Calcium restriction during lactation has minimal effects on post-weaning mineral metabolism and bone recovery

Springer Science and Business Media LLC - Tập 37 - Trang 648-657 - 2018
Ryan D. Ross1,2, Matthew J. Meagher1, D. Rick Sumner1,2
1Department of Cell and Molecular Medicine, Rush University Medical Center, Chicago, USA
2Department of Orthopedic Surgery, Rush University Medical Center, Chicago, USA

Tóm tắt

Dietary calcium (Ca) restriction during lactation in the rat, which induces intra-cortical and endocortical remodeling, has been proposed as a model to study bone matrix maturation in the adult skeleton. The purpose of this study was to assess the effects of dietary Ca restriction during lactation on post-weaning mineral metabolism and bone formation. Mated female Sprague–Dawley rats were randomized into groups receiving either 0.6% Ca (lactation/normal Ca) or 0.01% Ca (lactation/low Ca) diets during lactation. Virgin animals fed normal Ca were used as controls (virgin/normal Ca). At the time of weaning, animals on the low Ca diet were returned to normal Ca and cohorts of all three groups were sacrificed at days 0, 1, 2, 7, and 14 post-weaning. Lactation caused bone loss, particularly at the endocortical surface, but the amount was not affected by dietary Ca. Rats in the lactation/low Ca group had increased cortical porosity compared to the other groups, particularly within the size range of secondary osteons. Dietary Ca restriction during lactation did not affect post-weaning bone formation kinetics or serum Ca and phosphate levels. In both lactation groups, there was a transient increase in phosphate and fibroblast growth factor 23 (FGF23) post-weaning, which trended toward virgin/normal Ca levels over time. Thus, the additional challenge of low dietary Ca during lactation to induce intra-cortical remodeling in the rat has minimal effects on bone formation kinetics and mineral metabolism during the post-weaning period, providing further justification for this model to study matrix maturation in the adult skeleton.

Tài liệu tham khảo

Kovacs CS (2016) Maternal mineral and bone metabolism during pregnancy, lactation, and post-weaning recovery. Physiol Rev 96:449–547. https://doi.org/10.1152/physrev.00027.2015 Kovacs CS (2005) Calcium and bone metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 10:105–118 Brommage R, DeLuca HF (1985) Regulation of bone mineral loss during lactation. Am J Physiol 248:E182–E187 Ellinger GM, Duckworth J, Dalgarno AC, Quenouille MH (1952) Skeletal changes during pregnancy and lactation in the rat: effect of different levels of dietary calcium. Br J Nutr 6:235–253 Bowman BM, Siska CC, Miller SC (2002) Greatly increased cancellous bone formation with rapid improvements in bone structure in the rat maternal skeleton after lactation. J Bone Miner Res 17:1954–1960 Miller SC, Bowman BM (2004) Rapid improvements in cortical bone dynamics and structure after lactation in established breeder rats. Anat Rec A Discov Mol Cell Evol Biol 276:143–149 Ross RD, Sumner DR (2017) Bone matrix maturation in a rat model of intra-cortical bone remodeling. Calcif Tissue Int 101:193–203. https://doi.org/10.1007/s00223-017-0270-7 Kovacs CS (2011) Calcium and bone metabolism disorders during pregnancy and lactation. Endocrinol Metab Clin N Am 40:795–826 Kovacs CS, Kronenberg HM (1997) Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev 18:832–872 Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Muller R (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25:1468–1486 Duranova H, Martiniakova M, Omelka R, Grosskopf B, Bobonova I, Toman R (2014) Changes in compact bone microstructure of rats subchronically exposed to cadmium. Acta Vet Scand 56:64. https://doi.org/10.1186/s13028-014-0064-0 Martiniakova M, Chovancova H, Omelka R, Grosskopf B, Toman R (2011) Effects of a single intraperitoneal administration of cadmium on femoral bone structure in male rats. Acta Vet Scand 53:49. https://doi.org/10.1186/1751-0147-53-49 Burr DB, Akkus O (2014) Chapter 1—Bone morphology and organization. In: Burr DB, Allen MR (eds) Basic and applied bone biology. Academic Press, San Diego, pp 3–25. https://doi.org/10.1016/B978-0-12-416015-6.00001-0 Donnelly E, Baker SP, Boskey AL, van der Meulen MC (2006) Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res A 77:426–435 Parfitt AM, Drezner MK, Glorieux FH, Kanis JA, Malluche H, Meunier PJ, Ott SM, Recker RR (1987) Bone histomorphometry: standardization of nomenclature, symbols, and units. J Bone Miner Res 2:595–610 Miller SC, Shupe JG, Redd EH, Miller MA, Omura TH (1986) Changes in bone mineral and bone formation rates during pregnancy and lactation in rats. Bone 7:283–287 Garner SC, Peng TC, Hirsch PF, Boass A, Toverud SU (1987) Increase in serum parathyroid hormone concentration in the lactating rat: effects of dietary calcium and lactational intensity. J Bone Miner Res 2:347–352. https://doi.org/10.1002/jbmr.5650020412 Gonen E, Sahin I, Ozbek M, Kovalak E, Yologlu S, Ates Y (2005) Effects of pregnancy and lactation on bone mineral density, and their relation to the serum calcium, phosphorus, calcitonin and parathyroid hormone levels in rats. J Endocrinol Invest 28:322–326 Hirsch PF, Hagaman JR (1986) Reduced bone mass in calcitonin-deficient rats whether lactating or not. J Bone Miner Res 1:199–206. https://doi.org/10.1002/jbmr.5650010206 Honda A, Kurabayashi T, Yahata T, Tomita M, Matsushita H, Takakuwa K, Tanaka K (2000) Effects of pregnancy and lactation on trabecular bone and marrow adipocytes in rats. Calcif Tissue Int 67:367–372 Miller SC, Halloran BP, DeLuca HF, Jee WS (1982) Role of vitamin D in maternal skeletal changes during pregnancy and lactation: a histomorphometric study. Calcif Tissue Int 34:245–252 Peng TC, Garner SC, Kusy RP, Hirsch PF (1988) Effect of number of suckling pups and dietary calcium on bone mineral content and mechanical properties of femurs of lactating rats. Bone Miner 3:293–304 Rasmussen P (1977) Calcium deficiency, pregnancy, and lactation in rats. Microscopic and microradiographic observations on bones. Calcif Tissue Res 23:95–102 Tojo Y, Kurabayashi T, Honda A, Yamamoto Y, Yahata T, Takakuwa K, Tanaka K (1998) Bone structural and metabolic changes at the end of pregnancy and lactation in rats. Am J Obstet Gynecol 178:180–185 Warnock GM, Duckworth J (1944) Changes in the skeleton during gestation and lactation in the rat. Biochem J 38:220–224 Wong KM, Singer L, Ophaug RH (1980) Metabolic aspects of bone resorption in calcium-deficient lactating rats. Calcif Tissue Int 32:213–219 Vajda EG, Bowman BM, Miller SC (2001) Cancellous and cortical bone mechanical properties and tissue dynamics during pregnancy, lactation, and postlactation in the rat. Biol Reprod 65:689–695 Bowman BM, Miller SC (1999) Skeletal mass, chemistry, and growth during and after multiple reproductive cycles in the rat. Bone 25:553–559 Chen H, Hayakawa D, Emura S, Ozawa Y, Okumura T, Shoumura S (2002) Effect of low or high dietary calcium on the morphology of the rat femur. Histol Histopathol 17:1129–1135 de Winter FR, Steendijk R (1975) The effect of a low-calcium diet in lactating rats; observations on the rapid development and repair of osteoporosis. Calcif Tissue Res 17:303–316 Qing H, Ardeshirpour L, Pajevic PD, Dusevich V, Jahn K, Kato S, Wysolmerski J, Bonewald LF (2012) Demonstration of osteocytic perilacunar/canalicular remodeling in mice during lactation. J Bone Miner Res 27:1018–1029 Wysolmerski JJ (2013) Osteocytes remove and replace perilacunar mineral during reproductive cycles. Bone 54:230–236. https://doi.org/10.1016/j.bone.2013.01.025 Nango N, Kubota S, Hasegawa T, Yashiro W, Momose A, Matsuo K (2016) Osteocyte-directed bone demineralization along canaliculi. Bone 84:279–288. https://doi.org/10.1016/j.bone.2015.12.006 Kaya S, Basta-Pljakic J, Seref-Ferlengez Z, Majeska RJ, Cardoso L, Bromage TG, Zhang Q, Flach CR, Mendelsohn R, Yakar S, Fritton SP, Schaffler MB (2017) Lactation-induced changes in the volume of osteocyte lacunar-canalicular space alter mechanical properties in cortical bone tissue. J Bone Miner Res 32:688–697. https://doi.org/10.1002/jbmr.3044 Anderson JJ, Garner SC, Mar MH, Boass A, Toverud SU, Parikh I (1990) The ovariectomized, lactating rat as an experimental model for osteopenia: calcium metabolism and bone changes. Bone Miner 11:43–53 Boass A, Garner SC, Schultz VL, Toverud SU (1997) Regulation of serum calcitriol by serum ionized calcium in rats during pregnancy and lactation. J Bone Miner Res 12:909–914 Garner SC, Boass A, Toverud SU (1989) Hypercalcemia fails to suppress elevated serum parathyroid hormone concentrations during lactation in rats. J Bone Miner Res 4:577–583 Miller SC, Bowman BM (2007) Rapid inactivation and apoptosis of osteoclasts in the maternal skeleton during the bone remodeling reversal at the end of lactation. Anat Rec (Hoboken) 290:65–73 Pike JW, Parker JB, Haussler MR, Boass A, Toverud SV (1979) Dynamic changes in circulating 1,25-dihydroxyvitamin D during reproduction in rats. Science 204:1427–1429 Garner SC, Peng TC, Toverud SU (1988) Modulation of serum parathyroid hormone and ionized calcium concentrations during reproduction in rats fed a low calcium diet. J Bone Miner Res 3:319–323 Sowers MF, Hollis BW, Shapiro B, Randolph J, Janney CA, Zhang D, Schork A, Crutchfield M, Stanczyk F, Russell-Aulet M (1996) Elevated parathyroid hormone-related peptide associated with lactation and bone density loss. JAMA 276:549–554 Lippuner K, Zehnder HJ, Casez JP, Takkinen R, Jaeger P (1996) PTH-related protein is released into the mother’s bloodstream during lactation: evidence for beneficial effects on maternal calcium-phosphate metabolism. J Bone Miner Res 11:1394–1399. https://doi.org/10.1002/jbmr.5650111004 Datta NS, Abou-Samra AB (2009) PTH and PTHrP signaling in osteoblasts. Cell Signal 21:1245–1254. https://doi.org/10.1016/j.cellsig.2009.02.012 Kovacs CS (2014) The role of PTHrP in regulating mineral metabolism during pregnancy, lactation, and fetal/neonatal development. Clin Rev Bone Miner Metab 12:142–164 Blahosova A, Neradilova M, Velicky J, Titlbach M, Marsikova L, Reisenauer R (1974) Dynamics of changes of calcium and phosphorus metabolism in relation to the morphology of parafollicular thyroid cells in rats during lactation and forced weaning. Endokrinologie 63:122–136 Garner SC, Boass A, Toverud SU (1990) Parathyroid hormone is not required for normal milk composition or secretion or lactation-associated bone loss in normocalcemic rats. J Bone Miner Res 5:69–75 Martin A, David V, Quarles LD (2012) Regulation and function of the FGF23/klotho endocrine pathways. Physiol Rev 92:131–155. https://doi.org/10.1152/physrev.00002.2011 Razzaque MS (2009) The FGF23-Klotho axis: endocrine regulation of phosphate homeostasis. Nat Rev Endocrinol 5:611–619. https://doi.org/10.1038/nrendo.2009.196 Kumar N, Manimaran A, Kumaresan A, Jeyakumar S, Sreela L, Mooventhan P, Sivaram M (2017) Mastitis effects on reproductive performance in dairy cattle: a review. Trop Anim Health Prod 49:663–673. https://doi.org/10.1007/s11250-017-1253-4 Hodnett DW, DeLuca HF, Jorgensen NA (1992) Intestine, bone, and mammary gland contributions to maternal plasma calcium increase after abrupt weaning. Proc Soc Exp Biol Med 199:332–336