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Published in: BMC Musculoskeletal Disorders 1/2022

Open Access 01-12-2022 | Ovariectomy | Research

Early effects of ovariectomy on bone microstructure, bone turnover markers and mechanical properties in rats

Authors: Xingman Guo, Xiyue Yu, Qianqian Yao, Jian Qin

Published in: BMC Musculoskeletal Disorders | Issue 1/2022

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Abstract

Background

Fragility fracture is one of the most serious consequences of female aging, which can increase the risk of death. Therefore, paying attention to the pathogenesis of postmenopausal osteoporosis (PMOP) is very important for elderly women.

Methods and materials

Forty 12-week-old female rats were divided into two groups including the ovariectomy (OVX) group and the control group. Four rats in each group were selected at 1, 4, 8, 12 and 16 weeks after operation. Vertebral bones and femurs were dissected completely for micro-Computed Tomography (micro-CT) scanning, biological modulus detection and histomorphological observation.

Results

In OVX group, bone volume/total volume (BV/TV), bone trabecular connection density (Conn.D) and trabecular bone number (Tb.N) decreased significantly with time (P < 0.05). The elastic modulus of femur in OVX group was lower than that in control group, but there was no significant difference between them (P > 0.05). Over time, the tartrate resistant acid phosphatase (TRAP), osteocalcin (BGP), type I procollagen amino terminal propeptide (PINP) and type I collagen carboxy terminal peptide (CTX-I) in OVX group increased significantly (P < 0.05). The micrographs of the OVX group showed sparse loss of the trabecular interconnectivity and widening intertrabecular spaces with time.

Conclusion

The bone loss patterns of vertebral body and femur were different in the early stage of estrogen deficiency. The bone turnover rate of OVX rats increased, however the changes of biomechanical properties weren’t obvious.
Literature
1.
go back to reference Jamka K, Adamczuk P, Skowrońska A, Bojar I, Raszewski G. Assessment of the effect of estradiol on biochemical bone turnover markers among postmenopausal women. Ann Agric Environ Med. 2021;28(2):326–30.CrossRef Jamka K, Adamczuk P, Skowrońska A, Bojar I, Raszewski G. Assessment of the effect of estradiol on biochemical bone turnover markers among postmenopausal women. Ann Agric Environ Med. 2021;28(2):326–30.CrossRef
2.
go back to reference Jackson RD, Mysiw WJ. Insights into the epidemiology of postmenopausal osteoporosis: the Women’s Health Initiative. Semin Reprod Med. 2014;32(6):454–62.CrossRef Jackson RD, Mysiw WJ. Insights into the epidemiology of postmenopausal osteoporosis: the Women’s Health Initiative. Semin Reprod Med. 2014;32(6):454–62.CrossRef
3.
go back to reference Zhang RH, Zhang XB, Lu YB, et al. Calcitonin gene-related peptide and brain-derived serotonin are related to bone loss in ovariectomized rats. Brain Res Bull. 2021;176:85–92.CrossRef Zhang RH, Zhang XB, Lu YB, et al. Calcitonin gene-related peptide and brain-derived serotonin are related to bone loss in ovariectomized rats. Brain Res Bull. 2021;176:85–92.CrossRef
4.
go back to reference O'Sullivan LM, Allison H, Parle EE, Schiavi J, McNamara LM. 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. Osteoporos Int. 2020;31(3):587–99.CrossRef O'Sullivan LM, Allison H, Parle EE, Schiavi J, McNamara LM. 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. Osteoporos Int. 2020;31(3):587–99.CrossRef
5.
go back to reference Zhu M, Hao G, Xing J, et al. Bone marrow adipose amount influences vertebral bone strength. Exp Ther Med. 2019;17(1):689–94.PubMed Zhu M, Hao G, Xing J, et al. Bone marrow adipose amount influences vertebral bone strength. Exp Ther Med. 2019;17(1):689–94.PubMed
6.
go back to reference Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010;25(7):1468–86.CrossRef Bouxsein ML, Boyd SK, Christiansen BA, Guldberg RE, Jepsen KJ, Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010;25(7):1468–86.CrossRef
7.
go back to reference Mohsin S, Kaimala S, Sunny JJ, Adeghate E, Brown EM. Type 2 diabetes mellitus increases the risk to hip fracture in postmenopausal osteoporosis by deteriorating the trabecular bone microarchitecture and bone mass. J Diabetes Res. 2019;2019:3876957.CrossRef Mohsin S, Kaimala S, Sunny JJ, Adeghate E, Brown EM. Type 2 diabetes mellitus increases the risk to hip fracture in postmenopausal osteoporosis by deteriorating the trabecular bone microarchitecture and bone mass. J Diabetes Res. 2019;2019:3876957.CrossRef
8.
go back to reference Yang D, Wan Y. Molecular determinants for the polarization of macrophage and osteoclast. Semin Immunopathol. 2019;41(5):551–63.CrossRef Yang D, Wan Y. Molecular determinants for the polarization of macrophage and osteoclast. Semin Immunopathol. 2019;41(5):551–63.CrossRef
9.
go back to reference Shang Q, Zhao W, Shen G, et al. Jingui Shenqi pills regulate bone-fat balance in murine ovariectomy-induced osteoporosis with kidney yang deficiency. Evid Based Complement Alternat Med. 2020;2020:1517596.PubMedPubMedCentral Shang Q, Zhao W, Shen G, et al. Jingui Shenqi pills regulate bone-fat balance in murine ovariectomy-induced osteoporosis with kidney yang deficiency. Evid Based Complement Alternat Med. 2020;2020:1517596.PubMedPubMedCentral
10.
go back to reference Vanhooren V, Libert C. The mouse as a model organism in aging research: usefulness, pitfalls and possibilities. Ageing Res Rev. 2013;12(1):8–21.CrossRef Vanhooren V, Libert C. The mouse as a model organism in aging research: usefulness, pitfalls and possibilities. Ageing Res Rev. 2013;12(1):8–21.CrossRef
11.
go back to reference Shahrezaee M, Oryan A, Bastami F, Hosseinpour S, Shahrezaee MH, Kamali A. Comparative impact of systemic delivery of atorvastatin, simvastatin, and lovastatin on bone mineral density of the ovariectomized rats. Endocrine. 2018;60(1):138–50.CrossRef Shahrezaee M, Oryan A, Bastami F, Hosseinpour S, Shahrezaee MH, Kamali A. Comparative impact of systemic delivery of atorvastatin, simvastatin, and lovastatin on bone mineral density of the ovariectomized rats. Endocrine. 2018;60(1):138–50.CrossRef
12.
go back to reference Xu H, Liu T, Hu L, et al. Effect of caffeine on ovariectomy-induced osteoporosis in rats. Biomed Pharmacother. 2019;112:108650.CrossRef Xu H, Liu T, Hu L, et al. Effect of caffeine on ovariectomy-induced osteoporosis in rats. Biomed Pharmacother. 2019;112:108650.CrossRef
13.
go back to reference Emami AJ, Toupadakis CA, Telek SM, Fyhrie DP, Yellowley CE, Christiansen BA. Age dependence of systemic bone loss and recovery following femur fracture in mice. J Bone Miner Res. 2019;34(1):157–70.CrossRef Emami AJ, Toupadakis CA, Telek SM, Fyhrie DP, Yellowley CE, Christiansen BA. Age dependence of systemic bone loss and recovery following femur fracture in mice. J Bone Miner Res. 2019;34(1):157–70.CrossRef
14.
go back to reference Shi J, Lee S, Uyeda M, et al. Guidelines for dual energy X-ray absorptiometry analysis of trabecular bone-rich regions in mice: improved precision, accuracy, and sensitivity for assessing longitudinal bone changes. Tissue Eng Part C Methods. 2016;22(5):451–63.CrossRef Shi J, Lee S, Uyeda M, et al. Guidelines for dual energy X-ray absorptiometry analysis of trabecular bone-rich regions in mice: improved precision, accuracy, and sensitivity for assessing longitudinal bone changes. Tissue Eng Part C Methods. 2016;22(5):451–63.CrossRef
15.
go back to reference Surowiec RK, Ram S, Idiyatullin D, et al. In vivo quantitative imaging biomarkers of bone quality and mineral density using multi-band-SWIFT magnetic resonance imaging. Bone. 2021;143:115615.CrossRef Surowiec RK, Ram S, Idiyatullin D, et al. In vivo quantitative imaging biomarkers of bone quality and mineral density using multi-band-SWIFT magnetic resonance imaging. Bone. 2021;143:115615.CrossRef
16.
go back to reference Manolagas SC, Weinstein RS. New developments in the pathogenesis and treatment of steroid-induced osteoporosis. J Bone Miner Res. 1999;14(7):1061–6.CrossRef Manolagas SC, Weinstein RS. New developments in the pathogenesis and treatment of steroid-induced osteoporosis. J Bone Miner Res. 1999;14(7):1061–6.CrossRef
17.
go back to reference Wu ZX, Lei W, Hu YY, et al. Effect of ovariectomy on BMD, micro-architecture and biomechanics of cortical and cancellous bones in a sheep model. Med Eng Phys. 2008;30(9):1112–8.CrossRef Wu ZX, Lei W, Hu YY, et al. Effect of ovariectomy on BMD, micro-architecture and biomechanics of cortical and cancellous bones in a sheep model. Med Eng Phys. 2008;30(9):1112–8.CrossRef
18.
go back to reference Laib A, Kumer JL, Majumdar S, et al. The temporal changes of trabecular architecture in ovariectomized rats assessed by MicroCT. Osteoporos Int. 2001;12(11):936–41.CrossRef Laib A, Kumer JL, Majumdar S, et al. The temporal changes of trabecular architecture in ovariectomized rats assessed by MicroCT. Osteoporos Int. 2001;12(11):936–41.CrossRef
19.
go back to reference Shin YH, Cho DC, Yu SH, et al. Histomorphometric analysis of the spine and femur in ovariectomized rats using micro-computed tomographic scan. J Kor Neurosurg Soc. 2012;52(1):1–6.CrossRef Shin YH, Cho DC, Yu SH, et al. Histomorphometric analysis of the spine and femur in ovariectomized rats using micro-computed tomographic scan. J Kor Neurosurg Soc. 2012;52(1):1–6.CrossRef
20.
go back to reference Luu AN, Anez-Bustillos L, Aran S, et al. Microstructural, densitometric and metabolic variations in bones from rats with normal or altered skeletal states. PLoS One. 2013;8(12):e82709.CrossRef Luu AN, Anez-Bustillos L, Aran S, et al. Microstructural, densitometric and metabolic variations in bones from rats with normal or altered skeletal states. PLoS One. 2013;8(12):e82709.CrossRef
21.
go back to reference Zeitoun D, Caliaperoumal G, Bensidhoum M, Constans JM, Anagnostou F, Bousson V. Microcomputed tomography of the femur of diabetic rats: alterations of trabecular and cortical bone microarchitecture and vasculature-a feasibility study. Eur Radiol Exp. 2019;3(1):17.CrossRef Zeitoun D, Caliaperoumal G, Bensidhoum M, Constans JM, Anagnostou F, Bousson V. Microcomputed tomography of the femur of diabetic rats: alterations of trabecular and cortical bone microarchitecture and vasculature-a feasibility study. Eur Radiol Exp. 2019;3(1):17.CrossRef
22.
go back to reference Anumula S, Wehrli SL, Magland J, Wright AC, Wehrli FW. Ultra-short echo-time MRI detects changes in bone mineralization and water content in OVX rat bone in response to alendronate treatment. Bone. 2010;46(5):1391–9.CrossRef Anumula S, Wehrli SL, Magland J, Wright AC, Wehrli FW. Ultra-short echo-time MRI detects changes in bone mineralization and water content in OVX rat bone in response to alendronate treatment. Bone. 2010;46(5):1391–9.CrossRef
23.
go back to reference Giavaresi G, Fini M, Gnudi S, et al. Comparison of calcitonin, alendronate and fluorophosphate effects on ovariectomized rat bone. Biomed Pharmacother. 2001;55(7):397–403.CrossRef Giavaresi G, Fini M, Gnudi S, et al. Comparison of calcitonin, alendronate and fluorophosphate effects on ovariectomized rat bone. Biomed Pharmacother. 2001;55(7):397–403.CrossRef
24.
go back to reference Eastell R, Szulc P. Use of bone turnover markers in postmenopausal osteoporosis. Lancet Diabetes Endocrinol. 2017;5(11):908–23.CrossRef Eastell R, Szulc P. Use of bone turnover markers in postmenopausal osteoporosis. Lancet Diabetes Endocrinol. 2017;5(11):908–23.CrossRef
25.
go back to reference Abildgaard J, Tingstedt J, Zhao Y, et al. Increased systemic inflammation and altered distribution of T-cell subsets in postmenopausal women. PLoS One. 2020;15(6):e0235174.CrossRef Abildgaard J, Tingstedt J, Zhao Y, et al. Increased systemic inflammation and altered distribution of T-cell subsets in postmenopausal women. PLoS One. 2020;15(6):e0235174.CrossRef
26.
go back to reference Orchard T, Yildiz V, Steck SE, et al. Dietary inflammatory index, bone mineral density, and risk of fracture in postmenopausal women: results from the Women’s Health Initiative. J Bone Miner Res. 2017;32(5):1136–46.CrossRef Orchard T, Yildiz V, Steck SE, et al. Dietary inflammatory index, bone mineral density, and risk of fracture in postmenopausal women: results from the Women’s Health Initiative. J Bone Miner Res. 2017;32(5):1136–46.CrossRef
27.
go back to reference Vasikaran S, Cooper C, Eastell R, et al. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med. 2011;49(8):1271–4.CrossRef Vasikaran S, Cooper C, Eastell R, et al. International Osteoporosis Foundation and International Federation of Clinical Chemistry and Laboratory Medicine position on bone marker standards in osteoporosis. Clin Chem Lab Med. 2011;49(8):1271–4.CrossRef
28.
go back to reference Scheuren AC, Kuhn GA, Müller R. Effects of long-term in vivo micro-CT imaging on hallmarks of osteopenia and frailty in aging mice. PLoS One. 2020;15(9):e0239534.CrossRef Scheuren AC, Kuhn GA, Müller R. Effects of long-term in vivo micro-CT imaging on hallmarks of osteopenia and frailty in aging mice. PLoS One. 2020;15(9):e0239534.CrossRef
29.
go back to reference Fuggle NR, Curtis EM, Ward KA, Harvey NC, Dennison EM, Cooper C. Fracture prediction, imaging and screening in osteoporosis. Nat Rev Endocrinol. 2019;15(9):535–47.CrossRef Fuggle NR, Curtis EM, Ward KA, Harvey NC, Dennison EM, Cooper C. Fracture prediction, imaging and screening in osteoporosis. Nat Rev Endocrinol. 2019;15(9):535–47.CrossRef
Metadata
Title
Early effects of ovariectomy on bone microstructure, bone turnover markers and mechanical properties in rats
Authors
Xingman Guo
Xiyue Yu
Qianqian Yao
Jian Qin
Publication date
01-12-2022
Publisher
BioMed Central
Published in
BMC Musculoskeletal Disorders / Issue 1/2022
Electronic ISSN: 1471-2474
DOI
https://doi.org/10.1186/s12891-022-05265-1

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