Abstract
The reproductive performance of dairy animals is influenced by several factors, and accumulating lines of evidence indicate that mastitis is one of the determinants. Most of the published information relating mastitis with reproduction has evolved based on retrospective approach rather than controlled clinical studies. The complex nature of both mastitis and reproduction could be a limiting factor for understanding their relationship in detail. In this review, we analyzed the available retrospective studies on the effects of clinical mastitis on reproductive function and explained the possible mechanisms by which mastitis affects reproduction in dairy animals.
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Ahmadzadeh, A., Frago, F., Shafii, B., Dalton, J.C., Price, W. J. and McGuire, M. A. 2009. Effect of clinical mastitis and other diseases on reproductive performance of Holstein cows. Animal Reproduction Science, 112: 273–282.
Al-Katanani, Y. M., Paula-Lopes, F. F. and Hansen, P. J. 2002. Effect of season and exposure to heat stress on oocyte competence in Holstein cows. Journal of Dairy Science, 85:390–396.
Asaf, S., Leitner, G., Furman, O., Lavon, Y., Kalo, D., Wolfenson, D. and Roth, Z. 2013. Effects of Escherichia coli- and Staphylococcus aureus-induced mastitis in lactating cows on oocyte developmental competence. Reproduction, 147 (1): 33–43.
Barker, A., Schrick, F., Lewis, M., Dowlen, H. and Oliver, S. 1998. Influence of clinical mastitis during early lactation on reproductive performance of Jersey cows. Journal of Dairy Science, 81: 1285–1290.
Battaglia, D. F., Beaver, A. B., Harris, T. G., Tanhehco, E., Viguie, C. and Karsch, F. J. 1999. Endotoxin disrupts the estradiol-induced luteinizing hormone surge: interference with estradiol signal reading, not surge release. Endocrinology. 140: 2471–2492.
Battaglia, D. F., Krasa, H. B., Padmanabhan, V., Viguie, C. and Karsch, F. J. 2000. Endocrine alterations that underlie endotoxin-induced disruption of the follicular phase in ewes. Biology of Reproduction, 62:45–53.
Blum, J. W., Dosogne, H., Hoeben, D., Vangroenweghe, F., Hammon, H. M., Bruckmaier, R. M. and Burvenich, C. 2000. Tumor necrosis factor-a and nitrite/nitrate responses during acure mastitis induced by Escherichia coli infection and endotoxin in dairy cows. Domestic Animal Endocrinology, 19: 223–235.
Bouchard, L., Blais, S., Desrosiers, C., Zhao, X. and Lacasse, P. 1999. Nitric oxide production during endotoxin-induced mastitis in the cow. Journal of Dairy Science, 82:2574–2581
Boujenane, I., El Aimani, J. and By, K. 2015. Effects of clinical mastitis on reproductive and milk performance of Holstein cows in Morocco. Tropical Animal Health and Production, 47(1):207–11.
Breen, K. M., Billings, H. J., Debus, N. and Karsch, F. J. 2004. Endotoxin inhibits the surge secretion of gonadotropin-releasing hormone via a prostaglandin-independent pathway. Endocrinology. 145:221–7
Bromfield, J. J. and Sheldon, I. M. 2013. Lipopolysaccharide reduces the primordial follicle pool in the bovine ovarian cortex ex vivo and in the murine ovary in vivo. Biology of Reproduction, 88(4): 981–989
Chebel, R. C., Santos, J. E. P., Reynolds, J. P., Cerri, R. L. A., Juchem, S. O. and Overton, M. 2004. Factors affecting conception rate after artificial insemination and pregnancy loss in lactating dairy cows. Animal Reproduction Science, 84: 239–255
Cullor, J. S. 1990. Mastitis and its influence upon reproductive performance in dairy cattle. in Proc. Int. Symp. Bovine Mastitis, Indianapolis, IN. Natl. Mastitis Counc., Inc. and Am. Assoc. Bovine Pract., Arlington, VA
Deb, G. K., Dey, S. R., Bang, J. I., Cho, S. J., Park, H. C., Lee, J. G. and Kong, I. K. 2011. 9-cis retinoic acid improves developmental competence and embryo quality during maturation of bovine oocytes through the inhibition of oocyte TNF gene expression. Journal of Animal Science, 89:2759–2767
Edwards, J. L. and Hansen, P. J. 1997. Differential responses of bovine oocytes and preimplantation embryos to heat shock. Molecular Reproduction Development, 46:138–145
Filho, V. B. S., Schiavon, R. S., Gastal, G. D. A., Timm, C. D. and Lucia Jr, T. 2012. Association of the occurrence of some diseases with reproductive performance and milk production of dairy herds in southern Brazil. Revista Brasileira de Zootecnia, 41(2), 467–471
Fourichon, C., Seegers, H. and Malher, X. 2000. Effect of disease on reproduction in the dairy cow: a meta-analysis. Theriogenology, 53, 1729–1759
Fuenzalida, M. J. Fricke, P. M. and Ruegg, P. L. 2015. The association between occurrence and severity of subclinical and clinical mastitis on pregnancies per artificial insemination at first service of Holstein cows. Journal of Dairy Science, 98, 3791–3805
Furman, O., Leitner, G., Roth, Z., Lavon, Y., Jacoby, S., Wolfenson, D. 2014. Experimental model of toxin-induced subclinical mastitis and its effect on disruption of follicular function in cows. Theriogenology, 82(8), 1165–72
Gendelman, M., Aroyo, A., Yavin, S. and Roth, Z. (2010). Seasonal effects on gene expression, cleavage timing, and developmental competence of bovine preimplantation embryos. Reproduction, 140:73–82
Gilbert, R. O., Bosu, W. T. K. and Peter, A. T. 1990. The effect of Escherichia coli endotoxin on luteal function on Holstein heifers. Theriogenology, 33, 645–651
Giri, S. N., Emau, P., Cullor, J. S., Stabenfeldt, G. H., Bruss, M. L., Bondurant, R. H. and Osburn, B. I. 1990. Effects of endotoxin infusion on circulating levels of eicosanoids, progesterone, cortisol, glucose and lactic acid, and abortion in pregnant cows. Veterinary Microbiololgy, 21 (3), 211–231
Gómez-Cifuentes, Molineri, C. I., Signorini, A. I., Scandolo, M. L. and Calvinho, D. L. F. 2014. The association between mastitis and reproductive performance in seasonally-calved dairy cows managed on a pasture-based system. Archivos de Medicina Veterinaria, 46, 197–206
Gunay, A. and Gunay, U. 2008. Effects of Clinical Mastitis on Reproductive Performance in Holstein Cows. Acta Veterinaria Brno, 77, 555–560
Hansen, P. J., Soto, P. and Natzke, R. P. 2004. Mastitis and fertility in cattle – possible involvement of inflammation or immune activation in embryonic mortality. American Journal of Reproductive Immunology, 51, 294–301
Harman, J. L., Grohn, Y. T., Erb, H. N. and Casella, G. 1996. Event-time analysis of the effect of season of parturition, parity, and concurrent disease on parturition-to-conception interval in dairy cows. American Journal of Veterinary Research, 57(5), 640–645
Heringstad, B., Chang, Y. M., Andersen-Ranberg, I. M. and Gianola, D. 2006. Genetic analysis of number of mastitis cases and number of services to conception using a censored threshold model. Journal of Dairy Science, 89, 4042–4048
Heringstad, B., Wu, X.-L. and Gianola, D. 2009 Inferring relationships between health and fertility in Norwegian Red cows using recursive models. Journal of Diary Science, 92, 1778–1784
Hertl, J. A., Gröhn, J. A., Leach, J. A., Bar, D., Bennett, G. J., González, R. N., Rauch, B. J., Welcome, F. L., Tauer, L. W. and Schukken, Y. H. 2010. Effects of clinical mastitis caused by gram-positive and gram-negative bacteria and other organisms on the probability of conception in New York State Holstein dairy cows. Journal of Dairy Science, 93, 1551–1560
Hockett, M. E., Hopkins, F. M., Lewis, M. J., Saxton, A. A., Dowlen, H. H., Oliver, S. P. and Schrick, F. N. 2000. Endocrine profiles of dairy cows following experimentally induced clinical mastitis during early lactation. Animal Reproduction Science, 58, 241–251
Hockett, M. E., Almeida, R. A., Rohrbach, N. R., Oliver, S. P., Dowlen, H. H. and Schrick, F. N. 2005. Effects of induced clinical mastitis during preovulation on endocrine and follicular function, Journal of Dairy Science, 88, 2422–2431
Hoeben, D., Burvenich, C., Trevisi, E., Bertoni, G., Hamann, J., Bruckmaier, R.M., Blum, J.W., 2000. Role of endotoxin and TNF- in the pathogenesis of experimentally induced coliform mastitis in periparturient cows. Journal of Dairy Research, 67, 503–514
Hudson, C. D., Bradley, A. J., Breen, J. E. and Green, M. J. 2012. Associations between udder health and reproductive performance in United Kingdom dairy cows. Journal of Dairy Science, 95, 3683–97
Huszenicza, G. Y., Jánosi, S. Z., Kulcsar, M., Kóródi, P., Dieleman, S. J., Bartyik, J. and Ribiczei-Szabó, P. 1998. Gram negative mastitis in early lactation may interfere with ovarian and certain endocrine functions and metabolism in dairy cows. Reproduction in Domestic Animal, 33, 147–153
Jackson, L. R. Farin, C. E. and Whisnant, S. 2012. Tumor necrosis factor alpha inhibits in vitro bovine embryo development through a prostaglandin mediated mechanism. Journal of Animal Science and Biotechnology 3:7.
Kelton, D., Petersson, C., Leslie and Hansen, D. 2001. Associations between Clinical Mastitis and pregnancy on Ontario dairy farms. Proceedings of the 2nd International Symposium on Mastitis and Milk Quality: 200–202
Klaas, I. C., Wessels, U. H., Rothfuss, B. A., Tenhagen, W., Heuwieser and Schallenberger, E. 2004. Factors affecting reproductive performance in German Holstein-Friesian cows with a special focus on postpartum mastitis. Livestock Production Science, 86, 233–238
Krininger, C. E, Stephens, S. H. and Hansen, P. J. 2002. Developmental changes in inhibitory effects of arsenic and heat shock on growth of preimplantation bovine embryos. Molecular Reproduction and Development, 63, 335–340
Kulcsár, M., Jánosi, S., Kátai, L., Kóródy, P., Balogh, O., Delavaud, C., Chilliard, Y. 2004. Mastitis-related endocrine alterations in postpartum (pp) dairy cows. In: Proceedings Annual Meeting European Society of Domestic Animal Reproduction (p. 289). Reproduction in Domestic Animals, 39. Presented at Annual Meeting European Society of Domestic Animal Reproduction (ESDAR), Warsow, POL (2004-09-23 - 2004-09-25)
Lavon, Y., Leitner, G., Goshen, T., Braw-Tal, R., Jacoby, S. and 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., Voet, H. and Wolfenson, D. 2010. Naturally occurring mastitis effects on timing of ovulation, steroid and gonadotrophic hormone concentrations, and follicular and luteal growth in cows. Journal of Dairy Science, 93, 911–921
Lavon, Y., Leitner, G., Klipper, E., Moallem, U., Meidan, R. and Wolfenson, D. 2011a. Subclinical, chronic intramammary infection lowers steroid concentrations and gene expression in bovine preovulatory follicles. Domestic Animal Endocrinology, 40(2), 98–109
Lavon, Y., Leitner, G., Goshen, T., Braw-Tal, R. and Jacoby, S. 2011b. Immediate and carryover effects of Gram-negative or Gram positive toxin-induced mastitis on follicular functions in cows. Theriogenology, 76(5), 942–953.
Lavon, Y., Ezra, E., Leitner, G. and Wolfenson, D. 2011c. Association of conception rate with pattern and level of somatic cell count elevation relative to time of insemination in dairy cows. Journal of Dairy Science, 94(9), 4538–4545
Li, P. S. and Wagner W.C. 1983. In vivo and in vitro studies on the effect of adrenocorticotropic hormone or cortisol on the pituitary response to gonadotropin releasing hormone. Biology of Reproduction, 29, 25
Loeffler, S., Vries, M. and Schukken, Y. 1999. The effects of time of disease occurrence, milk yield, and body conditions on fertility of dairy cows. Journal of Dairy Science, 82, 2589–2604
Lomander, H., Svensson, C., Hallén-Sandgren, C., Gustafsson, H. and Frössling, J. 2013 Associations between decreased fertility and management factors, claw health, and somatic cell count in Swedish dairy cows. Journal of Diary Science, 96, 6315–6323
Lucy, M. C. 2001. Reproductive loss in high-producing dairy cattle: where will it end?. Journal of Diary Science, 84(6), 1277–93
Maizon, D. O., Oltenacu, P. A., Grohn, Y. T., Strawderman, R. L. and Emanuelson, U. 2004. Effects of diseases on reproductive performance in Swedish Red and White dairy cattle. Preventive Veterinary Medicines, 66,113–126
Maltz, E., Devir, S., Metz, J. H. M. and Hogeveen, H. 1997. The body weight of the dairy cow. Introductory study into body weight changes in dairy cows as a management aid. Livestock Production Science, 48, 175
Manimaran, A., Kumaresan, A., Sreela, L., Boopathi, V., Arul Prakash, M. (2014). Effects of Clinical Mastitis on Days Open in Dairy Cattle and Buffaloes. Indian Veterinary Journal, 91(12), 67–68
McCann, SM, Kimura, M., Karanth, S., Yu, W. H. and Rettori, V. 1997. Nitric oxide controls the hypothalamic-pituitary response to cytokines. Neuroimmunomodulation, 4, 98–106
Miller, R. H., Clay, J. S. and Norman, H. D. 2001. Relationship of somatic cell score with fertility measures. Journal of Dairy Science, 84, 2543–2548
Moore, D. A. and Connor, M. L. O. 1993. Coliform mastitis: its possible effects on reproduction in dairy cattle. Proc. Natl. Mastitis Counc. Kansas City, MO. National Mastitis Council, Inc., Arlington, VA. 162–166
Moore, D. A., Cullor, J. S., Bondurant, R. H. and Sischo, W. M. 1991. Preliminary field evidence for the association of clinical mastitis with altered interestrus intervals in dairy cattle. Theriogenology, 36, 257–265
Moore, D. A., M. W., Overton, R. C., Chebel, M. L., Truscott, and BonDurant, R. H. 2005. Evaluation of factors that affect embryonic loss in dairy cattle. Journal of the American Veterinary Medical Association, 226, 1112
Morris, M.J. Walker, S.L. Jones, D.N. Routly, J.E. Smith, R.F. Dobson, H. 2009. Influence of somatic cell count, body condition and lameness on follicular growth and ovulation in dairy cows. Theriogenology, 71: 801–806
Moussavi, A. H. and Mesgaran, M. D. and Gilbert, R. O. 2012. Effect of mastitis during the first lactation on production and reproduction performance of Holstein cows. 44(7), 1567–1573
Nakajima, Y., Mikami, O., Yoshioka, M., Motoi, Y., Ito, T., Ishikawa, Y., Fuse, M., Nakano, K. and Yasukawa, K. 1997. Elevated levels of tumor necrosis factor-a (TNF-a) and interleukin- 6 (IL-6) activities in the sera and milk of cows with naturally occurring coliform mastitis. Research in Veterinary Science, 62, 297–298
Nava-Trujillo, H., Soto-Belloso, E. and Hoet, A. E. 2010. Effects of clinical mastitis from calving to first service on reproductive performance in dual-purpose cows. Animal Reproduction Science, 121, 12–16
Nebel, R. L. and McGilliard, M. L. (1993). Interactions of high milk yield and reproductive performance in dairy cows. Journal of Dairy Science, 76, 3257–3268
Nguyen, T.C., Nakao, T., Gautam, G., Su, L.T., Ranasinghe, R.M.S.B.K., Yusuf, Y. 2011. Relationship between milk somatic cell count and postpartum ovarian cyclicity and fertility in dairy cows. Acta Veterinaria Hungarica, 59: 349–362
Padmanabhan, V., Keech, C. and Convey, E. M. 1983. Cortisol inhibits and adrenocorticotropin has no effect on luteinizing hormone-releasing hormone-induced release of luteinizing hormone from bovine pituitary cells in vitro. Endocrinology, 112:1782–1787
Peake, K. A., Biggs, A. M., Argo, C. M., Smith, R. F., Christley, R. M., Routly, J. E. and Dobson, H. 2011. Effects of lameness, subclinical mastitis and loss of body condition on the reproductive performance of dairy cows. Veterinary Record, 168: 301–307
Perrin, L., Bostelmann, R. W., and Sheldon, I. M. 2007. Reduced conception rates associated with bovine mastitis during a ‘window of opportunity’. Veterinary Record, 161:61–62
Peter, A. T., Bosu, W. T. and DeDecker, R. J. 1989. Suppression of preovulatory luteinizing hormone surges in heifers after intrauterine infusions of Escherichia coli endotoxin. American Journal of Veterinary Research, 50, 368–73
Pinedo, P. J., Donovan, A., Rae, O. and DeLapaz, J. 2009. Association between paratuberculosis infection and general immune status in dairy cattle, International Association for Paratuberculosis, Minneapolis, MN. 127
Podpečan, O., Mrkun, J. and Zrimšek, P. 2013. Associations between the fat to protein ration in milk, health stat us and repro ductive performance in dairy cattle. Slovenian Veterinary Research, 50 (2), 57–66
Rahman, M. M., Mazzilli, M., Pennarossa, G., Brevini, T. A. L., Zecconi, A. and Gandolfi F. 2012. Chronic mastitis is associated with altered ovarian follicle development in dairy cattle. Journal of Dairy Science, 95, 1885–1893
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. and 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
Risco, C. A., Donovan, G. A. and Hernandez, J. 1999. Clinical mastitis associated with abortion in dairy cows. Journal of Dairy Science, 82, 1684–1689
Roth, Z., Dvir, A., Kalo, D., Lavon, Y., Krifucks, O., Wolfenson, D. and Leitner, G. 2013. Naturally occurring mastitis disrupts developmental competence of bovine oocytes. Journal of Dairy Science, 96, 6499–6505.
Santos, J. E. P., Cerri, R. L. A., Ballou, M. A., Higginbotham, G. E. and Kirk, J. H. 2004. Effect of timing of first clinical mastitis occurrence on lactational and reproductive performance of Holstein dairy cows. Animal Reproduction Science, 80, 31–45
Schrick, F., Hockett, M., Saxton, A., Lewis, M., Dowlen, H. and Oliver, S. 2001. Influence of subclinical mastitis during early lactation on reproductive parameters. Journal of Dairy Science, 84, 1407–1412
Seals, R. C., Lemaster, J. W., Hopkins, F. M. and Schrick, F. N. 1998. Effects of elevated concentrations of prostaglandin F2 alpha on pregnancy rates in progestogen supplemented cattle. Prostaglandins & Other Lipid Mediators, 56, 377–89
Skarzynski DJ, Miyamoto Y, Okuda K 2000. Production of prostaglandin F 2a by cultured bovine endometrial cells in response to tumor necrosis factor a: cell type specificity and intracellular mechanisms. Biology of Reproduction, 62, 1116–1120
Soto, P., Natzke, R. P. and Hansen, P. J. 2003. Identification of possible mediators of embryonic mortality caused by mastitis: Actions of lipopolysaccharide, prostaglandin F2α, 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. and Hirose, H. 2001. Endotoxin induces delayed ovulation following endocrine aberration during the proestrous phase in Holstein heifers. Domestic Animal Endocrinology, 20, 267–78
Vacek, M., Stádník, L. and Štípk, M. 2007. Relationships between the incidence of health disorders and the reproduction traits of Holstein cows in the Czech Republic. Czech Journal of Animal Science, 52(8), 227–235
Waller, K.P., I.G. Colditz, K. and Östensson. 2003. Cytokines in mammary lymph and milk during endotoxin-induced bovine mastitis. Research in Veterinary Science, 74: 31
Wenz, J. R., Barrington, G. M., Garry, F. B., McSweeney, F. B., Dinsmore, R. P., Goodell, G. and Callan, R. J. 2001. Bacteremia associated with naturally occurring acute coliform mastitis dairy cows. Journal of the American Veterinary Medical Association, 219, 976
Wilson, D. J., Grohn,Y. T., Bennett, G. J., González, R. N., Schukken, Y. H. and Spatz, J. 2008. Milk Production Change Following Clinical Mastitis and Reproductive Performance Compared Among J5 Vaccinated and Control Dairy Cattle. Journal of Dairy Science, 91, 3869–3879
Windig, J.J., Calus, M.P.L. and Veerkamp, R.F. 2005. Influence of herd environment on health and fertility and their relationship with milk production. Journal of Dairy Science, 88(1), 335–347
Wuu, Y. D., Pampfer, S., Becquet, P., Vanderheyden, I., Lee, K. H. and De Hertogh, R. 1999. Tumor necrosis factor a decreases the viability of mouse blastocyst in vitro and in vivo. Biology of Reproduction, 60:479–483
Yang, F. L., Li, X. S., Yang, B. Z., Zhang, Y., Zhang, X. F., Qin, G. S. and Liang, X. W. 2012. Clinical mastitis from calving to next conception negatively affected reproductive performance of dairy cows in Nanning, China. African Journal of Biotechnology, 11(10), 2574–2580
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Kumar, N., Manimaran, A., Kumaresan, A. et al. Mastitis effects on reproductive performance in dairy cattle: a review. Trop Anim Health Prod 49, 663–673 (2017). https://doi.org/10.1007/s11250-017-1253-4
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DOI: https://doi.org/10.1007/s11250-017-1253-4