Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Influencing the future: interactions of skeleton, energy, protein and calcium during late gestation and early lactation

Ian J. Lean A B E , Peter J. DeGaris C , Pietro Celi B , David M. McNeill D , Rachael M. Rodney A B and David R. Fraser B
+ Author Affiliations
- Author Affiliations

A SBScibus, Camden, NSW 2570, Australia.

B Faculty of Veterinary Science, The University of Sydney, Camden, NSW 2570, Australia.

C Tarwin Veterinary Group, Leongatha, Vic. 3953, Australia.

D School of Veterinary Science, University of Queensland, Gatton, Qld 4072, Australia.

E Corresponding author. Email: IanL@sbscibus.com.au

Animal Production Science 54(9) 1177-1189 https://doi.org/10.1071/AN14479
Submitted: 4 April 2014  Accepted: 5 June 2014   Published: 10 July 2014

Abstract

Marked improvements in milk production, health and reproduction have resulted from manipulations of the pre-calving diet. An understanding of the underlying physiological changes resulting from manipulation of late gestational diets is needed in order to refine and enhance these responses. The physiology of late gestation and early lactation of the dairy cow is examined in the context of exploring the hypothesis that changes in physiology occur not only through homeostatic, but also homeorhetic change. Studies in mice and man have identified a pivotal role for skeleton, particularly through production of active forms of osteocalcin, in integrating energy metabolism. Skeleton appears to particularly influence lipid metabolism and vice versa. Further insights into the factors influencing skeletal function and calcium (Ca) metabolism are emerging, including the potential for negative dietary cation anion difference (DCAD) diets to upregulate the responses of the skeleton in metabolism through increased bone mobilisation and in enhancing responses to parathyroid hormone. The rumen appears to be an important site of absorption of Ca, but physiological mechanisms influencing this uptake are not clear. We provide quantitative evidence of the magnitude of responses that reflect relationships linking Ca metabolism, skeleton and production, using meta-analytic methods. Negative DCAD diets increase milk production in multiparous cattle, but not in heifers. Further, examination of concentrations of metabolites related to energy metabolism obtained from cattle exposed to a negative DCAD diet over calving identified a dominant role for Ca concentrations, which were associated with blood-free fatty acids (NEFA), blood 3-hydroxybutyrate, glucose and cholesterol. These relationships were homeostatic, occurring on the same day, but also homeorhetic with concentrations of Ca and NEFA being significantly associated over 21 days. The findings in cattle are consistent with those in the murine models. However, Ca and the skeleton are not the only significant factors in the transition period influencing future performance as hormonal treatments, metabolic demands and sex of the conceptus, and inflammation and the factors controlling this play a role in future performance. Homeorhetic, longer-term, adaptive responses are critical to achieving orchestrated longer-term adaptive responses to calving and lactation. We consider that the teleological question ‘why would a bone-specific hormone (osteocalcin) regulate energy metabolism?’ is answered by the specific needs for integrated metabolism to address the extreme metabolic demands of lactation in many species.

Additional keywords: calcium, health, metabolism, osteocalcin.


References

Allsop TF, Pauli JV (1985) Failure of 25-hydroxycholecalciferol to prevent milk fever in dairy cows. New Zealand Veterinary Journal 13, 19–22.

Ammann P, Brennan TC, Mekraldi S, Aubert ML, Rizzoli R (2010) Administration of growth hormone in selectively protein-deprived rats decreases BMD and bone strength. Bone 46, 1574–1581.
Administration of growth hormone in selectively protein-deprived rats decreases BMD and bone strength.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmsVShu7k%3D&md5=4f169bb308701cab27ce36e326cb53edCAS | 20178866PubMed |

Aurousseau B, Gruffat D, Durand D (2006) Gestation linked radical oxygen species fluxes and vitamins and trace mineral deficiencies in the ruminant. Reproduction, Nutrition, Development 46, 601–620.
Gestation linked radical oxygen species fluxes and vitamins and trace mineral deficiencies in the ruminant.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1SjsLc%3D&md5=98b56989ec3d9608f941d8700f0b8000CAS | 17169308PubMed |

Babel B (2007) Investigations on bone metabolism in intact and ovariohysterectomised miniature pigs. PhD Thesis. Institut für Physiologie, physiologische Chemie und Tierernährung der Tierärztlichen Fakultät der Ludwig-Maximilians-Universität, München, Geschäftsführender Vorstand, München, Germany.

Baldock PA, Allison SJ, Lundberg P, Lee NJ, Slack K, Lin EJ, Enriquez DRF, McDonald MM, Zhang L, During MJ, Little DG, Eisman JA, Gardiner EM, Yulyaningsih E, Lin S, Sainsbury A, Herzog H (2007) Novel role of Y1 receptors in the coordinated regulation of bone and energy homeostasis. The Journal of Biological Chemistry 282, 19 092–19 102.
Novel role of Y1 receptors in the coordinated regulation of bone and energy homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmvVart7s%3D&md5=a6bf9587f535ce229aac56dac6d3325bCAS |

Bauman DE, Currie WB (1980) Partitioning of nutrients during pregnancy and lactation: a review of mechanism involving homeostasis and homeorhesis. Journal of Dairy Science 63, 1514–1529.
Partitioning of nutrients during pregnancy and lactation: a review of mechanism involving homeostasis and homeorhesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXmtFygu7s%3D&md5=c19f766652cfef1e62946e1077b9d7aeCAS | 7000867PubMed |

Beardsworth L, Beardsworth P, Care AD (1989) Calcium fluxes across the wall of the ovine reticulorumen in vivo. Research in Veterinary Science 47, 404–405.

Bell AW (1995) Regulation of organic nutrient metabolism during transition from late pregnancy to early lactation. Journal of Animal Science 73, 2804–2819.

Belyea RL, Frost GR, Martz FA, Clark JL, Forkner LG (1978) Body composition of dairy cattle by potassium-40 scintillation detection. Journal of Dairy Science 61, 206–211.
Body composition of dairy cattle by potassium-40 scintillation detection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhtFygsL8%3D&md5=ca59a90860fa012806e842e356e62489CAS |

Berner HS, Lyngstadass SP, Spahr A, Monjo M, Thommesen L, Drevon CA, Syversen U, Reseland JE (2004) Adiponectin and its receptors are expressed in bone-forming cells. Bone 35, 842–849.
Adiponectin and its receptors are expressed in bone-forming cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvV2rtLo%3D&md5=d894fd86996388e103212cc147714910CAS | 15454091PubMed |

Bertics SJ, Grummer RR, Cadorniga-Valino C, Stoddard EE (1992) Effect of prepartum dry matter intake on liver triglyceride concentration and early lactation. Journal of Dairy Science 75, 1914–1922.
Effect of prepartum dry matter intake on liver triglyceride concentration and early lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltlSgsbs%3D&md5=a6ecfbad0718a1e40325bdf082de0488CAS | 1500587PubMed |

Bertoni G, Trevisi E, Piccioli-Cappelli F (2004) Effects of acetyl-salicylate used in post-calving of dairy cows. Veterinary Research Communications 28, 217–219.
Effects of acetyl-salicylate used in post-calving of dairy cows.Crossref | GoogleScholarGoogle Scholar | 15372961PubMed |

Bhanugopan MS, Fulkerson W, Hyde ML, Fraser DR, McNeill DM (2010) Carryover effects of potassium supplementation on calcium metabolism in dairy cows at parturition. Journal of Dairy Science 93, 2119–2129.
Carryover effects of potassium supplementation on calcium metabolism in dairy cows at parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnvVansrk%3D&md5=c25a1b0e5d842f7b7c7fd695e4cdd6cbCAS | 20412927PubMed |

Bigner DR, Goff JP, Faust MA, Burton JL, Tyler HD, Horst RL (1996) Acidosis effects on insulin response during glucose tolerance tests in jersey cows. Journal of Dairy Science 79, 2182–2188.
Acidosis effects on insulin response during glucose tolerance tests in jersey cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXls1GjsA%3D%3D&md5=2a19a0b7bdbf6cd8fc42fd9fd5fa33c3CAS | 9029356PubMed |

Block E (1984) Manipulating dietary anions and cations for prepartum dairy cows to reduce incidence of milk fever. Journal of Dairy Science 67, 2939–2948.
Manipulating dietary anions and cations for prepartum dairy cows to reduce incidence of milk fever.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXhtFWqtrk%3D&md5=79b5b1ff2c64bfb5e0f45190288850c4CAS | 6530489PubMed |

Bonavera JJ, Dube MG, Kalra PS, Kalra SP (1994) Anorectic effects of estrogen may be mediated by decreased neuropeptide-Y release in the hypothalamic paraventricular nucleus. Endocrinology 134, 2367–2370.

Borsberry S, Dobson H (1989) Periparturient diseases and their effect on reproductive performance in five dairy herds. The Veterinary Record 124, 217–219.
Periparturient diseases and their effect on reproductive performance in five dairy herds.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL1M7ovVemsw%3D%3D&md5=6a8b44eb83aba7a558eddfd13316cebdCAS | 2929110PubMed |

Bronner F (1987) Intestinal calcium absorption mechanisms and applications. The Journal of Nutrition 117, 51–58.

Capen CC, Rosol TJ (1989) Calcium-regulating hormones and disease of abnormal mineral metabolism. In ‘Clinical biochemistry of domestic animals’. 4th edn. (Ed. JJ Kaneko) pp. 678–752. (Academic Press: San Diego, CA)

Care AD, Brown RC, Farrar AR, Pickard DW (1984) Magnesium absorption from the digestive tract of sheep. Experimental Physiology 69, 577–587.

Castillo C, Hernandez J, Bravo A, Lopez-Alonso M, Pereira V, Benedito JL (2005) Oxidative status during late pregnancy and early lactation in dairy cows. Veterinary Journal (London, England) 169, 286–292.
Oxidative status during late pregnancy and early lactation in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhsVOitr0%3D&md5=1fcd49a1073b9ac08e086454ef50434fCAS |

Celi P (2011) Oxidative stress in ruminants. In ‘Studies on veterinary medicine. Vol. 5’. (Eds L Mandelker, P Vajdovich) pp. 191–231. (Humana Press: New York)

Cerri RLA, Rutigliano HM, Lima FS, Araújo DB, Santos JEP (2009) Effect of source of supplemental selenium on uterine health and embryo quality in high-producing dairy cows. Theriogenology 71, 1127–1137.
Effect of source of supplemental selenium on uterine health and embryo quality in high-producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsV2qs74%3D&md5=0d55312af47271261e352138b8adfaa8CAS |

Chapinal N, Carson ME, LeBlanc SJ, Leslie KE, Godden S, Capel M, Santos JEP, Overton MW, Duffield TF (2012) The association of serum metabolites in the transition period with milk production and early-lactation reproductive performance. Journal of Dairy Science 95, 1301–1309.
The association of serum metabolites in the transition period with milk production and early-lactation reproductive performance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtFWgsbg%3D&md5=068c16ada4f92f384722cafcc0357fcfCAS | 22365212PubMed |

Confavreux CB (2011) Bone: from a reservoir of minerals to a regulator of energy metabolism. Kidney International 79, S14–S19.
Bone: from a reservoir of minerals to a regulator of energy metabolism.Crossref | GoogleScholarGoogle Scholar |

Curtis MA (1997) Epidemiology of uterine infections in dairy cows. Antioxidant and metabolic investigations. PhD Thesis, University of Sydney.

Curtis CR, Erb EH, Sniffen CJ (1983) Association of parturient hypocalcemia with eight periparturient disorders in Holstein cows. Journal of the American Veterinary Medical Association 183, 559-561

Curtis CR, Erb EH, Sniffen CJ, Smith RD, Kronfeld DS (1985) Path analysis of dry period nutrition, postpartum metabolic and reproductive disorders, and mastitis in Holstein cows. Journal of Dairy Science 68, 2347–2360.
Path analysis of dry period nutrition, postpartum metabolic and reproductive disorders, and mastitis in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FmtVaqtQ%3D%3D&md5=0a916fdc08417d3cd25a593124c55c4cCAS | 4067048PubMed |

Cusack PMV, McMeniman NP, Rabiee AR, Lean IJ (2009) Assessment of the effects of supplementation with vitamin E on health and production of feedlot cattle using meta-analysis. Preventive Veterinary Medicine 88, 229–246.
Assessment of the effects of supplementation with vitamin E on health and production of feedlot cattle using meta-analysis.Crossref | GoogleScholarGoogle Scholar |

DeGaris PJ, Lean IJ, Rabiee AR, Heuer C (2008) Effects of increasing days of exposure to pre-partum transition diets on milk production and milk composition in dairy cows. Australian Veterinary Journal 86, 341–351.
Effects of increasing days of exposure to pre-partum transition diets on milk production and milk composition in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1ShtrvM&md5=6423c6d2bffabd51914c002cacfca304CAS | 18782415PubMed |

DeGaris PJ, Lean IJ, Rabiee AR, Heuer C (2010a) Effects of increasing days of exposure to pre-partum diets on reproduction and health in dairy cows. Australian Veterinary Journal 88, 84–92.
Effects of increasing days of exposure to pre-partum diets on reproduction and health in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3ntlOhsA%3D%3D&md5=2cc3050de23bfe305ce6a281311101e9CAS | 20402690PubMed |

DeGaris PJ, Lean IJ, Rabiee AR, Stevenson MA (2010b) Effects of increasing days of exposure to a pre-partum diet on the concentration of certain blood metabolites in dairy cows. Australian Veterinary Journal 88, 137–145.
Effects of increasing days of exposure to a pre-partum diet on the concentration of certain blood metabolites in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3ntlOgsg%3D%3D&md5=8788d515a63a195a7f5d47b768720cedCAS | 20402701PubMed |

DeGroot MA, Block E, French PD (2010) Effect of prepartum anionic supplementation on periparturient feed intake, health and milk production. Journal of Dairy Science 93, 5268–5279.
Effect of prepartum anionic supplementation on periparturient feed intake, health and milk production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsl2ruw%3D%3D&md5=fa8e6f2ece8ae01aa5203bf5a1d2bf40CAS | 20965343PubMed |

DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Controlled Clinical Trials 7, 177–188.
Meta-analysis in clinical trials.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2s7gsVamtA%3D%3D&md5=5eaf75c05b3ae7eaaf816f60a6785ef4CAS | 3802833PubMed |

Ducy P, Amling M, Takeda S, Priemel M, Schilling A, Beil F, Shen J, Vinson C, Rueger J, Karsenty G (2000) Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 100, 197–207.
Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotFChsw%3D%3D&md5=10f77b652999a909b6190df893832adcCAS | 10660043PubMed |

Dunshea FR, Leury BJ, Fahri F, DiGiacomo K, Hung A, Chauhan S, Clarke IJ, Collier R, Little S, Baumgard L (2013) Amelioration of thermal stress impacts in dairy cows. Animal Production Science 53, 965–975.

Erb HN, Smith RD, Oltenacu PA, Guard CL, Hillman RB, Powers PA, Smith MC, White ME (1985) Path model of reproductive disorders and performance, milk fever, mastitis, milk yield and culling in holstein cows. Journal of Dairy Science 68, 3337–3349.
Path model of reproductive disorders and performance, milk fever, mastitis, milk yield and culling in holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL287ktFWgtg%3D%3D&md5=81206e23a97c91042140344014f85cd0CAS | 4093528PubMed |

Farney JK, Mamedova LK, Coetzee JF, KuKanich B, Sordillo LM, Stoakes SK, Minton JE, Hollis LC, Bradford BJ (2013a) Anti-inflammatory salicylate treatment alters the metabolic adaptations to lactation in dairy cattle. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 305, R110–R117.
Anti-inflammatory salicylate treatment alters the metabolic adaptations to lactation in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1OmtrrJ&md5=cf1d6208456d03fdcf575c1511c35e00CAS | 23678026PubMed |

Farney JK, Mamedova LK, Coetzee JF, Minton JE, Hollis LC, Bradford BJ (2013b) Sodium salicylate treatment in early lactation increases whole-lactation milk and milk fat yield in mature dairy cows. Journal of Dairy Science 96, 7709–7718.
Sodium salicylate treatment in early lactation increases whole-lactation milk and milk fat yield in mature dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1CrurvL&md5=99a84dc05ec588ffc135a9c788bb059fCAS | 24140330PubMed |

Felson DT, Zhang Y, Hannan MT, Anderson JJ (1993) Effects of weight and body mass index on bone mineral density in men and women: the Framington study. Journal of Bone and Mineral Research 8, 567–573.
Effects of weight and body mass index on bone mineral density in men and women: the Framington study.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3s3ovFymug%3D%3D&md5=805d9c38a828e6380ea8062cccccc419CAS | 8511983PubMed |

Foresta C, Strapazzon G, De Toni L, Gianesello L, Calcagno A, Pilon C, Plebani M, Vettor R (2010) Evidence for osteocalcin production by adipose tissue and its role in human metabolism. The Journal of Clinical Endocrinology and Metabolism 95, 3502–3506.
Evidence for osteocalcin production by adipose tissue and its role in human metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXps12rtbo%3D&md5=5c1c16ac32e68abf8f0a812563abec25CAS | 20410230PubMed |

Fraser DR (1995) Vitamin D. Lancet 345, 104–107.
Vitamin D.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7hsFCmtw%3D%3D&md5=c73970f33616c06245f45d392de097b4CAS | 7815853PubMed |

Fredeen AH, DePeeters EJ, Baldwin RL (1988a) Characterisation of acid-base disturbances on calcium and phosphorus balances of dietary fixed ions in pregnant or lactating does. Journal of Animal Science 66, 157–173.

Fredeen AH, DePeeters EJ, Baldwin RL (1988b) Effects of acid-base disturbances caused by differences in dietary fixed ion balance on kinetics of calcium metabolism in ruminants with high calcium demand. Journal of Animal Science 66, 174–184.

Gaynor PJ, Mueller FJ, Miller JK, Ramsey N, Goff JP, Horst RL (1989) Parturient hypocalcemia in jersey cows fed alfalfa haylage-based diets with different cation to anion ratios. Journal of Dairy Science 72, 2525–2531.
Parturient hypocalcemia in jersey cows fed alfalfa haylage-based diets with different cation to anion ratios.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3c%2FpsVOkuw%3D%3D&md5=e9ba110c797d70bc8088f3b6a8f58f90CAS | 2600220PubMed |

Goff JP, Horst RL (1997) Effects of the addition of potassium or sodium but not calcium to prepartum rations on milk fever in dairy cows. Journal of Dairy Science 80, 176–186.
Effects of the addition of potassium or sodium but not calcium to prepartum rations on milk fever in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXpvFamtw%3D%3D&md5=db2957f13272ab1caa8ac917d6eb8abbCAS | 9120088PubMed |

Goff JP, Horst RL, Mueller FJ, Miller JK, Kiess GA, Dowlen HH (1991) Addition of chloride to a prepartal diet high in cations increases 1,25-dihydroxyvitamin D response to hypocalcemia preventing milk fever. Journal of Dairy Science 74, 3863–3871.
Addition of chloride to a prepartal diet high in cations increases 1,25-dihydroxyvitamin D response to hypocalcemia preventing milk fever.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XitVSrug%3D%3D&md5=d6ffb21b3f1d688a7f920d4c2b00803aCAS | 1757627PubMed |

Goff JP, Liesegang A, Horst RL (2014) Diet-induced pseudohypoparathyroidism: a hypocalcemia and milk fever risk factor. Journal of Dairy Science 97, 1520–1528.
Diet-induced pseudohypoparathyroidism: a hypocalcemia and milk fever risk factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFWit7s%3D&md5=652a277c0c53ddee2bb4c486e7d7a84eCAS | 24418271PubMed |

Grünberg W, Donkin SS, Constable PD (2011) Periparturient effects of feeding a low dietary cation-anion difference diet on acid-base, calcium and phosphorus homeostasis and on intravenous glucose tolerance test in high-producing dairy cows. Journal of Dairy Science 94, 727–745.
Periparturient effects of feeding a low dietary cation-anion difference diet on acid-base, calcium and phosphorus homeostasis and on intravenous glucose tolerance test in high-producing dairy cows.Crossref | GoogleScholarGoogle Scholar | 21257041PubMed |

Gulay MS, Garcia AN, Hayen MJ, Wilcox CJ, Head HH (2004a) Responses of Holstein cows to different bovine somatotropin (bST) treatments during the transition period and early lactation. Asian–Australasian Journal of Animal Sciences 17, 784–793.

Gulay MS, Hayen MJ, Liboni M, Belloso TI, Wilcox CJ, Head HH (2004b) Low doses of bovine somatotropin during the transition period and early lactation improves milk yield, efficiency of production, and other physiological responses of Holstein cows. Journal of Dairy Science 87, 948–960.
Low doses of bovine somatotropin during the transition period and early lactation improves milk yield, efficiency of production, and other physiological responses of Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivFyru7s%3D&md5=616a71ce423e5081dab0d8fa229508a4CAS | 15259229PubMed |

Hartung J, Knapp G (2001) A refined method for the meta analysis of controlled clinical trials with binary outcome. Statistics in Medicine 20, 3875–3889.
A refined method for the meta analysis of controlled clinical trials with binary outcome.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fls1Slsw%3D%3D&md5=4cdb378f064619a2caf528b6dcc2f1b8CAS | 11782040PubMed |

Hedges LV, Vevea JL (1998) Fixed- and random-effects models in meta-analysis. Psychological Methods 3, 486–504.
Fixed- and random-effects models in meta-analysis.Crossref | GoogleScholarGoogle Scholar |

Heuer C, Schukken YH, Dobbleaar P (1999) Postpartum body condition score and results form the first test day milk as predictors of disease, fertility, yield and culling in commercial dairy herds. Journal of Dairy Science 82, 295–304.
Postpartum body condition score and results form the first test day milk as predictors of disease, fertility, yield and culling in commercial dairy herds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVWhsb0%3D&md5=ee06ea8ffcc5b3b3d8a57a6185def1d7CAS | 10068951PubMed |

Hinde K, Carpenter AJ, Clay JC, Bradford BJ (2014) Holsteins favor heifers, not bulls: biased milk production programmed during pregnancy as a function of fetal sex. PLoS ONE 9, e86169
Holsteins favor heifers, not bulls: biased milk production programmed during pregnancy as a function of fetal sex.Crossref | GoogleScholarGoogle Scholar | 24498270PubMed |

Höller H, Breves G, Gerdes H, Kocabatmaz M (1988) Flux of calcium across the sheep rumen wall in vivo and in vitro. Experimental Physiology 73, 609–618.

Hyde ML, Fraser DR (2014) Measurement in vivo of the absorption of strontium from the rumen and intestines of sheep as an index of calcium absorption capacity. British Journal of Nutrition in press.

Kanazawa I, Yamaguchi T, Yano S, Yamauchi M, Yamamoto M, Sugimoto T (2007) Adiponectin and AMP kinase activator stimulate proliferation, differentiation, and mineralization of osteoblastic MC3T3-E1 cells. BMC Cell Biology 8, 51
Adiponectin and AMP kinase activator stimulate proliferation, differentiation, and mineralization of osteoblastic MC3T3-E1 cells.Crossref | GoogleScholarGoogle Scholar | 18047638PubMed |

Kehrer JP, Lund LG (1994) Cellular reducing equivalents and oxidative stress. Free Radical Biology & Medicine 17, 65–75.
Cellular reducing equivalents and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXhvFejtA%3D%3D&md5=18f408593f4eb74bf5d547ccc424b50fCAS |

Kim D, Kawakami Y, Yamagishi N, Abe I, Furuhama K, Devkota B, Okura N, Sato S, Ohashi S (2011) Response of plasma bone markers to a single intramuscular administration of calcitriol in dairy cows. Research in Veterinary Science 90, 124–126.
Response of plasma bone markers to a single intramuscular administration of calcitriol in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsVKltw%3D%3D&md5=23e8e67fb46de8e66c52a8c4f8c968d0CAS | 20553702PubMed |

Lacetera N, Bernabucci U, Ronchi B, Nardone A (1996) Effects of selenium and vitamin E administration during a late stage of pregnancy on colostrum and milk production in dairy cows, and on passive immunity and growth of their offspring. American Journal of Veterinary Research 57, 1776–1780.

Lean IJ, Farver TB, Trout HF, Bruss ML, Galland JC, Baldwin RL, Holmberg CA, Weaver LD (1992) Time series cross-correlation analysis of postparturient relationships among serum metabolites and yield variables in Holstein cows. Journal of Dairy Science 75, 1891–1900.
Time series cross-correlation analysis of postparturient relationships among serum metabolites and yield variables in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38zmsVWgtA%3D%3D&md5=13ef2c18e8ff0de4210654637da5e8cfCAS | 1500586PubMed |

Lean IJ, DeGaris PJ, Wade LK, Rajczyk ZK (2003) Transition Management of Dairy Cows: 2003. In ‘Australian and New Zealand combined dairy veterinarians’ conference’. (Ed T Parkinson) pp. 221–248. (Foundation for Continuing Education of the NZ Veterinary Association: Taupo, New Zealand)

Lean IJ, DeGaris PJ, McNeil DM, Block E (2006) Hypocalcemia in dairy cows: meta analysis and dietary cation anion difference theory revisited. Journal of Dairy Science 89, 669–684.
Hypocalcemia in dairy cows: meta analysis and dietary cation anion difference theory revisited.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlWrtL4%3D&md5=2ab59e0987266c7ff66313c78a1d32b9CAS | 16428636PubMed |

Lean IJ, Van Saun R, DeGaris PJ (2013) Energy and protein nutrition management of transition dairy cows. The Veterinary Clinics of North America. Food Animal Practice 29, 337–366.
Energy and protein nutrition management of transition dairy cows.Crossref | GoogleScholarGoogle Scholar | 23809895PubMed |

Leclerc H, Block E (1989) Effects of reducing dietary cation-anion balance for prepartum dairy cows with specific reference to hypocalcemic parturient paresis. Canadian Journal of Animal Science 69, 411–423.
Effects of reducing dietary cation-anion balance for prepartum dairy cows with specific reference to hypocalcemic parturient paresis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXltlejsrY%3D&md5=e2f648d5a119092198a6e964f7116282CAS |

Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G (2007) Endocrine regulation of energy metabolism by the skeleton. Cell 130, 456–469.
Endocrine regulation of energy metabolism by the skeleton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptlyntbs%3D&md5=c1bd62a5b77193f2e909e14bd8873291CAS | 17693256PubMed |

Liebler DC (1993) The role of metabolism in the antioxidant function of vitamin E. CRC Critical Reviews in Toxicology 23, 147–169.
The role of metabolism in the antioxidant function of vitamin E.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltVyht78%3D&md5=fc1f90ff9071def31820ca2f1cb02799CAS | 8329114PubMed |

Liesegang A, Sassi ML, Risteli J, Eicher R, Wanner M, Riond JL (1998) Comparison of bone resorption markers during hypocalcemia in dairy cows. Journal of Dairy Science 81, 2614–2622.
Comparison of bone resorption markers during hypocalcemia in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXntF2rtrY%3D&md5=e9f058e0a70b76350df166a4609aee6fCAS | 9812267PubMed |

Ludwig SKJ, Smits NGE, van der Veer G, Bremer MGEG, Nielen MWF (2012) Multiple protein biomarker assessment for recombinant bovine somatotropin (rbST) abuse in cattle. PLoS ONE 7, e52917
Multiple protein biomarker assessment for recombinant bovine somatotropin (rbST) abuse in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVKnsg%3D%3D&md5=d717c7843beb7386e2d831cee1eb24b8CAS |

Martinez N, Risco CA, Lima FS, Bisinotto RS, Greco LF, Riberio ES, Maunsell F, Galvao KN, Santos JEP (2012) Evaluation of peripartal calcium status, energetic profile and neutrophil function in dairy cows at low or high risk of developing uterine disease. Journal of Dairy Science 95, 7158–7172.
Evaluation of peripartal calcium status, energetic profile and neutrophil function in dairy cows at low or high risk of developing uterine disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs12gtb7P&md5=ac1808e8fe030d737db0d2a856496954CAS | 23021755PubMed |

Martinez N, Sinedino LDP, Bisinotto RS, Ribeiro ES, Gomes GS, Lima FS, Greco LF, Risco CA, Galvão KN, Taylor-Rodriguez D (2014) Effect of induced subclinical hypocalcemia on physiological responses and neutrophil function in dairy cows. Journal of Dairy Science 97, 874–887.
Effect of induced subclinical hypocalcemia on physiological responses and neutrophil function in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFOhtL3L&md5=dd4a5ad7c28f8de9f88653fcf65700e7CAS | 24359833PubMed |

McKay B (1994) Subclinical hypocalcaemia: a possible effect on fertility. In ‘Proceedings of the 11th seminar of The Society of Dairy Cattle Veterinarians of the New Zealand Veterinary Association’. (Ed. W Webber) pp. 89–98. (Dairy Cattle Society of the New Zealand Veterinary Association: Queenstown, New Zealand)

McNeill DM, Anderson ST (2012) Bone as an endocrine organ and the mineral nutrition of the dairy cow. In ‘International conference on livestock production and veterinary technology’. (Eds E Wina, L Hardi Prasetyo, I Inounu, A Priyanti, A Angraeni, D Yulistiani, A Sinurat, P Situmorang, A Wardhana, NLP Indi Dharmayanti, N Ilham, P James, Z Asnan) pp. 220–225. (Indonesian Centre for Animal Research and Development (ICARD): Bogor, Indonesia)

McNeill DM, Roche JR, McLachlan BP, Stockdale CR (2002) Nutritional strategies for the prevention of hypocalcaemia at calving for dairy cows in pasture-based systems. Australian Journal of Agricultural Research 53, 755–770.
Nutritional strategies for the prevention of hypocalcaemia at calving for dairy cows in pasture-based systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmt1GmtL0%3D&md5=453039c1dd39e6362e6f88332a9705fcCAS |

Miller JK, Brzezinska-Slebodzinska E, Madsen FC (1993) Oxidative stress, antioxidants, and animal function. Journal of Dairy Science 76, 2812–2823.
Oxidative stress, antioxidants, and animal function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXms1Olt7g%3D&md5=f75b60253ed0bb84395c3207ba209488CAS | 8227685PubMed |

Nagatani S, Guthikonda P, Thompson RC, Tsukamura H, Maeda KI, Foster DL (1998) Evidence for GnRH regulation by leptin: leptin administration prevents reduced pulsatile LH secretion during fasting. Neuroendocrinology 67, 370–376.
Evidence for GnRH regulation by leptin: leptin administration prevents reduced pulsatile LH secretion during fasting.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXktVKmurY%3D&md5=6ae085902a2d2d3689a406aad001957cCAS | 9662716PubMed |

   (a) National Research Council (2001) ‘Nutrient requirements of dairy cattle.’ 7th revised edn. (The National Academies Press: Washington, DC)
      Oetzel GR, Fettemn MJ, Hamar DW (1991) Screening of anionic salts for palatability, effects on acid-base status, and urinary calcium excretion in dairy cows. Journal of Dairy Science 74, 965–971.
Screening of anionic salts for palatability, effects on acid-base status, and urinary calcium excretion in dairy cows.Crossref | GoogleScholarGoogle Scholar |

Oury F, Sumara G, Sumara O, Ferron M, Chang H, Smith CE, Hermo L, Suarez S, Roth BL, Ducy P (2011) Endocrine regulation of male fertility by the skeleton. Cell 144, 796–809.
Endocrine regulation of male fertility by the skeleton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjsFeqt7k%3D&md5=07ea3d53913b0b6a3c5ee0f56fc68281CAS | 21333348PubMed |

Pedernera M, Celi P, Garcia SC, Salvin HE, Barchia I, Fulkerson WJ (2010) Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture. Veterinary Journal (London, England) 186, 352–357.
Effect of diet, energy balance and milk production on oxidative stress in early-lactating dairy cows grazing pasture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFWqtrbN&md5=6ae39d44238b7f17280233a304cfc0b9CAS |

Peng JB, Chen XZ, Berger UV, Vassilev PM, Tsukaguchi H, Brown EM, Hediger MA (1999) Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption. The Journal of Biological Chemistry 274, 22 739–22 746.
Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlt1Cnt7o%3D&md5=9bb9dc2ad5e58e97a9f43d851e828021CAS |

Phillippo M, Reid GW, Nevison IM (1994) Parturient hypocalcaemia in dairy cows: effects of dietary acidity on plasma mineral and calciotropic hormones. Research in Veterinary Science 56, 303–309.
Parturient hypocalcaemia in dairy cows: effects of dietary acidity on plasma mineral and calciotropic hormones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXmvF2ktb4%3D&md5=7476dcd66af357c51c67082817beff27CAS | 8073181PubMed |

Popa SM, Clifton DK, Steiner RA (2008) The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction. Annual Review of Physiology 70, 213–238.
The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkt1eqtro%3D&md5=978b76ed5a0d37bd15d6f3e726422cbfCAS | 17988212PubMed |

Putnam DE, Varga GA, Dann HM (1999) Metabolic and production responses to dietary protein and exogenous somatotropin in late gestation dairy cows. Journal of Dairy Science 82, 982–995.
Metabolic and production responses to dietary protein and exogenous somatotropin in late gestation dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1yksL0%3D&md5=d01e6715db3e19138a5c47b1c6714704CAS | 10342237PubMed |

Sato R, Onda K, Ochiai H, Iriki T, Yamazaki Y, Wada Y (2011) Serum osteocalcin in dairy cows: age-related changes and periparturient variation. Research in Veterinary Science 91, 196–198.
Serum osteocalcin in dairy cows: age-related changes and periparturient variation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFShtLjE&md5=486dafe2709fc3a5dbb0d1b0b25c85daCAS | 21300389PubMed |

Schröder B, Goebel W, Huber K, Breves G (2001) No effect of vitamin D3 treatment on active calcium absorption across ruminal epithelium of sheep. Journal Veterinary Medicine Series A 48, 353–363.
No effect of vitamin D3 treatment on active calcium absorption across ruminal epithelium of sheep.Crossref | GoogleScholarGoogle Scholar |

Shwartz G, Hill KL, VanBaale MJ, Baumgard LH (2009) Effects of flunixin meglumine on pyrexia and bioenergetic variables in postparturient dairy cows. Journal of Dairy Science 92, 1963–1970.
Effects of flunixin meglumine on pyrexia and bioenergetic variables in postparturient dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFynu7o%3D&md5=17beea19dd49278a21d90249395d4100CAS | 19389953PubMed |

Singh SP, Haussler S, Gross JJ, Schwarz FJ, Bruckmaier RM, Sauerwein H (2014) Short communication: Circulating and milk adiponectin change differently during energy deficiency at different stages of lactation in dairy cows. Journal of Dairy Science 97, 1535–1542.
Short communication: Circulating and milk adiponectin change differently during energy deficiency at different stages of lactation in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsV2jt7g%3D&md5=cc7c25199ab28db789ae11a9a24129d7CAS | 24472130PubMed |

Sordillo LM, Raphael W (2013) Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. The Veterinary Clinics of North America. Food Animal Practice 29, 267–278.
Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders.Crossref | GoogleScholarGoogle Scholar | 23809891PubMed |

Stevenson MA, Williamson NB, Hanlon DW (1999) The effects of calcium supplementation of dairy cattle after calving on milk, milk fat and protein production, and fertility. New Zealand Veterinary Journal 47, 53–60.
The effects of calcium supplementation of dairy cattle after calving on milk, milk fat and protein production, and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1ansrw%3D&md5=cb3e3c8e5634f7e0718306cedcefe987CAS | 16032071PubMed |

Takeda S, Elefteriou F, Levasseur R, Liu X, Shao L, Parker KL, Armstrong D, Ducy P, Karsenty G (2002) Leptin regulates bone formation via the sympathetic nervous system. Cell 111, 305–317.
Leptin regulates bone formation via the sympathetic nervous system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVakurk%3D&md5=d85dae7bce30f9373db6d598e002a638CAS | 12419242PubMed |

Taylor MS, Knowlton KF, McGilliard ML, Seymour WM, Herbein JH (2008) Blood mineral, hormone, and osteocalcin responses of multiparous Jersey cows to an oral dose of 25-hydroxyvitamin D3 or Vitamin D3 before parturition. Journal of Dairy Science 91, 2408–2416.
Blood mineral, hormone, and osteocalcin responses of multiparous Jersey cows to an oral dose of 25-hydroxyvitamin D3 or Vitamin D3 before parturition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmsVWmtbs%3D&md5=59892320cdb8470bd6ba52d1c24a2c7cCAS | 18487663PubMed |

Tomas FM, Potter BJ (1976) The site of magnesium absorption from the ruminant stomach. The British Journal of Nutrition 36, 37–45.
The site of magnesium absorption from the ruminant stomach.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XkvFSqt7s%3D&md5=a9bf7fc0b72988e7a01ea2e5c121fb93CAS | 949467PubMed |

Wadhwa DR, Care AD (2000) Effects of strontium on the absorption of calcium, magnesium and phosphate ions from the ovine reticulo-rumen. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 170, 225–229.
Effects of strontium on the absorption of calcium, magnesium and phosphate ions from the ovine reticulo-rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkt1Gju7Y%3D&md5=a9e870f31c644ebbe7467f14010df6b5CAS | 10841263PubMed |

Wallace JD, Cuneo RC, Lundberg PA, Rosén T, Jørgensen JOL, Longobardi S, Keay N, Sacca L, Christiansen JS, Bengtsson B-Å, Sönksen PH (2000) Responses of markers of bone and collagen turnover to exercise, growth hormone (GH) administration, and GH withdrawal in trained adult males. The Journal of Clinical Endocrinology and Metabolism 85, 124–133.

Wang C, Beede DK, Donovan GA, Archbald LF, DeLorenzo MA, Sanchez WK (1991) Effects of dietary negative cation-anion difference and high calcium content prepartum on calcium metabolism, health. Lactational and reproductive performance of Holstein cows. Journal of Dairy Science 74, 275

Westwood CT, Lean IJ, Garvin JK (2002) Factors influencing fertility of Holstein dairy cows: a multivariate description. Journal of Dairy Science 85, 3225–3237.
Factors influencing fertility of Holstein dairy cows: a multivariate description.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1aruw%3D%3D&md5=df07d8123824ebd07a9c5fa2fa6ee579CAS | 12512596PubMed |

Wilkens MR, Kunert-Keil C, Brinkmeier H, Schröder B (2009) Expression of calcium channel TRPV6 in ovine epithelial tissue. Veterinary Journal (London, England) 182, 294–300.
Expression of calcium channel TRPV6 in ovine epithelial tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtFWqur%2FE&md5=4ea5048134011ef4e788fddf8fcf5218CAS |

Wilkens MR, Mrochen N, Breves G, Schröder B (2011) Gastrointestinal calcium absorption in sheep is mostly insensitive to an alimentary induced challenge of calcium homeostasis. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 158, 199–207.
Gastrointestinal calcium absorption in sheep is mostly insensitive to an alimentary induced challenge of calcium homeostasis.Crossref | GoogleScholarGoogle Scholar |

Williams GL, Amstalden M, Garcia MR, Stanko RL, Nizielski SE, Morrison CD, Keisler DH (2002) Leptin and its role in the central regulation of reproduction in cattle. Domestic Animal Endocrinology 23, 339–349.
Leptin and its role in the central regulation of reproduction in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xls1Wkurw%3D&md5=a1af4d93e1638fcaba6204e16aedbba3CAS | 12142250PubMed |

Wolf G (2008) Energy regulation by the skeleton. Nutrition Reviews 66, 229–233.
Energy regulation by the skeleton.Crossref | GoogleScholarGoogle Scholar | 18366536PubMed |

Wolfenson D, Flamenbaum I, Berman A (1988) Dry period heat stress relief effects on prepartum progesterone, calf birth weight, and milk production. Journal of Dairy Science 71, 809–818.
Dry period heat stress relief effects on prepartum progesterone, calf birth weight, and milk production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhvVCgsb0%3D&md5=88c5575c4064c060a457d754ab7108a6CAS | 3372821PubMed |

Yamauchi T, Kamon J, Minokoshi YA, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K (2002) Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nature Medicine 8, 1288–1295.
Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotlWlsrg%3D&md5=dc51ef61858d8e99b992496786b1e22eCAS | 12368907PubMed |