Recent advances and future approaches for diagnosis, treatment and management of endometritis in dairy herds
Subject Areas : clinical veterinary scienceKeywords: endometritis, dairy herds, reproductive performance,
Abstract :
High reproductive performance is a decisive factor for production and, hence profitability in modern dairy herds. Although endometritis includes clinical and Cytological endometritis (CYTO) or subclinical endometritis (SCE) is highly prevalent, asymptomatic uterine disease in dairy cows can have numerous negative impacts on the reproductive performance and economic efficiency of the farms, such as reduction in the pregnancy per insemination, extension in calving to conception intervals, Infertility by disrupting uterine and ovarian functions and increase in culling rates. Endometritis can be defined as the superficial inflammation of the endometrium (no deeper than the stratum spongiosum).
References:
1. Ahmadi MR, Makki M, Mirzaei A, Gheisari HR. Effects of hypertonic dextrose and paraffin solution as non-antibiotic treatments of clinical endometritis on reproductive performance of high producing dairy cows. Reprod Domest Anim. 2019;54(5):762-71. http://dx.doi.org/10.1111/rda.13424. PMid:30811668.
2. Ametaj BN, Iqbal S, Selami F, Odhiambo JF, Wang Y, Ganzle MG, Dunn SM, Zebeli Q. Intravaginal administration of lactic acid bacteria modulated the incidence of purulent vaginal discharges, plasma haptoglobin concentrations, and milk production in dairy cows. Res Vet Sci. 2014;96(2):365-70. http://dx.doi.org/10.1016/j.rvsc.2014.02.007. PMid:24612560.
3. Barlund, C., Carruthers, T., Waldner, C., Palmer, C., 2008. A comparison of diagnostic techniques for postpartum endometritis in dairy cattle. Theriogenology 69, 714-723.
4. Barragan AA, Pineiro JM, Schuenemann GM, Rajala-Schultz PJ, Sanders DE, Lakritz J, Bas S. Assessment of daily activity patterns and biomarkers of pain, inflammation, and stress in lactating dairy cows diagnosed with clinical metritis. J Dairy Sci. 2018;101(9):8248-58. http://dx.doi.org/10.3168/jds.2018-14510. PMid:29937269.
5. Bicalho ML, Lima FS, Machado VS, Meira EB Jr, Ganda EK, Foditsch C, Bicalho RC, Gilbert RO. Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriogenology. 2016;85(2):267-74. http://dx.doi.org/10.1016/j.theriogenology.2015.09.043. PMid:26483313.
6. Bittar, J.H., Pinedo, P.J., Risco, C.A., Santos, J.E., Thatcher, W.W., Hencken, K.E., Croyle, S., Gobikrushanth, M., Barbosa, C.C., Vieira-Neto, A., Galvão, K.N., 2014. Inducing ovulation early postpartum influences uterine health and fertility in dairy cows. J Dairy Sci 97, 3558-3569.
7. Bogado Pascottini O, Probo M, LeBlanc SJ, Opsomer G, Hostens M. Assessment of associations between transition diseases and reproductive performance of dairy cows using survival analysis and decision tree algorithms. Prev Vet Med. 2020; 176:104908. http://dx.doi.org/10.1016/j.prevetmed.2020.104908. PMid:32036304.
8. Bondurant, R., 1999. Inflammation in the bovine female reproductive tract. Journal of Animal Science 77, 101-110.
9. Dervishi E, Zhang G, Hailemariam D, Mandal R, Wishart DS, Ametaj BN. Urine metabolic fingerprinting can be used to predict the risk of metritis and highlight the pathobiology of the disease in dairy cows. Metabolomics. 2018;14(6):83. http://dx.doi.org/10.1007/s11306-018-1379-z. PMid:30830348.
10. Dubuc, J., Duffield, T., Leslie, K., Walton, J., LeBlanc, S., 2011. A randomized clinical trial of antibiotic and prostaglandin treatments for uterine health and reproductive performance in dairy cows. Journal of Dairy Science 94, 1325-1338.
11. Escandón BM, Espinoza JS, Perea FP, Quito F, Ochoa R, Lopez GE, Galarza DA, Garzón JP. Intrauterine therapy with ozone reduces subclinical endometritis and improves reproductive performance in postpartum dairy cows managed in pasture-based systems. Trop Anim Health Prod. 2020. http://dx.doi.org/10.1007/s11250-020-02298-3. PMid:32445159.
12. Espadamala A, Pereira R, Pallares P, Lago A, Silva-Del-Rio N. Metritis diagnosis and treatment practices in 45 dairy farms in California. J Dairy Sci. 2018;101(10):9608-16. http://dx.doi.org/10.3168/jds.2017-14296. PMid:30077455.
13. Fabio Soares de Lima, 2020, Recent advances and future directions for uterine diseases diagnosis, pathogenesis, and management in dairy cows. Anim Reprod. 2020;17(3): e20200063 https://doi.org/10.1590/1984-3143-AR2020-0063
14. Farhoodi, M., Lashgari, S., Akbari, Gh., Eslampour, M. A., Tajik, P., Effects of G6G Timed Artificial Insemination Associated with 1 or 2 Prostaglandin F2α Pre-synchronization on Cytological Endometritis in Dairy Cows, 2023 under publication
15. Freick M, Kunze A, Passarge O, Weber J, Geidel S. Metritis vaccination in Holstein dairy heifers using a herd-specific multivalent vaccine - Effects on uterine health and fertility in first lactation. Anim Reprod Sci. 2017; 184:160-71. http://dx.doi.org/10.1016/j.anireprosci.2017.07.011. PMid:28760665.
16. Galvão KN, Bicalho RC, Jeon SJ. Symposium review: the uterine microbiome associated with the development of uterine disease in dairy cows. J Dairy Sci. 2019a;102(12):11786-97. http://dx.doi.org/10.3168/jds.2019-17106. PMid:31587913.
17. Galvão, K., Frajblat, M., Brittin, S., Butler, W., Guard, C., Gilbert, R., 2009. Effect of prostaglandin F2α on subclinical endometritis and fertility in dairy cows. Journal of Dairy Science 92, 4906-4913.
18. Genís S, Cerri RLA, Bach A, Silper BF, Baylao M, Denis-Robichaud J, Arís A. Pre-calving intravaginal administration of lactic acid bacteria reduces metritis prevalence and regulates blood neutrophil gene expression after calving in dairy cattle. Front Vet Sci. 2018; 5:135. http://dx.doi.org/10.3389/fvets.2018.00135. PMid:29977896.
19. Haimerl P, Heuwieser W, Arlt S. Short communication: a meta-analysis on therapy of bovine endometritis with prostaglandin F2alpha-An update. J Dairy Sci. 2018;101(11):10557-64. http://dx.doi.org/10.3168/jds.2018-14933. PMid:30172399.
20. Jeon SJ, Lima FS, Vieira-Neto A, Machado VS, Lima SF, Bicalho RC, Santos JEP, Galvão KN. Shift of uterine microbiota associated with antibiotic treatment and cure of metritis in dairy cows. Vet Microbiol. 2018; 214:132-9. http://dx.doi.org/10.1016/j.vetmic.2017.12.022. PMid:29408025.
21. Kasimanickam, R., Duffield, T., Foster, R., Gartley, C., Leslie, K., Walton, J., Johnson, W., 2005. The effect of a single administration of cephapirin or cloprostenol on the reproductive performance of dairy cows with subclinical endometritis. Theriogenology 63, 818-830.
22. Krpálková, L., Cabrera, V., Kvapilík, J., Burdych, J., Crump, P., 2014. Associations between age at first calving, rearing average daily weight gain, herd milk yield and dairy herd production, reproduction, and profitability. Journal of Dairy Science 97, 6573-6582.
23. LeBlanc, S.J., 2008. Postpartum uterine disease and dairy herd reproductive performance: a review. The Veterinary Journal 176, 102-114.
24. Lima FS, Bisinotto RS, Ribeiro ES, Greco LF, Ayres H, Favoreto MG, Carvalho MR, Galvão KN, Santos JE. Effects of 1 or 2 treatments with prostaglandin F (2)alpha on subclinical endometritis and fertility in lactating dairy cows inseminated by timed artificial insemination. J Dairy Sci. 2013;96(10):6480-8. http://dx.doi.org/10.3168/jds.2013-6850. PMid:23910554.
25. Lima FS, Vieira-Neto A, Snodgrass JA, De Vries A, Santos JEP. Economic comparison of systemic antimicrobial therapies for metritis in dairy cows. J Dairy Sci. 2019;102(8):7345-58. http://dx.doi.org/10.3168/jds.2018-15383. PMid:31178192.
26. Lima FS, Vieira-Neto A, Vasconcellos GS, Mingoti RD, Karakaya E, Sole E, Bisinotto RS, Martinez N, Risco CA, Galvão KN, Santos JE. Efficacy of ampicillin trihydrate or ceftiofur hydrochloride for treatment of metritis and subsequent fertility in dairy cows. J Dairy Sci. 2014;97(9):5401-14. http://dx.doi.org/10.3168/jds.2013-7569. PMid:24952780.
27. Lopes F, Rosa G, Pinedo P, Santos JEP, Chebel RC, Galvão KN, Schuenemann GM, Bicalho RC, Gilbert RO, Rodrigez-Zas S, Seabury CM, Thatcher W. Genome-enable prediction for health traits using high-density SNP panel in US Holstein cattle. Anim Genet. 2020;51(2):192-9. http://dx.doi.org/10.1111/age.12892. PMid:31909828.
28. McNeel AK, Reiter BC, Weigel D, Osterstock J, Di Croce FA. Validation of genomic predictions for wellness traits in US Holstein cows. J Dairy Sci. 2017;100(11):9115-24. http://dx.doi.org/10.3168/jds.2016-12323. PMid:28865850.
29. Moore SG, Ericsson AC, Behura SK, Lamberson WR, Evans TJ, McCabe MS, Poock SE, Lucy MC. Concurrent and long-term associations between the endometrial microbiota and endometrial transcriptome in postpartum dairy cows. BMC Genomics. 2019;20(1):405. http://dx.doi.org/10.1186/s12864-019-5797-8. PMid:31117952.
30. Overton, M., Fetrow, J., 2008. Economics of postpartum uterine health. Proc Dairy Cattle Reproduction Council, 39-44.
31. Piersanti RL, Horlock AD, Block J, Santos JEP, Sheldon IM, Bromfield JJ. Persistent effects on bovine granulosa cell transcriptome after resolution of uterine disease. Reproduction. 2019;158(1):35-46. http://dx.doi.org/10.1530/REP-19-0037. PMid:30933928.
32. Pinedo PJ, Velez JS, Bothe H, Merchan D, Pineiro JM, Risco CA. Effect of intrauterine infusion of an organic-certified product on uterine health, survival, and fertility of dairy cows with toxic puerperal metritis. J Dairy Sci. 2015;98(5):3120-32. http://dx.doi.org/10.3168/jds.2014-8944. PMid:25771053.
33. Pomeroy B, Sipka A, Hussen J, Eger M, Schukken Y, Schuberth HJ. Counts of bovine monocyte subsets prior to calving are predictive for postpartum occurrence of mastitis and metritis. Vet Res (Faisalabad). 2017;48(1):13. http://dx.doi.org/10.1186/s13567-017-0415-8. PMid:28222802.
34. Ribeiro ES. Symposium review: Lipids as regulators of conceptus development: Implications for metabolic regulation of reproduction in dairy cattle. J Dairy Sci. 2018;101(4):3630-41. http://dx.doi.org/10.3168/jds.2017-13469. PMid:29174158.
35. Sheldon IM, Rycroft AN, Dogan B, Craven M, Bromfield JJ, Chandler A, Roberts MH, Price SB, Gilbert RO, Simpson KW. 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. http://dx.doi.org/10.1371/journal.pone.0009192. PMid:20169203.
36. Sheldon IM. Metabolic stress and endometritis in dairy cattle. Vet Rec. 2018;183(4):124-5. http://dx.doi.org/10.1136/vr.k3186. PMid:30054409.
37. Sheldon, I.M., Lewis, G.S., LeBlanc, S., Gilbert, R.O., 2006. Defining postpartum uterine disease in cattle. Theriogenology 65, 1516-1530.
38. Stangaferro ML, Wijma R, Caixeta LS, Al-Abri MA, Giordano JO. Use of rumination and activity monitoring for the identification of dairy cows with health disorders: part III. Metritis. J Dairy Sci. 2016;99(9):7422-33. http://dx.doi.org/10.3168/jds.2016-11352. PMid:27372583.
39. Wagener, K., Gabler, C., Drillich, M., 2017. A review of the ongoing discussion about the definition, diagnosis and pathomechanism of subclinical endometritis in dairy cows. Theriogenology 94, 21-30.
40. Williams, E.J., Fischer, D.P., Pfeiffer, D.U., England, G.C., Noakes, D.E., Dobson, H., Sheldon, I.M., 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63, 102-117.
41. Wisnieski L, Norby B, Pierce SJ, Becker T, Gandy JC, Sordillo LM. Cohort-level disease prediction using aggregate biomarker data measured at dry-off in transition dairy cattle: A proof-of-concept study. Prev Vet Med. 2019; 169:104701. http://dx.doi.org/10.1016/j.prevetmed.2019.104701. PMid:31311637.
42. World Health Organization – WHO. WHO guidelines on the use of medically important antimicrobials in food-producing animals [Internet]. Genebra: WHO; 2017 [cited 2020 May 30]. Available from: https://apps.who.int/iris/handle/10665/258970
43. Zhang G, Deng Q, Mandal R, Wishart DS, Ametaj BN. DI/LC-MS/MS-based metabolic profiling for identification of early predictive serum biomarkers of metritis in transition dairy cows. J Agric Food Chem. 2017;65(38):8510-21. http://dx.doi.org/10.1021/acs.jafc.7b02000. PMid:28862839.
1. Ahmadi MR, Makki M, Mirzaei A, Gheisari HR. Effects of hypertonic dextrose and paraffin solution as non-antibiotic treatments of clinical endometritis on reproductive performance of high producing dairy cows. Reprod Domest Anim. 2019;54(5):762-71. http://dx.doi.org/10.1111/rda.13424. PMid:30811668.
2. Ametaj BN, Iqbal S, Selami F, Odhiambo JF, Wang Y, Ganzle MG, Dunn SM, Zebeli Q. Intravaginal administration of lactic acid bacteria modulated the incidence of purulent vaginal discharges, plasma haptoglobin concentrations, and milk production in dairy cows. Res Vet Sci. 2014;96(2):365-70. http://dx.doi.org/10.1016/j.rvsc.2014.02.007. PMid:24612560.
3. Barlund, C., Carruthers, T., Waldner, C., Palmer, C., 2008. A comparison of diagnostic techniques for postpartum endometritis in dairy cattle. Theriogenology 69, 714-723.
4. Barragan AA, Pineiro JM, Schuenemann GM, Rajala-Schultz PJ, Sanders DE, Lakritz J, Bas S. Assessment of daily activity patterns and biomarkers of pain, inflammation, and stress in lactating dairy cows diagnosed with clinical metritis. J Dairy Sci. 2018;101(9):8248-58. http://dx.doi.org/10.3168/jds.2018-14510. PMid:29937269.
5. Bicalho ML, Lima FS, Machado VS, Meira EB Jr, Ganda EK, Foditsch C, Bicalho RC, Gilbert RO. Associations among Trueperella pyogenes, endometritis diagnosis, and pregnancy outcomes in dairy cows. Theriogenology. 2016;85(2):267-74. http://dx.doi.org/10.1016/j.theriogenology.2015.09.043. PMid:26483313.
6. Bittar, J.H., Pinedo, P.J., Risco, C.A., Santos, J.E., Thatcher, W.W., Hencken, K.E., Croyle, S., Gobikrushanth, M., Barbosa, C.C., Vieira-Neto, A., Galvão, K.N., 2014. Inducing ovulation early postpartum influences uterine health and fertility in dairy cows. J Dairy Sci 97, 3558-3569.
7. Bogado Pascottini O, Probo M, LeBlanc SJ, Opsomer G, Hostens M. Assessment of associations between transition diseases and reproductive performance of dairy cows using survival analysis and decision tree algorithms. Prev Vet Med. 2020; 176:104908. http://dx.doi.org/10.1016/j.prevetmed.2020.104908. PMid:32036304.
8. Bondurant, R., 1999. Inflammation in the bovine female reproductive tract. Journal of Animal Science 77, 101-110.
9. Dervishi E, Zhang G, Hailemariam D, Mandal R, Wishart DS, Ametaj BN. Urine metabolic fingerprinting can be used to predict the risk of metritis and highlight the pathobiology of the disease in dairy cows. Metabolomics. 2018;14(6):83. http://dx.doi.org/10.1007/s11306-018-1379-z. PMid:30830348.
10. Dubuc, J., Duffield, T., Leslie, K., Walton, J., LeBlanc, S., 2011. A randomized clinical trial of antibiotic and prostaglandin treatments for uterine health and reproductive performance in dairy cows. Journal of Dairy Science 94, 1325-1338.
11. Escandón BM, Espinoza JS, Perea FP, Quito F, Ochoa R, Lopez GE, Galarza DA, Garzón JP. Intrauterine therapy with ozone reduces subclinical endometritis and improves reproductive performance in postpartum dairy cows managed in pasture-based systems. Trop Anim Health Prod. 2020. http://dx.doi.org/10.1007/s11250-020-02298-3. PMid:32445159.
12. Espadamala A, Pereira R, Pallares P, Lago A, Silva-Del-Rio N. Metritis diagnosis and treatment practices in 45 dairy farms in California. J Dairy Sci. 2018;101(10):9608-16. http://dx.doi.org/10.3168/jds.2017-14296. PMid:30077455.
13. Fabio Soares de Lima, 2020, Recent advances and future directions for uterine diseases diagnosis, pathogenesis, and management in dairy cows. Anim Reprod. 2020;17(3): e20200063 https://doi.org/10.1590/1984-3143-AR2020-0063
14. Farhoodi, M., Lashgari, S., Akbari, Gh., Eslampour, M. A., Tajik, P., Effects of G6G Timed Artificial Insemination Associated with 1 or 2 Prostaglandin F2α Pre-synchronization on Cytological Endometritis in Dairy Cows, 2023 under publication
15. Freick M, Kunze A, Passarge O, Weber J, Geidel S. Metritis vaccination in Holstein dairy heifers using a herd-specific multivalent vaccine - Effects on uterine health and fertility in first lactation. Anim Reprod Sci. 2017; 184:160-71. http://dx.doi.org/10.1016/j.anireprosci.2017.07.011. PMid:28760665.
16. Galvão KN, Bicalho RC, Jeon SJ. Symposium review: the uterine microbiome associated with the development of uterine disease in dairy cows. J Dairy Sci. 2019a;102(12):11786-97. http://dx.doi.org/10.3168/jds.2019-17106. PMid:31587913.
17. Galvão, K., Frajblat, M., Brittin, S., Butler, W., Guard, C., Gilbert, R., 2009. Effect of prostaglandin F2α on subclinical endometritis and fertility in dairy cows. Journal of Dairy Science 92, 4906-4913.
18. Genís S, Cerri RLA, Bach A, Silper BF, Baylao M, Denis-Robichaud J, Arís A. Pre-calving intravaginal administration of lactic acid bacteria reduces metritis prevalence and regulates blood neutrophil gene expression after calving in dairy cattle. Front Vet Sci. 2018; 5:135. http://dx.doi.org/10.3389/fvets.2018.00135. PMid:29977896.
19. Haimerl P, Heuwieser W, Arlt S. Short communication: a meta-analysis on therapy of bovine endometritis with prostaglandin F2alpha-An update. J Dairy Sci. 2018;101(11):10557-64. http://dx.doi.org/10.3168/jds.2018-14933. PMid:30172399.
20. Jeon SJ, Lima FS, Vieira-Neto A, Machado VS, Lima SF, Bicalho RC, Santos JEP, Galvão KN. Shift of uterine microbiota associated with antibiotic treatment and cure of metritis in dairy cows. Vet Microbiol. 2018; 214:132-9. http://dx.doi.org/10.1016/j.vetmic.2017.12.022. PMid:29408025.
21. Kasimanickam, R., Duffield, T., Foster, R., Gartley, C., Leslie, K., Walton, J., Johnson, W., 2005. The effect of a single administration of cephapirin or cloprostenol on the reproductive performance of dairy cows with subclinical endometritis. Theriogenology 63, 818-830.
22. Krpálková, L., Cabrera, V., Kvapilík, J., Burdych, J., Crump, P., 2014. Associations between age at first calving, rearing average daily weight gain, herd milk yield and dairy herd production, reproduction, and profitability. Journal of Dairy Science 97, 6573-6582.
23. LeBlanc, S.J., 2008. Postpartum uterine disease and dairy herd reproductive performance: a review. The Veterinary Journal 176, 102-114.
24. Lima FS, Bisinotto RS, Ribeiro ES, Greco LF, Ayres H, Favoreto MG, Carvalho MR, Galvão KN, Santos JE. Effects of 1 or 2 treatments with prostaglandin F (2)alpha on subclinical endometritis and fertility in lactating dairy cows inseminated by timed artificial insemination. J Dairy Sci. 2013;96(10):6480-8. http://dx.doi.org/10.3168/jds.2013-6850. PMid:23910554.
25. Lima FS, Vieira-Neto A, Snodgrass JA, De Vries A, Santos JEP. Economic comparison of systemic antimicrobial therapies for metritis in dairy cows. J Dairy Sci. 2019;102(8):7345-58. http://dx.doi.org/10.3168/jds.2018-15383. PMid:31178192.
26. Lima FS, Vieira-Neto A, Vasconcellos GS, Mingoti RD, Karakaya E, Sole E, Bisinotto RS, Martinez N, Risco CA, Galvão KN, Santos JE. Efficacy of ampicillin trihydrate or ceftiofur hydrochloride for treatment of metritis and subsequent fertility in dairy cows. J Dairy Sci. 2014;97(9):5401-14. http://dx.doi.org/10.3168/jds.2013-7569. PMid:24952780.
27. Lopes F, Rosa G, Pinedo P, Santos JEP, Chebel RC, Galvão KN, Schuenemann GM, Bicalho RC, Gilbert RO, Rodrigez-Zas S, Seabury CM, Thatcher W. Genome-enable prediction for health traits using high-density SNP panel in US Holstein cattle. Anim Genet. 2020;51(2):192-9. http://dx.doi.org/10.1111/age.12892. PMid:31909828.
28. McNeel AK, Reiter BC, Weigel D, Osterstock J, Di Croce FA. Validation of genomic predictions for wellness traits in US Holstein cows. J Dairy Sci. 2017;100(11):9115-24. http://dx.doi.org/10.3168/jds.2016-12323. PMid:28865850.
29. Moore SG, Ericsson AC, Behura SK, Lamberson WR, Evans TJ, McCabe MS, Poock SE, Lucy MC. Concurrent and long-term associations between the endometrial microbiota and endometrial transcriptome in postpartum dairy cows. BMC Genomics. 2019;20(1):405. http://dx.doi.org/10.1186/s12864-019-5797-8. PMid:31117952.
30. Overton, M., Fetrow, J., 2008. Economics of postpartum uterine health. Proc Dairy Cattle Reproduction Council, 39-44.
31. Piersanti RL, Horlock AD, Block J, Santos JEP, Sheldon IM, Bromfield JJ. Persistent effects on bovine granulosa cell transcriptome after resolution of uterine disease. Reproduction. 2019;158(1):35-46. http://dx.doi.org/10.1530/REP-19-0037. PMid:30933928.
32. Pinedo PJ, Velez JS, Bothe H, Merchan D, Pineiro JM, Risco CA. Effect of intrauterine infusion of an organic-certified product on uterine health, survival, and fertility of dairy cows with toxic puerperal metritis. J Dairy Sci. 2015;98(5):3120-32. http://dx.doi.org/10.3168/jds.2014-8944. PMid:25771053.
33. Pomeroy B, Sipka A, Hussen J, Eger M, Schukken Y, Schuberth HJ. Counts of bovine monocyte subsets prior to calving are predictive for postpartum occurrence of mastitis and metritis. Vet Res (Faisalabad). 2017;48(1):13. http://dx.doi.org/10.1186/s13567-017-0415-8. PMid:28222802.
34. Ribeiro ES. Symposium review: Lipids as regulators of conceptus development: Implications for metabolic regulation of reproduction in dairy cattle. J Dairy Sci. 2018;101(4):3630-41. http://dx.doi.org/10.3168/jds.2017-13469. PMid:29174158.
35. Sheldon IM, Rycroft AN, Dogan B, Craven M, Bromfield JJ, Chandler A, Roberts MH, Price SB, Gilbert RO, Simpson KW. 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. http://dx.doi.org/10.1371/journal.pone.0009192. PMid:20169203.
36. Sheldon IM. Metabolic stress and endometritis in dairy cattle. Vet Rec. 2018;183(4):124-5. http://dx.doi.org/10.1136/vr.k3186. PMid:30054409.
37. Sheldon, I.M., Lewis, G.S., LeBlanc, S., Gilbert, R.O., 2006. Defining postpartum uterine disease in cattle. Theriogenology 65, 1516-1530.
38. Stangaferro ML, Wijma R, Caixeta LS, Al-Abri MA, Giordano JO. Use of rumination and activity monitoring for the identification of dairy cows with health disorders: part III. Metritis. J Dairy Sci. 2016;99(9):7422-33. http://dx.doi.org/10.3168/jds.2016-11352. PMid:27372583.
39. Wagener, K., Gabler, C., Drillich, M., 2017. A review of the ongoing discussion about the definition, diagnosis and pathomechanism of subclinical endometritis in dairy cows. Theriogenology 94, 21-30.
40. Williams, E.J., Fischer, D.P., Pfeiffer, D.U., England, G.C., Noakes, D.E., Dobson, H., Sheldon, I.M., 2005. Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 63, 102-117.
41. Wisnieski L, Norby B, Pierce SJ, Becker T, Gandy JC, Sordillo LM. Cohort-level disease prediction using aggregate biomarker data measured at dry-off in transition dairy cattle: A proof-of-concept study. Prev Vet Med. 2019; 169:104701. http://dx.doi.org/10.1016/j.prevetmed.2019.104701. PMid:31311637.
42. World Health Organization – WHO. WHO guidelines on the use of medically important antimicrobials in food-producing animals [Internet]. Genebra: WHO; 2017 [cited 2020 May 30]. Available from: https://apps.who.int/iris/handle/10665/258970
43. Zhang G, Deng Q, Mandal R, Wishart DS, Ametaj BN. DI/LC-MS/MS-based metabolic profiling for identification of early predictive serum biomarkers of metritis in transition dairy cows. J Agric Food Chem. 2017;65(38):8510-21. http://dx.doi.org/10.1021/acs.jafc.7b02000. PMid:28862839.
