Circulating Docosahexaenoic Acid Levels Are Associated with Fetal Insulin Sensitivity

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2014 Jan 24

PMID 24454790

Citations 25

Authors

Jin-Ping Zhao

Emile Levy

William D Fraser

Pierre Julien

Edgard Delvin

Alain Montoudis

Schohraya Spahis

Carole Garofalo

Anne Monique Nuyt

Zhong-Cheng Luo

Affiliations

Soon will be listed here.

Abstract

Background: Arachidonic acid (AA; C20∶4 n-6) and docosahexaenoic acid (DHA; C22∶6 n-3) are important long-chain polyunsaturated fatty acids (LC-PUFA) in maintaining pancreatic beta-cell structure and function. Newborns of gestational diabetic mothers are more susceptible to the development of type 2 diabetes in adulthood. It is not known whether low circulating AA or DHA is involved in perinatally "programming" this susceptibility. This study aimed to assess whether circulating concentrations of AA, DHA and other fatty acids are associated with fetal insulin sensitivity or beta-cell function, and whether low circulating concentrations of AA or DHA are involved in compromised fetal insulin sensitivity in gestational diabetic pregnancies.

Methods And Principal Findings: In a prospective singleton pregnancy cohort, maternal (32-35 weeks gestation) and cord plasma fatty acids were assessed in relation to surrogate indicators of fetal insulin sensitivity (cord plasma glucose-to-insulin ratio, proinsulin concentration) and beta-cell function (proinsulin-to-insulin ratio) in 108 mother-newborn pairs. Cord plasma DHA levels (in percentage of total fatty acids) were lower comparing newborns of gestational diabetic (n = 24) vs. non-diabetic pregnancies (2.9% vs. 3.5%, P = 0.01). Adjusting for gestational age at blood sampling, lower cord plasma DHA levels were associated with lower fetal insulin sensitivity (lower glucose-to-insulin ratio, r = 0.20, P = 0.036; higher proinsulin concentration, r = -0.37, P <0.0001). The associations remained after adjustment for maternal and newborn characteristics. Cord plasma saturated fatty acids C18∶0 and C20∶0 were negatively correlated with fetal insulin sensitivity, but their levels were not different between gestational diabetic and non-diabetic pregnancies. Cord plasma AA levels were not correlated with fetal insulin sensitivity.

Conclusion: Low circulating DHA levels are associated with compromised fetal insulin sensitivity, and may be involved in perinatally "programming" the susceptibility to type 2 diabetes in the offspring of gestational diabetic mothers.

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References

Lepage G, Levy E, Ronco N, Smith L, Galeano N, Roy C . Direct transesterification of plasma fatty acids for the diagnosis of essential fatty acid deficiency in cystic fibrosis. J Lipid Res. 1989; 30(10):1483-90. View

Setia S, Sridhar M, Bhat V, Chaturvedula L, Vinayagamoorti R, John M . Insulin sensitivity and insulin secretion at birth in intrauterine growth retarded infants. Pathology. 2006; 38(3):236-8. DOI: 10.1080/00313020600696256. View

Clandinin M, Cheema S, Field C, Garg M, Venkatraman J, Clandinin T . Dietary fat: exogenous determination of membrane structure and cell function. FASEB J. 1991; 5(13):2761-9. DOI: 10.1096/fasebj.5.13.1916101. View

Dixon G, Nolan J, McClenaghan N, Flatt P, Newsholme P . Arachidonic acid, palmitic acid and glucose are important for the modulation of clonal pancreatic beta-cell insulin secretion, growth and functional integrity. Clin Sci (Lond). 2003; 106(2):191-9. DOI: 10.1042/CS20030261. View

Luo Z, Delvin E, Fraser W, Audibert F, Deal C, Julien P . Maternal glucose tolerance in pregnancy affects fetal insulin sensitivity. Diabetes Care. 2010; 33(9):2055-61. PMC: 2928362. DOI: 10.2337/dc10-0819. View

Konrad R, Major C, Wolf B . Diacylglycerol hydrolysis to arachidonic acid is necessary for insulin secretion from isolated pancreatic islets: sequential actions of diacylglycerol and monoacylglycerol lipases. Biochemistry. 1994; 33(45):13284-94. DOI: 10.1021/bi00249a015. View

Spahis S, Vanasse M, Belanger S, Ghadirian P, Grenier E, Levy E . Lipid profile, fatty acid composition and pro- and anti-oxidant status in pediatric patients with attention-deficit/hyperactivity disorder. Prostaglandins Leukot Essent Fatty Acids. 2008; 79(1-2):47-53. DOI: 10.1016/j.plefa.2008.07.005. View

Gibson R, Muhlhausler B, Makrides M . Conversion of linoleic acid and alpha-linolenic acid to long-chain polyunsaturated fatty acids (LCPUFAs), with a focus on pregnancy, lactation and the first 2 years of life. Matern Child Nutr. 2011; 7 Suppl 2:17-26. PMC: 6860743. DOI: 10.1111/j.1740-8709.2011.00299.x. View

Korotkova M, Gabrielsson B, Holmang A, Larsson B, Hanson L, Strandvik B . Gender-related long-term effects in adult rats by perinatal dietary ratio of n-6/n-3 fatty acids. Am J Physiol Regul Integr Comp Physiol. 2005; 288(3):R575-9. DOI: 10.1152/ajpregu.00342.2004. View

10.

Lambert M, Paradis G, OLoughlin J, Delvin E, Hanley J, Levy E . Insulin resistance syndrome in a representative sample of children and adolescents from Quebec, Canada. Int J Obes Relat Metab Disord. 2004; 28(7):833-41. DOI: 10.1038/sj.ijo.0802694. View

11.

Innis S, Elias S . Intakes of essential n-6 and n-3 polyunsaturated fatty acids among pregnant Canadian women. Am J Clin Nutr. 2003; 77(2):473-8. DOI: 10.1093/ajcn/77.2.473. View

12.

Bardenheier B, Elixhauser A, Imperatore G, Devlin H, Kuklina E, Geiss L . Variation in prevalence of gestational diabetes mellitus among hospital discharges for obstetric delivery across 23 states in the United States. Diabetes Care. 2012; 36(5):1209-14. PMC: 3631849. DOI: 10.2337/dc12-0901. View

13.

Konard R, Stoller J, Gao Z, Wolf B . Eicosapentaenoic acid (C20:5) augments glucose-induced insulin secretion from beta-TC3 insulinoma cells. Pancreas. 1996; 13(3):253-8. DOI: 10.1097/00006676-199610000-00007. View

14.

Min Y, Lowy C, Ghebremeskel K, Thomas B, Bitsanis D, Crawford M . Fetal erythrocyte membrane lipids modification: preliminary observation of an early sign of compromised insulin sensitivity in offspring of gestational diabetic women. Diabet Med. 2005; 22(7):914-20. DOI: 10.1111/j.1464-5491.2005.01556.x. View

15.

Resnick H, Harris M, Brock D, Harris T . American Diabetes Association diabetes diagnostic criteria, advancing age, and cardiovascular disease risk profiles: results from the Third National Health and Nutrition Examination Survey. Diabetes Care. 2000; 23(2):176-80. DOI: 10.2337/diacare.23.2.176. View

16.

Makrides M, Gibson R . Long-chain polyunsaturated fatty acid requirements during pregnancy and lactation. Am J Clin Nutr. 2000; 71(1 Suppl):307S-11S. DOI: 10.1093/ajcn/71.1.307S. View

17.

Min Y, Ghebremeskel K, Lowy C, Thomas B, Crawford M . Adverse effect of obesity on red cell membrane arachidonic and docosahexaenoic acids in gestational diabetes. Diabetologia. 2003; 47(1):75-81. DOI: 10.1007/s00125-003-1275-5. View

18.

Kaushik M, Mozaffarian D, Spiegelman D, Manson J, Willett W, Hu F . Long-chain omega-3 fatty acids, fish intake, and the risk of type 2 diabetes mellitus. Am J Clin Nutr. 2009; 90(3):613-20. PMC: 2728645. DOI: 10.3945/ajcn.2008.27424. View

19.

Whelan J, Jahns L, Kavanagh K . Docosahexaenoic acid: measurements in food and dietary exposure. Prostaglandins Leukot Essent Fatty Acids. 2009; 81(2-3):133-6. DOI: 10.1016/j.plefa.2009.05.008. View

20.

Ortega-Senovilla H, Alvino G, Taricco E, Cetin I, Herrera E . Gestational diabetes mellitus upsets the proportion of fatty acids in umbilical arterial but not venous plasma. Diabetes Care. 2008; 32(1):120-2. PMC: 2606843. DOI: 10.2337/dc08-0679. View