New postpartum strategies have been developed in dairy cows to ameliorate uterine health and reproductive performance, especially the first service conception rates. This study aimed to assess the effect of intrauterine therapy with ozone (IUTO) in early postpartum on subclinical endometritis prevalence and reproductive parameters in dairy cows under commercial farm conditions. For this purpose, eighty clinically healthy cows with a body condition score between 3.0 and 3.5, from four dairy farms, were randomly allocated into two groups: ozone therapy group (OG, n = 40), which were subjected to IUTO, and control group (CG, n = 40). Content of uterine polymorphonuclear (PMN) leukocytes and subclinical endometritis (SE) percentage were assessed at 35 days after calving by uterine cytology. A second cytology was performed 72 h after IUTO. Reproductive parameters such as interval calving to first service (IFS), number of services per conception (nSC), interval calving to conception (ICC) and first service conception rate (FSCR) were analysed. The second endometrial cytology demonstrated that IUTO reduced (P < 0.01) both PMN (3.7 ± 1.4 vs. 7.6 ± 1.1%) and SE (5.0 vs. 50.0%) percentages compared with CG. Likewise, after ozone treatment, both nSC (2.1 ± 0.3 vs. 3.1 ± 0.2; P < 0.01) and ICC (126.2 ± 9.7 vs. 149.0 ± 9.0; P = 0.0672) decreased, and FSCR increased (50.0 vs. 16.2%; P < 0.01) compared with CG. In conclusion, intrauterine ozone therapy applied at 35 days after calving reduced subclinical endometritis prevalence and improved reproductive performance in postpartum dairy cows managed in a pasture-based system.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
Tax calculation will be finalised during checkout.
Bialoszewski D, Bocian E, Bukowska B, Czajkowska M, Sokol-Leszczynska B, Tyski S. 2010. Antimicrobial activity of ozonated water. Medical Science Monitor, 16(9), MT71–MT75.
Bocci V. 2011. Ozone, a new medical drug. 2nd Edition. (Springer, London).
Bocci V, Borrelli E, Travagli V, Zanardi I. 2009. The ozone paradox: ozone is a strong oxidant as well as a medical drug. Medicinal Research Review, 29, 646–682.
Calderon I, Cohen M, Sagi-Dain L, Artzi O, Bejar J, Sagi S. 2016. The effect of ozonated sterile saline irrigation on the endometrium – A preliminary study. Journal of Obstetrics and Gynecology, 36(5), 635-640.
Constantin T, Bîrţoiu IA. 2016. Preliminary study on ozone therapy in postpartum endometritis of dairy cows. Agriculture and Agricultural Science Procedia, 10, 384–389.
Djuricic D, Vince S, Ablondi M, Dobranic T, Samardzija M. 2012a. Intrauterine ozone treatment of retained fetal membrane in Simmental cows. Animal Reproduction Science, 134(3–4), 119–124.
Djuricic D, Vince S, Ablondi M, Dobranic T, Samardžija M. 2012b. Effect of preventive intrauterine ozone application on reproductive efficiency in Holstein cows. Reproduction in Domestic Animals, 47, 87–91.
Đuričić D, Lipar M, Samardžija M. 2014. Ozone treatment of metritis and endometritis in Holstein cows. Veterinarski Arhiv, 84(2), 103–110.
Đuričić D, Valpotić H, Samardžija M. 2015. Prophylaxis and therapeutic potential of ozone in buiatrics: Current knowledge. Animal Reproduction Science, 159, 1–7.
Đuričić D, Valpotić H, Žura Žaja I, Samardžija M. 2016. Comparison of intrauterine antibiotics versus ozone medical use in sheep with retained placenta and following obstetric assistance. Reproduction in Domestic Animals, 51(4), 538–540.
Edmonson A, Lean I, Weaver L, Farver T, Webster G. 1989. A body condition scoring chart for Holstein dairy cows. Journal of Dairy Science, 72(1), 68–78.
Elliott L, McMahon KJ, Gier HT, Marion GB. 1968. Uterus of the cow after parturition: bacterial content. American Journal of Veterinary Research, 29(1), 77–81.
Ganaie BA, Japheth KP, Ali M, Lone SA, Mir SH, Malik TA. 2018. An insight into the pathophysiology, preventive and treatment strategies of retained fetal membranes in bovines – a review. Journal of Animal Health and Production, 6(2), 62–72.
Garzón JP, Barrera VH, Galarza DA, Soria ME, Rodríguez DF, López GE, Marini PR. 2017. Effect of zeolite on return of ovarian activity, involution and uterine health in postpartum dairy grazing bred cows. Livestock Research for Rural Development, 29(3), 1–5.
Gilbert RO, Santos NR. 2016. Dynamics of postpartum endometrial cytology and bacteriology and their relationship to fertility in dairy cows. Theriogenology, 85(8), 1367–1374.
Gilbert RO, Shin ST, Guard CL, Erb HN, Frajblat M. 2005. Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology, 64, 1879–1888
Hidalgo-Tallón FJ, Torres LM. 2013. Ozonoterapia en medicina del dolor: revisión. Revista de la Sociedad Española del dolor, 20(6), 291-300.
Inchaisri C, Jorritsma R, Vos PL, Van der Weijden GC, Hogeveen H. 2010. Economic consequences of reproductive performance in dairy cattle. Theriogenology, 74(5), 835–846
Janowski T, Barański W, Łukasik K, Skarżyński D, Rudowska M, Zduńczyk S. 2013. 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, 16(4), 693–699.
Lagos-Figueroa B, Narváez-Portilla JP. 2016. Prevalencia de endometritis diagnosticada por ultrasonido en vacas de pequeños productores de leche de seis municipios del departamento de Nariño, Colombia. Revista Investigaciones Pecuarias, 4(1), 23–30.
Lavon Y, Leitner G, Goshen T, Braw-Tal R, Jacoby S, Wolfenson D. 2008. Exposure to endotoxin during estrus alters the timing of ovulation and hormonal concentrations in cows. Theriogenology, 70, 956–967.
Lavon Y, Leitner G, Klipper E, Moallem U, Meidan R, Wolfenson D. 2011. Subclinical, chronic intramammary infection lowers steroid concentrations and gene expression in bovine preovulatory follicles. Domestic Animal Endocrinology, 40, 98–109.
LeBlanc SJ. 2014. Reproductive tract inflammatory disease in postpartum dairy cows. Animal, 8(s1), 54–63.
Lee JI, Kim IH. 2007. Pregnancy loss in dairy cows: the contributing factors, the effects on reproductive performance and the economic impact. Journal of Veterinary Science, 8(3), 283–288.
Lopdell T, Berg MC, Green MP, Back PJ. 2011. Effect of sub-clinical uterine infection on plasma amino acid concentrations in early lactation dairy cows. Proceeding New Zealand Society of Animal Production, 71, 291–295.
Madoz LV, Giuliodori MJ, Jaureguiberry M, Plöntzke J, Drillich M, De la Sota RL. 2013. The relationship between endometrial cytology during estrous cycle and cutoff points for the diagnosis of subclinical endometritis in grazing dairy cows. Journal of Dairy Science, 96(7), 4333–4339.
Madoz LV, Giuliodori MJ, Migliorisi AL, Jaureguiberry M, De la Sota R.L. 2014. Endometrial cytology, biopsy, and bacteriology for the diagnosis of subclinical endometritis in grazing dairy cows. Journal of Dairy Science, 97(1), 195–201.
Pascottini OB, LeBlanc SJ. 2020. Modulation of immune function in the bovine uterus peripartum. Theriogenology, doi: https://doi.org/10.1016/j.theriogenology.2020.01.042
Polat B, Cengiz M, Çolak A, Cannazik O. 2015. Comparison of intrauterine ozone and rifaximine treatment in cows with subclinical endometritis. Kafkas Universitesi Veteriner Fakultesi Dergisi, 21(5), 773–776.
Quintela LA, Fernández MV, Becerra JJ, Barrio MB, García PJ, Martínez IP. 2018. Subclinical Endometritis in Dairy Cattle. In: New Insights into Theriogenology.
Richter KS, Bugge KR, Bromer JG, Levy MJ. 2007. Relationship between endometrial thickness and embryo implantation, based on 1294 cycles of in vitro fertilization with transfer of two blastocyst-stage embryos. Fertility and Sterility, 87(1), 53–59.
Rinaldi M, Moroni P, Paape MJ, Bannerman DD. 2008. Differential alterations in the ability of bovine neutrophils to generate extracellular and intracellular reactive oxygen species during the periparturient period. The Veterinary Journal, 178(2), 208–213.
Rinaudo A, Bernardi SF, Marini PR. 2017. Relation between subclinical endometritis and reproductive efficiency in dairy cows in Argentina. Journal of Veterinary Science and Technology, 8(494), 1–4.
Salasel B, Mokhtari A, Taktaz T. 2010. Prevalence, risk factors for and impact of subclinical endometritis in repeat breeder dairy cows. Theriogenology, 74, 1271–1278.
Samardžija M, Turk R, Sobiech P, Valpotić H, Harapin I, Gračner D, Đuričić D. 2017. Intrauterine ozone treatment of puerperal disorders in domestic ruminants: a review. Veterinarski arhiv, 87(3), 363–375.
Sheldon IM. 2004. The postpartum uterus. Veterinary Clinics of North America. Large Animal Practice, 20(3), 569–591.
Sheldon IM, Dobson H. 2004. Postpartum uterine health in cattle. Animal Reproduction Science, 82, 295–306.
Sheldon IM, Cronin J, Goetze L, Donofrio G, Schuberth H.J. 2009. Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biology of Reproduction, 81(6), 1025–1032.
Sheldon IM, Cronin JG, Healey GD, Gabler C, Heuwieser W, Streyl D, Bromfield JJ, Miyamoto A, Fergani C, Dobson H. 2014. Innate immunity and inflammation of the bovine female reproductive tract in health and disease. Reproduction, 148(3), R41–R51
Soto P, Natzke RP, Hansen PJ. 2003a. Actions of tumor necrosis factor-alpha on oocyte maturation and embryonic development in cattle. American Journal of Reproductive Immunology, 50, 380–388.
Soto P, Natzke RP, Hansen PJ. 2003b. 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, 50, 263–272.
Suzuki C, Yoshioka K, Iwamura S, Hirose H. 2001. Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers. Domestic Animal Endocrinology, 20, 267–278.
Williams EJ, Fischer DP, Pfeiffer DU, England GC, Noakes DE, Dobson H, Sheldon IM. 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology, 63(1), 102–117.
Williams EJ, Fischer DP, Noakes DE, England GC, Rycroft A, Dobson H, Sheldon IM. 2007. The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology, 68(4), 549–559.
Williams EJ, Sibley K, Miller AN, Lane EA, Fishwick J, Nash DM, Herath S, England GC, Dobson H, Sheldon IM. 2008. The effect of Escherichia coli lipopolysaccharide and tumor necrosis factor alpha on ovarian function. American Journal of Reproductive Immunology, 60, 462–473.
Zobel R, Tkalčić S. 2013. Efficacy of ozone and other treatment modalities for retained placenta in dairy cows. Reproduction in Domestic Animals, 48(1), 121–125.
Zobel R, Martinec R, Ivanović D, Rošić N, Stančić Z, Žerjavić I, Flajsig B, Plavec H, Smolec O. 2014. Intrauterine ozone administration for improving fertility rate in Simmental cattle. Veterinarski arhiv, 84(1), 1–8.
The authors thank the Department of Research and Development of ‘La Colina Cia. Ltda’ for the contribution for the contribution to this research. In addition, the authors thank Dr. Gustavo Antunes, ‘La Estanzuela’ experimental station, National Institute of Agricultural Research, INIA, Uruguay, and Dr. Adolfo Toledano-Díaz, Department of Animal Reproduction, INIA, Spain for the critical reading of this manuscript.
The research was supported by Dirección de Investigación de la Universidad de Cuenca (DIUC), Ecuador, throughout project DIUC-XIV-2016-022.
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Escandón, B.M., Espinoza, J.S., Perea, F.P. et al. Intrauterine therapy with ozone reduces subclinical endometritis and improves reproductive performance in postpartum dairy cows managed in pasture-based systems. Trop Anim Health Prod 52, 2523–2528 (2020). https://doi.org/10.1007/s11250-020-02298-3
- Ozone therapy
- Subclinical endometritis
- Reproductive performance