Original ArticlesThree rules for bone adaptation to mechanical stimuli
Introduction
Bone architectures are elegant and structurally efficient as if they were designed based on an engineering blueprint. This blueprint for the skeleton is partially contained within the bone cells’ genetic program, but there is also an epigenetic component of skeletal design that is continuously updated in response to the mechanical forces exerted on the bones. Bone cells begin with the genetic blueprint and sculpt it until the skeletal design meets the loading requirements. This process, termed bone adaptation, requires bone cells to detect mechanical signals in situ and integrate these signals into appropriate changes in the bone architecture. Over 100 years ago, Roux28 and Wolff40 proposed that bone architecture is determined by mathematical laws: The thickness and number of trabeculae (i.e., the distribution of mass) must correspond to the quantitative distribution of mechanical stresses, and the trabeculae must be stressed axially in compression or tension (Figure 1). Pauwels furthered this work to describe the effects of mechanical stresses on long bone cross-sectional shape and fracture healing.23 These laws form the basis of our current concepts of bone adaptation and, from this basis, new concepts are emerging.
A great deal of experimental evidence has been gathered in the last 30 years, and common threads have emerged that allow us to describe the concept of bone adaptation in mathematical terms. Of greatest importance are the following three rules:
- 1.
Bone adaptation is driven by dynamic, rather than static, loading.
- 2.
Only a short duration of mechanical loading is necessary to initiate an adaptive response. Extending the loading duration has a diminishing effect on further bone adaptation.
- 3.
Bone cells accommodate to a customary mechanical loading environment, making them less responsive to routine loading signals.
In this study, the foregoing rules are converted into mathematical formulas and the utility of these formulas is demonstrated. The body of the article is divided into three sections, each describing one of the three rules, and culminates in a general discussion.
Section snippets
Rule 1: dynamic strain stimulus
The nature of the mechanical stimulus for bone adaptation has been debated for over 100 years. What follows is a brief chronicle of thoughts about this issue. In 1892, Wolff proposed that the stresses on the bones determined the bone architecture. Later, Thompson34 pointed out “the very important physiological truth that a condition of strain, the result of stress, is a direct stimulus to growth itself.” In 1964, Frost endorsed Thompson’s view and asserted that not only was mechanical strain
Rule 2: case of diminishing returns
Increased duration of skeletal loading does not yield proportional increases in bone mass. As loading duration is increased the bone formation response tends to saturate. This phenomenon of diminishing returns is best demonstrated in the study by Rubin and Lanyon30 using the isolated avian ulna loading model, and the study by Umemura et al.,39 where rats were trained to jump various numbers of times per day and changes in their tibial and femoral bone mass were measured (Figure 6). The data
Rule 3: bone cells accommodate to routine loading
Bone adaptation is “error-driven,” in other words the abnormal strains applied to the skeleton drive structural change. As stated by Lanyon,18 “the mechanically adaptive response is dominated not by the numerous cycles of ‘normal’ strain change engendered during the predominant activity but rather by far fewer cycles of relatively ‘abnormal’ strain changes produced during unusual loading situations.” This rule reflects accommodation, at a cellular level, that causes bone cells to become
Hydrostatic or shear strains?
Bone adaptation, it is often said, is dependent upon strain magnitude, duration, frequency, history, type (compression, tension or shear), and distribution. The three rules presented here provide a mathematical treatment that integrates the influences of strain magnitude, frequency, duration, and, to some extent, history. The importance of strain type and distribution has not yet been discussed. Generally, principal tensile or compressive strains are considered most important for bone
References (41)
- et al.
Bone curvatureSacrificing strength for load predictability?
J Theor Biol
(1988) - et al.
Trabecular bone density and loading historyRegulation of connective tissue biology by mechanical energy
J Biomech
(1987) - et al.
Functional adaptation in long bonesEstablishing in vivo values for surface remodeling rate coefficients
J Biomech
(1985) - et al.
The adaptation of bone apparent density to applied load
J Biomech
(1995) The success and failure of the adaptive response to functional loading-bearing in averting bone fracture
Bone
(1992)- et al.
Static vs dynamic loads as an influence on bone remodelling
J Biomech
(1984) - et al.
Strain magnitude related changes in whole bone architecture in growing rats
Bone
(1997) - et al.
The influence of strain rate on adaptive bone remodelling
J Biomech
(1982) Homeostatic control of bone structureAn application of feedback theory
Bone
(1991)- et al.
Propagation of a calcium pulse between osteoblastic cells
Biochem Biophys Res Commun
(1992)
An approach for time-dependent bone modeling and remodeling — ApplicationA preliminary remodeling simulation
J Orthop Res
Characterization of osteogenic response to mechanical stimulation in cancellous bone of rat caudal vertebrae
Am J Physiol
Cell-to-cell communication in osteoblastic networksCell line-dependent hormonal regulation of gap junction function
J Bone Miner Res
Morphological evidence of gap junctions between bone cells
Calcif Tissue Int
Mechanotransduction and the functional response of bone to mechanical strain
Calcif Tissue Int
Inducible cyclo-oxygenase (COX-2) mediates the induction of bone formation by mechanical loading in vivo
J Bone Miner Res
Increased bone formation in rat tibiae following a single short period of dynamic loading in vivo
Am J Physiol
The Laws of Bone Structure
Bone “mass” and the “mechanostat”A proposal
Anat Rec
Structural adaptations to mechanical usage (SATMU)1. Redefining Wolff’s law: The bone modeling problem
Anat Rec
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