Dynamic structure and composition of bone investigated by nanoscale infrared spectroscopy

PLoS One. 2018 Sep 4;13(9):e0202833. doi: 10.1371/journal.pone.0202833. eCollection 2018.

Abstract

Bone is a highly organized tissue in which each structural level influences the macroscopic and microscopic mechanical behavior. In particular, the quantity, quality, and distribution of the different bone components, i.e. collagen matrix and hydroxyapatite crystals, are associated with bone strength or fragility. Common spectroscopic techniques used to assess bone composition have resolutions limited to the micrometer range. In this study, our aims were two-fold: i) to develop and validate the AFM-IR methodology for skeletal tissues and ii) to apply the methodology to sheep cancellous bone with the objective to obtain novel findings on the composition and structure of trabecular packets.To develop the methodology, we assessed spatial and temporal reproducibility using a known homogeneous material (polymethylmethacrylate, PMMA). We verified that the major peak positions were similar and not shifted when compared to traditional Fourier Transform Infrared imaging (FTIRI). When AFM-IR was applied to sheep cancellous bone, the mineral-to-matrix ratio increased and the acid phosphate substitution ratio decreased as a function of tissue maturity. The resolution of the technique enabled visualization of different stages of the bone maturation process, particularly newly-formed osteoid prior to mineralization. We also observed alternating patterns of IR parameters in line and imaging measurements, suggesting the apposition of layers of alternating structure and / or composition that were not visible with traditional spectroscopic methods. In conclusion, nanoscale IR spectroscopy demonstrates novel compositional and structural changes within trabecular packets in cancellous bone. Based on these results, AFM-IR is a valuable tool to investigate cancellous bone at the nanoscale and, more generally, to analyze small dynamic areas that are invisible to traditional spectroscopic methods.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Validation Study

MeSH terms

  • Animals
  • Bone Matrix / chemistry
  • Bone Matrix / diagnostic imaging
  • Bone Matrix / drug effects
  • Calcification, Physiologic / drug effects
  • Cancellous Bone / chemistry*
  • Cancellous Bone / diagnostic imaging*
  • Cancellous Bone / drug effects
  • Collagen / chemistry
  • Durapatite / chemistry
  • Microscopy, Energy-Filtering Transmission Electron
  • Nanotechnology / methods*
  • Polymethyl Methacrylate / chemistry
  • Polymethyl Methacrylate / pharmacology
  • Reproducibility of Results
  • Sheep
  • Spectroscopy, Fourier Transform Infrared / methods*

Substances

  • Collagen
  • Polymethyl Methacrylate
  • Durapatite

Grants and funding

The present work was supported by the National Institutes of Health (https://www.nih.gov/), grant AR041325 (ALB), and the National Autonomous University of Mexico (https://www.unam.mx/), grants UNAM-DGAPA-PAPIIT IA207216 and UNAM-MIZTLI SC16-1-IR-90 (EVR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.