Elsevier

Journal of Biomechanics

Volume 36, Issue 10, October 2003, Pages 1487-1495
Journal of Biomechanics

The many adaptations of bone

https://doi.org/10.1016/S0021-9290(03)00124-6Get rights and content

Abstract

Studies concerned with the ‘adaptations’ in bones usually deal with modelling taking place during the individual's lifetime. However, many adaptations are produced over evolutionary time. This survey samples some adaptations of bone that may occur over both length scales, and tries to show whether short- or long-term adaptation is important. (a) Woven and lamellar bone. Woven bone is less mechanically competent than lamellar bone but is frequently found in bones that grow quickly. (b) Stress concentrations in bone. Bone is full of cavities that potentially may act as stress concentrators. Usually these cavities are oriented to minimise their stress-concentrating effect. Furthermore, the ‘flow’ of lamellae round the cavities will still further reduce their stress-concentrating effect, but the elastic anisotropy of bone will, contrarily, tend to enhance it in normal loading situations. (c) Stiffness versus toughness. The mineral content of bone is the main determinant of differences in mechanical properties. Different bones have different mineral contents that optimise the mix of stiffness and toughness needed. (d) Synergy of whole bone architecture and material properties. As bone material properties change during growth the architecture of the whole bone is modified concurrently, to produce an optimum mechanical behaviour of the whole bone. (e) Secondary remodelling. The formation of secondary osteones in general weakens bone. Various suggestions that have been put forward to account for secondary remodelling: enabling mineral homeostasis; removing dead bone; changing the grain of the bone; taking out microcracks. (f) The hollowness of bones. It is shown how the degree of hollowness is adapted to the life of the animal.

Introduction

The ability of a bone to function effectively under the loads that are imposed on it depends upon two factors: the properties of the bone material, and arrangement of this material in space—the size and shape of the bone. Most experiments and theory about bone adaptation are concerned with the latter, with the placing or replacing of bony mass. This is usually termed ‘modelling’ and is produced by the probably rather uncoordinated activity of bone cells. It should be distinguished from ‘remodelling’ which is also a matter of lively concern, particularly where it occurs in cancellous bone, in which osteoclasts and osteoblasts work together in a coordinated sequence to replace bone and usually leave the total amount of bone unaltered, in the form of secondary osteones (Haversian systems). There has been much less concern about the other adaptations that bone may have; in particular there has been little consideration of how bone material properties may be related to the loads falling on the bone. This review surveys some aspects of this subject. It is concerned particularly with distinguishing those properties that can be modified during a single lifetime (short-term adaptation) and those properties that cannot, even though they may be highly adaptive (evolutionary adaptation). There is also, it must be said, a school of thought that suggests that many features of organisms are not adaptive at all, either in the short term, or in evolutionary time. For an entertaining introduction to this view (cited more than 1400 times between 1981 and May 2003) read Gould and Lewontin (1979).

Many matters dealt with here are of some complexity, and the author is no doubt guilty of dogmatism in places. I think this is not very important because the purpose of this review is to point up issues concerning the question of adaptation, rather than to give incontrovertible proof that particular points of view are certainly correct.

Section snippets

Woven and lamellar bone

Mammalian bone exists in two usually fairly distinct forms: woven and lamellar. Woven bone is laid down rapidly, its collagen is fine-fibred, and oriented almost randomly (Weiner and Wagner, 1998). It becomes highly mineralised (Pritchard, 1972). Its osteocytes are approximately isodiametric. Lamellar bone is laid down much more slowly, having a more precisely defined structure. It is arranged in lamellae. The collagen and its associated mineral in these lamellae is oriented in the lamellar

Stress concentrations in bone

Most compact bone tissue is riddled with potential stress concentrators, in the form of blood channels, erosion cavities, osteocyte lacunae and canaliculi. A stress concentrator increases the local stress by a factor, SCF, compared with the stress at a distance from the concentrator. (The values given below are for infinitely large homogeneous solids. In bones of finite size the effects will be somewhat smaller.) The extent to which these stress concentrators increase the likelihood of bone

Range of stiffness and toughness in bone

Although most compact bone has roughly the same mechanical properties, there are some really extreme values, ranging from those of some antler bone, which has a Young's modulus of about 5 GPa and is extremely tough (Currey, 1979), to the rostrum of a toothed whale (Mesoplodon densirostris) which has a Young's modulus of about 40 GPa and is extremely brittle (Zioupos et al., 1997). Most of the differences are caused by differences in the amount of mineralisation, although structural anisotropy can

Architecture–material properties synergy

The mechanical properties of whole bones depend both on the material properties of the bone and the architecture of the whole bone. There may be adaptive links between these two features. This is most clearly shown during growth.

Brear et al. (1990) examined a set of five wild polar bear (Ursus maritimus) femurs of known age and weight. The ages ranged from 3 months to 7 years (maturity occurs at about 212 years) and the mass from 9.5 to 400 kg. The bone material was both weaker, having a lower

Secondary remodelling

Internal secondary remodelling is a striking feature of the bone of many ‘higher’ vertebrates, resulting in the production of Haversian bone, in which much of the bone is occupied by secondary osteones (Haversian systems) or interstitial lamellae (the remnants of secondary osteones now cut off from the local blood supply by later secondary remodelling). The reasons for secondary remodelling have been long debated. In the days when bones were seen mainly as temporary stores of calcium and

The hollowness of bones

Most long bones are hollow; this is one of their most striking features. It might seem easy to explain this, because, weight for weight, a hollow cylinder is stiffer and, to a lesser extent, stronger in bending than a solid cylinder. However, the situation is complicated by the fact that the great majority of these hollow long bones are filled with fat. In early life the fat is red and haematopoeitic, but with maturity it is converted to yellow fat, which seems to have little physiological

Conclusions

This survey gives some examples of how bones are adapted to their circumstances. There is a spectrum of immediacy in this adaptation. Some features, such as the amount of mineralisation, are determined in evolutionary time while others, like the positioning of secondary osteons in damaged bone, develop quickly during the life of the animal. Other features are determined both long term and short term. The main purpose of this survey is to remind readers that there are many more adaptations in

Acknowledgements

I thank Steve Cowin for persuading me to write this review and for pointing out that anisotropy had an effect on stress concentrations, and I thank two referees for making important criticisms and suggestions.

References (47)

  • P.J. Atkinson et al.

    The development of osteoporosis. A hypothesis based on a study of human bone structure

    Clinical Orthopaedics and Related Research

    (1973)
  • Bentolila, V., Hillam, R.A., Skerry, T.M., Boyce, T.M., Fyrhie, D.P., Schaffler, M.B., 1997. Activation of...
  • A.A. Biewener

    Bone strength in small mammals and bipedal birdsdo safety factors change with body size?

    Journal of Experimental Biology

    (1982)
  • A.A. Biewener

    Allometry of quadrupedal locomotionthe scaling of duty factor, bone curvature and limb orientation to body size

    Journal of Experimental Biology

    (1983)
  • M. Bouvier et al.

    Effect of bone strain on cortical bone structure in macaques (Macaca mulatta)

    Journal of Morphology

    (1981)
  • A. Boyde

    Electron microscopy of the mineralizing front

    Metabolic Bone Disease and Related Research

    (1980)
  • K. Brear et al.

    Ontogenetic changes in the mechanical properties of the femur of the polar bear Ursus maritimus

    Journal of Zoology London

    (1990)
  • P. Burton et al.

    Haversian bone remodeling in the human fetus

    Acta Anatomica

    (1989)
  • D. Carrier et al.

    Skeletal growth and function in the California gull (Larus californicus)

    Journal of Zoology, London

    (1990)
  • J. Castanet et al.

    Expression de la dynamique de croissance dans la structure de l’os périostique chez Anas platyrhyncos. Comptes rendus de l’Academie de Sciences Paris

    Sciences de la vie

    (1996)
  • J. Cohen et al.

    The three-dimensional anatomy of Haversian systems

    Journal of Bone and Joint Surgery

    (1958)
  • J.D. Currey

    Differences in the tensile strength of bone of different histological types

    Journal of Anatomy

    (1959)
  • J.D. Currey

    Differences in the blood-supply of bone of different histological types

    Quarterly Journal of Microscopical Science

    (1960)
  • Cited by (0)

    View full text