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  • Summary: fracture mechanics of bone

    I posted a question a few weeks ago regarding the use of fracture
    mechanics concepts in the analysis and prediction of fractures of
    bones. Here are the replies I received, plus a few opinions of my
    own.

    I asked why there seemed to be so little in the literature regarding
    the use of fracture mechanics concepts, although a number of people
    have measured (or attempted to measure) the fracture properties of
    bones. Here is what I think:

    (1) Fracture mechanics comes in two main flavours: the work of
    fracture/ critical strain energy release rate/ Gc approach, and the
    critical stress intensity/ Kc approach. Of these, the former uses a
    real material property which is easy to measure and has a proper
    physical meaning, but is very difficult to use to predict fracture
    since it is necessary to account for all of the stored strain energy
    and other energy coming in or out of the system. The latter approach
    is excellent for predicting fracture, from straightforward stress
    analysis, but depends on a variable (the stress intensity) that is an
    artefact of complicated mathematics and has little physical meaning.
    Since the maths that produces this variable assumes that the
    material is homogenous, isotropic and linearly elastic, it is dubious and
    difficult to apply this approach to biological materials such as
    bone.

    (2). Bones do not generally fail by a single large crack, but
    instead by a gradual accumulation of microcracking. In this respect,
    bone is similar to many composites, or to concrete. As a result, a
    continuum damage approach may be more fruitful.

    (3). The additional confounding factor is that bone is constantly
    repairing itself, and arguably exists in a state of permanent damage
    in equilibrium with constant repair processes. This makes the
    argument of Taylor et al. that fatigue processes are a controlling
    influence on bone remodelling seem quite persuasive. I was glad to
    see that this is being followed further.

    My conclusion:
    There are a lot of complications in applying fracture mechanics to
    bones- and fracture mechanics is complicated enough at the best of
    times. In many applications, moreover, it does not provide much
    information of any great value that cannot be obtained by other
    means. However, I suspect that there is still some scope for using
    computational fracture mechanics techniques to understand the
    mechanisms of some fractures, especially where fracture occurs very
    rapidly, for example as a result of an impact.

    Here are the replies I received:

    >From Peter Zioupos:

    Dear Dr Evans
    I saw your request for an exchange of ideas on Fracture mechanics bone
    data and how to use it. As you very well noted there are no studies or
    other work yet where the FM produced parameters have been usefully put
    into practice. This has been pointed out by Melvin in his review
    article of this field in the TRANS ASME 1994 paper. The problem is I
    think very fundamental and has three major directions: what kind of
    material bone really is; what do we expect from FM in the predictive
    sense? and what happens in nature (in-vivo) in fracture problems. 1)
    our perception of bone has changed considerably lately since more and
    more emphasis is given on the 'yielding' properties of bone (as by
    microcracking) in general and around stress concentrators. Bone is now
    safely called semi-brittle and LEFM is inappropriate to use. EPFM
    though may still derive more meaningful parameters in the future. 2)
    predicting critical conditions from the original LEFM results as by
    using the principle of a critical crack length and a critical stress
    intensity factor has also had its day. This approach did not offer
    something new even where it mattered most (in comparing dry.v.wet or
    gresh.v.embalmed bone). 3) the real in-vivo situation is more
    confusing though. Fractures in life are either sudden and catastrophic
    events (where impact properties may have been more relevant to study)
    or slow progressive 'stress fracture' phenomena. In the latter case
    the generation of a great number of microcracks over a length of time
    softens the tissue which is riddled with these tiny non-connecting
    cracks as oppossed to a single major crack driven through the
    structure. The tissue stays intact till the major crack is initiated
    (the critical conditions for which may have more to do with the local
    maximum sustainable density of microcracks than the stress/energy
    conditions at its tip) and invariably once the major crack is started
    the tissue is finished as this macrocrack drives through the tissue in
    very high speed. Therefore, finding the conditions that are needed to
    drive a single major crack through the bone structure (by fatigue
    cycling on CT specimens) is not a desperatelly important task. Even
    for the remodelling studies that you mentioned (Prof Taylor from
    Dublin is having a go at it) the relevant behaviour that matters is
    that of short (physically or even microscopically small) cracks. And
    we know nothing about it! I myself have been very critical of
    applications of FM of the past although I reckon that more holistic
    approaches (as by combining FM and Continuum Damage Mechanics) have a
    lot to offer. I expressed some of these views in
    J.Mat.Sci.29:978-986:1994; Med.Eng.Phys.16:203-212:1994;
    Phil.TransR.Soc.347:383-396:1995; J.Biomech.29:989-1002:1996; and
    Clin.Biomech.11:365-375:1996.

    >From John Hipp :

    Although we have not used classical fracture mechanics to understand
    actual clinical fractures of bones, we have tried many other methods
    that may help to understand the potential role of classical fracture
    mechanics. We have worked for many years to develop good clinical
    guidelines for predicting pathologic fractures in the spine and long
    bones that have metastatic defects. We have completed several
    investigations where simulated defects were created in whole bones and
    the failure load was measured. In most investigations, we also
    measured the failure load of intact bones for comparison. We have
    tried numerous techniques to predict the failure load of the bones,
    including finite element models (with various failure criteria),
    geometric properties from computed tomography and MRI, composite beam
    theory based analysis of CT and MRI data, and bone mineral content.
    For simple loading conditions, axial rigidity measured from CT does an
    excellent job at predicting failure load of intact vertebrae and
    vertebrae with simulated or actual defects (in press right now).
    Composite beam theory does an excellent job of predicting bending,
    axial and torsional failure loads of trabecular bone cores with
    simulated defects (manuscripts in preparation). In both these cases,
    excellent means that the relatively simple measurements that account
    for both the geometry of the bone and defect as well as the bone
    density predict over 90 percent of the variation in measured failure
    loads. Similar results have been reported by several investigators
    using a variety of test methods. These measurements do not account for
    nominal stress concentrations or stresses at crack tips. For the
    proximal femur, the bone mineral content alone predicts between 50 and
    95 percent of the variation in measured failure load, depending on
    whether there is a simulated defect in the bone and how the bone was
    tested. For an engineer, it is surprising that simple measurements
    that do not account for stress concentrations, complex multi-axial
    failure criteria, etc work as well as they do. Perhaps fracture
    mechanics can be used to improve our ability to predict failure loads,
    but there may be even bigger challenges to overcome before clinical
    fractures can be reliably predicted. As was nicely pointed out by in
    1957 by Backman and later strongly emphasized by Hayes and Myers and
    others, predicting failure load is only part of the problem. We also
    need to know the applied loads, and it is not easy to predict all of
    the loads that a bone will see. Finally, after you think you have the
    greatest way to predict failure loads and applied loads, you need to
    prove that your methods are sensitive and specific in clinical
    practice so that clinicains will be believers and insurance will pay.
    This generally requires finding true positive cases of people that
    have fractured and have pre-fracture measurements. Sophisticated
    engineering is only part of the solution.

    You should also read the excellent work of Lakes et al on
    couple-stress effects. There is also alot more literature available on
    fracture mechanics of bone then is suggested by your email as well as
    a growing body of literature on failure criteria for bone. I can send
    some references if requested.

    Good luck

    John A. Hipp, PhD
    Baylor College of Medicine

    >From Edward Draper :

    Sam, Hi

    I've been involved in bone fracture healing mechanics for
    years.

    It's my experience that the biological variability and the
    complexity of bone as a material/structure that trying to
    predict fracture configurations is difficult, except in the
    broadest terms eg spiral fracture is a a sign of a
    torsional load during injury.

    Every day we get in patients who have undergone what appear
    to be very similar modes of injuries with quite dissimilar
    fracture patterns.

    Edward Draper PhD BSc CEng MIMechE MIPEMB
    Principal Research Fellow in Bioengineering
    Royal Postgraduate Medical School


    >From Mark Taylor :

    Dear Dr Evans,

    I am a member of Prof Bonfields group at the IRC in Biomedical
    materials and though I cannot answer your question myself, I suggest
    that you contact Deepak Vashishth (email-D.Vashishth@qmw.ac.uk). He is
    nearing completion of his Ph.D. thesis on the fracture mechanics of
    bone and will probably be able to tell you why this technique has not
    been applied to whole bones.

    (....)

    Kind regards,

    Mark


    >From Craig Nevin :

    Hi Sam.

    I have just submitted a paper on the dynamic functions of the
    metatarsals. I am preparing another on a case study of a second
    metatarsal fracture in a runner, and have looked at primate feet. I
    am toying with various notions concerning bone fractures. My initial
    results look exceptionally good, but I have not yet delved into the
    literature.

    I think a lot of the problem is to do with the fact that most
    biomechanical models use either classical engineering principles which
    do not apply to bone. Also, most biomechanic work is based on muscle
    models. When these are combined to explain bone fractures, they just
    don't add up. Their predictive capacity is less than 50%, which means
    that you can never quite be sure whether the model is right or wrong.

    I am interested in your thoughts on the subject.

    Regards
    Craig Nevin
    Anatomical Engineer

    > Dear Craig,

    > My feeling is that the stress intensity factor approach, being based
    > on all sorts of mathematical assumptions, is unlikely to ever work
    > very well in a non- homogenous, anisotropic composite material such
    > as bone. However, the alternative approach of looking at the strain
    > energy release rate and the work of fracture seems to me to have
    > some potential, being based on fundamental material properties and
    > conservation of energy.

    Sounds promising.

    My ideas on stress fractures are that the bone remodels and resorbs
    at an equal rate. Increased stress merely induces bone healing in the
    microfractures, therefore standard ultimate fatigue strength is a none
    starter. My interest in the matter stems from an unlikely scource. I
    was measuring the kinematics of the metatarsals. To do this I clamped
    the shafts to a table. But as I moved the toe, the bones splintered.
    Now kinematic theory is defined as the study of motion without regard
    to the forces causing that motion. That, I discovered was fine in
    theory but try as I might I could not contrive the circumstances where
    the bones would not fracture. I then relised that the bones are only
    as strong as they need be to cope with the pysiological stress levels.


    Engineers design structures wastefully, huge factors of safety etc.
    But my approach is to learn from the bones, afterall they know EXACTLY
    what the stresses are that they are being subject to.

    It seems to me that you have a similar problem. The rib, for
    example, is stabbed. It breaks because it is not strong enough. My
    metatarsals fractured when I used invasive methods. If I had take the
    simple expedient of amputating the foot before testing the metatarsal,
    it would not have broken. But amputation, I seems to me, is hardly
    the best cure for bone fractures!

    I am therefore interested in (1) the process of bone remodelling as a
    measure of physiological function (2) attempting to understand
    physiological (mechanical) bone structure in terms of bone
    remodelling.

    Based on my kinematic work, I made certain predictions about the
    relative sizes of the metatarsals. The theoretical prediction was
    that the first metatarsal should be four times stronger than the
    second metatarsal in torsion; or twice the diameter. I measured the
    perimeters of the shafts in the main primates. Then I did the stats.
    I predicted a ratio of 2.0; the answer I got was 1.99!

    This prediction was based on equal torsional stress levels in
    all bone, wherever it may be.

    Recently I got a referral from a runner with a stress fracture. We
    recontructed MRI images of the metatarsals. I am now looking at
    relating the thickness of the cortex, to the biomechanical function.
    I have fiddled a bit, looking for patterns, as I believe that the data
    will enable me to make certain predictions on the precise mechanisms
    of bone remodelling. If I can recognize a pattern the theory must
    follow. Early stages and its digressing from my thesis.

    But, I am going to rigorously pull the data apart and see what I can
    make of it. But I first have to seen what has been done in the
    literature, and would like to know what curveballs to throw at my
    predictions.

    You comments

    Craig

    Dear Craig,

    There is a huge amount of literature about bone remodelling,
    associated especially with Rik Huiskes et al. at the University of
    Nijmegen. In particular Harry Weinans and subsequently Margarite (?)
    Mullender have developed a model that produces a realistic trabecular
    architecture from a simple remodelling theory by a chaotic process.
    You might be able to apply some of this work to your problems- I don't
    see why you shouldn't be able to work backwards from the structure of
    the bone to deduce its function. Also Patrick Prendergast has
    apparently done more work on the fatigue/ bone remodelling theory that
    I mentioned in my original query.

    Best wishes,

    Sam.


    >From Tom Persing :

    Dr. Evans,

    I am interested in hearing your responses. If it is convenient, you
    may simply forward relevant responses to me. If you were planning on
    summarizing the responses and posting the summary to the list, that
    would also work for me.

    I work the forensic side of the business, mainly car accidents. I've
    seen some literature a while back, but don't remember where it was.
    I'll do some digging and see if I can come up with it. Tom Persing
    lab@airmail.net


    >From viceconti@tecno.ior.it (Marco Viceconti):

    I'll tell you my opinion soon on your question; meanwhile look at

    Viceconti, M. and Seireg, A. A generalized procedure for predicting
    bone mass regulation by mechanical strain. Calcif Tissue Int
    47:196-301, 1990

    and to works from Patrick Prendergast on J biomechanics; both works
    assume the bone microfractures as the stimuli for the bone
    remodelling. David Taylor was at that time the advisor of Patrick.


    Marco


    Thanks once again to all that replied for you intelligent and helpful
    comments.

    Here is my original query again:

    >Does anyone know of any studies that have used fracture mechanics
    >concepts to predict and/ or analyse fractures of bones?
    >
    >My initial study of the literature has confirmed my impression that
    >while there have been a number of studies of the fracture properties
    >of bone (notably by Bonfield et al., Melvin and Evans and Norman et
    >al.), there have been few serious attempts to use the measured
    >properties to predict actual fractures. In fact, apart from an
    >intriguing paper by Taylor, presented at Fatigue '94 (?), which
    >argued that fatigue processes could provide a controlling mechanism
    >for bone remodelling, I don't know of any successful attempts to use
    >fracture mechanics to predict or understand actual clinical fractures
    >of bones.
    >
    >Why have fracture mechanics concepts not been more widely used in
    >this context? I can think of plenty of possible reasons myself- what
    >is your opinion?
    >
    >Thank you very much for your help,
    >
    >Best wishes,
    >
    >Sam.
    Dr. Sam Evans,
    Medical Systems Engineering Research Unit,
    UWC School of Engineering,
    PO Box 688, The Parade,
    Cardiff CF2 3TE, UK.
    Tel. (01222) 874533 or (01222) 874000 x5926
    Fax. (01222) 874533
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