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Understanding the stability, biological impact, and exposure markers of black raspberries and strawberries using an untargeted metabolomics approach Dissertation Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University By Matthew D. Teegarden, M.S. Graduate Program in Food Science and Technology The Ohio State University 2018 Dissertation Committee Devin G. Peterson Ph.D., Advisor Jessica L. Cooperstone Ph.D., Advisor Steven K. Clinton M.D., Ph.D. David M. Francis Ph.D. 1 Copyrighted by Matthew Daniel Teegarden 2018 2 Abstract Pre-clinical and clinical evidence suggest that dietary berries may help prevent against the development of some chronic diseases such as cardiovascular disease and oral cancer. Berries contain hundreds to thousands of phytochemicals that are thought to act synergistically to produce a wide range of biological effects. While most of the research with berries have been performed with fresh or minimally processed products, thermally processed and stored berry products also represent important dietary sources. The overall goal of this work is to build upon our understanding of the potential role of berry phytochemicals in the prevention of chronic diseases by investigating how they exist in foods and are metabolized by the body. We hypothesize that an untargeted metabolomics approach will provide novel insights to this end. The objective of these studies are to: profile the thermal processing-induced changes in the phytochemical profile of a black raspberry nectar beverage, investigate the impact of storage on the chemistry and bioactivity of this nectar against premalignant oral cancer cells, and profile the urinary metabolome of individuals consuming strawberry- based confections. Thermal processing of black raspberries was shown to lower relative levels of some chemical features, while elevating proportionally more chemical features. Some of the elevated features were characterized as potential phenolic degradation products. The ii stability of several classes of black raspberry (poly)phenolics was also demonstrated. Storage of black raspberry nectar at 4 °C – 35 °C induced large amounts of chemical variation in the product, without markedly affecting its overall bioactivity. A model system that mimicked the chemistry of the stored nectar products indicted that black raspberry phytochemical degradation products may play a role in maintaining the bioactivity of the product. Untargeted metabolomics revealed a chemical signature of strawberry exposure in a free-living population following a low-anthocyanin background diet. These studies support the use of untargeted metabolomics in berry research and provide novel insight that will be useful for the future development and evaluation of berry-based functional foods. iii Dedication To my family and friends iv Acknowledgments First, I would like to thank Dr. Jessica Cooperstone who has been one of my biggest champions and greatest mentors, and her support has never wavered over the past six years. I would also like to thank Dr. Devin Peterson for his willingness to take on a new student before he even moved to Ohio State and for his support ever since. I also owe Dr. Steven Schwartz a debt of gratitude for inspiring me to pursue a Ph.D. I would also like to thank my committee members Dr. Steve Clinton and Dr. David Francis for their advice and guidance throughout my degree. A special thanks to Dr. Tom Knobloch for helping me learn cell culture, and to Dr. Ken Riedl who taught me everything I know about mass spectrometry. Their technical guidance helped me become a more confident scientist. I am so grateful to have met an amazing bunch of students and labmates who passed through the office of Parker 240. To the same end, I am also thankful for my family at the Institute of Food Technologists Student Association. The comradery and support of these friends has been invaluable over the past six years. v I would like to thank the United States Department of Agriculture for providing me with funding throughout my Ph.D. and Dr. Ken Lee for administering this funding, as well as his continual support throughout my degree. I would also like to thank Lisa and Dan Wampler for their support of students involved in food and health research. Finally, I would like to thank my family, whose love and support has been constant throughout my education. vi Vita June 2008 .......................................................Sycamore High School, Cincinnati, OH June 2012 .......................................................B.S. Food Science and Technology, Summa cum Laude, The Ohio State University, Columbus, OH August 2012 to present ..................................Graduate Research Associate, Department of Food Science and Technology, The Ohio State University, Columbus, OH August 2012 to July 2013 ..............................University Fellow, The Ohio State University, Columbus, OH August 2014 to July 2017 ..............................USDA National Needs Fellow, The Ohio State University, Columbus, OH December 2014 ..............................................M.S. Food Science and Technology, The Ohio State University, Columbus, OH August 2017 to present .................................Lisa and Dan Wampler Endowed Fellow for Food and Health Research, Department of Food Science and Technology, The Ohio State University, Columbus, OH vii Publications Teegarden, M.D.; Campbell, A.; Cooperstone, J.L.; Tober, K.L.; Schwartz, S.J.; Oberyszyn, T.M. 25-hydroxyvitamin D3 and its C-3 epimer are elevated in the skin and serum of Skh-1 mice supplemented with vitamin D3. Mol. Nutr. Food Res. 2017; 61; 1700293. Cooperstone, J.L.; Tober, K.L.; Riedl, K.M.; Teegarden, M.D.; Cichon, M.J.; Francis, D.M.; Schwartz, S.J.; Oberyszyn, T.M. Tomatoes protect against development of UV- induced keratinocyte carcinoma via metabolomic alterations. Scientific Reports 2017; 7:5106. Ahn-Jarvis, J.H.; Teegarden, M.D.; Schwartz, S.J.; Lee, K; Vodovotz, Y. Modulating conversion of isoflavone glycosides to aglycones by crude beta-glycosidase extracts from almonds and processed soy. Food Chemistry. 2017; 237:685-692. Obodai, M.; Mensah, D.L.N.; Fernandes, Â.; Kortei, N.K.; Dzomeku, M.; Teegarden, M.D.; Schwartz, S.J.; Barros, L.; Prempeh, J.; Takli, R.K.; Ferreira, I.C.F.R. Chemical Characterization and Antioxidant Potential of Wild Ganoderma Species from Ghana. Molecules. 2017; 22: 196. Teegarden, M.D.; Riedl, K.M.; Schwartz, S.J. Chromatographic Separation of PTAD- derivatized 25-hydroxyvitamin D-3 and its epimer from human serum and murine skin. J. Chromatography B. 2015; 991:118-121 Fields of Study Major Field: Food Science and Technology viii Table of Contents Abstract ............................................................................................................................... ii Dedication .......................................................................................................................... iv Acknowledgments............................................................................................................... v Vita .................................................................................................................................... vii List of Tables .................................................................................................................... xii List of Figures .................................................................................................................. xiii Chapter 1. Literature Review.............................................................................................. 1 1.1 Evidence for the role of berries in chronic diseases ............................................. 1 1.1.1 Black Raspberries .......................................................................................... 2 1.1.2 Strawberries ................................................................................................... 5 1.2 Berry Phytochemicals ........................................................................................... 6 1.2.1 Flavonoids ...................................................................................................... 9 1.2.2 Ellagitannins ................................................................................................ 12 1.2.3 Phenolic acids .............................................................................................. 14 1.2.4 Phenolic profile and content of Black Raspberries ...................................... 15 1.2.5 Phenolic profile and content of strawberries ............................................... 19 1.3 Absorption and Metabolism of Berry Phytochemicals ....................................... 21 1.3.1 Absorption and Metabolism of Flavonoids.................................................. 22 1.3.2 Absorption and Metabolism of Procyanidins .............................................. 26 1.3.3 Absorption and Metabolism of Ellagitannins .............................................. 27 1.3.4 Absorption and Metabolism of Phenolic Acids ........................................... 31 1.4 Effects of Food Processing and Storage on Berry (Poly)phenols ....................... 32 1.4.1 Processing Effects ........................................................................................ 40 1.4.2 Effects of Storage ......................................................................................... 44 1.4.3 Effects
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