Effect of Metabolic Stress on Ovarian Activity and Reproductive Performance of Dairy Cattle: A Review
الموضوعات :م. فرمان 1 , س. ناندی 2 , و. گریش کومار 3 , س.ک. تریپاسی 4 , پ.س.پ. گوپتا 5
1 - College of Veterinary Science, KVAFSU, Bangalore Campus, Hebbal, Bangalore, India
2 - National Institute of Animal Nutrition and Physiology, Bangalore, India
3 - College of Veterinary Science, KVAFSU, Bangalore Campus, Hebbal, Bangalore, India
4 - National Institute of Animal Nutrition and Physiology, Bangalore, India
5 - National Institute of Animal Nutrition and Physiology, Bangalore, India
الکلمات المفتاحية: dairy cattle, Fertility, non-esterified fatty acids, metabolic stress, negative energy balance,
ملخص المقالة :
Reproductive efficiency in dairy cattle has been decreased over the last 5 decades despite significant gains in genetic selection, improved reproductive technologies and nutritional care. In high-yielding dairy cattle, the negative energy balance (NEB) during the first week post-partum adversely affects ovarian activity, mainly follicle growth and steroidogenesis. Circulating levels of non-esterified fatty acids (NEFAs) and urea are elevated during NEB and are known to be accumulated in the follicular fluid of dominant follicle where they exert adverse effect on oocyte maturation, leading to low fertilization rate and early embryonic development. This study aimed to review the literatures on the interaction between NEB, metabolic stress and reproductive performance of dairy cattle. In this review, the adverse effects of high circulating NEFAs, a biomarker of NEB and urea on oocyte maturation, embryonic quality and developmental and pregnancy outcomes is highlighted.
Adamiak S., Ewen M., Rooke J., Webb R. and Sinclair K. (2005). Diet and fatty acid composition of bovine plasma, granulosa cells and cumulus-oocyte complexes. Reprod. Fertil. Dev. 17, 200-201.
Adewuyi A.A., Gruys E. and Van Eerdenburg F.J. (2005). Non-esterified fatty acids (NEFAs) in dairy cattle: A review. Vet. Quart. 27, 117-126.
Bell A.W. (1995). Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. J. Anim. Sci.73, 2804-2819.
Britt J.H. (1992). Impacts of early postpartum metabolism on follicular development and fertility. Proc. Am. Assoc. Bov. Pract. 24, 39-43.
Butler S.T., Marr A.L., Pelton S.H., Radcliff R.P., Lucy M.C. and Butler W.R. (2003). Insulin restores GH responsiveness during lactation-induced negative energy balance in dairy cattle: effects on expression of IGF-I and GH receptor 1A. J. Endocrinol. 176, 205-217.
Butler W.R. (1998). Effect of protein nutrition on ovarian and uterine physiology in dairy cattle. J. Dairy Sci. 81, 2533-2539.
Butler W.R. and Smith R.D. (1989). Interrelationships between energy balance and postpartum reproductive function in dairy cattle. J. Dairy Sci. 72, 767-783.
Butler W.R., Calaman J.J. and Beam S.W. (1996). Plasma and milk urea nitrogen in relation to pregnancy rate in lactating dairy cattle. J. Anim. Sci. 74, 858-865.
CarsonM.E. (2008). The association of selected metabolites in peripartum dairy cattle with health and production. MS Thesis. University of Guelph, Canada.
Dawuda P.M., Scaramuzzi R.J., Leese H.J., Hall C.J., Peters A.R., Drew S.B. and WathesD.C. (2002). Effect of timing of urea feeding on the yield and quality of embryos in lactating dairy cows. Theriogenology. 58, 1443-1455.
De Wit A.A.C., Cesar M.L.F. and Kruip T.A.M. (2001). Effect of urea during in vitro maturation on nuclear maturation and embryo development of bovine cumulus-oocyte-complexes. J. Dairy Sci. 84, 1800-1804.
El-Azab A.I., Khadr N.A. and Zahran K. (1998). Effect of non-protein nitrogen in the ration on ram semen quality. Small. Rumin. Res. 27, 73-77.
El-Chahida A.A., El-Azab A.I., Rakha A.M. and Farag Y.A. (1977). Some attributes of consideration in buffalo bull selection for artificial insemination purposes. Egypt. J. Vet. Sci. 14, 63-69.
Elrod C.C. and Butler W.R. (1993). Reduction of fertility and alteration of uterine pH in heifers fed excess ruminally degradable protein. J. Anim. Sci. 71, 694-701.
Fahey J., Boland M.P. and O’Callaghan D. (2001). The effects of dietary urea on embryo development in superovulated donor ewes and on early embryo survival and development in recipient ewes. Anim. Sci. 72, 395-400.
Fouladi-Nashta A.A., Carlos G., Gutierrez J.G., Gong G., Garnsworthy P.C. and Robert W. (2007). Impact of dietary fatty acids on oocyte quality and development in lactating dairy cows. Biol. Reprod. 77, 9-17.
Gardner D.K. and Lane M. (1993). Amino acids and ammonium regulate mouse embryo development in culture. Biol. Reprod. 48, 377-385.
Gath V., Lonergan P., Boland M.P. and O’Callaghan D. (1999). Effects of diet type on establishment of pregnancy and embryo development in beef heifers. Theriogenology. 51, 224.
Hammon D.S., Wang S. and Holyoak G.R. (2000a). Ammonia concentration in bovine follicular fluid and its effect during in vitro maturation on subsequent embryo development. Anim. Reprod. Sci. 58, 1-8.
Hammon D.S., Wang S. and Holyoak G.R. (2000b). Effects of ammonia during different stages of culture on development of in vitro produced bovine embryos. Anim. Reprod. Sci. 59, 23-30.
Jordan E.R., Chapman T.E., Holtan D.W. and Swanson L.V. (1983). Relationship of dietary crude protein to composition of uterine secretions and blood in high-producing postpartum dairy cows. J. Dairy Sci. 66, 1854-1862.
Jorritsma R., César M.L., Hermans J.T., Kruitwagen C.L.J.J., Vos P.L.A.M. and Kruip T.A.M. (2004). Effects of non-esterified fatty acids on bovine granulosa cells and developmental potential of oocytes in vitro. Anim. Reprod. Sci. 81, 225-235.
Kenny D.A., Boland M.P., Diskin M.G. and Sreenan J.M. (2002). Effect of rumen degradable protein with or without fermentable carbohydrate supplementation on blood metabolites and embryo survival. Anim. Sci. 74, 529-537.
Kenny D.A., Boland M.P., Diskin M.G. and Sreenan J.M. (2001). Effect of pasture crude protein and fermentable energy supplementation on blood metabolite and progesterone concentrations and on embryo survival in heifers. Anim. Sci. 73, 501-511.
Khadr N.E. (1995). Response of small ruminants to diets containing low quality roughages treated with non-protein nitrogenous substances. Ph D. Thesis. ZagazigUniv., Benha, Egypt.
Kim J.Y., Kinoshita M., Ohnishi M. and Fukui Y. (2001). Lipid and fatty acid analysis of fresh and frozen–thawed immature and in vitro matured bovine oocytes. Reproduction. 122, 131-138.
Konigsson K., Savoini G., Govoni N., Invernizzi G., Prandi A., Kindahl H. and Veronesi M.C. (2008). Energy balance, leptin, NEFA and IGF-I plasma concentrations and resumption of post partum ovarian activity in Swedish red and white breed cows. Acta. Vet. Scandinavica. 50, 3-10.
Kruif A., Leroy J.L.M.R. and Opsomer G. (2008). Reproductive performance in high producing dairy cows: practical implications. Tierarztl. Prax. 36, 29-33.
Lacetera N., Scalia D., Franci O., Bernabucci U., Ronchi B. and Nardone A. (2004). Lymphocyte functions in overconditioned cows around parturition. J. Dairy Sci. 88, 2010-2016.
Lane M. and Gardner D.K. (2003). Ammonium induces aberrant blastocyst differentiation, metabolism, pH regulation and gene expression and subsequently alters fetal development in the mouse. Biol. Reprod. 69, 1109-1117.
Laven R.A., Dawuda P.M., Scaramuzzi R.J., Wathes D.C., Biggadike H.J. and Peters A.R. (2004). The effect of feeding diets high in quickly degradable nitrogen on follicular development and embryo growth in lactating Holstein dairy cows. Anim. Reprod. Sci. 84, 41-52.
LeBlanc S.J., Leslie K.E. and Duffield T.D. (2005). Metabolic predictors of displaced abomasum in dairy cattle. J. Dairy Sci. 88, 159-170.
Leroy J.L.M.R., Opsomer G., Van S.A., Goovaerts I.G.F. and Bols P.E.J. (2008a). Reduced fertility in high-yielding dairy cows: are the oocyte and embryo in danger? Part II: mechanisms linking nutrition and reduced oocyte and embryo quality in high-yielding cows. Reprod. Dom. Anim. 43, 623-632.
Leroy J.L.M.R., Van S.A., Opsomer G. and Bols P.E.J. (2008b). The consequences of metabolic changes in high-yielding dairy cows on oocyte and embryo quality. Animal. 2, 1120-1127.
Leroy J.L.M.R., Vanholder T., Van K.A.T.M., Garcia-IspiertoI. and Bols P.E.J. (2008c). Nutrientprioritization in dairy cows early postpartum: mismatchbetween metabolism and fertility? Reprod. Dom. Anim. 43, 96-103.
Leroy J.L.M.R., Vanholder T., Delanghe J.R., Opsomer G., Van S.A., Bols P.E.J. and Kruif A. (2004). Metabolite and ionic composition of follicular fluid from different-sized follicles and their relationship to serum concentrations in dairy cows. Anim. Reprod. Sci. 80, 201-211.
Leroy J.L.M.R., Vanholder T., Mateusen B., Christophe A., Opsomer G., Kruif A., Genicot G. and Van S.A. (2005). Non-esterified fatty acids in follicular fluid of dairy cows and their effect on development capacity of bovine oocytes in vitro. Reproduction. 130, 485-495.
Leroy J.L.M.R., Van Soom A., Kruif A. and Opsomer G. (2006). Modern research in the reduced fertility in high producing dairy cows: an innovative way of thinking. Vlaams. Diergen. Tijdschr. 75, 18-22.
Lonergan P., Gutierrez-Adan A., Rizos D., Pintalo B., De La Fuente J. and Boland M.P. (2003). Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 h after the preovulatory luteinizing hormone surge. Mol. Reprod. Dev. 66, 297-305.
Lucy M.C. (2001). Reproductive loss in high-producing dairy cattle: where will it end? J. Dairy Sci. 84, 1277-1293.
Macmillan K.L.S., Lean I.J. and Westwood C.T. (1996). The effects of lactation on the fertility of dairy cows. Australian Vet. J. 73, 141-147.
McEvoy T.G., Sinclair K.D., StainesM.E., Robinson J.J., Armstrong D.G. and Webb R. (1997a). In vitro blastocyst production in relation to energy and protein intake prior to collection. J. Reprod. Fertil. Abstr. Series. 19, 132.
McEvoy T.G., Robinson J.J., Aitken R.P., Findlay P.A. and Robertson I.S. (1997b). Dietary excesses of urea influence the viability and metabolism of preimplantation sheep embryos and may affect fetal growth among survivors. Anim. Reprod. Sci. 47, 71-90.
Melendez P., Donovan A., Hernandez J., Bartolome J., Risco C.A., Staples C. and Thatcher W.W. (2003). Milk, plasma, and blood urea nitrogen concentrations, dietary protein, and fertility in dairy cattle. J. Am. Vet. Med. Assoc. 223, 628-634.
Mikkola M., Mantysaari P., Tammiranta N., Peippo J. and Taponen J. (2005). Effect of dietary protein on embryo recovery rate and quality in superovulated heifers. Anim. Reprod. Sci. 87, 193-202.
Ocon O.M. and Hansen P.J. (2003). Disruption of bovine oocytes and preimplantation embryos by urea and acidic pH. J. Dairy Sci. 86, 1194-2000.
Papadopoulos S., Lonergan P., Gath V., Quinn K.M., Evans A.C., O’Callaghan D. and Boland M.P. (2001). Effect of diet quantity and urea supplementation on oocyte and embryo quality in sheep. Theriogenology. 55, 1059-1069.
Quiroz-Rocha G.F., LeBlanc S.J., Duffield T., Wood D., Leslie K. and Jacobs R.M. (2009). Evaluation of prepartum serum cholesterol and fatty acids concentrations as predictors of postpartum retention of the placenta in dairy cows. J. Am. Vet. Med. Assoc. 234, 790-793.
Rhoads M.L., Rhoads R.P., Gilbert R.O., Toole R. and Butler W.R. (2006). Detrimental effects of high plasma urea nitrogen levels on viability of embryos from lactating dairy cows. Anim. Reprod. Sci. 91, 1-10.
Rooke J.A., Ewen M., Mackie K., StainesM.E., McEvoy T.G. and Sinclair K.D. (2004) Effect of ammonium chloride on the growth and metabolism of bovine ovarian granulosa cells and the development of ovine oocytes matured in the presence of bovine granulosa cells previously exposed to ammonium chloride. Anim. Reprod. Sci. 84, 53-71.
Rooke J.A., Ewen M., Reis A. and McEvoy T.G. (2006). Comparison of the fatty acid contents of bovine follicular fluid, granulose cells and cumulus enclosed or denuded oocytes. Reprod. Dom. Anim. 41, 306.
Roth Z., Arav A., Bor A., Zeron Y., Braw-Tal R. and Wolfenson D. (2001). Improvement of quality of oocytes collected in the autumn by enhanced removal of impaired follicles from previously heat-stressed cows. Reproduction. 122, 737-744.
Sinclair K.D., Kuran M., Gebbie F.E., Webb R. and McEvoy T.G. (2000b). Nitrogen metabolism and fertility in cattle: II. Development of oocytes recovered from heifers offered diets differing in their rate of nitrogen release in the rumen. J. Anim. Sci. 78, 2670-2680.
Sinclair K.D., Sinclair L.A. and Robinson J.J. (2000a). Nitrogen metabolism and fertility in cattle: I. Adaptive changes intake and metabolism to diets differing in their rate of energy and nitrogen release in the rumen. J. Anim. Sci. 78, 2659-2669.
Snijders S.E., Dillon P., O’Callaghan D. and Boland M.P. (2000). Effect of genetic merit, milk yield, body condition and lactation number on in vitro oocyte development in dairy cows. Theriogenology. 53, 981-989.
Sreenan J.M. (1986). The extent and timing of embryonic mortality in cattle. Pp. 1-11 in Embryonic Mortality in Farm Animals. M.G. Diskin, Ed. Martinus Nijhoff Publishers, Dordrecht, Netherlands.
Thatcher W.W., Guzeloglu A., Mattos R., Binelli M., Hansen T.R. and PRU J.K. (2000). Uterine-conceptus interactions and reproductive failure in cattle. Theriogenology. 56, 1435-1450.
Van Den Hurk R. and Zhao H. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology. 63, 1717-1751.
Vanholder T., Leroy J.L.M.R., Van S.A., Maes D., Coryn M., Fiers T., Kruif A. and Opsomer G. (2006). Effect of non-esterified fatty acids on bovine theca cell steroidogenesis and proliferation in vitro. Anim. Reprod. Sci. 9, 51-63.
Vassena R., Mapletoft R.J., Allodi S., Singh J. and Adams G.P. (2003). Morphology and developmental competence of bovine oocytes relative to follicular status. Theriogenology. 60, 923-932.
Westwood C.T., Lean I.J. and Kellaway R.C. (1998). Indications and implications for testing of milk urea in dairy cattle: a quantitative review: Part 2. Effect of dietary protein on reproductive performance. New Zealand Vet. J. 46, 123-130.