Subclinical Endometritis in Dairy Cattle

  1. Angel Quintela Arias, Luis 1
  2. Vigo Fernández, Marcos 1
  3. José Becerra González, Juan 1
  4. Barrio López, Mónica 1
  5. Pedro José García Herradón 1
  6. Ana Isabel Peña Martínez 1
  1. 1 Unit of Reproduction & Obstetrics, Faculty of Veterinary Medicine, Department of Animal Pathology, Lugo, Spain
Libro:
New Insights into Theriogenology

Ano de publicación: 2018

Tipo: Capítulo de libro

DOI: 10.5772/INTECHOPEN.80229 GOOGLE SCHOLAR lock_openAcceso aberto editor

Resumo

Subclinical endometritis is recognized as a cause of poor reproductive performance in dairy cows. Inflammation of the endometrium persisting after postpartum uterine involution has been related with prolonged calving-conception intervals and low fertility in dairy cows. The subclinical nature of this condition makes it necessary in the use of endometrial cytology or biopsy for diagnosing it. There are some controversies among authors in relation to the postpartum period from which a physiological endometrial inflammation should be considered a pathological subclinical endometritis. Therefore, depending on the sampling period after calving, different studies establish a different degree of polymorphonuclear leukocyte infiltration as cutoff point to diagnose subclinical endometritis. Controversies also exist regarding the pathogenesis of the disease and its consequences on the fertility of dairy cattle. The aim of this chapter was to review the current knowledge on this uterine pathology.

Referencias bibliográficas

  • Le Blanc S, Duffield T, Leslie K, Bateman K, Keefe G, Walton JS, et al. Defining and diagnosing postpartum clinical endometritis and its impact on reproductive performance in dairy cows. Journal of Dairy Science. 2002;85:2223-2236. DOI: 10.3168/jds.S0022-0302(02)74302-6
  • Gautam G, Nakao T, Yusuf M, Koike K. Prevalence of endometritis during the postpartum period and its impact on subsequent reproductive performance in two Japanese dairy herds. Animal Reproduction Science. 2009;116:175-187. DOI: 10.1016/j.anireprosci.2009.02.001
  • Sheldon IM, Price SB, Cronin J, Gilbert RO, Gadsby JE. Mechanisms of infertility associated with clinical and subclinical endometritis in high producing dairy cattle. Reproduction in Domestic Animals. 2009;44(Suppl. 3):1-9. DOI: 10.1111/j.1439-0531.2009.01465.x
  • Sheldon IM, Rycroft AN, Dogan B, Craven M, Bromfield JJ, Chandler A, et al. Specific strains of Escherichia coli are pathogenic for the endometrium of cattle and cause pelvic inflammatory disease in cattle and mice. PLoS One. 2010;5(2):e9192. DOI: 10.1371/journal.pone.0009192
  • Priest N. The Effect of a Non-steroidal Anti-Inflammatory Drug on Subclinical Endometritis in Dairy Cows and the Identification of at-Risk Cows. [MSc Thesis]. New Zealand: Lincoln University; 2013
  • Kasimanickam R, Duffield TF, Foster RA, Gartley CJ, Leslie KE, Walton JS, et al. Endometrial cytology and ultrasonography for the detection of subclinical endometritis in postpartum dairy cows. Theriogenology. 2004;62:9-23. DOI: 10.1016/j.theriogenology.2003.03.001
  • Lazzari G, Duchi R, Colleoni S, Baldazzi L, Benedetti V, Galli A, et al. Le patologie uterine cliniche e subcliniche come causa di infertilità nelle bovine da latte: Studio epidemiologico in due allevamenti della regione Lombardia. Large Animal Review. 2011;17:43-47
  • Madoz LV, Giuliodori MJ, Migliorisi AL, Jaureguiberry M, de la Sota RL. Endometrial cytology, biopsy, and bacteriology for the diagnosis of subclinical endometritis in grazing dairy cows. Journal of Dairy Science. 2014;97:1-7. DOI: 10.3168/jds.2013-6836
  • Mariño B, Quintela LA, Becerra JJ, Barrio L, Mociños JE, Guillin JL, et al. Agreement between postmortem endometrial cytology, biopsy and bacteriology in culled dairy cows. Animal Reproduction. 2017;14(4):1024-1033. DOI: 10.21451/1984-3143-AR826
  • Herath S, Williams EJ, Lilly ST, Gilbert RO, Dobson H, Bryant CE, et al. Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction. 2007;134:683-693. DOI: 10.1530/REP-07-0229
  • Williams EJ, Fischer DP, Noakes DE, England GCW, Rycroft A, Dobson H, et al. The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology. 2007;68:549-559. DOI: 10.1016/j.theriogenology.2007.04.056
  • Shimizu T, Miyauchi K, Shirasuna K, Bollwein H, Magata F, Murayama C, et al. Effects of lipopolysaccharide (LPS) and peptidoglycan (PGN) on estradiol production in bovine granulosa cells from small and large follicles. Toxicology in Vitro. 2012;26:1134-1142. DOI: 10.1016/j.tiv.2012.06.014
  • Lavon Y, Leitner G, Goshen T, Braw-Tal R, Jacoby S, Wolfenson D. Exposure to endotoxin during estrus alters the timing of ovulation and hormonal concentrations in cows. Theriogenology. 2008;70:956-967. DOI: 10.1016/j.theriogenology.2008.05.058
  • Lavon Y, Leitner G, Voet H, Wolfenson D. Naturally occurring mastitis effects on timing of ovulation, steroid and gonadotrophic hormone concentrations, and follicular and luteal growth in cows. Journal of Dairy Science. 2010;93:911-921. DOI: 10.3168/jds.2009-2112
  • Herath S, Lilly ST, Fischer DP, Williams EJ, Dobson H, Bryant CE, et al. Bacterial lipopolysaccharide induces an endocrine switch from prostaglandin F2α to prostaglandin E2 in bovine endometrium. Endocrinology. 2009;150:1912-1920. DOI: 10.1210/en.2008-1379
  • Soto P, Natzke RP, Hansen PJ. Identification of possible mediators of embryonic mortality caused by mastitis: Actions of lipopolysaccharide, prostaglandin F2a, and the nitric oxide generator, sodium nitroprusside dihydrate, on oocyte maturation and embryonic development in cattle. American Journal of Reproductive Immunology. 2003;50:263-272. DOI: 10.1034/j.1600-0897.2003.00085.x
  • Sheldon IM, Lewis GS, LeBlanc S, Gilbert RO. Defining postpartum uterine disease in cattle. Theriogenology. 2006;65:1516-1530. DOI: 10.1016/j.theriogenology.2005.08.021
  • Prunner I, Pothmann H, Wagener K, Giuliodori M, Huber J, Ehling-Schulz M, et al. Dynamics of bacteriologic and cytologic changes in the uterus of postpartum dairy cows. Theriogenology. 2014;82:1316-1322. DOI: 10.1016/j.theriogenology.2014.08.018
  • Gärtner MA, Peter S, Jung M, Drillich M, Einspanier R, Gabler C. Increased mRNA expression of selected pro-inflammatory factors in inflamed bovine endometrium in vivo as well as in endometrial epithelial cells exposed to Bacillus pumilus in vitro. Reproduction, Fertility, and Development. 2015;28:982-994. DOI: 10.1071/RD14219
  • Fischer C, Drillich M, Odau M, Heuwieser W, Einspanier R, Gabler C. Selected pro-inflammatory factor transcripts in bovine endometrial epithelial cells are regulated during the estrus cycle and elevated in case of subclinical or clinical endometritis. Reproduction, Fertility, and Development. 2010;22:818-829. DOI: 10.1071/RD09120
  • Gabler C, Fischer C, Drillich M, Einspanier R, Heuwieser W. Time-dependent mRNA expression of selected pro-inflammatory factors in the endometrium of primiparous cows postpartum. Reproductive Biology and Endocrinology. 2010;8:152. DOI: 10.1186/1477-7827-8-152
  • Galvão KN, Santos NR, Galvão JS, Gilbert RO. Association between endometritis and endometrial cytokine expression in postpartum Holstein cows. Theriogenology. 2011;76:290-299. DOI: 10.1016/j.theriogenology.2011.02.006
  • Ghasemi F, Gonzalez-Cano P, Griebel PJ, Palmer C. Proinflammatory cytokine gene expression in endometrial cytobrush samples harvested from cows with and without subclinical endometritis. Theriogenology. 2012;78:1538-1547. DOI: 10.1016/j.theriogenology.2012.06.022
  • Kasimanickam R, Kasimanickam V, Kastelic JP. Mucin 1 and cytokines mRNA in endometrium of dairy cows with postpartum uterine disease or repeat breeding. Theriogenology. 2014;81:952-958. DOI: 10.1016/j.theriogenology.2014.01.018
  • Mattmiller SA, Carlson BA, Sordillo LM. Regulation of inflammation by selenium and selenoproteins: Impact on eicosanoid biosynthesis. Journal of Nutritional Science. 2013;2(e28):1-13. DOI: 10.1017/jns.2013.17
  • Herath S, Lilly ST, Santos NR, Gilbert RO, Goetze I, Bryant CE, et al. Expression of genes associated with immunity in the endometrium of cattle with disparate postpartum uterine disease and fertility. Reproductive Biology and Endocrinology. 2009;7:1-13. DOI: 10.1186/1477-7827-7-55
  • Brodzki P, Kostro K, Brodzki A, Wawron W, Marczuk J, Kurek L. Inflammatory cytokines and acute-phase proteins concentrations in the peripheral blood and uterus of cows that developed endometritis during early postpartum. Theriogenology. 2015;84:11-18. DOI: 10.1016/j.theriogenology.2015.02.006
  • Salehi R, Colazo MG, Gobikrushanth M, Basu U, Ambrose DJ. Effects of prepartum oilseed supplements on subclinical endometritis, pro- and anti-inflammatory cytokine transcripts in endometrial cells and postpartum ovarian function in dairy cows. Reproduction, Fertility, and Development. 2017;29(4):747-758. DOI: 10.1071/RD15334
  • Silvestre FT, Carvalho TS, Crawford PC, Santos JE, Staples CR, Jenkins T, et al. Effects of differential supplementation of fatty acids during the peripartum and breeding periods of Holstein cows: II. Neutrophil fatty acids and function, and acute-phase proteins. Journal of Dairy Science. 2011;94:2285-2301. DOI: 10.3168/jds.2010-3371
  • Bernabucci U, Ronchi B, Lacetera N, Nardone A. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. Journal of Dairy Science. 2005;88:2017-2026. DOI: 10.3168/jds.S0022-0302(05)72878-2
  • Goff JP. Major advances in our understanding of nutritional influences on bovine health. Journal of Dairy Science. 2006;89:1292-1301. DOI: 10.3168/jds.S0022-0302(06)72197-X
  • Douglas GN, Rehage J, Beaulieu AD, Bahaa AO, Drackley JK. Prepartum nutrition alters fatty acid composition in plasma, adipose tissue, and liver lipids of periparturient dairy cows. Journal of Dairy Science. 2007;90:2941-2959. DOI: 10.3168/jds.2006-225
  • Sordillo LM, Aitken SL. Impact of oxidative stress on the health and immune function of dairy cattle. Veterinary Immunology and Immunopathology. 2009;128:104-109. DOI: 10.1016/j.vetimm.2008.10.305
  • Miller JK, Brzezinska-Slebodzinska E, Madsen FC. Oxidative stress, antioxidants, and animal function. Journal of Dairy Science. 1993;76:2812-2823. DOI: 10.3168/jds.S0022-0302(93)77620-1
  • Sordillo LM, O’Boyle N, Gandy JC, Corl CM, Hamilton E. Shifts in thioredoxin reductase activity and oxidant status in mononuclear cells obtained from transition dairy cattle. Journal of Dairy Science. 2007;90:1186-1192. DOI: 10.3168/jds.S0022-0302(07)71605-3
  • Weaver JA, Maddox JF, Cao YZ, Mullarky IK, Sordillo LM. Increased 15-HPETE production decreases prostacyclin synthase activity during oxidant stress in aortic endothelial cells. Free Radical Biology & Medicine. 2001;30:299-308. DOI: 10.1016/S0891-5849(00)00466-4
  • Sordillo LM, Weaver JA, Cao Y-Z, Corl C, Sylte MJ, Mullarky IK. Enhanced 15-HPETE production during oxidant stress induces apoptosis of endothelial cells. Prostaglandins & Other Lipid Mediators. 2005;76:19-34. DOI: 10.1016/j.prostaglandins.2004.10.007
  • Sordillo LM, Streicher KL, Mullarky IK, Gandy JC, Trigona W, Corl CM. Selenium inhibits 15-hydroperoxyoctadecadienoic acid-induced intracellular adhesion molecule expression in aortic endothelial cells. Free Radical Biology & Medicine. 2008;44:34-43. DOI: 10.1016/j.freeradbiomed.2007.09.002
  • Drillich M, Tesfayec D, Ringsc F, Schellanderc K, Heuwiesera W, Hoelkerc M. Effects of polymorphonuclear neutrophile infiltration into the endometrial environment on embryonic development in superovulated cows. Theriogenology. 2012;77:570-578. DOI: 10.1016/j.theriogenology.2011.08.033
  • Fernandez-Sanchez FI, Barrio-Lopez M, Quintela-Arias LA, Becerra-Gonzalez JJ, Peña-Martinez AI, Martinez-Bello D, et al. Use of endometrial cytology and metabolic profiles for selection of embryo donor cows. Spanish Journal of Agricultural Research. 2014;12(3):664-671. DOI: 10.5424/sjar/2014123-4948
  • Gabler C, Drillich M, Fischer C, Holder C, Heuwieser W, Einspanier R. Endometrial expression of selected transcripts involved in prostaglandin synthesis in cows with endometritis. Theriogenology. 2009;71:993-1004. DOI: 10.1016/j.theriogenology.2008.11.009
  • Baranski W, Lukasik K, Skarzynski D, Sztachanska M, Zdunczyk S, Janowski T. Secretion of prostaglandins and leukotrienes by endometrial cells in cows with subclinical and clinical endometritis. Theriogenology. 2013;80:766-772. DOI: 10.1016/j.theriogenology.2013.07.001
  • Sakumoto R, Shibaya M, Okuda K. Tumor necrosis factor-α (TNF-α) inhibits progesterone and estradiol 17-β production from cultured granulosa cells: Presence of TNF-α receptors in bovine granulosa and theca cells. The Journal of Reproduction and Development. 2003;49(6):441-449. DOI: 10.1262/jrd.49.441
  • Sakumoto R, Okuda K. Possible actions of tumor necrosis factor- α in ovarian function. The Journal of Reproduction and Development. 2004;50(1):39-46. DOI: 10.1262/jrd.50.39
  • Field SL, Dasgupta T, Cummings M, Orsi NM. Cytokines in ovarian folliculogenesis, oocyte maturation and luteinisation. Molecular Reproduction and Development. 2013;81(4):284-314. DOI: 10.1002/mrd.22285
  • Barlund CS, Carruthers TD, Waldner CL, Palmer CW. A comparison of diagnostic techniques for postpartum endometritis in dairy cattle. Theriogenology. 2008;69:714-723. DOI: 10.1016/j.theriogenology.2007.12.005
  • Meira EBS Jr, Henriques LCS, Sá LRM, Gregory L. Comparison of ultrasonography and histopathology for the diagnosis of endometritis in Holstein-Friesian cows. Journal of Dairy Science. 2012;95:6969-6973. DOI: 10.3168/jds.2011-4950
  • Quintela LA, Becerra JJ, Herradón PG. Essential Guides on Cattle Farming: Uterine Diseases. Servet: Zaragoza; 2016. 69 p
  • López-Helguera I, López-Gatius F, García-Ispiero I. The influence of genital tract status in postpartum period on the subsequent reproductive performance in high producing dairy cows. Theriogenology. 2012;77(7):1334-1342. DOI: 10.1016/j.theriogenology.2011.10.038
  • Debertolis L, Gaetano M, Barbara M, Sabine M, Eleonora I, Heinrich B. Effects of an induced endometritis on uterine blood flow in cows evaluated by transrectal Doppler sonography. Journal of Veterinary Science. 2015;17(2):189-197. DOI: 10.4142/jvs.2016.17.2.189
  • Kasimanickam R, Duffield TF, Foster RA, Gartley CJ, Leslie KE, Walton JS, et al. A comparison of the cytobrush and uterine lavage techniques to evaluate endometrial cytology in clinically normal postpartum dairy cows. The Canadian Veterinary Journal. 2005;46:255-259
  • Pascottini OB. Subclinical Endometritis in Dairy Cattle: A Practical Approach. [PhD Thesis]. Department of Reproduction, Obstetrics and Herd Health, Faculty of Veterinary Medicine, Ghent University; 2016
  • Lopdell T, Berg MC, Green MP, Back PJ. Effect of sub-clinical uterine infection on plasma aminoacid concentrations in early lactation dairy cows. Proc NZ Soc Anim Prod. 2011;71:291-295
  • Heidarpour M, Mohri M, Fallah Rad AH, Shahreza FD, Mohammadi M. Acute-phase protein concentration and metabolic status affect the outcome of treatment in cows with clinical and subclinical endometritis. The Veterinary Record. 2012;171:1-5. DOI: 10.1136/vr.100947
  • Kaufmann T, Drillich M, Tenhagen B-A, Heuwieser W. Correlations between periparturient serum concentrations of non-esterified fatty acids, beta-hydroxybutyric acid, bilirubin, and urea and the occurrence of clinical and subclinical postpartum bovine endometritis. BMC Veterinary Research. 2010;6:47. DOI: 10.1186/1746-6148-6-47
  • Barrio M, Becerra JJ, Herradon PG, Sebastian F, Fernandez M, Quintela LA. Fertility in cows with endometritis diagnosed by cytology at day 30 postpartum. Proc 12th Cong AERA; 2014. Abstract
  • Madoz LV, Giuliodori MJ, Plontzke J, Drillich M, de la Sota RL. The relationship between endometrial cytology during estrus cycle and cutoff points for the diagnosis of subclinical endometritis in grazing dairy cows. Journal of Dairy Science. 2013;96(7):4333-4337. DOI: 10.3168/jds.2012-6269
  • Dubuc J, Duffield TF, Leslie KE, Walton JS, LeBlanc SJ. Definitions and diagnosis of postpartum endometritis in dairy cows. Journal of Dairy Science. 2010;93:5225-5234. DOI: 10.3168/jds.2010-3428
  • Plöntzke J, Madoz LV, De la Sota RL, Drillich M, Heuwieser W. Subclinical endometritis and its impact on reproductive performance in grazing dairy cattle in Argentina. Animal Reproduction Science. 2010;122:52-57. DOI: 10.1016/j.anireprosci.2010.07.006
  • Barrio M, Vigo M, Quintela LA, Becerra JJ, García-Herradón PJ, Martínez-Bello D, et al. Influence of subclinical endometritis on the reproductive performance of dairy cows. Spanish Journal of Agricultural Research. 2015;13(4):05-02. DOI: 10.5424/sjar/2015134-8129
  • Hammon DS, Evjen IM, Dhiman TR, Goff JP, Walters JL. Neutrophil function and energy status in Holstein cows with uterine health disorders. Veterinary Immunology and Immunopathology. 2006;113:21-29. DOI: 10.1016/j.vetimm.2006.03.022
  • Gilbert RO, Shin ST, Guard CL, Erb HN, Frajblat M. Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology. 2005;64:1879-1888. DOI: 10.1016/j.theriogenology.2005.04.022
  • Cheong SH, Nydam DV, Galvao KN, Croiser BM, Ricci A, Caixeta LS, et al. Cow-level and herd-level risk factors for subclinical endometritis in lactating Holstein cows. Journal of Dairy Science. 2011;94:762-770. DOI: 10.3168/jds.2010-3439
  • McDougall S, Hussein H, Aberdein D, Buckle K, Roche J, Burke C, et al. Relationships between cytology, bacteriology and vaginal discharge scores and reproductive performance in dairy cattle. Theriogenology. 2011;76:229-240. DOI: 10.1016/j.theriogenology.2010.12.024
  • Ohtani S, Okuda K, Nishimura K, Mohri S. Histological changes in bovine endometrium during the estrous cycle. Theriogenology. 1993;39:1033-1042. DOI: 10.1016/0093-691X(93)90004-O
  • Santos NR, Roman HB, Gilbert RO. The use of leukocyte esterase reagent strips for diagnosis of subclinical endometritis in dairy cows. Theriogenology. 2006;66:666-667. DOI: 10.1016/j.theriogenology.2006.04.027
  • Cheong SH, Nydam DV, Galvão KN, Crosier BM, Ricci A, Caixeta LS, et al. Use of reagent test strips for diagnosis of endometritis in dairy cows. Theriogenology. 2012;77:858-864. DOI: 10.1016/j.theriogenology.2011.09.009
  • Couto GB, Vaillancourt DH, Lefebvre RC. Comparison of a leukocyte esterase test with endometrial cytology for diagnosis of subclinical endometritis in postpartum dairy cows. Theriogenology. 2013;79:103-107. DOI: 10.1016/j.theriogenology.2012.09.014
  • Strowitzki T, Germeyer A, Popovici R, von Wolff M. The human endometrium as a fertility-determining factor. Human Reproduction Update. 2006;12:617-630. DOI: 10.1093/humupd/dml033
  • Brandt GW, Manning JP. Improved uterine biopsy technics for diagnosing infertility in the mare. Veterinary Medicine, Small Animal Clinician. 1969;64:977-983
  • Nielsen JM. Endometritis in the mare: A diagnostic study comparing cultures from swab and biopsy. Theriogenology. 2005;64:510-518
  • Zaayer D, van der Horst CJ. Non-fertility in cows: Treatment with PGF and investigation of uterine biopsies. Cytobios. 1986;45:55-70
  • De Boer NW, LeBlanc SJ, Dubuc J, Meier S, Heuwieser W, Arlt S, et al. Systematic review of diagnostic tests for reproductive-tract infection and inflammation in dairy cows. Journal of Dairy Science. 2014;97:3983-3999. DOI: 10.3168/jds.2013-7450
  • Prunner I, Wagener K, Pothmann H, Ehling-Schulz M, Drillich M. Risk factors for uterine diseases on small- and medium-sized dairy farms determined by clinical, bacteriological, and cytological examinations. Theriogenology. 2014;82:857-865. DOI: 10.1016/j.theriogenology.2014.06.015
  • Gobikrushanth M, Salehi R, Ambrose DJ, Colazo MG. Categorization of endometritis and its association with ovarian follicular growth and ovulation, reproductive performance, dry matter intake, and milk yield in dairy cattle. Theriogenology. 2016;86:1842-1849. DOI: 10.1016/j.theriogenology.2016.06.003
  • Burke CR, Meier S, McDougall S, Compton C, Mitchell M, Roche JR. Relationships between endometritis and metabolic state during the transition period in pasture-grazed dairy cows. Journal of Dairy Science. 2010;93:5363-5373. DOI: 10.3168/jds.2010-3356
  • Green MP, Ledgard AM, Beaumont SE, Berg MC, McNatty KP, Peterson AJ, et al. Long-term alteration of follicular steroid concentrations in relation to subclinical endometritis in postpartum dairy cows. Journal of Animal Science. 2011;89:3551-3560. DOI: 10.2527/jas.2011-3958
  • Salasel B, Mokhtari A, Taktaz T. Prevalence, risk factors for and impact of subclinical endometritis in repeat breeder dairy cows. Theriogenology. 2010;74:1271-1278. DOI: 10.1016/j.theriogenology.2010.05.033
  • Janowski T, Barański W, Łukasik K, Skarżyński D, Rudowska M, Zduńczyk S. Prevalence of subclinical endometritis in repeat breeding cows and mRNA expression of tumor necrosis factor α and inducible nitric oxide synthase in the endometrium of repeat breeding cows with and without subclinical endometritis. Polish Journal of Veterinary Sciences. 2013;16(4):693-699
  • Pothmann H, Prunner I, Wagener K, Jaureguiberry M, de la Sota RL, Erber R, et al. The prevalence of subclinical endometritis and intrauterine infections in repeat breeder cows. Theriogenology. 2015;83:1249-1253. DOI: 10.1016/j.theriogenology.2015.01.013
  • Bell MJ, Roberts DJ. The impact of uterine infection on a dairy cow's performance. Theriogenology. 2007;68(7):1074-1079. DOI: 10.1016/j.theriogenology.2007.08.010
  • Green MP, Ledgard AM, Berg MC, Peterson AJ, Back PJ. Prevalence and identification of systemic markers of sub-clinical endometritis in postpartum dairy cows. Proceedings of the New Zealand Society of Animal Production. 2009;69:37-42
  • Dubuc J, Duffield TF, Leslie KE, Walton JS, Leblanc SJ. Effects of postpartum uterine diseases on milk production and culling in dairy cows. Journal of Dairy Science. 2011;94:1339-1346. DOI: 10.3168/jds.2010-3758
  • Haimerl P, Arlt S, Heuwieser W. Evidence-based medicine: Quality and comparability of clinical trials investigating the efficacy of prostaglandin F2α for the treatment of bovine endometritis. The Journal of Dairy Research. 2012;79:287-296. DOI: 10.1017/S002202991200012X
  • Lefebvre RC, Stock AE. Therapeutic efficiency of antibiotics and prostaglandin F2α in postpartum dairy cows with clinical endometritis: An evidence-based evaluation. Veterinary Clinics of North America. Food Animal Practice. 2012;28:79-96. DOI: 10.1016/j.cvfa.2012.01.002
  • Galvão KN, Greci LF, Vilela JM, Sá Filho MF, Santos JEP. Effect of intrauterine infusion of ceftiofur on uterine health and fertility in dairy cows. Journal of Dairy Science. 2009;92:1532-1542. DOI: 10.3168/jds.2008-1615
  • Denis-Robichaud J, Dubuc J. Randomized clinical trial of intrauterine cephapirin infusion in dairy cows for the treatment of purulent vaginal discharge and cytological endometritis. Journal of Dairy Science. 2015;98:6856-6864. DOI: 10.3168/jds.2014-9129
  • Galvão KN, Frajblat M, Brittin SB, Butler ER, Guard CL, Gilbert RO. Effect of prostaglandin F2α on subclinical endometritis and fertility in dairy cows. Journal of Dairy Science. 2009;92:4906-4913. DOI: 10.3168/jds.2008-1984
  • Lima FS, Bisinotto RS, Ribeiro ES, Greco LF, Ayres H, Favoreto MG, et al. Effects of 1 or 2 treatments with prostaglandin F2α on subclinical endometritis and fertility in lactating dairy cows inseminated by timed artificial insemination. Journal of Dairy Science. 2013;96:6480-6488. DOI: 10.3168/jds.2013-6850
  • Meier S, Priest NV, Burke CR, Kay JK, McDougall S, Mitchell MD, et al. Treatment with a nonsteroidal anti-inflammatory drug after calving did not improve milk production, health or reproduction parameters in pasture-grazed dairy cows. Journal of Dairy Science. 2014;97(5):2932-2943. DOI: 10.3168/jds.2013-7838
  • Brinsko SP, Blanchard TL, Varner DD, Schumacher J, Love CC, Hinrichs K, Hartman DL. Endometritis. In: Brinsko SP, Blanchard TL, Varner DD, Schumacher J, Love CC, Hinrichs K, Hartman DL, editors. Manual of Equine Reproduction. 3rd ed. St Louis: Mosby; 2011. pp. 73-84
  • Ahmadi MR, Dehghan SA. Evaluation of the treatment of repeat breeder dairy cows with uterine lavage plus PGF2α with or without cephapirin. Turkish Journal of Veterinary and Animal Sciences. 2007;31:125-129
  • Dini P, Farhoodi M, Hostens M, Van Eetvelde M, Pascottini OB, Fazeli MH, et al. Effect of uterine lavage on neutrophil counts in postpartum dairy cows. Animal Reproduction Science. 2015;158:25-30. DOI: 10.1016/j.anireprosci.2015.04.005
  • Brick TA, Schuenemann GM, Bas S, Daniels JB, Pinto CR, Rings DM, et al. Effect of intrauterine dextrose or antibiotic therapy on reproductive performance of lactating dairy cows diagnosed with clinical endometritis. Journal of Dairy Science. 2012;95:1894-1905. DOI: 10.3168/jds.2011-4892
  • Djuricic D, Vince S, Ablondi M, Dobranic T, Samardzija M. Effect of preventive intrauterine ozone application on reproductive efficiency in Holstein cows. Reproduction in Domestic Animals. 2012;47:87-91. DOI: 10.1111/j.1439-0531.2011.01805.x
  • Tras B, Dinc DA, Uney K. The effect of N-acetylcysteine on the treatment of clinical endometritis and pregnancy rate in dairy cows. Eurasian Journal of Veterinary Sciences. 2014;30(3):133-137