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Chronic consumption of fructose in combination with trans fatty acids but not with saturated fatty acids induces nonalcoholic steatohepatitis with fibrosis in rats

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Abstract

Purpose

Consumption of Western diet high in fat and fructose has been attributed to the recent epidemic of nonalcoholic fatty liver disease (NAFLD). However, the impact of specific fatty acids on the progression of NAFLD to nonalcoholic steatohepatitis (NASH) is poorly understood. In the present study, we investigated the chronic effects of consumption of fructose in combination with saturated fatty acids (SFA) or trans fatty acids (TFA) on the development of NAFLD.

Methods

Male Sprague–Dawley rats were randomly assigned to six isocaloric starch/high fructose (44% of calories), high fat (39% calories) diet containing either starch–peanut oil, fructose–peanut oil, fructose–palmolein, fructose–clarified butter, fructose–coconut oil or fructose–partially hydrogenated vegetable oil and fed for 24 weeks. Palmolein, clarified butter and coconut oil were used as the source of SFA whereas partially hydrogenated vegetable oil was used as the source of TFA. Peanut oil was used as the reference oil.

Results

Long-term feeding of fructose in combination with SFA or TFA induced hepatic steatosis of similar extent associated with upregulation of stearoyl CoA desaturase-1. In contrast, fructose in combination with TFA induced NASH with fibrosis as evidenced by upregulation of hepatic proinflammatory cytokine and fibrogenic gene expression, increased hepatic oxidative stress and adipocytokine imbalance. Histopathological analysis revealed the presence of NASH with fibrosis. Further, peanut oil prevented the development of NAFLD in fructose-fed rats.

Conclusion

Fructose in combination with TFA caused NASH with fibrosis by inducing oxidative stress and inflammation, whereas, fructose in combination with SFA caused simple steatosis, suggesting that the type of fatty acid is more important for the progression of NAFLD.

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Abbreviations

ACC α:

Acetyl CoA carboxylase alpha

ALT:

Alanine aminotransferases

AST:

Aspartate aminotransferases

AUC:

Area under the curve

CB:

Clarified butter

ChREBP:

Carbohydrate responsive element binding protein

CO:

Coconut oil

CPT 1:

Carnitine palmotyl tranferase 1

ELISA:

Enzyme linked immunosorbent assay

FAME:

Fatty acid methyl ester

FAS:

Fatty acid synthase

FR-PNO:

Fructose–peanut oil

FR-PO:

Fructose–palmolein

FR-CB:

Fructose–clarified butter

FR-CO:

Fructose–coconut oil

FR-PHVO:

Fructose–partially hydrogenated vegetable oil

GPx:

Glutathione peroxidase

GSH:

Reduced glutathione

H&E:

Hematoxylin and eosin

HDL:

High-density lipoprotein

HOMA-IR:

Homeostasis model assessment-insulin resistance

HSC:

Hepatic stellate cells

IL-1β:

Interleukin-1 beta

IL-6:

Interleukin-6

IPGTT:

Intraperitoneal glucose tolerance test

NAFLD:

Nonalcoholic fatty liver disease

NAS:

NAFLD Activity score

NASH:

Nonalcoholic steatohepatitis

PAI-1:

Plasminogen activator inhibitor-1

PCR:

Polymerase chain reaction

PHVO:

Partially hydrogenated vegetable oil

PNO:

Peanut oil

PO:

Palmolein

PPAR α:

Peroxisome proliferator-activated receptor alpha

PPAR γ:

Peroxisome proliferator-activated receptor gamma

SCD-1:

Stearoyl CoA desaturase-1

SFA:

Saturated fatty acid

SOD:

Superoxide dismutase

SREBP 1c:

Sterol regulatory element binding protein 1c

TBARS:

Thiobarbituric acid reactive substances

TFA:

Trans fatty acid

TNF α:

Tumor necrosis factor alpha

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Acknowledgements

This study was funded by Grants in aid (5/4/3-7/TF/2011/NCD-II) from Indian Council of Medical Research, Government of India to AI. JS was supported by a fellowship from Indian Council of Medical Research, Government of India.

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Authors and Affiliations

  1. Department of Lipid Chemistry, National Institute of Nutrition, Hyderabad, India

    Sugeedha Jeyapal, Anil Sakamuri, Suryam Reddy Kona, Sai Santosh Vadakattu, Chandana Madakasira & Ahamed Ibrahim

  2. Department of Pathology, National Institute of Nutrition, Hyderabad, India

    Uday Kumar Putcha & Venkata Surekha Mullapudi

  3. Department of Molecular Biology, National Institute of Nutrition, Hyderabad, India

    Sudip Ghosh

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  1. Sugeedha Jeyapal
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  2. Uday Kumar Putcha
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Contributions

AI and JS designed the study, analyzed the data and wrote the manuscript. JS, AS, KSR and VSS conducted the animal experiment and prepared the experimental diets. PUK and MVS carried out histopathological analysis of liver and NAS scoring. SG and JS involved in mRNA expression studies by RT-qPCR. JS, KSR and CM carried out biochemical estimations. All the authors read and approved the manuscript.

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Correspondence to Ahamed Ibrahim.

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Jeyapal, S., Putcha, U.K., Mullapudi, V.S. et al. Chronic consumption of fructose in combination with trans fatty acids but not with saturated fatty acids induces nonalcoholic steatohepatitis with fibrosis in rats. Eur J Nutr 57, 2171–2187 (2018). https://doi.org/10.1007/s00394-017-1492-1

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