Research Papers

The In Situ Mechanics of Trabecular Bone Marrow: The Potential for Mechanobiological Response

[+] Author and Article Information
Thomas A. Metzger, Tyler C. Kreipke

Department of Aerospace
and Mechanical Engineering
and Bioengineering Graduate Program,
Tissue Mechanics Laboratory,
University of Notre Dame,
Notre Dame, IN 46556

Ted J. Vaughan, Laoise M. McNamara

Department of Biomedical Engineering,
National University of Ireland,
Galway, Ireland

Glen L. Niebur

Department of Aerospace
and Mechanical Engineering
and Bioengineering Graduate Program,
Tissue Mechanics Laboratory,
University of Notre Dame,
Notre Dame, IN 46556
e-mail: gniebur@nd.edu

1Corresponding author.

Manuscript received June 26, 2014; final manuscript received October 30, 2014; accepted manuscript posted November 5, 2014; published online December 10, 2014. Assoc. Editor: Blaine Christiansen.

J Biomech Eng 137(1), 011006 (Jan 01, 2015) Paper No: BIO-14-1295; doi: 10.1115/1.4028985 History: Received June 26, 2014; Revised October 30, 2014; Accepted November 05, 2014; Online December 10, 2014

Bone adapts to habitual loading through mechanobiological signaling. Osteocytes are the primary mechanical sensors in bone, upregulating osteogenic factors and downregulating osteoinhibitors, and recruiting osteoclasts to resorb bone in response to microdamage accumulation. However, most of the cell populations of the bone marrow niche, which are intimately involved with bone remodeling as the source of bone osteoblast and osteoclast progenitors, are also mechanosensitive. We hypothesized that the deformation of trabecular bone would impart mechanical stress within the entrapped bone marrow consistent with mechanostimulation of the constituent cells. Detailed fluid-structure interaction models of porcine femoral trabecular bone and bone marrow were created using tetrahedral finite element meshes. The marrow was allowed to flow freely within the bone pores, while the bone was compressed to 2000 or 3000 microstrain at the apparent level. Marrow properties were parametrically varied from a constant 400 mPa·s to a power-law rule exceeding 85 Pa·s. Deformation generated almost no shear stress or pressure in the marrow for the low viscosity fluid, but exceeded 5 Pa when the higher viscosity models were used. The shear stress was higher when the strain rate increased and in higher volume fraction bone. The results demonstrate that cells within the trabecular bone marrow could be mechanically stimulated by bone deformation, depending on deformation rate, bone porosity, and bone marrow properties. Since the marrow contains many mechanosensitive cells, changes in the stimulatory levels may explain the alterations in bone marrow morphology with aging and disease, which may in turn affect the trabecular bone mechanobiology and adaptation.

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Grahic Jump Location
Fig. 1

(a) Hematoxylin and eosin staining of freshly harvested trabecular bone marrow from a porcine vertebra. Matrix is stained light, and nuclei are dark spots. The marrow consists predominantly of cells (B = bone tissue). (b) Bone marrow is located within the pore space of trabecular bone, where it is subject to mechanical stress during bone deformation.

Grahic Jump Location
Fig. 2

(a) Conforming finite element meshes of a trabecular bone sample with bone marrow. (b) Displacement boundary conditions were applied to the superior surface of the trabecular bone. Confined compression conditions were applied to the bottom and sides. (c) The bone marrow had a zero pressure boundary condition at the bottom surface while the pressure and velocity were unconstrained on all other free surfaces. The interface between bone and marrow had no slip boundary conditions.

Grahic Jump Location
Fig. 3

The deformation of the bone induced shear stress within the marrow (a). A pressure gradient developed during loading due to the differential displacements of the bone and marrow (b), which resulted in fluid velocity on the order of 10 μm/s (c). The results displayed are at 0.1 s, using the power-law viscosity model.

Grahic Jump Location
Fig. 4

The mean shear stress (a) and pressure gradient (b) were calculated by volume averaging over the nodal finite element results at selected time points. An initial transient increase in both outputs was followed by a decrease as the bone deformation reached its maximum, and then increased as the bone reached its maximum strain rate. Only the compressive portion of the load cycle is displayed here.

Grahic Jump Location
Fig. 5

The spatial distribution of the marrow shear stress for the 1 Hz simulation to 3000 μ-strain at 0.5 s (maximum velocity). Marrow shear stress was highest at the bone–marrow interface, with stress dissipating toward the middle of the pores. Shear stress was below mechanostimulatory levels when the viscosity was assume to be 0.4 Pa·s (a). Shear stress increased when marrow was modeled at 85 Pa·s (b) and as a power-law material (c). However, the spatial distribution of shear stress and the velocity gradients were similar for all cases, indicating that viscous forces dominate the solution.

Grahic Jump Location
Fig. 6

The mean shear stress (a) and pressure gradient magnitude (b) were proportional to the maximum strain rate for all three marrow constitutive models

Grahic Jump Location
Fig. 7

The pressure gradient (a), velocity gradient magnitude (b), and shear stress (c) calculated for the power law viscosity model increased proportionally with strain rate

Grahic Jump Location
Fig. 8

Distributions of shear stress in the two specimens at the peak shear rate demonstrate that increased trabecular bone density (BV/TV) increases the shear stress in the marrow, and subjects a larger fraction of the marrow to higher shear stress



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