Skip to main content
Top
Published in: Calcified Tissue International 2/2017

01-08-2017 | Original Research

Bone Matrix Maturation in a Rat Model of Intra-Cortical Bone Remodeling

Authors: Ryan D. Ross, D. Rick Sumner

Published in: Calcified Tissue International | Issue 2/2017

Login to get access

Abstract

Matrix maturation within cortical bone is an important but oft-neglected component of bone remodeling because of the lack of a suitable small animal model. Intra-cortical remodeling can be induced in rodents by feeding virgin or lactating animals a low-calcium diet. The current study aimed to determine which of these two models is most suitable for studying intra-cortical matrix maturation. We compared intra-cortical remodeling in female rats fed a normal calcium diet (virgin/normal Ca), a low-calcium diet (virgin/low Ca), or a low-calcium diet during lactation (lactation/low Ca). The low-calcium diet was administered for 23 days (induction phase) followed by return to normal calcium for 30 days (recovery phase). At the end of induction, the virgin/normal Ca and virgin/low-Ca animals had no difference in cortical porosity, but the lactation/low-Ca animals had elevated cortical porosity at various diaphyseal sites in the femur and tibia. The distal femoral site had the greatest amount of induced porosity in the size range of rat secondary osteons. Neither global mineralization nor tissue age-specific mineral-to-matrix ratio in the bone formed during recovery were affected in the lactation/low-Ca rats. Serum calcium levels did not differ from controls, but phosphate levels were slightly elevated, consistent with the rapid recovery of lost bone mass. We conclude that the lactation/low-Ca model represents a means to increase intra-cortical remodeling in adult rats with no apparent detrimental effect on matrix maturation. This model will provide researchers with a new tool to study matrix maturation throughout the cortex.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lelovas PP, Xanthos TT, Thoma SE, Lyritis GP, Dontas IA (2008) The laboratory rat as an animal model for osteoporosis research. Comp Med 58:424–430PubMedPubMedCentral Lelovas PP, Xanthos TT, Thoma SE, Lyritis GP, Dontas IA (2008) The laboratory rat as an animal model for osteoporosis research. Comp Med 58:424–430PubMedPubMedCentral
2.
go back to reference Jee WS, Yao W (2001) Overview: animal models of osteopenia and osteoporosis. J Musculoskelet Neuronal Interact 1:193–207PubMed Jee WS, Yao W (2001) Overview: animal models of osteopenia and osteoporosis. J Musculoskelet Neuronal Interact 1:193–207PubMed
3.
go back to reference Ruth EB (1953) Bone studies. II. An experimental study of the Haversian-type vascular channels. Am J Anat 93:429–455CrossRefPubMed Ruth EB (1953) Bone studies. II. An experimental study of the Haversian-type vascular channels. Am J Anat 93:429–455CrossRefPubMed
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 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
6.
go back to reference Stauffer M, Baylink D, Wergedal J, Rich C (1973) Decreased bone formation, mineralization, and enhanced resorption in calcium-deficient rats. Am J Physiol 225:269–276PubMed Stauffer M, Baylink D, Wergedal J, Rich C (1973) Decreased bone formation, mineralization, and enhanced resorption in calcium-deficient rats. Am J Physiol 225:269–276PubMed
7.
go back to reference Stauffer M, Baylink D, Wergedal J, Rich C (1972) Bone repletion in calcium deficient rats fed a high calcium diet. Calcif Tissue Res 9:163–172CrossRefPubMed Stauffer M, Baylink D, Wergedal J, Rich C (1972) Bone repletion in calcium deficient rats fed a high calcium diet. Calcif Tissue Res 9:163–172CrossRefPubMed
8.
go back to reference Sissons HA, Kelman GJ, Marotti G (1984) Mechanisms of bone resorption in calcium-deficient rats. Calcif Tissue Int 36:711–721CrossRefPubMed Sissons HA, Kelman GJ, Marotti G (1984) Mechanisms of bone resorption in calcium-deficient rats. Calcif Tissue Int 36:711–721CrossRefPubMed
9.
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 & amp. Histopathol 17:1129–1135 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 & amp. Histopathol 17:1129–1135
10.
go back to reference Seto H, Aoki K, Kasugai S, Ohya K (1999) Trabecular bone turnover, bone marrow cell development, and gene expression of bone matrix proteins after low calcium feeding in rats. Bone 25:687–695CrossRefPubMed Seto H, Aoki K, Kasugai S, Ohya K (1999) Trabecular bone turnover, bone marrow cell development, and gene expression of bone matrix proteins after low calcium feeding in rats. Bone 25:687–695CrossRefPubMed
11.
go back to reference Geng W, DeMoss DL, Wright GL (2000) Effect of calcium stress on the skeleton mass of intact and ovariectomized rats. Life Sci 66:2309–2321CrossRefPubMed Geng W, DeMoss DL, Wright GL (2000) Effect of calcium stress on the skeleton mass of intact and ovariectomized rats. Life Sci 66:2309–2321CrossRefPubMed
12.
go back to reference Drivdahl RH, Liu CC, Baylink DJ (1984) Regulation of bone repletion in rats subjected to varying low-calcium stress. Am J Physiol 246:R190–R196PubMed Drivdahl RH, Liu CC, Baylink DJ (1984) Regulation of bone repletion in rats subjected to varying low-calcium stress. Am J Physiol 246:R190–R196PubMed
13.
go back to reference 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 53:49CrossRefPubMedPubMedCentral 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 53:49CrossRefPubMedPubMedCentral
14.
go back to reference 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 56:64CrossRefPubMedPubMedCentral 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 56:64CrossRefPubMedPubMedCentral
15.
go back to reference Ross RD, Edwards LH, Acerbo AS, Ominsky MS, Virdi AS, Sena K, Miller LM, Sumner DR (2014) Bone matrix quality following sclerostin antibody treatment. J Bone Miner Res 29:1597–1607CrossRefPubMed Ross RD, Edwards LH, Acerbo AS, Ominsky MS, Virdi AS, Sena K, Miller LM, Sumner DR (2014) Bone matrix quality following sclerostin antibody treatment. J Bone Miner Res 29:1597–1607CrossRefPubMed
16.
go back to reference Acerbo AS, Carr GL, Judex S, Miller LM (2012) Imaging the material properties of bone specimens using reflection-based infrared microspectroscopy. Anal Chem 84:3607–3613CrossRefPubMedPubMedCentral Acerbo AS, Carr GL, Judex S, Miller LM (2012) Imaging the material properties of bone specimens using reflection-based infrared microspectroscopy. Anal Chem 84:3607–3613CrossRefPubMedPubMedCentral
17.
go back to reference Osborne DL, Curtis J (2005) A protocol for the staining of cement lines in adult human bone using toluidine blue. J Histotechnol 28:73–79CrossRef Osborne DL, Curtis J (2005) A protocol for the staining of cement lines in adult human bone using toluidine blue. J Histotechnol 28:73–79CrossRef
18.
19.
go back to reference Fujisawa R, Tamura M (2012) Acidic bone matrix proteins and their roles in calcification. Front Biosci 17:1891–1903CrossRef Fujisawa R, Tamura M (2012) Acidic bone matrix proteins and their roles in calcification. Front Biosci 17:1891–1903CrossRef
20.
go back to reference Marotti G, Favia A, Zallone AZ (1972) Quantitative analysis on the rate of secondary bone mineralization. Calcif Tissue Res 10:67–81CrossRefPubMed Marotti G, Favia A, Zallone AZ (1972) Quantitative analysis on the rate of secondary bone mineralization. Calcif Tissue Res 10:67–81CrossRefPubMed
21.
go back to reference Boivin G, Meunier PJ (2003) Methodological considerations in measurement of bone mineral content. Osteoporos Int 14(Suppl 5):S22–S27CrossRefPubMed Boivin G, Meunier PJ (2003) Methodological considerations in measurement of bone mineral content. Osteoporos Int 14(Suppl 5):S22–S27CrossRefPubMed
22.
go back to reference Boivin G, Meunier PJ (2002) Changes in bone remodeling rate influence the degree of mineralization of bone. Connect Tissue Res 43:535–537CrossRefPubMed Boivin G, Meunier PJ (2002) Changes in bone remodeling rate influence the degree of mineralization of bone. Connect Tissue Res 43:535–537CrossRefPubMed
23.
go back to reference Bala Y, Farlay D, Delmas PD, Meunier PJ, Boivin G (2010) Time sequence of secondary mineralization and microhardness in cortical and cancellous bone from ewes. Bone 46:1204–1212CrossRefPubMed Bala Y, Farlay D, Delmas PD, Meunier PJ, Boivin G (2010) Time sequence of secondary mineralization and microhardness in cortical and cancellous bone from ewes. Bone 46:1204–1212CrossRefPubMed
24.
go back to reference Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB (2003) Aging of microstructural compartments in human compact bone. J Bone Miner Res 18:1012–1019CrossRefPubMed Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB (2003) Aging of microstructural compartments in human compact bone. J Bone Miner Res 18:1012–1019CrossRefPubMed
25.
go back to reference Fuchs RK, Allen MR, Ruppel ME, Diab T, Phipps RJ, Miller LM, Burr DB (2008) In situ examination of the time-course for secondary mineralization of Haversian bone using synchrotron Fourier transform infrared microspectroscopy. Matrix Biol 27:34–41CrossRefPubMed Fuchs RK, Allen MR, Ruppel ME, Diab T, Phipps RJ, Miller LM, Burr DB (2008) In situ examination of the time-course for secondary mineralization of Haversian bone using synchrotron Fourier transform infrared microspectroscopy. Matrix Biol 27:34–41CrossRefPubMed
26.
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
27.
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
28.
go back to reference Ross RD, mashiatulla M, Robling AG, Miller LM, Sumner DR (2015) Bone matrix composition following PTH treatment is not dependent on sclerostin status. Calcif. Tissue Int 98(2):149–157CrossRefPubMed Ross RD, mashiatulla M, Robling AG, Miller LM, Sumner DR (2015) Bone matrix composition following PTH treatment is not dependent on sclerostin status. Calcif. Tissue Int 98(2):149–157CrossRefPubMed
29.
go back to reference Roschger P, Paschalis EP, Fratzl P, Klaushofer K (2008) Bone mineralization density distribution in health and disease. Bone 42:456–466CrossRefPubMed Roschger P, Paschalis EP, Fratzl P, Klaushofer K (2008) Bone mineralization density distribution in health and disease. Bone 42:456–466CrossRefPubMed
30.
go back to reference Wergedal JE, Baylink DJ (1974) Electron microprobe measurements of bone mineralization rate in vivo. Am J Physiol 226:345–352PubMed Wergedal JE, Baylink DJ (1974) Electron microprobe measurements of bone mineralization rate in vivo. Am J Physiol 226:345–352PubMed
31.
go back to reference Donnelly E, Boskey AL, Baker SP, van der Meulen MC (2010) Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A 92:1048–1056PubMedPubMedCentral Donnelly E, Boskey AL, Baker SP, van der Meulen MC (2010) Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A 92:1048–1056PubMedPubMedCentral
32.
go back to reference Ruffoni D, Fratzl P, Roschger P, Klaushofer K, Weinkamer R (2007) The bone mineralization density distribution as a fingerprint of the mineralization process. Bone 40:1308–1319CrossRefPubMed Ruffoni D, Fratzl P, Roschger P, Klaushofer K, Weinkamer R (2007) The bone mineralization density distribution as a fingerprint of the mineralization process. Bone 40:1308–1319CrossRefPubMed
33.
go back to reference Fuchs RK, Faillace ME, Allen MR, Phipps RJ, Miller LM, Burr DB (2011) Bisphosphonates do not alter the rate of secondary mineralization. Bone 49:701–705CrossRefPubMed Fuchs RK, Faillace ME, Allen MR, Phipps RJ, Miller LM, Burr DB (2011) Bisphosphonates do not alter the rate of secondary mineralization. Bone 49:701–705CrossRefPubMed
34.
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
35.
go back to reference Rasmussen P (1977) Calcium deficiency, pregnancy, and lactation in rats. Some effects on blood chemistry and the skeleton. Calcif Tissue Res 23:87–94CrossRefPubMed Rasmussen P (1977) Calcium deficiency, pregnancy, and lactation in rats. Some effects on blood chemistry and the skeleton. Calcif Tissue Res 23:87–94CrossRefPubMed
36.
go back to reference Wong KM, Singer L, Ophaug RH, Klein L (1981) Effect of lactation and calcium deficiency, and of fluoride intake, on bone turnover in rats: isotopic measurements of bone resorption and formation. J Nutr 111:1848–1854PubMed Wong KM, Singer L, Ophaug RH, Klein L (1981) Effect of lactation and calcium deficiency, and of fluoride intake, on bone turnover in rats: isotopic measurements of bone resorption and formation. J Nutr 111:1848–1854PubMed
37.
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
38.
go back to reference Lozupone E, Favia A (1988) Distribution of resorption processes in the compacta and spongiosa of bones from lactating rats fed a low-calcium diet. Bone 9:215–224CrossRefPubMed Lozupone E, Favia A (1988) Distribution of resorption processes in the compacta and spongiosa of bones from lactating rats fed a low-calcium diet. Bone 9:215–224CrossRefPubMed
39.
go back to reference Gruber HE, Stover SJ (1994) Maternal and weanling bone: the influence of lowered calcium intake and maternal dietary history. Bone 15:167–176CrossRefPubMed Gruber HE, Stover SJ (1994) Maternal and weanling bone: the influence of lowered calcium intake and maternal dietary history. Bone 15:167–176CrossRefPubMed
40.
go back to reference Harrison M, Fraser R (1960) Bone structure and metabolism in calcium-deficient rats. J Endocrinol 21:197–205CrossRefPubMed Harrison M, Fraser R (1960) Bone structure and metabolism in calcium-deficient rats. J Endocrinol 21:197–205CrossRefPubMed
41.
go back to reference Cuisnier-Gleizes P, Thomasset M, Sainteny-Debove F, Mathieu H (1976) Phosphorus deficiency, parathyroid hormone and bone resorption in the growing rat. Calcif Tissue Res 20:235–249CrossRefPubMed Cuisnier-Gleizes P, Thomasset M, Sainteny-Debove F, Mathieu H (1976) Phosphorus deficiency, parathyroid hormone and bone resorption in the growing rat. Calcif Tissue Res 20:235–249CrossRefPubMed
42.
go back to reference Sharp PE, LaRegina MC (1998) The laboratory rat. CRC Press LLC, Boca Raton Sharp PE, LaRegina MC (1998) The laboratory rat. CRC Press LLC, Boca Raton
44.
go back to reference Kim C, Park D (2013) The effect of restriction of dietary calcium on trabecular and cortical bone mineral density in the rats. J Exerc Nutr Biochem 17:123–131CrossRef Kim C, Park D (2013) The effect of restriction of dietary calcium on trabecular and cortical bone mineral density in the rats. J Exerc Nutr Biochem 17:123–131CrossRef
Metadata
Title
Bone Matrix Maturation in a Rat Model of Intra-Cortical Bone Remodeling
Authors
Ryan D. Ross
D. Rick Sumner
Publication date
01-08-2017
Publisher
Springer US
Published in
Calcified Tissue International / Issue 2/2017
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-017-0270-7

Other articles of this Issue 2/2017

Calcified Tissue International 2/2017 Go to the issue