Relationship between bacteria-induced endometritis and subfertility in Peruvian Paso mares
DOI:
https://doi.org/10.20453/stv.v13i2.6823Keywords:
mare, fertility, endometritis, bacterial culture, endometrial cytologyAbstract
The objective of this study was to determine the relationship between enterobacteria-induced endometritis and subfertility in Peruvian Paso mares. A total of 38 cyclic females, aged 5 to 15 years and raised in stud farms in Lima, Cañete, and Chincha, were evaluated. Nineteen mares were assigned to the control group (healthy), and the remaining 19 mares constituted the case group (subfertile). Uterine mucosa samples were collected on day 2 of estrus for bacterial culture and cytology using uterine brushing. Endometritis of varying degrees was diagnosed in 100% of the subfertile mares. Post-mating endometritis (PME), previous antimicrobial treatment, and the number of artificial inseminations per season were factors associated with subfertility. The main bacterial species and genera isolated were Bacillus sp. (36.8%), Staphylococcus sp. (26.3%), Escherichia coli (18.4%), Klebsiella sp. (13.2%), and Citrobacter sp. (7.9%). The presence of positive bacterial cultures was not related to subfertility. The results demonstrate that endometritis, regardless of its etiology, is one of the main factors associated with subfertility in these mares.
Downloads
References
Albihn, A., Båverud, V. y Magnusson, U. (2003). Uterine microbiology and antimicrobial susceptibility in isolated bacteria from mares with fertility problems. Acta Veterinaria Scandinavica, 44(3-4), 121-129. https://doi.org/10.1186/1751-0147-44-121
Barbary, H. A., Abo-ghonema, I. I., El-Bawab, I. E. y Fadel, M. S. (2016). Diagnosis and treatment of bacterial endometritis in arabian mares. Alexandria Journal of Veterinary Sciences, 49(2), 116-125. https://doi.org/10.5455/ajvs.211432
Beltaire, K. A., Cheong, S. H. y Da Silva, M. A. (2012). Retrospective study on equine uterine fungal isolates and antifungal susceptibility patterns (1999-2011). Equine Veterinary Journal, 44(supl. 43), 84-87. https://doi.org/10.1111/j.2042-3306.2012.00608.x
Buczkowska, J., Kozdrowski, R., Nowak, M., Raś, A., Staroniewicz, Z. y Siemieniuch, M. J. (2014). Comparison of the biopsy and cytobrush techniques for diagnosis of subclinical endometritis in mares. Reproductive Biology and Endocrinology, 12, 27. https://doi.org/10.1186/1477-7827-12-27
Canisso, I. F., Segabinazzi, L. G. y Fedorka, C. E. (2020). Persistent breeding-induced endometritis in mares - a multifaceted challenge: From clinical aspects to immunopathogenesis and pathobiology. International Journal of Molecular Sciences, 21(4), 1432. https://doi.org/10.3390/ijms21041432
Card, C. (2005). Post-breeding inflammation and endometrial cytology in mares. Theriogenology, 64(3), 580-588. https://doi.org/10.1016/j.theriogenology.2005.05.041
Cavalieri, S. J. (2005). Manual de pruebas de susceptibilidad antimicrobiana. En M. B. Coyle, (ed.). American Society for Microbiology.
Christoffersen, M., Brandis, L., Samuelsson, J., Bojesen, A. M., Troedsson, M. H. y Petersen, M. R. (2015). Diagnostic double-guarded low-volume uterine lavage in mares. Theriogenology, 83(2), 222-227. https://doi.org/10.1016/j.theriogenology.2014.09.008
Christoffersen, M. y Troedsson, M. H. (2017). Inflammation and fertility in the mare. Reproduction in Domestic Animals, 52(supl.3), 14-20. https://doi.org/10.1111/rda.13013
Da Silva, A., Villalobos, E. M., Cunha, E. M., Lara, M. do C., Nassar, A. F., Piatti, R. M., Castro, V., Pinheiro, E., Carvalho, A. y Del Fava, C. (2020). Causes of equine abortion, stillbirth, and perinatal mortality in Brazil. Arquivos do Instituto Biológico, 87, e0092020. https://doi.org/10.1590/1808-1657000092020
Davies, M. C., Lawlor, O. y Nash, D. M. (2013). Equine endometrial cytology and bacteriology: effectiveness for predicting live foaling rates. The Veterinary Journal, 198(1), 206-211. https://doi.org/10.1016/j.tvjl.2013.08.002
Davis, H. A., Stanton, M. B., Thungrat, K. y Boothe, D. M. (2013). Uterine bacterial isolates from mares and their resistance to antimicrobials: 8,296 cases (2003-2008). Journal of the American Veterinary Medical Association, 242(7), 977-983. https://doi.org/10.2460/javma.242.7.977
Derisoud, E., Grimard, B., Gourtay, C., Auclair-Ronzaud, J. y Chavatte-Palmer, P. (2022). Factors affecting post-breeding endometritis, pregnancy rate and embryonic/fetal death in sport mares in two French commercial stud farms: special focus on age, parity and lactating status effects. bioRxiv. https://doi.org/10.1101/2022.01.21.477204
Díaz-Bertrana, M. L. (2013). Estudio Microbiológico de Infertilidad en yeguas [tesis de doctorado, Universidad de Las Palmas de Gran Canaria]. https://accedacris.ulpgc.es/jspui/handle/10553/10282
Díaz‐Bertrana, M. L., Deleuze, S., Pitti, L. P., Yeste, M., Morales, I. y Rivera, M. M. (2021). Microbial prevalence and antimicrobial sensitivity in equine endometritis in field conditions. Animals, 11(5), 1476. https://doi.org/10.3390/ani11051476
Dooleweerdt, C., Petersen, M. R., Bojesen, A. M., Pedersen, H., Lehn-Jensen, H. y Christoffersen, M. (2015). Equine infectious endometritis-clinical and subclinical cases. Journal of Equine Veterinary Science, 35(2), 95-104. https://doi.org/10.1016/j.jevs.2014.12.002
Ferris, R. A., Bohn, A. y McCue, P. M. (2015). Equine endometrial cytology: collection techniques and interpretation. Equine Veterinary Education, 27(6), 316-322. https://doi.org/10.1111/eve.12280
Gallego, R. S., Ruíz, A. F. y Ruíz, J. D. (2020). Frecuencia del aislamiento bacteriano y patrones de sensibilidad en yeguas criollas colombianas diagnosticadas con endometritis. Revista de Medicina Veterinaria, 1(41), 13-21. https://doi.org/10.19052/mv.vol1.iss41.2
Guevara, M., Urcia, F. y Casquero, J. (2007). Manual de procedimientos y técnicas de laboratorio para la identificación de los principales hongos oportunistas causantes de micosis humanas. Ministerio de Salud; Instituto Nacional de Salud.
Heil, B. A., Paccamonti, D. L. y Sones, J. L. (2019). Role for the mammalian female reproductive tract microbiome in pregnancy outcomes. Physiological Genomics, 51(8), 390-399. https://doi.org/10.1152/physiolgenomics.00045.2019
Hoffmann, C., Ellenberger, C., Costa, R., Aupperle, H., Dhein, S., Stief, B. y Schoon, H-A. (2009). The equine endometrosis: new insights into the pathogenesis. Animal Reproduction Science, 111(2-4), 261-278. https://doi.org/10.1016/j.anireprosci.2008.03.019
Høiby, N., Bjarnsholt, T., Moser, C., Bassi, G. L., Coenye, T., Donelli, G., Hall-Stoodley, L., Holá, V., Imbert, C., Kirketerp-Møller, K., Lebeaux, D., Oliver, A., Ullman, A. J. y Williams, C.; ESCMID Study Group for Biofilms (ESGB) and Consulting External Expert Werner Zimmerli. (2015). ESCMID* guideline for the diagnosis and treatment of biofilm infections 2014. Clinical Microbiology and Infection, 21(supl.1), S1-S25. https://doi.org/10.1016/j.cmi.2014.10.024
Holyoak, G. R. y Lyman, C. C. (2021). The equine endometrial microbiome: a brief review. American Journal of Biomedical Science y Research, 11(6), 532-534. https://doi.org/10.34297/ajbsr.2021.11.001689
Jones, E. (2019). Characterization of the equine microbiome during late gestation and the early postpartum period, and at various times during the estrous cycle in mares being bred with raw or extended semen [tesis de maestría, Kansas State University]. https://krex.k-state.edu/server/api/core/bitstreams/8b2f820c-0642-4ae3-83b8-f3712a911823/content
Jorge, M. L., Orlandi, C. M. y Santana, A. E. (2017). Citocentrifugação e métodos convencionais na citologia uterina de éguas em estro e diestro. Arquivo Brasileiro de Medicina Veterinaria e Zootecnia, 69(4), 802-806. https://doi.org/10.1590/1678-4162-9222
Katila, T. (2016). Evaluation of diagnostic methods in equine endometritis. Reproductive Biology, 16(3), 189-196. https://doi.org/10.1016/j.repbio.2016.06.002
Katila, T. y Ferreira-Dias, G. (2022). Evolution of the concepts of endometrosis, post breeding endometritis, and susceptibility of mares. Animals, 12(6), 779. https://doi.org/10.3390/ani12060779
Kozdrowski, R., Sikora, M., Buczkowska, J., Nowak, M., Raś, A. y Dzięcioł, M. (2015). Effects of cycle stage and sampling procedure on interpretation of endometrial cytology in mares. Animal Reproduction Science, 154, 56-62. https://doi.org/10.1016/j.anireprosci.2015.01.009
Laseca, N., Anaya, G., Peña, Z., Pirosanto, Y., Molina, A. y Demyda-Peyrás, S. (2021). Impaired reproductive function in equines: from genetics to genomics. Animals, 11(2), 393. https://doi.org/10.3390/ani11020393
LeBlanc, M. M. (2010). Ascending placentitis in the mare: an update. Reproduction in Domestic Animals, 45(Supl.2), 28-34. https://doi.org/10.1111/j.1439-0531.2010.01633.x
LeBlanc, M. M. y Causey, R. C. (2009). Clinical and subclinical endometritis in the mare: both threats to fertility. Reproduction in Domestic Animals, 44(Supl.3), 10-22. https://doi.org/10.1111/j.1439-0531.2009.01485.x
LeBlanc, M. M., Magsig, J. y Stromberg, A. J. (2007). Use of a low-volume uterine flush for diagnosing endometritis in chronically infertile mares. Theriogenology, 68(3), 403-412. https://doi.org/10.1016/j.theriogenology.2007.04.038
Ley n.o 25919. Declaran el Caballo de Paso como espacie oriunda del Perú. Diario Oficial El Peruano (3 de diciembre de 1992). https://www.deperu.com/legislacion/ley-25919-pdf.html
Marcolongo-Pereira, C., Adrien, M., Ladeira, S. R., Soares, M. P., Assis-Brasil, N. D. y Schild, A. L. (2012). Abortos em equinos na região Sul do Rio Grande do Sul: estudo de 72 casos. Pesquisa Veterinaria Brasileira, 32(1), 22-26. https://doi.org/10.1590/S0100-736X2012000100005
Marth, C. D., Firestone, S. M., Hanlon, D., Glenton, L. Y., Browning, G. F., Young, N. D. y Krekeler, N. (2018). Innate immune genes in persistent mating-induced endometritis in horses. Reproduction, Fertility and Development, 30(3), 533-545. https://europepmc.org/article/MED/28834688
McCue, P. M. (2008). The problem mare: management philosophy, diagnostic procedures, and therapeutic options. Journal of Equine Veterinary Science, 28(11), 619-626. https://doi.org/10.1016/j.jevs.2008.10.009
Meloun, M. y Militký, J. (2011). Statistical analysis of multivariate data. En Statistical Data Analysis. A practical guide (pp. 151-403). WPI. https://doi.org/10.1533/9780857097200.151
Morales, P. C. y Castro, R. A. (2018). Estimación de la integridad uterina en yeguas Pura Raza Chilena y su asociación con edad y número de partos. Revista de Investigaciones Veterinarias del Perú, 29(2), 565-574. https://doi.org/10.15381/rivep.v29i2.14489
Morrell, J. M. y Rocha, A. (2022). A novel approach to minimising acute equine endometritis that may help to prevent the development of the chronic state. Frontiers in Veterinary Science, 8, 799619. https://doi.org/10.3389/fvets.2021.799619
Morris, L. H., McCue, P. M. y Aurich, C. (2020). Equine endometritis: a review of challenges and new approaches. Reproduction, 160(5), R95-R110. https://doi.org/10.1530/REP-19-0478
Nielsen, J. M., Troedsson, M. H., Pedersen, M. R., Bojesen, A. M., Lehn-Jensen, H. y Zent, W. W. (2010). Diagnosis of endometritis in the mare based on bacteriological and cytological examinations of the endometrium: comparison of results obtained by swabs and biopsies. Journal of Equine Veterinary Science, 30(1), 27-30. https://doi.org/10.1016/j.jevs.2009.11.006
Overbeck, W., Jäger, K., Schoon, H. y Witte, T. S. (2013). Comparison of cytological and histological examinations in different locations of the equine uterus-an in vitro study. Theriogenology, 79(9), 1262-1268. https://doi.org/10.1016/j.theriogenology.2013.02.007
Overbeck, W., Witte, T. S. y Heuwieser, W. (2011). Comparison of three diagnostic methods to identify subclinical endometritis in mares. Theriogenology, 75(7), 1311-1318. https://doi.org/10.1016/j.theriogenology.2010.12.002
Pacheco, V. S. (2011). Identificación de bacterias aeróbicas patógenas en yeguas peruano de paso mediante hisopado uterino. Spermova, 1(1), 116-118. https://spermova.pe/site2/files/Revistas/Rev.No.1Vol1/116-118IDENTIFICACION-DE-BACTERIAS-AEROBICASpacheco2011-116-118.pdf
Pasolini, M. P., Del Prete, C., Fabbri, S. F. y Auletta, L. (2016). Endometritis and infertility in the mare – the challenge in equine breeding industry-a review. Genital Infections and Infertility. https://doi.org/10.5772/62461
Petersen, M. R., Rosenbrock, A., Osborne, M. y Bojesen, A. M. (2018). High prevalence of subclinical endometritis in problem mares-effect of activation and treatment on fertility. Journal of Equine Veterinary Science, 66, 117. https://doi.org/10.1016/j.jevs.2018.05.162
Petersen, M. R., Skive, B., Christoffersen, M., Lu, K., Nielsen, J. M., Troedsson, M. H. y Bojesen, A. M. (2015). Activation of persistent Streptococcus equi subspecies zooepidemicus in mares with subclinical endometritis. Veterinary Microbiology, 179(1-2), 119-125. https://doi.org/10.1016/j.vetmic.2015.06.006
Pisello, L., Rampacci, E., Stefanetti, V., Beccati, F., Hyatt, D. R., Coletti, M. y Passamonti, F. (2019). Temporal efficacy of antimicrobials against aerobic bacteria isolated from equine endometritis: an Italian retrospective analysis (2010-2017). Veterinary Record, 185(19), 598. https://doi.org/10.1136/vr.105413
Pugh, G. (2018). The role of microbial diversity in female reproductive health: an analysis of the microbiome’s influence on pregnancy outcomes in postparturient mares [tesis de maestría, Eastern Kentucky University]. https://encompass.eku.edu/etd/580/
Riddle, W. T., LeBlanc, M. M. y Stromberg, A. J. (2007). Relationships between uterine culture, cytology and pregnancy rates in a Thoroughbred practice. Theriogenology, 68(3), 395-402. https://doi.org/10.1016/j.theriogenology.2007.05.050
Rinaudo, A. (2012). Endometritis subclínica en vacas lecheras: diagnóstico, tratamiento e incidencia productiva y reproductiva [tesis de doctorado, Universidad Nacional de Rosario]. https://rephip.unr.edu.ar/server/api/core/bitstreams/18cc101d-f0a6-43b5-8db9-5619da15cbe4/content
Rizzo, M., Ducheyne, K. D., Deelen, C., Beitsma, M., Cristarella, S., Quartuccio, M., Stout, T. A. y De Ruijter-Villani, M. (2019). Advanced mare age impairs the ability of in vitro-matured oocytes to correctly align chromosomes on the metaphase plate. Equine Veterinary Journal, 51(2), 252-257. https://doi.org/10.1111/evj.12995
Rodríguez, P. A. y Arenas, R. (2018). Hans Christian Gram y su tinción. Dermatología Cosmética, Medica y Quirúrgica, 16(2), 166-167. https://www.medigraphic.com/pdfs/cosmetica/dcm-2018/dcm182n.pdf
Romero-Márquez, C., Pérez-Anzúrez, G., Huerta-Bravo, M., López-Ordaz, R. y Ruíz-Flores, A. (2022). Fertilidad en yeguas y caracterización de la dinámica ovárica. Nova Scientia, 14(28), 1-17. https://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S2007-07052022000100112
Rose, B. V., Firth, M., Morris, B., Roach, J. M., Wathes, D. C., Verheyen, K. L. y De Mestre, A. M. (2018). Descriptive study of current therapeutic practices, clinical reproductive findings and incidence of pregnancy loss in intensively managed thoroughbred mares. Animal Reproduction Science, 188, 74-84. https://doi.org/10.1016/j.anireprosci.2017.11.011
Rus, M. A., Ștefan, I. S., Mihăiță, C., Daradics, Z. y Morar, I. (2021). Comparison of the cytology brush and low volume lavage techniques to evaluate endometrial cytology for diagnosing endometritis in chronically infertile mares. Bulletin of University of Agricultural Scienes and Veterinary Medicine Cluj-Napoca, 78(1), 123-128. https://doi.org/10.15835/buasvmcn-vm:2020.0038
Sacsaquispe, R. E. y Velásquez, J. (2002). Manual de procedimientos para la prueba de sensibilidad antimicrobiana por el método de disco difusión. Ministerio de Salud; Instituto Nacional de Salud. https://www.gob.pe/institucion/minsa/informes-publicaciones/353004-manual-de-procedimientos-para-la-prueba-de-sensibilidad-antimicrobiana-por-el-metodo-de-disco-difusion
Salam, A., Al-Amin, Y., Tabassoom, M., Singh, J., Akhter, N., Rabaan, A. A. y Alqumber, M. A. (2023). Antimicrobial resistance: a growing serious threat for global public health. Healthcare, 11(13), 1946. https://doi.org/10.3390/healthcare11131946
Scarlet, D., Malama, E., Fischer, S., Knutti, B. y Bollwein, H. (2023). Relationship between clinical uterine findings, therapy, and fertility in the mare. Veterinary Sciences, 10(4), 259. https://doi.org/10.3390/vetsci10040259
Schöniger, S. y Schoon, H-A. (2020). The healthy and diseased equine endometrium: a review of morphological features and molecular analyses. Animals, 10(4), 625. https://doi.org/10.3390/ani10040625
Sikora, M., Król, J., Nowak, M., Stefaniak, T., Aubertsson, G. y Kozdrowski, R. (2016). The usefulness of uterine lavage and acute phase protein levels as a diagnostic tool for subclinical endometritis in Icelandic mares. Acta Veterinaria Scandinavica, 58, 50. https://doi.org/10.1186/s13028-016-0233-4
Silva Rua, M. A., Quirino, C. R., Bittencourt, R. R., Carvalho, E. C., Bernadino, M. L., Bartholazzi Junior, A., Cipagalta, L. F. y Barreto, M. A. (2018). Diagnostic methods to detect uterus illnesses in mares. Theriogenology, 114, 285-292. https://doi.org/10.1016/j.theriogenology.2018.03.042
Sotomayor, C., Manchego, A., Chiok, K., Sandoval, N., Ramírez, M., Rojas, M. y Rivera, H. (2012). Seroprevalencia de anticuerpos contra serovares de Leptospira spp en yeguas de un haras de la ciudad de Lima. Revista de Investigaciones Veterinarias del Perú, 23(4), 499-503. http://www.scielo.org.pe/scielo.php?script=sci_arttext&pid=S1609-91172012000400014
Thurlow, L. R., Hanke, M. L., Fritz, T., Angle, A., Aldrich, A., Williams, S. H., Engebretsen, I. L., Bayles, K. W., Horswill, A. R. y Kielian, T. (2011). Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. The Journal of Immunology, 186(11), 6585-6596. https://doi.org/10.4049/jimmunol.1002794
Troedsson, M. H. y Woodward, E. M. (2016). Our current understanding of the pathophysiology of equine endometritis with an emphasis on breeding-induced endometritis. Reproductive Biology, 16(1), 8-12. https://doi.org/10.1016/j.repbio.2016.01.003
Walter, J., Neuberg, K. P., Failing, K. y Wehrend, A. (2012). Cytological diagnosis of endometritis in the mare: investigations of sampling techniques and relation to bacteriological results. Animal Reproduction Science, 132(3-4), 178-186. https://doi.org/10.1016/j.anireprosci.2012.05.012
World Health Organization. (2024). WHO Bacterial Priority Pathogens List, 2024: bacterial pathogens of guide research, development and strategies to prevent and control antimicrobial resistance. World Health Organization. https://www.who.int/publications/i/item/9789240093461
World Health Organization [WHO]. (2016). Critically Important Antimicrobials for Human Medicine 5th Revision 2016 Ranking of medically important antimicrobials for risk management of antimicrobial resistance due to non-human use (5.a ed.). World Health Organization. https://www.who.int/publications/i/item/9789241512220#:~:text=This%20document%20provides%20a%20ranking%20of%20medically%20important,in%20Raleigh%2C%20United%20States%20of%20America%20in%202016.
Woodward, E. M., Christoffersen, M., Campos, J., Squires, E. L. y Troedsson, M. H. (2012). Susceptibility to persistent breeding-induced endometritis in the mare: relationship to endometrial biopsy score and age, and variations between seasons. Theriogenology, 78(3), 495-501. https://doi.org/10.1016/j.theriogenology.2012.02.028
Zurita, S., Urcia, F. y Navarro, A. (2017). Manual de procedimientos técnicos para el diagnóstico micológico. Ministerio de Salud; Instituto Nacional de Salud.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2026 Elsa Lucila del Carmen Chavez Chavez,William Barrios Santos, Alfredo Delgado Castro

This work is licensed under a Creative Commons Attribution 4.0 International License.
All articles published in Salud y Tecnología Veterinaria are under a Creative Commons Reconocimiento 4.0 International license.
The authors retain the copyright and grant the journal the right of first publication, with the work registered with the Creative Commons License, which allows third parties to use what is published whenever they mention the authorship of the work, and to the first publication in this magazine.
Authors can make other independent and additional contractual agreements for the non-exclusive distribution of the version published in this journal, provided they clearly indicate that the work was published in this journal.
The authors can file in the repository of their institution:
The research work or thesis of degree from which the published article derives.
The pre-print version: the version prior to peer review.
The Post-print version: final version after peer review.
The definitive version or final version created by the publisher for publication.








