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J. Biomechanws, 1976. Vol. 9. pp. 27-M. Pcrgamon Press.

Printed in GreatBr~ra~n

FATIGUE LIFE OF COMPACT BONE-I


EFFECTS OF STRESS AMPLITUDE,
TEMPERATURE AND DENSITY”?
D. R. CARTER and W. C. HAYES
Department of Applied Mechanics, Stanford University, Stanford,
California 94305, U.S.A.

Ah&act-Fatigue tests to failure of compact adult bovine bone specimens were conducted at five
stress amplitudes (65-108 MN/m’) and four temperature levels (21-45”C) which span the physiologic
range of bone temperature in the human foot. After testing, determinations were made of specimen
density and microstructure and fracture surfaces were examined by scanning electron microscopy. The
test results demonstrated highly significant (P < 001) negative correlations between fatigue life and
stress amplitude and between fatigue life and temperature. A highly significant positive correlation
between fatigue life and bone density was also shown. The microstructure studies indicated that primary
compact bone has a longer fatigue life than secondary Haversian bone. A multiple regression analysis
was used to derive an equation for fatigue life as a function of stress amplitude, temperature and
bone density. This statistically derived equation correlates well with previous fatigue studies of human
compact bone.

INTRODUCTION specimens to amplitude


The system is the structural framework of
the body. It must not only protect vital organs from (fatigue life). The resulting
accidental injury but also support the body tissues amplitude versus cycles to failure (or reversals
and facilitate movement. In fulfilling these tasks, bone
is subjected repeated or cyclic stresses.
stresses are generally required to cause material (Forrest,
fracture. Repeated everyday activi- Kennedy, 1963; Sandor, 1972).
ties or prolonged exercise, however, Evans and Lebow (1957) were the first to determine
roscopic damage 1970; Nash, 1966). The Rectangu-
normal remodeling response lar cross section specimens
maintain the structural integrity of subjected to fatigue
the bone (Nash, 1966; Todd et al., 1972; Simon et tests with a stress amplitude
al., 1972). if damage accumulates
repaired fatigue of bone may result
(Nash, 1966). Such fractures observed clini-
cally in the metatarsals, calcaneous, tibia, fibula,
femoral shaft and femoral neck (Morris and
staff, 1967; Griffiths fractures
often occur during prolonged exercise amplitude vs
distance running and are especially com- fatigue life (!&N curve) for specimens extracted from
mon in the metatarsals military human remora. A fatigue test was
(Krause and Thompson, Blicken- employed.
staff, 1967). In many cases, the patient may be un- examined the fatigue proper-
aware of the initiation of a fatigue crack until it is ties of human femoral compact bone specimens
well developed complete frac- rotating cantilever experiment. specimen sur-
ture. faces were kept wet by a wick from a
Fatigue is the progressive material un- reservoir. An S-N curve was generated
der cyclic or fluctuating loading,
materials Griffiths et
required to cause static Fatigue tests are al. (1971) studied the fatigue properties of the proxi-
usually conducted identical mal third of thirty-seven
simulate physiologic loadings. Based
* 17 1974.
t This was supported National Science on the test results it was concluded
Foundation through the Center for Materials Research fractures in the elderly may be fatigue fractures
Stanford University. walking.
27
28 D. R. CARTERand W. C. HAYES

Evans and Riolo (1970) examined the relation using a cutting tool mounted on a rotating pivot of
between fatigue life and histology in adult human the lathe toolpost (rotation radius = 1.27 cm). The tip
compact bone. Specimens were extracted from unem- radius of the tool was approx. 05 mm and the feed
balmed tibia and consisted principally of secondary of the final finish was about 0*05mm per rev. The
osteons, osteon remnants and interstitial lamellae. specimens were kept cool and wet by dripping water
After flexural fatigue tests at a stress amplitude of over them during all lathe work.
345 MN/m’, frozen cross sections of the specimens The final test specimens were therefore 4.45 cm long
were taken near the fracture site and their areas deter- with a 0635cm dia. and contained a central waisted
mined. Using enlarged photomicrographs the area of section of 0,475 cm dia. (Fig. 1). The specimen central
the section representing Haversian canals. resorption axis was parallel to the longitudinal axis of the femur.
areas. and blood vessels was determined and sub- Immediately after machining the specimens were
tracted from the total area to yield a “corrected break equilibrated in Ringer’s solution overnight. They were
area”. Significant positive correlations (P < @Ol) were then removed from solution and stored at -20°C
found between fatigue life and percent of osteonal (Sedlin and Hirsch, 1966; Wall et al., 1970). After all
area plus fragments in the corrected break area. Sig- of the specimens had been stored, 120 specimens were
nificant negative correlations were also found between randomly assigned to the test groups under conside-
fatigue life and interstitial lamellar area in the cor- ration and kept at -20°C until testing. Five stress
rected break area. The authors stated that these amplitudes (65, 76, 86,97, 108 MN/m*) and four tem-
results suggest that osteons tend to increase bone perature levels (21, 29. 37, 45°C) were examined with
fatigue life while interstitial lamellae decrease it. six specimens allocated to each of the twenty test
Previous investigations of bone fatigue ignored the groups. Prior to testing, each specimen was removed
possible effect of temperature. However, thermal gra- from storage and equilibrated in water at the appro-
dients exist along the length of the limbs and temper- priate temperature.
atures in the hands and feet may vary over a large The specimens were tested as rotating cantilevers
range (Bazett, 1949). In cool environments, foot sur- with a Budd RBF-200 rotating beam fatigue testing
face temperature of 15°C for prolonged periods do machine (Fig. 2). Approximately 1.1 cm of the speci-
not result in permanent tissue damage (Speahnan, men on both ends was held by the machine collets.
1949). Foot skin temperatures of up to 43°C have Stress amplitudes in the waisted section were estab
also been recorded in subjects walking briskly in a lished by adjusting the bending moment applied to
warm environment (Robinson, 1949). The tempera- the specimen by the machine. The bone samples were
ture gradients from the surface to the bone and deep rotated about their long axis at 125 cps and thereby
tissues of the hands and feet, however, are small subjected to a fully reversed, constant amplitude cyc-
(Bazett, 1949). When needle thermocouples were used lic loading with zero mean stress. Testing proceeded
to measure thermal gradients in hands with skin sur- until complete failure occurred. A cycle counter on
face temperatures near 18”C, Bazett et al. (1948) found the fatigue machine stopped when the specimens
maximum deep tissue temperatures to be within 2°C broke, thus automatically recording the number of
of the surface temperature. Similar deep tissue tem- cycles to failure. During testing, the temperature of
perature gradients are assumed to exist in the foot the bone was established and wetness assured using
(Bazett, 1949; Reader and Whyte, 1951). Thus, it may a water recirculating pump (Braum Melsungen Type
be assumed that bone temperatures in the foot may 851853) with a built-in temperature controller. A
vary from about room temperature to a few degrees small plastic chamber was used to enclose the speci-
above body core temperature. men and a nozzle which sprayed the bone with water
The objective of this investigation was to examine was built into the top of the chamber. The flow rate
the effects of temperature. bone density, and micro- of water over the specimen was about 1 1. per mm.
structure on the fatigue life of compact bone when The chamber served to collect the circulating water
tested throughout a range of stress amplitudes. and keep the local air temperature close to that of
the water. To estimate the bone surface temperature,
encapsulated temperature crystals were attached to
MATERIALS AND METHODS
one bone specimen which was not in the test group.
Identical procedures were followed in the machin- This specimen was tested throughout the experimen-
ing and storage of 140 bone specimens prior to test- tal temperature range and surface temperatures were
ing. The mid-diaphysis of fresh beef femora were cut
out with a band saw, each femur providing an 4.45 cm
.475cm 0
annulus of cortical bone approx. 5.7 cm long. Longi-
-4- ‘,
tudinal saw cuts through the annulus produced up ,655 cm
- b .2
to ten pieces of bone which were roughly @95 x
7
095 x 5.7cm. These pieces were turned on a lathe 2
to 0.635 cm dia. cylinders and the length reduced to 9
4.45cm. A central waisted section was then made by F
rotating each dowel1 shaped bone in the lathe and Fig. 1. Dimensions of test specimens.
Fatigue life of compact bone-1 29

found to be equal to that of the circulating fluid (+


1°C). In rotating cantilever tests. the stresses imposed Mean dry density I963 gm/cc
are maximum at the surface and decrease linearly to
zero at the specimen neutral axis. Failure generally
occurs at the specimen surface. Adequate control of
the specimen surface temperature, therefore. is more
critical than internal temperature levels.
After testing, cylindrical sections approximately one
centimeter long were cut with a diamond saw from
one end of each specimen away from the fracture site.
These sections were thoroughly dried in a desiccator
with phosphorous pentoxide for nineteen days. Six
of the samples were weighed on an analytical balance
TEMPERATURE (“c)
after 11, 15 and 19 days. The weight loss from the Fig. 3. Reversals to failure plotted against bone tempera-
11th to 15th day was about two per cent and from ture. Each datum point represents the mean fatigue life
the 15th to 19th day from zero to 05%. It was there- (+ S.E.) of thirty specimens (6 specimens at each of 5
fore assumed that the samples were completely dry stress amplitudes). The average stress amplitude was 86
after nineteen days. All of the samples were then MN/m2.
weighed and their diameters and lengths determined
The results of the experiment and this initial analy-
with a micrometer. The dry density of each specimen
sis indicated that the fatigue life of bone is signifi-
tested was estimated on the basis of these measure-
cantly dependent upon temperature as well as stress
ments.
amplitude. Figure 3 shows values of log 2N (2N = re-
Microstructure studies of several specimens were
versals to failure) plotted against bone temperature.
done by cutting away small cross sections of bone
Each datum point represents the mean of thirty test
near the fracture site. These samples were ultrasoni-
specimens (six specimens at each of five stress levels).
cally degreased in trichloroethylene, embedded in
These data suggest that a linear relationship exists
methylmethacrylate, and viewed with a reflected light
between log 2N and temperature in the physiologic
microscope. After ultrasonically degreasing with tri-
range of interest. In Fig. 4, values of log 2N are plot-
chloroethylene and gold coating the bone surface, frac-
ted against log B (a = stress amplitude). These data
ture surfaces were studied by scanning electron micro-
points represent the mean of twenty-four test speci-
=oPY. mens (six specimens at each of four temperatures). This
graph suggests that in bone, log 2N and log a are
RESULTS AND ANALYSIS linearly related. This relationship between stress and
fatigue life has also been shown to exist in many
The major results of the study are tabulated in engineering materials (Sandor, 1972).
Table 1. The mean fatigue lives (*SE.) are shown An analysis of covariance established there was no
for each of the twenty test groups. The initial phase statistically significant interaction between the tem-
of data analysis was restricted to the effects of stress perature effect and the stress effect. Therefore. the
amplitude and temperature on specimen fatigue life. data are consistent with the hypothesis that the slope
Since a random allocation scheme was used, vari-
ations in density or microstructure would manifest
themselves only as data scatter within the twenty test
groups examined. This scatter would not significantly
alter the relationships seen between the mean values
of each group.

Table 1. Summary of test results

‘” 60 70 60 so 100 II(

STRESS AMPLITUDE (MN/i+) (log scale)

Fig. 4. Reversals to failure plotted against stress amplitude.


Each datum point represents the mean fatigue life (+ SE.)
of 24 specimens (6 specimens at each of 4 temperatures).
The average temperature was 33°C.
30 D. R. CARTERand W. C. HAYES

1
dual while specimens with strong fatigue resistance
would have positive residuals. Using this residual
value as a common indicator of fatigue resistance at
a particular temperature and stress amplitude, the
effects of density and microstructure were examined.
Figure 6 shows residual values plotted against bone
density for each of the specimens tested. A Pearson
moment correlation established that residual values
were significantly dependent on density (r = @483,
I I J P = O=OOl)with lower density specimens having less
104 Id Id resistance to fatigue (negative residuals).
REVERSALS To FAILURE (ba Sal*)
Microscopic examination of transverse specimen
Fig. 5. Stress amplitude plotted against reversals to failure sections revealed two general histological types: pri-
for specimens at 45°C ( a~) and 21°C ( UU). Mean test mary compact bone and secondary Haversian bone.
values (+ SE.) are shown as well as the statistically de-
rived S-N curves. The primary bone was characterized by a laminar
structure containing irregular primary osteons (Cur-
of the curve shown in Fig. 3 is independent of the rey, 1959; Heit et al., 1965) (Fig. 7a). The Haversian
stress amplitude. Similarly, the slope of the curve in bone consisted of secondary osteons. osteon frag-
Fig. 4 is temperature independent. These findings in- ments, and interstitial bone (Fig. 8a). In most mam-
dicate that the relationship between fatigue life, stress mals, bone growth is achieved through a deposition
amplitude, and temperature can be expressed as of primary bone tissue. This bone is subsequently
remodeled and replaced by secondary Haversian
log(2N) = ‘4 log f7 + BT+ c, (1)
bone (Heit et al., 1965; Enlow. 1962). The rate at which
where 4. h and C are constants, 2N = reversals to this substitution occurs varies between species and
failure, rr = stress amplitude and T = temperature. A location in the skeletal system (Smith, 1960).
multiple regression technique was used to fit the data Microscopic examinations were made of five speci-
of this investigation in accordance with equation (1). mens with the highest residuals (positive), five with
With stress given in MN/m2 and temperature in the lowest residuals (negative), and five with residual
degrees Centigrade, A, B and C were found to be: values nearest to zero. The five specimens with the
A = - 7.415 (S.E. = 0.478). E = -00202 (S.E. = lowest residuals (short fatigue life) were shown to
0004), and C = 20042. Using these values with have a secondary Haversian microstructure. Of the
equation (1) to estimate log 2N for any of the tested five specimens with the highest residuals. four had
specimens, the standard error of the estimate is 0412. a primary structure and one was mostly primary bone
The regression coefficients A and B are significantly with a small Haversian section. The five specimens
different from zero (P < @Ol). closest to their predicted fatigue life (zero residuals)
The S-N curves for specimens tested at 21 and at tended to have sections of both primary and second-
45°C are shown in Fig. 5. Specimens tested at 29°C ary bone. Typical cross section photomicrographs for
and at 37°C resulted in S-N curves between these these specimens with large positive and large negative
two limits and thus the curves of Fig. 5 provide a residuals are shown in Figs. 7 and 8 respectively.
band of fatigue life values for compact bovine bone The corresponding fracture surfaces as seen with elec-
in the temperature range examined. These fatigue tron microscopy are also shown.
properties reflect cumulative structural damage in the The results shown in Fig. 6 suggest that log (2N)
inert bone specimens. The test data, however, do not varies linearly with respect to bone density. No inter-
account for in vivo bone remodeling which may act action between this density effect and bone tempera-
to repair damage and prolong fatigue life. The curves ture or stress amplitude was apparent. Therefore,
of Fig. 5 therefore represent lower bounds of in viva
bone fatigue resistance.
The statistically derived equation (1) which is illus-
trated for 45°C and 21°C in Fig. 5 does not account
for all parameters which might affect devitalized bone
fatigue life. Therefore, the actual fatigue life values
for each specimen deviate somewhat from the values
predicted by the equation. This variation from the
predicted value can be quantitatively defined by the
specimen residual.
SPECIMEN RESIDUAL = actual (log 2N)
- predicted (log 2N). (2)
Fig. 6. Fatigue resistance plotted against dry bone density.
Specimens failing at a lower number of cycles than Data points show deviations from the fatigue life predicted
predicted by equation (1) would have a negative resi- by equation (1).
Fig. 2. Test specimen in fatigue machine collets.

Fig. 7. (a) Cross section photomicrograph (10x ) of specimen with a long fatigue life compared
with prediction of equation (1) (specimen residual = + 0.816, density = 1 .999 g/cm). Specimen
shows primary bone structure. (b) SEM photomicrograph (20 x ) of corresponding fatigue fracture
surface.

Fig. 8. (a) Cross section photomicrograph (10 x) of specimen with a short fatigue life compared with
prediction of equation (1) (specimen residual = -0.855, density = 1 ,897 g/cm). Specimen shows
secondary Haversian bone structure. (b) SEM photomicrograph (20 ,: ) of corresponding fatigue
fracture surface.

(Fucityp. 30)
Fatigue life of compact bone-1 31

equation (1) can be expanded to the form differences in the fatigue life of human compact bone
specimens.
log(2N) = H log u + JT + Kp + M, (3) Drying of compact bone specimens is known to
where H, J, K, M are constants, 2N = reversals to alter its static mechanical properties. Anticipating
failure, u = stress amplitude, T= temperature and that fatigue properties are also affected by drying the
p = dry bone density. Again using multiple regression test specimens were equilibrated in water before test-
analysis with stress in MN/m’. temperature in c”, ing and bathed in a water spray during testing. To
and density in g/cm3, H, J, K and M were found evaluate the necessity of circulating fluid over the
to be: H = -7.837 (SE. = 0.425), J = -0.0213 bone, twelve specimens of the original random pool
(S.E. = 0@04), K = 4463 (SE. = 0.740) M = 12043. were tested at an ambient temperature of 21°C after
Using these values with equation (3) the standard equilibration in water but without circulating water.
error of the estimate for log 2N is 0360. Equation Six of these specimens were tested at a stress ampli-
(3) therefore provides a better estimate of specimen tude of 108 MN/m’ and six with a stress amplitude
fatigue life than does equation (1). The regression of 97 MN/m’. The mean fatigue lives (reversals to
coefficients H, J and K are significantly different from failure) of these two groups was found to be approxi-
zero (P < @Oi). mately fifty per cent lower than specimens tested at
Using equation (3) an estimate of fatigue life for the same temperature under fully wet test conditions.
each specimen was made as a function of stress ampli- It has generally been assumed that the fatigue life
tude, temperature, and specimen density. New resi- of devitalized compact bone is independent of the fre-
duals were then calculated as deviations from this pre- quency of loading (Evans, 1973). This assumption has
diction. Thus the previous residuals were, in effect, been shown to be true in most metals except at ex-
corrected to compensate for density variations. These tremely high frequencies (Kennedy, 1963). However,
corrected residuals were used to assess whether the fatigue in polymer composites is considerably more
increased fatigue resistance shown by primary bone frequency dependent (SaIkind 1971). There may be
is simply due to increased density or whether the some effect of loading frequency in bone due to its
structure of the bone itself provides increased fatigue complex, composite structure. Definitive studies in
resistance. The microstructure of specimens with the this area have not been made.
five highest and five lowest new residuals were exam-
ined. The five specimens with the greatest negative Temperature
corrected residuals proved to have secondary Haver- In this investigation, the log of compact bone fati-
sian structures while the five specimens with highest gue life was shown to vary linearly by approximately
positive corrected residuals (high fatigue resistance) a factor of three over the temperature range examined
had primary structures. These results suggest that a (21--45”C), with higher temperatures resulting in de-
specimen with a primary structure will have a creased fatigue life (Fig. 3, Fig 5). An analogous rela-
longer fatigue life than one with a secondary Haver- tionship between fatigue life and temperature is seen
sian structure with the same density. with most metals and composite materials (Kennedy,
1962; Salkind, 1971). Since no previous studies of the
DISCUSSION
effect of temperature on bone fatigue life have been
Testing conditions made, direct comparisons with other investigations
In fatigue testing of metals, specimen geometry, are not possible. However, these results seem consis-
methods of preparation, and surface finish may in- tent with studies of temperature effects on other
fluence the test results (Forrest, 1962). The machining mechanical properties of bone. Smith and Walmsley
process can create small defects which tend to concen- (1959) showed that a linear relation exists between
trate stresses and decrease fatigue life. This effect may bone bending modulus and temperature. In quasi-sta-
be less critical in fatigue testing of bone. Devitalized tic tests of compact bone specimens at temperatures
bone is a composite material consisting of hydroxy- between 4.4 and 43.3°C higher temperatures resulted
apatite reinforced collagen. Fatigue tests with compo- in lower bending moduli. Bonfield and Li (1966)
site engineering materials show that they are often examined the effect of temperature on the energy
more damage tolerant than metals. Ultimate failure absorbed to failure of compact bovine bone specimens
depends more on general cumulative damage such as subjected to tensile impact. It was found that a maxi-
fiber breaking, debonding and microcracking rather mum amount of energy was absorbed in the range
than specific sites of damage initiation (Salkind. 1971). of zero to 25°C. As temperature was increased to 25,
In addition, bone contains many natural defects (vas- 100, 200 and 300°C. the energy absorbed to failure
cular channels, resorption cavities, and lacunae) was successively reduced. Bone is therefore weaker
which may act to blunt the growth of cracks created in tensile impact at these higher temperatures. Bon-
during machining (Currey, 1962; Swanson et al., field and Li (1968) also examined the effects of tem-
1971). The chances of introducing a critical flaw perature in quasi-static tensile tests of compact
which would seriously affect fatigue life are therefore bovine bone. It was found that increasing the tempera-
reduced. Indeed, Swanson et al. (1971) found that a ture throughout a range of -58-9o”C caused a sig-
wide range of surface finishes produced no significant nificant reduction in the bone modulus of elasticity.
32 D. R. CARTERand W. C. Hans

The effect of temperature on bone fatigue life and per cent osteonal area. Evans and Riolo’s findings
shown in this investigation may have important prac- were from a specimen population consisting entirely
tical implications. If a similar effect exists in humans, of secondary Haversian bone. Test specimens in the
maintaining reduced local temperatures in bone cycli- present investigation, however, included primary bone
cally stressed during prolonged exercise (e.g. the meta- tissue. secondary Haversian bone, and samples having
tarsals during hiking) may be helpful in preventing both primary and secondary areas. The microstruc-
fatigue fractures. Environmental conditions, footwear ture findings of thjs investigation do not compare
and clothing design, and type of exercise are known osteonal bone to interstitial bone. but rather primary
to affect deep tissue and bone temperature in the bone structure to secondary Haversian structure.
limbs (Newburgh, 1949). A consideration of these fac-
tors may be appropriate in future clinical and epide- Comparisons with human hone fatigue tests
miologic studies of fatigue fractures. Previous investigations of compact bone fatigue life
over a range of stress amplitudes were conducted by
Density King and Evans (1967) and Swanson et al. (1971) used
Fatigue life of the test specimens was also found specimens extracted from fresh human femora and
to be significantly dependent on bone density. The stored at - 20°C while King and Evans used specimens
density correlation illustrated in Fig. 6 shows that from embalmed human femora. Both tests were
a six per cent increase in bone density (from 1.86 conducted at room temperature.
to 1.98 g/cm’) results in a threefold increase in fati- The fatigue lives of the bovine specimens in the
gue life. Although no previous correlations between present investigation were generally higher than those
density and fatigue life have been shown, this effect found in either of the two previous studies. This is
is not surprising. Swanson et al. (1971) suggested that probably due to the fact that the density of the bovine
a negative correlation exists between fatigue life and femora used in this investigation was significantly
age (hence, a positive density correlation according greater than that of the human femur. McElhaney,
to Atkinson and Weatherell, 1967) but were unable Alem and Roberts (1970) determined the dry bone
to show statistical significance. Amtmann (1971) density of 160 specimens extracted from human
showed that compact bone with a high density tends femora. Although density varied significantly both
to be stronger than lower density bone in quasi-static between bones and within different regions of the
compression tests. Wall et al. (1972) demonstrated same bone, the average dry density was found to be
similar results for compact bone in tension. 1.85g/cm’. The bovine specimens tested in this in-
The density correlation with fatigue life shown in vestigation, however, had an average dry density of
this investigation may be an important factor in un- 1.983g/cm3. In view of the dependence of fatigue
derstanding fatigue fracture in the femoral neck of life on density shown in the present investigation, it
the elderly. Amtmann (1971) reported significant is not surprising that the bovine femur specimens
reductions in bone density in the femora of elderly were found to be more fatigue resistant than human
individuals. The percentage of density lost was espe- femur specimens.
cially high in the proximal end of the femur, some- In order to compare the results of this investigation
times being as much as 37%. Considering the correla- to those of Swanson et al. and King and Evans,. dif-
tion shown in Fig. 6, a marked reduction in bone ferences in bone densities and test temperatures must
fatigue life in these individuals would be expected. be considered (ignoring, in the first approximation,
other species differences). Assuming that the two pre-
Microstructure vious studies were conducted at a temperature of
The preliminary microstructure studies suggest that 21°C using bone specimens with an average dry den-
primary bone is more fatigue resistant than secondary sity of 1.85 g/cm3 (McElhaney et al., 1970), equation
Haversian bone structure (Figs. 7.8). This finding is (3)predicts an S-N curve which correlates well with the
consistent with other investigations which compared data of King and Evans (1967) and Swanson et al.
the mechanical properties of these two histological (1971). The test data of these other two studies as
types. Wahnsley and Smith (1957) first suggested that well as the prediction of their results based on equa-
primary bone tissue is stronger than secondary tion (3) of this investigation are shown in Fig. 9.
Haversian bone. Currey (1959) confirmed these. initial
observations with quasi-static tension tests of sixty-
SUMMARY
four specimens extracted from oxen femora. Heft et
al. (1965) showed that fully mineralized primary Fatigue tests to failure of compact adult bovine
bovine bone is as strong or stronger than Haversian bone specimens were conducted at five stress ampli-
bone in quasi-static compression tests. Saha (1973) tudes (65-108 MN/m2) and four temperature levels
found the same result when bovine bone was tested (21-4SQ A multiple regression technique was used
in tensile impact. to derive an equation for fatigue life as a function
The results of this investigation do not necessarily of stress amplitude, temperature, and bone density.
contradict the test results of Evans and Riolo (1970) This statistically derived equation correlates well with
who found positive correlations between fatigue life fatigue studies of human compact bone.
bone-1 33

Evans. F. G. and Lebow, M. (1957) Strength of human


compact bone under repetitive loading. J. appl. Physiol.
10. 127-130.
Evans. F. G. and Riolo, M. L. (1970) Relations between
the fatigue life and histology of adult human cortical
bone. J. Bone Jnt Stag. (A) 52. 15791586.
Evans. F. G. (1973) Mechanical Properties a/ Bone. Thomas.
Springfield, IL.
Forrest. P. G. (19621 Fatigue of Metals. Addison-Wesley.
Reading, MA.
Griffiths. W. E. G.. Swanson. S. A. V. and Freeman, M.
REVERSALS TO FAIWRE (log SCdr)
A. R. (1971) Experimental fatigue fracture of the human
Fig. 9. Comparison of the multiple regression results of cadaveric femoral neck. J. Bone. Jnt Surg. (B) 53. 136
this investigation (equation 3) with data from previous 143.
studies of human compact bone fatigue life. Heit. J.. KuEera. P.. Vavra. M. and Volenik. V. (1965)
Comparison of the mechanical properties of both
primary and Haversian bone tissue. Acta Anat. 61, 412
423.
A temperature decrease of 24°C was shown to in- Kennedy. A. J. (1963) Processes of Creep and Fatigue in
Metals, Wiley, NY.
crease bone fatigue life by approximately a factor of
King, A. I. and Evans, F. G. (1967) Analysis of fatigue
three. This result may be important in understanding strength of human compact bone by the Weibull
fatigue fractures in the extremities where local bone method. In Digest of The Seventh International Confer-
temperatures may vary. ence on Medical and Biological Engineering (Edited by
A six per cent increase in bone density was also Jacobson, B.). Stockholm, The Organizing Committee
of The Conference., p. 514.
shown to produce approximately a threefold increase Krause, G. R. and Thompson, J. R. Jr. (1944) March frac-
in fatigue life. This result has obvious clinical implica- ture: an analysis of two hundred cases. Am. J. Roenrg.
tions especially in elderly or osteoporotic individuals. 52. 281-290.
Preliminary microstructure studies suggest that pri- Lease. G. O’D. and Evans. F. G. (1959) Strength of human
metatarsal bones under repetitive loading. J. appl. Phy-
mary bone has greater fatigue resistance than second-
siol. 14. 49-51.
ary Haversian bone. Further studies in this area are McElhaney, J. H., Alem, N. M. and Roberts, V. L. (1970)
in progress. A porous block model for cancellous bone. Am. Sot.
Mech. Engng Publ. No. 70-WA/BHF-2. NY.
Morris, J. M. and Blickenstaff, L. D. (1967) Fatigue Frac-
Acknowledgements-The authors thank Arthur Leach. tures. Thomas, Springfield, IL.
Rosemarie Koch and Loren Anderson for their assistance Nash. C. D. (1966) Fatigue of self-healing structures: A
in specimen preparation and analysis. Professor Brad Efron generalized ~theoiy of “fatigue failure. &. Sot. Mech.
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“MY, c
34 D. R. CARTERand W. C. HAYES

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