"10.1155\/2016\/8239258","article-title":"Annexin A1 and the resolution of inflammation: Modulation of neutrophil recruitment, apoptosis, and clearance","volume":"2016","author":"Sugimoto","year":"2016","journal-title":"J. Immunol. Res."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1002\/(SICI)1098-2795(199708)47:4<363::AID-MRD2>3.0.CO;2-I","article-title":"Equine inhibin\/activin A-subunit mRNA is expressed in the endometrial gland, but not in the trophoblast, during pregnancy","volume":"47","author":"Yamanouchi","year":"1997","journal-title":"Mol. Reprod. Develop."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1210\/en.2005-1183","article-title":"Activin A and Inhibin A differentially regulate human uterine matrix metalloproteinases: Potential interactions during decidualization and trophoblast invasion","volume":"147","author":"Jones","year":"2006","journal-title":"Endocrinology"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1080\/09513590500168399","article-title":"Expression of matrix metalloproteinase-3 in mouse endometrial stromal cells during early pregnancy: Regulation by interleukin-1\u03b1 and tenascin-C","volume":"21","author":"Nishiura","year":"2009","journal-title":"Gynecol. Endocrinol."},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Tobolski, D., Lukasik, K., Bas\u0142awska, A., Skarzynski, D.J., Hostens, M., and Baranski, W. (2021). Prediction of calving to conception interval length using algorithmic analysis of endometrial mRNA expression in bovine. Animals, 11.","DOI":"10.3390\/ani11010236"}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/12\/3493\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:42:55Z","timestamp":1760168575000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/11\/12\/3493"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,12,8]]},"references-count":43,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2021,12]]}},"alternative-id":["ani11123493"],"URL":"https:\/\/doi.org\/10.3390\/ani11123493","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,12,8]]}}}