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Electromechanical Properties of Bone at the Nanometre and Micrometre Scale

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Electromechanical Properties of Bone at the Nanometre and Micrometre Scale Electromechanical Properties of Bone at the Nanometre and Micrometre Scale by Yuqi Zhang B.Eng Materials, M.Sc Biomed Department of Physics and Energy Materials and Surface Science Institute Thesis submitted in fulfilment of the requirements for the Degree of Doctor of Philosophy Supervisors: Dr. Syed A. M. Tofail (University of Limerick) Dr. Brian Rodriguez (University College Dublin) Prof. Hugh J. Byrne (Dublin Institute of Technology) Submitted to the University of Limerick October 2012 Declaration “I, Yuqi Zhang, hereby declare that this thesis is entirely my own work and has not been submitted to any other university or higher education institute, or for any academic award in this university. Where use has been made of the work of other people, it has been fully acknowledged or referenced.” ___________________________ 28 th September 2012 I Acknowledgements I would like first and foremost to thank my supervisor Dr. Tofail Syed, for all his support, encouragement and advice during my research. He has brought me into a new scientific world and has inspired me with his philosophy and believes of life. He was a true source of inspiration and confidence when I had become lost in my study. I sincerely appreciate the generous research contributions from my co-supervisors – Dr. Brian Rodriguez and Prof. Hugh Byrne. Their patient guidance and excellent advice have driven my scientific achievements to a higher level. I would like to express my gratitude to Dr. Abbasi Gandhi for his academic and personal support throughout my studies. Special thanks are due to Dr. Maros Gregor, Dr. Jacek Zeglinski, Dr. Calum Dickinson, Dr. Fathima Laffir, Dr. Anna Piterina, Dr. Serguei Belochapkine, Dr. James Butler and Dr. Wynette Redington for their assistance in completion of my experiments. Our manager John Mulcahy, my colleagues Karina McNamara, Patrick Cronin, Eoghan Twohigs, Drahomir Chovan and all my friends in University of Limerick deserve credit for helping solve problems, sharing information in the past. Denise Denning and Liam Collin from University College, Dublin for their help with PFM experiments. I am also very grateful to the Joyce and Keely families, who have taken me in and treated me as a part of their family. Finally and never enough thanks to my mum and dad, my wonderful mother in- law Eileen, my families in China and Ireland, for all their constant love, kindness and encouragement. Especially to my husband Ivan, for his love and support. I love you all! II Dedication For Grandmother Josephine Joyce, very sadly missed, (1921-2010) who said to me ‘Never give up on your dreams!’ III Abstract The mechanical and electromechanical behaviour of bone such as elasticity and piezoelectricity have long been considered to be a consequence of its hierarchical architecture, the basic building block of which, at the nanostructural level, is a finely interleaved composite of collagen fibrils and apatite, a substituted calcium orthophosphate. Also, stress generated surface charge in bone in the form of piezoelectricity and streaming potential is believed to be the driving force behind bone remodelling. However, very little is known about the basic mechanism for dissipating stress and surface charge at the local level of organisation between the composites. In this study, the relationship between electromechanical properties of bone and its molecular foundation is investigated. To achieve this, the organic and inorganic constituents of a bovine bone were separated from each other using chemical extraction methods. Microscopic techniques were then employed to analyse the morphology of the unextracted (raw) bone and the results were compared with that of the extracted bone. Chemical characterisation techniques were used to determine the purity of the extracted constituents of bone. The electromechanical properties of bone were studied using both vertical and lateral Piezoresponse Force Microscopy (PFM). To obtain a common framework for comparison of quantitative values obtained for piezoelectricity measured in both nano and microscopic scales, the standard equivalent single crystal structures of bone was resorted. For this, a transformation of reference axes was necessary to take into consideration the PFM probe/sample orientation as well as the mode of scanning. Piezoelectric coefficients measured in lateral PFM (represented as d34 constants) showed a trend of increasing value when the angle of the sample was varied between 0°, 45° and 90° with respect to the bone’s macroscopic axis. The shear piezoelectricity measured by PFM in micro and nanoscopic scale, 3.48±0.08 pC/N and 4.06±0.30 pC/N respectively, are comparable to collagen’s macroscopic piezoelectric constant (1.4 pC/N) and its single crystal equivalent standards (2.89 pC/N). Finally, the work revisited the original investigation of the orientation dependence of macroscopically measured piezoelectricity in light of the PFM technique and suggested that there was a variation in PFM response for bone and collagen if one switches from a transverse lateral measurement to a longitudinal lateral measurement. While the subject matter of this article is bone and collagen, this developed methodology can be useful in quantitative analysis of nano and microscopic piezoresponse measured on any piezoelectric composite or biopolymer possessing uniaxial texture. Keywords: Bone, Piezoelectricity, Orientation dependent, Piezoresponse Force Microscopy IV Table of Contents Declaration .............................................................................................................. I Acknowledgements ................................................................................................ II Dedication ............................................................................................................ III Abstract ................................................................................................................ IV Table of Contents ................................................................................................... V List of Tables........................................................................................................ IX List of Figures ........................................................................................................ X List of Abbreviations......................................................................................... XIV Chapter 1 Introduction ........................................................................................... 1 1.1. Introduction ............................................................................................. 1 1.2. Research Questions and Hypotheses ....................................................... 2 1.3. Methodological Approach: Why Nanoscale Characterisation is Important ............................................................................................................ 2 1.4. Importance of the Study: The Gap in Literature that it Fulfils ................ 4 1.5. Scope of the Thesis: Chapter Overviews ................................................ 8 Chapter 2 Literature Review .................................................................................. 9 2.1. Introduction ............................................................................................. 9 2.2. Anatomy of Bone .................................................................................. 10 2.2.1. Skeletal System .............................................................................. 10 2.2.2. Structure of Bone ........................................................................... 12 2.2.3. Major Types of Bone ..................................................................... 14 2.2.4. Chemical Composition of Bone ..................................................... 19 2.2.5. Bone as a Composite Material ....................................................... 28 V 2.2.6. Bone Growth and Substitutes ......................................................... 28 2.3. Bone Remodelling and Modelling ......................................................... 31 2.4. Mechanical Properties of Bone and its Constituents ............................. 35 2.4.1. Ultimate Strength ............................................................................ 36 2.4.2. Ultimate strain ................................................................................ 39 2.4.3. Hierarchical Organisation and Anisotropic Mechanical Properties of Bone 40 2.4.4. Elastic Properties of Collagen and its Role in Bone ....................... 43 2.4.5. Elastic Properties of Hydroxyapatite .............................................. 45 2.4.6. Mechanical Properties of Bone at the Nanoscale ........................... 49 2.5. Electromechanical Properties of Bone ................................................... 50 2.5.1. Dielectric Properties and Crystal Physics ....................................... 50 2.5.2. Piezoelectricity, Pyroelectricity and Ferroelectricity of Bone ........ 59 2.5.3. Piezoelectricity of Bone at Nanometric scale ................................. 65 2.5.4. Physiological Significance of Piezoelectricity ............................... 70 2.6. Piezoelectric and Micromechanical Modelling of Bone ........................ 72 2.7. Conclusions ............................................................................................ 77 Chapter 3 Methodology: Characterisation Techniques ........................................ 79 3.1 Introduction ...........................................................................................
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