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Plasma and Urine Metabolite Profiles Impacted by Increased Dietary Navy Bean Intake in Colorectal Cancer Survivors: a Randomized-Controlled Trial

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Plasma and Urine Metabolite Profiles Impacted by Increased Dietary Navy Bean Intake in Colorectal Cancer Survivors: a Randomized-Controlled Trial Published OnlineFirst December 24, 2020; DOI: 10.1158/1940-6207.CAPR-20-0270 CANCER PREVENTION RESEARCH | RESEARCH ARTICLE Plasma and Urine Metabolite Profiles Impacted by Increased Dietary Navy Bean Intake in Colorectal Cancer Survivors: A Randomized-Controlled Trial A C Iman Zarei1, Bridget A. Baxter1, Renee C. Oppel1, Erica C. Borresen1, Regina J. Brown2, and Elizabeth P. Ryan1 ABSTRACT ◥ Navy beans contain bioactive phytochemicals with colon (3.89-fold), and urine S-adenosylhomocysteine (2.09-fold) cancer prevention properties as demonstrated in carcino- and cysteine (1.60-fold) represent metabolites with cancer- gen-induced animal models. Human studies support that protective actions following navy bean consumption. Diet- dietary navy bean intake modulates metabolism by the gut derived metabolites were detected in plasma or urine and microbiome. This study investigated the effect of navy bean confirmed for presence in the navy bean intervention ingestion on plasma and urine metabolite profiles of over- meals and snacks. These included 3-(4-hydroxyphenyl) weight and obese colorectal cancer survivors. Twenty parti- propionate, betaine, pipecolate, S-methylcysteine, choline, cipants completed a single-blinded, randomized-controlled eicosapentaenoate (20:5n3), benzoate, S-adenosylhomo- dietary intervention with precooked navy beans (35 g bean cysteine, N-delta-acetylornithine, cysteine, 3-(4-hydroxy- powder/day) or control (0 g/day) for 4 weeks. Plasma and phenyl)lactate, gentisate, hippurate, 4-hydroxyhippurate, urine were collected at baseline, 2 weeks, and 4 weeks and salicylate. The navy bean dietary intervention for following consumption. Nontargeted metabolomics was 4 weeks showed changes to pathways of metabolic impor- applied to study meals and snacks, navy beans, plasma, and tance to colorectal cancer prevention and merit continued urine. Increased navy bean consumption was hypothesized attention for dietary modulation in future high-risk cohort to (i) delineate dietary biomarkers and (ii) promote meta- investigations. bolic shifts relevant for cancer protection in the plasma and urine metabolome. At 4 weeks, 16 plasma and 16 urine Prevention Relevance: This clinical study suggests that metabolites were significantly different in the navy bean increased consumption of navy beans would deliver bioac- intervention group compared with placebo control (P < tive metabolites to individuals at high risk for colorectal 0.05). Increased plasma 2,3-dihydroxy-2-methylbutyrate cancer recurrence and produce metabolic shifts in plasma (1.34-fold), S-methylcysteine (1.92-fold), and pipecolate and urine profiles. Introduction prevention (4–7), and additionally promote lower risk of chronic diseases such as obesity (8–13), cardiovascular dis- Legumes are globally recognized as high-quality sources ease (14, 15), and type II diabetes (16). Hughes and colleagues of dietary fibers with prebiotic functions and are sustainable reported that 59 g of pinto beans per 100 g of diet reduced colon sources of essential amino acids and many other bioactive tumor (azomethane-induced) incidence by 50% in rats com- plant secondary metabolites (1–3). Epidemiologic studies pared with 24% by casein-fed rats (17). Similar to the findings and multiple clinical cohort investigations now support of previous studies, Hangen and Bennink found that diets fed to regular consumption of common beans for colorectal cancer rats containing 75% navy beans resulted in 44% decreased colon tumor and adenocarcinoma incidence (18). The con- 1 1Department of Environmental and Radiological Health Sciences, College of sumption of /2 cup of cooked dry beans per day for adults was Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort practical and significantly increased intake of fiber, protein, and Collins, Colorado. 2University of Colorado School of Medicine, Aurora, Colorado. minerals such as folate, zinc, iron, and magnesium, while Note: Supplementary data for this article are available at Cancer Prevention lowers the intake of saturated fats and total fat (19–21). Research Online (http://cancerprevres.aacrjournals.org/). Emerging evidence exists for diet-derived small molecules to Iman Zarei and Bridget A. Baxter contributed equally to this article. signal as modifiers of cancer risk and tumor behavior. Reliable Corresponding Author: Elizabeth P. Ryan, Colorado State University, 200 West dietary intake assessment methods are required to understand Lake Street, 1680 Campus Delivery, Fort Collins, CO 80523-1680. Phone: 970- the associations between diet, nutritional status, and colon 491-1536; Fax: 970-491-7569; E-mail: [email protected] cancer risk. Nontargeted metabolomics is a well-established Cancer Prev Res 2021;14:497–508 and sensitive tool for the comprehensive and concomitant doi: 10.1158/1940-6207.CAPR-20-0270 characterization of multiple metabolites within a biological Ó2020 American Association for Cancer Research. matrix, and is increasingly applied to cancer research to screen AACRJournals.org | 497 Downloaded from cancerpreventionresearch.aacrjournals.org on September 28, 2021. © 2021 American Association for Cancer Research. Published OnlineFirst December 24, 2020; DOI: 10.1158/1940-6207.CAPR-20-0270 Zarei et al. and discover shifts in metabolism (22, 23). In recent years, that each contained 17.5 g of cooked navy bean powder; ref. 36). metabolomics has also been used for identifying putative The control study arm received placebo meals and snacks biomarkers of food consumption and dietary patterns (24, 25). without the addition of navy bean powder as previously Less is known about whether bioactive food components reach described (34, 36). The study protocol and written informed effective cancer-protective concentrations in people due to consent was approved by the Colorado State University extensive interindividual variability that can occur in host Research Integrity and Compliance Review Board and the digestion and gut metabolism. Some mechanisms linking University Colorado Cancer Center–North Institutional common dry bean consumption and cancer prevention Review Board (Protocol # 09-1530H and 10-1038, respectively) include, but are not limited to, induction of apoptosis and in accordance with the 1964 Helsinki Declaration and its 2013 modulation of cell cycle and proliferation (2, 26, 27). Other amendments. The 20 individuals completed the 4-week mechanisms for common bean intake to inhibit colon carci- pilot dietary intervention trial between August 2010 and nogenesis involve changes to energy metabolism (28) and December 2014. phase II detoxification (29) as shown by tissue microarray analysis in animals. Metabolomics has utility for measuring Blood and urine sample collection for metabolomics downstream products of metabolic disturbances shown by Fasting blood samples were collected into 4-mL ethylene- gene expression and for associations with environmental diamine-tetra-acetic acid (EDTA) blood collection tubes from exposures involved in cancer risk (30, 31). the 20 participants who completed study visits at baseline, Plasma and urine are ideal biological fluids to examine the 2 weeks, and week 4 and kept immediately on ice until the physiologic effects of dietary exposures and have shown sensi- centrifugation step to extract the plasma (1,500 rpm for 10 tivity to detect subtle and major changes in metabolite abun- minutes). Plasma was further stored at À80 C until processed dance over time (32, 33). A nontargeted metabolite approach for metabolomics analysis using ultra-high-performance liquid was applied herein to assess metabolic modulation of colo- chromatography–tandem mass spectrometry (UHPLC-MS/ rectal cancer risk following increased navy bean intake. The MS). At each study visit (baseline, 2 weeks, and 4 weeks), purposeofthisstudywastoassesstheimpactofnavybean participants were given study-labeled containers for self- consumption on the plasma and urine metabolome for collection of first void of the morning urine. Urine was stored colorectal cancer prevention when compared with place- at À80 C until extracted for analysis by UHPLC-MS/MS. bo-control foods, and to identify a suite of metabolites that Urine samples were subjected to the osmolality normalization originated from navy beans. It was hypothesized that using a Fiske 210 Micro-Sample Osmometer to correct for the increased consumption of navy beans would deliver bioac- fluid intake variability between participants. tive metabolites to individuals at high risk for colorectal cancer recurrence and produce metabolic shifts in plasma Plasma and urine extraction for metabolomics and urine profiles. The global nontargeted metabolomics was performed through Metabolon, Inc. The extraction method has been described previously (33). Briefly, 80% methanol was added Materials and Methods on plasma and urine in a ratio of 300 mL solvent per 100 mg Study design and dietary interventions plasma or urine. The samples were shaken for 2 minutes, and Twenty overweight or obese colorectal cancer survivors that then centrifuged for 10 minutes at 4C (12,000 rpm). The were a minimum of 4 months after cancer treatment were metabolite extracts from plasma and urine were analyzed using recruited for this single-blinded, placebo-controlled, random- UHPLC-MS/MS with positive and negative ion mode electro- ized intervention trial as previously described (3, 34, 35). All spray ionization (ESI). the participants were blinded to the study arms, and only the study coordinator was aware of the
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