BfOfl/IECFI,ANIC

OF BONE
MargareaNordin
VictorH. Franke

The purpose of the skeletal qrstem is to

protect consists of cells and art orgarric extracellular
internal organs, provide ritrd icinematic matrix of
rinl6 and fibers and gronnd substance
murle attachnrent sites, ana facilitate _produced by til ..ttr.
muscle action The distinFishing feattue of bone is ie
'tnd t'*cdy movemenl Bone tras unique t igh .oii.r,t
siruct.oal and of inoqganic materiah, in the forur of mineral
nrtrhanical groperties that allow it salts,
io cary out these ftat combine intimately with the organic
r'lt"s' Bone is among the bod/s matrix. The
turdest stnrct'res, inorganic cornponent of bone maki ur.
'nlv dentin and enasrel in the tissue hard
teeth being harder. It
is ()ne of the most dynasdc
and metaboEllly active Td-rrtrd, while the o{gardc component gives bone its
tissues -. flelibility and resilience.
body and remains active throughout
lifc- A highlv*.. The ffi:=l portion of bone consists primaril y of
vasgular tissue, it has -rn excetent
t"lpacit)' for self-repair and calcitun and phosphate, mainly in the fo'rm
ctn alter its properties of smatt
t''nfigu:ation in t"tpot '; and crystels res€mbli"g slEthetic h.yto*Jr"patite
t" to changes mechanical cystals
tlcmand- Fo1 *.o,pi.,,."h"og, with the pmposition Gro(poj.(oH)r.'These
in bone dersity are -the miner-
('()mmonly observed als, which account for at to /On of
after Ft.ar of diilse and of bone,s dry
grcatlv increased weight, F e bone its sotid coruistency.
*: o*g, in bone shape :rre Bone seryes
note'd during fracturS :ls a reservoir for essential minerah'in
hearini"r,a after certain or)er- the body,
att,ns' Thus, bon" partiailarlv calciun.
adapts * a" mechanicat demands
placedon it. Bone mineral is embedded in rrariously
oriented
This chapter des,qibes fibers of
the composition and stmc- tg protein 5o!s9n, the fibrous portion of
ture of bone the octracellular matrix. CJUagen fibers are
dszue, the mechanical tough and
bone' and $,e--uetnvior prcperties of pliable,
loading conditio*- of bone trnder different I.t t"r resist sreiching have rirtre
atensibility. collagen cgmposesapproximatery
"r,l gsvo
various hctors that affect the
mechanical behavio, of the ocracellular-matrix a .*d,i"ts for abodt
of bone
-r ir, ,.iuo and in vivo are
rzr''rlE rrl
"t of bone. 25
.rlso di_<ctrssgd. to 30% of the dry weight A universal
building block of the bodt, gollag.r, ir also
the chief
ftrous component of oti ei 'skeietal ,t ,r.t
rr.r. (A
BON.E CO,tfpOStTION detailed dToiption of the misostmchrre
VUITTVI' AND and me_
STRUCTURE" chanicalbehaviorof collagen is provided in
Chapters
2 and 3.)
Bone 6ssue is
a specialized The g"l".ti"gys tround substancesurrounding
-rG connective tissue the
"r'hose *,r.g ."*p"sitigir mineralizecl.c.ollagenfibers coruists mainly of pr3t"ir,
-tn.i pro:ectire i, for its supportive polysaccharides,or
'ollr- ut* o-,h.] icairl, pi-
connective tissues, it maril)rin the form ofSrcosaminoglycanr
iomprex macromorecules calred
 BIOMECHANICS
OF NSSUES
AND STRUCTURES
OF THE MUSCULOSKELETAL
proteoglycans (PGs). The GAGs ser:\reas a cementing
substance between layers of mineralized collagei
fibers. These GAGs, along with various nonco[Jgu-
nous glycoproteins, constitute about svo of the
cellular matrix. (The structure of PGs, which are"*iu-
vital
components of articular cartila ge, is described in
detail in Chapter 2.)
Water is fairly abundant in live bone, account-
ing for up to 25% of its total weight. About gsvo
of the water is found in the organic matrix, around
the collagen fibers and ground substance, and in the
hydration shells surrounding the bone crystals. The
other L57o is located in canals and cavities that house
bone cells and carry nutrients to the bone tissue.
At the microscopic level, the fundamental struc-
fural unit of bone is the osteon , ot haversian system
(Fig. t-1). At the center of each osteon is a small
channel, called a haversian canal, that contains blood
vessels and nen/e fibers. The osteon itself consists of
a concentric series of layers (lamellae) of mineralized
matrix surrounding the central canal, d configuration
similar to growth rings in a tree trunk.
Along the boundaries of each layer, or lamella, are
small cavities known as lacunae, each containing one
LAMELLAE
CANALICULI
OSTEOCYTE
LACUNA
CIRCUMFERENTIAL
IAMELLAE
HAVERSIAN
SYSTEMS
C E M E N TL I N E
INTERSTITIAL
LAMELLAE
TRABECULAE
HAVERSIAN
CANALS
BLOODVESSEL
VOLKMANN'S BRANCHESOF
CANALS PERIOSTEAL
BLOODVESSELS
sYsTEM
bone cell, or osteocyte (see Fig. l-tc). Numerous
small channels, calea canali*-li, rad.iate from each
lacrrna/ connecting the lacunae of adjacent lamellae
and ultimately reaching the haversian canal. Cell
processes extend from the osteorytes into the cana-
liculi, allowing nufrients from the blood vessels in the
haversian canal to reach the osteocytes.
At the periphery of each osteon is a cement line, a
narrow area of cementlike ground substance com-
posed primarily of glycosaminoglycans. The canalic-
uli of the osteon do not pass this cement Line. Like the
canaliculi, the collagen fibers in the bone matrix
interconnect from one lamella to another within an
osteon but do not cross the cement line. This
intertwining of collagen fibers within the osteon
undoubtedly increases the bone's resistance to me-
chanical stress and probably explains why the cement
line is the weakest portion of the bone's microstruc-
ture (Dempster and Colemdrr, L960; Evans and Bang,
Le67).
A typicalosteonis about200micrometers(pm) in
diameter. Hence, everypoint in the osteonis no more
than 100 F.mfrom the centrally located blood supply.
In the long bones, the osteons usually run longitudi
F I G .I - I
A. The fine structureof bone is iflustrated
schematicalfyin a sectionof the shaft/ofa long
bone depictedwithout inner marrow.The os-
teons,or haversian systems,areapparentas the
structurafunits of bone. fn the center of the
osteonsare the haversiancanafs,which form
the main branchesof the circulatory networkin
bone.Eachosteonis boundedby a cementline.
One osteonis shown extending from the bone
(20x1. fAdaptedfrom Bassen,1965.lB, Each
osteon consistsof fameflae, concentricrings
composedof mineral matrix surroun ding the
haversiancanaf. (Adapted from Tortora and
Anagnostakos, l9g4.l C. Along rhe boundaries
of the lamelfaeare small cavitiesknown as
lacunae,eachof which containsa singfebone
celf,or osteoqrte.Radiating fromthe lacunaeare
tiny canafs,or canaliculi,into which the ryto-
pfasmic processesof the osteoq/tes extend.
(Adapted from Tortora and AnagnostakoS,
te8+.1

nally, but they branch frequently and anastomose
extensively with each other.
Interstitial lamellae span the regions between com-
plete osteons (see Fig. 1-1A). Th"y are continuous
with the osteons and are just the same material in a
different geometric configuration. As in the osteons,
no point in the interstitiat lamellae is farther than 100
pm from its blood supply. The interfaces between
these lamellae contain an array of lacunae in which
osteorytes lie and from which canaliculi extend.
At the macroscopic level, all bones are composed
of two types of osseous tissue: cortical, or compact,
bone and cancellous, or trabecular, bone (Fig. l-Z).
Cortical bone forms the outer shell, or cortex, of the
bone and has a dense structure similar to that of
ivory. Cancellous bone within this shell is composed
of thin plates , ot trabeculae, in a loose mesh struc-
ture; the interstices between the trabeculae are filled
with red marrow. Cancellous bone tissue is arranged
in concentric lacunae-containing lamellae, but it does
not contain haversian canals. The osteorytes receive
nutrients through canaliculi from blood vessels pass-
irg through the red marrow. Cortical bone always
surrounds cancellous bone, but the relative quantity
of each Vpe varies among bones and within individ-
ual bones according to functional requirements.
FrG.1-2
Frontal longitudinal section through the
head, neck, greater trochanter,and prox-
imaf shaft of an aduft femur. Cancellous
bone, with its trabecufae oriented in a
lattice, lies within the shell of cortical
bone. (Reprinted with permission from
Gray, H.. Anatomy of the Human Body.
l3th American Ed. Edired by C. D.
Clemente. Philadelphia"Lea & Febiger,
le8s.)
BIOMECHANICSOF BONE
Since the lamellar pattern and material composi-
tion of cancellous and cortical bone appear identical,
the basic distinction between the two is the degree of
porosify. Biomechanically, the two bone types can be
considered as one material whose porosify and
density vary over a wide range (Carter and Hayes,
1977b). The difference in the porosif of cortical and
cancellous bone can be seen in cross sections from
human tibiae (Fig. 1-3). The porosity ranges from 5
to 30Vo in cortical bone and from 30 to over 90Vo in
cancellous bone. The distinction between porous
cortical bone and dense cancellous bone is somewhat
arbitrary.
All bones are surroundedby a dense fibrous
membrane called the periosteum (see Fig. 1-1A). Its
outer layer is permeated by blood vessels and nen/e
fibers that pass into the cortex via Volkmann's canals,
connecting with the haversian canals and extendi*g
to the cancellous bone. An inner, osteogenic layer
contains bone cells responsible for generating new
bone during growth and repair (osteoblasts). The
periosteum covers the entire bone except for the joint
surfaces, which are covered with articular cartilage.
In the long bones, a thinner membrane, the endos-
teum, lines the central (medullary) cavity, which is
filled with yellow fut!y marrow. The endosteum
ff*
^&--*
#*
{fr
dt
(t BIOMECHANICS
OF TISSUES
AND STRUCTURES
OF THE MUSCULOSKELETAL
SYSTEM

FrG.| -3
ightphotomicrograph
r{. Reflected-f of
cortical bone from a human tibia
(+}xl. (Courtesyof Dennis R. Carter,
Ph.D.l B. Scanningelectron photo-
micrographof cancelfousbone from
a human tibia {30x,. (Courtesyof
DennisR.Caner,Ph.D.|

contains osteoblasts and also giant multinucleated A hypothetical load-deformation curve for a some-
bone cells called osteoclasts, which play a role in the what pliable fibrous structure, such as a long bone, is
resorytion of bone. shown in Figure "1,-4. The initial (straight line)
portion of the curye, the elastic region, reveals the
elasticify of the structure, i.e., its capacity,for return-
BIOMECF{ANICALPROPERTIES
OF
BONE

Biomechanically, bone tissue may be regarded

as a two-phase (biphasic) composite material, with PI.ASTICREGION C
the mineral as one phase and the collagen and
D
t
ground substance as the other. In such materials (a YIELD ,/ ULTIMATE
o
nonbiologic example is fiberglass)-in which a
strong, brittle material is embedded in a weaker,
o
J

8
F POINT ;

I
I
f
I

ENERGY
FAILURE
POINT

more flexible one-the combined substances are

stronger for their weight than either substance alone
F I
I
f

f
f
(Bassett, 7965). I
r
Functionally, the most important mechanical prop-
erties of bone are its strength and stiffness. These and DEFORMATION
other characteristics can best be understood for bone, FIG.I _4
or any other structure, by examining its behavior Load-deformation curue far a structurecomposedof a some-
under loadinB, r.e., under the influence of externally what pfiablematerial.ff a load is appliedwithin the elasticrange
applied forces. Loading causes a deformation, or a of the structure(A to B on the curvefand is then refeased,no
permanentdeformationoccurs.lf loadingis continuedpastthe
change in the dimensions, of the structure. When a
yieldpoint (B)and into the structure's
pfasticrange(Bto Con the
load in a known direction is imposed on a structure,
curvef and the load is then released,permanentdefoimation
the deformation of that structure can be measured Theamountof permanentdeformationthat occursif the
results.
and plotted on a load-deformation curve. Much structureis foadedto point D in the plasticregion and then
information about the strength, stiffness, and other unfoadedis represented by the distancebetweenA and D,. lf
mechanical properties of the structure can be gained loadingcontinueswithin the pfasticrange,an ultimatefailure
by examining this cun/e. point (C)is reached.
 ffi
i!:
a
r*
a,,!.rlt

*
;+ BIOMECHANICSOF BONE
Ni,
ii:,
,tl
rl;;i
# ing to its original shape after the load is remov€d. As response to externally applied loads. The three units
:::::
+
,:l;
the load is applied, deformation occurs but is not most commonly used for measuring stress in stan-
:,i' permanen| the structure recovers its original shape dardtzed samples of bone are newtons Per centimeter
ir:
when unloaded. As loading continues, the outermost squared (NI/cm2); newtons per meter squared, or
fibers of the structure begin to yield at some point. pascals (N/m2, Pu); and meganewtons per meter
This yield point signals the elastic limit of the squared, or me gapascals (MN/m2, MPa).
structure. As the load exceeds this limit, the structure Strain is the deformation (change in dimension)
exhibits plastic behavior, reflected in the second that develops within a strucfure in resPonse to
(curved) portion of the curve, the plastic region. The externally applied loads. The two basic tyPes of strain
structure will no longer return to its original dimen- are linear strain, which causes a change in the length
sions when the load has been released; some residual of the specimen, and shear strain, which causes a
deformation will be permanent. If loading is progres- change in the angular relationships within the struc-
sively increased, the structure will fail at some point ture. Linear strain is measured as the amount of
(bone will fracture). This point is indicated by the linear deformation (lengthening or shorted^g) of the
ultimate failure point on the curve. sample divided by the sample's original length. It is a
Three parameters for determinirg the strength of a nondimensional parameter expressed as a percentage
structure are reflected on the load-deformation curve: (for example, centimeter per centimeter). Shear strain
(1) the load that the structure can sustain before is measured as the a*onttt of angular change (^y)in a
failing, (2) the deformation that it can sustain before right angle lying in the plane of interest in the
failing, and (3) the energy that it can store before sample. It is expressed in radians (one radian equals
failing. The strength in terms of load and deforma- approximately 57.3 degrees) (International Society of
tion, or ultimate strength, is indicated on the curve by Biomechanics, 1988).
the ultimate failure point. The strength in terms of Stress and strain values can be obtained for bone
energy storage is indicated by the size of the area by placing a stan dardtzed specimen of bone tissue in
under the entire curve. The larger the area is, the a testing jig and loading it to failure (Fig. 1-5). These
greater the energy that builds up in the structure as values can then be plotted on a stress-strain curve
the load isr applied. The stiffness of the strucfure is
indicated by the slope of the curve in the elastic
region. The steeper the slope is, the stiffer the
material.
The load-deformation curye is useful for determin-
irg the mechanical properties of whole structures
such as a whole bone, an entire ligament or tendon,
or a metal implant. This knowledge is helpful in the
study of fracture behavior and repair, the response of
a strucfure to physical stress, or the effect of various
treatment programs; however, characterizing a bone
or other structure in terms of the material that
composes 7t, independent of its geome{r, requires
standardization of the testing conditions and the size
and shape of the test specimens. Such standardized
testing is useful for comparing the mechanical prop-
erties of two or more materials, such as the relative
strength of bone and tendon tissue or the relative
stiffness of various materials used in prosthetic
implants. More precise units of measure can be used
when standardized samples are tested, i.€., the load
per unit of area of the sarnple (stress) and the amount
of deformation in terms of the percentage of change FfG. I -5
in the sample's dimensions (strain). Tha curve gen- Standardizedbone specimen in a testing machine. The strain in
erated is a stress-strain curve. the segment of bone between the two gauge arms is measured
Stress is the load, or force, per unit area that with a strain gauge. The stressis calculated from the totaf foad
develops on a plane surface within a structure in measured.(Courtesyof Dennis R. Carter,Ph.D.)
g OF n55UE5AND STRUCTURES
BTOMECHA.N|CS OF rHE MUSCULOSKEJTALSYSTEM

(Fig. 1-6). The regions of this cr.rn'eare similar to

those of the load-deformation curve. Loads in the
elastic region do not cause perrnanent cieformation,
but once the yield point is exceeded, some deforma-
tion is permanent. The strength of the material in
terms of enerry storage is represented by the area
under the entire curve. The stiffness is represented
by the slope of the curve in the elastic region. A value
for stiffness is obtained by dividing the stress at any
point in the elastic (straight line) portion of the curve
by the strain at that point. This value is called the
modulus of elasticity (Young's modulus). Stiffer
materials have higher moduli.
Mechanical properties differ in the two bone t1pes.
Cortical bone is stiffer than cancellous bone, with-
standing greater stress but less strain before failure.
Cancellous bone in vitro does not fracture until the
strain exceeds 75Vo,but cortical bone fracttrres when
the strain exceeds ZVa.Becauseof its porous stnrc-
ture, cancellous bone has a large capacity for energy
storage (Carter and Hayes, 1975).
Stress-strain curves for cortical bone, met-|, and
glass illustrate the differences in mechanicalbehavior
among these materials (Fig. L-n The variations in
stiffness are reflected in the different slopes of the
curves in the elastic region. Metal has the steepest
slope and is thus the stiffest material.
a
a
l,rl
(r
F
U'
B" STRAIN c'
FlG. | -6 !
Sress-straincurve for a conrcalbone sampfe tested in tersion
(pufledf. Yield poinr (Bl pornt past whrch some permanent
deformarionof the bone sampleoccurred.YieldsresslB'l: foad
per untt area susrarnedby rhe bone sampfe before plasdc
deformationtook place. Yieldsvain lB'l' amount of de!'onnauon
wrthsrood by rhe sampte before plasticdeformauonoccuned.
The strain at any point in the elasucregion of the cun€ is
proponional to rhe srressat that pornl tJtomarcfatlurepoint (Cl:
the pofnr pasr which faitureof fie sample occuned.Ultirnarc
srresslC'l: ioad per unir areasustainedby the sarnplebefore
farfure.Ultimatesrran lCl: amount of deformauonsusulineclby
the samplebeforefallure.
a
U'
UJ
E
F
o
STRAIN
FlG. | -7
Sress-straincun/€s for three materials. Meal has rhe steepest
sfope in rhe etasricregion and is thus the sdffestmaterial.The
elasticporcionof trre cune br menf is a suaight fine, indicating
lineartyetasucbefravior.The fact dut meaf has a long pfastic
region irrdicates fiat trris tlpical ducdle material deforms
exrensivclybeforefailure.Gla<s.a brinfe material,exhibis linearty
elastic befravior but faifs abrupdy wifr licle deformadon, as
indicaredby me |act of a plasdcregion on trte sUess-strain curve.
Conicalbone. u/hicfi possesses both ductile and brinle qualities.
e,rhibirs nonlinear elasric behavior. This behavior is demon-
straredAy a slight curue in trre elastic region, which it'dicates
some yefding durlng loading witrrin dris region. Conical bone
condnus to deform before failure but to a lesserextent than
does meal.
The elastic portion of the cturle for glass and metal
is a straight line, indicating linearly elastic behavior;
virtually no yielding takes place before the yield point
is reached. By comparisor, precise testing of cortical
bone has shown that the elastic portion of the curye is
not straight but is slightly cruved, indicating tlrat
bone is not linearly elastic in its behavior but yields
somerr"hat dudng loading in the elastic region @one-
field and Li, I95n.
After the )""td point is reached, glass deforms very
little before failing, ?s indicated by the absence of a
plastic region on the stress-strain curve. By contrast,
metal €rKhibits extensive deformation before failing,
as indicated by a long plastic region on the curve.
Bone also deforms before failing but to a much lesser
extent than metal. The difference in the plastic
beharior of metal and bone is due to differences in
 EiCMECHAAJICSOF EONE

micromechanical et'ents at yield. Yield.ing in metal

(tested in teruion,-or pulled) is caused Uy pLil
flow li
and formation of prastic rlp lines; ,fup
n ,., are
iormed when the molecul"r oi the lattice srrrcture DUCTILE FRACTURE
of
metal dislocate' Yieldingin bone (tested in tension)
is
caused by debonding of the osteons at the
cement
lines and microfriactrrre.
lvlaterials are classified as brittle or ductile
depend-
ing on the extent of deformation before failure.'Ct FlG. I _g
* Fracure surftces of sarnplesof a ducrile
is a t'"ical brittle material, and soft metal is and a britde marenal.
a tlet- The broken frnes on fte dr,rcrifemateriat
ductile material- The difference in the indicate tfre origirul
of lengfi of dre sampfe. before ft deformed.
deforrration is reflected in the fractrrre surfaces "o,o#t The bride marenat
of the deformed rcry lirde befure ftacnrre.
hvo materi*
-(Hg- l-g). when pieced together after
trachue, the ductile material *iit not conform
to its
origrnal shaPe whereas the brittle material will.
Bone
e.xhibits more brittte or more ductile behavior these loading modes- The folrowing
de- descriptions of
pelding on its age bl"being more these *d- appb' to strrcturr
9-o,*ger ducrile) in equilibri,.r* (at
and the rate at whidr it is loaded (b"i" rest or moring at a
I being more speed); toaaing prod,r..,
brittle at higher loading speeds). T"rTt
an internal deforrning effect'on the structure.
Because the stmchrre of Uor,e is dissimilar
in the
transverse and the longitudinal directions,
it exhibits Tersim
different mechariicat pioperties when
loaded along
different axes, a characteristic known Dudry teruile
as arrisotropy. .l*dTg, equal and opposite
Figure l-9 shows the variations in Ioads are applied outward Fo^ the strrface of the
strength and
sriffness for cortical bone samples stmchrre' and tensrle shess and
from a human strain result inside
femoral shaft, tested in tension in the sbnrchre- Tensrle stness can
four d.irections be thought of as
(Frankel and Burstein rg70). Erany small forces directed aw ay
, The 'alues for both from the surface of
parameters.T highest for the sampres the stnrchrre- ldaximal tensile
loaded in the stress occurs on a
longitudinal direcfion. Although pJT" perpsrdicular to the applied load (Fig. 1-11).
the relatior,ship be_
trveen loading_patterns and tf," under tens.le loading, the rt*.t ,,"
mechanical prop"r_ lengthens and
ties of bone throughout the narrows- At the microscopic level,
skereton is ..*t"*er), the far,rre mech-
compl€X, it cat g".'-*rally be said anism for bone tissue loaded in tension
that bone strength is mainlv
and stiffness are gre-atestin
the direction in which
loads are most co'uncnty
imposed (Franker and
Burstein, 1970).
-\-.-/
:>
BIOMECT{ANTCALBEFI,AWOR
OF -l;l
BONE LJ
- I

The mechanicalbehavior
ct
CN J">
of bone-its behavior UT
under the influence
of forces and moments-is
cc
F
Cn
57
aftected by its mechallcal
properties, its geometric I
characteriiHcs,the
luadi.g, and the
roading ;-,ode applied, the rate
fr"qr"ncy of loadirg.
of @
f T I
BON-EBEF{,AVIOR
UNDER VARIOUS
LOADING MODES STRATN
Ffc. t-9
Forces and moments Anisotroplcbe-avior of c3nicalbone
ture in various can b" to a stmc- specrmensftoma human
dite.dons, producing "pplied femoral s|Eft :esred in rension (puiledl
pression, 'torsion, tension, com_ in four direcrions:
bendi f,g, shear, fongirudinal(L,-:lted 30 cegreeswirh
loadits (Fig- and combined respec to g1eneuraf axrs
1- l0i. &rne in rivo is of dre bone. =:ed & decrees.and
subjected to all of rransversefTl. (Data from
Frankeland B,-iern . lg73 l
'tiil
t t
: 1

to oF TrssuEs
BtoMEcHANrcs ANDsrRUCfuREs SYSTEM
oF THEMUSCULOSKELETAL

v -.
UNLOADED TENSION C O M P R E S S I O NB E N D I N G

a a v
D-t:t F r G .| - 1 2

ryLt4
Reflectedlight photomicrograph of a human corficalbone
specimentestedin tension{30x }.Arrowsindicatedebondingat
the cementlinesand pullingout of the osteons.(Courtesyof
DennisR.Carter,Ph.D.)
->
SHEAR TORSION COMBINED
LOADING
F r G .I - l 0
of various loading modes.
Schematicrepresentation

debonding at the cement lines and pulling out of the

osteons (Fig. L-Lz).
Clinic ally, fractures produced by tensile loading
are usually seen in bones with a large ProPortion of
cancellous bone. Examples are fractures of the base of
the fifth metatarsal adjacent to the attachment of the
peroneus brevis tendon and fracfures of the calca-
neus adjacent to the attachment of the Achilles
tendon. Figure 1- L3 shows a tensile fracture through
the calcaneus; intense contraction of the triceps surae
muscle produced abnormally high tensile loads on
the bone.

F t G .I - t 3

nil
Tensilefracturethrough the calcaneusproduced by suong
contraction of the tricepssuraemuscleduringa tennismatch.
{Courtesy RobertA. Winquist,M.D.)
of

UU Compression
During compressive loading, equal and oPPo-
site loads are applied toward the surface of the
F t G .t - t l structure and comPressive stress and strain result
Tensileloading. inside the strucfure. Compressive stress can be
thought of as many small forces directed into the
 OF BONE
BIOMECHANICS ll

F l G .1 - t 4
ComPressive loading.

surface of the structure. Maximal compressive stress

occurs on a plane PerPendicular to the applied load
(Fig. 1,-1,4). Under comPressive loading the structure
shortens and widens. At the microscopic level, the
failure mechanism fof bone tissue loaded in comPres-
sion is mainly oblique cracking of the osteons (Fig.
1- 15).
Ctinically, compression fractures are commonly
found in the vertebrae, which are subjected to high
compressive loads. These fractures are most often
seen in the elderly, whose bones weaken as a
function of apng. Figure 1,-1,5 shows the shortetitg
and widening that took place in a human vertebra
subjected to a high comPressive load. In a joint,
compressivb loading to failure can be produced by
abnormally strong contraction of the surrounding
muscles. An example of this effect is Presented in
Figure L-L7; bilateral subcapital fractures of the
femoral neck were sustained by u patient undergoing F f G .t - 1 6
Compression fractureof a human first lumbar vertebra.The
electroconvulsive therapy; strong confractions of the
vertebrahasshortenedand widened.
muscles around the hip joint comPressed the femoral
head against the acetabulum.

F f G .t - 1 5
Scanningelectronphotomicrographof
a human coftical bone specimen
testedin compression {30x). Arrows
indicateoblique crackingof the os-
teons. (Courtesyof Dennis R. Carter,
Ph.D.l
 l2 OF TTSSUES
B|OMECHAN|CS AND STRUCTURES
OF THE MUSCULOSKELETAL
SYSTEM
F r G .| - t 7
Bilateraf subcapitalcompression of the femoralnecksin
fractures
a patientwho underwentelectroconvulsive therapy.
Shear
During shear loading, a load is applied parallel
to the surface of the structure, and shear stress and
strain result inside the structure. Shear stress can be
thought of as many small forces acting on the surface
of the structure on a plane Parallel to the applied load
(Fig. 1-18). A structure subjected to a shear load
deforms internally in an angular manner; right angles
on a plane surface within the strucfure become
obtuse or acute (Fig. L-L9). Whenever a structure is
subjected to tensile or comPressive loading, shear
stress is produced. Figure L-20 illustrates angular
deformation in structures subjected to these loading
modes.
Clinic ally, shear fracfures are most often seen in
cancellous bone. Examples are fracfures of the femo-
ral condyles and the tibial plateau. A shear fracture of
the tibial plateau is shown in Figure L-zL.
F t G .I - t 8
Shearloading.
l ' t i ,
li,1,
M,r;
L
BEFORELOADING UNDERSHEARLOADING
F f G .| - 1 9
When a structureis loaded in shear,lines originallyat right
angleson a pfane surfacewithin the structurechangetheir
orientation,and the angle becomesobtuse or acute. This
angular deformationindicatesshear strain. (Adapted from
, 11970.1
Frankeland Burstein
Human adult cortical bone exhibits different val-
ues for ultimate stress under compressive, tensile,
and shear loading (Fig. L-22). Cortical bone can
withstand greater stress in comPression than in
tension and greater stress in tension than in shear
(Reilty and Burstein, 1975). The value for the stiffness
of a material under shear loading is known as the
shear modulus rather than the modulus of elasticity.
Bending f.
In bendirrg, loads are applied to a structure in a
manner that causes it to bend about an axis. When a
bone is loaded in bendin1, it is subjected to a
combination of tension and comPression. Tensile
rtt
+++
t t t
+tt UNDER
COMPRESSIVE
UNLOADED UNDER LOADING
TENSILE
LOADING
FtG. | -20
Thepresence of shearstrainin a structurefoadedin tensionand
in compression is indicatedby angulardeformation.(Adapted
from Frankeland Burstein,1970.'l
 w'
'&,
,1,'t$,
i : OF BONE
BOMECHANICS | 3
::aattk
':.:.i;l+i

':::,
rffi
::::l:tl,!1.

',::,.:'"4i
'a::l::a'::t,
stresses and strains act on one side of the neutral axis,
ffi
,ffi and compressive stresses and strains act on the other
;i.'i:r ll'
!# side (Fig. 1,-23); there are no stresses and strains
along the neutral axis. The magnitude of the stresses
,ir;:;ti;

is proportional to their distance from the neutral axis

,ifirl
ft
:;:::,{i
of the bone. The farther the stresses are from the
# neutral axis, the higher their magnitude. Because
,,,.,:.,::
l,::,i,!E
bone is asymmetrical, the tensile and comPressive
'::#
,'"',,',' stresses may not be equal.
:: rj:itii_i':

Bending may be produced by three forces (three-

i

::;ilPi:. point bending) or four forces (four-point bending)

.f,fi
,:i:i.t

(Fig. 1,-24). Fractures produced by both tyPes of

::ili::Fi

..i...-.i$i' bending are commonly obsenred clinically, Particu-

,:,ii,it,
'# larly in long bones.
ft Three-point bending takes place when three forces
';*j
1,.r,,|,!i acting on a structure Produce two equal moments,
,$
"1f9't
each being the product of one of the two peripheral
E forces and its perpendicular distance from the axis of
,'*i rotation (the point at which the middle force is
.' applied) (see Fig. 1,-24A). If loading continues to the
j n
FfG. | -21 yield point, the structure, if homogeneous and sym-
,t=i1i
t,,
'$ Shearand compressionfractureoF the lateraftibial plateau. metrical, will break at the Point of application of the
:E {Courtesy of StevenLubin,M.D.) middle force.
',ti$i A typical three-Point bending fracture is the "boot
top" fracture sustained by skiers. In the "boot toP"
-if fracture shown in Figure 1 -25, one bending moment
'tfi acted on the proximal tibia as the skier fell fonnrard
H
loo
i,ii over the top of the ski boot. An equal mornent,
# produced by the fixed foot and ski, acted on the distal
.ii
F 150 tibia. As the proximal tibia was bent fonvard, tensile
c =
ct) z stresses and strains acted on the Posterior side of the
fr 1oo a bone and compressive stresses and strains acted on
cr a
F U)
z the anterior side. The tibia and fibula fractured at the
;ii ct) tU
E. o top of the boot. Since adult bone is weaker in tension
-$ o- ct)
z
tr
tU than in compression, failure begins on the side
:r$j o uJ
'i+
O F a subjected to tension. Immature bone may fail first in
iliirLi,$
:;,i:
FfG. | -22 compression, and a buckle fracfure may result on the
ifl
,i$ Ultimate stressfor human adult corticafbone specimenstested compressive side.
iii
in in compression,tension,and shear {averageof data from Reilly Four-point bending takes place when two force
and Burstein, 1975l|.shaded area indicates ultimate stressfor couples acting on a structure produce two equal
i+i
iiir.:
human aduft cancellousbone with an apparent densiryof 35o/o moments. A force couPle is formed when two parallel
tested in tension and compression {Carter,1979). forces of equal magnitude but oPPosite direction are
.i:i:

lii
'1,-248).
$ applied to a structure (see Fig. Because the

FfG. | -23
Cross section of a bone subjected to bending, showing
distribution of stresses around tne neutral axis. Tensile

r#
stressesact on the Superiorside, and compressiveStresses
act on the inferior side. The stressesare highest at the
peripheryof the bone and lowest near the neutrafaxis.The
tensile and compressiveStressesare Unequal because the
bone is asymmetrical.
l4 OF TISSUES
BIOMECHANICS AND STRUCTURES
OF THE MUSCULOSKELFTAL
SYSTEM

FrG.| -2+
Twotypesof bending.A.Three-point B.
bending.
Four-pointbending.
A

rnagnitude of the bending moment is the same Torsion

throughout the area between the fwo force couples,
In torsion, a load is applied to a structure in a
the stmcture breaks at its weakest point. An example
manner that causes it to twist about an axis, and a
of a four-point bending fracture is shown in Figure
torque (or moment) is produced within the structure.
I-26. A stiff knee joint was manipulated incorrectly
When a strucfure is loaded in torsion, shear stresses
during rehabilitation of a patient with a femoral
are distributed over the entire structure. As in
fracture. Duting the manipulation, the posterior knee
bendin1, the magnitude of these stresses is ProPor-
joint capsule and tibia formed one force couple and
tional to their distance from the neqtral axis (Fig.
the femoral head and hip joint capsule formed the
L-27). The farther the stresses are from the neutral
other. As a bending moment was applied to the
axis, the higher their magnitude.
femur, the bone failed at its weakest point, the
Under torsional loading, maximal shear stresses
origrnal fracture site.
act on planes parallel and PerPendicular to the
neutral axis of the structure. In addition, madmal
tensile and compressive sfresses act on a plane
diagonal to the neutral axis of the structure. FigUre
1-28 illustrates these planes in a small segment of
bone loaded in torsion.
The fracture pattern for bone loaded in torsion
suggests that the bone fails first in shear, with the
formation of an initial crack parallel to the neutral axis
of the bone. A second crack usually forms along the
plane of maximal tensile stress. Such a pattern can be
seen in the experimentally produced torsional frac-
fure of a canine femur shown in Figure L -29.

Combined Loading
Although each loading mode has been consid-
ered separately,living bone is seldom loaded in one
mode only. Loading of bone in vivo is complex for
FrG. | -25 two principal reasons: bones are constantly subjected
Lateralroentgenogramof a "boot top" fractureproducedby to multiple indeterminate loads, and their geometric
of RobertA. Winquist,M.D.)
three-pointbending.(Courtesy strucfure is irregular. Measurement in vivo of the
 BIOMECHANICSOF BONE T5
"ffi
#
E
ffi
#
SHEAR

# COMPRESSION

$
ff
H TENSION

€
,# FfG. | -28
Schematic representationo1'asmallsegmentof bone foadedin
$ torsion.Maximal shear stressesact on planes paralleland

tr
i,F
'ff
perpendicular
sivestresses
to the neutralaxis.Maximaltensifeandcompres-
act on planesdiagonalto this axis.
sl
!*
s
#
s
S*.
tr
*
ffi
w
*
s
$
ffi
H
*
d FrG.| -29
# AB Experimentalfy producedtorsionalfractureof a canine femur.

ffi FfG. | -26 The short crack(arrow)parallefto the neutralaxis represents

w
ffi
r{. Duringmanipulationof a stiff kneeduring fracturerehabili-
tation,four-pointbendingcausedthe femur to fractureat its
weakestpoint, the originaffracturesite.B. Lateralroentgeno-
axisrepresents
angleto the neutraf
shearfailure;the fracturefineat a 30-degree
the pfaneof maximaltensifestress.

& gramof the fracturedfemur.{Counesyof Kaj Lundborg,M.D.)

strains on the anteromedial surface of a human adult

* tibia during walking and jogstg demonstrated the
s'
#
as complexity of the loading patterns during these
fs
.itr common physiologic activities (Lanyon et dl., 1975).
ffi Stress values calculated from these strain measure-
'*:
,& ments by Carter (1978) showed that during normal
'ffi walking the stresses were comPressive during heel
i€
strike, tensile during the stance phase, and again
ffi
compressive during push-off (Fig. 1-30A). Values for
r#
:* shear stress were relatively high in the later portion of
w the gait cycle, denoting significant torsional loaditg.
#
$
This torsional loading was associated with external
,& rotation of the tibia during stance and push-off.
iql FfG. | -27
:.* During jogpng the stress pattern was quite differ-
,& Crosssection of a ryfinder loaded in torsion,showing the
,# ent (Fig. 1-308). The compressive stress predomineit-
tr
tr
'.9
distributionof shear stressesaround the neutral axis. The
magnitudeof the stressesis highestat the peripheryof the
ryfinder and fowestnearthe neutralaxis.
ing at toe strike was followed by high tensile stress
during push-off. The shear stress was low through-

$
t*.
s
w
,ffi
.s
I
g
s
.*d

$
l6 EIOMECI{ANIC5CF NSSUES
AND SIRUCTURES
OF T}JEMUSCULOSKELEI'AL
SYSTEM

WALKING (1.4 m/sec) 12

4 JOGGING (22 m/sec)
STRESS
_- TENSTLE -
3
-.- @UPRESSI\IE STRESS
- SIGAR (EXTEF
RNAL ROTATION}
2 .

ll
-IE}ISiLE
G. -.- @UFRESSIVE
o-1 - $€An GXTERI{AL ROTATIOiO
3 I
E o r
l,n t.u e6
- slGAlR (INTERNAL ROTATION)

ut i It i'.. r o-
It t a
P'
l'..1
E
a

t --j
F1 il
l -

It | ."1i
-rt
CT' a

I It l

ll
a

E 4
\.ot o I i".. .i'i UJ
l . a

.ii E
| \4.. 'fi F
I
tt t\ t
(t,
I
t a

t'- t 2
I
I i -t

I
a [, \/ \
HS FF FIO S
HO TO
A

TS TS.TO
B
FrG.| -30
11. Calculatedsucses on the ancromedial conex of a hurnan adult tibia durirg wdking.
HS-heel strike:FF-foot llat; FlO-heel-ofr TO-toeofr S-virq. {After|.arDonet al..
1975;counesyof DennisR C-aner,Ph.D.lB. Calculated$resseson fte anteromedialcortexof an
aduft human tibb during jqgirg.TS-toe srike; TO-toeotr hfter Lanlon et al- 1975;
courtesyof DennisR.Caner,Ph.D.l t

out the stride, denoting minimal torsional loading or eliminates tensile sress on the bone by producing
produced by slight external and internal rotation of compressive stress that neutralizes it either partialll'
the tibia in an alternating pattern. The increase in or totally.
speed from slorv walking to jogpng increased both The effect of muscle contraction can be illustrated
the stress and the strain on the tibia (I-anyon et al., in a tibia zubjected to three-point bending. Figure
L975). This increa* in strain with greater speed was 1-31A represents the l"g of a skier who is falting
confirmed in studies of locomotion in sheep, which forward, zubjecting the tibia to a bending moment.
demonstrated a fivefold increase in strain values from High tensile stress is produced on dre posterior
slow walking to fast trotting (Lanyon and Bourn, aspect of the Hbda,and high compressive stress acts
1979). on the anterior aspect. Contraction of the triceps
Clinical exarrrination of fracture patterns indicates surae muscle produces great comPressive stress on
that few fractures are produc€d by one loading mode the posterior aspect (Fig. 1-3lB), neutralizt4g the
or even by hvo modes. lndeed, most frachrres are great tensile sfress and therebv protecting the tibia
produced Ly cornbination of severalloading modes. from failnre in tension. ThiS musde contraction may
" result in higher comprressivestress on the anterior
strrface of the tibia. Adult bone can usually withstand
INFLUENCEOF MUSCLEACTIVIW ON this stress, but imrnahue bone, which is weaker, rnay
STRESSDISTRIBUTIONIN BONE fail in compression.
Musde contraction produces a similar effect in the
When bone is loaded in vivo, contraction of the hip joint (Fig. 1-32). During locomotion, bending
musdes attached to the bone alters the stress distri- moments aneapplied to the femoral neck and tensile
bution in the bone. This musde contraction decreases stressis produced on the superior cortex- Contraction
 EfoMECFr N|CSOF BONE l7

t
of the gluteus medius musde produces compressive
stress that neutralizes this tensile stress, with the net
result that neither compressive nor tensile stress acts
on the superior cortex. Thus, the uruscle contraction
allows the femoral neck to zustain higt er loads than
would otherwise be possible-

RATE DEPENDENCYIN BONE

Because bone is a viscoetasfic material, its

biomechanical behavior varies with the rate at which
the bone is loaded (Le., the rate at rryirictrthe load is
applied and removed). Bone is stiffer and sustains a
higher load to failure when loads are applied at
AB higher rates. Bone also stores morre energy before
FfG. | -3 | failure at higho loading rates, provided tnat these
A. Disribmion of cornpressir'eaN tersite $ressesin a dbia rates are within the physiologic range.
subleced to firee-point bending. 8. Conracion of trre riceps The loaddeformation curves in Figure l-33 show
suraemuscle produceshigh cqnpressirrre$rcss on trte po*erior the difference in the mechanical properties of paired
aspecLneuualang dre hgh tensilestress. canine tibiae tested in vitro at a high and a very low
loading_rate, 0.01. second and 200 seconds, respec-
tively (Sammarco et aI., l97L)- The amount of enirry
stored before failure approximately doubled at tfie
higher loading rate. The load to failure almost
doubl€d, but the deformation to failure did not
change significantly. The bone was about sa% stiffer
at the high"r speed.
The loading rate is dinically significant because it
influences both the fracture pattern and the aurount
of soft tissue damage at fnacture. When a bone
fracfures, the stored energy is released. At a low
loading rate, the ener6y can dissipate through the
formation of a single crack; the bone and soft tissues

LOADING RATE O.O1SEC

o
o
J

FtG. I _32
stresscrsrnbuuonin fernoral DEFORTATION
a rrecksubjecredto bending.when FfG. r -33
ine -oluteusrnecrus
muscreis refaxedfopl. tensilestressacE on Rate dependency of bone is demonsrrated in paireC canine
ine sucerlorcorTex
and compressivesress acE on dre inferior ubiaetestedat a high arrt a low foad,ngrare-The foad ro failure
cciex' conc'acton
':lieSS. of drismuscle(bonomfneuralizestrle tensile andthe energystoredro faifureafrpst doubled at d'rehigh rare.
lAdaptedftom Sammarcoer al., lg7l.l
 T8 BIOMECHANICS
OF NSSUES
AND STRUCIUREs
OF THE MUSCULOSKELETAL
SYSTEM

FtG. | -34
Human tibia experimentafly testedto
failurein torsionat a high loadingrate.
Displacementof the numerousfrag-
mentswas pronounced.

remain relatively intact, and there is little or no
displacement of the bone fragments. At a high
loading rate, however, the greater energy stored
cannot dissipate rapidly enough through a single
crack, and comminution of bone and extensive soft
tissue damage result. Figure 7-34 shows a human
tibia tested in vitro in torsion at a high loadin g rate;
numerous bone fragments were produced, and dis-
placement of the fragments was pronounced.
Clinic ally, bone fractures fall into three general
categoriesbased on the amount of energy releasedat
fracture: low-en ergf , high-energy, and very high-
energy. A low-enerry fracture is exemplified by the
simple torsional ski fracture; ahigh-energy fracture is
often sustained during automobile accidents; and a
very high- energy fracture is produded by very
high- muzzle velocity gunshot.
only a small proportion of the total energy storage
capacity of bone is utilized during normal activity.
Figure 1-35 illustrates just how little of this capacity
is used during the normal physiologic activity of
jogsrg.

U)
FATIGUEOF BONE UNDER
@
ut
REPETITIVE
LOADING
E
F
a Bone fractures can be produced by u single load
that exceeds the ultimate strength of the bone or
by repeated applications of a load of lower magni-
PHYSIOLOGIC tude. A fracture caused by repeated applications of
a lower load is called a fatigue fracture and is Vpi-
STRAIN cally produced either by few repetitions of a high
FrG.I -35 load or by many repetitions of a relatively normal
Tensilestrainvaluesfrom a human adult tibia duringlogging load.
{Lanyonet al., 19751havebeen pfottedon a stress-strain curue The interpluy of load and repetition for any
for bone samplestestedto failurein tension.A smallproponion material can be plotted on a fatigue curye (Fig. l-g1).
of the totalenergystoragecapacityof the boneis utilize
d during For some materials (some metals, for example), the
this normalphysiologicactiviiy. fatigue curve is asymptotic, indicating that if the load
 OF EONE
BIOMECFTANICS l9
fracture in the lower extremities is outlined in the
following schema:

o
o
J STRENUOUSEXERCISE
I
FATIGUED IIUSCLE
\'
^/-
7

REPETITIO}.I
FtG. t-lE--
Loss oF sHo{ }1.RED GAfr
The inrerplayof load dfr repetidm is represen*ct qt a faog* AITSOREING.CIPACITY
/
CUn/€.
\/
ABNORMAL
LOADING

is kepl below a certain level theoretiolly,

material will remain intact, no matter how many
tre
I
ALTERED STRESS OISTRIBUTION

repetitions. For bone tested in vito, the curve is not

/
asymPtotic- When bone is s,tbiected to repetitive low HIGH COMpRESStOfTf
+ COMBTNED-6Gg TENSION
loads, it may sustain fatigue microfractires (C-arter taow -pRocESS- FAST
I I
and Hayes, l9T7a). Testing of bone in vitro also
reveals that bone fatigues rapi<tly nrhen load or
deformation aPProadres the )aeld strength of the
I
OBUQUE CRACKS
I
I
DEBONDING OF OSTEONS
bone (Carter and Hayes, l9i7a); that is, tfre nnrrrber I TRANSVERSE CRACKS
I
of rePetitions needed to produe a fractr:re dimin-
ishes rapidly.
I
OBLIQUE FRACTURE
I
TRANSVERSE FRACTURE
In repetitive loading of living bone, the fatigue
Processis affected not only by the arnount of load i"a
the number of
-t"P"titions b'trt afso by tt* nrrnber of
applications of the load rrithin a gro, time (fte-
INRUENCE OF BONE GEOMETRY
qu-encyof loading). sin-celiving bon"L selt-r€pairing,
a fatigue frachrre results onlir,nhen the ,e-bdeling
ON BIOMECI{ANICAL BEFI,AVIOR
Processis outpaced by the f",is"e process, Le., rvhen The teometry of a bone greatly influences its
loading is so freg.r"t i that it
irerrudes the remodel- meclranical behavior. In tension a'd compression,
lng necessary to prrevent faillrrre.
the load to failure and the stiffiress are proportional
Fatigue fractures :rre 'sually' zustained
drrring to the cnoss-sectional area of the bone. ft e larger
continuous strenuo's physical
which cluses the :rnea is, the stronger and stiffer the bone. I"
the muscles to become r"ugu"d "cti"ity,i reduces
their bending, both the cross-sectional :uea and the
ability to contract- As a r"tirt "t ane less able
thev to distribution of bone tissue around a neutral axis
store enerty and thus to
neutrilize the stresses affect the bone's mechanical behavior. The quantilv
imposed on the bone. The
resulting alteration of the that takes into account these two factors in bending
stress distribution in the
bone cluses abnormally is called the area moment of inertia. A laqger anea
nrgn loads to be
L ' r i

Tposed, and a fatigue fract're may moment of inertia results in a stronger and stiffur
result- Bone f"il on the tensile sile, the comp'es-
T"y
sive side, or uour bone.
sides. Failure on the tensile side Figure t-37 shows the influence of the area
results in a transverce
sack, and,'the bone proceeds moment of inertia on the load to failure and the
rapidly to complete
fractrrre. Fatsue fract'res on the stiffness of three rectangutar stmcj1rres that have the
comPressive
a.ppearto_b" produced rnore srowly; same :rrieabut different shalres. tir uending bea' Itr
the remodeling Id:
is less easily oltp"ced
and the bone -"i; h. th" fatigue is the stiffest of the three and c:ln wi**tana the

t [:H::: i**d-to complete highest load, because the greatest asrount of material
This theory of muscle is distributed at a distance from the neutral anis. For
iatigue as a cause of fatitue rectangular cnoss sectiors, the forrrrula for the anea
20 BIOMECI.IANIG OF I65UE5 AND STRUCTURES
OF fiE MUSCT'LOSKELETAT
SIsIEM

FfG. | -37
Three beams of equal area brx different
shapessubjecredto bending. Fs recangular
ooss secdors. fie area moment of inerua is
B:
cahrlarcd ry fie formura $ rahere B is
t2
tfn widtrt aN H. trte height The area
mqnent of inenia for beam I is elZ: for beam
tf, lUlZ: aN for beam ltl. 64112.[Adapred
fiorn FrankefaN Bursrein l970-t

2x2 1x4
ll til

moment of inertia is the width (B) multiplied by the
cube of the h.ight (H1 dividedby 12:
B.H3
t2
Because of its large area moment of inertia, beasr III
can wiftstand four times more load in bending than
bearn I-
A third facbr, the length of the bone, influenc€s
the strength and stiffness in bending. The longer the
bone is, the greater the magnitude of the bending
moment caused by the application of a force. In a
rectangutar stnrcture, the magnitude of the stresses
produced at the point of application of the bending
moment is proportional to the length of the stmcttrre.
Figure l-38 dqplcts the forces acting on two beams
wift the same width and height but different lengths:
beam B is twice as long as bearn A. The bending
moment for the longer beasr is twice ilrat for the
shorter bearu coruiequently, the stress magnitude
ttuoughout the beam is twice as high.
Becauseof their leogth, the long bones of the skel-
eton are subjected to high bending moments and, so,
high teruile and compressive stresses. Their tubuiar

BEAM A STRESS FlG. | -39

=S
MAGNITUDE Eearn B is rwice as fong as beam A and
sr.rsEinstwice fie berxling momenl Hence.
fie $ress rnagniude firo4hour beam B is
twice as high. fAdapred from Frankel and
Bur$ein. 1970.1
-.
BEAM B L-.-J
I
STRESS
= 2S
MAGNTTUDE
 OF BONE
EIOMECFdAT'.IICS 2l
shape gives them the ability to resist bending mo-
ments in all directions. These bones have a large area
moment of inertia becausemuch of the bone tissue is V
(-
distributed at a distance from the neutral a)ds.
The factors that affect bone strength and stiffness
in torsion are the same ones that operate in bending
the cross-sectional area and the distribution of bone
Hssuearound a neutrial axis. The quantity that takes
V .A\

into account these two factors in torsiornl loading is

the polar moment of inertia. The larger the polar .-.
Fv

moment of inertia is, the stronger and sfitrd the

' \-o'rl
bone.
Figure 1-39 shows distal and proximal cnoss
sections of a tibia subjected to torsional loading.
Although the proximal section has a slightly suraller
bony area than does the distal section, it tras a much
higher polar moment of inertia becausemuch of the
bone tissue is distributed at a distance from the
neutral ilds. The distal section, while it has a larger
bony area, is subjected to much high"r shear stress
becausemuch of the bone tissue is distributed close
to the neutral axis. The magnifude of the shear stress
in the distal section is approximately double that in
the proximal section. Clinically, torsiornl fractrrres of
the tibia conrmonly occrr distally.
when bone begins to heal after ftactnre, blood
vessels and connective tissue from the periosteusr
migrate inlo the region of the fracture, forrting a cuff
of dense fibrous tissue, or callus, anound the fr"ct rru
site, which stabiti-es that area (Fig. l-40A). The
callus significantly increases the ate and polar
moments of inertia, thereby increasing the strength
and stiffness of the bone in bending and torslon
during the healing period. As the fracture heals and
,h: bone gradually regains its norrnal strength, the
callus cuff is progressively resorbed and th" bone
returns to as near its normal size and shape as
possible(Fig. l-4OB).
certain surgical procedures produce defects that
greatly weaken the bone, partiarlarty
in tonsion.
These defects fall into two categories: those
whose
length is less than the diameteiof
the bone (stress
raisers) and those whose length
exceeds the bone
diarneter(open section defects).
\\-/
\
B
FfG. t -39
Disribtttion of sfiear stress in two cross secrions of a ribia
subjeced to tqsirnal loadlng. The proximaf section (Al fras a
higher morrfem d Frnia dran does fre disal secion (Bl.
becausemore Wry nEterial is distributed away from trre netrral
axis. fAdaptedfun frankel and Bursrein, l971.l
1-41). The wealcening effect of a stress raiser is
partictrlarly marked under torsional loading the total
decrease in bone strength in this loading mode can
reach 60Vo.
Bnrstein and associates (1972) showed the effect of
stress raisers pTdrced by screws and by empty
screw holes on the eneqty storage capacity of rabbit
bones tested in torsion at a high loading rate. The
immediate eftct of drilling a hole and inserting a
scnewin a rabbit femnr was a74vo decrease in energy
storage capacity. After 8 weel$, the stress raiser effect
produced W the scrervrsand by the holes without
scrrewshad disappeared completely because the bone
had resrodele& bone had been laid down around the
screws to stabilize them, and the empty screw holes
had been fiUed in with bone. In femora from which
the screws had been removed immediately before
testing howetrer, the energy storage capacity of the
bone decreased by 50%, mainly because the bone
tissue arund the scnew sustained microdamage

o'.t"'I,Til:T
::HllH:
: :HffiffiH il*
strength is reduced because
during screw removal (Fig. !-42).
An open section defect is a discontinuity in the
the stresses imposed bone caused by s,rrgrcal remorral of a piece of bone
during loading_are prevented
from beirg distributed longer than the bone's diameter (for example, by the
s1'ehlt throufhout the
bone and instead become ctrtting of a slot during a bone biopsy). Because the
concentrated around
the defect. This defect is anaL outer surface of the bone cross section is no longer
.Bousto a rock in a stream, which
producing high diverts the water, continuous, the bone's abitity to resist loads is
water turburence around it (Fig. dtered, partiorlarly in torsion.
22 BIOMECHANICS
OF NSSUES
AND STRUCTURES
OF THE MUSCULOSKELF|AL
SYSTEM

FtG. | -40
A, Earlycallusformation in a femoraffracturefixed with an
intramedullary
naif.B, Nine monthsafterinjurythe fracturehas
heafedand mostof the calluscuffhasbeenresorbed.{Counesy
of RobertA. WinquistM.D.)

o.o<-.oEMPWSCREWHOLE
}.'o- < SCREWIN PLACE
o SCREW REMOVEDAT TESTING

E
o
E
(f

(,
tr
[rJ
z
I.IJ

012345678
WEEKS
FfG. | -41 FtG. | -42
Stressconcentrationaround a defecg such a defect is analogous Effectof screwsandof emptyscrewhofeson the energystorage
to a rock in a stream. capacityof rabbit femora.The energystoragefor experimentaf
animalsis expressed as a percentageof the total energystorage
capacity for controf animals. When screws were removed
immediatelybefore testing,the energy storagecapacityde-
creasedby 50o/o.(Adaptedfrom Bursteinet af., 1972.)

In a normal bone subjected to torsion, the shear
stress is distributed throughout the bone and acts to
resist the torque. This stress pattern is illustrated in
the cross section of a long bone shown in Figure
1-43A. (A cross section with a continuous outer
surface is called a closed section.) In a bone with an
open section defect, only the shear stress at the
periphery of the bone resists the applied torque. As
the shear stress encounters the discontinuity , it is
forced to change direction (Fig. L-438). Through-
 OF BONE
BIOMECHANICS 23

1n
as
'rr/(
sy
,nrN
__:
\t'Y'// \t
I

A B
FtG. | -43
Stresspatternin an open and closedsectionunder torsional
loading.A. In the cfosedsection,allthe shearstressresiststhe
appliedtorque.B. fn the open section,onfythe shearstressat
the peripheryof the bone resiststhe appliedtorgue.{Adapted
from Frankeland Burstein,1970.1

out the interior of the bone, the stress runs parallel to

to the applied torqu€, and the amount of bone tissue
resisting the load is greatly decreased.
In torsion tests in vitro of human adult tibiae, an
open section defect reduced the load to failure and
energy storage to failure by as much as 90%. The
deformation to failure was diminished by about 70Vo
(Frankel and Burstein, 1970) (FiS. 1-M).
Clinically, surgical removal of a piece of bone can
FlG. | -45
greatly wdaken the bone, particularly in torsion. A patient sustained a tibial fracture through a surgically
Figure 7-45 is a roentgenogram of a tibia from which produced open section defect when she trippeda few weeks
a graft was removed for use in an arthrodesis of the after operation.
hip. A few weeks after operation, the patient tripped
while twisting in an attempt to rescue the Christmas
ham from toppling onto the floor, and the bone
fractured through the defect.
BONE REMODELING
Bone has the ability to rernodel, by altering its
size, shape, and structure, to meet the mechanical
demands placed on it. This phenomenon, in which
CONTROL bone gains or loses cancellous and/or cortical bone in
response to the level of stress sustained, is summa-
rized as Wolff 's law, which states that bone is laid
3 down where needed and resorbed where not needed
rf o
(Wolff , 7892).
3 o
If, because of partial or total imm obllization, bone
1
is not subjected to the usual mechanical stresses,
periosteal and subperiosteal bone is resorbed (Jenkins
and Cochrdn, 7969) and strength and stiffness de-
crease. This decrease in bone strength and stiffness
DEFORMATION
I was shown by Kazarian and Von Gierke (1969), who
FtG. | -+4
3 Load-deformation curves for hum an adult tibiae tested in vitro
irnmobilized Rhesus monkeys in full-body casts for 60
) under torsionalloading.The control curverepresentsa tibia with days. Subsequent compressive testing in vitro of the
) no defecg the open section curye representsa tibia with an open vertebrae from the immobilized monkeys and from
section defect. (Adapted from Frankel and Burstein,1970.1 controls showed up to a threefold decrease in load to
 24 BIOMECHANICS
OF TISSUES
AND STRUCTURES
OF IHE MUSCULOSKELETAL
SYSTEM

fracture
hadheared.
Theboneunderth" il#fiJ$,
o
o :Jff:
andthel",: of"-ff]:
* 3:l^?
diameter :l r:- resorb#
q-""i"dt
Fudiaphysis bu.u*L
ryi:ffi
aium
Hit*:';decrea
greatly *fj"::'^": : s:*-'l
sesbone :! "parricular;
trength, ":;i,,.u ;f et
:,^rl#ol."Jit" ;F; il ;;i;'_"
i:T:-#
IMMOBILIZED
ilg#i. 1o,,1:o-1
moments of inertia. A 2AVodecrease
in bone diamerurtt#

ilT#iH"',i"":":ffi1'1,1",H"
suggest that rigid plates should 'fi
DEFORMATTON be removea shortly J*
Ffc. | _+6 hearedulJ beroreii; bone
Load-deformation
curuesfor vertebral
segmenEL5to L7 from diminishedin size.sucha ,cecr";;;ffi: has '
{t:::^[::yl:,lf
markedly
normal and immobilizedRhesus "J
monkeys.fAdaptedfrom
:i:" which
*_i:l"l1m::Tl_"Tud bysecondary
osteoporo_
*
Kazarian andVonGierke,..969.) sis, further#eakensinu-;;;;i6rrnr:i[:;
1vr'*Lrtr (tL dr', tt;
1980)

An imprant may cause bone hypurfrophy

attachment sites el exampre at its
failure uld energy sjolage capaciv of bohe hypertrophy
in the vertebrae around screws is illusfrated in
that had been immobilizEd, ,,iffr,um Figure r-4g. A nail
was also signif_ plate was applied to a femoral
icantly decreased(Fig. I_4'6). neck fracture, and the
An implant that remains firmry bone hyperirophied around the
attachedto a bone screwsin responseto
after a fracfure has healed may the increased road at these
arso diminish the sites Hrpertrophy may
strength and stiffness of the bone. also result if bone is repeatedry
In the case of a ,"u;".ted to high
plate fixed to the bone with screws, mechanical stresses within the
the plate and the normal physiologic
bone share the road range. Hypertrophy ofnormal
adult bone in response
geometry and materiall'.proporuons det"r*i'ed by the to strenuousexerciiehas been
p-ropertiesof eachstructure. A observed(Joneset ar.,
large plate, carryilg high t,ouJr, 7977; Dal6n and Olsson, I9T4;
unroads the bone to Huddleiton et aI.,
a great extenu the bone then atrophies 7980)'as has an increasein bone
in responseto density
---'d.'-
(Nilsson and
this diminished load. (The bone Westlin, 1g7I).
may hypertrophy at
the bone-screw interface in an 1-potitive correlation exists between bone mass
attempt to reduce and body weight. A greater
micromotion of the screws.) body weight has been
Bone resorption under a prate associatedwith a largei bot
is ilrustrated in mass(Exne"ret ar.,i,g7g).
Figure 1-47 ' A compressionplate conversely, a proloriged condition
"
made of a material of weightlessness,
such as that experienced ,curing
space travel, has

FtG. I _47
AnteroposteriorIAt andlateraltBf roenrgenogramsof an ulna
afterplate removalshow a decreased
bone diameterdue to
resorptionof the bone under
the plate. cancelfizatianof the
cortexandthe presenceof screw
horesarsoweakenthe bone.
{Courtesy of MarcMartens,M.D.f

,i;
B
L
 oF BONE
BloMECHANlcs 25

been found to result in a decreased bone mass in

weight-bearirg bones (Rambaut and |ohnston, 1979;
Gazenkoet dl., 1981).

DEGENERATIVE CI.I,ANGESIN BONE

ASSOCTATEDWITH AGING

A progressive loss of bone density has been

observed aJ part of the normal aging Process. The
longitudinal trabeculae become thinner, and some of
the transverse trabeculae are resorbed (Siffert and
Levy, 1981) (Fig. I-49). The result is marked reduc-
tionin the amount of cancellous bone and thinning of
cortical bone. This decrease in the total amount of
bone tissue and the slight decrease in the size of the
bone reduce bone strength and stiffness.
Stress-strain curves for specimens from human
adult tibiae of two widely differing ages tested in
tension are shown in Figure 1-50. The ultimate stress
was approximately the same for the young and the
old bone. The old bone specimen could withstand
only half the strain that the young bone could,
indicatitg greater brittleness and a reduction in
energy storage caPacitY.
''
FfG. | -+8
Roentgenogramof a fracturedfemoral neck to which a nail plate
was applied. Loads are transmittedfrom the plate io the bone
via the screws.Bone has been laid down around the screws to
bear these loads.

j'ffi
qffiffin
lu4l
tnn c
A B
FtG.t-49
Vertebralcrosssectionsfromautopsyspecimens of young fAf and old lBf boneshow a marked
reductionin cancellousbone in the latter.(Reprinted with permissionfrom Nordin, B.E.C.:
MetabolicBoneand StoneDisease. Edinburgh,ChurchillLivingstone, 1973.1
C. Bonereduction
depicted.As normalbone (top)is subjectedto absorption{shaded
with aging is schematically
areafduringthe agingprocess,the longitudinaltrabeculaebecomethinnerand sometransverse
trabeculaedisappear{bottom).(Adaptedfrom Siffertand Levy,1981.)
 26 BIOMECI{ANICS
OFNSSUES
AND STRUCruRE
OFTHEMTSCULOSKEI..ETAL
SYsTEM

o
q,
trJ
cE
F
o

FtG. | -50
stress-srain cun es for sampfg of aduft lrurnan dbbe of nno
vudely differing ages tested in tersion. (Adapredfiom Br.rrsrein
et
al., 1976.1

SUMII/IARY

1. Bone is a two-phas€ composite material, inor- produced by a combination of seneral loading

ganic mineral salts b.irg one phase and an modes.
organic matrix of collagen and ground strbstancre 6. Musde contraction affects stress patErns in bone
the other. The ino€anic component makes bone
by producing compressive stress that partially or
hard and rigtd, whereas the oqganic component totally nzutralizes the tensile stress acting on the
gives bone its flexibility and resilience.
bone-
2- Microscopic"fly, the fundarnental stmctural unit
7. Bone is stiffer, sustains higher loads before
of bone is the ost@n, or haversian qlsteul, failing, and stores morre energ:r wherr loaded at
composed of conc€ntric layers of mineralized high"" rates.
matrix srurounding a central canal containing
E. Lirirg bone fatigues wher. the fnequencv of
blood vessels and nerve fibers.
loading precludes the remodeling necessarv to
3. Macroscopic"lly, the skeleton is composed of
prevent f,ailure.
cortical and cancellous bone. Bone of both t,"es
9. The mechanical behavior of a bone is influenced
can be considered as one material whose potoiity
by its geometry Oength, cross+ectional area, and
and density vary over a wide range. .
distribution of bone tissue around the neutral
4. Bone is an anisotropic material, exhibitirg differ-
axis).
ent mechanical properties when loaded in differ-
10. Bone remodels in response to the mechanical
ent directions. Mahre bone is strongest and
demands placed on it; it is laid down where
stiffest in .9-pression.
needed and resorbed where not needed.
5. Bone is subjected to complex loading patterns
11. with agng there is a marked reduction in the
dtrring courmon physiologic activities luch :rs
amount of cancellous bone and a decrease in the
walking and jogging. Most bone fracttrres ane
thicrcnessof cortical bone. These .h*ges dimin-
ish bone strength and stiffness.

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