The Association Between the Dietary Inflammatory Index (DII) and Some Serum Oxidative Stress Markers in Non‑Alcoholic Fatty Liver Disease: Case‑ Control

Fateme Moradi, Zahra Heidari, Azam Teimori, Mohammadreza Ghazvini, Zahra Faghih Imani, Amirmansour Alavi Naeini

Abstract


Purpose: Non‑alcoholic fatty liver disease (NAFLD) is the most common liver disorder. The purpose of this study was to determine the relationship between the dietary inflammatory index (DII) and the serum oxidative stress markers in patients with NAFLD. Methods: In this case‑control study, 121 patients with NAFLD and 119 healthy subjects were frequency‑matched on gender. DII scores were calculated by using a 168‑item food frequency questionnaire (FFQ). Blood samples were collected to measure serum oxidative markers. Linear regression and odds ratio (OR) were also used in this study. Results: The mean ± standard deviation of age for case and control group was 38.04 ± 6.7 and 35.6 ± 10.2, respectively. The gender ratio (female to male) for the case and control group was 1:1.42 and 1:1.38, respectively. The mean of the DII in the patient group was significantly higher than the healthy group, (P‑values < 0.01). There was a significant negative relationship between TAC and DII (B = ‑2.63 (95%CI: ‑4.59, ‑0.68) and there was also a positive relationship between Malondialdehyde (MDA) and DII (B = 0.15 (95%CI: 0.02, 0.28) in the healthy group, but they were not significant in the case group. After multivariate adjustment, subjects in the most pro‑inflammatory DII group had 73 times higher odds of NAFLD compared to subjects in tertile 1 (OR = 72.9; 95%CI (14.3‑371.9)). Conclusions: Our findings suggest a direct association between the pro inflammatory properties of diet in patient and healthy group, but no relationship between TAC, MDA, and DII in the case group.

Keywords


Dietary inflammatory index malondialdehyde; non‑alcoholic fatty liver disease; total antioxidant capacity

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References


Angulo P. Nonalcoholic fatty liver disease. N Engl J Med

;346:1221‑31.

Ferramosca A, Di Giacomo M, Zara V. Antioxidant dietary

approach in treatment of fatty liver: New insights and updates.

World J Gastroenterol 2017;23:4146‑57.

Vernon G, Baranova A, Younossi Z. Systematic review: The

epidemiology and natural history of non-alcoholic fatty liver

disease and non-alcoholic steatohepatitis in adults. Aliment

Pharmacol Ther 2011;34:274‑85.

Lankarani KB, Ghaffarpasand F, Mahmoodi M, Lotfi M,

Zamiri N, Heydari ST, et al. Non alcoholic fatty liver disease

in Southern Iran: A population based study. Hepat Mon

;13:e9248.

Bellentani S, Scaglioni F, Marino M, Bedogni G. Epidemiology

of non‑alcoholic fatty liver disease. Dig Dis 2010;28:155‑61.

Rinella ME. Nonalcoholic fatty liver disease: A systematic

review. JAMA 2015;313:2263‑73.

Begriche K, Igoudjil A, Pessayre D, Fromenty B. Mitochondrial

dysfunction in NASH: Causes, consequences and possible means

to prevent it. Mitochondrion 2006;6:1‑28.

Bastard J‑P, Jardel C, Bruckert E, Blondy P, Capeau J, Laville M,

et al. Elevated levels of interleukin 6 are reduced in serum and

subcutaneous adipose tissue of obese women after weight loss.

J Clin Endocrinol Metab 2000;85:3338‑42.

Wannamethee SG, Lowe GD, Rumley A, Bruckdorfer KR,

Whincup PH. Associations of vitamin C status, fruit and

vegetable intakes, and markers of inflammation and hemostasis.

Am J Clin Nutr 2006;83:567‑74; quiz 726‑7.

Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L,

Hu FB, Willett WC. Dietary patterns and markers of systemic

inflammation among Iranian women. J Nutr 2007;137:992‑8.

Shivappa N, Steck SE, Hurley TG, Hussey JR,

Hébert JR. Designing and developing a literature‑derived,

population‑based dietary inflammatory index. Public Health

Nutr 2014;17:1689‑96.

Machin D, Campbell MJ, Tan SB, Tan SH. Sample sizes for clinical, laboratory and epidemiology studies.: Wiley Online

Library; 2018.

Oddy WH, Herbison CE, Jacoby P, Ambrosini GL, O’sullivan TA,

Ayonrinde OT, et al. The Western dietary pattern is prospectively

associated with nonalcoholic fatty liver disease in adolescence.

Am J Gastroenterol 2013;108:778‑85.

Kim HY, Lee J, Kim J. Association between dietary inflammatory

index and metabolic syndrome in the general Korean population.

Nutrients 2018;10:648.

Monteiro CA, Moura EC, Conde WL, Popkin BM.

Socioeconomic status and obesity in adult populations of

developing countries: A review. Bull World Health Organ

;82:940‑6.

Lean M, Han T, Morrison C. Waist circumference as a

measure for indicating need for weight management. BMJ

;311:158‑61.

Eshaghi SR, Farajzadegan Z, Babak A. Healty lifestyle

assessment questionnaire in elderly: Translation, reliability and

validity. Payesh (Health Monitor) 2010;9:91‑9.

Arvidsson D, Slinde F, Hulthen L. Physical activity questionnaire

for adolescents validated against doubly labelled water. Eur J

Clin Nutr 2005;59:376‑83.

Mirmiran P, Esfahani FH, Mehrabi Y, Hedayati M, Azizi F.

Reliability and relative validity of an FFQ for nutrients

in the Tehran lipid and glucose study. Public Health Nutr

;13:654‑62.

Wirth M, Burch J, Shivappa N, Violanti JM, Burchfiel CM,

Fekedulegn D, et al. Association of a dietary inflammatory index

with inflammatory indices and the metabolic syndrome among

police officers. J Occup Environ Med 2014;56:986‑9.

Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in

animal tissues by thiobarbituric acid reaction. Anal Biochem

;95:351‑8.

Benzie IF, Strain JJ. The ferric reducing ability of plasma (FRAP)

as a measure of “antioxidant power”: The FRAP assay. Anal

Biochem 1996;239:70‑6.

Lidén M, Kristjánsson G, Valtysdottir S, Venge P, Hällgren R.

Self‑reported food intolerance and mucosal reactivity after rectal

food protein challenge in patients with rheumatoid arthritis.

Scand J Rheumatol 2010;39:292‑8.

Luukkonen PK, Zhou Y, Sädevirta S, Leivonen M, Arola J,

Orešič M, et al. Hepatic ceramides dissociate steatosis and

insulin resistance in patients with non‑alcoholic fatty liver

disease. J Hepatol 2016;64:1167‑75.

Malin SK, Rynders CA, Weltman JY, Barrett EJ, Weltman A.

Exercise intensity modulates glucose‑stimulated insulin secretion

when adjusted for adipose, liver and skeletal muscle insulin

resistance. PloS One 2016;11:e0154063.

Vahid F, Shivappa N, Karamati M, Naeini AJ, Hebert JR,

Davoodi SH. Association between Dietary inflammatory

index (DII) and risk of prediabetes: A case‑control study. Appl

Physiol Nutr Metab 2017;42:399‑404.

Dandona P, Ghanim H, Chaudhuri A, Dhindsa S, Kim SS.

Macronutrient intake induces oxidative and inflammatory stress:

Potential relevance to atherosclerosis and insulin resistance. Exp

Mol Med 2010;42:245‑53.

Hermsdorff HHM, Puchau B, Volp ACP, Barbosa KB, Bressan J,

Zulet MÁ, et al. Dietary total antioxidant capacity is inversely

related to central adiposity as well as to metabolic and oxidative

stress markers in healthy young adults. Nutr Metab (Lond)

;8:59.

Varkaneh K, Varkaneh HK, Rahmani J, Tajik S, Zarezadeh M,

Nazari A, et al. Association between dietary inflammatory index

with obesity in women who referred to health centers affiliated

to Tehran University of medical sciences. Razi J Med Sci

;24:21‑30.

Wirth MD, Hébert JR, Shivappa N, Hand GA, Hurley TG,

Drenowatz C, et al. Anti‑inflammatory dietary inflammatory

index scores are associated with healthier scores on other dietary

indices. Nutr Res 2016;36:214‑9.

Shivappa N, Hébert JR, Rietzschel ER, De Buyzere ML,

Langlois M, Debruyne E, et al. Associations between dietary

inflammatory index and inflammatory markers in the Asklepios

Study. Br J Nutr 2015;113:665‑71.

Paeschke A, Erben U, Kredel LI, Kühl AA, Siegmund B. Role

of visceral fat in colonic inflammation: From Crohn’s disease to

diverticulitis. Curr Opin Gastroenterol 2017;33:53‑8.

Cantero I, Abete I, Babio N, Arós F, Corella D, Estruch R, et al.

Dietary inflammatory index and liver status in subjects with

different adiposity levels within the PREDIMED trial. Clin Nutr

;37:1736‑43.

Bedogni G, Miglioli L, Masutti F, Castiglione A, Croce LS,

Tiribelli C, et al. Incidence and natural course of fatty liver

in the general population: The Dionysos study. Hepatology

;46:1387‑91.

Lee DS, Evans JC, Robins SJ, Wilson PW, Albano I, Fox CS,

et al. Gamma glutamyl transferase and metabolic syndrome,

cardiovascular disease, and mortality risk: The Framingham

heart study. Arterioscler Thromb Vasc Biol 2007;27:127‑33.

Armstrong MJ, Adams LA, Canbay A, Syn WK. Extrahepatic

complications of nonalcoholic fatty liver disease. Hepatology

;59:1174‑97.

Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM,

Cusi K, et al. The diagnosis and management of non-alcoholic

fatty liver disease: Practice guideline by the American

association for the study of liver diseases, American college

of gastroenterology, and the American gastroenterological

association. Hepatology 2012;55:2005‑23.

Mazidi M, Shivappa N, Wirth MD, Hebert JR, Kengne AP. Diet

with greater inflammatory potential is associated with higher

prevalence of fatty liver among US adults. Eur J Clin Nutr

;73:1653‑6.

Ruiz‑Canela M, Bes‑Rastrollo M, Martínez‑González MA.

The role of dietary inflammatory index in cardiovascular

disease, metabolic syndrome and mortality. Int J Mol Sci

;17:1265.

Namazi N, Larijani B, Azadbakht L. Dietary inflammatory index

and its association with the risk of cardiovascular diseases,

metabolic syndrome, and mortality: A systematic review and

meta‑analysis. Horm Metab Res 2018;50:345‑58.

Akhlaghi M. Non-alcoholic fatty liver disease: Beneficial effects

of flavonoids. Phytother Res 2016;30:1559‑71.

Xu H, Sjögren P, Ärnlöv J, Banerjee T, Cederholm T,

Risérus U, et al. A proinflammatory diet is associated with

systemic inflammation and reduced kidney function in elderly

adults. J Nutr 2015;145:729‑35.

Arya A, Azarmehr N, Mansourian M, Doustimotlagh AH.

Inactivation of the superoxide dismutase by malondialdehyde

in the nonalcoholic fatty liver disease: A combined molecular

docking approach to clinical studies. Arch Physiol Biochem

;1‑8. doi: 10.1080/13813455.2019.1659827. Online ahead of

print.

Rodrigo CP, Aranceta J, Salvador G, Varela‑Moreiras G. Food

frequency questionnaires. Nutr Hosp 2015;31:49‑56.