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Multimodal Quantitative Imaging in a Canine Model of Osteoarthritis

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Multimodal Quantitative Imaging in a Canine Model of Osteoarthritis Multimodal Quantitative Imaging in a Canine Model of Osteoarthritis Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Maria Isabel Menendez Graduate Program in Comparative and Veterinary Medicine The Ohio State University 2015 Dissertation/Thesis Committee: Michael V. Knopp, Advisor Michael F. Tweedle Thomas J. Rosol David C. Flanigan Copyrighted by Maria Isabel Menendez 2015 Abstract Osteoarthritis (OA) of the knee is a major public health problem that primarily affects the elderly. Almost 10% of the U. S. population suffers from symptomatic knee OA by the age of 60. There are no approved interventions that ameliorate structural progression of this disorder. The increasing importance of imaging in animal models of osteoarthritis for diagnosis, prognostication, and follow-up is of paramount importance and plays a crucial role in increasing our understanding of the etiology of OA and in the development of new therapies. A primary aim of this study was to provide a comprehensive imaging analysis of the whole knee joint serially in a surgically induced in vivo canine model of OA. We elucidated that quantitative magnetic resonance imaging (MRI) markers demonstrated early changes in the cartilage of the knees that underwent anterior cruciate ligament transection (ACLT) relative to the control knee. This study provided evidence that T2 mapping and delayed gadolinium-enhanced MRI of cartilage (dGEMRIC) are imaging markers relevant to the initiation and progression of OA. Conventional radiography knee assessment, the gold standard in OA diagnosis showed OA signs at a later stage of OA, lacking evidence of premature signs of OA. Serial in vivo imaging utilizing 2-deoxy-2- [fluorine-18] fluoro- D-glucose (18F-FDG) and sodium 18 F-fluoride (18F-NaF) Positron Emission Tomography /Computed Tomography (PET/CT) were performed to characterize knee metabolic and remodeling activity. PET was co-registered with MRI to allow us to improve the location of the regions of interest, otherwise unattainable with PET alone. This work demonstrated, providing imaging evidence, that 18F-FDG and 18F-NaF served an ii important role in detecting early OA metabolic and remodeling changes in the knee prior to the expression of gross changes. These in vivo changes, in addition to ex vivo micro- PET/CT using 18F-NaF and histomorphometry assessment provided a more valuable understanding of OA. Radiography in combination with clinical imaging technologies, such as, MRI, PET and microcomputed tomography (μCT) produced multimodal imaging techniques that allowed to merge molecular, functional, and anatomical data. These technologies provide a more precise and rigorous methods for exploring OA animal models in greater depth. Collectively, these findings can be interpreted as strong evidence that imaging markers play an important role in post-traumatic OA and that these markers, aimed to detect early signs in OA, may be used clinically to diagnose and follow up therapy treatments in OA. iii Dedication Dedicated to my parents, Justin Scott, Michael James and Henry Edward Williams and Natalia iv Acknowledgments Dr Menendez was supported by The Wright Center of Innovation in Biomedical Imaging, Department of Radiology at The Ohio State University Wexner Medical Center. A portion of this work was supported by canine research funds provided by the College of Veterinary Medicine at The Ohio State University. The authors would like to thank Drs. Bianca Hettlich, Kristin Lewis, Steven Weisbrode, Lai Wei, Karen Briley, Amir Abduljalil, Daniel Clark, Katherine Binzel, Jun Zhang, Wenbo Wei and Timothy Vojt for professional assistance. I would like to personally thank the five Beagles and five ponies; which allowed us to complete this research and advance our knowledge in osteoarthritis. Special consideration is given to the members of Dr. Menendez’s graduate committee for their constructive comments and support during the course of this work. Finally, Dr. Michael Knopp receives highest appreciation for his role as advisor to Dr. Menendez, and for setting the standard of an outstanding mentor. v Vita 2002………………………………………….Doctor of Veterinary Medicine, Leon University, Spain 2010 to present………………………………Graduate Research Associate, Department of Veterinary Clinical Sciences, The Ohio State University Publications 1. Menendez MI, Ishihara A, Weisbrode S, Bertone A. Radiofrequency energy on Cortical bone and Soft Tissue: a Pilot Study; Clinical Orthopaedics and Related Research. October 2010 Apr; 137(4):890-7. 2. Menendez MI, Clark DJ, Carlton M, Flanigan DC, Jia G, Sammet S, Knopp MV, Bertone AL. Direct Human Adenoviral BMP-2 or BMP-6 Gene Therapy for Bone and Cartilage Regeneration in a Pony Osteochondral Model. Osteoarthritis and Cartilage. 2011 Aug;19(8):1066-75. vi 3. Jennifer A. Dulin, Wm T. Drost, Mitch A. Phelps, Elizabeth M. Santschi, Maria I. Menendez, Alicia L. Bertone. Influence of Exercise on the Distribution of a Radiopharmaceutical (99mTechnetium-Methylene Diphosphonate) Following Intra- Articular Injection in Horses. Am J Vet Res. 2012 Mar; 73(3):418-25. 4. Menendez MI, Phelps MA, Hothem EA, Bertone AL. Pharmacokinetics of methylprednisolone acetate after intra-articular administration and subsequent suppression of endogenous hydrocortisone secretion in exercising horses. Am J Vet Res. 2012 Sep; 73(9):1453-61. 5. Hayam Hussein, Akikazu Ishihara, Maria Menendez, Alicia Bertone. Pharmacokinetics and bone resorption evaluation of a novel Cathepsin K inhibitor (VEL-0230) in healthy adult horses. J Vet Pharmacol Ther. 2014 Dec; 37(6):556-64. 6. Menendez MI, Phelps M, Bertone A. Pharmacokinetics of Betamethasone sodium phosphate and acetate after intra-articular administration and its effect on endogenous hydrocortisone in exercised horses. J. vet. Pharmacol. Therap. 2015 Apr 3. doi: 10.1111/jvp.12229 [Epub ahead of print] vii Fields of Study Major Field: Comparative and Veterinary Medicine Minor Field: Imaging and Translational Medicine viii Table of Contents Abstract ...............................................................................................................................ii Dedication ..........................................................................................................................iv Acknowledgments ...............................................................................................................v Vita .....................................................................................................................................vi List of Tables......................................................................................................................ix List of Figures .....................................................................................................................x Chapter 1: The Role of Imaging in Osteoarthritis………………………………………...1 Chapter 2: Non-Invasive Quantitative Imaging Assessment in an In Vivo Canine Model of Osteoarthritis……………………………………………………………………………....7 Chapter 3: Two-deoxy-2-[fluorine-18] fluoro- D-glucose Positron Emission Tomography /Computed Tomography and co-registered Magnetic Resonance Imaging Knee Assessment after Anterior Cruciate Ligament Transection in an In Vivo Canine Model…………………………………………………………………………………….30 Chapter 4: 18F Fluoride Positron Emission Tomography /Computed Tomography and co- registered Magnetic Resonance Imaging Knee Assessment after Anterior Cruciate Ligament Transection in an In Vivo Canine Model…………………………………………………………………………………….42 Chapter 5: 18F-Fluoride Micro Positron Emission Tomography/ Computed Tomography for Ex Vivo Quantification of Bone Metabolism and Morphometry in a Canine Model of Osteoarthritis……………………………………………………………………………..54 ix References .........................................................................................................................74 Appendix A: Direct Human Adenoviral BMP-2 or BMP-6 Gene Therapy for Bone and Cartilage Regeneration in a Pony Osteochondral Model………………………………………………………………………………….....89 x List of Tables Table A.1. Histomorphometry and gross photograph osteochondral parameters………105 xi List of Figures Figure 2.1. Conventional radiographic scoring showing the overall disease, joint effusion and osteophytes at baseline, 3 and 12 weeks after ACLT. Asterisks (*) showed significant difference (P<0.05). NS: there were no significant differences between groups……..………………………………....…………………………………………...24 Figure 2.2. Mean T2, T1Gd, and MTRasym from ACLT and control articular cartilage in the femoral condyles at baseline, 3, 6 and 12 weeks after ACLT. Asterisks (*) showed significant difference (P<0.05). abc: different letters differ significantly (P<0.05). NS: there were no significant differences between groups…………………………………....25 Figure 2.3. ACLT femoral condyle articular cartilage T2 ROI (A) showing higher T2 than the control contralateral knee (B) at 12 weeks in a T2 color map……………………………………………………………………………………….26 Figure 2.4. dGEMRIC color map ACLT femoral condyle articular cartilage ROIs at baseline (A) 6 weeks (B) and 12 weeks (C) showing decreasing T1Gd over time………………………………………………………………………………………27 Figure 2.5. Representative gross morphology in the control distal femur with an intact ACL (A), articular cartilage lesions in the femoral condyles (B, C and D). Severe synovial pathology with diffuse involvement, severe discoloration and proliferation/fimbriation/thickening with fibrosis and
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