Abstract
Aging, from 40 to +80 years old, causes geometrical and mechanical properties changes in the proximal femur. The subperiosteal width expands faster in men compared to women during aging, while the cortical thickness varies unequally in each sector and differently between men and women. Another change which occurs during aging is bone mechanical properties such as stiffness and ultimate strains. Numerical analysis allows us to study the potential effects of each of the age-dependent changes on the fracture forces separately and combined. We investigated the effects of the geometrical and bone mechanical properties changes due to aging on the femoral strength during a common falling scenario using a transverse isotropic continuum damage model. First, the femur model was adapted from a previously developed human body model named THUMS v4.02. Then, three sets of models were developed to address each of the changes separately and combined for both sexes. We found that the fracture forces in women are on average 1500 N less than in men of the same age. The age-dependent geometrical changes increased the fracture forces in men (25 N/decade), whereas it reduced the fracture forces by 116 N/decade in women. The mechanical properties changes reduced the fracture forces in men more than in women (354.5 N/ decade vs. 225.4 N/decade). When accounting for both geometrical and mechanical properties changes due to aging, the fracture forces decreased by 10.7% of the baseline in women per decade compared to 7.2% per decade in men.
Introduction
Adults older than 65 are at risk of a fall, and this risk increases as they get older (). During 2014, 25% of older adults in the United States experienced falling at least once (). Falls are the leading cause of accidental death and nonfatal injuries in this age group (). Nonfatal and fatal falls cost $50 billion, and falling is the costliest nonfatal injury in the US (). estimated growth in the population of older adults, which without preventive plans, could lead to a 100% increase in the number of injuries caused by a fall in the year 2030.
Falls, commonly to the sideways, cause more than 95% of all hip fractures (; ; ). Hip fractures lead to hospitalization and cause long-term consequences on mobility and independence of the patients (). Elderly women are at a higher risk of hip fracture comparing to men at a similar age (; ; ), and the fracture risk increases exponentially as men and women get older (; ).
The geometry of the bone, bone mechanical properties, and loading mode are three factors that affect the femoral strength (). The first two factors are changing with aging, and the loading mode represents an extrinsic factor. The geometrical parameters of the bone, such as the cortical thickness, cortical cross-sectional area, and cross-sectional moment of inertia, are negatively correlated with aging (). In other words, the endosteal resorption and periosteal expansion cause geometrical changes of the bone. In general, the cross-sectional area of the femoral neck is larger in men comparing to women; and these differences increase as they get older (; ). Several studies suggested that the cortical thicknesses are changing dissimilarly in each quadrant of the femoral neck (; ; ; ; ; ). A longitudinal study by suggested that the average superior cortical thickness gets thinner at a higher rate than the inferior thickness in a 5-year period for both sexes. Moreover, the thickness decreases slower in men comparing to women. Similar behavior was reported in several cross-sectional studies (; ; ; ). have reported the corresponding cortical thicknesses in 16 sectors of the femoral neck. The average superior cortical thickness decreases with aging in men and women (; ; ; ), while the average inferior cortical thickness remains constant with aging. Mechanical properties of the cortical and trabecular bone are changing with age, and these changes are site-dependent (). Unlike as observed for vertebrae, trabecular bone in the femur merely has a minor contribution to the biomechanical strength of the whole-bone compared to the cortical bone (; ). In the femoral neck, the cortical bone loses stiffness in terms of Young’s and shear modulus by 3 and 4% per decade of age, respectively. Ultimate strains decrease about 5–10% of the initial value per decade while yield properties of the bone do not change significantly with age (; ; ; ; ; ; ). Those changes, combined, cause a transition from a ductile bone to a more brittle one with age (). Trabecular bone is experiencing similar mechanical properties changes in the femoral neck where the modulus is decreasing approximately 5% per decade (; ). In contrary to the geometrical changes, mechanical properties changes of bone are sex-independent (; ; ).
Several whole-bone experiments and finite element models are designed to investigate the aging effect on the femoral strength. Age, sex, bone mineral density (BMD), loading rate, loading configuration, and individual geometrical characteristics are widely used to explain the variation of the femoral strength in test subjects (; ; ; ; ). A recent study by has concluded that the aBMD, sex, and age are sufficient parameters to clinically evaluate the femoral strength. In addition to them, they also explored the effect of loading rate and neck-shaft angle. They discovered that the inclusion of the two latter variables would not considerably improve the prediction of the femoral strength (). Several other clinical and whole-bone experiments indicate the effect of bone size and mechanical properties of the bone on the femoral strength (; ).
The majority of current computational studies on the strength of femur are focused on developing subject-specific finite element models, which are typically using isotropic mechanical properties to evaluate the femur strength (; ). While those models are capable of predicting the subject-specific femoral strength accurately, they are not developed to predict the effect of changes that occur to the bone of average men and women due to aging. There has been no work published so far to the best of authors’ knowledge, which explicitly studies the separate and combined effects of the geometrical and mechanical properties changes due to aging in each of the sexes. Moreover, many studies (; ; ; ; ; ; ; ) have shown that the yield and ultimate strains of the cortical bone are asymmetric which in turn could affect the femoral strength predictions and fracture initiation. The subject-specific models are also getting computationally expensive to the extent that it becomes impractical to implement them into whole-body models. In the current study, we aim to investigate the separate and combined effect of geometrical and mechanical properties changes on fall-induced femur fractures using a transverse isotropic continuum damage model. Simultaneously, it is intended to keep the simplicity of the model while improving the accuracy of bone modeling to allow direct application of this method in the whole-body models. We applied the geometrical and mechanical properties change for 4 decades of age, from 40 to 80 years old with the aim to evaluate the effect of each of the age-dependent changes on the femoral strength.
Materials and Methods
Three distinct sets of numerical models were developed to investigate the separated and combined effects of key changes in the geometry and mechanical properties on the strength of femur. The first set accounted only for age-dependent geometrical changes (GeomAge), the second set accounted only for age-dependent mechanical properties changes (MechAge), and the third set accounted for both changes in 4 decades of age (MechGeomAge), from 40 to 80 years old.
Baseline Model
The geometry of the baseline model for 40 years old men and women was obtained from the total human model for safety (THUMS) v4.02. It represents the 50th percentile adult man with the height and weight of 77 and 1.75 m, respectively (). Albeit, the initial model needed several modifications to represent elderly men and women. Foremost, the cortical thickness was uniform around the femoral neck in the initial model, whereas the cortical thickness naturally varies in each sector of the femoral neck (; ; ). Additionally, the subperiosteal width of the narrowest point of the neck is different among men and women (; ), which indicated the significance of developing two distinctive baseline models for men and women.
The geometry of the initial THUMS model is based on a healthy man, and the subperiosteal width is in close agreement with the reported value from the national health and nutrition examination survey (NHANES III) database (; ). On the other hand, the baseline model for women required scaling down to the representative subperiosteal width following the NHANES III (). The homogenous scaling factor for this adjustment was around 0.859. Afterward, the baseline model for men and women was adjusted for the corresponding cortical thickness in each sector of the femoral neck. The cortical thicknesses in each sector were calculated using the combination of the average cortical thicknesses for each age group from the NHANES III database (; ) and the relative thicknesses in each sector of the femoral neck from the study by . Since the average inferior cortical thicknesses in the study by was not in agreement with similar studies (see Supplementary Material), we decided to transform the reported cortical thicknesses of each sector to a relative thickness by dividing those thicknesses by the maximum reported thickness . Then, we used the average of the relative cortical thicknesses and the NHANES III average cortical thicknesses for each age group to evaluate the new maximum cortical thickness (Eq. 1):
Finally, the relative cortical thicknesses of each sector were transformed back to absolute thicknesses using the new maximum thickness (; ; Figures 1A,B).
FIGURE 1
The mechanical properties of both cortical and trabecular bones were modified. The material model of the cortical bone was altered to a transverse isotropic continuum damage model since it better can represent the cortical bone than an isotropic model (
TABLE 1
| Direction | A | B/C transverse plane | Isotropic properties | ||
|---|---|---|---|---|---|
| Loading direction | Tension | Compression | Tension | Compression | Average properties for the femoral head |
| 17.9 | 10.1 | 12.7 | |||
| 0.3 | |||||
| NA | |||||
| 0.0224 | −0.022 | 0.0072 | −0.0462 | NA | |
Mechanical properties used for the healthy 40 years old subject. See Figure 1C for material directions.
The transverse isotropic elastic model was combined with a linear damage model. Six damage parameters were applied independently to the stiffness parameters in respective directions. The damage initiates as an element reaches the yield strain in the respective direction. Subsequently, it linearly decreases the stiffness in the corresponding direction until the ultimate strain is reached. In each timestep, the damage parameters were automatically calculated using Eq. 2:whereis the positive part of: ; and are yield and ultimate strains in the respective directions. Thexstiffness parameters were set to 1% of their initial value as the strain reaches its ultimate value. It adequately secured the integrity of the mesh. Moreover, it alleviated the demand for a smoother mesh, which might increase the computational costs for the whole-body model. The update to the mechanical properties of the trabecular bone was limited to the stiffness and ultimate strain values. The material model remained isotropic elastic-plastic with continuum damage mechanics.
The geometry of the cortical bone was divided into two distinct sections. The shaft and neck region were assumed to be transverse isotropic. The principal axis of the transverse plane is respectively along the shaft and neck hollow (Figure 1C). Contrary to the shaft and neck, the femoral head typically undergoes multidirectional loading; therefore, it was assumed to have an isotropic continuum damage model with similar mechanical properties to the average value of the shaft and neck regions. The cortical bone was meshed with selectively reduced hexahedron elements, and the trabecular bone was meshed using tetrahedron elements (average dimension of elements 1.7 mm, and the total number of 32,823 nodes and 127,821 elements). A convergence study on the mesh was performed using a one-step division of the cortical bone elements, and remeshing of the trabecular bone according to the new surrounding cortical bone elements. It was found that the maximum forces differed approximately 10% and the refined model was utilized in this study.
Aging Effects
Two geometrical parameters were varied in the GeomAge set, which corresponds to the subperiosteal expansion and the endocortical resorption. Two distinct models were developed for men and women since those changes are different between sexes. First, the subperiosteal width of the baseline model was scaled to the corresponding width for each decade (
In the MechAge set, mechanical properties of the bone, such as stiffness, were changed due to aging. The Young’s and shear modulus of the cortical bone was reduced by 3 and 4% per decade of age, respectively (
The geometry from the GeomAge set was combined with the corresponding mechanical properties from the MechAge set to produce the MechGeomAge set. Since the GeomAge consisted of both sexes, the MechGeomAge could explore the potential differences between men and women as well. The MechGeomAge conveniently represented the general aging effects on the femur for both men and women.
Fall Simulations
The femur was positioned in the sideways fall experimental setup in all three sets. Initially, the femoral shaft was rotated 10° with respect to the horizontal plane, and the femoral neck was rotated internally to 15° (
FIGURE 2

The proximal section of the femur was positioned in the sideways fall configuration. The rigid fixture was connected to external nodes of the distal femur that could rotate in the sagittal plane. The displacement was applied to the femoral head.
Results
The geometrical changes due to aging in the femoral neck affect the fracture forces differently for men and women (Figure 3). Combination of subperiosteal expansion and endocortical resorption caused a slight increase in fracture forces in men, whereas it caused a decrease in women (Figure 3). The fracture forces increased by 25 N per decade, 0.5% of the baseline, for men, while it decreased by 116 N per decade, 3% of the baseline, for women.
FIGURE 3

The fracture forces in GeomAge set slightly increased (25 N per decade) for men, and it reduced by 116 N per decade for women.
The changes in mechanical properties due to aging progressively reduced the fracture forces in both men and women (Figure 4). However, the fracture forces reduced differently in men compared to women. While the fracture force decreased 354.5 N per decade, 7% of the baseline, for men, it decreased 225.4 N, 5.7% of the baseline, for Women. It is noteworthy that the geometry was kept intact for various ages in the MechAge set.
FIGURE 4

The fracture forces in the MechAge set reduced by 354.5 N per decade for men and 225.4 N per decade for women.
Similar to the MechAge, the fracture forces decreased with aging for both men and women in the MechGeomAge set (Figure 5). In general, women had a lower fracture force comparing to men of a similar age, whereas both men and women experienced a similar trend in the age-dependent fracture forces. The fracture forces decreased by 373.3 N per decade, 7.2% of the baseline, and 368.1 N per decade, 10.7% of the baseline, for men and women, respectively.
FIGURE 5

The combined changes (MechGeomAge set) reduced the fracture forces in both men and women. The fracture forces reduced by 373.3 N per decade for men and 368.1 N per decade for women.
Force-displacement curves from the simulations of the MechGeomAge set were compared to the experimental results (
FIGURE 6

(A) Comparison of experimental force-displacement curves of a similar test setup with simulation results of MechGeomAge set (
FIGURE 7

Initial fracture pattern results from the instance that the force-displacement curve reached the global maximum in the (A) 40 years old and (B) 80 years old men, (C) 40 years old, and (D) 80 years old women simulation. The initial pattern slightly changed due to aging in men and women.
Discussions
Aging causes two major changes in the femoral neck, geometrical and mechanical properties. Numerical simulations made it possible to split the effect of the geometrical and mechanical properties due to aging. In this study, we conducted a distinct series of simulations to investigate the potential effect of each of those changes separately and combined. In order to account for the asymmetry of the yield and ultimate strains as well as Young’s and shear modulus, we implemented a transverse isotropic continuum damage model for the cortical bone. Overall, the fracture forces decreased with aging when accounting for both geometrical and mechanical properties changes in men and women. Likewise, the fracture forces reduced with aging in men and women when accounting for only the mechanical properties changes. However, the geometrical changes caused a diverging effect on the fracture forces in each of the sexes with a slight increase in men and a decrease in women with aging.
The geometrical changes in the femoral neck consist of the changes in cortical thickness, cortical cross-sectional area, and moment of inertia.
Despite the geometrical changes, the variations in the mechanical properties of the cortical and trabecular bone due to aging affect men and women in an analogous way (
Accounting for both mechanical and geometrical changes due to aging, the fracture forces reduced for both men and women. Women experienced a lower fracture force (average of all age groups: 3359 N) and a higher reduction rate (10.7% of the baseline) compared to men (4909 N, 7.2%). This finding is consistent with previous research, which found a smaller fracture force for women compared to men in general (
In the current study, THUMS v4.02 was used to acquire the geometry of the femur. In the baseline model, we aimed to modify the primary model to address the shortcomings of the current model. Afterward, we investigated the potential effects of the major aging changes of the geometry and mechanical properties on the fracture forces of the femur. Meanwhile, the findings of the current study are subject to several limitations. First, the model was simplified at the structural and material properties level, although several previous studies were focused on sophisticated CT image-based modeling of the femur. At the structural level, the accuracy of the cortical thickness estimation could be improved using a recently developed cortical bone mapping (CBM) technique (
Conclusion
Aging changes the geometry of the femoral neck, and it affects the mechanical properties of the bone. In the current study, those changes were explored separately and combined to demonstrate the possible effect of both changes in altering the femoral strength during aging. The results of the current study suggest that the fracture forces reduced in both men and women when accounting for both mechanical and geometrical changes due to aging. The geometrical changes due to aging counteracted some of the adverse effects of the mechanical changes in men, whereas it adversely affected the fracture forces in women.
Statements
Data availability statement
The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.
Author contributions
PS and SK designed the study. PS performed and analyzed the finite element simulations, wrote the original draft. SK performed supervision, funding acquisition, writing review, and editing. All authors critically reviewed and revised the manuscript.
Funding
This study was supported by a grant from “BVFF—Bana väg för framtiden” (BVFF number 2016-025) and the Center for Biomechanical Modeling and Experimentation (BioMEx) at KTH—Royal Institute of Technology.
Acknowledgments
The computations were enabled by resources provided by the Swedish National Infrastructure for Computing (SNIC) at the center for High-Performance Computing (PDC).
Conflict of interest
SK has a financial interest in a company aiming to produce safety flooring (Igelkott Golv AB), and both he and the company may benefit from the results of this research.
The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fmech.2021.691171/full#supplementary-material
Abbreviations
THUMS, total human model for safety; BMD, bone mineral density; GeomAge, simulation set for the geometrical changes due to aging; MechAge, simulation set for the mechanical properties changes due to aging; MechGeomAge, simulation set for the geometrical and mechanical properties changes; NHANES III, National Health and Nutrition Examination Survey; , yield strains; , ultimate strains; , cortical thicknesses of each sector; , maximum reported thickness in
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Summary
Keywords
hip fracture, sideways fall, transverse isotropic continuum damage model, aging, elderly, femoral strength
Citation
Sahandifar P and Kleiven S (2021) Separate and Combined Effects of Geometrical and Mechanical Properties Changes Due to Aging on the Femoral Strength in Men and Women. Front. Mech. Eng 7:691171. doi: 10.3389/fmech.2021.691171
Received
05 April 2021
Accepted
10 May 2021
Published
24 May 2021
Volume
7 - 2021
Edited by
Omid Bavi, Shiraz University of Technology, Iran
Reviewed by
Cristina Falcinelli, Campus Bio-Medico University, Italy
Ali Alijani, Islamic Azad University of Anzali, Iran
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© 2021 Sahandifar and Kleiven.
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*Correspondence: Pooya Sahandifar, pooysaha@kth.se
This article was submitted to Biomechanical Engineering, a section of the journal Frontiers in Mechanical Engineering
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