Table 2 Summary of study characteristics, specimen demographic details, and main findings or summaries
From: The role of bone marrow on the mechanical properties of trabecular bone: a systematic review
Experimental methods | Authors, year of publication | Journal of publication | Types of specimens | Numbers of specimens | Gender | Age | Anatomic sites | Main findings or summaries |
|---|---|---|---|---|---|---|---|---|
FEM under compressive loading | Kasra et al. 1998 | Journal of Biomechanical Engineering | A 3D-FEM of a rod-strut trabecular structure filled with bone marrow | – | – | – | Vertebrae trabecular bone | Hydraulic stiffening of trabecular bone due to the presence of bone marrow occurs when the applied loading rate is higher than the pore fluid diffusion rate |
Dynamic compressive strain cycles | Ochoa et al. 1991 | Journal of Biomechanical Engineering | Intact bone samples | 26 limbs | – | About 2 years | Femoral heads (mature dogs) | A nature stiffening mechanism of viscous fluid may be present in intact trabecular bone, and the overall stiffness reflects the material properties of both the porous solid matrix and entrapped fluid |
Static and dynamic tests | Swanson et al. 1966 | Medical & biological engineering & computing | Intact bone samples | 4 | – | – | Femora | Trabecular bone is not hydraulically strengthened by the presence of bone marrow under moderate and physiological loading conditions such as normal walking |
Small amplitude mechanical excitation | Pugh et al. 1973 | Journal of Biomechanics | Bone slabs | 20 | – | – | Distal ends of the human left femora | The fluid in the intertrabecular spaces has no effect on the dynamic mechanical behavior |
Stress-relaxation and cyclic loading | Metzger, Schwaner, et al. 2015 | Journal of Biomechanics | Intact bone samples | 9 | – | 6–8 months | Porcine femurs | The deformation of the pores under external forces would induce the motion of the fluid-like marrow, resulting in pressure and velocity gradients |
Compressive loads tests | Kazarian et al. 1977 | Spine | Intact bone samples | 48 | Male | 26, 27, 32 and 38 years | Thoracic vertebrae | The mechanical behavior of the vertebral centrum was dependent on the strain rate. This was due to the hydraulic strengthening caused by the internal marrow at the higher strain rates |
Split-Hopkinson bar testing and FEM | Pilcher, et al. 2010 | Journal of Biomechanical Engineering | Cylindrical and cubic trabecular bone samples | 34 | – | – | Bovine tibia (proximal region) | The strength of trabecular bone significantly increases when testing at high strain rates in the range of 102–103 s−1 |
FEM under compressive loading | Rabiatul, et al. 2022 | Journal of Materials: Design And Applications | A 3D-constructed FEM | – | – | – | Bovine femur bones | The fluid flow of bone marrow not only causes shear stress to the trabecular structure, but also has a certain hydraulic stiffening effect that occurs due to the presence of bone marrow |
Porous elastic model | Hong et al. 2001 | KSME International Journal | A cylindrical trabecular bone sample | 1 | – | – | Calf vertebral trabecular bone | The difference in pore pressure generation resulted in a significant increase in the predicted total stress at the fastest strain rate (10 per second) |
A one-dimensional poro-elastic model | Hong et al. 1998 | KSME International Journal | Trabecular bone | – | – | – | – | The total stress–strain behavior of trabecular bone was greatly affected by the applied strain rate. The incorporation of the fluid effect is recommended |
FEM under compressive loading | Pense et al. 2017 | Journal of the Mechanical Behavior Of Biomedical Materials | Cubic bone samples | 7 | Female | 61 years | Human femoral neck | There is a significant strain rate-dependent poro-elastic hydraulic stiffening of bone tissue due to the fluid in trabecular bone pores |
FEM under a realistic impact load | Haider et al. 2013 | Journal of Biomechanics | Intact bone samples | 1 | – | – | Cadaveric femur | Hydraulic strengthening has little effect on whole bones in realistic fall conditions, as this load condition causes no volumetric strain |
FEM under stress relaxation experiments | Sandino et al. 2015 | Journal of the Mechanical Behavior Of Biomedical Materials | Cubes of trabecular bone (10 mm side-length) | 33 | – | 64.35 (49–85) | Human distal tibia | The contribution of viscoelasticity (fluid flow-independent mechanism) to the mechanical response of the tissue is significantly greater than the contribution of the poro-elasticity (fluid flow-dependent mechanism) |
FEM and in vitro permeability experiments | Sandino et al. 2014 | Journal of Biomechanics | Cubes of trabecular bone (10 mm side-length) | 23 | – | – | Human distal tibia | The changes in the trabecular bone microarchitecture have an exponential relationship with permeability |
FEM for mechanical stimuli of trabecular bone | Sandino et al. 2017 | Journal of the Mechanical Behavior Of Biomedical Materials | Cubes of trabecular bone (10 mm side-length) | 76 | 14 females, 6 males | 68 ± 15 (49–95) years | Human distal tibia | With variations in the morphology of the trabecular bone, such as an increase of 30% porosity, there is a significant decrease in the mechanical stimuli of the tissue when subjected to constant strain |
A one-dimensional poro-elastic model of trabecular bone | Lim et al. 1998 | Journal of Musculoskeletal Research | – | – | – | – | – | Trabecular bone is poro-elastic and the fluid effect on the mechanical behavior at the continuum level is significant |
Sinusoidal strain excitation | Ochoa et al. 1997 | Journal of Biomechanical Engineering | Intact bone samples | 38 | – | About 2 years | Femoral heads (mature dogs) | Hydraulic effects measured in vivo accounted for an average of 19 percent of the load-bearing capabilities of the structure over the frequency range considered |
A fluid structure interaction model | Birmingham et al. 2013 | Annals of Biomechanical Engineering | – | – | – | – | – | Lower bone mass leads to an increase in the shear stress generated within the marrow, while a decrease in bone marrow viscosity reduces this generated shear stress |
Fluid–structure interaction models (FEM under compressive loading) | Metzger, Kreipke, et al. 2015 | Journal of Biomechanical Engineering | Cubes of trabecular bone (4 mm side-length) | 2 | – | – | Proximal and distal femoral neck | Compression of the bone caused a flow of the marrow within the trabecular pore space. The marrow moved slowly, with velocities lower than 0.1 mm/s, which was accompanied by concomitant shear stress and pressure gradient |
Non-destructive impact loads | Bryant 1983 | Journal of Biomechanics | Intact bone samples | – | – | – | Sheep tibiae | In non-destructive impact loading, low marrow pressures would provide only a trivial amount of hydraulic strengthening |
Dynamic loading cycles | Ochoa et al. 1991 | The Journal Of Rheumatology | Intact bone samples | 24 | – | At least 2 years | Hind limbs of dogs | The removal of fluid phase decreases the stiffness of trabecular bone in intact canine femoral head specimens (a more than 30% decrease in stiffness) |
A load of physiologic magnitude | Nuccion et al. 2001 | Orthopedics | Intact bone samples | 24 | – | – | Femora of mature dogs | Removal of the intraosseous fluid decrease the mechanical stiffness of canine trabecular bone (a 40% decrease in stiffness) |
Hydrostatic pressure response | Simkin 1985 | Journal of Biomechanics | Intact bone samples | 20 | 4 female, 6 male | – | Arms and shoulders of dogs | When the trabecular bone deforms under unconstrained load, fluid will flow freely and will play no mechanical role as surrounding trabeculae are compressed. while enclosed fluid will directly transmit a portion of the loading rate |
Hydraulic resistance testing | Ochia et al. 2006 | Spine | Intact bone samples | 21 | – | 67.4 ± 12.0 years, 73.3 ± 8.8 years | Human lumbar vertebrae (L3 and L4) | Marrow flow can be biphasic in nature at flow rates, and that marrow flow could potentially damage trabeculae and weaken the vertebral body during high-speed injury events |
Compression testing | Deligianni et al.1994 | Biorheology | Cylindrical and cubic specimens | 22 | 10 females | 55–70 years | Femoral heads | Under a step load and at strain rate, 10 min−1, the marrow can bear about 25% of the applied load |
Solid and fluid constitutive models | Metzger et al. 2016 | Journal of Biomechanics | Cubes (3 mm side-length) | 2 | – | – | Human femurs | The results differed substantially between elastic, hyperelastic, and viscoelastic constitutive models, even when using the same modulus |
Unconfined compression test and FEM simulation | Halgrin et al. 2012 | Journal of the Mechanical Behavior Of Biomedical Materials | Cubic trabecular bone samples | 48 | – | Less than 24 months | Bovine ribs | The bone marrow contributes to decrease the mechanical properties of trabecular bone, i.e., 26% for the elastic modulus, 38% for the maximum compressive stress, and 33% for the average stress |
Unconfined compression test | Bravo et al. 2019 | Biomedical Physics & Engineering Express | Cubic trabecular bone samples | 60 | – | About 5 months of age | Porcine femur bones | The samples extracted marrow and replaced with saline solution have higher mechanical properties |
Unconfined compression test | Linde et al. 1993 | Journal of Biomechanics | Cylindrical trabecular bone samples | 74 | Male | 35 and 61 years | Human proximal tibial | Defatted trabecular bone specimens contribute to a 30% increase in stiffness and a 50% decrease in viscoelastic dissipation |
Compression test and FEM | Chaari et al. 2007 | International Journal Of Crashworthiness | Cylindrical trabecular bone samples | 97 | – | – | Beef ribs | The fluid influence is essentially observed in the last compression stage, when the sample’s strain is higher than 30% |
Semi-constrained compression test | Carter et al. 1977 | The Journal Of Bone And Joint Surgery | Cylindrical trabecular bone samples | 124 | – | – | Human tibial plateaus and bovine femoral condyles | The presence of marrow increased the strength, modulus, and energy absorption of specimens only at the highest strain rate of 10.0 per second |
Dynamic compressive loading (FEM simulation) | Laouira et al. 2015 | Computer Methods In Biomechanics And Biomedical Engineering | Cubic trabecular bone samples | 1 | – | – | Porcine femoral neck | Confined marrow plays a non-negligible role upon the mechanical properties of trabecular bone |
Static and dynamic load | Bryant 1988 | Journal of Engineering In Medicine | Human and sheep long bones | 2 | Male for human bones | 50 years for human bones | Sheep tibia and human radius | Hydraulic strengthening and viscous resistance by the marrow can be negligible when there is little or no volume change, as well as no significant movement between the marrow and the adjacent trabecular bone |
FEM under compressive loading | Chen et al. 2015 | Annual International Conference Of The IEEE Engineering In Medicine And Biology Society | FEM of trabecular bone | 4 | Female | Post-menopausal | Human L3 lumbar spine | Trabecular models filled with marrow fat have less maximum stress (3–9%) and larger average stress in volume (9–56%) than that of models with only trabeculae |
FEM under compressive loading | Ma et al. 2014 | Annual International Conference of the IEEE Engineering In Medicine And Biology Society | FEM of trabecular bone | 1 | Female | 63 years | Human L3 lumbar spine | The trabecular bone with marrow fat suffered larger apparent stress and compressive stress than the model with merely trabecular bone for unconfined compressive tests, i.e., 18.81% for the maximum compressive stress, 10.25% for the average stress |
Creep test | Simon et al. 1985 | Spine | FEM of trabecular bone | – | – | – | Rhesus monkey L2/L3 lumbar spine | The fluid phase included in the FEMs plays a significant role in the mechanical response of spinal motion segments |
Shear test | Mitton et al. 1997 | Medical Engineering & Physics | Cylindrical trabecular bone samples | 43 | Female | 9 years (5.6–10.3 years) | Ewe vertebral trabecular bone (L1–L5) | The shear test performed in a bath at 37 ℃ reduced the strength from 32.5 to 37.3% compared with the test in “standard” test conditions. Friction was regarded as a non-negligible factor |
Shear properties under torsional loading | Kasra et al. 2007 | Journal of Biomechanics | Cylindrical trabecular bone samples | 52 | Female | 6 months and 2 years | Merino sheep lumbar segments (L2–L3) | The presence of bone marrow did not affect trabecular bone shear strength and modulus |