Skip to main content
Top
Published in: Journal of Bone and Mineral Metabolism 4/2019

01-07-2019 | Original Article

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

Authors: Ryan D. Ross, Matthew J. Meagher, D. Rick Sumner

Published in: Journal of Bone and Mineral Metabolism | Issue 4/2019

Login to get access

Abstract

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.
Appendix
Available only for authorised users
Literature
2.
go back to reference Kovacs CS (2005) Calcium and bone metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 10:105–118CrossRefPubMed Kovacs CS (2005) Calcium and bone metabolism during pregnancy and lactation. J Mammary Gland Biol Neoplasia 10:105–118CrossRefPubMed
3.
go back to reference Brommage R, DeLuca HF (1985) Regulation of bone mineral loss during lactation. Am J Physiol 248:E182–E187PubMed Brommage R, DeLuca HF (1985) Regulation of bone mineral loss during lactation. Am J Physiol 248:E182–E187PubMed
4.
go back to reference 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 6:235–253CrossRefPubMed 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 6:235–253CrossRefPubMed
5.
go back to reference 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 17:1954–1960CrossRefPubMed 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 17:1954–1960CrossRefPubMed
6.
go back to reference 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 276:143–149CrossRefPubMed 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 276:143–149CrossRefPubMed
8.
go back to reference Kovacs CS (2011) Calcium and bone metabolism disorders during pregnancy and lactation. Endocrinol Metab Clin N Am 40:795–826CrossRef Kovacs CS (2011) Calcium and bone metabolism disorders during pregnancy and lactation. Endocrinol Metab Clin N Am 40:795–826CrossRef
9.
go back to reference Kovacs CS, Kronenberg HM (1997) Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev 18:832–872PubMed Kovacs CS, Kronenberg HM (1997) Maternal-fetal calcium and bone metabolism during pregnancy, puerperium, and lactation. Endocr Rev 18:832–872PubMed
10.
go back to reference 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 25:1468–1486CrossRefPubMed 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 25:1468–1486CrossRefPubMed
14.
go back to reference 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 77:426–435CrossRefPubMedPubMedCentral 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 77:426–435CrossRefPubMedPubMedCentral
15.
go back to reference 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 2:595–610CrossRefPubMed 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 2:595–610CrossRefPubMed
16.
go back to reference 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 7:283–287CrossRefPubMed 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 7:283–287CrossRefPubMed
18.
go back to reference 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 28:322–326CrossRefPubMed 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 28:322–326CrossRefPubMed
20.
go back to reference 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 67:367–372CrossRefPubMed 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 67:367–372CrossRefPubMed
21.
go back to reference 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 34:245–252CrossRefPubMed 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 34:245–252CrossRefPubMed
22.
go back to reference 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 3:293–304PubMed 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 3:293–304PubMed
23.
go back to reference Rasmussen P (1977) Calcium deficiency, pregnancy, and lactation in rats. Microscopic and microradiographic observations on bones. Calcif Tissue Res 23:95–102CrossRefPubMed Rasmussen P (1977) Calcium deficiency, pregnancy, and lactation in rats. Microscopic and microradiographic observations on bones. Calcif Tissue Res 23:95–102CrossRefPubMed
24.
go back to reference 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 178:180–185CrossRefPubMed 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 178:180–185CrossRefPubMed
26.
go back to reference Wong KM, Singer L, Ophaug RH (1980) Metabolic aspects of bone resorption in calcium-deficient lactating rats. Calcif Tissue Int 32:213–219CrossRefPubMed Wong KM, Singer L, Ophaug RH (1980) Metabolic aspects of bone resorption in calcium-deficient lactating rats. Calcif Tissue Int 32:213–219CrossRefPubMed
27.
go back to reference 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 65:689–695CrossRefPubMed 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 65:689–695CrossRefPubMed
28.
go back to reference Bowman BM, Miller SC (1999) Skeletal mass, chemistry, and growth during and after multiple reproductive cycles in the rat. Bone 25:553–559CrossRefPubMed Bowman BM, Miller SC (1999) Skeletal mass, chemistry, and growth during and after multiple reproductive cycles in the rat. Bone 25:553–559CrossRefPubMed
29.
go back to reference 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 17:1129–1135PubMed 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 17:1129–1135PubMed
30.
go back to reference 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 17:303–316CrossRefPubMed 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 17:303–316CrossRefPubMed
31.
go back to reference 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 27:1018–1029CrossRefPubMedPubMedCentral 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 27:1018–1029CrossRefPubMedPubMedCentral
34.
go back to reference 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 CrossRefPubMed 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 CrossRefPubMed
35.
go back to reference 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 11:43–53CrossRefPubMed 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 11:43–53CrossRefPubMed
36.
go back to reference 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 12:909–914CrossRefPubMed 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 12:909–914CrossRefPubMed
37.
go back to reference Garner SC, Boass A, Toverud SU (1989) Hypercalcemia fails to suppress elevated serum parathyroid hormone concentrations during lactation in rats. J Bone Miner Res 4:577–583CrossRefPubMed Garner SC, Boass A, Toverud SU (1989) Hypercalcemia fails to suppress elevated serum parathyroid hormone concentrations during lactation in rats. J Bone Miner Res 4:577–583CrossRefPubMed
38.
go back to reference 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) 290:65–73CrossRef 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) 290:65–73CrossRef
39.
go back to reference Pike JW, Parker JB, Haussler MR, Boass A, Toverud SV (1979) Dynamic changes in circulating 1,25-dihydroxyvitamin D during reproduction in rats. Science 204:1427–1429CrossRefPubMed Pike JW, Parker JB, Haussler MR, Boass A, Toverud SV (1979) Dynamic changes in circulating 1,25-dihydroxyvitamin D during reproduction in rats. Science 204:1427–1429CrossRefPubMed
40.
go back to reference 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 3:319–323CrossRefPubMed 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 3:319–323CrossRefPubMed
41.
go back to reference 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 276:549–554CrossRefPubMed 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 276:549–554CrossRefPubMed
44.
go back to reference Kovacs CS (2014) The role of PTHrP in regulating mineral metabolism during pregnancy, lactation, and fetal/neonatal development. Clin Rev Bone Miner Metab 12:142–164CrossRef Kovacs CS (2014) The role of PTHrP in regulating mineral metabolism during pregnancy, lactation, and fetal/neonatal development. Clin Rev Bone Miner Metab 12:142–164CrossRef
45.
go back to reference 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 63:122–136PubMed 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 63:122–136PubMed
46.
go back to reference 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 5:69–75CrossRefPubMed 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 5:69–75CrossRefPubMed
50.
go back to reference 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 199:332–336CrossRefPubMed 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 199:332–336CrossRefPubMed
Metadata
Title
Calcium restriction during lactation has minimal effects on post-weaning mineral metabolism and bone recovery
Authors
Ryan D. Ross
Matthew J. Meagher
D. Rick Sumner
Publication date
01-07-2019
Publisher
Springer Japan
Published in
Journal of Bone and Mineral Metabolism / Issue 4/2019
Print ISSN: 0914-8779
Electronic ISSN: 1435-5604
DOI
https://doi.org/10.1007/s00774-018-0969-1

Other articles of this Issue 4/2019

Journal of Bone and Mineral Metabolism 4/2019 Go to the issue