{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,27]],"date-time":"2026-04-27T19:48:58Z","timestamp":1777319338063,"version":"3.51.4"},"reference-count":37,"publisher":"Springer Science and Business Media LLC","issue":"3","license":[{"start":{"date-parts":[[2019,11,30]],"date-time":"2019-11-30T00:00:00Z","timestamp":1575072000000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"},{"start":{"date-parts":[[2019,11,30]],"date-time":"2019-11-30T00:00:00Z","timestamp":1575072000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"funder":[{"DOI":"10.13039\/501100001602","name":"Science Foundation Ireland","doi-asserted-by":"crossref","award":["14\/IA\/2884"],"award-info":[{"award-number":["14\/IA\/2884"]}],"id":[{"id":"10.13039\/501100001602","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Osteoporos Int"],"published-print":{"date-parts":[[2020,3]]},"DOI":"10.1007\/s00198-019-05239-5","type":"journal-article","created":{"date-parts":[[2019,12,2]],"date-time":"2019-12-02T11:58:00Z","timestamp":1575287880000},"page":"587-599","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":18,"title":["Secondary alterations in bone mineralisation and trabecular thickening occur after long-term estrogen deficiency in ovariectomised rat tibiae, which do not coincide with initial rapid bone loss"],"prefix":"10.1007","volume":"31","author":[{"given":"L. M.","family":"O\u2019Sullivan","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"H.","family":"Allison","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"E. E.","family":"Parle","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"J.","family":"Schiavi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"L. M.","family":"McNamara","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2019,11,30]]},"reference":[{"key":"5239_CR1","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/0002-9343(87)90274-9","volume":"82","author":"AM Parfitt","year":"1987","unstructured":"Parfitt AM (1987) Trabecular bone architecture in the pathogenesis and prevention of fracture. Am J Med 82:68\u201372","journal-title":"Am J Med"},{"key":"5239_CR2","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1016\/0169-6009(89)90039-1","volume":"6","author":"JE Compston","year":"1989","unstructured":"Compston JE, Mellish RWE, Croucher P, Newcombe R, Garrahan NJ (1989) Structural mechanisms of trabecular bone loss in man. Bone Miner 6:339\u2013350. https:\/\/doi.org\/10.1016\/0169-6009(89)90039-1","journal-title":"Bone Miner"},{"key":"5239_CR3","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1359\/jbmr.1998.13.2.229","volume":"13","author":"NE Lane","year":"1998","unstructured":"Lane NE, Thompson JM, Haupt D, Kimmel DB, Modin G, Kinney JH (1998) Acute changes in trabecular bone connectivity and osteoclast activity in the ovariectomized rat in vivo. J Bone Miner Res 13:229\u2013236. https:\/\/doi.org\/10.1359\/jbmr.1998.13.2.229","journal-title":"J Bone Miner Res"},{"key":"5239_CR4","doi-asserted-by":"publisher","first-page":"936","DOI":"10.1007\/s001980170022","volume":"12","author":"A Laib","year":"2001","unstructured":"Laib A, Kumer JL, Majumdar S, Lane NE (2001) The temporal changes of trabecular architecture in ovariectomized rats assessed by micro-CT. Osteoporos Int 12:936\u2013941. https:\/\/doi.org\/10.1007\/s001980170022","journal-title":"Osteoporos Int"},{"key":"5239_CR5","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1016\/8756-3282(95)80027-N","volume":"16","author":"DW Dempster","year":"1995","unstructured":"Dempster DW, Birchman R, Xu R, Lindsay R, Shen V (1995) Temporal changes in cancellous bone structure of rats immediately after ovariectomy. Bone 16:157\u2013161. https:\/\/doi.org\/10.1016\/8756-3282(95)80027-N","journal-title":"Bone"},{"key":"5239_CR6","doi-asserted-by":"publisher","first-page":"1371","DOI":"10.1007\/s00198-009-1082-z","volume":"21","author":"E Perilli","year":"2010","unstructured":"Perilli E, Le V, Ma B et al (2010) Detecting early bone changes using in vivo micro-CT in ovariectomized, zoledronic acid-treated, and sham-operated rats. Osteoporos Int 21:1371\u20131382. https:\/\/doi.org\/10.1007\/s00198-009-1082-z","journal-title":"Osteoporos Int"},{"key":"5239_CR7","doi-asserted-by":"publisher","first-page":"202","DOI":"10.1007\/s00223-007-9084-3","volume":"82","author":"JEM Brouwers","year":"2008","unstructured":"Brouwers JEM, Lambers FM, Gasser JA et al (2008) Bone degeneration and recovery after early and late bisphosphonate treatment of ovariectomized Wistar rats assessed by in vivo micro-computed tomography. Calcif Tissue Int 82:202\u2013211. https:\/\/doi.org\/10.1007\/s00223-007-9084-3","journal-title":"Calcif Tissue Int"},{"key":"5239_CR8","doi-asserted-by":"publisher","first-page":"926","DOI":"10.1002\/jor.20063","volume":"24","author":"JH Waarsing","year":"2006","unstructured":"Waarsing JH, Day JS, Verhaar JAN, Ederveen AG, Weinans H (2006) Bone loss dynamics result in trabecular alignment in aging and ovariectomized rats. J Orthop Res 24:926\u2013935. https:\/\/doi.org\/10.1002\/jor.20063","journal-title":"J Orthop Res"},{"key":"5239_CR9","doi-asserted-by":"publisher","first-page":"854","DOI":"10.1016\/j.bone.2006.04.017","volume":"39","author":"SK Boyd","year":"2006","unstructured":"Boyd SK, Davison P, M\u00fcller R, Gasser JA (2006) Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. Bone 39:854\u2013862. https:\/\/doi.org\/10.1016\/j.bone.2006.04.017","journal-title":"Bone"},{"key":"5239_CR10","doi-asserted-by":"publisher","first-page":"1034","DOI":"10.1016\/j.bone.2009.08.002","volume":"45","author":"B Busse","year":"2009","unstructured":"Busse B, Hahn M, Soltau M et al (2009) Increased calcium content and inhomogeneity of mineralization render bone toughness in osteoporosis: mineralization, morphology and biomechanics of human single trabeculae. Bone 45:1034\u20131043. https:\/\/doi.org\/10.1016\/j.bone.2009.08.002","journal-title":"Bone"},{"key":"5239_CR11","doi-asserted-by":"publisher","first-page":"396","DOI":"10.22203\/eCM.v021a30","volume":"21","author":"M Brennan","year":"2011","unstructured":"Brennan M, Gleeson J, Browne M et al (2011) Site specific increase in heterogeneity of trabecular bone tissue mineral during oestrogen deficiency. Eur Cells Mater 21:396\u2013406. https:\/\/doi.org\/10.22203\/eCM.v021a30","journal-title":"Eur Cells Mater"},{"key":"5239_CR12","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1007\/s00223-012-9657-7","volume":"91","author":"O Brennan","year":"2012","unstructured":"Brennan O, Kuliwaba JS, Lee TC, Parkinson IH, Fazzalari NL, McNamara L, O'Brien FJ (2012) Temporal changes in bone composition, architecture, and strength following estrogen deficiency in osteoporosis. Calcif Tissue Int 91:440\u2013449. https:\/\/doi.org\/10.1007\/s00223-012-9657-7","journal-title":"Calcif Tissue Int"},{"key":"5239_CR13","doi-asserted-by":"publisher","first-page":"161","DOI":"10.1016\/j.jmbbm.2013.08.029","volume":"29","author":"MA Brennan","year":"2014","unstructured":"Brennan MA, Gleeson JP, O\u2019Brien FJ, McNamara LM (2014) Effects of ageing, prolonged estrogen deficiency and zoledronate on bone tissue mineral distribution. J Mech Behav Biomed Mater 29:161\u2013170. https:\/\/doi.org\/10.1016\/j.jmbbm.2013.08.029","journal-title":"J Mech Behav Biomed Mater"},{"key":"5239_CR14","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1016\/S8756-3282(00)00448-8","volume":"28","author":"M Kneissel","year":"2001","unstructured":"Kneissel M, Boyde A, Gasser J (2001) Bone tissue and its mineralization in aged estrogen-depleted rats after long-term intermittent treatment with parathyroid hormone (PTH) analog SDZ PTS 893 or human PTH(1-34). Bone 28:237\u2013250. https:\/\/doi.org\/10.1016\/S8756-3282(00)00448-8","journal-title":"Bone"},{"key":"5239_CR15","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/J.BONE.2005.03.013","volume":"37","author":"A Valenta","year":"2005","unstructured":"Valenta A, Roschger P, Fratzl-Zelman N, Kostenuik PJ, Dunstan CR, Fratzl P, Klaushofer K (2005) Combined treatment with PTH (1\u201334) and OPG increases bone volume and uniformity of mineralization in aged ovariectomized rats. Bone 37:87\u201395. https:\/\/doi.org\/10.1016\/J.BONE.2005.03.013","journal-title":"Bone"},{"key":"5239_CR16","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1359\/jbmr.81005","volume":"24","author":"Z Cheng","year":"2009","unstructured":"Cheng Z, Yao W, Zimmermann EA, Busse C, Ritchie RO, Lane NE (2009) Prolonged treatments with antiresorptive agents and PTH have different effects on bone strength and the degree of mineralization in old estrogen-deficient osteoporotic rats. J Bone Miner Res 24:209\u2013220. https:\/\/doi.org\/10.1359\/jbmr.81005","journal-title":"J Bone Miner Res"},{"key":"5239_CR17","doi-asserted-by":"publisher","first-page":"1587","DOI":"10.1016\/j.bpj.2015.02.031","volume":"108","author":"SW Verbruggen","year":"2015","unstructured":"Verbruggen SW, Mc Garrigle MJ, Haugh MG et al (2015) Altered mechanical environment of bone cells in an animal model of short- and long-term osteoporosis. Biophys J 108:1587\u20131598. https:\/\/doi.org\/10.1016\/j.bpj.2015.02.031","journal-title":"Biophys J"},{"key":"5239_CR18","doi-asserted-by":"publisher","first-page":"1325","DOI":"10.1002\/jor.20439","volume":"25","author":"JEM Brouwers","year":"2007","unstructured":"Brouwers JEM, van Rietbergen B, Huiskes R (2007) No effects of in vivo micro-CT radiation on structural parameters and bone marrow cells in proximal tibia of Wistar rats detected after eight weekly scans. J Orthop Res 25:1325\u20131332. https:\/\/doi.org\/10.1002\/jor.20439","journal-title":"J Orthop Res"},{"key":"5239_CR19","doi-asserted-by":"publisher","first-page":"1468","DOI":"10.1002\/jbmr.141","volume":"25","author":"ML Bouxsein","year":"2010","unstructured":"Bouxsein ML, Boyd SK, Christiansen BA et al (2010) Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 25:1468\u20131486. https:\/\/doi.org\/10.1002\/jbmr.141","journal-title":"J Bone Miner Res"},{"key":"5239_CR20","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1016\/j.bone.2007.10.021","volume":"42","author":"P Roschger","year":"2008","unstructured":"Roschger P, Paschalis EP, Fratzl P, Klaushofer K (2008) Bone mineralization density distribution in health and disease. Bone 42:456\u2013466. https:\/\/doi.org\/10.1016\/j.bone.2007.10.021","journal-title":"Bone"},{"key":"5239_CR21","first-page":"424","volume":"58","author":"PP Lelovas","year":"2008","unstructured":"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\u2013430","journal-title":"Comp Med"},{"key":"5239_CR22","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1016\/0169-6009(91)90124-I","volume":"15","author":"DN Kalu","year":"1991","unstructured":"Kalu DN (1991) The ovariectomized rat model of postmenopausal bone loss. Bone Miner 15:175\u2013191. https:\/\/doi.org\/10.1016\/0169-6009(91)90124-I","journal-title":"Bone Miner"},{"key":"5239_CR23","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1002\/jbmr.5650040210","volume":"4","author":"JJ \u0160t\u011bp\u00e1n","year":"2009","unstructured":"\u0160t\u011bp\u00e1n JJ, Musilov\u00e1 J, Pacovsk\u00fd V (2009) Bone demineralization, biochemical indices of bone remodeling, and estrogen replacement therapy in adults with Turner\u2019s syndrome. J Bone Miner Res 4:193\u2013198. https:\/\/doi.org\/10.1002\/jbmr.5650040210","journal-title":"J Bone Miner Res"},{"key":"5239_CR24","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/0169-6009(90)90039-I","volume":"9","author":"JC Gallagher","year":"1990","unstructured":"Gallagher JC (1990) The pathogenesis of osteoporosis. Bone Miner 9:215\u2013227. https:\/\/doi.org\/10.1016\/0169-6009(90)90039-I","journal-title":"Bone Miner"},{"key":"5239_CR25","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1172\/JCI109516","volume":"64","author":"JC Gallagher","year":"1979","unstructured":"Gallagher JC, Riggs BL, Eisman J, Hamstra A, Arnaud SB, DeLuca H (1979) Intestinal calcium absorption and serum vitamin D metabolites in normal subjects and osteoporotic patients. J Clin Invest 64:729\u2013736. https:\/\/doi.org\/10.1172\/JCI109516","journal-title":"J Clin Invest"},{"key":"5239_CR26","doi-asserted-by":"publisher","first-page":"86","DOI":"10.1111\/j.1753-4887.1983.tb07709.x","volume":"41","author":"RP Heaney","year":"2009","unstructured":"Heaney RP, Recker RR, Omaha PDS (2009) Menopausal changes in calcium balance performance. Nutr Rev 41:86\u201389. https:\/\/doi.org\/10.1111\/j.1753-4887.1983.tb07709.x","journal-title":"Nutr Rev"},{"key":"5239_CR27","doi-asserted-by":"publisher","first-page":"1340","DOI":"10.1136\/bmj.280.6228.1340","volume":"280","author":"J Reeve","year":"1980","unstructured":"Reeve J, Meunier PJ, Parsons JA et al (1980) Anabolic effect of human parathyroid hormone fragment on trabecular bone in involutional osteoporosis: a multicentre trial. BMJ 280:1340\u20131344. https:\/\/doi.org\/10.1136\/bmj.280.6228.1340","journal-title":"BMJ"},{"key":"5239_CR28","doi-asserted-by":"publisher","first-page":"810","DOI":"10.1210\/endo-125-2-810","volume":"125","author":"TJ Wronski","year":"1989","unstructured":"Wronski TJ, Dann LM, Scott KS, Crooke LR (1989) Endocrine and pharmacological suppressors of bone turnover protect against osteopenia in ovariectomized rats. Endocrinology 125:810\u2013816. https:\/\/doi.org\/10.1210\/endo-125-2-810","journal-title":"Endocrinology"},{"key":"5239_CR29","doi-asserted-by":"publisher","first-page":"681","DOI":"10.1210\/endo-123-2-681","volume":"123","author":"TJ WronskiI","year":"1988","unstructured":"WronskiI TJ, Cintron M, Doherty AL, Dann LM (1988) Estrogen treatment prevents osteopenia and depresses bone turnover in ovariectomized rats. Endocrinology 123:681\u2013686. https:\/\/doi.org\/10.1210\/endo-123-2-681","journal-title":"Endocrinology"},{"key":"5239_CR30","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1007\/BF02555706","volume":"40","author":"A Simkin","year":"1987","unstructured":"Simkin A, Ayalon J, Leichter I (1987) Increased trabecular bone density due to bone-loading exercises in postmenopausal osteoporotic women. Calcif Tissue Int 40:59\u201363. https:\/\/doi.org\/10.1007\/BF02555706","journal-title":"Calcif Tissue Int"},{"key":"5239_CR31","doi-asserted-by":"publisher","first-page":"S125","DOI":"10.1016\/8756-3282(95)00285-L","volume":"17","author":"DD Thompson","year":"1995","unstructured":"Thompson DD, Simmons HA, Pirie CM, Ke HZ (1995) FDA guidelines and animal models for osteoporosis. Bone 17:S125\u2013S133. https:\/\/doi.org\/10.1016\/8756-3282(95)00285-L","journal-title":"Bone"},{"key":"5239_CR32","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1016\/j.bone.2011.04.008","volume":"49","author":"GM Campbell","year":"2011","unstructured":"Campbell GM, Bernhardt R, Scharnweber D, Boyd SK (2011) The bone architecture is enhanced with combined PTH and alendronate treatment compared to monotherapy while maintaining the state of surface mineralization in the OVX rat. Bone 49:225\u2013232. https:\/\/doi.org\/10.1016\/j.bone.2011.04.008","journal-title":"Bone"},{"key":"5239_CR33","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1016\/S0092-8674(01)00268-9","volume":"104","author":"S Kousteni","year":"2001","unstructured":"Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, Han K, DiGregorio G, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors. Cell 104:719\u2013730. https:\/\/doi.org\/10.1016\/S0092-8674(01)00268-9","journal-title":"Cell"},{"key":"5239_CR34","doi-asserted-by":"publisher","first-page":"3128","DOI":"10.1210\/jc.82.9.3128","volume":"82","author":"A Tomkinson","year":"1997","unstructured":"Tomkinson A (1997) The death of osteocytes via apoptosis accompanies estrogen withdrawal in human bone. J Clin Endocrinol Metab 82:3128\u20133135. https:\/\/doi.org\/10.1210\/jc.82.9.3128","journal-title":"J Clin Endocrinol Metab"},{"key":"5239_CR35","doi-asserted-by":"publisher","first-page":"119","DOI":"10.3109\/03008209309014239","volume":"29","author":"AJ Bailey","year":"1993","unstructured":"Bailey AJ, Wotton SF, Sims TJ, Thompson PW (1993) Biochemical changes in the collagen of human osteoporotic bone matrix. Connect Tissue Res 29:119\u2013132. https:\/\/doi.org\/10.3109\/03008209309014239","journal-title":"Connect Tissue Res"},{"key":"5239_CR36","doi-asserted-by":"publisher","first-page":"522","DOI":"10.1016\/S1357-2725(02)00312-6","volume":"35","author":"J Mansell","year":"2003","unstructured":"Mansell J, Bailey A (2003) Increased metabolism of bone collagen in post-menopausal female osteoporotic femoral heads. Int J Biochem Cell Biol 35:522\u2013529. https:\/\/doi.org\/10.1016\/S1357-2725(02)00312-6","journal-title":"Int J Biochem Cell Biol"},{"key":"5239_CR37","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1007\/s00198-005-2035-9","volume":"17","author":"S Viguet-Carrin","year":"2006","unstructured":"Viguet-Carrin S, Garnero P, Delmas PD (2006) The role of collagen in bone strength. Osteoporos Int 17:319\u2013336. https:\/\/doi.org\/10.1007\/s00198-005-2035-9","journal-title":"Osteoporos Int"}],"container-title":["Osteoporosis International"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00198-019-05239-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1007\/s00198-019-05239-5\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1007\/s00198-019-05239-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,11,29]],"date-time":"2020-11-29T00:39:48Z","timestamp":1606610388000},"score":1,"resource":{"primary":{"URL":"http:\/\/link.springer.com\/10.1007\/s00198-019-05239-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,11,30]]},"references-count":37,"journal-issue":{"issue":"3","published-print":{"date-parts":[[2020,3]]}},"alternative-id":["5239"],"URL":"https:\/\/doi.org\/10.1007\/s00198-019-05239-5","relation":{},"ISSN":["0937-941X","1433-2965"],"issn-type":[{"value":"0937-941X","type":"print"},{"value":"1433-2965","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,11,30]]},"assertion":[{"value":"9 May 2019","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 November 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"30 November 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Compliance with ethical standards"}},{"value":"None.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflicts of interest"}}]}}