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      Spices in a High-Saturated-Fat, High-Carbohydrate Meal Reduce Postprandial Proinflammatory Cytokine Secretion in Men with Overweight or Obesity: A 3-Period, Crossover, Randomized Controlled Trial

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          ABSTRACT

          Background

          Postprandial inflammation that occurs concurrently with hyperglycemia and hyperlipidemia after ingestion of a high-saturated-fat, high-carbohydrate meal (HFCM) is a risk factor for cardiovascular disease (CVD). Numerous preclinical and clinical studies demonstrate anti-inflammatory effects of individual spices. However, the effect of consumption of a spice blend on inflammatory mediators has not been examined in a randomized controlled trial.

          Objectives

          The objective of this study was to investigate the postprandial effect of a blend of spices in a HFCM on inflammatory cytokine responses.

          Methods

          Nonsmoking men (40–65 y old) with overweight/obesity (25 ≤ BMI ≤ 35 kg/m 2), elevated waist circumference (≥ 94 cm), and ≥ 1 CVD risk factor were recruited for a 3-period crossover study ( n = 12). In random order, participants consumed the following: a HFCM (∼1000 kcal, 33% kcal from saturated fat and 36% kcal from carbohydrate), a HFCM containing 2 g spice blend, or an HFCM containing 6 g spice blend. The spice blend consisted of basil, bay leaf, black pepper, cinnamon, coriander, cumin, ginger, oregano, parsley, red pepper, rosemary, thyme, and turmeric. Blood was collected before, and hourly for 4 h after the HFCM. Peripheral blood mononuclear cells (PBMCs) were isolated, and the percentage of CD14 +/Human Leukocyte Antigen-DR isotype + (HLA-DR +) monocytes and proinflammatory cytokine concentrations in plasma and LPS-stimulated PBMCs were quantified as secondary outcomes.

          Results

          There was a significant spice-by-time interaction on IL-1β ( P < 0.001), IL-8 ( P = 0.020), and TNF-α ( P = 0.009) secretion from LPS-stimulated PBMCs. IL-1β secretion from LPS-stimulated PBMCs was significantly reduced (1314%) at 240 min after HFCM consumption containing 6 g, but not 2 g, of spice blend compared with 0 g spice blend.

          Conclusions

          A HFCM containing 6 g spice blend attenuated HFCM-induced postprandial IL-1β secretion in men with overweight/obesity.

          This trial was registered at clinicaltrials.gov as NCT03064958.

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          Most cited references62

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          Postprandial hyperglycemia/hyperlipidemia (postprandial dysmetabolism) is a cardiovascular risk factor.

          Epidemiologic data indicate that a postprandial state characterized by abnormally increased levels of glucose and lipids (also referred to as postprandial dysmetabolism) is an independent predictor of future cardiovascular events, even in nondiabetic subjects. The cardiovascular toxicity of postprandial dysmetabolism is mediated by oxidant stress, which is directly proportional to the increase in glucose after a meal. This transient increase in free radicals acutely triggers inflammation, endothelial dysfunction, hypercoagulability, sympathetic hyperactivity, and a cascade of other atherogenic changes. The postprandial dysmetabolism hypothesis has been bolstered by interventional studies that have demonstrated that blunting the postprandial spikes in glucose and lipids improves inflammation and endothelial function immediately. Early randomized controlled trials indicate that reducing postprandial dysmetabolism appears to significantly slow atherosclerotic progression and may improve cardiovascular prognosis. In conclusion, postprandial dysmetabolism appears to be an important proximate cause of adverse cardiovascular events. Addressing this fundamental and largely unrecognized condition will require specific screening and treatment strategies. Diet, exercise, and various pharmacologic agents can improve postprandial dysmetabolism. Using these strategies may help improve the prognosis for patients with diabetes mellitus and/or coronary heart disease.
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            Nutrients and phytochemicals: from bioavailability to bioefficacy beyond antioxidants.

            The effect of any dietary compound is influenced by the active bioavailable dose rather than the dose ingested. Depending on the individual predisposition, including genetics and medication, a bioavailable dose may cause different magnitudes of effects in different people. Age might affect the predisposition and thus the requirements for nutrients including phytonutrients (e.g. phytochemicals such as flavonoids, phenolic acids and glucosinolates). These are not essential for growth and development but to maintain body functions and health throughout the adult and later phases of life; they are 'lifespan essentials'. Major mechanisms involved in chronic, age-related diseases include the oxidant/antioxidant balance, but the latest research indicates indirect effects of dietary bioactives in vivo and adaptive responses in addition to direct radical scavenging.
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              The varying faces of IL-6: From cardiac protection to cardiac failure.

              IL6 is a pleiotropic cytokine that is made in response to perturbations in homeostasis. IL6 becomes elevated in the acute response to host injury and can activate immune cells, direct immune cell trafficking, signal protective responses in local tissue, initial the acute phase response or initiate wound healing. In the short term this proinflammatory response is protective and limits host damage. It is when this acute response remains chronically activated that IL6 becomes pathogenic to the host. Chronically elevated IL6 levels lead to chronic inflammation and fibrotic disorders. The heart is a tissue where this temporal regulation of IL6 is very apparent. Studies from myocardial infarction show how short-term IL6 signaling can protect and preserve the heart tissue in response to acute damage, where long term IL6 signaling or an over-production of IL6R protein plays a causal role in cardiovascular disease. Thus, IL6 can be both protective and pathogenic, depending on the kinetics of the host response.
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                Author and article information

                Journal
                J Nutr
                J. Nutr
                jn
                The Journal of Nutrition
                Oxford University Press
                0022-3166
                1541-6100
                June 2020
                25 March 2020
                25 March 2020
                : 150
                : 6
                : 1600-1609
                Affiliations
                [1 ] Department of Nutritional Sciences, The Pennsylvania State University, University Park , PA, USA
                [2 ] Center for Molecular Immunology and Infectious Disease, The Pennsylvania State University , University Park, PA, USA
                Author notes
                Address correspondence to CJR (e-mail: cjr102@ 123456psu.edu ).
                Author information
                http://orcid.org/0000-0001-6012-4900
                http://orcid.org/0000-0003-4072-2721
                Article
                nxaa063
                10.1093/jn/nxaa063
                7269750
                32211803
                c53c4962-28ad-4a6b-bd8f-18537eff6ad0
                Copyright © The Author(s) on behalf of the American Society for Nutrition 2020.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 25 July 2019
                : 25 September 2019
                : 24 February 2020
                Page count
                Pages: 10
                Funding
                Funded by: McCormick Science Institute;
                Award ID: MSI-10001
                Funded by: National Institutes of Health, DOI 10.13039/100000002;
                Award ID: TL1TR002016
                Award ID: 1UL1TR002014-01
                Funded by: National Center for Advancing Translational Sciences, DOI 10.13039/100006108;
                Categories
                Nutritional Immunology
                AcademicSubjects/MED00060
                AcademicSubjects/SCI00960

                Nutrition & Dietetics
                monocytes,inflammatory cytokines,obesity,nutritional intervention,randomized controlled trial

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