Abstract
The purpose of this study was to evaluate the effect of retained placenta (RP) and clinical mastitis (CM) on the reproductive efficiency of crossbred dairy cows during the postpartum period and the effect in some innate immune system indicators. For this, two experiments were carried out. In the first, a total of 232 cows were evaluated and divided as: healthy control (n = 184), RP (n = 22), and CM (n = 26) groups. The RP and CM was evaluated until 30 days postpartum (DPP) and reproductive rates were measured. In experiment 2, cows were divided in control (n = 10), RP (n = 10), and CM (n = 30) groups. Between 40 and 50 DPP, clinical, gynecological examination and endometrial cytobrush were performed to evaluate subclinical endometritis (SE) and gene expression of interleukins 1β (IL-1β) and 6 (IL-6), chemokine ligand 5 (CCL5), estrogen α (ESR1), and progesterone (PGR) receptors by qRT-PCR analysis. In experiment 1, the conception rate at 1st artificial insemination (AI) was lower in RP and CM groups and pregnancy rate at 150 days decreased in CM group. Calving-to-1st AI interval and days open were shorter in healthy cows. In experiment 2, the occurrence of SE was 26.7% and higher in RP and CM groups. The expression of IL-1β increased in RP and CM groups, while IL-6 was less expressed in RP group. The CCL5, ESR1, and PGR were similar between groups. In conclusion, cows with RP and CM had their reproductive efficiency negatively affected and had they initial pro-inflammatory response improved by the increase of IL-β.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability
Not applicable.
References
Barlund, C.S., Carruthers, T.D., Waldner, C.L., Palmer, C.W., 2008. A comparison of diagnostic techniques for postpartum endometritis in dairy cattle. Theriogenology, 69, 714–723. https://doi.org/10.1016/j.theriogenology.2007.12.005
Boos, A., Kohtes, J., Janssen, V., Mülling, C., Stelljes, A., Zerbe, H., Hässig, M., Thole, H.H., 2006. Pregnancy effects on distribution of progesterone receptors, oestrogen receptor α, glucocorticoid receptors, Ki-67 antigen and apoptosis in the bovine interplacentomal uterine wall and foetal membranes. Animal Reproduction Science, 91, 55–76. https://doi.org/10.1016/j.anireprosci.2005.03.012
Bromfield, J.J., Santos, J.E.P., Block, J., Williams, R.S., Sheldon, I.M., 2015. PHYSIOLOGY AND ENDOCRINOLOGY SYMPOSIUM: Uterine infection: Linking infection and innate immunity with infertility in the high-producing dairy cow1,2. Journalof Animal Science, 93, 2021–2033. https://doi.org/10.2527/jas.2014-8496
Buso, R.R., Campos, C.C., Santos, T.R., Saut, J.P.E., Santos, R.M., 2018. Retenção de placenta e endometrite subclínica: prevalência e relação com o desempenho reprodutivo de vacas leiteiras mestiças. Pesquisa Veterinária Brasileira, 38, 1–5. https://doi.org/10.1590/1678-5150-pvb-4707
Campos, C.C., Hartling, I., Kaur, M., Fernandes, A.C.C., Santos, R.M., Cerri, R.L.A., 2018. Intramammary infusion of lipopolysaccharide promotes inflammation and alters endometrial gene expression in lactating Holstein cows. Journal of Dairy Science, 101, 10440–10455. https://doi.org/10.3168/jds.2018-14393
Campos, C.C., do Prado, F.L., dos Reis, J.P.J., Carneiro, L.C., Silva, P.R.B., de Moraes, G.F., dos Santos, R.M., 2020. Effects of clinical mastitis and puerperal diseases on reproductive efficiency of dairy cows. Tropical Animal Health Production, https://doi.org/10.1007/s11250-020-02326-2
Carneiro, L.C., Ferreira, A.F., Padua, M., Saut, J.P., Ferraudo, A.S., dos Santos, R.M., 2014. Incidence of subclinical endometritis and its effects on reproductive performance of crossbred dairy cows. TropicalAnimal Health and Production,. 46, 1435–1439. https://doi.org/10.1007/s11250-014-0661-y
Carneiro, L.C., Cronin, J.G., Sheldon, I.M., 2016. Mechanisms linking bacterial infections of the bovine endometrium to disease and infertility. Reproductive Biology, 16. https://doi.org/10.1016/j.repbio.2015.12.002
Carvalho, M.R., Peñagaricano, F., Santos, J.E.P., DeVries, T.J., McBride, B.W., Ribeiro, E.S., 2019. Long-term effects of postpartum clinical disease on milk production, reproduction, and culling of dairy cows. Journal of Dairy Science, 102, 11701–11717. https://doi.org/10.3168/jds.2019-17025
Collins, T., Read, M.A., Neish, A.S., Whitley, M.Z., Thanos, D., Maniatis, T., 1995. Transcriptional regulation of endothelial cell adhesion molecules: NF-κB and cytokine-inducible enhancers. The FASEB Jounal, 9, 899–909. https://doi.org/10.1096/fasebj.9.10.7542214
Dadarwal, D., Palmer, C., Griebel, P., 2017. Mucosal immunity of the postpartum bovine genital tract. Theriogenology, 104, 62–71. https://doi.org/10.1016/j.theriogenology.2017.08.010
Dahl, M.O., Maunsell, F.P., De Vries, A., Galvao, K.N., Risco, C.A., Hernandez, J.A., 2017. Evidence that mastitis can cause pregnancy loss in dairy cows: A systematic review of observational studies. Journal of Dairy Science, 100, 8322–8329. https://doi.org/10.3168/jds.2017-12711
Dalanezi, F.M., Joaquim, S.F., Guimarães, F.F., Guerra, S.T., Lopes, B.C., Schmidt, E.M.S., Cerri, R.L.A., Langoni, H., 2020. Influence of pathogens causing clinical mastitis on reproductive variables of dairy cows. Journal of Dairy Science, 103, 3648–3655. https://doi.org/10.3168/jds.2019-16841
Dinarello, C.A., 2002. The IL-1 family and inflammatory diseases. Clinical and Experimental Rheumatology, . 20, S1–S13.
Dohmen, M.J.W., Joop, K., Sturk, A., Bols, P.E.J., Lohuis, J.A.C.M., 2000. Relationship between intra-uterine bacterial contamination, endotoxin levels and the development of endometritis in postpartum cows with dystocia or retained placenta. , 54, 1019–1032. https://doi.org/10.1016/S0093-691X(00)00410-6
Dubuc, J., Duffield, T.F., Leslie, K.E., Walton, J.S., LeBlanc, S.J., 2011. Effects of postpartum uterine diseases on milk production and culling in dairy cows. Journal ofDairy Science, 94, 1339–1346. https://doi.org/10.3168/jds.2010-3758
Edmonson, A.J., Lean, I.J., Weaver, L.D., Farver, T., Webster, G., 1989. A Body Condition Scoring Chart for Holstein Dairy Cows. Journal of Dairy Science, 72, 68–78. https://doi.org/10.3168/jds.S0022-0302(89)79081-0
Fagundes, N.S., Rezende, A.L., Alvarenga, P.B., Magalhães, L.Q., Santos, R.M., Headley, S.A., Silva, M.J.B., Beletti, M.E., Saut, J.P.E., 2019. Short communication: Proinflammatory gene expression relative to the collection technique of endometrial samples from cows with and without subclinical endometritis. Journal of Dairy Science, . 102, 5511–5517. https://doi.org/10.3168/jds.2018-15212
Francisco Leydson F. Feitosa, 2008. Semiologia Veterinária - A Arte do Diagnóstico.
Fischer, C., Drillich, M., Odau, S., Heuwieser, W., Einspanier, R., Gabler, C., 2010. Selected pro-inflammatory factor transcripts in bovine endometrial epithelial cells are regulated during the oestrous cycle and elevated in case of subclinical or clinical endometritis. Reproduction, Fertility and Developmen, 22, 818. https://doi.org/10.1071/RD09120
Fourichon, C., Seegers, H., Malher, X., 2000. Effect of disease on reproduction in the dairy cow: a meta-analysis. Theriogenology, 53, 1729–1759. https://doi.org/10.1016/S0093-691X(00)00311-3
Gilbert, R.O., Shin, S.T., Guard, C.L., Erb, H.N., Frajblat, M., 2005. Prevalence of endometritis and its effects on reproductive performance of dairy cows. Theriogenology, 64, 1879–1888. https://doi.org/10.1016/j.theriogenology.2005.04.022
Hammer, J., Morton, J., Kerrisk, K., 2012. Quarter-milking-, quarter-, udder- and lactation-level risk factors and indicators for clinical mastitis during lactation in pasture-fed dairy cows managed in an automatic milking system. The Australian Veterinary Journal,90, 167–174. https://doi.org/10.1111/j.1751-0813.2012.00917.x
Hammon, D.S., Evjen, I.M., Dhiman, T.R., Goff, J.P., Walters, J.L., 2006. Neutrophil function and energy status in Holstein cows with uterine health disorders. Veterinary immunology and immunopathology,113, 21–29. https://doi.org/10.1016/j.vetimm.2006.03.022
Heinrich, P.C., Castell, J. V, Andus, T., 1990. Interleukin-6 and the acute phase response. Biochemical Journal 265, 621–636. https://doi.org/10.1042/bj2650621
Horlock, A.D., Piersanti, R.L., Ramirez-Hernandez, R., Yu, F., Ma, Z., Jeong, K.C., Clift, M.J.D., Block, J., Santos, J.E.P., Bromfield, J.J., Sheldon, I.M., 2020. Uterine infection alters the transcriptome of the bovine reproductive tract three months later. Reproduction, 160, 93–107. https://doi.org/10.1530/REP-19-0564
Huber, A., Kunkel, S., Todd, R., Weiss, S., 1991. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science, (80-. ). 254, 99–102. https://doi.org/10.1126/science.1718038
Hudson, C.D., Bradley, A.J., Breen, J.E., Green, M.J., 2012. Associations between udder health and reproductive performance in United Kingdom dairy cows. Journal of Dairy Science, 95, 3683–3697. https://doi.org/10.3168/jds.2011-4629
Huszenicza, G., Janosi, S., Kulcsar, M., Korodi, P., Reiczigel, J., Katai, L., Peters, A., De Rensis, F., 2005. Effects of Clinical Mastitis on Ovarian Function in Post-partum Dairy Cows. Reproduction in Domestic Animals, 40, 199–204. https://doi.org/10.1111/j.1439-0531.2005.00571.x
Ishikawa, Y., Nakada, K., Hagiwara, K., Kirisawa, R., Iwai, H., Moriyoshi, M., Sawamukai, Y., 2004. Changes in Interleukin-6 Concentration in Peripheral Blood of Pre- and Post-Partum Dairy Cattle and Its Relationship to Postpartum Reproductive Diseases. The Journal of Veterinary Medical Science, 66, 1403–1408. https://doi.org/10.1292/jvms.66.1403
Karsch, F.J., Battaglia, D.F., Breen, K.M., Debus, N., Harris, T.G., 2002. Mechanisms for Ovarian Cycle Disruption by Immune/inflammatory Stress. Stress, 5, 101–112. https://doi.org/10.1080/10253890290027868
Kasimanickam, R., Duffield, T.., Foster, R.., Gartley, C.., Leslie, K.., Walton, J.., Johnson, W.., 2004. Endometrial cytology and ultrasonography for the detection of subclinical endometritis in postpartum dairy cows. Theriogenology, 62, 9–23. https://doi.org/10.1016/j.theriogenology.2003.03.001
Kimura, K., Goff, J.P., Kehrli, M.E., Reinhardt, T.A., 2002. Decreased Neutrophil Function as a Cause of Retained Placenta in Dairy Cattle. Journal of Dairy Science 85, 544–550. https://doi.org/10.3168/jds.S0022-0302(02)74107-6
Koh, A., da Silva, A.P.B., Bansal, A.K., Bansal, M., Sun, C., Lee, H., Glogauer, M., Sodek, J., Zohar, R., 2007. Role of osteopontin in neutrophil function. Immunology, 122, 466–475. https://doi.org/10.1111/j.1365-2567.2007.02682.x
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. https://doi.org/10.1016/j.domaniend.2010.09.004
LeBlanc, S.J., 2014. Reproductive tract inflammatory disease in postpartum dairy cows. Animal, 8, 54–63. https://doi.org/10.1017/S1751731114000524
LeBlanc, S.J., Osawa, T., Dubuc, J., 2011. Reproductive tract defense and disease in postpartum dairy cows. Theriogenology, 76, 1610–1618. https://doi.org/10.1016/j.theriogenology.2011.07.017
McDougall, S., Macaulay, R., Compton, C., 2007. Association between endometritis diagnosis using a novel intravaginal device and reproductive performance in dairy cattle. Animal Reproduction Science, 99, 9–23. https://doi.org/10.1016/j.anireprosci.2006.03.017
Moraes, F.E., 2010. Reprodução da fêmea bovina: fisiologia aplicada e problemas mais comuns (causas e tratamentos).
Nobre, M.M., Coelho, S.G., Haddad, J.P.A., Campos, E.F., Lana, A.M.Q., Reis, R.B., Saturnino, H.M., 2012. Avaliação da incidência e fatores de risco da retenção de placenta em vacas mestiças leiteiras. Arquivo Brassileiro de Medicina Veterinária e Zootecnica, 64, 101–107. https://doi.org/10.1590/S0102-09352012000100015
Remnant, J., Green, M.J., Huxley, J., Hirst-Beecham, J., Jones, R., Roberts, G., Hudson, C.D., 2019. Association of lameness and mastitis with return-to-service oestrus detection in the dairy cow. Veterinay Record, 185, 442–442. https://doi.org/10.1136/vr.105535
Ribeiro, E.S., Carvalho, M.R., 2017. Impact and mechanisms of inflammatory diseases on embryonic development and fertility in cattle. Animal Reproduction, 14, 589–600. https://doi.org/10.21451/1984-3143-AR1002
Ribeiro, E.S., Lima, F.S., Greco, L.F., Bisinotto, R.S., Monteiro, A.P.A., Favoreto, M., Ayres, H., Marsola, R.S., Martinez, N., Thatcher, W.W., Santos, J.E.P., 2013. Prevalence of periparturient diseases and effects on fertility of seasonally calving grazing dairy cows supplemented with concentrates. Journal of Dairy Science, 96, 5682–5697. https://doi.org/10.3168/jds.2012-6335
Ribeiro, E.S., Gomes, G., Greco, L.F., Cerri, R.L.A., Vieira-Neto, A., Monteiro, P.L.J., Lima, F.S., Bisinotto, R.S., Thatcher, W.W., Santos, J.E.P., 2016. Carryover effect of postpartum inflammatory diseases on developmental biology and fertility in lactating dairy cows. Journal of Dairy Science, 99, 2201–2220. https://doi.org/10.3168/jds.2015-10337
Risco, C.A., Donovan, G.A., Hernandez, J., 1999. Clinical Mastitis Associated with Abortion in Dairy Cows. Journal of Dairy Science, 82, 1684–1689. https://doi.org/10.3168/jds.S0022-0302(99)75397-X
Roberson, J.R., 2012. Treatment of Clinical Mastitis. Veterinary Clinics of North America: Food Animal Practice, 28, 271–288. https://doi.org/10.1016/j.cvfa.2012.03.011
Schäubli, M., Ritter, N., Hässig, M., Zerbe, H., Bleul, U., Boos, A., 2008. Progesterone receptors, oestrogen receptor α and glucocorticoid receptors in the bovine intercaruncular uterine wall around parturition. Animal Reproduction Science, 103, 215–227. https://doi.org/10.1016/j.anireprosci.2006.12.015
Shaheen, T., Bilal Ahmad, S., Rehman, M.U., Muzamil, S., Razak Bhat, R., Hussain, I., Bashir, N., Mir, M.U.R., Paray, B.A., Dawood, M.A.O., 2020. Investigations on cytokines and proteins in lactating cows with and without naturally occurring mastitis. Journal of King Saud University - Science,32, 2863–2867. https://doi.org/10.1016/j.jksus.2020.07.009
Sheldon, I.M., Owens, S.E., 2017. Postpartum uterine infection and endometritis in dairy cattle. Animal Reproduction, 14, 622–629. https://doi.org/10.21451/1984-3143-AR1006
Sheldon, I.M., Rycroft, A.N., Zhou, C., 2004. Association between postpartum pyrexia and uterine bacterial infection in dairy cattle. Veterinary Record,154, 289–293. https://doi.org/10.1136/vr.154.10.289
Sheldon, I.M., Lewis, G.S., LeBlanc, S., Gilbert, R.O., 2006. Defining postpartum uterine disease in cattle. Theriogenology, 65, 1516–1530. https://doi.org/10.1016/j.theriogenology.2005.08.021
Sheldon, I.M., Williams, E.J., Miller, A.N.A., Nash, D.M., Herath, S., 2008. Uterine diseases in cattle after parturition. The Veterinary Journal, 176, 115–121. https://doi.org/10.1016/j.tvjl.2007.12.031
Sheldon, I.M., 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 Cattle1. Biology of Reproduction, 81, 1025–1032. https://doi.org/10.1095/biolreprod.109.077370
Sheldon, I.M., Cronin, J.G., Bromfield, J.J., 2019. Tolerance and Innate Immunity Shape the Development of Postpartum Uterine Disease and the Impact of Endometritis in Dairy Cattle. Annual Review of Animal Bioscience, 7, 361–384. https://doi.org/10.1146/annurev-animal-020518-115227
Singh, J., Murray, R.D., Mshelia, G., Woldehiwet, Z., 2008. The immune status of the bovine uterus during the peripartum period. The Veterinary Journal, 175, 301–309. https://doi.org/10.1016/j.tvjl.2007.02.003
van den Borne, B.H.P., van Schaik, G., Lam, T.J.G.M., Nielen, M., 2010. Variation in herd level mastitis indicators between primi- and multiparae in Dutch dairy herds. Preventive Veterinary Medicine, 96, 49–55. https://doi.org/10.1016/j.prevetmed.2010.05.010
Wathes, D.C., Cheng, Z., Chowdhury, W., Fenwick, M.A., Fitzpatrick, R., Morris, D.G., Patton, J., Murphy, J.J., 2009. Negative energy balance alters global gene expression and immune responses in the uterus of postpartum dairy cows. Physiological Genomics, 39, 1–13. https://doi.org/10.1152/physiolgenomics.00064.2009
Zerbe, H., Schneider, N., Leibold, W., Wensing, T., Kruip, T.A.M., Schuberth, H.J., 2000. Altered functional and immunophenotypical properties of neutrophilic granulocytes in postpartum cows associated with fatty liver. Theriogenology, 54, 771–786. https://doi.org/10.1016/S0093-691X(00)00389-7
Acknowledgements
The authors thank the dairy farms and their employees for allowing their animals for this study, the Nanobiotechnology Laboratory (NANOBIO), Tumors Osteoimmunology and Immunology Laboratory and Animal Biotechnology Laboratory (LABIO) of the Federal University of Uberlândia (UFU); the Fundação de Amparo à Pesquisa de Minas Gerais (FAPEMIG) (Universal Demand – 01/2016 process CVZ – APQ-01199-16 – RM Santos); the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship granted (OP Ramos), the São Paulo Research Foundation (FAPESP) Post Doc Scholarship under grant number [2018/16051-7]. and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the productivity scholarship (JPE Saut). This work was carried out with the support of the CAPES – Financing Code 001.
Funding
This study was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)– Financing Code 001, and Fundação de Amparo à Pesquisa de Minas Gerais - FAPEMIG (APQ-01199-16 – RM Santos).
Author information
Authors and Affiliations
Contributions
Oglênia Pereira Ramos: investigation, methodology, writing—original draft. Amanda Lima Rezende: investigation, methodology. Paula Batista de Alvarenga: investigation, methodology. Carla Cristian Campos: investigation, methodology. Estevão Vieira de Rezende: investigation, methodology. Marcelo José Barbosa Silva: methodology. Luisa Cunha Carneiro: writing—review and editing. Giovanna Faria de Moraes: writing—review and editing. João Paulo Saut: conceptualization, funding acquisition, project administration, writing—review and editing. Ricarda Maria dos Santos: investigation, methodology, writing—review and editing.
Corresponding author
Ethics declarations
Ethics approval
All procedures in this study were conducted according to the Ethical Principles in Animal Experimentation approved by the Committee of Ethics in the Use of Animals (CEUA) of the Federal University of Uberlândia, under the protocol 003/17.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ramos, O.P., Rezende, A.L., de Alvarenga, P.B. et al. Effect of retained placenta and clinical mastitis on reproduction parameters, immune response, and steroidogenic receptors gene expression in postpartum crossbred dairy cows. Trop Anim Health Prod 54, 180 (2022). https://doi.org/10.1007/s11250-022-03140-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11250-022-03140-8