Elsevier

Bone

Volume 54, Issue 1, May 2013, Pages 118-125
Bone

Original Full Length Article
Composition and microarchitecture of human trabecular bone change with age and differ between anatomical locations

https://doi.org/10.1016/j.bone.2013.01.045Get rights and content

Abstract

The microarchitecture of trabecular bone adapts to its mechanical loading environment according to Wolff's law and alters with age. Trabecular bone is a metabolically active tissue, thus, its molecular composition and microarchitecture may vary between anatomical locations as a result of the local mechanical loading environment. No comprehensive comparison of composition and microarchitecture of trabecular bone in different anatomical locations has been conducted. Therefore, the objective of this study was to compare the molecular composition and microarchitecture, evaluated with Fourier transform infrared (FTIR) microspectroscopy and micro-computed tomography (μCT), respectively, in the femoral neck, greater trochanter and calcaneus of human cadavers. Specimens were harvested from 20 male human cadavers (aged 17–82 years) with no known metabolic bone diseases. Significant differences were found in composition and microarchitecture of trabecular bone between the anatomical locations. Compositional differences were primarily observed between the calcaneus and the proximal femur sites. Mineralization was higher in the greater trochanter than in the calcaneus (+ 2%, p < 0.05) and crystallinity was lowest in the calcaneus (− 24%, p < 0.05 as compared to the femoral neck). Variation in the composition of trabecular bone within different parts of the proximal femur was only minor. Collagen maturity was significantly lower in greater trochanter than in femoral neck (− 8%, p < 0.01) and calcaneus (− 5%, p < 0.05). The greater trochanter possessed a less dense trabecular bone microarchitecture compared to femoral neck or calcaneus. Age related changes were mainly found in the greater trochanter. Significant correlations were found between the composition and microarchitecture of trabecular bone in the greater trochanter and calcaneus, indicating that both composition and microarchitecture alter similarly. This study provides new information about composition and microarchitecture of trabecular bone in different anatomical locations and their alterations with age with respect to the anatomical loading environments.

Highlights

► Molecular composition and microarchitecture of human trabecular bone in the femoral neck, greater trochanter and calcaneus was quantified and compared. ► Micro-computed tomography and Fourier transform infrared spectroscopy were used to evaluate the microarchitecture and molecular composition, respectively. ► We found significant differences in the molecular composition and microarchitecture of trabecular bone between different anatomical locations.

Introduction

Trabecular bone microarchitecture is adapted to the local mechanical environment according to Wolff's law [1], [2]. Moreover, the microarchitecture also changes as the individual ages [3]. Trabecular bone is a metabolically very active tissue, resulting in possible changes in the composition due to loading or aging [4], [5]. Hence, the molecular composition and microarchitecture of trabecular bone may vary between different anatomical locations due to different mechanical loading and remodeling rates.

Dual energy X-ray absorptiometry (DXA) provides a measure of the areal bone mineral density (BMD). However, the effects of bone thickness and the degree of mineralization cannot be directly distinguished by DXA. Therefore, BMD measured by DXA alone cannot fully depict or predict bone mechanical properties or fracture risk [6], [7], [8]. Other important factors for predicting fracture risk include, e.g. geometry [9], [10], micro-damage [11], composition [12], [13] and trabecular bone microarchitecture [14], [15]. The combined effect of all of these factors defines the bone quality, which depends on the structural and compositional parameters as well as the mechanical properties [16]. Thus, to understand the mechanisms that affect bone strength, it is important to understand both the microarchitecture and the molecular composition.

Micro-computed tomography (μCT) can be used to quantify the microarchitecture of trabecular bone [17], [18], [19]. The evaluation of three-dimensional morphology of trabecular bone provides an estimation of several indices, such as bone volume fraction (BV/TV), average trabecular thickness (Tb.Th), separation (Tb.Sp) and number (Tb.N) as well as information about the trabecular plate-rod-like shape (structural model index, SMI) and the degree of anisotropy (DA). These indices have been used to examine human trabecular bone in different anatomical locations, e.g. vertebrae, iliac crest, proximal femur and calcaneal bone [3], [19], [20], [21], [22].

Fourier transform infrared (FTIR) microspectroscopy represents a tool for fast measurements of the spatial molecular composition of bone [4], [5], [23]. In FTIR transmission spectroscopy, a wide band of infrared (IR) light is guided through the sample. The different molecular bonds absorb IR light of different wavelengths and thus an absorption spectrum is created. Several compositional parameters can be calculated from the bone IR spectra. Mineralization can be evaluated from the mineral/matrix ratio (M/M), whereas carbonate substitution is evaluated from the carbonate/phosphate (C/P) ratio [24], [25]. In addition, collagen maturity (C.Mat) [26], and crystallinity [27], [28] can be evaluated through second derivative peak fitting.

The femoral neck has to withstand continuous high compressive and shear forces. During standing these are roughly 1 × BW (body weight), but they can be higher during physical activities (Fig. 1A) [29]. The greater trochanter is mainly subjected to tensile forces from the muscles (e.g. gluteus maximus, medius and minimus) [29] (Fig. 1A), whereas in the calcaneus tensile forces act through the Achilles tendon, plantar fascia and plantar ligaments [30] (Fig. 1B). Since the weight is divided between the heel and forefoot, the calcaneus does not experience as high static compressive loading as the femoral neck. However, the calcaneus has to withstand impact loading during e.g. walking and running, which may be up to 10 × BW [30]. Bone adaptation is driven by dynamic loading [31] which typically increases bone strength through increased cross-sectional area of bone [32], [33]. However, it is possible that concomitant changes in composition occur during adaptation, e.g., the mineral/matrix ratio increases without an increase in cross-sectional area [34]. However, these changes in bone quality have been investigated much more rarely. Hence, trabecular bone adapts to loading environments through modeling and remodeling, which alter its microarchitecture. Moreover, the molecular composition is also altered, at least temporarily, during the process of remodeling [28], [35]. Thus, local compositional and structural evaluations can provide important information about normal development of trabecular bone and its adaptation to different loading environments.

Currently, data on the variation in the composition of trabecular bone at several anatomic sites within the same donor is limited [36]. Specifically, the composition at the femoral neck, greater trochanter and calcaneus within the same donor has not been studied. Thus, in the present study, we quantified and compared the molecular composition and microarchitecture of trabecular bone in the femoral neck, greater trochanter and calcaneus in human donors with healthy bones. Additionally, changes in and relationships between molecular composition and microarchitecture of trabecular bone with age during adult life were investigated.

Section snippets

Experimental overview

Trabecular bone samples were harvested from the femoral neck, greater trochanter and calcaneus of male human cadavers (age range 17–82 years, n = 20) with permission from the National Authority for Medicolegal Affairs (TEO, 5783/04/044/07) (Fig. 1). Medical records were available and none of the cadavers had any known metabolic bone diseases. First, DXA measurements were conducted on the intact proximal femur and calcaneus. Thereafter, two trabecular bone samples (diameter 10 mm, length 10–15 mm)

Results

In order to compare the relative difference in compositional and structural parameters between different anatomical locations within each individual, all parameters were first normalized to the corresponding parameter value in the femoral neck (Fig. 3). Any of the locations could have been selected. The non-normalized values of all parameters are presented in Table 1. For BMD, significant differences (p < 0.01) were found between each anatomical location. BMD was highest in femoral neck and

Discussion

In the present study, the composition and microarchitecture of trabecular bone in the human femoral neck, greater trochanter and calcaneus were studied using FTIR microspectroscopy and micro-computed tomography, and then compared with BMD measurements from the clinical gold standard DXA. The anatomical location and age dependency in these parameters were investigated. Significant differences in the composition and the microarchitecture of trabecular bone were detected between the anatomical

Conclusion

Little is known about the variation in molecular composition of bone across anatomical locations. This study supplements other recent studies investigating this important topic [36], [50]. Moreover, the understanding of the interplay between molecular composition and microarchitecture is still limited. No previous study has addressed the composition of trabecular bone from the human femur neck, greater trochanter and calcaneus. In the present study, significant differences were identified in

Acknowledgments

The research was supported by the strategic funding of the University of Eastern Finland, the Academy of Finland (128863), Kuopio University Hospital (EVO project 5031342, PY 120 musculoskeletal disorders) and the National Doctoral Programme of Musculoskeletal Disorders and Biomaterials (TBDP). We want to acknowledge Ewen MacDonald for wording revision.

References (56)

  • D. Faibish et al.

    Infrared imaging of calcified tissue in bone biopsies from adults with osteomalacia

    Bone

    (2005)
  • R.Y. Huang et al.

    Characterization of bone mineral composition in the proximal tibia of cynomolgus monkeys: effect of ovariectomy and nandrolone decanoate treatment

    Bone

    (2002)
  • M.E. Ruppel et al.

    Chemical makeup of microdamaged bone differs from undamaged bone

    Bone

    (2006)
  • B.R. McCreadie et al.

    Bone tissue compositional differences in women with and without osteoporotic fracture

    Bone

    (2006)
  • A.L. Boskey et al.

    Collagen and bone strength

    J Bone Miner Res

    (1999)
  • J.J. Wolff

    Das gesetz der transformation der knochen

    (1892)
  • E.M. Lochmuller et al.

    Site-specific deterioration of trabecular bone architecture in men and women with advancing age

    J Bone Miner Res

    (2008)
  • M.J. Turunen et al.

    Age-related changes in organization and content of the collagen matrix in rabbit cortical bone

    J Orthop Res

    (2012)
  • M.J. Turunen et al.

    Comparison between infrared and Raman spectroscopic analysis of maturing rabbit cortical bone

    Appl Spectrosc

    (2011)
  • B.R. McCreadie et al.

    Biomechanics of fracture: is bone mineral density sufficient to assess risk?

    J Bone Miner Res

    (2000)
  • M.R. Law et al.

    Strategies for prevention of osteoporosis and hip fracture

    BMJ

    (1991)
  • D. Marshall et al.

    Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures

    BMJ

    (1996)
  • T. Yoshikawa et al.

    Geometric structure of the femoral neck measured using dual-energy X-ray absorptiometry

    J Bone Miner Res

    (1994)
  • I.R. Reid et al.

    Relation between increase in length of hip axis in older women between 1950s and 1990s and increase in age specific rates of hip fracture

    BMJ

    (1994)
  • D.B. Burr et al.

    Bone microdamage and skeletal fragility in osteoporotic and stress fractures

    J Bone Miner Res

    (1997)
  • S. Gourion-Arsiquaud et al.

    Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture

    J Bone Miner Res

    (2009)
  • T.E. Ciarelli et al.

    Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls

    J Bone Miner Res

    (2000)
  • D.W. Dempster

    The contribution of trabecular architecture to cancellous bone quality

    J Bone Miner Res

    (2000)
  • Cited by (0)

    View full text