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Magnetic Particle Imaging for Intraoperative Breast Cancer Margin Assessment and Functional Brain Imaging Erica Ellis Mason

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Magnetic Particle Imaging for Intraoperative Breast Cancer Margin Assessment and Functional Brain Imaging Erica Ellis Mason Magnetic Particle Imaging for Intraoperative Breast Cancer Margin Assessment and Functional Brain Imaging by Erica Ellis Mason B.S., University of California, Santa Barbara (2013) Submitted to the Harvard-MIT Program in Health Sciences and Technology in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the MASSACHUSETTS INSTITUTE OF TECHNOLOGY February 2020 ○c Massachusetts Institute of Technology 2020. All rights reserved. Author................................................................ Harvard-MIT Program in Health Sciences and Technology December 12, 2019 Certified by. Lawrence L. Wald, PhD Professor of Radiology, Harvard Medical School/Affiliated Faculty, HST, MIT Thesis Supervisor Accepted by . Emery N. Brown, MD, PhD Director, Harvard-MIT Program in Health Sciences and Technology/Professor of Computational Neuroscience and Health Sciences and Technology 2 Magnetic Particle Imaging for Intraoperative Breast Cancer Margin Assessment and Functional Brain Imaging by Erica Ellis Mason Submitted to the Harvard-MIT Program in Health Sciences and Technology on December 12, 2019, in partial fulfillment of the requirements for the degree of Doctor of Philosophy Abstract Magnetic Particle Imaging (MPI) is an emerging tracer-based imaging modality that uniquely images the nonlinear magnetization of superparamagnetic iron oxide nanopar- ticles (SPIOs). MPI boasts high sensitivity, zero background signal, positive contrast, fast temporal resolution, and quantitative detection. The field of MPI is currently preclinical, and this work aims to scale MPI to human sizes by developing and val- idating it for two clinical applications: tumor detection and imaging for intraop- erative margin assessment during breast-conserving surgery (BCS), and functional neuroimaging. For margin assessment in BCS, a hand-held Magnetic Particle detec- tor and a small-bore MPI imager are assessed for intraoperative use along with an injected SPIO agent. The goal is to detect positive margins during surgery and thus reduce the need for future reexcision. Both hardware systems are validated using clinically relevant phantoms. For functional Magnetic Particle Imaging (fMPI) of the brain, a continuous time-series MPI imager is developed and validated for imaging of cerebral blood volume (CBV) changes during functional activation. The goal is improved sensitivity beyond the capabilities of current functional imaging modalities. We present initial results of in vivo rodent fMPI in a small-bore imager, and the design of a human head-sized system, with implementation underway. Through the collective development of these MPI hardware systems and validation of their poten- tial for these two clinical applications, this work aims to catalyze the expansion of MPI into the clinical setting. Thesis Supervisor: Lawrence L. Wald, PhD Title: Professor of Radiology, Harvard Medical School/Affiliated Faculty, HST, MIT 3 4 Acknowledgments I have been fortunate in my graduate school experience in many ways, first due to the rare opportunity to build imaging hardware from the ground up in an emerging field, and more importantly, due to the incredible communities within the Martinos Center and Harvard-MIT Health Sciences and Technology. They are not only enthusiastic about science, but care about the impact of their research toward important clinical needs. My overall experience was made possible by so many people both in and out of lab, and I want to thank a few who have most significantly impacted my journey. First and foremost I am grateful to my thesis advisor, Larry Wald. Thank you for envisioning these projects, and for entrusting me to work on them. You have given me great independence while staying excitedly involved in the details. Thank you for your visionary leadership, and for always being so generous with your time. Thank you to Clarissa Zimmerman Cooley, who has been involved hands-on, as a mentor, and as a member of my thesis committee. Clarissa, I would have been very, very lost when I began building coils if I hadn’t been able to learn from your example, and I have learned so much from your thoughtful and insightful approach to research. To my committee chair, Elfar Adalsteinsson. You’ve guided and supported me from the start of my HST career, and your focused, strategic leadership in meetings was instrumental in shaping the trajectory of this thesis. Everyone deserves a mentor like you in their corner. Priscilla Slanetz, thank you for your thoughtful clinical perspective, enthusiasm about the potential applications of MPI, and for helping shape this work to optimize its path toward clinical utility. Jacob White, I have valued and appreciated your insightful comments and ques- tions during our committee meetings. Thank you for encouraging me to challenge my patterns of thinking and to approach my research with fresh perspectives. To my MPI team, Eli Mattingly and Konstantin Herb. Eli, your enthusiasm and excitement about research and science ignites mine every day. You are a wonderful teammate and a strongly independent researcher. Konstantin, we were incredibly lucky to have you join the MPI projects for a short but remarkable six months. Learning both from and alongside you was the most transformative experience of my graduate career. I’m so proud of what we accomplished as a team, and am grateful to consider you both good friends. Danke, dass ihr mein Team seid. Verstärker! To the Martinos Center community and particularly the Wald Lab MRPIGs. Our little corner of the Navy Yard contains so many brilliant individuals who are also genuine and caring. Joe and Emiri Mandeville, thank you for collaborating and enabling our first ever in vivo imaging. Bruce Rosen, for sharing your time, energy and vision with us grad students. To Jason Stockmann, thank you for the continual, behind-the-scenes work you do for the MRPIGs—it does not go unnoticed and is deeply appreciated. To Thomas Witzel, Patrick McDaniel, and Matthew Rosen, thank you for the insightful discussions and sharing your immense technical expertise. To Monika Śliwiak and Krista Fariel, you both work magic in your respective domains to keep the lab running and progressing forward. I also want to thank a number 5 of staff members and student interns who have contributed directly to the hardware presented in this thesis, including but not limited to, Simon Sigalovsky, Sofia Franconi, and Robin Armstrong. Finally, thank you to Melissa Haskell, my first officemate and friend at Martinos. I’ll be forever grateful for your friendship, support, and camaraderie; without it, I’m not sure how I would have made it through those first few years. Thank you to the HST staff and faculty: my academic advisor Thomas Heldt, the HST admin team, Julie Greenberg, Traci Anderson, Joe Stein, and especially Laurie Ward, who greets me with a big smile and hug every time I stop by the office. Cheers to my HST classmates—I’m grateful to have learned alongside you, and a big thank you to my signal processing buddies turned lifelong friends, Richard Fineman and Roman Stolyarov. I am so grateful for my friends outside of grad school—those from home and college who’ve stayed in touch from various corners of the country, as well as the wonderful humans I’ve met and become close to in Cambridge these past few years. Each of you has enriched my life immeasurably. Anne Hébert, I am forever grateful to UCSB Physics and the Weld Lab for bringing us together, and thank goodness you picked Harvard so we could survive our PhDs and Cambridge winters together. I value our friendship so much. I got pretty lucky with my family—immediate, “chosen” extended, and friends who will always be like family. To my parents, George and Stacey, who have shown me firsthand what unconditional love is and are my biggest supporters every day, ILYMTATSITNS. Dad, thank you for being my personal proofreader for every piece of writing I’ve ever sent out into the world (including this!). Lynsie, thank you—for giving and receiving, having and sharing. You’re the best sister and built-in best friend I could have asked for. Finally, to Madison, for teaching me to always stop and smell the flowers. Funding sources: NIH/NIBIB 5T32EB001680 (Neuroimaging Training Program (NTP)) NIH T90DA022759/R90DA023427 (Advanced Multimodal NTP) NSF Graduate Research Fellowships Program (GRFP) 1122374 NIH R24MH106053 NIBIB U01EB025121 6 Contents 1 Introduction 15 1.1 Magnetic Particle Imaging (MPI) background . 17 1.1.1 Physics of MPI . 17 1.1.2 Current state of the field . 24 1.2 Clinical motivation . 25 1.2.1 Breast-conserving surgery (BCS) and the need for intraopera- tive tumor margin analysis . 27 1.2.2 Functional neuroimaging with cerebral blood volume . 38 1.3 Hardware implementation overview . 40 2 MPI simulation 47 2.1 Biot-Savart coil builder module . 47 2.2 Sensitivity map simulator . 48 2.3 2D FFL projection imager simulator . 55 2.4 Discussion . 59 3 Hand-held magnetic particle surface detector 61 3.1 Overall design concept and detection goals . 61 3.2 Version 1 . 62 3.2.1 Design and development . 63 3.2.2 Detection results . 65 3.3 Version 2 . 71 3.3.1 Useful learning experience . 71 7 3.4 Version 3 . 72 3.4.1 Design and development . 72 3.4.2 Detection results and proof-of-concept hand-held use . 80 3.5 Discussion . 83 4 Small-bore MPI imager 89 4.1 System design and development . 89 4.1.1 Transmit/receive chain . 91 4.1.2 Detection sensitivity results . 93 4.1.3 Complex baseline . 96 4.1.4 Gradient/shift hardware . 98 4.1.5 Shift field phase lag . 100 4.2 Imaging results . 103 4.2.1 Imaging sensitivity . 106 4.2.2 Spatial resolution . 107 4.2.3 Temporal resolution . 108 4.2.4 Other considerations . 109 4.3 Imaging of excised lumpectomy specimens: a proof-of-concept intraop- erative margin assessment .
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