Elsevier

Bone

Volume 23, Issue 5, November 1998, Pages 399-407
Bone

Original Articles
Three rules for bone adaptation to mechanical stimuli

https://doi.org/10.1016/S8756-3282(98)00118-5Get rights and content

Abstract

The primary mechanical function of bones is to provide rigid levers for muscles to pull against, and to remain as light as possible to allow efficient locomotion. To accomplish this bones must adapt their shape and architecture to make efficient use of material. Bone adaptation during skeletal growth and development continuously adjusts skeletal mass and architecture to changing mechanical environments. There are three fundamental rules that govern bone adaptation: (1) It is driven by dynamic, rather than static, loading. (2) Only a short duration of mechanical loading is necessary to initiate an adaptive response. (3) Bone cells accommodate to a customary mechanical loading environment, making them less responsive to routine loading signals. From these rules, several mathematical equations can be derived that provide simple parametric models for bone adaptation.

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

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