Skip to main content
SpringerLink
Log in

Low Docosahexaenoic Acid Content in Plasma Phospholipids is Associated with Increased Non-alcoholic Fatty Liver Disease in China

  • Original Article
  • Published:
Lipids

Abstract

A large proportion of the Chinese population is now at risk of non-alcoholic fatty liver disease (NAFLD). We aimed to investigate the relationship between plasma phospholipids (PL) fatty acids and the risk of NAFLD. One hundred NAFLD patients and 100 healthy subjects were recruited in Hangzhou, China. Plasma PL and selected biochemical and hematological parameters were analyzed by using standard methods. Stepwise logistic regression was used to identify independent risk factors of NAFLD. Plasma PL total saturated fatty acid (SFA), C20:3n-6, serum alanine aminotransferase, high-density lipoprotein cholesterol, and body mass index were independent risk factors of NAFLD. The risk of NAFLD was significantly increased with higher quartiles of plasma PL total SFA (P for trend = 0.028) and C20:3n-6 (P for trend <0.001); plasma PL docosahexaenoic acid (C22:6n-3) was significantly lower in NAFLD patients than in controls (P = 0.032) and the OR of NAFLD in the highest quartile of C22:6n-3 was 0.41 (95 % CI = 0.17–0.97) compared with the lowest quartile. In conclusion, plasma PL total SFA and C20:3n-6 are positively correlated with the risk of NAFLD, while C22:6n-3 is negatively correlated with the risk of NAFLD.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

ALP:

Alkaline phosphatase

ALT:

Alanine aminotransferase

BMI:

Body mass index

BUN:

Blood urea nitrogen

DBP:

Diastolic blood pressure

DBil:

Direct bilirubin

GGT:

Gamma-glutamyl transferase

HDL-C:

High-density lipoprotein cholesterol

IBil:

Indirect bilirubin

LDL-C:

Low-density lipoprotein cholesterol

MS:

Metabolic syndrome

NAFLD:

Non-alcoholic fatty liver disease

OR:

Odds ratio

PL:

Phospholipids

PUFA:

Polyunsaturated fatty acid(s)

SBP:

Systolic blood pressure

SFA:

Saturated fatty acid(s)

TBil:

Total bilirubin

TC:

Total cholesterol

TG:

Triacylglycerol(s)

References

  1. Angulo P (2007) GI epidemiology: nonalcoholic fatty liver disease. Aliment Pharmacol Ther 25:883–889

    Article  PubMed  CAS  Google Scholar 

  2. Fan JG, Farrell GC (2009) Epidemiology of non-alcoholic fatty liver disease in China. J Hepatol 50:204–210

    Article  PubMed  Google Scholar 

  3. Farrell GC, Chitturi S, Lau GK, Sollano JD (2007) Guidelines for the assessment and management of non-alcoholic fatty liver disease in the Asia-Pacific region: executive summary. J Gastroenterol Hepatol 22:775–777

    Article  PubMed  Google Scholar 

  4. Riquelme A, Arrese M, Soza A, Morales A, Baudrand R, Perez-Ayuso RM, Gonzalez R, Alvarez M, Hernandez V, Garcia-Zattera MJ, Otarola F, Medina B, Rigotti A, Miquel JF, Marshall G, Nervi F (2009) Non-alcoholic fatty liver disease and its association with obesity, insulin resistance and increased serum levels of C-reactive protein in Hispanics. Liver Int 29:82–88

    Article  PubMed  CAS  Google Scholar 

  5. Goessling W, Massaro JM, Vasan RS, D’Agostino RB Sr, Ellison RC, Fox CS (2008) Aminotransferase levels and 20-year risk of metabolic syndrome, diabetes, and cardiovascular disease. Gastroenterology 135:1935–1944

  6. Targher G (2007) Non-alcoholic fatty liver disease, the metabolic syndrome and the risk of cardiovascular disease: the plot thickens. Diabet Med 24:1–6

    Article  PubMed  CAS  Google Scholar 

  7. Fan JG, Zhu JN, Li XJ, Chen L, Lu YS, Li L, Dai F, Li F, Chen SY (2005) Fatty liver and the metabolic syndrome among Shanghai adults. J Gastroenterol Hepatol 20:1825–1832

    Article  PubMed  Google Scholar 

  8. Sathiaraj E, Chutke M, Reddy MY, Pratap N, Rao PN, Reddy DN, Raghunath M (2011) A case-control study on nutritional risk factors in non-alcoholic fatty liver disease in Indian population. Eur J Clin Nutr 65:533–537

    Article  PubMed  CAS  Google Scholar 

  9. Fan JG, Saibara T, Chitturi S, Kim BI, Sung JJ, Chutaputti A (2007) What are the risk factors and settings for non-alcoholic fatty liver disease in Asia-Pacific? J Gastroenterol Hepatol 22:794–800

    Article  PubMed  Google Scholar 

  10. Amarapurkar DN, Hashimoto E, Lesmana LA, Sollano JD, Chen PJ, Goh KL (2007) How common is non-alcoholic fatty liver disease in the Asia-Pacific region and are there local differences? J Gastroenterol Hepatol 22:788–793

    Article  PubMed  Google Scholar 

  11. Sessler AM, Ntambi JM (1998) Polyunsaturated fatty acid regulation of gene expression. J Nutr 128:923–926

    PubMed  CAS  Google Scholar 

  12. Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, Faga E, Silli B, Pagano G (2003) Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology 37:909–916

    Article  PubMed  CAS  Google Scholar 

  13. Zelber-Sagil S, Nitzan-Kaluski D, Goldsmith R, Webb M, Blendis L, Halpern Z, Oren R (2007) Long term nutritional intake and the risk for non-alcoholic fatty liver disease (NAFLD): A population based study. J Hepatol 47:711–717

    Article  Google Scholar 

  14. Oya J, Nakagami T, Sasaki S, Jimba S, Murakami K, Kasahara T, Wasada T, Sekiguchi H, Hasegawa M, Endo Y, Iwamoto Y (2010) Intake of n-3 polyunsaturated fatty acids and non-alcoholic fatty liver disease: a cross-sectional study in Japanese men and women. Eur J Clin Nutr 64:1179–1185

    Article  PubMed  CAS  Google Scholar 

  15. Spadaro L, Magliocco O, Spampinato D, Piro S, Oliveri C, Alagona C, Papa G, Rabuazzo AM, Purrello F (2008) Effects of n-3 polyunsaturated fatty acids in subjects with nonalcoholic fatty liver disease. Dig Liver Dis 40:194–199

    Article  PubMed  CAS  Google Scholar 

  16. Sofi F, Giangrandi I, Cesari F, Corsani I, Abbate R, Gensini GF, Casini A (2010) Effects of a 1-year dietary intervention with n-3 polyunsaturated fatty acid-enriched olive oil on non-alcoholic fatty liver disease patients: a preliminary study. Int J Food Sci Nutr 61:792–802

    Article  PubMed  CAS  Google Scholar 

  17. Huang T, Wahlqvist ML, Xu TC, Xu A, Zhang AZ, Li D (2010) Increased plasma n-3 polyunsaturated fatty acid is associated with improved insulin sensitivity in type 2 diabetes in China. Mol Nutr Food Res 54:S112–S119

    Article  PubMed  CAS  Google Scholar 

  18. Huang T, Bhulaidok S, Cai ZZ, Xu TC, Xu F, Wahlqvist ML, Li D (2010) Plasma phospholipids n-3 polyunsaturated fatty acid is associated with metabolic syndrome. Mol Nutr Food Res 54:1628–1635

    Article  PubMed  CAS  Google Scholar 

  19. Neuschwander-Tetri BA, Caldwell SH (2003) Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology 37:1202–1219

    Article  PubMed  Google Scholar 

  20. Sinclair AJ, O’Dea K, Dunstan G, Ireland PD, Niall M (1987) Effects on plasma lipids and fatty acid composition of very low fat diets enriched with fish or kangaroo meat. Lipids 22:523–529

    Article  PubMed  CAS  Google Scholar 

  21. Riboli E, Ronnholm H, Saracci R (1987) Biological Markers of Diet. Cancer Surv 6:685–718

    PubMed  CAS  Google Scholar 

  22. Hunter D (1995) Biochemical indicators of dietary intake. In: Willett WC (ed) Nutritional epidemiology, Oxford University Press, New York, p 143–203

  23. Larter CZ, Yeh MM, Van Rooyen DM, Teoh NC, Brooling J, Hou JY, Williams J, Clyne M, Nolan CJ, Farrell GC (2009) Roles of adipose restriction and metabolic factors in progression of steatosis to steatohepatitis in obese, diabetic mice. J Gastroenterol Hepatol 24:1658–1668

    Article  PubMed  CAS  Google Scholar 

  24. Woollett LA, Spady DK, Dietschy JM (1992) Regulatory effects of the saturated fatty-acids 6-0 through 18-0 on hepatic low-density-lipoprotein receptor activity in the Hamster. J Clin Invest 89:1133–1141

    Article  PubMed  CAS  Google Scholar 

  25. Spady DK, Woollett LA, Dietschy JM (1993) Regulation of plasma LDL-cholesterol levels by dietary cholesterol and fatty acids. Annu Rev Nutr 13:355–381

    Article  PubMed  CAS  Google Scholar 

  26. Vallim T, Salter AM (2010) Regulation of hepatic gene expression by saturated fatty acids. Prostaglandins Leukot Essent Fatty Acids 82:211–218

    Article  PubMed  CAS  Google Scholar 

  27. Yoshikawa T, Shimano H, Yahagi N, Ide T, Amemiya-Kudo M, Matsuzaka T, Nakakuki M, Tomita S, Okazaki H, Tamura Y, Iizuka Y, Ohashi K, Takahashi A, Sone H, Osuga Ji J, Gotoda T, Ishibashi S, Yamada N (2002) Polyunsaturated fatty acids suppress sterol regulatory element-binding protein 1c promoter activity by inhibition of liver X receptor (LXR) binding to LXR response elements. J Biol Chem 277:1705–1711

    Article  PubMed  CAS  Google Scholar 

  28. Allard JP, Aghdassi E, Mohammed S, Raman M, Avand G, Arendt BM, Jalali P, Kandasamy T, Prayitno N, Sherman M, Guindi M, Ma DW, Heathcote JE (2008) Nutritional assessment and hepatic fatty acid composition in non-alcoholic fatty liver disease (NAFLD): a cross-sectional study. J Hepatol 48:300–307

    Article  PubMed  CAS  Google Scholar 

  29. Tanaka N, Sano K, Horiuchi A, Tanaka E, Kiyosawa K, Aoyama T (2008) Highly purified eicosapentaenoic acid treatment improves nonalcoholic steatohepatitis. J Clin Gastroenterol 42:413–418

    Article  PubMed  CAS  Google Scholar 

  30. Araya J, Rodrigo R, Videla LA, Thielemann L, Orellana M, Pettinelli P, Poniachik J (2004) Increase in long-chain polyunsaturated fatty acid n-6/n-3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin Sci 106:635–643

    Article  PubMed  CAS  Google Scholar 

  31. Fan JG, Peng YD (2007) Metabolic syndrome and non-alcoholic fatty liver disease: Asian definitions and Asian studies. Hepatobiliary Pancreat Dis Int 6:572–578

    PubMed  Google Scholar 

  32. Puri P, Wiest MM, Cheung O, Mirshahi F, Sargeant C, Min HK, Contos MJ, Sterling RK, Fuchs M, Zhou H, Watkins SM, Sanyal AJ (2009) The plasma lipidomic signature of nonalcoholic steatohepatitis. Hepatology 50:1827–1838

    Article  PubMed  CAS  Google Scholar 

  33. Fu CC, Chen MC, Li YM, Liu TT, Wang LY (2009) The risk factors for ultrasound-diagnosed non-alcoholic fatty liver disease among adolescents. Ann Acad Med Singap 38:15–21

    PubMed  Google Scholar 

  34. Cardoso CRL, Leite NC, Salles GF, Araujo ALE, Villela-Nogueira CA (2009) Prevalence and associated factors of non-alcoholic fatty liver disease in patients with type-2 diabetes mellitus. Liver Int 29:113–119

    Article  PubMed  Google Scholar 

  35. Ruhl CE, Everhart JE (2003) Determinants of the association of overweight with elevated serum alanine aminotransferase activity in the United States. Gastroenterology 124:71–79

    Article  PubMed  CAS  Google Scholar 

  36. Zelber-Sagi S, Nitzan-Kaluski D, Halpern Z, Oren R (2006) Prevalence of primary non-alcoholic fatty liver disease in a population-based study and its association with biochemical and anthropometric measures. Liver Int 26:856–863

    Article  PubMed  Google Scholar 

  37. Kim BK, Han KH, Ahn SH (2011) “Normal” range of alanine aminotransferase levels for Asian population. J Gastroenterol Hepatol 26:219–220

    Article  PubMed  Google Scholar 

  38. Ford ES, Giles WH, Dietz WH (2002) Prevalence of the metabolic syndrome among US adults—findings from the third national health and nutrition examination survey. JAMA 287:356–359

    Article  PubMed  Google Scholar 

  39. Nestel P, Lyu R, Low LP, Sheu WH, Nitiyanant W, Saito I, Tan CE (2007) Metabolic syndrome: recent prevalence in East and Southeast Asian populations. Asia Pac J Clin Nutr 16:362–367

    PubMed  Google Scholar 

  40. Li Y, Xu C, Yu C, Xu L, Miao M (2009) Association of serum uric acid level with non-alcoholic fatty liver disease: a cross-sectional study. J Hepatol 50:1029–1034

    Article  PubMed  CAS  Google Scholar 

  41. Bajaj S, Nigam P, Luthra A, Pandey RM, Kondal D, Bhatt SP, Wasir JS, Misra A (2009) A case-control study on insulin resistance, metabolic co-variates & prediction score in non-alcoholic fatty liver disease. Indian J Med Res 129:285–292

    PubMed  CAS  Google Scholar 

  42. Uchil D, Pipalia D, Chawla M, Patel R, Maniar S, Narayani, Juneja A (2009) Non-alcoholic fatty liver disease (NAFLD)–the hepatic component of metabolic syndrome. J Assoc Physicians India 57:201–204

    PubMed  Google Scholar 

  43. Ma J, Folsom AR, Shahar E, Eckfeldt JH (1995) Plasma fatty-acid composition as an indicator of habitual dietary-fat intake in middle-aged adults. Am J Clin Nutr 62:564–571

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The study was funded by the National Natural Science Foundation of China (NSFC, No. 30972464), the National Basic Research Program of China (973 Program: 2011CB504002), Natural Science Foundation of Zhejiang Province (Y205709) and Zhejiang University (No. H20091920).

Conflict of interest

The authors have declared that there is no potential conflict of interest with respect to this manuscript.

Author information

Authors and Affiliations

  1. Department of Food Science and Nutrition, Zhejiang University, 866 Yuhangtang Road, Hangzhou, 310058, China

    Ju-Sheng Zheng, Amei Xu, Tao Huang & Duo Li

  2. APCNS Centre of Nutrition and Food Safety, Hangzhou, China

    Ju-Sheng Zheng, Amei Xu, Tao Huang & Duo Li

  3. Department of Clinical Laboratory, Zhejiang Hospital, Hangzhou, China

    Xiaomei Yu

Authors
  1. Ju-Sheng Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amei Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaomei Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Duo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Duo Li.

About this article

Cite this article

Zheng, JS., Xu, A., Huang, T. et al. Low Docosahexaenoic Acid Content in Plasma Phospholipids is Associated with Increased Non-alcoholic Fatty Liver Disease in China. Lipids 47, 549–556 (2012). https://doi.org/10.1007/s11745-012-3671-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11745-012-3671-4

Keywords

Search

Navigation