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Characterization of Zearalenone and Its Metabolites in Older

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Characterization of Zearalenone and Its Metabolites in Older CHARACTERIZATION OF ZEARALENONE AND ITS METABOLITES IN OLDER WOMEN AND THE RELATIONSHIP WITH FOOD INTAKE By TARA MAURO A thesis submitted to the Graduate School-New Brunswick Rutgers, The State University of New Jersey In partial fulfillment of the requirements For the degree of Master of Science Graduate Program in Nutritional Sciences Written under the direction of Dr. Sue A. Shapses And approved by _____________________________________ _____________________________________ _____________________________________ New Brunswick, New Jersey January 2016 ! ! ! ABSTRACT OF THE THESIS Characterization of Zearalenone and its Metabolites in Older Woman and the Relationship with Food Intake by TARA MAURO Thesis Director: Sue A. Shapses, PhD The environmental estrogen, zearalenone (ZEA), is found in the food supply from Fusarium fungal contamination in grains. Zeranol (Ralgro©), a synthetic form of the metabolite α-ZAL, is an FDA approved growth promoter for use in beef cattle. Animal studies have found ZEA to be associated with reproductive impairment. Circulating concentrations of ZEA and its metabolites [α-zearalenol, zeranol, β-zearalenol, β- zearalanol and zearalanone] have not been previously examined in adults and could have an estrogenic effect. The aim of this research was to characterize the free and total Z metabolite concentrations in human serum and urine samples, and determine associations with food intake. A cross-sectional analysis in 48 women (25-69 years, body mass index of 25 ± 5 kg/m2) was conducted. An HPLC/MS/MS technique analyzed for metabolites and an average of three 24-hour food diaries was used to assess intakes. Re-analysis of the metabolites was performed using more strict quantitative criteria. The total (free and conjugated) summed metabolite concentration for urine and serum was 43.8 ± 37.8 ng/mL and 1.8 ± 0.9 ng/mL, respectively. The detection of urinary metabolites ranged from 13-88% and 46-100% for free and total metabolites, respectively. In serum, ! ii ! ! ! detection ranged from 17-92% and 17-100% for free and total, respectively. ZEA showed the highest detection rate of all metabolites in both serum and urine. Women with highest (10-17 oz/day) versus lowest (0-4 oz/day) meat intake had higher total serum metabolite concentrations (2.0 ± 0.9ng/mL) compared to those with low intakes (1.1± 0.8 ng/mL) (p<0.05). After re-analysis with more strict criteria, concentrations for urinary and serum total metabolites were 27.7 ± 22.2 ng/mL and 1.0 ± 0.7 ng/mL, respectively. The detection rates for urinary metabolites ranged from 2-88% (free) and 8-100% (total). Serum metabolite detection ranged from 2-45%(free) and 4-96%(total). Despite the lower detection rate and concentrations, the same significant relationship with meat intake remained. There is a wide range of ZEA and metabolites present in the serum and urine of adult women and total serum concentrations are associated with meat intake. More investigation into the effects of ZEA exposure in humans is necessary. ! iii ! ! ! TABLE OF CONTENTS ABSTRACT OF THE THESIS!..............................................................................................!ii! TABLE OF CONTENTS!........................................................................................................!iv! LIST OF TABLES!....................................................................................................................!v! LIST OF FIGURES!.................................................................................................................!vi! Introduction to Zearalenone!.............................................................................................................!1! Historical Identification ........................................................................................................... 1! Chemical Properties ................................................................................................................. 1! Classification ........................................................................................................................... 2! Sources ..................................................................................................................................... 2! Regulations .............................................................................................................................. 3! Occurrence ............................................................................................................................... 3! Metabolism .............................................................................................................................. 6! Estrogenic Activity .................................................................................................................. 9! Assessment of Exposure in Vivo ........................................................................................... 11! Assessment of Exposure in Humans ...................................................................................... 13! Rationale and Hypothesis!...............................................................................................................!17! Methods!..............................................................................................................................................!19! Subjects and Study Design .................................................................................................... 19! Biomarker Analysis ............................................................................................................... 19! Analysis of Livestock Feed and Selected Food Samples ...................................................... 20! Statistical Analysis ................................................................................................................. 21! Results!.................................................................................................................................................!22! Discussion!...........................................................................................................................................!26! Appendix I: ZEA analysis of selected grains and meats!..........................................................!43! References:!.........................................................................................................................................!45! ! iv ! ! ! LIST OF TABLES Table 1: European regulations for Zearalenone in food…………………………………………………….32 Table 2: Participants demographics………………………………………………...……………………….32 Table 3: Serum concentrations (ng/mL) of zearalenone and metabolites in adult women (n=48)………….33 Table 4: Urinary concentrations(ng/mL) of zearalenone and metabolites in adult women (n=48)……...….33 Table 5: Serum concentrations (ng/mL) of zearalenone and metabolites in adult women (n=48) with strict criteria applied……………………………………………...……………………………………..34 Table 6: Urinary concentrations (ng/mL) of zearalenone and metabolites in adult women (n=48) with strict criteria applied………………………………………...…………………………………………..34 ! v ! ! ! LIST OF FIGURES Figure 1: Structure of Zearalenone (ZEA) and its metabolites………………………………….…………..35 Figure 2: Metabolism of ZEA Phase I: Reduction……………………………………………...........……..36 Figure 3: Metabolism: Phase II-Conjugation…………………………………...…………………………..37 Figure 4: Structure of ZEA Compared to Structure of Estradiol………………………………….………...38 Figure 5: Sum of serum Z metabolites grouped by BMI categories. ……………………………………….39 Figure 6: Sum of serum Z metabolites grouped by meat intake…………………………………………….40 Figure 7: Sum of serum Z metabolites grouped by meat intake-Strict Criteria……………………………..41 APPENDIX Figure A: ZEA Content of Livestock Feeds……………….…………………………………….……….....44 Figure B: ZEA Content of Meat Samples……………………………………………………….…………..44 ! vi 1 Introduction to Zearalenone Historical Identification Zearalenone (ZEA) (Figure 1) was discovered, identified and named by two separate groups of investigators in the 1960s. Christensen et al. found symptoms associated with ZEA in livestock feed more than 50 years ago (1963)[1]. In 1963, herds of young swine in Minnesota that consumed pelleted feeds and were found to have symptoms including: tumefaction of the vulva, prolapsed vagina, and hypertrophy of the mammary glands. The same feed was then fed to guinea pigs and white rats, both of which developed enlarged uteri. In 1964, a herd of swine that was fed grain (30% mold ridden corn and 70% sound corn) developed the same set of symptoms [1]. Christensen and colleagues were able to isolate compounds from the moldy corn, which were not isolated from the sound corn, deemed F-1 and F-2. F-1 was confirmed through various reactions to be ergosterol. F-2 was purified and absorbance spectrum was identified[1]. Urry et al. used nuclear magnetic resonance and mass spectrometric measures to identify the chemical structures of the same compound, F-2, later naming it zearalenone (6-[10-hydroxy-6-oxo-trans-1-undecenyl]-B-resorcyclic acid lactone) due to its structural name in combination with the name of the fungus it is produced by (Fusarium graminearum [teleomorph Gibberella zeae])(1966)[2]. Chemical Properties ZEA is an enantiomer of 6-β-resorcyclic acid lactone I, a member of the class of β-resorcyclates. It was identified as a white crystalline substance, with the chemical molecular breakdown of C18H22O5, with a melting point of 164-165°C[2]. It was also insoluble in water, but soluble
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