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Mechanical Characterisation of Biological Materials Using Brillouin IMPERIAL COLLEGE LONDON DEPARTMENT OF BIOENGINEERING Thesis submitted in fulfilment of the requirements for the degree of Doctor of Philosophy Mechanical Characterisation of Biological Materials using Brillouin Microscopy Pei-Jung Wu Supervisors: Dr. Darryl R Overby Prof. Peter Török 1 Abstract Biomechanics studies how biomaterials deform subjected to external loads. Most techniques used in biomechanics require direct contact or lack of subcellular resolution. By contrast, Brillouin microscopy is a contactless and label-free technique used to characterise mechanical properties of cells and tissues. Despite Brillouin microscopy measuring longitudinal modulus 푀 , an empirical power law has been widely used to interpret Brillouin measurements as stiffness. In this thesis, we focused on the interpretation and relevance between the Brillouin microscopy measurements and quasi-static mechanical properties using hydrogels and cells. To investigate how Brillouin measurements relate to the mechanical properties of biological materials, we use hydrogels that approximate the mechanics of biphasic hydrated materials. By varying water content ε and Young’s modulus 퐸 in hydrogels, we found Brillouin measurements reflect changes in ε and the relationship between 푀 and 퐸 arises due to their mutual dependence on ε. We further used binary mixture theory and polymer theory to explain the underlying physics. However, cells are neither passive nor homogeneous, we discussed the assumptions required to relate 푀 and 퐸 to contextualise measurements made. We varied the osmotically active water content ε∗ of cells by controlling the external osmotic stress whilst measuring 푀 and 퐸 . We found both 푀 and 퐸 depends on ε∗ in a manner that can be explained by binary mixture theory and the ideal gas law. However, the correlation between 푀 and 퐸 does not always exist when comparing different cellular components. Furthermore, we also assessed the potential of using Brillouin microscopy as an early diagnostic tool to detect the structural changes of ECM degradation in osteoarthritis (OA). To mimic OA, porcine cartilage was digested by enzyme and our results show that Brillouin microscopy can detect the structure change in OA and hence Brillouin microscopy could develop to a minimally-invasive arthroscope. (word: 300/300) 2 You were not born to live like animals, but to pursue virtue and possess knowledge. -Dante 3 To my grandparents, parents and brothers for the love, joy, and support at all time. 4 Acknowledgements When I was little, people asked me what I wanted to do in the future. My answer was always science. In my mind, doing science is to find the beauty of our universe. After I got my master degree in Taiwan, I had a lot of questions about science, education, society, and the meaning of life. I doubted if perusing science is suitable for people who are not smart enough like me. Then I decided to go to a bigger place to find the answers, and my journey has begun. I thank my supervisors, Dr. Darryl Overby and Professor Peter Török, Dr. Irina Kabakova, for the help of the research. I thank people in Overby lab: Alice Spenlehauer, Anabela Cepa Areias, Ester Reina Torres, Foivos Chatzidimitriou, Jacques Bertrand, Jason Chang, Justino Rodrigues, Michael Madekurozwa; people in Török lab: Chengze Song, Cheryl Seow, Jack Maxwell, and Yuchen Xiang; friends: Anna Stejskalova, Christine Wang, Cynthia Huang, Lucy Huang, Gaelle Chapuis, Martin Shippey, people in the squash teams, active Imperial sessions and FLC club. Co-authors and collaborators: Professor Mengxing Tang, Dr.Carl Paterson, Dr. Jeffery Ruberti, Dr. Iain Dunlop, Maryam Imani Masouleh, Dr. Daniele Dini, Dr. Shengtao Lin and Dr. Joseph Sherwood. I would not be able to finish this challenging project without their support. I have learned a lot from the project as well as from the people. Thanks to these people around me. They gave me support and opinions. They gave me warmth and happiness. They made me think about things that I never thought about. We shared our ideas and the things that we struggled. I am lucky to be able to open myself to all of you and you always welcome me. I will never forget the things I want to do: to be a better person and making the world a better place. Science is not my career. Science is my belief. Science does not serve me. I serve science. I realise I do not need to be smart to do science. I just need to appreciate the mother nature, be humble as a human being, be open to different perspectives and work hard. I thank science for giving me the purpose of my life. This is not the end of the story. My journey will continue. 5 Contribution Statement Several researchers have contributed to the work presented in this thesis. Their contributions are acknowledged below: All chapters: • Dr Darryl Overby, Prof. Peter Török, Dr Carl Paterson, Dr Irina Kabakova and Pei-Jung Wu were involved in the design of research, planning of the experiments, and discussions on data analysis. • Chengze Song and Yuchen Xiang helped for using the Brillouin microscope. • Pei-Jung Wu did the experiments and data analysis. Chapter 3: • Prof. Mengxing Tang and Dr. Shengtao Lin helped for ultrasound experiments. • Dr Jeffrey Ruberti, Dr Joseph Sherwood consulted on data analysis. • Dr Iain Dunlop consulted on the experiments. Chapter 4: • Richard Thorogate (London centre for Nanotechnology) helped for Atomic force microscopy. Chapter 5: • Maryam Imani Masouleh prepared the sample and performed histology. • Dr Daniele Dini consulted on the experiments and data analysis. 6 Copyright and Financial Disclosure I hereby declare that the studies presented in this thesis are my own work, performed in Dr. Overby’s and Prof. Török’s laboratory between October 2014 to November 2017. All data, results and figures from third party works have been referenced. Contributions by other researchers are specified in the Contribution Statement. I certify that this thesis complies with copyright laws and does not contain any instance of plagiarism. This study was supported by a PhD scholarship from the Ministry of Education, Taiwan. The copyright of this thesis rests with the author and is made available under a Creative Commons Attribution-Non Commercial-No Derivatives licence. Researchers are free to copy, distribute or transmit the thesis on the condition that they attribute it, that they do not use it for commercial purposes and that they do not alter, transform or build upon it. For any reuse or distribution, researchers must make clear to others the license terms of this work. 7 Associated Publications Refereed Journal Publications: • Pei-Jung Wu, Maryam Imani Masouleh, Daniele Dini, Carl Paterson, Peter Török, Darryl R Overby, Irina V Kabakova, Detection of Proteoglycan Loss from Articular Cartilage using Brillouin Microscopy, with Applications to Osteoarthritis, Biomed. Opt. Express 10, 2457- 2466, 2019. • Pei-Jung Wu, Irina V Kabakova, Jeffrey W Ruberti, Joseph M Sherwood, Iain E Dunlop, Carl Paterson, Peter Török, Darryl R Overby, Water content, not stiffness, dominates Brillouin spectroscopy measurements in hydrated materials, Nature Methods, 15, 8, pp. 561–562, 2018. Conference Presentations: • Pei-Jung Wu, Irina Kabakova, Jeffrey Ruberti, Joseph M. Sherwood, Iain E. Dunlop, Carl Paterson, Peter Török, Darryl R. Overby, Brillouin microscopy measures water content in hydrated materials, BioBrillouin meeting, Perugia (Italy), Sep 11-14, 2018 (Oral presentation) • Pei-Jung Wu, Irina Kabakova, Jeffrey Ruberti, Joseph M. Sherwood, Iain E. Dunlop, Carl Paterson, Peter Török, Darryl R. Overby, Brillouin microscopy measures water content in hydrated materials, BioMedEng, London (UK), Sep 13-14, 2018 (Poster presentation) • Pei-Jung Wu, Irina Kabakova, Jeffrey Ruberti, Joseph M. Sherwood, Iain E. Dunlop, Carl Paterson, Peter Török, Darryl R. Overby Brillouin microscopy, what is it really measuring?, World Congress of Biomechanics, Dublin (Ireland), Jul 8-12, 2018 (Poster presentation) • P.-J. Wu, I. V. Kabakova, M. Imani Masouleh, D. Dini, P. Török, D.R. Overby, Brillouin spectroscopy for osteoarthritis studies in articular cartilage, BioBrillouin meeting, Vienna (Austria), Sep 13-15, 2017 (Poster presentation) 8 • Pei-Jung Wu, Irina V. Kabakova, ChengZe Song, Carl Paterson, Darryl R. Overby, Peter Török, Mechanical characterisation of hydrogels using Brillouin microscopy, ultrasound and unconfined compression tests, SPIE BiOS, San Francisco (USA), Jan 28 – Feb 2, 2017 (Oral presentation) 9 List of Abbreviations AFM Atomic force microscopy FSR Free spectral range ECM Extracellular matrix GAG Glycosaminoglycan MRI Magnetic resonance imaging MTC Magnetic twisting cytometry NA Numerical aperture NBF Natural buffer formalin OA Osteoarthritis PA Polyacrylamide PBS Phosphate-buffered saline PEO Polyethylene oxide PG Proteoglycan PSF Point spread function RMSE Root mean-squared error SHG Second harmonic generation 10 Symbols 푐 Polymer chain density 푐∗ Overlap concentration 퐸 Young’s modulus 푒 = (푒푥, 푒푦, 푒푧) Strain 퐹(푈, 푇, 푆) Helmholtz free energy 푓0 Frequency of the laser light 푓′ Frequency of the scattered light 퐺 Shear modulus 퐾 Bulk modulus 푘 Boltzmann constant 푀 Longitudinal modulus 푚 Number of independent chains in a hydrogel 푁 Chain length (number of monomers per unit chain) 푛 Refractive index of the material 푛푝푟푠푚 Refractive index of the glass box in the interferometer 푃 Pressure 푝(풓, 푁) Gaussian distribution of the end-to-end distance 푄 Swelling ratio 푅푔 Radius of gyration 푟푙푎푡푒푟푎푙 Lateral minimum resolved distance 푟푎푥푎푙
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