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Measurements of Pre-Clinical Liver Perfusion Using Arterial Spin Labelling MRI

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Measurements of Pre-Clinical Liver Perfusion Using Arterial Spin Labelling MRI Measurements of Pre-Clinical Liver Perfusion Using Arterial Spin Labelling MRI Rajiv Ramasawmy, MPhys, MRes. Submitted for the degree of Doctor of Philosophy in Medical Physics April 2015 Department of Medical Physics and Bioengineering And Centre for Advanced Biomedical Imaging, Division of Medicine University College London “It’s still magic even if you know how it’s done.” Terry Pratchett - A Hat Full of Sky (2004) 1 Declaration I, Rajiv Ramasawmy, confirm that the work presented in this thesis is my own, except where stated otherwise in the text. This work is based on research which has been conducted by me, during the time period from October 2010 to September 2014 at University College London. Rajiv Ramasawmy 14th August 2015 2 Abstract Magnetic Resonance Imaging (MRI) has been at the focus of medical research as its availability and fidelity has improved in the last thirty years. MRI offers both high spatial resolution and excellent soft tissue contrast compared to complimentary medical imaging techniques, without the need to expose patients to ionising radiation. Novel MRI methods that utilise the intrinsic body water signal are still being developed and refined. Arterial Spin Labelling (ASL) MRI provides a non-invasive method to measure tissue perfusion, which has been extensively applied in the brain, and demonstrated pre-clinically in the heart and kidneys. However, there is currently no literature reporting the development and use pre-clinical liver ASL – possibly due to complex methodology and quantification necessary in small animals. Clinical liver perfusion imaging is predominantly carried out using an injected Gadolinium- based contrast agent; this technique can be challenging to quantify, cannot be immediately re-administered and may have complications for patients with renal impairment. A methodology to measure liver perfusion without the need for a contrast agent would find utility in a number of different hepatic diseases; monitoring pathophysiology and therapy efficacy. This research investigates the feasibility of a pre-clinical measure of liver perfusion using ASL and its potential application to a pre-clinical model of hepatic disease. We aim to apply the method to monitor novel therapy efficacy in pre-clinical disease models, to eventually translate both therapy and hepatic ASL into the clinical environment. 3 Acknowledgements Despite declaring two pages back this work is my own, nothing could be further from the truth. I must thank a number of people for their relentless support, generous patience and unswerving friendships, without which the following thesis would just be 100 blank pages soaked in tears. Firstly, Dr Simon Walker-Samuel, who literally pulled me through the mud. His drive, intuition and ultimately, his friendship has been the fulcrum of my PhD. He has pushed me to be proud of the work I have achieved and so thanks, Simon! I would also be very far behind and, heaven forbid, even more disorganised without Dr Jack Wells joining the team and perennially bringing his enthusiasm. I would like to thank Professor Barbara Pedley and Professor Mark Lythgoe for allowing me to make a mess in their labs, and always willing to have a conversation when needed. Everything I know is thanks to Dr Adrienne Campbell-Washburn. For some reason she never screamed at me to go away, but I’m so grateful that she instead, patiently explained it all. Dr Peter Johnson and I were thrown together, and I am so grateful to have him around as a long-standing collaborator and temporary yoga partner. Dr Manil Chouhan revolutionised my knowledge of the liver, and also gave me hope that I wasn’t crazy to be interested in such an organ. I cannot put in to words what I owe to both Dr Thomas Roberts and Dr Niral Patel, who have been the most fantastic friends and sounding boards in the last few years. A special mention must be passed to Isabel Christie, Holly Holmes, Rupy Ghatrora, Ozy Ismail, Miguel Goncalves, Ben Duffy, Katy Ordidge, Anthony Price, James O’Callaghan, Bernard Siow, Simon Richardson, Magda Sokolska, Adam Badar, Tammy Kalber, Daniel Stuckey and the whole CABI family for making the last few years so enjoyable. I would like to thank my dear friends who have always been a phone call, a smile and a pub away: Valentin Hamy, Charlie Meyrick, Rory Toher, Mat Pannell, Chris Fiander, Nic Clarke, Paul Wahnon, Corrie Lencz, James Sayers, Dan & Terri Amos, Seb Weidt, Anne Faber, Anette Reisjo, Kieran Flew, Damian Hartley, Ben Leonard and Kyle Davison. I am indebted to Julie Desrousseaux, who was inspiring and encouraging throughout my PhD. Finally, to my parents, my brother and my sister. You have always been the perfect blend of supportive, distracting and crazy. Mostly crazy. Lots of love, Raj 4 Publications and Proceedings S. Walker-Samuel, R. Ramasawmy, F. Torrealdea, M. Rega, V. Rajkumar, S.P. Johnson, S. Richardson, M. Gonçalves, H.G Parkes, E. Arstad, D.L. Thomas, R.B. Pedley, M.F. Lythgoe and X. Golay. In vivo imaging of glucose uptake and metabolism in tumors, Nature Medicine; 2013, 19, 1067–1072. R. Ramasawmy, A.E. Campbell-Washburn, J.A. Wells, S.P. Johnson, R.B. Pedley, S. Walker- Samuel and M.F. Lythgoe. Hepatic arterial spin labelling MRI: an initial evaluation in mice. NMR Biomed; 2014, DOI: 10.1002/nbm.3251. M. R. Gonçalves, S. Walker-Samuel, S. P. Johnson, R. Ramasawmy, R. B. Pedley and M. F. Lythgoe. Pulse Oximetry and Independent Component Analysis Separate Systemic from Tumor-specific Influences on Oxygen Spontaneous Fluctuations in Colorectal Carcinomas. British Journal of Cancer; 2015. In print. S. Walker-Samuel, T.A. Roberts, R. Ramasawmy, S.P. Johnson, B. Siow, S. Richardson, M. Gonçalves, D. Pendsé, R.B. Pedley, M.F. Lythgoe. Technical feasibility of interstitial fluid flow measurement in tumours with EVAC MRI. In submission. R. Ramasawmy, S.P. Johnson, T.A. Roberts, D.J. Stuckey, A.L. David, R.B. Pedley, M.F. Lythgoe, B. Siow, S. Walker-Samuel. Monitoring the growth of orthotopic tumour xenograft models: multi-modal imaging assessment with high-field MRI (9.4T), benchtop MRI (1T), ultrasound and bioluminescence. In submission. S.P. Johnson, R. Ramasawmy, A.E. Campbell-Washburn, J.A. Wells, M. Robson, V. Rajkumar, M.F. Lythgoe, R.B. Pedley, S. Walker-Samuel. Hyper-acute changes in liver tumour perfusion measured noninvasively with arterial spin labelling. In submission. Conference Proceedings R. Ramasawmy, S. Walker-Samuel, A. Campbell, S.P. Johnson, J. Wells, R.B. Pedley and M.F. Lythgoe. Look-Locker Arterial Spin Labelling (ASL) of Liver Metastases. Proc Intl Soc Mag Reson Med. 2012; (20); P1520. S.P. Johnson, R. Ramasawmy, A.E. Campbell-Washburn, M. Robson, V. Rajkumar, S. Walker- Samuel, M.F. Lythgoe and R.B. Pedley. Comparison of Arterial Spin Labelling and R2* as Predictive Response Biomarkers for Vascular Targeting Agents in Liver Metastases. Proc Intl Soc Mag Reson Med. 2013; (21); O506. 5 R. Ramasawmy, A.E. Campbell-Washburn, S.P. Johnson, J.A. Wells, R.B. Pedley, S. Walker- Samuel and M.F. Lythgoe. Multi-Slice Look-Locker FAIR for Hepatic Arterial Spin Labelling. Proc Intl Soc Mag Reson Med. 2013; (21); P2188. M. Chouhan, R. Ramasawmy, A.E. Campbell-Washburn, A. Bainbridge, J.A. Wells, N. Davies, R. Mookerjee, S. Punwani, S.A. Taylor, S. Walker-Samuel and M.F. Lythgoe. Measurement of bulk liver perfusion: initial assessment of agreement between ASL and phase-contrast MRI at 9.4T. Proc Intl Soc Mag Reson Med. 2013; (21); P2190. R. Ramasawmy, T.A. Roberts, B. Siow, S.P. Johnson, J.A. Wells, A. Bainbridge, R.B. Pedley, M.F. Lythgoe and S. Walker-Samuel. 1 Tesla Bench-top MRI of a Mouse Model of Colorectal Carcinoma Metastasis in the Liver: Comparison with 9.4 Tesla, Proc Intl Soc Mag Reson Med. 2014; (22); P1153 R. Ramasawmy, M. Chouhan, D.K. Dhar, A.E. Campbell-Washburn, J.A. Wells, R.B. Pedley, M. Malago, R. Mookerjee, S.A. Taylor, M. F. Lythgoe and S. Walker-Samuel. Monitoring of Rat Liver Regeneration following Portal Vein Ligation using MR Volumetry and Hepatic Arterial Spin Labelling, Proc Intl Soc Mag Reson Med. 2014; (22); eP3618. R. Ramasawmy, A.E. Campbell-Washburn, S.P. Johnson, J.A. Wells, R.B. Pedley, S. Walker- Samuel and M.F. Lythgoe. Repeatability and Variability of Pre-Clinical Hepatic Arterial Spin Labelling, Proc Intl Soc Mag Reson Med. 2014; (22); P2725. M.R. Goncalves, S. Walker-Samuel, R. Ramasawmy, S.P. Johnson, R.B. Pedley, and M.F. Lythgoe. Assessment of the response of colorectal tumours to imatinib mesylate therapy using carbogen and hypercapnia gas challenges. Proc Intl Soc Mag Reson Med. 2014; (22); O914. Y. Zhu, R. Ramasawmy, S.P. Johnson, V. Taylor, R.B. Pedley, A. Berger, N. Chattopadhyay, D. Bradley, M.F. Lythgoe, and S. Walker-Samuel. Detection of Acute Response to Proteasome Inhibitor Treatment in Mouse Colorectal Tumour Models Using Amide Proton Transfer (APT) Magnetic Resonance Imaging. Proc Intl Soc Mag Reson Med. 2014; (22); O844. R. Ramasawmy, T.A. Roberts, S.P. Johnson, D.J. Stuckey, A. David, R.B. Pedley, M.F. Lythgoe, B. Siow, S. Walker-Samuel. Multimodal Imaging of a Mouse Model of Colorectal Carcinoma Metastasis in the Liver. Proc Intl Soc Mag Reson Med. 2015; (23); P1094. R. Ramasawmy, J.A. Wells, J.A. Meakin, M. Sokolska, A.E. Campbell-Washburn, S.P. Johnson, R.B. Pedley, M. F. Lythgoe & S. Walker-Samuel. Separation of arterial and portal blood 6 supply to mouse liver and tumour tissue using pseudo-Continuous Arterial Spin Labelling (pCASL). Proc Intl Soc Mag Reson Med. 2015; (23); O532. H. Holmes, R. Ramasawmy, M. Da, N. Powell, M Cardoso, M Modat, S Ourselin, M.F.
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