Fatigue and Fracture Resistance of Bone

, David B. Burr2, Neil A. Sharkey3 and David P. Fyhrie4

Orthopaedic Surgery, UC Davis Medical Center, Olga, WA, USA

Department of Anatomy and Cell Biology, Indiana University School of Medicine, Indianapolis, IN, USA

Kinesiology, Orthopedics and Rehabilitation, Pennsylvania State University, University Park, PA, USA

Orthopaedic Surgery, Biomedical Engineering, UC Davis Medical Center, Sacramento, CA, USA



In Chap. 7, we examined the mechanical properties of bone when it is fractured by a load sufficient to exceed the failure stress of the material. Structures may also fail more gradually. There are two principal ways in which this can happen: creep and fatigue. In both, a stress less than the ultimate stress is applied, and damage from this stress grows and accumulates until failure occurs.

FatigueCreepFracture mechanicsMicrocracksToughnessTargeted remodeling

Textbooks and Heaven only are ideal;

Solidity is an imperfect state.

Within the cracked and dislocated Real

Nonstochiometric Crystals dominate.

John Updike in “The Dance of the Solids”

8.1 Introduction

In Chap. 7, we examined the mechanical properties of bone when it is fractured by a load sufficient to exceed the failure stress of the material. Structures may also fail more gradually. There are two principal ways in which this can happen: creep and fatigue. In both, a stress less than the ultimate stress is applied, and damage from this stress grows and accumulates until failure occurs. In creep, the stress is applied continuously; in fatigue, the stress is applied periodically. Obviously, these phenomena may occur simultaneously in the components of an engineering structure like a bridge, where the weight of the structure provides creep loading and the periodic passage of vehicles produces fatigue. Similarly, in the skeleton, bones often support more or less constant loads for prolonged periods of time (such as the vertebral bodies in your spine as you sit reading this book), and equally often carry cyclic loads (such as when you walk to class). In this chapter we shall see that creep and fatigue are closely related and explore the ways in which bone limits and repairs the damage that they produce. We also discuss what seems to happen when the limits of this capacity for damage control are exceeded and the bone fails by what is called a stress fracture.

At least some of the damage caused by creep and fatigue can be seen in histologic sections of normal, healthy bones (Fig. 8.1). These microcracks can, under continued loading, multiply and grow into “macrocracks,” eventually resulting in complete fracture. Ordinarily, microcracks (or other kinds of microdamage) are removed by remodeling. If fatigue damage in bone accumulates more rapidly than remodeling can remove it, fatigue failure or a “stress fracture” can occur. These fractures can be partial or complete, and tend to occur in soldiers and joggers, as well as ballet dancers and other elite athletes, including racehorses. In principle, inhibition of normal bone remodeling could cause an accumulation of unrepaired fatigue damage that, over time, could lead to fracture.


Figure 8.1
A typical microcrack (arrows) as seen in a 100-μm-thick histologic cross section of human cortical bone. The specimen was stained in basic fuchsin en bloc to mark the surfaces of cracks existing before the section was cut. Artifactual cracks produced by the sectioning process are not stained (Burr and Stafford 1990). This crack is about 80 μm long in the plane of the section, and its ends about the cement lines of two secondary osteons. Most microcracks in cortical bone are of this type.

It is important to understand, however, that the prevention of fatigue failure is not entirely dependent on repair by remodeling. The growth of microdamage is also controlled by the lamellar structure of bone. In ways completely analogous to the crack deflection and blunting effects achieved in man-made composite materials, bone’s internal structure limits the development of fatigue damage. Much of the information contained in this chapter has been extrapolated from the extensive experimental data on the fatigue behavior of nonbiologic composite laminates (e.g., graphite-reinforced epoxies, or polyester laminates). Knowledge of their behavior allows us to understand how various features of lamellar bone structure function to improve its fatigue properties. Before considering such crack-resistant materials, however, we should look at what is known about cracking in simpler materials.

8.2 Basic Fracture Mechanics

Fracture mechanics considers the conditions under which an existing flaw or crack in a load-bearing structure grows and causes catastrophic failure. In conventional engineering applications, the flaws of concern may be produced as the structure is manufactured or by overloading or repetitive loading of the structure thereafter. In the case of skeletal structures, “manufacturing flaws” are usually (i.e., in healthy people) of less concern than those arising from heavy usage. However, genetic errors can result in abnormal bone tissue (usually because of a collagen defect) that becomes damaged under normal loads. Sometimes damage is introduced by surgeons as they try to correct other difficulties. Whatever the cause of the cracking, bones have an exceptional ability to control it. The purpose of this section is to provide a brief summary of fracture mechanics to help us understand how cracks are propagated generally and how they are controlled in bone.

8.2.1 Linear Elastic Fracture Mechanics

Perhaps the simplest way to approach this topic is to consider it in the context of stress concentrations. Consider the stress concentration on the edge of an elliptical hole in an infinite plate (Fig. 8.2a). The plate bears a tensile stress, s, normal to the long axis of the ellipse. The stress at each end of this axis is


Figure 8.2
(a) An elliptical hole in a plate or solid structure bearing a tension stress s has a stress concentration several times s at the point shown. (b) A crack may be thought of as a very eccentric elliptical hole. The stress at a point near the crack tip (dot) is a function of its distance r and angular position θ.

$$ {\sigma}_A=s\left(1+2a/b\right) $$

where b and a are the minor and major radii of the ellipse. (For a circular hole, this reduces to 3 s.) However, this equation loses its validity if a»b and the ellipse becomes crack-like (Fig. 8.2b). In that case, the stresses at a point given by polar coordinates (r, Θ) relative to the end of the b-axis are

$$ {\sigma}_x=s{\left(a/2r\right)}^{1/2} \cos \left(\theta \right)/\left[2\left(1- \sin \left(\theta \right)/2 \sin \left(3\theta /2\right)\right)\right] $$


$$ {\sigma}_y=s{\left(a/2r\right)}^{1/2} \cos \left(\theta \right)/\left[2\left(1- \sin \left(\theta \right)/2 \sin \left(3\theta /2\right)\right)\right] $$


$$ {\sigma}_{xy}=s{\left(a/2r\right)}^{1/2} \cos \left(\theta \right)/\left[2 \sin \left(\theta \right)/2 \sin \left(3\theta /2\right)\right] $$

The stress in the y direction along the Θ = 0 line is

$$ \sigma {}_y=s{\left(a/2r\right)}^{1/2} $$

As one approaches the crack tip, r becomes very small relative to the crack length, a, and the stress concentration very large. At the crack tip itself, r = 0 and σ y is singular (i.e., it is infinite). To avoid this difficulty, one may move the 2r term to the other side of the equation, obtaining σ y (2r)1/2, which is not singular at the crack tip but is still proportional to the “intensity” of the stress at the crack tip. One can then define:

$$ \mathrm{Stress}\ \mathrm{Intensity}={\sigma}_y{(2r)}^{1/2}=s{a}^{1/2} $$

That is, the stress intensity in the vicinity of the crack tip is proportional to the nominal stress, s, and the square root of the crack length, a. This stress intensity is what drives the crack forward.

Irwin (1957) used linear elasticity theory to obtain equations for the stresses near the tips of cracks with several different geometries and loading situations. He found that in general

$$ \sigma =k{\left(2\pi r\right)}^{-1/2}+\mathrm{other}\ \mathrm{terms} $$

where k is a coefficient peculiar to the particular problem. As one approaches the crack tip, the “other terms” became less important and can be ignored. Because of the π in these equations, a formal stress intensity factor, K, was defined so as to include π as well:

$$ K=Cs{\left(\pi a\right)}^{1/2} $$

K has units of Pa m1/2; compare Eq. (8.6) with Eq. (8.4). C is a dimensionless constant depending on the size and shape of the flaw and the size, shape, and mode of loading of the specimen, and s is a pertinent stress component in the specimen beyond the influence of the crack, for example, tensile stress perpendicular to the plane of the crack. K characterizes the state of stress near the crack tip; therefore it is known as a characterizing parameter. Its utility stems from the fact that if K exceeds a critical value, the crack will propagate; otherwise, it will not. There is no need to make calculations of the local stresses to gain this information.

To reiterate, the fundamental concept in linear elastic fracture mechanics is that K determines whether a crack will propagate or not, and if so, how fast. In practice, K bears a subscript denoting the type of cracking that is being considered.

8.2.2 Kinds of Cracks

Of the various ways in which a specimen may be loaded to extend cracks, three are commonly discussed in fracture mechanics (Fig. 8.3). Mode I cracks are propagated perpendicular to the line of action of a tensile load, as when a wedge splits a log lengthwise. Mode II cracks result when shearing forces are applied parallel to the plane of the crack and parallel to the direction of its propagation. Mode III cracks are a “tearing” phenomenon; in this case, the shearing is perpendicular to the crack propagation direction. Mode I is the most commonly discussed type of cracking.


Figure 8.3
Modes of cracking.

8.2.3 Modes of Cracking

As an example, consider the Mode I cracking that occurs when a plate of width b, containing a crack of length a on one edge, is loaded in tension. In this case, the C in Eq. (8.6) turns out to be:

$$ C={\left[\left( \tan q\right)/q\right]}^{1/2}\frac{0.752+2.02\left(a/b\right)+0.37\left(1- \sin q\right)}{ \cos q} $$

where q = π a/2b. As shown in Eq. (8.6), when multiplied by (π a)1/2 and the tensile stress in the plate, this C gives the stress intensity factor, K I, for this situation. If this K I is greater than a critical stress intensity factor, K Ic, the crack propagates rapidly clear through the structure. K Ic is also called the fracture toughness; it is a material property, like yield stress. Table 8.1 gives some typical values of K Ic for metals, ceramics, polymers, and cortical bone (Pilkey 1994). By conducting many experiments and tabulating the results, the means for calculating K I in various situations and comparing them to the critical values have been amassed for many conventional engineering applications. Figure 8.4 gives formulae for C in a few simple cases.

Table 8.1
Fracture toughness for several materials


K Ic, MPa-m1/2

2024 Aluminum


4330V Steel






Al2O3 ceramic


SiC ceramic


PMMA polymer


Polycarbonate polymer


Cortical bone



Figure 8.4
Equations for the constant C in three simple cases.

The measurement of K is beyond the scope of this book because it is complicated by the need to ensure that all the assumptions underlying its calculation are fulfilled. The basic process is simple, however, as illustrated in Fig. 8.5 for mode I cracking. A specimen with a standardized crack is manufactured, and the crack is propagated across the specimen by loading it in tension. The applied load and crack opening displacement are measured and plotted. A failure load is identified on the load-displacement curve using several rules. K Ic is then calculated by multiplying the failure load by a formula derived from the length of the crack and the shape and dimensions of the specimen.


Figure 8.5
The basics of measuring KIc. A specimen with a notch is loaded in tension to drive a crack to the right as shown. The tensile force F is plotted against the crack opening displacement, d. A failure point, P(FF, dF), on the curve is defined by certain rules, and KIc is calculated from FF and dF using a formula.

Several investigators have measured K Ic for cortical bone (Table 8.2). Values for bone are an order of magnitude less than those for structural metals but similar to a tough ceramic like Al2O3. In making these comparisons, it needs to be emphasized that the values for bone are for crack propagation parallel to the long axis of the bone, which is to say “with the grain.” If one tries to propagate a crack transversely, or perpendicular to the primary and secondary lamellar structure, the crack immediately turns and goes “with the grain.” Thus, the fracture toughness of bone is decidedly anisotropic, and the values shown are for the direction offering the least resistance to cracking.

Table 8.2
Experimental values of K c and G c for bone (Behiri and Bonfield 1984; Norman et al. 1992, 1992; Melvin and Evans 1973; Bonfield and Datta 1976; Alto and Pope 1979; Wang et al. 2002)

Bone type

K c, MPa m1/2

G c, Jm−2


Mode I, transverse fracture

 Bovine femur



Melvin and Evans (1973)

 Bovine tibia



Bonfield and Datta (1976)

 Equine metacarpus



Alto and Pope (1979)

 Human tibia



Norman et al. (1992)

 Human femur (young and old)

5.1 and 4.3

2262 and 1712 (derived from Kc and E)

Wang et al. (2002)

Mode I, longitudinal fracture

 Bovine femur



Melvin and Evans (1973)

 Bovine tibia



Behiri and Bonfield (1984)

 Human femur



Norman et al. (1992)

Mode II

 Human tibia



Norman et al. (1992)

8.2.4 Maximum Tolerable Flaw Size

By rearranging Eq. (8.6) and setting the stress intensity factor equal to the critical value, one may solve for the flaw size that will precipitate unstable crack propagation. For human tibial compact bone, Norman et al. (1995) found that K Ic ≈ 4 MPa m1/2. For a semicircular crack of radius a at the surface of a semi-infinite body loaded in tension (e.g., on the tension side of a large bone loaded in bending), the stress intensity factor is Pilkey (1994).

$$ {K}_I=2{\left(a/\pi \right)}^{1/2}s\left[1.211-0.186{\left( \cos \theta \right)}^{1/2}\right] $$

Here, θ is as defined in Fig. 8.2 and s is the stress elsewhere in the body, far from the crack. Setting θ = 0, the maximum tolerable crack radius would be

$$ {a}_c=0.238\pi {K_{Ic}}^2/{s}^2 $$

Assuming that E = 20 GPa and the strain (ε) is a physiologic 2000 micro-strain, one has s = E ε = (20 × 109) (2 × 10−3) = 40 MPa and

$$ {a}_c=0.238\pi \left({4}^2/{40}^2\right)=0.0075\mathrm{m}=7.5\mathrm{m}\mathrm{m} $$

which is a rather large flaw. Remember also that the K Ic used here is probably considerably smaller than the one for a crack propagating across a bone.

8.2.5 It Takes Energy to Propagate a Crack

Before Irwin and others developed the concept of a stress intensity factor, Griffith (1920) formulated the problem of crack propagation in brittle solids in terms of energy. He reasoned that energy was required to create the surfaces of the extended crack because all surfaces have “surface energy” associated with them. He conducted many experiments with glass rods to develop his idea into a theory.

Suppose it takes energy or work, dW c, to propagate a crack for a distance, da. This energy usually comes from the work done in deforming the specimen via the strain energy, U, stored throughout its interior. Conservation of energy requires that

$$ d{W}_c/da=dU/da $$

The right side of this equation is called the strain energy release rate and is denoted by G, after Griffith, who showed that for mode I propagation of a thin ellipsoidal crack the strain energy release rate is

$$ G=dU/da=\pi a{s}^2/E $$

where E is the elastic modulus. By setting up an experiment in which a crack can be slowly propagated in a material of modulus E, and its length (a) measured as a function of the applied stress (s), the strain energy release rate can be determined from Eq. (8.12).

The left side of Eq. (8.11) is called the crack growth resistance, R:

$$ R=d{W}_c/da $$

For a crack to grow, strain energy must be produced and released at least as fast as it is consumed by breaking molecular bonds in the material to extend the crack. For the crack to grow precipitously, G must be greater than a critical value, which is R; that is, G ≥ R.

By comparing Eqs. (8.6) and (8.12), it is apparent that G is proportional to K 2. For mode I cracking in a plane stress situation,

$$ {G}_I={K}_I^2/E $$

It is important to understand that a propagating crack is “nourished” by the elastic energy of the mass under stress. Finkel (1985) pointed out that although cracks are driven by the strain energy stored in the mass under stress, they are themselves without inertia, and thus capable of turning instantaneously in any direction that promises more elastic energy.

8.2.6 Beyond the Linear Theory: Real Cracks Have Ears

In most materials, and certainly in bone, linear elasticity theory does not hold when stresses become high, and that includes the situation at the tip of a crack. There is a zone of plastic deformation around the crack tip that is generally shaped as depicted in Fig. 8.6. Note the “Mickey Mouse ears” shape of the plastic zone. Finkel has called the plastic zone the “ears” of the crack, and refers to computations showing that these ears may “wiggle” as the crack propagates. The plastic zone at the leading edge of a propagating crack has an ear-like characteristic shape.


Figure 8.6
The plastic zone at the leading edge of a propagating crack has an ear-like characteristic shape.

For mode I cracking, the distance directly ahead of the crack that is plastically deformed is given by

$$ {r}_p=\frac{1}{k\pi }{\left(\frac{K_I}{\sigma_y}\right)}^2 $$

where σ y is the yield stress; k = 2 for plane stress or 6 for plane strain.1 One way to accommodate the presence of a plastic zone in linear elastic fracture mechanics theory is to add this r p (or some portion of it) to the crack length in the equations for K and G. Equivalently, when using the energy approach, another term must be added to Eq. (8.14): the rate at which energy is consumed by plastic deformation per unit length of crack extension.

Box 8.1 Dynamic Fracture Mechanics

Things break differently when they break extremely rapidly. Dynamic fracture mechanics is the study of cracking under these conditions (Freund 1990). When a bone is broken very rapidly in a situation involving a great deal of kinetic energy, the fracture is highly comminuted (i.e., the bone breaks into many pieces). The reasons for this are complex, but stem from two important phenomena. When a crack propagates slowly through a structure, it causes the adjacent material to be unloaded. This load change prevents nucleation of, or arrests, other cracks in the vicinity. When a structure is impulsively loaded, a stress wave passes through it at the speed of sound (about 3000 m/s for bone). This results in crack initiation and propagation at many sites simultaneously, before any one crack can arrest others. When these many cracks grow to intersect one another, many fracture fragments are produced. Emergency room physicians see this result in victims of high energy trauma.

The second phenomenon promoting fragmentation at high fracture rates is bone’s viscoelastic nature. The more rapidly bone is loaded, the stiffer it is (Fig. 7.​13). The velocity of the stress wave increases as the square root of the elastic modulus, so that the stress field more rapidly fills the bone, accentuating the effects just described. On the other hand, bone strength increases with loading rate. This effect is seen in other materials, too. The reasons for it are not clear.

In summary, when a bone is rapidly loaded, it is more fracture resistant, but if it breaks, the fracture is more fragmented. Also, logically enough, the severity of damage to the soft tissues tends to parallel the degree of damage to the bone; thus, the seriousness of severe fractures is compounded by impairment of the associated soft tissues, on which fracture healing depends.

8.2.7 Beyond the Linear Theory: Real Cracks Are Complicated

Propagation of a crack in bone is slowed (or accelerated!) by changes in the material ahead of or behind the tip of the propagating crack (Fig. 8.7). Crack toughening mechanisms ahead of the crack tip are called “Intrinsic mechanisms” and those that occur behind the crack tip are called “Extrinsic mechanisms” (Ritchie 2011). Intrinsic mechanisms involve changes in the material properties—for example, in a metal the material properties change from elastic to plastic in front of the crack tip. Extrinsic mechanisms act at the location of crack propagation (not in front of the crack) and, in bone, are strongly related to bridging of the crack by “ligaments” of unbroken tissue. For relatively large cracks (the kind in a fracture toughness specimen) a great deal of toughening comes from unbroken “ligaments” of bone tissue that bridge across the faces of the propagating crack. The ligaments hold the faces of the crack together creating a “closure stress”. Examination of the crack faces after failure of a piece of bone finds the remains of numerous ligaments that had to be broken in order to finally fracture the tissue.


Figure 8.7
The extrinsic and intrinsic toughening mechanisms of bone. Crack bridging by uncracked ligaments (large cracks) and by the protein/collagenous bone matrix (small cracks) are very important to bone toughness. Removal of, or damage to, the bone matrix leaves an extremely brittle remnant mineral matrix. The energy absorbing mechanisms of the bone matrix include uncoiling of hidden length, fibrillar sliding and molecular uncoiling, all of which depend on the animal’s genetic background, age and matrix cross-linking (Figure modified from Launey et al. 2010).

There continues to be some debate about the role of microcrack formation in the toughening of bone tissue, but it is clear that younger/tougher bone forms much greater numbers of microcracks during failure than does older more brittle bone (Green et al. 2011). This is likely due to a more functional collagen matrix, a very important contributor to bone fracture toughness (Barth et al. 2011; Russell et al. 2012; Nyman et al. 2005; Nalla et al. 2003). The fracture toughness of bone tissue with the collagen matrix removed is extremely low and almost no ligaments are observed in the wake of the crack tip. Ligament bridging between the faces of microcracks by collagen fibers allows the microcrack to open, changing the shape of the surrounding tissue which consumes energy and thereby blunts propagation. One effect is that arrays of collagen bridged cracks at the micro level provide enough controlled deformation to enable tissue bridging across larger cracks at the macro level. This is an example of a hierarchical dependency in bone tissue where a macroscopic toughening mechanism (i.e. ligament bridging of large macroscopic cracks) depends on a more microscopic toughening mechanism (collagen matrix bridging of microcracks).

As a crack is propagated in a fracture specimen, the stress intensity to propagate the crack could decrease, stay the same or increase. Recall for linear elastic fracture mechanics that: 
$$ K=Cs{\left(\pi a\right)}^{1/2} $$
. Experimentally, the process is to determine “s” and “a” as the crack propagates and then calculate the stress intensity factor “K.” Clearly, the best situation is for the stress intensity factor to increase with crack length so that there is a tendency for the crack to stop propagating. Healthy bone has the property that K increases with crack length resulting in what is called a “rising R-curve” where “R” is for “Resistance” (Fig. 8.8). The name “R-curve” is probably the most obscure in all of bone mechanics. Fortunately the concept is simple: An R-curve plots the changing fracture propagation toughness of the tissue as a crack elongates.


Figure 8.8
The increase in bending fracture toughness with crack length is strongly affected by age (Zimmerman et al. 2012).

Both age and sequential degradation of the bone matrix using radiation correlate with a reduction of the propagation resistance (Fig. 8.9). The radiation experiment strongly shows the importance of the collagen matrix to fracture toughness. The implication of the age related decrease in the propagation resistance is that the collagen matrix is degrading with age in humans. There is a great deal of research currently being done to characterize how age and other conditions in humans affect both the bone matrix and fracture toughness. It is clear at the time of this writing that a significant portion of age related bone fragility in humans is caused by changes in the collagen matrix. What remains to be determined is what is changing in the matrix and whether it can be prevented or treated in vivo.


Figure 8.9
The increase in bending fracture toughness with crack length is strongly reduced by radiation damage to the collagen matrix (Zimmerman et al. 2012).

8.2.8 Crack Growth and Fatigue

Paris (1964) proposed that the number of cycles required for fatigue failure of a specimen with a crack could be related to the crack’s stress intensity factor. His idea was that the crack length increase per load cycle, da/dN, would be proportional to the range of K values experienced during the loading: Δ K = K max − K min. A commonly suggested form for such a relationship is

$$ da/dN=\xi {\left(\varDelta K\right)}^{\zeta } $$

where ξ and ζ are constants. Unfortunately, the Paris equation has not proven to be a consistently valid relationship. It describes the results at intermediate crack growth rates better than at low or high values of da/dN. Within that range, if crack propagation data are presented as a log-log plot of da/dN vs. Δ K, the slope and intercept should yield the coefficients ζ and ξ respectively.

8.3 Fatigue Behavior of Bone

Depending on the fracture toughness of a material, and the magnitude of the applied loads, cracks start and grow more or less rapidly under repetitive loading. In this section we examine the basic fatigue and fatigue damage behavior of bone.

8.3.1 The S-N Curve

The basic means of presenting fatigue data is an S-N curve: a plot of the applied stress or strain vs. the number of cycles required for failure at that load level. A fatigue S-N curve was first measured for bone by King and Evans (1967). Subsequently, in the 1970s and 1980s, several other investigators (notably Carter and co-workers) reported similar experiments, establishing that bone behaves similar to engineering materials in fatigue. That is, its elastic modulus declines as fatigue progresses, the log of N is linearly proportional to the log of S, and cracks can be seen within fatigued bone which is apparently fatigue damage. The concept that the fatigue behavior of bone is similar to that of composite materials was also established in this period.

Fatigue life, which we now represent by N F, is related to the applied stress in a very nonlinear way. When one regresses log N F vs. log S for bone specimens fatigued in various modes of loading, one finds that

$$ {N}_F=c/{S}^q $$

where c is a coefficient and the exponent q is a number between 5 and 15, depending on the type of bone and the mode of loading. Clearly, small changes in load magnitude (S), or the kind of bone and mode of loading (q), can result in very large changes in fatigue life. Caler and Carter (1989) and Pattin et al. (1996) have shown that the fatigue life of human femoral cortex is longer in compression than in tension. Testing in uniaxial tensile and compressive fatigue at 2 Hz, Pattin et al. produced data that, when fitted to Eq. (8.17), had the following coefficients:

$$ {N}_F=1.445\times {10}^{53}/{S}^{14.1}\kern0.37em \left(\mathrm{tension}\right) $$


$$ {N}_F=9.333\times {10}^{40}/{S}^{10.3}\;\left(\mathrm{compression}\right) $$

where the stress range, S, is from zero to a peak stress normalized by the initial elastic modulus. (Therefore, S is also the initial strain, and has units of microstrain.) These data were obtained at superphysiologic strains (2600–6600 με). If one may extrapolate the results to a physiologic peak strain of 2000 με, the fatigue life would be 4.1 million cycles in tension and 9.3 million cycles in compression.

8.3.2 Fatigue Damage in Bone

Although we typically think of microdamage in bone as linear cracks, damage caused by cyclic loading of bone actually comes in different flavors. Three distinct forms of damage can be identified in bone, distinguished by their morphology, their mechanical and physiological roles, and by the manner in which they are repaired. Linear microcracks (Fig. 8.10a) are typically about 40–100 μm “long” in cross-section, but may run for hundreds of microns or more than a millimeter longitudinally in bone (Burr and Martin 1993; Taylor and Lee 1998). They are less than 2 μm “wide” in cross-section and are typically repaired by normal bone remodeling processes in which the crack is resorbed by osteoclasts, and new bone is laid down in its place. If many linear microcracks accumulate, either because of high and repeated stresses or because remodeling is suppressed through disease or treatments for disease (e.g. bisphosphonates used to mitigate osteoporosis), they can degrade the elastic modulus of the bone to the extent that a stress fracture (as in athletes and soldiers), or a complete fracture (as in osteoporotic people who sustain atypical femoral fractures) can occur. A second form of microdamage, diffuse damage (Fig. 8.10b), is composed of a collection of very small cracks, most less than 10 μm long in cross-section. The cracks themselves can be difficult to detect with standard light microscopy, even on stained sections, but can be identified as individual cracks using confocal microscopy (Fazzalari et al. 1998; Vashishth et al. 2000). These cracks probably do not cause a significant degradation of the mechanical properties of bone, but, like linear microcracks, may be important in stress relief when bone is repeatedly loaded. They do not create the signals necessary to stimulate whole bone remodeling (Herman et al. 2010), so why do they not accumulate? Recent observational and experimental evidence suggests that they may heal through an intrinsic matrix repair process in which the defect is eliminated by filling with mineral (Boyde 2003), or in which non-collagenous proteins (perhaps osteopontin) act like a glue to bring the surfaces of bone back into contact (Seref-Ferlengez et al. 2012). Microfractures are a third type of microdamage in bone. These are not cracks at all, but full fractures of trabecular bone, which heal through callus formation and subsequent callus remodeling, just as a full fracture of a long bone would heal. Microfractures have a deleterious effect on the mechanical properties of whole bone as they disrupt the connectivity of the trabecular lattice.


Figure 8.10
Microdamage (indicated by arrows) typical of (a) compressive and (b) tensile regions in a beam loaded in four-point bending. Human femoral cortex, 100-μm-thick section stained with basic fuchsin. Field width, ~500 μm (Griffin et al. 1997).

Thus, fatigue damage is not a narrowly defined quantity in either bone or other materials. In the engineering literature, it has usually been defined theoretically as a parameter that varies from zero in virgin structures to unity in failed structures, based on changes in mechanical properties, but without any specific reference to cracks or other evidence of physical damage, which may be difficult to detect. For example, damage is often defined as the fractional reduction in elastic modulus. Alternatively, when cracks are apparent, as in certain kinds of composite materials, damage may be defined in terms of the numbers or lengths of microscopic cracks that appear after loading.

Cracks are relatively easy to find in normal bone. Frost (1960) first described such damage, and linked it to fatigue. Burr and Stafford (1990) counted 0.14 such cracks/mm2 in the ribs of a 60-year-old man. The number of such cracks increases with age in the human femoral diaphysis and neck cortex (Schaffler et al. 1995), and in the trabecular bone of the femoral head (Mori et al. 1997). Microcracks accumulate exponentially after age 40 (Schaffler et al. 1995). Although the data suggest increased skeletal fragility caused by microcrack damage in aging women, they do not show why some older women fracture and others do not. Mori et al. (1997) found that older women have significantly more microcracks than younger women, but older women who fracture did not have more microcracks than older women who did not fracture.

Microdamage burdens may be higher in trabecular than cortical bone; Wenzel et al. (1996) found approximately 5 microcracks/mm2 in trabecular bone from the spine, without a significant increase with age. In the spine, disk pathology may contribute to microdamage (Hasegawa et al. 1995), either because loads are improperly attenuated or because stress concentrations are created in the vertebral body.

If linear microcracks and diffuse damage both perform the function of stress relief, then why are two different kinds of damage created? This probably has to do with the nature of the stresses, and with the quality of the bone matrix. Linear microcracks are preferentially found in areas of higher compressive stress (Diab and Vashishth 2005), are associated with greater matrix deformation before the cracking occurs (Diab et al. 2006) and may be associated with shear strains/stresses in the matrix caused by the compression (Yeni et al. 2003). About 80–90 % of all linear microcracks in cortical bone are found in the interstitial matrix between osteons where mineralization is high (Schaffler et al. 1995; Norman and Wang 1997; Wasserman et al. 2005). Also, because bone from older individuals tends to be more highly cross-linked and may be more fully mineralized, linear microcracks are found more commonly in older people than younger people, and tend to be on average three times longer (136 μm in older people vs. 63 μm in younger folks) (Diab et al. 2006). This reduces the fatigue life of bone by about 75 % between the ages of 40 and 80 years old. Diffuse damage, on the other hand, is more likely to be found in areas of high tensile stress, and more often seen than linear microcracks in bone from younger people (Diab and Vashishth 2005; Diab et al. 2006). Although stress is dissipated by linear microcracks that are attracted to and trapped by lamellar interfaces, the stress reduction associated with larger areas of smaller cracks initially increases the toughness of bone (Parsamian and Norman 2001), and is likely to be more effective in resisting a catastrophic fracture (Green et al. 2011). When linear cracks form, on the contrary, residual toughness declines. Although some have suggested that linear cracks are simply the natural sequelae to diffuse damage (Parsamian and Norman 2001; Vashishth et al. 1997), the very specific age- location- and stress-associated patterns of these two types of damage (Boyce et al. 1998) make it more likely that they are very distinct forms of damage that are not related by any temporal sequence.

8.4 Creep Behavior of Bone and Its Relationship to Fatigue

As we noted in Chap. 7, bone is viscoelastic. It therefore creeps, that is, it deforms for a prolonged period of time under a constant load. If a bone specimen is loaded to a constant stress well below the ultimate stress, it gradually deforms and eventually fractures. Figure 8.11a shows this behavior for cortical bone from a human femur. The initial strain is immediate and therefore elastic; then, as time goes by, the material deforms nonelastically as the result of damage processes. The strain-time curve is similar to the damage-cycle number curve for fatigue. After a period of rapid creep there is a plateau, and the rate of damage then increases again just before failure. If groups of specimens are loaded to various stress levels, σ, and the time to failure, t F, is recorded, the log-log graph of σ vs. t F is linear (Fig. 8.11b) and described by an equation similar to Eq. (8.17):

$$ {t}_F=A/{\sigma}^B $$

where A and B are coefficients peculiar to the kind of bone and the mode of loading. Caler and Carter (1989) found that the exponent B was about 17 and similar for tensile and compressive creep. On the other hand, the coefficient A was greater for compression than for tension.


Figure 8.11
(a) Typical plot of strain vs. time for a cortical bone creep test to failure. The initial elastic response is followed by relatively constant strain during slow damage accumulation, eventually leading to rapid damage accumulation and failure. (b) Log-log plot of applied stress vs. creep time-to-failure is linear with different behaviors for compression and tension. (c) Cyclic loading from zero to a tensile or compressive stress produces a nonzero mean stress that superimposes creep effects on fatigue behavior. (d) Comparison of creep and fatigue responses for human femoral bone.

If the creep damage (D c) occurs at a constant rate, its formation rate would be

$$ d{D}_c/dt={\sigma}^B/A $$

If the stress varies with time, the creep damage at any time, t, is

$$ {D}_c={\displaystyle {\int}_0^t\Big[{\sigma}^B/A}\Big]dt $$

In this formulation, failure occurs when D c = 1, and the time required can be obtained by solving Eq. (8.22) for this condition. Carter and Caler pointed out that creep and fatigue often occur simultaneously. If a specimen is loaded in tensile fatigue, for example, the stress varies from zero to a peak tensile value. The loading is cyclic and therefore it is “fatigue loading,” but it also has a creep component because there is an average load value that is not zero (Fig. 8.11c). The creep component is only zero if the fatigue loading is “fully reversed,” that is, it cycles between peak tensile and compressive stresses that are equal in magnitude.

If fatigue loading occurs at a constant stress range, S, then the fatigue damage may be written as

$$ {D}_f(t)={R}_Lt{S}^{\beta }/\alpha $$

where R L is the loading rate (number of load cycles/day) and α and β are coefficients. If fracture occurs from fatigue damage alone, then the time to fracture is obtained by setting D F = 1 and solving for t = t F. When damage is accumulating in response to simultaneous creep and fatigue effects, it might be possible to formulate the result as a simple summation:

$$ {D}_{total}={D}_c+{D}_f $$

with D total = 1 at failure. For cyclic loading with a non-zero mean stress, creep and fatigue damage combine to produce failure after N F cycles and at time t F, and

$$ {D}_{total}={\displaystyle {\int}_0^{t_F}\Big[\sigma {(t)}^B/A}\Big]dt+{R}_L{t}_F{S}^{\beta }/\alpha =1 $$

For a zero-tension fatigue test in which stress is a haversine function of time and the peak stress is S, the stress history may be written as

$$ \sigma (t)=\left(1+ \sin 2\pi {R}_Lt\right)S/2 $$

Substituting this function into Eq. (8.22) gives, at failure,

$$ 1=\left(1/A\right){\left(S/2\right)}^B{{\displaystyle {\int}_0^{t_F}\left(1+ \sin 2\pi {R}_Lt\right)}}^Bdt $$

which with two changes of variables can be solved to give

$$ {t}_F=KA/{S}^B $$

for the time to failure in the zero-tension fatigue test. Here,

$$ K=\frac{2^B}{{{\displaystyle {\int}_0^1\left(1+ \sin 2\pi \left(t/{t}_F\right)\right)}}^Bd\left(t/{t}_F\right)} $$

Now compare Eq. (8.20), for time-to-failure in a creep test, to Eq. (8.28), for time-to-failure in a zero-tension fatigue test. The only difference is the coefficient K in Eq. (8.28). If we rewrite these equations in log-log form so as to place stress on the y-axis and time on the x-axis, as is customary, we have

$$ \log S=B \log A-B \log {t}_F\kern1em \left(\mathrm{creep}\right) $$


$$ \log S=B \log KA-B \log {t}_F\kern1em \left(\mathrm{zero}\hbox{-} \mathrm{tension}\ \mathrm{fatigue}\right) $$

The slopes of the two equations are the same but their intercepts are different. Figure 8.11d shows the results of creep and zero-tension fatigue experiments on human femoral bone performed by Carter and Caler (1983). Note that the fatigue data fall along a line with the same slope as the creep data, but displaced up and to the right. The specimens loaded in fatigue required longer to fail at a given stress level because the stress noted on the y-axis was only applied part of the time; in the case of the creep specimens, it was applied continuously.

In later papers, Carter and Caler (1989, 1985) showed that when fatigue stresses are high, so that N F and t F are low, creep damage dominates, and vice versa. This is significant because most fatigue experiments are done with superphysiologic stresses to keep the time necessary to bring the specimen to failure reasonable. See Exercise 8.3. Damage in these experimental specimens is mostly caused by creep. Conversely, bones are fatigued in vivo at relatively low stresses, so N F and t F are large; damage then is mostly caused by fatigue. Insofar as the mechanisms of damage caused by creep and by fatigue are different, the results of laboratory experiments cannot be extrapolated to the in vivo situation. On the other hand, differences between creep and fatigue damage have not been identified. These are important caveats to bear in mind as you read the remainder of this chapter and work through the exercises at the end.

8.5 Fatigue Behavior of Fiber-Reinforced Composite Laminates

Engineers have learned to manufacture materials with exceptional creep and fatigue resistance. These materials limit damage through the presence of lamellae or fibers in their structure. Because bone is a lamellar structure in which both ultrastructural (i.e., collagen fibrils) and micro-structural (i.e., osteons) fibers figure prominently, we can gain some insight about bone’s damage resistance by examining the behaviors of these man-made materials.

8.5.1 The Birth and Growth of Cracks

The resistance of any material to fatigue failure is a function of its resistance to both the initiation and propagation of cracks. These two factors are in turn highly dependent on the microstructural characteristics of the material. Materials that resist the initiation of microcracks often cannot effectively resist their propagation; on the other hand, those materials in which cracks are easily started are often difficult to propagate a crack through. Because the fatigue life of a material is a function of both crack nucleation and growth, a material in which cracks are easily started, but find it difficult to grow, can often provide greater resistance to fatigue failure than one in which cracks are difficult to initiate. In fact, many highly fatigue-resistant materials derive this property primarily from their resistance to crack growth rather than initiation. Bone is such a material.

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May 22, 2017 | Posted by in ORTHOPEDIC | Comments Off on Fatigue and Fracture Resistance of Bone

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