Chapter 2:
Bone
Purpose:
1.
To describe the basic structural and material properties of cortical and trabecular bone.
2.
To describe how bone remodels and adapts.
SEM of dried long bone with marrow removed (from http://mcrcr4.med.nyu.edu/Histology/Unit4-14.html)
The skeletal system is designed to protect internal organs, provide rigid supports, provide
muscle attachment sites, and to facilitate muscle actions that stabilize and move the body. Bone
has unique mechanical properties that allow it to perform these functions. Bone is one of the
body’s hardest materials, with dentin and enamel in the teeth being harder. It is one of the most
metabolically active materials within the body and it remains active throughout life. It has an
excellent capacity to repair itself and adapt to changing environmental stresses.
Structure:
Bone is described as a connective tissue, helping to support and bind together various
parts of the body. Bone is a composite material consisting of both fluid and solid phases. Its
specific gravity is about 2.0 but varies depending on the type of bone. Bone obtains its hard
structure because the organic extracellular collagenous matrix is impregnated with inorganic
materials, principally hydroxyapatite Ca10(PO4)6(OH)2 consisting of the minerals calcium and
phosphate. Calcium and phosphate account for roughly 65 to 70 % of the bone's dry weight.
Collagen fibers compose approximately 95 % of the extracellular matrix and account for 25 to 30
% of the dry weight of bone. The organic material gives bone its flexibility while the inorganic
material gives bone its resilience.
Surrounding the mineralized collagen fibers is a ground substance consisting of protein
polysaccharides, or glycosaminoglycans (GAGs), primarily in the form of complex
macromolecules called proteoglycans. The GAGs serve to cement together the various layers of
mineralized collagen fibers.
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Water accounts for up to 25 % of the total weight of bone with about 85 % of the water
being located in the organic matrix around the collagen fibers and ground substance. The other
15 % is located in canals and cavities that house the bone cells.
At the gross level bone exists in a variety of shapes and sizes (see Figure 1). The general
shapes of bones are conserved across vertebrate skeletons, but the specific morphology varies
considerably (e.g. a rat femur has the same general shape as a human femur, but it differs greatly
in its size and specific architectural details). Bone is identified as either cancellous (also referred
to as trabecular or spongy) or cortical (also referred to as compact). Cortical bone represents
approximately 4 times the mass of cancellous bone in any long bone. The basic material
comprising cancellous and compact bone appear identical, thus the distinction between the two is
the degree of porosity and the organization. The porosity of cortical bone ranges from 5% to 30
% (mostly in the range 5%-10%) while cancellous bone porosity ranges from 30% to 90 %
(mostly in the range 75%-95%). Bone porosity is not fixed and can change in response to altered
loading, disease, and aging.
Figure 1 - Bone exists in a variety of shapes and sizes. Shown here are illustrations of bones
within the human body (A) bones of the foot, (B) bones of the wrist, (C) long bone of the upper
arm, (D) vertebral bones, (E) bones of the pelvis.
The fibrous layer covering all bones is the periosteum. This membrane covers the entire
bone except the joint surfaces, which are covered with articular cartilage (discussed in the next
chapter). The periosteum is permeated by blood vessels and nerve fibers that pass into the bone
via Volkman's canals. The periosteum contains an osteogenic layer that contain stromal cells
and hematopoietic cells that are precursors to osteoblasts and osteoclasts respectively. These
cells are important during growth and repair.
There are numerous terms used to describe the complex architecture of bone at a finer
resolution. Both cortical and cancellous bone may contain two types of basic architecture,
woven and lamellar. Woven bone appears in newborns, callus, and metaphyseal regions. It can
be quickly formed and is coarse fibered with no uniform collagen orientation. Woven bone may
become more mineralized than lamellar bone. Lamellar bone is slow forming, highly organized
tissue appearing as trabecular bone, circumferential lamellae, interstitial lamellae, and osteons
with concentric lamellae. Lamellar bone is organized into parallel layers similar to ‘plywood’.
Collagen orientation within these layers may vary between layers. Lamellar bone starts forming
one month after birth. By age four most bone in the body is lamellar.
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Bone can also be described as primary or secondary bone. Primary bone is tissue laid
down de novo on an existing bone surface during growth. Secondary bone results from the
resorption of bone and its replacement with new bone. This process is known as remodeling.
Adult bone is almost entirely secondary bone.
Cancellous bone is spongy in appearance and has a large surface area. There are no
blood vessels located within this type of bone. Cancellous bone is typically found in cuboidal
bones (e.g. vertebrae), flat bones, and the ends of long bones. Cancellous bone is composed of
concentric layers (lamellae) of the mineralized matrix described above. Located along the
boundaries of each concentric layer are small cavities called lacunae, each containing one bone
cell or osteocyte. Radiating from each lacunae and connecting adjacent lacunae are numerous
small channels called canaliculi. The osteocytes receive nutrients through canaliculi from blood
vessels located in the red marrow surrounding the trabeculae. Cancellous bone is always
surrounded by cortical bone.
The space between the struts, or trabeculae, making up cancellous bone is filled with
marrow. Bone marrow is a tissue composed of blood vessels, nerves, and various cells. Bone
marrow is functionally significant because it generates the cells found in blood and it provides
some mechanical support during bone loading. Marrow is highly osteogenic and can stimulate
bone formation if placed in other parts of the body.
Cortical bone is typically found in the shaft of long bones and as a shell around spongy
bone. Regions within cortical bone are often described as either haversian or laminar (Figure
2). The haversian type consists of an osteon with a central channel called the haversian canal.
This canal contains blood vessels and nerves. Surrounding the canal are lamellae, lacunae and
osteocytes, same as those described above for cancellous bone. The network of canaliculi allows
blood and nutrients from the haversian canal to reach the osteocytes. Each osteon has a cement
line at its periphery. Neither the canaliculi nor the collagen fibers of an osteon cross the cement
line. A typical osteon is about 200 micrometers in diameter. Every point in an osteon is no more
than 100 micrometers away from the centrally located blood supply. Osteons usually run
longitudinally in long bones, but they branch often and intertwine with each other. The second
type of cortical bone span the regions between osteons. These interstitial lamellae are
continuous with the osteon and they are composed of the same material but in a different
configuration. The interstitial lamellae do not have a haversian canal but they do have an array
of lacunae in which osteocytes lie and from which canaliculi extend.
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osteocyte
canaliculli
lacuna
lamellae
cement line
circumferential
lamellae
haversian
canal
periosteum
Volkman's canal
collagen fibers
surrounded by
a mineral matrix
Figure 2 -Illustration of the structure of cortical bone.
Structural and Material Properties:
The properties of bone and other biological tissues depend on the freshness of the tissue.
The properties of bone can change within a matter of minutes if allowed to dry out. Cortical
bone has an ultimate strain of around 1.2 % when wet and about 0.4 % if the water content is not
maintained. Thus, it is very important to keep bone specimens wet during testing.
The material properties of bone are generally determined using mechanical testing
procedures, however ultrasonic techniques have also been employed. Mechanical testing
consists of applying tensile, compressive, torsional, or shear loads to bone specimens and
recording the deformation of the material. Force-deformation (structural properties) or stressstrain (material properties) curves can then be determined. Mechanical testing of bone is
complicated because of the anisotropy of bone (requires multiple samples for testing) and the
small sample sizes that are obtainable. For this reason efforts have been made to use ultrasonic
techniques. These techniques make use of the relations between the speed of sound in a material
and the elastic properties of that material. Ultrasound requires fewer and smaller specimens to
characterize the material properties of bone. The disadvantage is that the relationship between
the speed of sound and the tissues elastic properties must already be known.
The typical geometry of a specimen used in a bone tensile test is shown in Figure 3 along
with an illustration of the material properties of cortical bone. Bone shows a linear range in
which the stress increases in proportion to the strain. The slope of this region is defined as
Young's Modulus or the Elastic Modulus. An illustration of the material properties of bone
relative to other material is shown in Figure 4. Both steel and glass are stiffer and stronger than
bone.
Bone is strain rate sensitive (Figure 5) and tends to be more strain-rate sensitive than
other biological tissues. This has implications for bone-ligament and bone-tendon injuries
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(discussed in later chapters). The optimal strain rate for energy absorption appears to be between
0.1 and 1/second.
Three important parameters that characterize some of the mechanical properties of bone:
ultimate force, maximum deformation to failure, and energy that it can store before failing, can
be obtained from a force-deformation curve. The ultimate force represents the maximum load
that the bone can sustain before it breaks. The ultimate force varies depending on the type of
load applied (e.g. tensile, compressive, shear) and the loading rate. The deformation at failure is
self-explanatory and also depends on the loading rate and direction. The energy absorbed before
failing can be calculated from the area under the force-deformation curve and therefore depends
on both the ultimate force and the ultimate strain. Children’s bones tend to absorb more energy
before failure compared to adults (as much as 45 % more). Children’s bones are weaker, but
more compliant (children’s bones can be 68% as stiff as adult bone).
Material properties of the two types of bone differ. Cortical bone is stiffer than
cancellous bone. It can sustain greater stress but less strain before failure. Cancellous bone can
sustain strains of 75 % before failing in-vivo, but cortical bone will fracture if the strain exceeds
2 %. Cancellous bone has a greater capacity to store energy compared to compact bone.
Figure 3 - Illustration of a bone test specimen and a stress-strain curve resulting from a tensile
test.
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Figure 4 - Material properties of bone relative to other common materials.
Figure 5 - Illustration of the strain-rate sensitivity of cortical bone. As the strain-rate increases
the ultimate stress increases and the ultimate strain decreases.
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Figure 6 - Illustration of the different types of loading that can be imposed on bone. Bones can
be subjected to axial compression, axial tension, torsion, shear, bending, or any combination of
these.
Loading of Bones:
Bones are routinely subjected to a variety of loads (see Figure 6). As a person stands on
one leg, his femoral shaft will be subjected to a compressive load due to the person’s body
weight. It may also be subjected to a bending moment if the compressive force does not act
through the neutral axis of the femur. A bending moment will cause a portion of the bone to act
in tension while another portion acts in compression. The femur may be subjected to a shear
load as the leg bumps into a table. Loading of bone can come from external forces applied to the
body or internal forces generated by the muscles and connective tissue.
An axial compressive force will create a stress (σ=-F/A) where F is the axial force and A
is the cross-sectional area. The standard convention is to express compression as negative and
tension as positive. It can be shown from a strength of materials analysis that the linear variation
in stress across the cross-section of a beam subjected to a bending moment (M) is (σ=+ My/I)
where I is the area moment of inertia and y is the distance from the neutral axis. Maximum
stresses are generated on the surface of the material. If the bending moments are large enough to
cause fracture, the fracture will be initiated along the material surface. During combined loading
of compression and bending the stress across the cross-section of a specimen will be (σ=-F/A +
My/I). In this case the neutral axis (i.e. the axis of 0 stress) is no longer coincident with the
centroid axis.
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Figure 7 - Illustration of the effect that muscle forces can have on bone stresses. During normal
standing approximately 35% of body weight (BW) is support by the femoral head. The midshaft of the femur must support an axial compression force of approximately 40% of BW and a
bending moment proportional to 40% of BW. This places the lateral surface of the femur in
tension and the medial surface in compression. If the person activates his hip adductor muscles
and develops a 10% of BW force, then the compressive force on the femoral head increases to
42% of BW. The bending moment at the mid-shaft of the femur is reduced, which reduces the
tensile and compressive forces on the medial and lateral surfaces (bottom half of the illustration).
The neutral axis of the femur also shifts medially.
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Muscle forces can play an important role in bone loading. They can act to increase or
decrease bone loading. For example consider a simple standing task (see Figure 7). During
normal standing approximately 35% of body weight (BW) is support by the femoral head. The
mid-shaft of the femur must support an axial compression force of approximately 40% of BW
(the 35% of body weight at the hip plus half the weight of the femur) and a bending moment
created by the eccentric loading of the femur. This places the lateral surface of the femur in
tension and the medial surface in compression. The neutral axis of the femur would be lateral to
the area center of the femur. If the person activates his hip adductor muscles and develops a
10% of BW force, then the compressive force on the femoral head increases to 42% of BW (35%
BW plus 10% BW *sin 45°, neglecting the weight of the femoral head). An additional lateral
force must be developed at the femoral head. The bending moment at the mid-shaft of the femur
is reduced by the muscle moment (as long as the neutral axis is located within the bone crosssection), which reduces the tensile and compressive forces on the medial and lateral surfaces.
The neutral axis of the femur shifts medially toward the area center. What would happen if hip
abductor muscles developed force on the greater trochantor? For this case the bending moment
would be increased which would increase tensile force on the lateral surface of the mid-shaft of
the femur and increase the compressive force on the medial side. Can you see how muscle
forces might contribute to a hip fracture in an elderly person?
Growth:
Longitudinal bone growth occurs primarily at the epiphysis. The epiphysis is separated
from the main part of the bone by a layer of hyaline cartilage. During growth this cartilage is
converted to lamellar bone in a process called enchondral ossification. This process stops at the
time of skeletal maturity. Longitudinal growth appears to progress at a natural rate where-as
transverse growth appears to depend on the loading of the bone. These loads can come from
body weight, muscle forces, or external forces.
There are two cells that are important in bone growth and remodeling: osteoblasts and
osteoclasts. Osteoblasts are responsible for laying down new bone. Osteoclasts remove old and
damaged bone. The state of formation or resorption of the skeleton depends on the relative
activity of each of these types of cells. On average 10 % of the adult skeleton is remodeled
annually. Remodeling is a surface phenomenon. The turnover rate for cortical bone may be as
high as 50 % annually in children and as low as 2 % annually in the elderly. The turnover rate
for trabecular bone tends to be 5 to 10 times higher than that of cortical bone due to its greater
surface area. Osteoblasts and osteoclasts develop from stromal and hematopoietic cells
respectively when appropriate signals are generated. Stromal and hematopoietic cells reside in
marrow and vascularized areas (such as the periosteum, haversion canals, etc.).
Changes in bone may take place slowly (months or years) due to the action of bone cells
or rapidly (days) due to the uptake or output of minerals. Julius Wolff was the first to promote
the idea that bones remodel in response to the stresses and strains acting on them. Limb
immobilization can cause calcium and phosphorus to be removed from the bone. Astronauts
subjected to only 4 days of weightlessness showed bone mineral losses. After normal activity is
resumed, it may take several months to regain the mineral lost during the immobilized or
weightlessness period.
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Dysfunction of Bone Remodeling:
Any alteration in the normal coupling between bone formation and resorption results in
alterations in the structure and mass of bone. Bone remodeling is affected by a variety of
metabolic and non-metabolic factors. These factors include weight bearing, genetics, stress,
extracellular mineral concentrations, parathyroid hormone, vitamin D, estrogens, and thyroid
hormone. These factors can act to increase the activity of osteoclasts (resorption) or osteoblasts
(bone formation). Most metabolic bone diseases result from an imbalance in the formation and
resorptive processes.
Aging:
Skeletal mass increases rapidly during the growth period, being maximal at about 25 to
30 years of age and decreases slowly throughout the rest of life (thus, the rationale for leading
active youthful lives so that bone content is maximized prior to the deterioration phase of later
life). Bone loss occurs in all bones of the body though the rate of bone loss may vary for
different bones. The magnitude of bone loss varies greatly with gender and race, being more
severe in white females compared to blacks or males. From the third to the ninth decades of life,
respectively, the ultimate tensile strength of cortical bone taken from the femur, for longitudinal
loading, decreases from approximately 130 MPa to 110 MPa, and the corresponding elastic
moduli change from approximately 17 GPA to 15.6 GPa. The slope of the stress-strain curve
after yielding increases by 8% per decade. The overall result is a decrement in the energy
absorbing capacity of bone by approximately 7% per decade. Cortical bone material becomes
less strong, less stiff, and more brittle with aging.
Age related changes in cancellous and cortical bone consist of progressive loss of mineral
content associated with a decrease in the mechanical strength of bone, a reduction of cortical
thickness, and a decrease in the amount of cancellous bone. Cancellous bone loses more bone
material than does cortical bone, perhaps due to its greater surface area. Evidence suggests that
bone loss comes as a result of depression of osteoblast activity rather than an increase in
osteoclast activity.
Injury and Repair:
Remodeling occurs on a daily basis to replace dead cells or repair damaged cells. When
an injury (bone fracture) occurs a special sequence of events takes place. First a hematoma
appears followed by a vascular tissue which supports a fibrin structure. Osteoblasts then appear
in the tissue and start to lay down new bone to form a callus. The callus acts as solder to hold
the bones together and allows function of the bone to resume. The callus usually takes 3 to 20
weeks to develop, generally being strong enough to resume function at the magic 5-6 weeks
recommended by orthopaedic surgeons. This time varies with age and extent of injury. Over the
next five years the callus is removed and replaced with lamellar bone. New bone is laid down
along the oriented lines of greatest stress.
Bone fractures can be produced by a single large load or by repeated applications of a
small load. A fracture caused by repeated applications of a small load is called a fatigue fracture.
There is an interaction between the magnitude of the load and the number of cycles that a bone
can withstand before fracture (Figure 8). In repetitive loading of living bone, the fatigue process
is affected not only by the amount of load and the number of repetitions, but also the number of
applications within a given time (frequency of loading). Since living bone is self-repairing, a
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fatigue fracture results only when the fatigue process proceeds at a faster rate than the
remodeling rate.
Fatigue fractures usually occur during sustained strenuous activities. Fatigue of muscle
during these activities may also contribute to the injury. A reduction in the muscle's ability to
generate force will also result in a decrease in the muscle's ability to absorb energy. The bone
loading profiles may be increased as a result.
Figure 8 - Illustration of an Injury Threshold dependent on the magnitude of the load and the
number of times the load is applied. The curve indicates that the bone can withstand “n1” cycles
of stress “σ1” and “n2” cycles of the lower stress “σ2”. The equation indicates the number of
cycles (n) (i.e. fatigue life), that the bone can withstand when loaded repeatedly to a strain (εexpressed in units of microstrain). K and q are constants, q typically having a value between 5
and 15 and K being a large number (Martin, et al., 1998).
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Summary:
Bone is often considered a two-phase composite material. It is composed of inorganic
mineral salts and an organic matrix of collagen and ground substance. The inorganic substance
makes bone hard while the organic substance gives bone flexibility. Microscopically, the osteon
is the fundamental unit composed of concentric layers of mineralized matrix surrounding a
central canal. Macroscopically, the skeleton is composed of two types of bone: compact and
cancellous. These two types of bone are similar in structure but different in porosity. Bone is an
anisotropic material. Bone is subjected to complex loading patterns during daily activities.
Muscle forces can act to reduce or increase the stresses acting in bone. Bone sustains fatigue
fractures when the frequency of loading is such that the rate of remodeling is slower than the rate
of microfracture accumulation. Bone remodels in response to the mechanical demands placed
upon it. With aging there is a marked reduction in the amount of cancellous bone and a decrease
in the thickness of cortical bone. These changes diminish bone strength and stiffness.
References:
Cruess, R.L. Physiology of Bone Formation, Function, and Destruction. Chapter 9 in The
Musculoskeletal System: Embryology, Biochemistry, and Physiology. Edited by Cruess, R.L.
Churchill Livingstone, New York, 1982.
Cowin, S.C., Van Buskirk, W.C., and Ashman, R.B. Properties of Bone. Chapter 2 in
Handbook of Engineering. Edited by Skalak, R. and Chien, S. McGraw-Hill book Company,
New York, New York,
Frost, H.M. An Introduction to Biomechanics, Charles C. Thomas Publisher, Springfield, Ill.
1971.
Fung, Y.C. Biomechanics: Mechanical Properties of Living Tissues. Springer-Verlag, New
York, 1981.
Marie, P.J. Structure, Organization, and Healing. Chapter 6 in The Musculoskeletal System:
Embryology, Biochemistry, and Physiology. Edited by Cruess, R.L. Churchill Livingstone, New
York, 1982.
Martin, R. Bruce, Burr, David. Burr, and Sharkey, Neil, A.. Skeletal Tissue Mechanics.
Springer-Verlag, New York, 1998.
Mow, V.C. and Hayes, W.C. Basic Orthopaedic Biomechanics. Raven Press, New York, 1991.
Nordin, M and Frankel, V. Biomechanics of Bone. Chapter 1 in Basic Biomechanics of the
Musculoskeletal System. 2nd Edition. Edited by Nordin, M. and V.H. Frankel. Lea and Febiger,
Philadelphia, 1989.
Orthopaedic Basic Science, Edited by Sheldon Simon. American Academy of Orthopaedic
Surgeons. Park Ridge, IL, 1994
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Sample Questions:
1. Water constitutes approximately how much of the wet weight of bone?
2. Describe the role that ground substance, consisting of protein polysaccharides or
glycosaminoglycans (GAGs) play in bone.
3. Describe the difference between cancellous and compact bone.
4. Can cancellous or cortical bone specimens of similar dimensions typically absorb more
energy?
5. Please describe a haversian system.
6. Describe the function of osteoblasts and osteoclasts.
7. On average, how much of an adult skeleton is remodeled annually? How does this value
differ from that estimated for children and elderly?
8. Joe starts off on a journey hoping to run across the country. He plans to run 30 miles per day.
He will take approximately 2,640 steps per mile (1,320 loading cycles per leg per mile) and
experience 1500 µε per loading cycle. Use the equation given in Figure 8 and values of 10x1040
and 11 for K and q respectively to determine the number of miles Joe will run before sustaining a
fatigue fracture.
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