Effect of parathyroid hormone on the structural, densitometric and failure behaviors of mouse tibia in the spatiotemporal space

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Abstract

Parathyroid hormone (PTH) is an anabolic bone drug approved by the US Food and Drug Administration (FDA) to treat osteoporosis. However, previous studies using cross-sectional designs have reported variable and sometimes contradictory results. The aim of the present study was to quantify the localized effect of PTH on the structural and densitometric behaviors of mouse tibia and their links with the global mechanical behavior of bone using a novel spatiotemporal image analysis approach and a finite element analysis technique. Twelve female C57BL/6J mice were divided into two groups: the control and PTH treated groups. The entire right tibiae were imaged using an in vivo micro-computed tomography (μCT) system eight consecutive times. Next, the in vivo longitudinal tibial μCT images were rigidly registered and divided into 10 compartments across the entire tibial space. The bone volume (BV), bone mineral content (BMC), bone tissue mineral density (TMD), and tibial endosteal and periosteal areas (TEA and TPA) were quantified in each compartment. Additionally, finite element models of all the tibiae were generated to analyze the failure behavior of the tibia. It was found that both the BMC and BV started to increase in the proximal tibial region, and then the increases extended to the entire tibial region after two weeks of treatment ( p < 0.05). PTH intervention significantly reduced the TEA in most tibial compartments after two weeks of treatment, and the TPA increased in most tibial regions after four weeks of treatment ( p < 0.05). Tibial failure loads significantly increased after three weeks of PTH treatment ( p < 0.01). The present study provided the first evidence of the localized effect of PTH on bone structural and densitometric properties, as well as their links with the global mechanical behaviors of bone, which are important pieces of information for unveiling the mechanism of PTH intervention.

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Most cited references 31

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Age-related changes in trabecular architecture differ in female and male C57BL/6J mice.

Vaida Glatt, Ernesto Canalis, Lisa Stadmeyer … (2007)

We used microCT and histomorphometry to assess age-related changes in bone architecture in male and female C57BL/6J mice. Deterioration in vertebral and femoral trabecular microarchitecture begins early, continues throughout life, is more pronounced at the femoral metaphysis than in the vertebrae, and is greater in females than males. Despite widespread use of mice in the study of musculoskeletal disease, the age-related changes in murine bone structure and the relationship to whole body BMD changes are not well characterized. Thus, we assessed age-related changes in body composition, whole body BMD, and trabecular and cortical microarchitecture at axial and appendicular sites in mice. Peripheral DXA was used to assess body composition and whole body BMD in vivo, and microCT and histomorphometry were used to measure trabecular and cortical architecture in excised femora, tibia, and vertebrae in male and female C57BL/6J mice at eight time-points between 1 and 20 mo of age (n = 6-9/group). Body weight and total body BMD increased with age in male and female, with a marked increase in body fat between 6 and 12 mo of age. In contrast, trabecular bone volume (BV/TV) was greatest at 6-8 wk of age and declined steadily thereafter, particularly in the metaphyseal region of long bones. Age-related declines in BV/TV were greater in female than male. Trabecular bone loss was characterized by a rapid decrease in trabecular number between 2 and 6 mo of age, and a more gradual decline thereafter, whereas trabecular thickness increased slowly over life. Cortical thickness increased markedly from 1 to 3 mo of age and was maintained or slightly decreased thereafter. In C57BL/6J mice, despite increasing body weight and total body BMD, age-related declines in vertebral and distal femoral trabecular bone volume occur early and continue throughout life and are more pronounced in females than males. Awareness of these age-related changed in bone morphology are critical for interpreting the skeletal response to pharmacologic interventions or genetic manipulation in mice.

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Requirements for DXA for the management of osteoporosis in Europe.

J Kanis, O. Johnell (2005)

The availability of dual energy X-ray absorptiometry (DXA) varies markedly in different countries. There is, however, little information to indicate the optimal requirements for this technology. The principal aim of this study was to estimate the requirements for DXA in Europe for the assessment and treatment of osteoporosis. Three assessment scenarios were chosen. The first envisaged screening of all women with DXA at the age of 65 years. A second scenario comprised a screening programme based on the identification of clinical risk factors with the selective addition of BMD tests in those close to an intervention threshold. The third scenario envisaged a case finding strategy where women aged 65 years were identified on the basis of risk factors and referred for DXA. Requirements for women aged more than 65 years were amortised over a 10-year period. A secondary aim was to estimate the number and cost of osteoporotic fractures in Europe. The requirements for DXA in assessment ranged from 4.21 to 11.21 units/million of the population. The most efficient assessment scenario was the use of clinical risk factors with the selective use of BMD. With this scenario, an additional 6.39 units/million would be required to monitor treatment giving a total requirement of 10.6 units/million. In 2000, the number of osteoporotic fractures was estimated at 3.79 million, of which 0.89 million were hip fractures (179,000 hip fractures in men and 711,000 in women). The total direct costs were estimated at 31.7 billion Euros (21.165 billion UK pounds), which were expected to increase to 76.7 billion Euros (51.1 billion UK pounds) in 2050 based on the expected changes in the demography of Europe.

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Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques.

H Genant, B A Blunt, Claus Glüer … (1994)

Assessment of precision errors in bone mineral densitometry is important for characterization of a technique's ability to detect longitudinal skeletal changes. Short-term and long-term precision errors should be calculated as root-mean-square (RMS) averages of standard deviations of repeated measurements (SD) and standard errors of the estimate of changes in bone density with time (SEE), respectively. Inadequate adjustment for degrees of freedom and use of arithmetic means instead of RMS averages may cause underestimation of true imprecision by up to 41% and 25% (for duplicate measurements), respectively. Calculation of confidence intervals of precision errors based on the number of repeated measurements and the number of subjects assessed serves to characterize limitations of precision error assessments. Provided that precision error are comparable across subjects, examinations with a total of 27 degrees of freedom result in an upper 90% confidence limit of +30% of the mean precision error, a level considered sufficient for characterizing technique imprecision. We recommend three (or four) repeated measurements per individual in a subject group of at least 14 individuals to characterize short-term (or long-term) precision of a technique.

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Author and article information

Contributors

Yongtao Lu:

ORCID: http://orcid.org/0000-0002-8511-6111

Role: Funding acquisitionRole: InvestigationRole: SupervisionRole: Writing – original draftRole: Writing – review & editing

Jintao He: Role: Methodology

Hanxing Zhu: Role: Writing – review & editing

Yongxuan Wang: Role: Data curationRole: Project administrationRole: Writing – review & editing

Dengshun Miao: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 10 July 2019

Publication date Collection: 2019

Volume: 14

Issue: 7

Electronic Location Identifier: e0219575

Affiliations

[1 ] Department of Engineering Mechanics, Dalian University of Technology, Dalian, China

[2 ] State Key Laboratory of Structural Analysis for Industrial Equipment, Dalian University of Technology, Dalian, China

[3 ] School of Engineering, Cardiff University, Cardiff, United Kingdom

[4 ] Affiliated Zhongshan Hospital of Dalian University, Dalian, Liaoning, China

Nanjing Medical University, CHINA

Author notes

Competing Interests: The authors have declared that no competing interests exist.

* E-mail: wangyongxuan@ 123456dlu.edu.cn

Author information

Yongtao Lu http://orcid.org/0000-0002-8511-6111

Article

Publisher ID: PONE-D-19-09038

DOI: 10.1371/journal.pone.0219575

PMC ID: 6619825

PubMed ID: 31291372

SO-VID: adc05234-fe12-4191-bd59-ca4866997521

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 30 March 2019

Date accepted : 26 June 2019

Page count

Figures: 5, Tables: 1, Pages: 15

Funding

Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 11702057

Award Recipient :

ORCID: http://orcid.org/0000-0002-8511-6111

Yongtao Lu

Dr. Yongtao Lu received the funding from the National Natural Science Foundation of China (grant number: 11702057 to Dr. Yongtao Lu) and from the Chinese Fundamental Research Funds for the Central Universities (grant number: DUT18LK19). These fundings sponsored Dr. Yongtao Lu’s research activities including study design, data analysis and preparation of the manuscript. Dr. Yongtao Lu and Dr. Hanxing Zhu jointly received the funding from the State Key Laboratory of Structural Analysis for Industrial Equipment (grant number: GZ18104). This funding sponsored Dr. Hanxing Zhu's research activities including the revision of the manuscript.

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Data Availability The datasets used in the present study are available at https://doi.org/10.6084/m9.figshare.8234144.

Effect of parathyroid hormone on the structural, densitometric and failure behaviors of mouse tibia in the spatiotemporal space

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Most cited references 31

Age-related changes in trabecular architecture differ in female and male C57BL/6J mice.

Requirements for DXA for the management of osteoporosis in Europe.

Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques.

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