Optimization of digital volume correlation computation in SR‐microCT images of trabecular bone and bone‐biomaterial systems

A micromechanical characterization of biomaterials for bone tissue engineering is essential to understand the quality of the newly regenerated bone, enabling the improvement of tissue regeneration strategies. A combination of microcomputed tomography in conjunction with in situ mechanical testing and digital volume correlation (DVC) has become a powerful technique to investigate the internal deformation of bone structure at a range of dimensional scales. However, in order to obtain accurate three‐dimensional strain measurement at tissue level, high‐resolution images must be acquired, and displacement/strain measurement uncertainties evaluated. The aim of this study was to optimize imaging parameters, image postprocessing and DVC settings to enhance computation based on ‘zero‐strain’ repeated high‐resolution synchrotron microCT scans of trabecular bone and bone‐biomaterial systems. Low exposures to SR X‐ray radiation were required to minimize irradiation‐induced tissue damage, resulting in the need of advanced three‐dimensional filters on the reconstructed images to reduce DVC‐measured strain errors. Furthermore, the computation of strain values only in the hard phase (i.e. bone, biomaterial) allowed the exclusion of large artefacts localized in the bone marrow. This study demonstrated the suitability of a local DVC approach based on synchrotron microCT images to investigate the micromechanics of trabecular bone and bone‐biomaterial composites at tissue level with a standard deviation of the errors in the region of 100 microstrain after a thorough optimization of DVC computation.

[1]  Jérôme Darbon,et al.  Fast nonlocal filtering applied to electron cryomicroscopy , 2008, 2008 5th IEEE International Symposium on Biomedical Imaging: From Nano to Macro.

[2]  Philipp Schneider,et al.  Deformable image registration and 3D strain mapping for the quantitative assessment of cortical bone microdamage. , 2012, Journal of the mechanical behavior of biomedical materials.

[3]  H. Gundersen,et al.  Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. , 1993, Bone.

[4]  Gianluca Tozzi,et al.  Composite Hydrogels for Bone Regeneration , 2016, Materials.

[5]  Simo Saarakkala,et al.  Automatic Segmentation of Bone Tissue from Computed Tomography Using a Volumetric Local Binary Patterns Based Method , 2017, SCIA.

[6]  E. Dall’Ara,et al.  Effect of SR-microCT radiation on the mechanical integrity of trabecular bone using in situ mechanical testing and digital volume correlation. , 2018, Journal of the mechanical behavior of biomedical materials.

[7]  A. Accuracy assessment of a Lucas-Kanade based correlation method for 3D PIV , 2014 .

[8]  Jean-Michel Morel,et al.  Non-Local Means Denoising , 2011, Image Process. Line.

[9]  G. Blunn,et al.  The effect of an alginate carrier on bone formation in a hydroxyapatite scaffold. , 2016, Journal of biomedical materials research. Part B, Applied biomaterials.

[10]  M Viceconti,et al.  About the inevitable compromise between spatial resolution and accuracy of strain measurement for bone tissue: a 3D zero-strain study. , 2014, Journal of biomechanics.

[11]  R. Müller,et al.  Time-lapsed microstructural imaging of bone failure behavior. , 2004, Journal of biomechanics.

[12]  Eric Maire,et al.  In situ observation of ductile fracture using X-ray tomography technique , 2011 .

[13]  Christopher Martin,et al.  Regularization methods for inverse problems in x-ray tomography , 2010, Optical Engineering + Applications.

[14]  Gianluca Tozzi,et al.  Application of digital volume correlation to study the efficacy of prophylactic vertebral augmentation. , 2016, Clinical biomechanics.

[15]  S. Ho,et al.  Strain mapping and correlative microscopy of the alveolar bone in a bone–periodontal ligament–tooth fibrous joint , 2016, Proceedings of the Institution of Mechanical Engineers. Part H, Journal of engineering in medicine.

[16]  Robert O Ritchie,et al.  On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone. , 2010, Bone.

[17]  Gianluca Tozzi,et al.  Three-dimensional local measurements of bone strain and displacement: comparison of three digital volume correlation approaches. , 2015, Journal of biomechanical engineering.

[18]  K. Yeung,et al.  Bone grafts and biomaterials substitutes for bone defect repair: A review , 2017, Bioactive materials.

[19]  Paul E Barbone,et al.  Digital Volume Correlation for Study of the Mechanics of Whole Bones. , 2012, Procedia IUTAM.

[20]  L. Cristofolini,et al.  Precision of Digital Volume Correlation Approaches for Strain Analysis in Bone Imaged with Micro-Computed Tomography at Different Dimensional Levels , 2017, Front. Mater..

[21]  Himadri S. Gupta,et al.  Structure and mechanical quality of the collagen–mineral nano-composite in bone , 2004 .

[22]  B. Bay,et al.  Digital volume correlation: Three-dimensional strain mapping using X-ray tomography , 1999 .

[23]  G. Niebur,et al.  Comparison of the elastic and yield properties of human femoral trabecular and cortical bone tissue. , 2004, Journal of biomechanics.

[24]  Sergey V. Dorozhkin,et al.  Calcium Orthophosphate-Based Bioceramics , 2013, Materials.

[25]  J. Tong,et al.  3D real-time micromechanical compressive behaviour of bone-cement interface: experimental and finite element studies. , 2012, Journal of biomechanics.

[26]  L. Grassi,et al.  Extracting accurate strain measurements in bone mechanics: A critical review of current methods. , 2015, Journal of the mechanical behavior of biomedical materials.

[27]  A J Bodey,et al.  Launch of the I13-2 data beamline at the Diamond Light Source synchrotron , 2017 .

[28]  Molly M. Stevens,et al.  Biomaterials for bone tissue engineering , 2008 .

[29]  Sandra J Shefelbine,et al.  BoneJ: Free and extensible bone image analysis in ImageJ. , 2010, Bone.

[30]  G. Brüggemann,et al.  What do we currently know from in vivo bone strain measurements in humans? , 2011, Journal of musculoskeletal & neuronal interactions.

[31]  P. Doumalin,et al.  3D Strain Field Measurement by Correlation of Volume Images Using Scattered Light: Recording of Images and Choice of Marks , 2007 .

[32]  Mao-Jiun J. Wang,et al.  Image thresholding by minimizing the measures of fuzzines , 1995, Pattern Recognit..

[33]  K. Hing,et al.  Strontium substituted bioactive glasses for tissue engineered scaffolds: the importance of octacalcium phosphate , 2015, Journal of Materials Science: Materials in Medicine.

[34]  Michael Drakopoulos,et al.  A high-throughput system for high-quality tomographic reconstruction of large datasets at Diamond Light Source , 2015, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[35]  Kyle E. Niemeyer,et al.  Three‐dimensional surface texture visualization of bone tissue through epifluorescence‐based serial block face imaging , 2009, Journal of microscopy.

[36]  John Immerkær,et al.  Fast Noise Variance Estimation , 1996, Comput. Vis. Image Underst..

[37]  Harrie Weinans,et al.  An Improved Segmentation Method for In Vivo μCT Imaging , 2004 .

[38]  Qizhi Chen,et al.  Biomaterials for Bone Tissue Engineering , 2013 .

[39]  Jean-Michel Morel,et al.  A Review of Image Denoising Algorithms, with a New One , 2005, Multiscale Model. Simul..

[40]  Olof Svensson,et al.  Data Analysis WorkbeNch (DAWN) , 2015, Journal of synchrotron radiation.

[41]  F. Hild,et al.  Computation of full-field displacements in a scaffold implant using digital volume correlation and finite element analysis. , 2013, Medical engineering & physics.

[42]  E. Maire,et al.  In Situ Experiments with X ray Tomography: an Attractive Tool for Experimental Mechanics , 2010 .

[43]  Asadul Haque,et al.  1-D Compression Behaviour of Acid Sulphate Soils Treated with Alkali-Activated Slag , 2016, Materials.

[44]  M. Viceconti,et al.  Local displacement and strain uncertainties in different bone types by digital volume correlation of synchrotron microtomograms. , 2017, Journal of biomechanics.

[45]  Ferry Schrijer,et al.  Effect of predictor–corrector filtering on the stability and spatial resolution of iterative PIV interrogation , 2008 .

[46]  Max A. Viergever,et al.  Quantitative evaluation of convolution-based methods for medical image interpolation , 2001, Medical Image Anal..

[47]  Elena García-Gareta,et al.  Osteoinduction of bone grafting materials for bone repair and regeneration. , 2015, Bone.

[48]  Gianluca Tozzi,et al.  Elastic Full‐Field Strain Analysis and Microdamage Progression in the Vertebral Body from Digital Volume Correlation , 2016 .

[49]  E. Morgan,et al.  Accuracy and precision of digital volume correlation in quantifying displacements and strains in trabecular bone. , 2007, Journal of biomechanics.

[50]  I. Sinclair,et al.  The application of digital volume correlation (DVC) to study the microstructural behaviour of trabecular bone during compression. , 2014, Journal of the mechanical behavior of biomedical materials.

[51]  Gianluca Tozzi,et al.  Microdamage assessment of bone-cement interfaces under monotonic and cyclic compression. , 2014, Journal of biomechanics.

[52]  Pascal Doumalin,et al.  Full 3D Measurement of Strain Field by Scattered Light for Analysis of Structures , 2007 .

[53]  Gianluca Tozzi,et al.  Digital volume correlation can be used to estimate local strains in natural and augmented vertebrae: An organ-level study. , 2016, Journal of biomechanics.

[54]  Fulvio Scarano,et al.  Tomographic PIV: principles and practice , 2012 .

[55]  Hai-Shan Wu,et al.  Iterative thresholding for segmentation of cells from noisy images , 2000 .

[56]  W. Hayes,et al.  Theoretical analysis of the experimental artifact in trabecular bone compressive modulus. , 1993, Journal of biomechanics.

[57]  Egon Perilli,et al.  Application of the digital volume correlation technique for the measurement of displacement and strain fields in bone: a literature review. , 2014, Journal of biomechanics.

[58]  Gianluca Tozzi,et al.  Strain uncertainties from two digital volume correlation approaches in prophylactically augmented vertebrae: Local analysis on bone and cement-bone microstructures. , 2017, Journal of the mechanical behavior of biomedical materials.

[59]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[60]  Gianluca Tozzi,et al.  The use of digital image correlation in the biomechanical area: a review , 2016 .