Journal of Biomechanical Engineering.

Received July 03, 2018;

Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

STUDIES ON THE STRESS-STRAIN RELATIONSHIP IN

BOVINE CORTICAL BONE BASED ON RAMBERG-OSGOOD EQUATION

N.K. Sharma*

Department of Mechanical Engineering, University of Saskatchewan, Saskatoon, S7N5A9, Canada

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enksharma@yahoo.com

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MD. Sarker

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Division of Biomedical Engineering, University of Saskatchewan, Saskatoon, S7N5A9, Canada

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mas921@mail.usask.ca

Saman Naghieh

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Division of Biomedical Engineering, University of Saskatchewan, Saskatoon, S7N5A9, Canada
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san908@mail.usask.ca
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X.B. Chen
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Department of Mechanical Engineering and Division of Biomedical Engineering, University of Saskatchewan,

Saskatoon, S7N5A9, Canada
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xbc719@mail.usask.ca
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Abstract

Bone is a complex material that exhibits an amount of plasticity before bone fracture takes place, where the non-linear
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relationship between stress and strain is of importance to understand ing the mechanism behind the fracture. This brief
presents our study on the examination of the stress-strain relationship of bovine femoral cortical bone and the
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relationship representation by employing the Ramberg-Osgood (R-O) equation. Samples were taken and prepared
from different locations (upper, middle and lower) of bone diaphysis and were then subjected to the uniaxial tensile
tests under longitudinal and transverse loading conditions, respectively. The stress-strain curves obtained from tests
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were analyzed via linear regression analysis based on the R-O equation. Our results illustrated that the R-O equation
is appropriate to describe the non-linear stress-strain behavior of cortical bone, while the values of equation parameters
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vary with the sample locations (upper, middle and lower) and loading conditions (longitudinal and transverse).

Keywords: Cortical bone; Ramberg-Osgood equation; J-toughness; Strain hardening exponent; Plastic Modulus.

*corresponding author

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

Introduction

Knowing the mechanical properties of bone is fundamental to discovering the bone structure-function relationship [1]
and to repairing damaged bone [2–4] with tissue scaffolds used widely in tissue engineering applications [5–13]. Bone
is considered a highly heterogeneous and anisotropic material with a hierarchical structure that varies from nano-scale
to macro-scale [1,14]. The composite-like structure of bone exhibits complex mechanical properties [15–18],
including toughening mechanisms where bone experiences a significant amount of plastic deformation prior to its
fracture [19–22]. In the presence of extensive plastic deformation, the elastic-plastic fracture mechanics approach is

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of an effective means to assess the fracture toughness in terms of J-integral [23,24], where the key is to represent the

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non-linear relationship between stress and strain. For this, the Ramberg-Osgood (R-O) equation [25] has been shown
promising as described in the literature [26], where Ritchie et al. outlined the experimental procedures of measuring
the toughness of bone for small animal studies. Meanwhile, it is noticed the non-linear stress-strain relationship of

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cortical bone has not been well documented in the literature. Furthermore, this relationship may be affected by factors
such as the location and orientation of samples taken from donor bone. As inspired, the present work aimed to examin e

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the stress-strain relationship of the bovine femoral cortical bone and its modeling by employing t he R-O equation,
where the equation parameters were estimated for the samples taken from different locations of bone under

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longitudinal and transverse loading orientations. The R-O equation with estimated parameters would be useful for
future studies to evaluate the J-toughness values of cortical bone at different anatomic locations of the bone diaphysis
and loading orientations.

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Materials and Methods tN
In this study, the femoral bones were obtained from a young bovine of about 36 months. Upon the removal from the
body, the bones were wrapped in gauze and soaked in normal saline, and then covered with plastic wrap and placed
in sealed and airtight plastic bags. These plastic bags with bones were stored in a freezer at -20°C within 1 hr after the
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bones had been harvested. The bones were kept hydrated in saline upon removal from the freezer and during all stages
of tissue preparation. For the specimen preparation, the epiphyses ends of the long bone were removed by using a
vertical band saw, leaving only the diaphysis section. The round cylindrical edges of the diaphysis were flattened into
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flat rectangular prismatic edges with the help of a belt sander. After flattening, the whole diaphysis of the cortical
bone was sectioned into three equal segments , i.e., the upper, middle and lower parts of the bone diaphysis. In all, 30
specimens of dumbbell shape strip were prepared from three locations (upper, middle and lower) of the bone diaphysis
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for the uniaxial tensile tests. These specimens were extracted from four anatomic locations of the bone circumference.
The schematic representation of specimen preparation is shown in Fig. 1 along with the orientations of specimen
prepared. Of the 30 specimens, 15 specimens were prepared for the tensile tests with loading in longitudinal direction
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(i.e., the loading was applied along the long axis of femur) with a gauge length 25 mm, gauge width 4 mm and total
length 80 mm; and the other 15 specimens were prepared for the transverse tensile tests (i.e., the loading was applied
perpendicular to the long axis of femur) with a gauge length 8 mm, gauge width 4 mm and total length 22 mm. All
specimens were stored at room temperature in a solution of 50% saline and 50% ethanol at all time until testing. The
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division of tensile specimens from each part (i.e., upper, middle and lower) of the bone diaphysis according to the
anatomic quadrants locations is given in Table 1. One specimen was prepared from the lateral, anterior and posterior
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locations, respectively; while two specimens were extracted from the medial location. The number of specimens fro m
each anatomic quadrant was one or two according to the materials and specimens prepared for the present study.
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Ac

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

Long axis of bone (1)

Circumferential
Radial direction (3) direction (2)

Upper diaphysis h/3 Anterior

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ite
h
Middle diaphysis h/3 Medial
Lateral

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Posterior

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Lower diaphysis h/3
Division of anatomic quadrants
(c)

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(b) Bone diaphysis
(a) Bovine femur bone

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Longitudinal specimen oriented
Transverse specimen oriented along the
along the long axis of bone
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circumferential direction of bone
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Orientation of tensile specimens

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(d)
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Fig. 1 Schematic diagram of (a) bovine femur bone, (b) bone diaphysis obtained after removing the epiphyses ends of
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the femur and further division of diaphysis into three parts namely upper, middle and lower diaphysis , (c) four
locations of anatomic quadrants, and (d) orientation of longitudinal and transverse specimens prepared for tensile tests.

Table 1: Number of longitudinal and transverse tensile specimens taken from the four anatomic quadrants
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Orientation of Number of specimens taken from the

tensile specimen anatomic quadrant of bone
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Lateral Medial Anterior Posterior

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Longitudinal 1 2 1 1
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Transverse 1 2 1 1

The uniaxial longitudinal tensile test was performed on a Zwick 7250 Universal Testing Machine. An extensometer
with a gauge length of 25 mm was used to measure displacement in the gauge region and the load was measured by a
5 kN load cell. The uniaxial transverse tensile test was performed on a MTS 858 Table Top Machine. A miniature
extensometer of a gauge length of 5 mm was used to measure the strain values. The tensile tests were performed at a

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

displacement rate of 1.8 mm/min; and the results from the tensile tests were characterized in term of the relationship
between the engineering/true stress and strain as per our previous study [27]. The values of yield stress were evaluated
at a strain of 0.2%.

The R-O equation for the plastic strain is given in Equation (1), where n is the strain hardening exponent and F is the
plastic modulus with a value associated with the elastic modulus. Taking the logarithm of Equation (1) yields Equation
(2). This logarithmic equation is of a straight line with a slope of n and an intercept of –log (F).

𝜎𝑛
𝜀𝑝 = (1)

d
𝐹

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𝑙𝑜𝑔𝜀𝑝 = 𝑛 𝑙𝑜𝑔𝜎 − log 𝐹 (2)

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For both elastic and plastic strains, the R-O equation is written by [25,28]

𝜀 𝜎 𝜎 𝑛
= +𝛼[ ] (3)

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𝜀0 𝜎𝑜 𝜎𝑜

where σo is the yield stress, εo is the corresponding yield strain, and α is a dimensionless number and given by (σo )n /

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(F.εo ).

Results and Discussion

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The true stress-strain curves of longitudinal and transverse tensile specimens for different locations of bone diaphysis
are shown in Fig. 2 and Fig. 3 respectively. The plastic strain values can be obtained by extracting the elastic strain
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part from the total strain values based on Equation (3), as per our previous study [27]. By doing so, the relationships
between true stress and plastic strain were determined for different locations of bone diaphysis; and the results, i.e.,
the true stress-plastic strain curves for longitudinal and transverse directions of loading are shown in Fig. 4 and Fig. 5
rip

respectively.
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Upper diaphysis
Middle diaphysis
Lower diaphysis
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160
True stress (MPa)

120
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80
pt
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40
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0
0.00 0.01 0.02 0.03
True strain

Fig. 2 Longitudinal stress-strain curves for different locations of

bone diaphysis.

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

Upper Diaphysis
Middle diaphysis
Lower diaphysis
100

True Stress (MPa)

d
50

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ed
0
0.000 0.008 0.016

py
Truecurves
Fig. 3 Transverse stress-strain strain for different locations
of bone diaphysis.

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ot
150 tN
True Stress (MPa)

100
rip

Upper diaphysis
Middle diaphysis
50
Lower diaphysis
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0
0.00 0.01 0.02 0.03
Plastic strain (p)
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Fig. 4 Longitudinal true stress -plastic strain curves different

locations of bone diaphysis .
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90
pt
True stress (MPa)
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60

Upper diaphysis
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Middle diaphysis
30
Lower diaphysis

0
0.000 0.005 0.010
Plastic strain (p)

Fig. 5 Transverse true stress-plastic strain curves for

different locations of bone diaphysis .

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

The parameters of R-O equation for different locations of bone diaphysis under the longitudinal and transverse loading
conditions were determined based on the data shown in Fig. 4 and Fig. 5. the results of linear regression analysis for
the longitudinal and transverse loading condition are shown in Fig. 6 and Fig. 7, respectively. The corresponding
results of linear regression analysis , in terms of linear regression equations, coefficient of determination (COD) r2 ,
and p (probability)-values, are listed in Table 3.

1 𝐵
log(𝜀𝑝 ) = log(𝜎) − (4)

d
𝐴 𝐴

ite
1 𝐵
𝑛= ; 𝐹 = Antilog [ ] (5)
𝐴 𝐴

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py
Upper diaphysis
Middle diaphysis
2.2 Lower diaphysis

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2.1
Log ()

2.0

1.9
ot
tN
1.8
rip

-4 -3 -2 -1
Log (p)
sc

Fig. 6 Linear fit of log (true stress) versus log (true plastic strain) curves for
different locations of bone diaphysis under the longitudinal loading.
nu
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Upper diaphysis
2.0 Middle diaphysis
Lower diaphysis
ed

1.9
pt Log ()
ce

1.8
Ac

1.7

-4 -3 -2
Log (p)

Fig.7. Linear fit of log (true stress) versus log (true plastic strain) curves for
different locations of bone diaphysis under the transverse loading

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

Table 2 Results of linear regression analysis for different diaphysis locations and loading directions

Longitudinal direction of loading

Sample location
Linear regression equation COD (r2 ) p-value
Upper log(σ) = (0.08137) log (𝜀𝑝) + 2.21499 0.96 1.36E-7
Middle log(σ) = (0.07747) log (𝜀𝑝) + 2.33742 0.98 1.69E-14
Lower log(σ) = (0.13612) log (𝜀𝑝) + 2.28678 0.99 2.89E-15

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Sample location Transverse direction of loading
Linear regression equation COD (r2 ) p-value

ite
Upper log(σ) = (0.03982) log (𝜀𝑝) + 1.92698 0.99 6.49E-7
Middle log(σ) = (0.0423) log (𝜀𝑝) + 2.07551 0.99 7.18E-6

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Lower log(σ) = (0.0646) log (𝜀𝑝) + 1.90962 0.96 1.15E-4

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Table 3 Parameters of R-O equation evaluated for different diaphysis locations and loading directions

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Longitudinal direction of loading
Sample location F
σo (MPa) εo n α
(MPa) α

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Upper 95.6 0.00685 12.29 1.66E27 0.19
Middle 132.5 0.00715 12.91 1.49E30 0.0017
Lower 81.6 0.00715 7.35 6.31E16 0.0018
tN
Transverse direction of loading
Sample location
F
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σo (MPa) εo n α
(MPa) α
Upper 65.7 0.00711 25.11 2.47E48 0.61
Middle 89.7 0.00865 23.64 1.16E49 0.17
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Lower 55.1 0.00811 15.48 3.64E29 0.30

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As seen in Table 2, the values of coefficient of determination (r2 ) for different linear regression curves of cortical bone
were found to be in a range from 0.96 to 0.99 with p-values less than 0.0001. This suggests a strong linear relationship
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between the values of log (true plastic strain) and log (true stress) and also provides strong evidence for the
applicability of R-O equation in case of bone material. The values of strain hardening exponent (n) were found to be
maximu m for the middle diaphysis and minimum for the lower diaphysis of cortical bone under the longitudinal
loading; and maximu m for the upper diaphysis and minimum for the lower diaphysis of cortical bone under the
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transverse loading. The values of plastic modulus (F) were found to be maximu m for the middle diaphysis and
minimum for the lower diaphysis of cortical bone under both longitudinal and transverse loading. This signifies higher
hardening rate and thus higher amount of energy consumption at this location of bone diaphysis during plastic
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deformation, which may due to the multiple, concurrent deformation mechanisms at various hierarchical levels of
bone. Taken together, the stress-strain behavior of cortical bone at different diaphysis locations under the longitudinal
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and transverse loading condition, as examined in the present study, can be represented by using the R-O equation with
the parameters in Table 3. The values of strain hardening exponent (n) and plastic modulus (F) evaluated in this study
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would be helpful to derive the values of plastic part of J-toughness of cortical bone [25,28].

Conclusions
Mechanical properties of bone are of importance to discover the bone structure -function relationship and to repair
damaged bone with tissue scaffolds. This study was to examine the mechanical properties of bovine femoral cortical
bone and represent the non-linear stress-strain relationship by using the R-O equation. The linear regression analysis
was carried out with the results illustrating that a linear relationship existed between the values of log (true stress) and

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

log (true plastic strain) obtained at different locations of bovine bone diaphysis, which justified the applicability of R-
O equation for the case of bovine bone material. Our results also illustrated that the parameters of R-O equation, i.e.,
the strain hardening exponent (n) and plastic modulus (F), varied, depending on the locations of bovine bone diaphysis
and the loading directions.

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 Journal of Biomechanical Engineering. Received July 03, 2018;
Accepted manuscript posted February 19, 2019. doi:10.1115/1.4042901
Copyright (c) 2019 by ASME

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