Reproduction in Domestic Animals

Reprod Dom Anim 43 (Suppl. 2), 96–103 (2008); doi: 10.1111/j.1439-0531.2008.01148.xISSN 0936-6768Nutrient Prioritization in Dairy Cows Early Postpartum: Mismatch BetweenMetabolism and Fertility?JLMR Leroy 1 , T Vanholder 1 , ATM Van Knegsel 2 , I Garcia-Ispierto 3 and PEJ Bols 11 Veterinary Centre Someren, Someren; 2 Adaptation Physiology Group and Animal Nutrition Group, Wageningen Institute of Animal Sciences,Wageningen University, Wageningen, The Netherlands; 3 Department of Animal Health and Anatomy, Autonomous University of Barcelona,Barcelona, SpainContentsFor several decades, researchers worldwide report a decreasein fertility in high-yielding dairy cows, most probably based onconflicting metabolic and reproductive needs. The dairy herdmanager’s success at improving milk production has beenaccompanied by a negative trend for the most visible reproductiveparameters such as calving intervals, number of daysopen and number of inseminations needed per pregnancy. Inparallel, many research groups studied the metabolic andendocrine factors that influence follicular growth and thedevelopmental competence of oocytes and embryos. In thepast, herd managers and reproductive biologists each tried totackle the same problems with limited consultation. Morerecently, the situation has improved significantly and theriogenologists,nutritionists and veterinarians now conductresearch in multidisciplinary teams. This review paper startsin a general way by discussing nutrient prioritization towardsthe udder to guarantee milk production and by describinginteractions between the somatotropic and gonadotropic axis.It then focuses on the consequences of the negative energybalance on follicular growth and environment, oocyte andembryo quality, not only by summarizing the currentlyaccepted hypotheses but also based on clear scientific evidenceat the follicular level. All this, with one question in mind: isthere a mismatch between metabolism and fertility and whatcan the dairy manager learn from research to tackle theproblem of reduced fertility?IntroductionDisappointing reproductive performance in high-producingdairy herds is a global problem, characterized asmultifactorial and urged a multidisciplinary approach inwhich animal scientists, veterinarians and molecularbiologists were required to unravel the complex pathogenesisof this ‘subfertility syndrome’. After all, producinga calf at regular intervals is considered a prerequisitefor profitable lactational performance (Royal et al.2000; Huirne et al. 2002). After giving birth, the processof becoming pregnant again in dairy cows starts withclearance and involution of the uterus followed byresumption of ovarian activity. This should result in thecompletion of the growth of a healthy follicle, enclosinga competent oocyte, and ultimately in oestrus, ovulation,fertilization and uterine attachment by a viableembryo. Any upset of these balanced and fine-tunedbiological and mechanical events leads to failing reproduction– and this is exactly where the shoe pinches inour modern dairy herds.The subfertility syndrome can be divided into twomajor sub-problems. First of all, up to 50% of moderndairy cows display abnormal oestrus cycles postpartumleading to prolonged calving to first inseminationintervals (Opsomer et al. 1998). In this context, especiallyinstability within the hypothalamo–pituitary–ovarian–uterine axis has been studied thoroughly (Lucy2001; Butler 2003). The concomitant reduced oestrusexpression or even anoestrus, cyst formation anddelayed first ovulation have been extensively documented(Beam and Butler 1997; de Vries and Veerkamp2000; Lopez et al. 2004; Vanholder et al. 2006a).Secondly, attention was focussed on disappointingconception rates (Bousquet et al. 2004) and the increasinglyhigh incidence of early embryonic mortality(Dunne et al. 1999; Mann and Lamming 2001; Bilodeau-Goeseelsand Kastelic 2003). Fertilization ofoocytes from high-genetic merit cows resulted in significantlylower blastocyst yields in vitro, irrespective ofmilk production as such (Snijders et al. 2000). Embryoquality was also reduced in high-producing dairy cowscompared with non-lactating counterparts (Wiltbanket al. 2001; Leroy et al. 2005a). A high proportion ofnon-viable embryos were found in lactating cowscompared with non-lactating cows (Sartori et al.2002). Approximately 70–80% of the total embryonicand foetal losses typically occur during the earlyembryonic, pre-attachment period (Santos et al. 2004a)(for review, see Leroy et al. 2007).Modern dairy cows, albeit sub-fertile, produce vastamounts of milk mainly because of significant geneticimprovements, combined with nutritional managementoptimized towards lactation. Based on almostunchanged heifer fertility, we can conclude that thereproductive processes of modern dairy cattle areessentially normal when lactation demands are notimposed (Lucy 2007). Why do modern dairy cowsprioritize milk production at the expense of sustainedreproductive efficiency? In this review, we aim to answerthis question. Are high milk yields and good fertilityoutcomes conflicting interests metabolically speaking?From Phylogenetically Driven to GeneticallyEnforced Nutrient Prioritization: TheConsequences on MetabolismFrom a biological point of view, it makes sense formammals in early lactation to favour milk productionover fertility: this we can refer to as nutrient prioritization(Lucy 2003). As nutrition becomes scarce, thelactating dam will preferentially invest the limitedresources in the survival of living offspring rather thangambling on the oocyte that is yet to be ovulated,Ó 2008 The Authors. Journal compilation Ó 2008 Blackwell Verlag