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      Dietary Carotenoids and Non-Alcoholic Fatty Liver Disease among US Adults, NHANES 2003–2014

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          Abstract

          Non-alcoholic fatty liver disease (NAFLD) is highly prevalent worldwide. Oxidative stress is thought to be a major mechanism, and previous epidemiological studies found higher serum levels of antioxidant carotenoids were associated with reduced risk for development and progression of NAFLD. The objective of this analysis is to examine cross-sectional associations between dietary and serum levels of carotenoids in relation to NAFLD among a nationally representative sample of US adults. We used data from the 2003–2014 National Health and Nutrition Examination Survey (NHANES). Dietary carotenoid intake was estimated from a 24-hour recall, while serum carotenoids were measured from 2003 to 2006. The NAFLD status was determined based upon US Fatty Liver Index (FLI) value ≥30. Regression models were used to estimate associations between carotenoids and NAFLD by controlling for covariates and adjusting for survey design variables. Overall, 33% of participants were classified as having NAFLD. Intake of all carotenoids, with the exception of lycopene, was lower among those with NAFLD. This association was significant for the highest quartiles of intake of α-carotene, β-carotene, β-cryptoxanthin, and lutein/zeaxanthin. For serum measures, the highest level of all carotenoids was associated with significantly reduced odds of NAFLD. In conclusion, higher intake and serum levels of most carotenoids were associated with lower odds of having NAFLD. Identification of such modifiable lifestyle factors provide an opportunity to limit or prevent the disease and its progression.

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          Most cited references 18

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          The non-provitamin A carotenoid, lutein, inhibits NF-kappaB-dependent gene expression through redox-based regulation of the phosphatidylinositol 3-kinase/PTEN/Akt and NF-kappaB-inducing kinase pathways: role of H(2)O(2) in NF-kappaB activation.

          Reactive oxygen species (ROS) have been implicated in the regulation of NF-kappaB activation, which plays an important role in inflammation and cell survival. However, the molecular mechanisms of ROS in NF-kappaB activation remain poorly defined. We found that the non-provitamin A carotenoid, lutein, decreased intracellular H(2)O(2) accumulation by scavenging superoxide and H(2)O(2) and the NF-kappaB-regulated inflammatory genes, iNOS, TNF-alpha, IL-1beta, and cyclooxygenase-2, in lipopolysaccharide (LPS)-stimulated macrophages. Lutein inhibited LPS-induced NF-kappaB activation, which highly correlated with its inhibitory effect on LPS-induced IkappaB kinase (IKK) activation, IkappaB degradation, nuclear translocation of NF-kappaB, and binding of NF-kappaB to the kappaB motif of the iNOS promoter. This compound inhibited LPS- and H(2)O(2)-induced increases in phosphatidylinositol 3-kinase (PI3K) activity, PTEN inactivation, NF-kappaB-inducing kinase (NIK), and Akt phosphorylation, which are all upstream of IKK activation, but did not affect the interaction between Toll-like receptor 4 and MyD88 and the activation of mitogen-activated protein kinases. The NADPH oxidase inhibitor apocynin and gp91(phox) deletion reduced the LPS-induced NF-kappaB signaling pathway as lutein did. Moreover, lutein treatment and gp91(phox) deletion decreased the expressional levels of the inflammatory genes in vivo and protected mice from LPS-induced lethality. Our data suggest that H(2)O(2) modulates IKK-dependent NF-kappaB activation by promoting the redox-sensitive activation of the PI3K/PTEN/Akt and NIK/IKK pathways. These findings further provide new insights into the pathophysiological role of intracellular H(2)O(2) in the NF-kappaB signal pathway and inflammatory process.
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            Fatty liver indices in the multiethnic United States National Health and Nutrition Examination Survey.

             J Everhart,  C Rühl (2014)
            Validated non-invasive measures of fatty liver are needed that can be applied across populations and over time. A fatty liver index (FLI) including body mass index, waist circumference, triglycerides and gamma glutamyltransferase (GGT) activity was developed in an Italian municipality, but has not been validated widely or examined in a multiethnic population. We evaluated this FLI in the multiethnic U.S. National Health and Nutrition Examination Survey (NHANES) and also to explore whether an improved index for the U.S. population (US FLI) could be derived. The US FLI would then used to examine U.S. time trends in fatty liver prevalence. We studied 5869 fasted, viral hepatitis negative adult participants with abdominal ultrasound data on fatty liver in the 1988-1994 NHANES. Time trend analyses included 21 712 NHANES 1988-1994 and 1999-2012 participants. The prevalence of fatty liver was 20%. For the FLI, the area under the receiver operating characteristic curve [AUC; 95% confidence interval (CI)] was 0.78 (0.74-0.81). The US FLI included age, race-ethnicity, waist circumference, GGT activity, fasting insulin and fasting glucose and had an AUC (95% CI) of 0.80 (0.77-0.83). Defining fatty liver as a US FLI ≥ 30, the prevalence increased from 18% in 1988-1991 to 29% in 1999-2000 to 31% in 2011-2012. For predicting fatty liver, the US FLI was a modest improvement over the FLI in the multiethnic U.S. population. Using this measure, the fatty liver prevalence in the U.S. population increased substantially over two decades. © 2014 John Wiley & Sons Ltd.
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              Plasma levels of vitamin E and carotenoids are decreased in patients with nonalcoholic steatohepatitis (NASH)

              Objectives Oxidative stress is suggested to play an important role in the pathogenesis of nonalcoholic steatohepatitis (NASH). The present study was aimed to compare plasma levels of antioxidants in patients suffering from NASH and healthy controls. Methods Plasma levels of the antioxidants α-tocopherol, γ-tocopherol, lutein, zeaxanthin, β-cryptoxanthin, lycopene, α-carotene β-carotene were determined in 57 patients with biopsy-proven NASH and 40 healthy controls. Results Levels of α-tocopherol (22.4 vs. 26.8 nmol/ ml; p < 0.01), lutein (0.19 vs. 0.33 nmol/ml; p < 0.0001), zeaxanthin (0.04 vs. 0.08 nmol/ml; p < 0.0001), lycopene (0.15 vs. 0.42 nmol/ml; p < 0.0001), α-carotene (0.03 vs. 0.06 nmol/ml; p < 0.005) and β-carotene (0.25 vs. 0.39 nmol/ml; p < 0.01) were significantly decreased in NASH patients compared to controls. Age, aminotransferase status (ALT, AST) and BMI were not correlated with the levels of tocopherols or carotenoids. Conclusions Given the decreased levels supplementation of lipophilic antioxidants might be a rational treatment option for patients with NASH.
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                Author and article information

                Journal
                Nutrients
                Nutrients
                nutrients
                Nutrients
                MDPI
                2072-6643
                17 May 2019
                May 2019
                : 11
                : 5
                Affiliations
                [1 ]Department of Ophthalmology and Visual Sciences, University of Wisconsin, 610 N. Walnut Street, 1069 WARF Building, Madison, WI 53726, USA; jmarespe@ 123456wisc.edu
                [2 ]Department of Nutritional Sciences, University of Wisconsin, 1415 Linden Drive, Madison, WI 53706, USA; tlawler2@ 123456wisc.edu
                Author notes
                [* ]Correspondence: krista.christensen@ 123456wisc.edu ; Tel.: +1-60-8265-3192
                Article
                nutrients-11-01101
                10.3390/nu11051101
                6566688
                31108934
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

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