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DISSERTATION SUPPLEMENTING POWDERED HIGH-FIBER FOODS TO ALTER GUT MICROBIAL METABOLISM FOR COLORECTAL CANCER PREVENTION Submitted by Amy Marie Sheflin Department of Food Science and Human Nutrition In partial fulfillment of the requirements For the Degree of Doctor of Philosophy Colorado State University Fort Collins, Colorado Summer 2016 Doctoral Committee: Advisor: Tiffany Weir Corey Broeckling Chris Melby Michael Pagliassotti Copyright by Amy Marie Sheflin 2016 All Rights Reserved ABSTRACT SUPPLEMENTING POWDERED HIGH-FIBER FOODS TO ALTER GUT MICROBIAL METABOLISM FOR COLORECTAL CANCER PREVENTION Trillions of microorganisms populate the human digestive tract and enhance immunity, improve digestion and inhibit pathogens when in healthy balance. However, a disruption of gut community balance is associated with a number of diseases including colorectal cancer (CRC). The purpose of this research was to investigate supplementation with two high-fiber foods, heat stabilized rice bran (SRB) and cooked navy bean powder (NBP), for potential to favorably alter the intestinal environment for CRC prevention. Study 1 aimed to assess differences in stool microbiota and associated metabolites in healthy individuals versus those diagnosed with CRC. Next, two pilot dietary interventions were undertaken (Study 2 and 3), one in healthy individuals and another in CRC survivors. Both pilot studies provided diets supplemented with SRB or NBP or macronutrient matched control foods and changes in stool microbiota and associated metabolites were assessed at baseline and after 2 and 4 weeks. The collective body of this research supports the hypothesis that gut microbiota and their metabolites differ with respect to CRC and that intervention with SRB or NBP can alter this profile. Despite similar increases in dietary fiber intake, SRB induced more significant change to gut microbiota and metabolites possibly due to differing chemical composition of plant fibers. Relative to NBP, SRB is rich in arabinoxylans, which structurally mimic the protective mucins lining the intestinal surface. Changes in both microbiota and metabolites observed with SRB supplementation are consistent with enrichment of glycan-foraging bacteria able to switch ii between dietary glycans (arabinoxylans in this case) and host glycans for energy. Acetate and propionate, potentially beneficial byproducts of microbial fermentation of glycans and other fiber components, increased at 2 weeks in CRC survivors. However, some of the observed changes did not persist at 4 weeks and further research is necessary to determine if more lasting changes are possible with these dietary interventions, as well as whether these altered microbial/metabolite profiles are associated with reduced risk of CRC incidence and recurrence. iii ACKNOWLEDGEMENTS In the middle of our campus at Colorado State University is a larger-than-life metal sculpture complete with a stone bench that is engraved with this quote from Sir Isaac Newton, “If I have seen further than others, it is by standing upon the shoulders of giants.” I have been fortunate to have many giants to lead the way for me during my graduate education. First, I would like to thank my advisor, Dr. Tiffany Weir. I truly had a Most Excellent Advisor in Dr. Weir, because she has provided the perfect balance of sage-like advice and freedom to explore my own ideas and hunches. I will dearly miss our many exciting brainstorming sessions, troubleshooting huddles, and a-ha! moments that have been part of my being on her research team. I am also grateful for my ‘Dream Team’ Graduate Committee: Drs. Corey Broeckling, Chris Melby, and Mike Pagliassotti. Each of them saw greatness in me at times that I could not see it in myself and through their vision I kept moving forward in spite of my own doubts. Each of these individuals also provided resources and guidance indispensible to my finishing this PhD program, I will be forever grateful to each of them for all they have given to me. If there is one person that I am impossibly more grateful for than even these amazing advisors it is my one-of-a-kind, beyond-compassionate husband, John. John has tolerated more than any husband should have to tolerate in the name of science including long-winded conversations about the world-saving superpowers of bacteria and tear-filled grievances of science gone wrong. He is my emotional rock, my best friend, and my soul mate. John, thank you for making it possible for me to chase my unicorns. You earned this PhD every bit as much as I did and if I could give it to you, in honor, I would. iv Johnny and Elwood, I know having a mother in graduate school for many of your formative years has not been easy. There were events that were missed, details overlooked, and long days waiting at the lab for Mom to finish her work. You both truly know about balancing needs in a family even when yours aren’t at the top and you learned it at a young age. I am so proud of both of you and if you learn anything from my graduate school experience I hope it is to believe in your own potential and to stretch yourself to contribute to the world in the way that you love the most. To my parents, I know you haven’t always understood what drives my wild wanderings and I’m sure it was hard for you to see me under so much stress as I’ve challenged myself over many years. You are the largest giants of all, because you loved me and encouraged me and valued me before anyone else did. It’s because of you that I am not afraid of anything and think I can do all the exciting things in this wide world that I might want to try. It’s a rare gift you gave me and I thank you for it. I am incredibly blessed with a wide support net of incredibly inspiring and talented family and friends that are too many to list by name (but I think you know who you are). Some live near and others farther away, some are older than me and some much, much younger, and some I see often, some only rarely. Yet, each of you has given me something unique to fuel me along this journey that it’s impossible to put into words. To all of you dear kindred spirits - thank you. I also have some more formal thanks to make. This research was supported with funding from National Institutes of Health (NIHR21CA161472), the Colorado Agriculture Experiment Station, and International Life Sciences Institute. I would also like to thank CSU Proteomics and Metabolomics Facility for their support for this work and time spent educating me in v understanding metabolomics data. I also appreciate the CSU nutrition science group, Daniel K. Manter (USDA-ARS), and fellow students in the Weir lab for camaraderie and helpful comments on data interpretation/analysis. vi TABLE OF CONTENTS ABSTRACT ................................................................................................................................... ii ACKNOWLEDGEMENTS ........................................................................................................... iv CHAPTER 1: LITERATURE REVIEW ......................................................................................... 1 Importance of whole grains and legumes in food security and human health ............................. 1 Health benefits of fiber consumption ........................................................................................... 2 Selection of two high-fiber foods to be used for the current research ......................................... 4 Nutrient and phytochemical composition of stabilized rice bran (SRB) ..................................... 5 Heat stabilization of rice bran ...................................................................................................... 7 Nutrient and phytochemical composition of cooked navy bean powder (NBP) .......................... 8 Gut microbiota, diet and disease ................................................................................................ 10 Research Objectives ................................................................................................................... 11 Figures ........................................................................................................................................ 14 CHAPTER 2: SPECIFIC TOPIC REVIEW CANCER-PROMOTING EFFECTS OF MICROBIAL DYSBIOSIS ............................................................................................... 15 Summary .................................................................................................................................... 15 Introduction ................................................................................................................................ 16 Proposed mechanisms for microbiome involvement in colorectal cancer ................................. 17 Microorganisms associated with tumor occurrence and formation in CRC .............................. 20 Microbiome Involvement in Gastric and Esophageal Cancers .................................................. 22 Microbiome Involvement in Other Forms of Cancer ................................................................. 24 Role of microbial metabolites in cancer development and progression .................................... 26 Conclusion .................................................................................................................................. 28 Figures ........................................................................................................................................ 30 vii CHAPTER 3: STOOL
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