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Preventive effects of caffeine on nicotine plus high-fat diet-induced hepatic steatosis and gain weight: a possible explanation for why obese smokers with high coffee consumption tend to be leaner

Published online by Cambridge University Press:  27 December 2023

Naiyan Lu
Affiliation:
School of Food Science and Technology, Jiangnan University, Wuxi, People’s Republic of China
Xue Mei
Affiliation:
School of Food Science and Technology, Jiangnan University, Wuxi, People’s Republic of China
Xu Li
Affiliation:
School of Food Science and Technology, Jiangnan University, Wuxi, People’s Republic of China
Xue Tang
Affiliation:
School of Food Science and Technology, Jiangnan University, Wuxi, People’s Republic of China
Guofeng Yang
Affiliation:
School of Food Science and Technology, Jiangnan University, Wuxi, People’s Republic of China
Wen Xiang*
Affiliation:
School of Food Science and Technology, Jiangnan University, Wuxi, People’s Republic of China School of Medicine, Nankai University, Tianjin, People’s Republic of China
*
*Corresponding author: Wen Xiang, email 1120200668@mail.nankai.edu.cn

Abstract

Non-alcoholic fatty liver disease (NAFLD) is a prevalent liver disorder, affecting approximately 25 % of the population. Coffee-drinking obese smokers exhibit lower body weights and decreased NAFLD rates, but the reasons behind this remain unclear. Additionally, the effect of nicotine, the main component of tobacco, on the development of NAFLD is still controversial. Our study aimed to explore the possible reasons that drinking coffee could alleviate NAFLD and gain weight and identify the real role of nicotine in NAFLD of obese smokers. A NAFLD model in mice was induced by administering nicotine and a high-fat diet (HFD). We recorded changes in body weight and daily food intake, measured the weights of the liver and visceral fat, and observed liver and adipose tissue histopathology. Lipid levels, liver function, liver malondialdehyde (MDA), superoxide dismutase (SOD), serum inflammatory cytokine levels and the expression of hepatic genes involved in lipid metabolism were determined. Our results demonstrated that nicotine exacerbated the development of NAFLD and caffeine had a hepatoprotective effect on NAFLD. The administration of caffeine could ameliorate nicotine-plus-HFD-induced NAFLD by reducing lipid accumulation, regulating hepatic lipid metabolism, alleviating oxidative stress, attenuating inflammatory response and restoring hepatic functions. These results might explain why obese smokers with high coffee consumption exhibit the lower incidence rate of NAFLD and tend to be leaner. It is essential to emphasise that the detrimental impact of smoking on health is multifaceted. Smoking cessation remains the sole practical and effective strategy for averting the tobacco-related complications and reducing the risk of mortality.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press on behalf of The Nutrition Society

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References

Rojano, A, Sena, E, Manzano-Nunez, R, et al. (2023) NAFLD as the metabolic hallmark of obesity. Intern Emerg Med 18, 3141.CrossRefGoogle ScholarPubMed
Huang, DQ, El-Serag, HB & Loomba, R (2021) Global epidemiology of NAFLD-related HCC: trends, predictions, risk factors and prevention. Nat Rev Gastroenterol Hepatol 18, 223238.CrossRefGoogle ScholarPubMed
Ioannou, GN (2021) Epidemiology and risk-stratification of NAFLD-associated HCC. J Hepatol 75, 14761484.CrossRefGoogle ScholarPubMed
Machado, MV & Cortez-Pinto, H (2023) NAFLD, MAFLD and obesity: brothers in arms? Nat Rev Gastroenterol Hepatol 20, 6768.CrossRefGoogle Scholar
Li, Y, Chen, Y, Tian, X, Zhang, S, et al. (2021) Comparison of clinical characteristics between obese and non-obese patients with Nonalcoholic Fatty Liver Disease (NAFLD). Diabetes Metab Syndr Obes 14, 20292039.CrossRefGoogle Scholar
Jang, YS, Joo, HJ, Park, YS, et al. (2023) Association between smoking cessation and non-alcoholic fatty liver disease using NAFLD liver fat score. Front Public Health 11, 1015919.CrossRefGoogle ScholarPubMed
Carreras-Torres, R, Johansson, M, Haycock, PC, et al. (2018) Role of obesity in smoking behaviour: Mendelian randomisation study in UK Biobank. BMJ 361, k1767.CrossRefGoogle Scholar
Park, S, Kim, SG, Lee, S, et al. (2023) Causal effects from tobacco smoking initiation on obesity-related traits: a Mendelian randomization study. Int J Obes 47, 12321238.CrossRefGoogle Scholar
Azzalini, L, Ferrer, E, Ramalho, LN, et al. (2010) Cigarette smoking exacerbates nonalcoholic fatty liver disease in obese rats. Hepatology 51, 15671576.CrossRefGoogle ScholarPubMed
Sinha-Hikim, AP, Sinha-Hikim, I & Friedman, TC (2017) Connection of nicotine to diet-induced obesity and non-alcoholic fatty liver disease: cellular and mechanistic insights. Front Endocrinol (Lausanne) 8, 23.CrossRefGoogle ScholarPubMed
Li, DJ, Liu, J, Hua, X, et al. (2018) Nicotinic acetylcholine receptor alpha7 subunit improves energy homeostasis and inhibits inflammation in nonalcoholic fatty liver disease. Metabolism 79, 5263.CrossRefGoogle ScholarPubMed
Seoane-Collazo, P, Martinez de Morentin, PB, Ferno, J, et al. (2014) Nicotine improves obesity and hepatic steatosis and ER stress in diet-induced obese male rats. Endocrinology 155, 16791689.CrossRefGoogle ScholarPubMed
Kanamori, H, Nakade, Y, Yamauchi, T, et al. (2017) Influence of nicotine on choline-deficient, L-amino acid-defined diet-induced non-alcoholic steatohepatitis in rats. PLoS One 12, e0180475.CrossRefGoogle ScholarPubMed
Saimaiti, A, Zhou, D-D, Li, J, et al. (2023) Dietary sources, health benefits, risks of caffeine. Crit Rev Food Sci Nutr 63(29), 9648–9666.CrossRefGoogle ScholarPubMed
Wijarnpreecha, K, Thongprayoon, C & Ungprasert, P (2017) Coffee consumption and risk of nonalcoholic fatty liver disease: a systematic review and meta-analysis. Eur J Gastroenterol Hepatol 29, e8e12.CrossRefGoogle ScholarPubMed
Sewter, R, Heaney, S & Patterson, A (2021) Coffee consumption and the progression of NAFLD: a systematic review. Nutrients 13, 2381.CrossRefGoogle ScholarPubMed
Kositamongkol, C, Kanchanasurakit, S, Auttamalang, C, et al. (2021) Coffee consumption and non-alcoholic fatty liver disease: an umbrella review and a systematic review and meta-analysis. Front Pharmacol 12, 786596.CrossRefGoogle Scholar
Hayat, U, Siddiqui, AA, Okut, H, et al. (2021) The effect of coffee consumption on the non-alcoholic fatty liver disease and liver fibrosis: a meta-analysis of 11 epidemiological studies. Ann Hepatol 20, 100254.CrossRefGoogle ScholarPubMed
Shan, L, Wang, F, Zhai, D, et al. (2022) Caffeine in liver diseases: pharmacology and toxicology. Front Pharmacol 13, 1030173.CrossRefGoogle ScholarPubMed
Helal, MG, Ayoub, SE, Elkashefand, WF, et al. (2018) Caffeine affects HFD-induced hepatic steatosis by multifactorial intervention. Hum Exp Toxicol 37, 983990.CrossRefGoogle ScholarPubMed
Sinha, RA, Farah, BL, Singh, BK, et al. (2014) Caffeine stimulates hepatic lipid metabolism by the autophagy-lysosomal pathway in mice. Hepatology 59, 13661380.CrossRefGoogle ScholarPubMed
Martins, BC, Soares, AC, Martins, FF, et al. (2023) Coffee consumption prevents obesity-related comorbidities and attenuates brown adipose tissue whitening in high-fat diet-fed mice. J Nutr Biochem 117, 109336.CrossRefGoogle Scholar
Lee, A, Lim, W, Kim, S, et al. (2019) Coffee intake and obesity: a meta-analysis. Nutrients 11, 1274.CrossRefGoogle ScholarPubMed
Duan, Y, Zeng, L, Zheng, C, et al. (2018) Inflammatory links between high fat diets and diseases. Front Immunol 9, 2649.CrossRefGoogle ScholarPubMed
Ohashi, T, Nakade, Y, Ibusuki, M, et al. (2019) Conophylline inhibits high fat diet-induced non-alcoholic fatty liver disease in mice. PLoS One 14, e0210068.CrossRefGoogle ScholarPubMed
Fu, Y, Zhou, Y, Shen, L, et al. (2022) Diagnostic and therapeutic strategies for non-alcoholic fatty liver disease. Front Pharmacol 13, 973366.CrossRefGoogle ScholarPubMed
Wijarnpreecha, K, Scribani, M, Kim, D, et al. (2019) The interaction of nonalcoholic fatty liver disease and smoking on mortality among adults in the United States. Liver Int 39, 12021206.CrossRefGoogle ScholarPubMed
Ivey, R, Desai, M, Green, K, et al. (2014) Additive effects of nicotine and high-fat diet on hepatocellular apoptosis in mice: involvement of caspase 2 and inducible nitric oxide synthase-mediated intrinsic pathway signaling. Horm Metab Res 46, 568573.Google ScholarPubMed
Coelho, M, Patarrão, RS, Sousa-Lima, I, et al. (2022) Increased intake of both caffeine and non-caffeine coffee components is associated with reduced NAFLD severity in subjects with type 2. Diabetes 15, 4.Google ScholarPubMed
Shen, H, Rodriguez, AC, Shiani, A, et al. (2016) Association between caffeine consumption and nonalcoholic fatty liver disease: a systemic review and meta-analysis. Therap Adv Gastroenterol 9, 113120.CrossRefGoogle ScholarPubMed
Seoane-Collazo, P, Dieguez, C, Nogueiras, R, et al. (2021) Nicotine' actions on energy balance: friend or foe? Pharmacol Ther 219, 107693.CrossRefGoogle ScholarPubMed
Liu, CW, Tsai, HC, Huang, CC, et al. (2018) Effects and mechanisms of caffeine to improve immunological and metabolic abnormalities in diet-induced obese rats. Am J Physiol Endocrinol Metab 314, E433E47.CrossRefGoogle ScholarPubMed
Wu, L, Meng, J, Shen, Q, et al. (2017) Caffeine inhibits hypothalamic A(1)R to excite oxytocin neuron and ameliorate dietary obesity in mice. Nat Commun 8, 15904.CrossRefGoogle ScholarPubMed
Driva, S, Korkontzelou, A, Tonstad, S, et al. (2022) The effect of smoking cessation on body weight and other metabolic parameters with focus on people with type 2 diabetes mellitus. Int J Environ Res Public Health 19, 13222.CrossRefGoogle ScholarPubMed
Ostlund, C, Hernandez-Ono, A & Shin, JY (2020) The nuclear envelope in lipid metabolism and pathogenesis of NAFLD. Biology (Basel) 9, 338.CrossRefGoogle Scholar
Deprince, A, Haas, JT & Staels, B (2020) Dysregulated lipid metabolism links NAFLD to cardiovascular disease. Mol Metab 42, 101092.CrossRefGoogle ScholarPubMed
Li, H, Yu, XH, Ou, X, et al. (2021) Hepatic cholesterol transport and its role in non-alcoholic fatty liver disease and atherosclerosis. Prog Lipid Res 83, 101109.CrossRefGoogle ScholarPubMed
Ahn, N & Kim, K (2016) High-density lipoprotein cholesterol (HDL-C) in cardiovascular disease: effect of exercise training. Integr Med Res 5, 212215.CrossRefGoogle ScholarPubMed
Vidal-Quintanar, RL, Mendívil, RL, Peña, M, et al. (2007) Lime-treated maize husks lower plasma LDL-cholesterol levels in normal and hypercholesterolaemic adult men from northern Mexico. Br J Nutr 81, 281288.CrossRefGoogle Scholar
Zhao, Y, Yang, L, Huang, Z, et al. (2017) Synergistic effects of caffeine and catechins on lipid metabolism in chronically fed mice via the AMP-activated protein kinase signaling pathway. Eur J Nutr 56, 23092318.CrossRefGoogle ScholarPubMed
Xu, M, Yang, L, Zhu, Y, et al. (2019) Collaborative effects of chlorogenic acid and caffeine on lipid metabolism via the AMPKα-LXRα/SREBP-1c pathway in high-fat diet-induced obese mice. Food Funct 10, 74897497.CrossRefGoogle ScholarPubMed
Huang, Y-W, Wang, L-T, Zhang, M, et al. (2023) Caffeine can alleviate non-alcoholic fatty liver disease by augmenting LDLR expression via targeting EGFR. Food Funct 14, 32693278.CrossRefGoogle ScholarPubMed
Alisi, A, Carpino, G, Oliveira, FL, et al. (2017) The role of tissue macrophage-mediated inflammation on NAFLD pathogenesis and its clinical implications. Mediators Inflamm 2017, 8162421.CrossRefGoogle ScholarPubMed
Wang, M, Li, L, Xu, Y, et al. (2022) Roles of hepatic stellate cells in NAFLD: from the perspective of inflammation and fibrosis. Front Pharmacol 13, 958428.CrossRefGoogle ScholarPubMed
Gupta, G, Khadem, F & Uzonna, JE (2019) Role of hepatic stellate cell (HSC)-derived cytokines in hepatic inflammation and immunity. Cytokine 124, 154542.CrossRefGoogle ScholarPubMed
Rives, C, Fougerat, A, Ellero-Simatos, S, et al. (2020) Oxidative stress in NAFLD: role of nutrients and food contaminants. Biomolecules 10, 1702.CrossRefGoogle ScholarPubMed
Shoukry Heba, S, Taher Maha, M, Enany, A, et al. (2019) Combination of caffeine and liver albumin plus protects against smoking-induced liver injury in rats. Dubai Med J 2, 2330.CrossRefGoogle Scholar