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Research Papers

Reproduction Differentially Affects Trabecular Bone Depending on Its Mechanical Versus Metabolic Role

[+] Author and Article Information
Chantal M. J. de Bakker

McKay Orthopaedic Research Laboratory,
Department of Orthopaedic Surgery,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: chantald@seas.upenn.edu

Wei-Ju Tseng

McKay Orthopaedic Research Laboratory,
Department of Orthopaedic Surgery,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: weits@pennmedicine.upenn.edu

Yihan Li

McKay Orthopaedic Research Laboratory,
Department of Orthopaedic Surgery,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: yihanl@seas.upenn.edu

Hongbo Zhao

McKay Orthopaedic Research Laboratory,
Department of Orthopaedic Surgery,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104;
Key Laboratory of Biorheological Science and
Technology,
Ministry of Education and Bioengineering
College,
Chongqing University,
Chongqing 400044, China
e-mail: zhhongbo@pennmedicine.upenn.edu

Allison R. Altman-Singles

McKay Orthopaedic Research Laboratory,
Department of Orthopaedic Surgery,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104;
Department of Kinesiology,
Pennsylvania State University,
Berks Campus,
Reading, PA 19610
e-mail: ara5093@psu.edu

Yonghoon Jeong

Division of Orthodontics,
College of Dentistry,
The Ohio State University,
Columbus, OH 43210
e-mail: yonghoonj@yahoo.com

Juhanna Robberts

McKay Orthopaedic Research Laboratory,
Department of Orthopaedic Surgery,
Perelman School of Medicine,
University of Pennsylvania,
Philadelphia, PA 19104
e-mail: robberts@seas.upenn.edu

Lin Han

School of Biomedical Engineering,
Science, and Health Systems,
Drexel University,
Philadelphia, PA 19104
e-mail: lh535@drexel.edu

Do-Gyoon Kim

Division of Orthodontics,
College of Dentistry,
The Ohio State University,
Columbus, OH 43210
e-mail: kim.2508@osu.edu

X. Sherry Liu

McKay Orthopaedic Research Laboratory,
Perelman School of Medicine,
Department of Orthopaedic Surgery,
University of Pennsylvania,
426C Stemmler Hall,
36th Street and Hamilton Walk Philadelphia,
Philadelphia, PA 19104
e-mail: xiaoweil@pennmedicine.upenn.edu

1Corresponding author.

Manuscript received May 18, 2017; final manuscript received September 15, 2017; published online October 13, 2017. Assoc. Editor: Kyle Allen.

J Biomech Eng 139(11), 111006 (Oct 13, 2017) (10 pages) Paper No: BIO-17-1221; doi: 10.1115/1.4038110 History: Received May 18, 2017; Revised September 15, 2017

During pregnancy and lactation, the maternal skeleton provides calcium for fetal/infant growth, resulting in substantial bone loss, which partially recovers after weaning. However, the amount of bone that is lost and the extent of post-weaning recovery are highly variable among different skeletal sites, and, despite persistent alterations in bone structure at some locations, reproductive history does not increase postmenopausal fracture risk. To explain this phenomenon, we hypothesized that the degree of reproductive bone loss/recovery at trabecular sites may vary depending on the extent to which the trabecular compartment is involved in the bone’s load-bearing function. Using a rat model, we quantified the proportion of the load carried by the trabeculae, as well as the extent of reproductive bone loss and recovery, at two distinct skeletal sites: the tibia and lumbar vertebra. Both sites underwent significant bone loss during pregnancy and lactation, which was partially recovered post-weaning. However, the extent of the deterioration and the resumption of trabecular load-bearing capacity after weaning varied substantially. Tibial trabecular bone, which bore a low proportion of the total applied load, underwent dramatic and irreversible microstructural deterioration during reproduction. Meanwhile, vertebral trabecular bone bore a greater fraction of the load, underwent minimal deterioration in microarchitecture, and resumed its full load-bearing capacity after weaning. Because pregnancy and lactation are physiological processes, the distinctive responses to these natural events among different skeletal sites may help to elucidate the extent of the trabecular bone’s structural versus metabolic functions.

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Copyright © 2017 by ASME
Topics: Bone , Stress
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Figures

Grahic Jump Location
Fig. 1

(a) Representative three-dimensional renderings of trabecular microstructure at the proximal tibia and the L4 vertebra in virgin, pregnancy, lactation, and 6-week post-weaning rats. (b)–(g) Microstructural parameters at the tibia and L4 at each reproductive stage, including: (b) BV/TV, (c) Tb.N, (d) Tb.Th, (e) Tb.Sp, (f) SMI, and (g) Conn.D. * indicate significant differences among groups (p < 0.05), # indicate trends toward differences among groups (p < 0.1).

Grahic Jump Location
Fig. 2

Trabecular bone remodeling in virgin, pregnancy, lactation, and 2-week post-weaning rats. (a) Representative calcein-labeled histology slides used to evaluate bone formation. (b) Representative trichrome-stained slides. Triangles indicate osteoblast locations; asterisks indicate osteoclast locations. Close-up images of osteoblasts (in virgin and post-weaning groups) and osteoclasts (in pregnancy and lactation groups) are shown in the bottom left-corner of each slide. (c)–(e) Bone formation parameters during each reproductive phase, including (c) BFR/BS, (d) MS/BS, and (e) MAR, as quantified through fluorescent-labeled dynamic histomorphometry. (f) Serum TRAP. (g)–(j) Static histomorphometry-based cell numbers and surfaces, including (g) Ob.N/BS, (h) Ob.S/BS, (i) Oc.N/BS, and (e) Oc.S/BS. * indicate significant differences among groups (p < 0.05), # indicate trends toward differences among groups (p < 0.1).

Grahic Jump Location
Fig. 3

Finite element analysis (FEA). (a) Schematic illustrating the isolation of trabecular (gray) and cortical (black) compartments at L4 (left) and the tibia (right) for calculation of load-share fraction. (b) Whole-bone stiffness and (c) trabecular load-share fraction in virgin, pregnancy, lactation, and 6-week post-weaning groups. * indicate significant differences among groups (p < 0.05).

Grahic Jump Location
Fig. 4

Lumbar vertebra mechanics in virgin, lactation, and 6-week post-weaning rats. (a)–(c) Extrinsic properties of the vertebra measured through compression testing of L2: (a) peak load, (b) stiffness, (c) energy to failure. (d)–(f) Apparent-level properties derived through normalization of L2 compression results for bone size: (d) ultimate stress, (e) elastic modulus, (f) toughness. (g)–(h) Nanoindentation of L1: (g) schematic illustrating the locations where nanoindentation was performed to assess material properties of the surface and center regions of the trabeculae, (h) nanoindentation-based Young’s modulus at the center and surface regions. * indicate significant differences among groups (p < 0.05).

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