Login Register Cart 0
Generic placeholder image

Current Vascular Pharmacology

Editor-in-Chief

ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
General Review Article

Maternal Dyslipidaemia in Pregnancy with Gestational Diabetes Mellitus: Possible Impact on Foetoplacental Vascular Function and Lipoproteins in the Neonatal Circulation

Author(s): Susana Contreras-Duarte, Lorena Carvajal, Bárbara Fuenzalida, Claudette Cantin, Luis Sobrevia and Andrea Leiva*

Volume 17, Issue 1, 2019

Page: [52 - 71] Pages: 20

DOI: 10.2174/1570161115666171116154247

Price: $65

Abstract

Dyslipidaemia occurs in pregnancy to secure foetal development. The mother shows a physiological increase in plasma total cholesterol and Triglycerides (TG) as pregnancy progresses (i.e. maternal physiological dyslipidaemia in pregnancy). However, in some women pregnancy-associated dyslipidaemia exceeds this physiological adaptation. The consequences of this condition on the developing fetus include endothelial dysfunction of the foetoplacental vasculature and development of foetal aortic atherosclerosis. Gestational Diabetes Mellitus (GDM) associates with abnormal function of the foetoplacental vasculature due to foetal hyperglycaemia and hyperinsulinaemia, and associates with development of cardiovascular disease in adulthood. Supraphysiological dyslipidaemia is also detected in GDM pregnancies. Although there are several studies showing the alteration in the maternal and neonatal lipid profile in GDM pregnancies, there are no studies addressing the effect of dyslipidaemia in the maternal and foetal vasculature. The literature reviewed suggests that dyslipidaemia in GDM pregnancy should be an additional factor contributing to worsen GDM-associated endothelial dysfunction by altering signalling pathways involving nitric oxide bioavailability and neonatal lipoproteins.

Keywords: Dyslipidaemia, gestational diabetes, endothelium, lipoprotein, pregnancy, triglycerides.

« Previous Next »
Graphical Abstract

[1]
Herrera E, Desoye G. Maternal and fetal lipid metabolism under normal and gestational diabetic conditions. Horm Mol Biol Clin Investig 2016; 26(2): 109-27.
[2]
Napoli C, D’Armiento FP, Mancini FP, et al. Fatty streak formation occurs in human fetal aortas and is greatly enhanced by maternal hypercholesterolemia. Intimal accumulation of low density lipoprotein and its oxidation precede monocyte recruitment into early atherosclerotic lesions. J Clin Invest 1997; 100(11): 2680-90.
[3]
Napoli C, Glass CK, Witztum JL, Deutsch R, D’Armiento FP, Palinski W. Influence of maternal hypercholesterolaemia during pregnancy on progression of early atherosclerotic lesions in childhood: Fate of Early Lesions in Children (FELIC) study. Lancet 1999; 354(9186): 1234-41.
[4]
Liguori A, D’Armiento FP, Palagiano A, et al. Effect of gestational hypercholesterolaemia on omental vasoreactivity, placental enzyme activity and transplacental passage of normal and oxidised fatty acids. BJOG 2007; 114(12): 1547-56.
[5]
Ethier-Chiasson M, Forest J-C, Giguere Y, et al. Modulation of placental protein expression of OLR1: Implication in pregnancy-related disorders or pathologies. Reproduction 2008; 136(4): 491-502.
[6]
Marseille-Tremblay C, Ethier-Chiasson M, Forest J-C, et al. Impact of maternal circulating cholesterol and gestational diabetes mellitus on lipid metabolism in human term placenta. Mol Reprod Dev 2008; 75(6): 1054-62.
[7]
Leiva A, Salsoso R, Saez T, Sanhueza C, Pardo F, Sobrevia L. Cross-sectional and longitudinal lipid determination studies in pregnant women reveal an association between increased maternal LDL cholesterol concentrations and reduced human umbilical vein relaxation. Placenta 2015; 36(8): 895-902.
[8]
Zhang R, Dong S, Ma W-W, et al. Modulation of cholesterol transport by maternal hypercholesterolemia in human full-term placenta. PLoS One 2017; 12(2): e0171934.
[9]
Montes A, Walden CE, Knopp RH, Cheung M, Chapman MB, Albers JJ. Physiologic and supraphysiologic increases in lipoprotein lipids and apoproteins in late pregnancy and postpartum. Possible markers for the diagnosis of “prelipemia”. Arteriosclerosis 1984; 4(4): 407-17.
[10]
Leiva A, de Medina CD, Salsoso R, et al. Maternal hypercholesterolemia in pregnancy associates with umbilical vein endothelial dysfunction: Role of endothelial nitric oxide synthase and arginase II. Arterioscler Thromb Vasc Biol 2013; 33(10): 2444-53.
[11]
Barrett HL, Dekker Nitert M, McIntyre HD, Callaway LK. Normalizing metabolism in diabetic pregnancy: Is it time to target lipids? Diabetes Care 2014; 37(5): 1484-93.
[12]
Leiva A, Fuenzalida B, Salsoso R, et al. Tetrahydrobiopterin role in human umbilical vein endothelial dysfunction in maternal supraphysiological hypercholesterolemia. Biochim Biophys Acta 2016; 1862(4): 536-44.
[13]
Leiva A, Fuenzalida B, Barros E, et al. Nitric oxide is a central common metabolite in vascular dysfunction associated with diseases of human pregnancy. Curr Vasc Pharmacol 2016; 14(3): 237-59.
[14]
Palinski W, Nicolaides E, Liguori A, Napoli C. Influence of maternal dysmetabolic conditions during pregnancy on cardiovascular disease. J Cardiovasc Transl Res 2009; 2(3): 277-85.
[15]
Barrett HL, Dekker Nitert M, McIntyre HD, Callaway LK. Maternal lipids in pre-eclampsia: Innocent bystander or culprit? Hypertens Pregnancy 2014; 33(4): 508-23. b
[16]
American Diabetes Association.Standards of medical care in diabetes-2017: Summary of revisions. Diabetes Care 2017; 40(Suppl. 1): 4-5.
[17]
Lappas M, Hiden U, Desoye G, Froehlich J, Hauguel-de Mouzon S, Jawerbaum A. The role of oxidative stress in the pathophysiology of gestational diabetes mellitus. Antioxid Redox Signal 2011; 15(12): 3061-100.
[18]
Di Fulvio P, Pandolfi A, Formoso G, et al. Features of endothelial dysfunction in umbilical cord vessels of women with gestational diabetes. Nutr Metab Cardiovasc Dis 2014; 24(12): 1337-45.
[19]
Guzmán-Gutiérrez E, Arroyo P, Salsoso R, et al. Role of insulin and adenosine in the human placenta microvascular and macrovascular endothelial cell dysfunction in gestational diabetes mellitus. Microcirculation 2014; 21(1): 26-37.
[20]
Sreckovic I, Birner-Gruenberger R, Obrist B, et al. Distinct composition of human fetal HDL attenuates its anti-oxidative capacity. Biochim Biophys Acta 2013; 1831(4): 737-46.
[21]
Herrera E, Amusquivar E, Lopez-Soldado I, Ortega H. Maternal lipid metabolism and placental lipid transfer. Horm Res 2006; 65(Suppl. 3): 59-64.
[22]
Woollett LA. Where does fetal and embryonic cholesterol originate and what does it do? Annu Rev Nutr 2008; 28: 97-114.
[23]
Montelongo A, Lasuncion MA, Pallardo LF, Herrera E. Longitudinal study of plasma lipoproteins and hormones during pregnancy in normal and diabetic women. Diabetes 1992; 41(12): 1651-9.
[24]
Herrera E, Ortega-Senovilla H. Disturbances in lipid metabolism in diabetic pregnancy - Are these the cause of the problem? Best Pract Res Clin Endocrinol Metab 2010; 24(4): 515-25.
[25]
Scifres CM, Chen B, Nelson DM, Sadovsky Y. Fatty acid binding protein 4 regulates intracellular lipid accumulation in human trophoblasts. J Clin Endocrinol Metab 2011; 96(7): 1083-91.
[26]
Woollett LA. Maternal cholesterol in fetal development: Transport of cholesterol from the maternal to the fetal circulation. Am J Clin Nutr 2005; 82(6): 1155-61.
[27]
Knopp RH, Warth MR, Charles D, et al. Lipoprotein metabolism in pregnancy, fat transport to the fetus, and the effects of diabetes. Biol Neonate 1986; 50(6): 297-317
[28]
Desoye G, Schweditsch MO, Pfeiffer KP, Zechner R, Kostner GM. Correlation of hormones with lipid and lipoprotein levels during normal pregnancy and postpartum. J Clin Endocrinol Metab 1987; 64(4): 704-12.
[29]
Saarelainen H, Laitinen T, Raitakari OT, et al. Pregnancy-related hyperlipidemia and endothelial function in healthy women. Circ J 2006; 70(6): 768-72.
[30]
Saarelainen H, Valtonen P, Punnonen K, et al. Subtle changes in ADMA and l-arginine concentrations in normal pregnancies are unlikely to account for pregnancy-related increased flow-mediated dilatation. Clin Physiol Funct Imaging 2008; 28(2): 120-4.
[31]
Palinski W. Effect of maternal cardiovascular conditions and risk factors on offspring cardiovascular disease. Circulation 2014; 129(20): 2066-77.
[32]
Reaven GM, Chen YD. Role of insulin in regulation of lipoprotein metabolism in diabetes. Diabetes Metab Rev 1988; 4(7): 639-52.
[33]
Gratacos E, Casals E, Gomez O, et al. Increased susceptibility to low density lipoprotein oxidation in women with a history of pre-eclampsia. BJOG 2003; 110(4): 400-4.
[34]
Metzger BE, Phelps RL, Freinkel N, Navickas IA. Effects of gestational diabetes on diurnal profiles of plasma glucose, lipids, and individual amino acids. Diabetes Care 1980; 3(3): 402-9.
[35]
Huidobro A, Fulford A, Carrasco E. Incidence of gestational diabetes and relationship to obesity in Chilean pregnant women. Rev Med Chil 2004; 132(8): 931-8.
[36]
Grandi C, Tapia JL, Cardoso VC. Impact of maternal diabetes mellitus on mortality and morbidity of very low birth weight infants: A multicenter Latin America study. J Pediatr 2015; 91(3): 234-41.
[37]
Schwartz N, Nachum Z, Green MS. Risk factors of gestational diabetes mellitus recurrence: A meta-analysis. Endocrine 2016; 53(3): 662-71.
[38]
Desoye G, Nolan CJ. The fetal glucose steal: An underappreciated phenomenon in diabetic pregnancy. Diabetologia 2016; 59(6): 1089-94.
[39]
Pedersen J. Weight and length at birth of infants of diabetic mothers. Acta Endocrinol (Copenh) 1954; 16(4): 330-42.
[40]
Ogonowski J, Miazgowski T, Czeszynska MB, Jaskot B, Kuczynska M, Celewicz Z. Factors influencing risk of macrosomia in women with gestational diabetes mellitus undergoing intensive diabetic care. Diabetes Res Clin Pract 2008; 80(3): 405-10.
[41]
Olmos PR, Borzone GR, Olmos RI, et al. Gestational diabetes and pre-pregnancy overweight: Possible factors involved in newborn macrosomia. J Obstet Gynaecol Res 2012; 38(1): 208-14.
[42]
Kc K, Shakya S, Zhang H. Gestational diabetes mellitus and macrosomia: A literature review. Ann Nutr Metab 2015; 66(Suppl. 2): 14-20.
[43]
Caballero AE. Endothelial dysfunction in obesity and insulin resistance: A road to diabetes and heart disease. Obes Res 2003; 11(11): 1278-89.
[44]
Sobrevia L, Abarzua F, Nien JK, et al. Review: Differential placental macrovascular and microvascular endothelial dysfunction in gestational diabetes. Placenta 2011; 32(Suppl. 2): 159-64.
[45]
Sobrevia L, Salsoso R, Fuenzalida B, et al. Insulin is a key modulator of fetoplacental endothelium metabolic disturbances in gestational diabetes mellitus. Front Physiol 2016; 7: 119.
[46]
Lee H, Jang HC, Park HK, Cho NH. Early manifestation of cardiovascular disease risk factors in offspring of mothers with previous history of gestational diabetes mellitus. Diabetes Res Clin Pract 2007; 78(2): 238-45.
[47]
Lekva T, Michelsen AE, Aukrust P, Henriksen T, Bollerslev J, Ueland T. Leptin and adiponectin as predictors of cardiovascular risk after gestational diabetes mellitus. Cardiovasc Diabetol 2017; 16(1): 5.
[48]
Bergel R, Hadar E, Toledano Y, Hod M. Pharmacological management of gestational diabetes mellitus. Curr Diab Rep 2016; 16(11): 118.
[49]
Brown J, Ceysens G, Boulvain M. Exercise for pregnant women with gestational diabetes for improving maternal and fetal outcomes. Cochrane Database Syst Rev 2017; 6: CD012202.
[50]
Uma R, Bhavadharini B, Ranjani H, et al. Pregnancy outcome of gestational diabetes mellitus using a structured model of care: WINGS project (WINGS-10). J Obstet Gynaecol Res 2017; 43(3): 468-75.
[51]
Gillman MW, Oakey H, Baghurst PA, Volkmer RE, Robinson JS, Crowther CA. Effect of treatment of gestational diabetes mellitus on obesity in the next generation. Diabetes Care 2010; 33(5): 964-8.
[52]
Silva L, Subiabre M, Araos J, et al. Insulin/adenosine axis linked signalling. Mol Aspects Med 2017; 55: 45-61.
[53]
Subiabre M, Silva L, Villalobos-Labra R, et al. Maternal insulin therapy does not restore foetoplacental endothelial dysfunction in gestational diabetes mellitus. Biochim Biophys Acta 2017; 1863: 2987-98.
[54]
Monteiro LJ, Norman JE, Rice GE, Illanes SE. Fetal programming and gestational diabetes mellitus. Placenta 2016; 48(Suppl. 1): 54-60.
[55]
Deanfield J, Donald A, Ferri C, et al. Endothelial function and dysfunction. Part I: Methodological issues for assessment in the different vascular beds: A statement by the working group on endothelin and endothelial factors of the European society of hypertension. J Hypertens 2005; 23(1): 7-17.
[56]
Marzioni D, Tamagnone L, Capparuccia L, et al. Restricted innervation of uterus and placenta during pregnancy: Evidence for a role of the repelling signal Semaphorin 3A. Dev Dyn 2004; 231(4): 839-48.
[57]
Mitchell JA, Warner TD. Cyclo-oxygenase-2: pharmacology, physiology, biochemistry and relevance to NSAID therapy. Br J Pharmacol 1999; 128(6): 1121-32.
[58]
Mitchell JA, Ali F, Bailey L, Moreno L, Harrington LS. Role of nitric oxide and prostacyclin as vasoactive hormones released by the endothelium. Exp Physiol 2008; 93(1): 141-7.
[59]
Majed BH, Khalil RA. Molecular mechanisms regulating the vascular prostacyclin pathways and their adaptation during pregnancy and in the newborn. Pharmacol Rev 2012; 64(3): 540-82.
[60]
Sheppard SJ, Khalil RA. Risk factors and mediators of the vascular dysfunction associated with hypertension in pregnancy. Cardiovasc Hematol Disord Drug Targets 2010; 10(1): 33-52.
[61]
Robaut C, Mondon F, Bandet J, Ferre F, Cavero I. Regional distribution and pharmacological characterization of [125I]endothelin-1 binding sites in human fetal placental vessels. Placenta 1991; 12(1): 55-67.
[62]
Sabry S, Mondon F, Ferre F, Dinh-Xuan AT. In vitro contractile and relaxant responses of human resistance placental stem villi arteries of healthy parturients: Role of endothelium. Fundam Clin Pharmacol 1995; 9(1): 46-51.
[63]
Read MA, Boura AL, Walters WA. Vascular actions of purines in the foetal circulation of the human placenta. Br J Pharmacol 1993; 110(1): 454-60.
[64]
Dobronyi I, Hung KS, Satchell DG, Maguire MH. Evidence for a novel P2X purinoceptor in human placental chorionic surface arteries. Eur J Pharmacol 1997; 320(1): 61-4.
[65]
Valdecantos P, Briones R, Moya P, Germain A, Huidobro-Toro JP. Pharmacological identification of P2X1, P2X4 and P2X7 nucleotide receptors in the smooth muscles of human umbilical cord and chorionic blood vessels. Placenta 2003; 24(1): 17-26.
[66]
Buvinic S, Poblete MI, Donoso MV, et al. P2Y1 and P2Y2 receptor distribution varies along the human placental vascular tree: Role of nucleotides in vascular tone regulation. J Physiol 2006; 573(Pt 2): 427-43.
[67]
Ralevic V, Burrell S, Kingdom J, Burnstock G. Characterization of P2 receptors for purine and pyrimidine nucleotides in human placental cotyledons. Br J Pharmacol 1997; 121(6): 1121-6.
[68]
Myatt L, Brockman DE, Eis AL, Pollock JS. Immunohistochemical localization of nitric oxide synthase in the human placenta. Placenta 1993; 14(5): 487-95.
[69]
Moncada S, Higgs EA. The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol 2006; 147(Suppl. 1): 193-201.
[70]
San Martín R, Sobrevia L. Gestational diabetes and the adenosine/L-arginine/nitric oxide (ALANO) pathway in human umbilical vein endothelium. Placenta 2006; 27(1): 1-10.
[71]
Fotiadis D, Kanai Y, Palacin M. The SLC3 and SLC7 families of amino acid transporters. Mol Aspects Med 2013; 34(2-3): 139-58.
[72]
Förstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 2012; 33(7): 829-37.
[73]
Mori M. Regulation of nitric oxide synthesis and apoptosis by arginase and arginine recycling. J Nutr 2007; 137(6)(Suppl. 2): 1616-20.
[74]
Prieto CP, Krause BJ, Quezada C, San Martin R, Sobrevia L, Casanello P. Hypoxia-reduced nitric oxide synthase activity is partially explained by higher arginase-2 activity and cellular redistribution in human umbilical vein endothelium. Placenta 2011; 32(12): 932-40.
[75]
Ryoo S, Gupta G, Benjo A, et al. Endothelial arginase II: A novel target for the treatment of atherosclerosis. Circ Res 2008; 102(8): 923-32.
[76]
Ignarro LJ, Napoli C. Novel features of nitric oxide, endothelial nitric oxide synthase, and atherosclerosis. Curr Atheroscler Rep 2004; 6(4): 281-7.
[77]
Szostak-Wegierek D, Szamotulska K. Fetal development and risk of cardiovascular diseases and diabetes type 2 in adult life. Med Wieku Rozwoj 2011; 15(3): 203-15.
[78]
Mitanchez D, Yzydorczyk C, Siddeek B, Boubred F, Benahmed M, Simeoni U. The offspring of the diabetic mother--short- and long-term implications. Best Pract Res Clin Obstet Gynaecol 2015; 29(2): 256-69.
[79]
Mayret-Mesquiti M, Perez-Mendez O, Rodriguez ME, et al. Hypertriglyceridemia is linked to reduced nitric oxide synthesis in women with hypertensive disorders of pregnancy. Hypertens Pregnancy 2007; 26(4): 423-31.
[80]
Tabas I, Garcia-Cardena G, Owens GK. Recent insights into the cellular biology of atherosclerosis. J Cell Biol 2015; 209(1): 13-22.
[81]
Garg P, Badhwar S, Jaryal AK, Kachhawa G, Deepak KK, Kriplani A. The temporal trend of vascular function in women with gestational diabetes. Vasc Med 2017; 22(2): 96-102.
[82]
Davenport MH, Goswami R, Shoemaker JK, Mottola MF. Influence of hyperglycemia during and after pregnancy on postpartum vascular function. Am J Physiol Regul Integr Comp Physiol 2012; 302(6): 768-75.
[83]
Anastasiou E, Lekakis JP, Alevizaki M, et al. Impaired endothelium-dependent vasodilatation in women with previous gestational diabetes. Diabetes Care 1998; 21(12): 2111-5.
[84]
Paradisi G, Biaggi A, Ferrazzani S, De Carolis S, Caruso A. Abnormal carbohydrate metabolism during pregnancy: Association with endothelial dysfunction. Diabetes Care 2002; 25(3): 560-4.
[85]
Fakhrzadeh H, Alatab S, Sharifi F, et al. Carotid intima media thickness, brachial flow mediated dilation and previous history of gestational diabetes mellitus. J Obstet Gynaecol Res 2012; 38(8): 1057-63.
[86]
Guimaraes MFB, Brandao AHF, Rezende CA, et al. Assessment of endothelial function in pregnant women with preeclampsia and gestational diabetes mellitus by flow-mediated dilation of brachial artery. Arch Gynecol Obstet 2014; 290(3): 441-7.
[87]
Karoli R, Siddiqi Z, Fatima J, Shukla V, Mishra PP, Khan FA. Assessment of noninvasive risk markers of subclinical atherosclerosis in premenopausal women with previous history of gestational diabetes mellitus. Heart Views 2015; 16(1): 13-8.
[88]
Sokup A, Ruszkowska B, Goralczyk B, et al. Elevation of sE-selectin levels 2-24 months following gestational diabetes is associated with early cardiometabolic risk in nondiabetic women. Int J Endocrinol 2012; 2012: 278050.
[89]
Sokup A, Ruszkowska-Ciastek B, Walentowicz-Sadlecka M. Heterogeneity of cardiovascular risk factors profile in non-diabetic women 2-24 months post gestational diabetes mellitus. Gynecol Endocrinol 2014; 30(5): 350-4.
[90]
Brewster S, Floras J, Zinman B, Retnakaran R. Endothelial function in women with and without a history of glucose intolerance in pregnancy. J Diabetes Res 2013; 2013: 382670.
[91]
Kurt M, Zulfikaroglu E, Ucankus NL, Omeroglu S, Ozcan U. Expression of intercellular adhesion molecule-1 in umbilical and placental vascular tissue of gestational diabetic and normal pregnancies. Arch Gynecol Obstet 2010; 281(1): 71-6.
[92]
Díaz-Pérez FI, Hiden U, Gauster M, et al. Post-transcriptional down regulation of ICAM-1 in feto-placental endothelium in GDM. Cell Adhes Migr 2016; 10(1-2): 18-27.
[93]
Hiden U, Lang U, Desoye G. Fetoplacental disturbances in gestational diabetes mellitus. Gynakol Geburtshilfliche Rundsch 2009; 49(4): 224-9.
[94]
Vasquez G, Sanhueza F, Vasquez R, et al. Role of adenosine transport in gestational diabetes-induced L-arginine transport and nitric oxide synthesis in human umbilical vein endothelium. J Physiol 2004; 560(Pt 1): 111-22.
[95]
Guzmán-Gutiérrez E, Westermeier F, Salomon C, et al. Insulin-increased L-arginine transport requires A(2A) adenosine receptors activation in human umbilical vein endothelium. PLoS One 2012; 7(7): e41705.
[96]
Westermeier F, Salomon C, Gonzalez M, et al. Insulin restores gestational diabetes mellitus-reduced adenosine transport involving differential expression of insulin receptor isoforms in human umbilical vein endothelium. Diabetes 2011; 60(6): 1677-87.
[97]
Mittermayer F, Mayer BX, Meyer A, et al. Circulating concentrations of asymmetrical dimethyl-L-arginine are increased in women with previous gestational diabetes. Diabetologia 2002; 45(10): 1372-8.
[98]
Sobrevia L, Cesare P, Yudilevich DL, Mann GE. Diabetes-induced activation of system y+ and nitric oxide synthase in human endothelial cells: Association with membrane hyperpolarization. J Physiol 1995; 489(Pt 1): 183-92.
[99]
Thomas SR, Chen K, Keaney JFJ. Oxidative stress and endothelial nitric oxide bioactivity. Antioxid Redox Signal 2003; 5(2): 181-94.
[100]
Gonzalez M, Rojas S, Avila P, et al. Insulin reverses D-glucose-increased nitric oxide and reactive oxygen species generation in human umbilical vein endothelial cells. PLoS One 2015; 10(4): e0122398.
[101]
Biri A, Onan A, Devrim E, Babacan F, Kavutcu M, Durak I. Oxidant status in maternal and cord plasma and placental tissue in gestational diabetes. Placenta 2006; 27(2-3): 327-32.
[102]
Sobrevia L, Gonzalez M. A role for insulin on L-arginine transport in fetal endothelial dysfunction in hyperglycaemia. Curr Vasc Pharmacol 2009; 7(4): 467-74.
[103]
Gonzalez M, Gallardo V, Rodriguez N, et al. Insulin-stimulated L-arginine transport requires SLC7A1 gene expression and is associated with human umbilical vein relaxation. J Cell Physiol 2011; 226(11): 2916-24.
[104]
Dubé E, Ethier-Chiasson M, Lafond J. Modulation of cholesterol transport by insulin-treated gestational diabetes mellitus in human full-term placenta. Biol Reprod 2013; 88(1): 16.
[105]
AbouGhalia AH, Khater LM, Abd El-Wahed MA, El-Badrawy MF. Lipoprotein (a) and lipid profile in neonates from mothers with three different types of diabetes mellitus. Clin Biochem 2003; 36(7): 563-9.
[106]
Akcakus M, Koklu E, Baykan A, et al. Macrosomic newborns of diabetic mothers are associated with increased aortic intima-media thickness and lipid concentrations. Horm Res 2007; 67(6): 277-83.
[107]
Grissa O, Ategbo J-M, Yessoufou A, et al. Antioxidant status and circulating lipids are altered in human gestational diabetes and macrosomia. Transl Res 2007; 150(3): 164-71.
[108]
Koklu E, Akcakus M, Kurtoglu S, et al. Aortic intima-media thickness and lipid profile in macrosomic newborns. Eur J Pediatr 2007; 166(4): 333-8.
[109]
Sreckovic I, Birner-Gruenberger R, Besenboeck C, et al. Gestational diabetes mellitus modulates neonatal high-density lipoprotein composition and its functional heterogeneity. Biochim Biophys Acta 2014; 1841(11): 1619-27.
[110]
Meyer B, Calvert D, Moses R. Free fatty acids and gestational diabetes mellitus. Aust N Z J Obstet Gynaecol 1996; 36(3): 255-7.
[111]
de Arcos F, Castelo-Branco C, Casals E, Sanllehy C, Cararach V. Normal and gestational diabetic pregnancies. Lipids, lipoproteins and apolipoproteins. J Reprod Med 1998; 43(2): 144-8.
[112]
Seghieri G, Breschi MC, Anichini R, et al. Serum homocysteine levels are increased in women with gestational diabetes mellitus. Metabolism 2003; 52(6): 720-3.
[113]
Sobki SH, Al-Senaidy AM, Al-Shammari TA, Inam SS, Al-Gwiser AA, Bukhari SA. Impact of gestational diabetes on lipid profiling and indices of oxidative stress in maternal and cord plasma. Saudi Med J 2004; 25(7): 876-80.
[114]
Kinalski M, Telejko B, Kuzmicki M, Kretowski A, Kinalska I. Tumor necrosis factor alpha system and plasma adiponectin concentration in women with gestational diabetes. Horm Metab Res 2005; 37(7): 450-4.
[115]
Bartha JL, Gonzalez-Bugatto F, Fernandez-Macias R, Gonzalez-Gonzalez NL, Comino-Delgado R, Hervias-Vivancos B. Metabolic syndrome in normal and complicated pregnancies. Eur J Obstet Gynecol Reprod Biol 2008; 137(2): 178-84.
[116]
Molnar J, Garamvolgyi Z, Herold M, Adanyi N, Somogyi A, Rigo JJ. Serum selenium concentrations correlate significantly with inflammatory biomarker high-sensitive CRP levels in Hungarian gestational diabetic and healthy pregnant women at mid-pregnancy. Biol Trace Elem Res 2008; 121(1): 16-22.
[117]
Rizzo M, Berneis K, Altinova AE, et al. Atherogenic lipoprotein phenotype and LDL size and subclasses in women with gestational diabetes. Diabet Med 2008; 25(12): 1406-11.
[118]
Schaefer-Graf UM, Meitzner K, Ortega-Senovilla H, et al. Differences in the implications of maternal lipids on fetal metabolism and growth between gestational diabetes mellitus and control pregnancies. Diabet Med 2011; 28(9): 1053-9.
[119]
Näf S, Escote X, Yanez RE, et al. Zinc-alpha2-glycoprotein is unrelated to gestational diabetes: anthropometric and metabolic determinants in pregnant women and their offspring. PLoS One 2012; 7(12): e47601.
[120]
Niu J, Lei Q, Lu L, et al. Evaluation of the diagnostic criteria of gestational metabolic syndrome and analysis of the risk factors. Zhonghua Fu Chan Ke Za Zhi 2013; 48(2): 92-7.
[121]
Todoric J, Handisurya A, Leitner K, Harreiter J, Hoermann G, Kautzky-Willer A. Lipoprotein(a) is not related to markers of insulin resistance in pregnancy. Cardiovasc Diabetol 2013; 12: 138.
[122]
Wang D, Zhu W, Li J, An C, Wang Z. Serum concentrations of fibroblast growth factors 19 and 21 in women with gestational diabetes mellitus: association with insulin resistance, adiponectin, and polycystic ovary syndrome history. PLoS One 2013; 8(11): e81190.
[123]
Iimura Y, Matsuura M, Yao Z, et al. Lack of predictive power of plasma lipids or lipoproteins for gestational diabetes mellitus in Japanese women. J Diabetes Investig 2015; 6(6): 640-6.
[124]
Sanchez-Vera I, Bonet B, Viana M, et al. Changes in plasma lipids and increased low-density lipoprotein susceptibility to oxidation in pregnancies complicated by gestational diabetes: consequences of obesity. Metabolism 2007; 56(11): 1527-33.
[125]
Li G, Kong L, Zhang L, et al. Early pregnancy maternal lipid profiles and the risk of gestational diabetes mellitus stratified for body mass index. Reprod Sci 2015; 22(6): 712-7.
[126]
Tarim E, Bagis T, Kilicdag E, et al. Elevated plasma homocysteine levels in gestational diabetes mellitus. Acta Obstet Gynecol Scand 2004; 83(6): 543-7.
[127]
Di Cianni G, Miccoli R, Volpe L, et al. Maternal triglyceride levels and newborn weight in pregnant women with normal glucose tolerance. Diabet Med 2005; 22(1): 21-5.
[128]
Di Cianni G, Seghieri G, Lencioni C, et al. Normal glucose tolerance and gestational diabetes mellitus: what is in between? Diabetes Care 2007; 30(7): 1783-8.
[129]
Davari-Tanha F, Khan-Mohamadi F, Kaveh M, Shariat M. Homocysteine in gestational diabetes and normal pregnancy plus effects of folic acid. Ijph 2008; 37(3): 118-26.
[130]
Bojadzhieva M, Atanassova I, Dimitrova V, et al. Screening for gestational diabetes in Bulgaria--preliminary results. Akush Ginekol (Sofiia) 2010; 49(3): 3-9.
[131]
Savvidou M, Nelson SM, Makgoba M, Messow C-M, Sattar N, Nicolaides K. First-trimester prediction of gestational diabetes mellitus: examining the potential of combining maternal characteristics and laboratory measures. Diabetes 2010; 59(12): 3017-22.
[132]
Alanbay I, Coksuer H, Ercan M, et al. Can serum gamma-glutamyltransferase levels be useful at diagnosing gestational diabetes mellitus? Gynecol Endocrinol 2012; 28(3): 208-11.
[133]
Zhou J, Zhao X, Wang Z, Hu Y. Combination of lipids and uric acid in mid-second trimester can be used to predict adverse pregnancy outcomes. J Matern Fetal Neonatal Med 2012; 25(12): 2633-8.
[134]
Wei J, Gao J, Cheng J. Gestational diabetes mellitus and impaired glucose tolerance pregnant women. Pak J Med Sci 2014; 30(6): 1203-8.
[135]
Ghafoor S, Shaikh AW. Shaheena. Maternal lipids in pregnancies with gestational diabetes mellitus. PJMHS 2012; 6(1): 81-4.
[136]
Atay AE, Simsek H, Demir B, et al. Noninvasive assessment of subclinical atherosclerosis in normotensive gravidae with gestational diabetes. Herz 2014; 39(5): 627-32.
[137]
Hollingsworth DR, Grundy SM. Pregnancy-associated hypertriglyceridemia in normal and diabetic women. Differences in insulin-dependent, non-insulin-dependent, and gestational diabetes. Diabetes 1982; 31(12): 1092-7.
[138]
Koukkou E, Watts GF, Lowy C. Serum lipid, lipoprotein and apolipoprotein changes in gestational diabetes mellitus: A cross-sectional and prospective study. J Clin Pathol 1996; 49(8): 634-7.
[139]
Vijayalaxmi KG, Urooj A. Biochemical profile and outcome in normal and high risk subjects. Indian J Clin Biochem 2009; 24(3): 269-74.
[140]
Giannubilo SR, Tiano L, Cecchi S, Principi F, Tranquilli AL, Littarru GP. Plasma coenzyme Q10 is increased during gestational diabetes. Diabetes Res Clin Pract 2011; 94(2): 230-5.
[141]
dos Santos-Weiss ICR, Rea RR, Fadel-Picheth CMT, et al. The plasma logarithm of the triglyceride/HDL-cholesterol ratio is a predictor of low risk gestational diabetes in early pregnancy. Clin Chim Acta 2013; 418: 1-4.
[142]
Knopp RH, Magee MS, Walden CE, Bonet B, Benedetti TJ. Prediction of infant birth weight by GDM screening tests. Importance of plasma triglyceride. Diabetes Care 1992; 15(11): 1605-13.
[143]
Ersanli ZO, Damci T, Sen C, et al. Lipid metabolism alterations in patients with gestational diabetes mellitus associated fetal macrosomia. Ann Ist Super Sanita 1997; 33(3): 411-5.
[144]
Schaefer-Graf UM, Graf K, Kulbacka I, et al. Maternal lipids as strong determinants of fetal environment and growth in pregnancies with gestational diabetes mellitus. Diabetes Care 2008; 31(9): 1858-63.
[145]
Son GH, Kwon JY, Kim YH, Park YW. Maternal serum triglycerides as predictive factors for large-for-gestational age newborns in women with gestational diabetes mellitus. Acta Obstet Gynecol Scand 2010; 89(5): 700-4.
[146]
Olmos P, Martelo G, Reimer V, et al. Nutrients other than glucose might explain fetal overgrowth in gestational diabetic pregnancies. Rev Med Chil 2013; 141(11): 1441-8.
[147]
Olmos PR, Rigotti A, Busso D, et al. Maternal hypertriglyceridemia: A link between maternal overweight-obesity and macrosomia in gestational diabetes. Obesity (Silver Spring) 2014; 22(10): 2156-63.
[148]
Krstevska B, Jovanovska SM, Krstevska SS, Nakova VV, Serafimoski V. Maternal lipids may predict fetal growth in type 2 diabetes mellitus and gestational diabetes mellitus pregnancies. Prilozi (Makedon Akad Nauk Umet Odd Med Nauki) 2016; 37(2-3): 99-105.
[149]
Kitajima M, Oka S, Yasuhi I, Fukuda M, Rii Y, Ishimaru T. Maternal serum triglyceride at 24-32 weeks’ gestation and newborn weight in nondiabetic women with positive diabetic screens. Obstet Gynecol 2001; 97(5 Pt 1): 776-80.
[150]
Kushtagi P, Arvapally S. Maternal mid-pregnancy serum triglyceride levels and neonatal birth weight. Int J Gynaecol Obstet 2009; 106(3): 258-9.
[151]
Thomas B, Ghebremeskel K, Lowy C, et al. Plasma fatty acids of neonates born to mothers with and without gestational diabetes. Prostaglandins Leukot Essent Fatty Acids 2005; 72: 335-41.
[152]
Kralisch S, Bluher M, Paschke R, Stumvoll M, Fasshauer M. Adipokines and adipocyte targets in the future management of obesity and the metabolic syndrome. Mini Rev Med Chem 2007; 7(1): 39-45.
[153]
Siddiqui K, George TP. Resistin role in development of gestational diabetes mellitus. Biomarkers Med 2017; 11(7): 579-86.
[154]
Friedman JM. A tale of two hormones. Nat Med 2010; 16(10): 1100-6.
[155]
Steppan C, Lazar M. The current biology of resistin. J Intern Med 2004; 255: 439-47.
[156]
Vitoratos N, Deliveliotou A, Dimitrakaki A, et al. Maternal serum resistin concentrations in gestational diabetes mellitus and normal pregnancies. J Obstet Gynaecol Res 2011; 37: 112-8.
[157]
Vitoratos N, Deliveliotou A, Vlahos NF, et al. Serum adiponectin during pregnancy and postpartum in women with gestational diabetes and normal controls. Gynecol Endocrinol 2008; 24: 614-9.
[158]
Abell SK, De Courten B, Boyle JA, Teede HJ. Inflammatory and other biomarkers: Role in pathophysiology and prediction of gestational diabetes mellitus. Int J Mol Sci 2015; 16(6): 13442-73.
[159]
Ajala O, Jensen LA, Ryan E, Chik C. Women with a history of gestational diabetes on long-term follow up have normal vascular function despite more dysglycemia, dyslipidemia and adiposity. Diabetes Res Clin Pract 2015; 110(3): 309-14.
[160]
Leiva A, Guzmán-Gutiérrez E, Contreras-Duarte S, et al. Adenosine receptors: Modulators of lipid availability that are controlled by lipid levels. Mol Aspects Med 2017; 55: 26-44.
[161]
Qiu C, Rudra C, Austin MA, Williams MA. Association of gestational diabetes mellitus and low-density lipoprotein (LDL) particle size. Physiol Res 2007; 56(5): 571-8.
[162]
Tall AR. An overview of reverse cholesterol transport. Eur Heart J 1998; 19(Suppl. A): 31-5.
[163]
Ruiz M, Frej C, Holmer A, Guo LJ, Tran S, Dahlback B. High-density lipoprotein-associated apolipoprotein M limits endothelial inflammation by delivering sphingosine-1-phosphate to the sphingosine-1-phosphate receptor 1. Arterioscler Thromb Vasc Biol 2017; 37(1): 118-29.
[164]
Taskinen MR, Boren J. New insights into the pathophysiology of dyslipidemia in type 2 diabetes. Atherosclerosis 2015; 239(2): 483-95.
[165]
Nagasaka H, Chiba H, Kikuta H, et al. Unique character and metabolism of high density lipoprotein (HDL) in fetus. Atherosclerosis 2002; 161(1): 215-23.
[166]
Carlson SE. Plasma cholesterol and lipoprotein levels during fetal development and infancy. Ann N Y Acad Sci 1991; 623: 81-9.
[167]
Gugliucci A, Numaguchi M, Caccavello R, Kimura S. Paraoxonase 1 lactonase activity and distribution in the HDL subclasses in the cord blood. Redox Rep 2014; 19(3): 124-32.
[168]
Kontush A, Chapman MJ. Antiatherogenic small, dense HDL--guardian angel of the arterial wall? Nat Clin Pract Cardiovasc Med 2006; 3(3): 144-53.
[169]
McConathy WJ, Lane DM. Studies on the apolipoproteins and lipoproteins of cord serum. Pediatr Res 1980; 14(5): 757-61.
[170]
Dolphin PJ, Breckenridge WC, Dolphin MA, Tan MH. The lipoproteins of human umbilical cord blood apolipoprotein and lipid levels. Atherosclerosis 1984; 51(1): 109-22.
[171]
Averna MR, Barbagallo CM, Di Paola G, et al. Lipids, lipoproteins and apolipoproteins AI, AII, B, CII, CIII and E in newborns. Biol Neonate 1991; 60(3-4): 187-92.
[172]
Duvillard L, Pont F, Florentin E, Galland-Jos C, Gambert P, Verges B. Metabolic abnormalities of apolipoprotein B-containing lipoproteins in non-insulin-dependent diabetes: A stable isotope kinetic study. Eur J Clin Invest 2000; 30(8): 685-94.
[173]
Arca M, Pigna G, Favoccia C. Mechanisms of diabetic dyslipidemia: Relevance for atherogenesis. Curr Vasc Pharmacol 2012; 10(6): 684-6.
[174]
Wu L, Parhofer KG. Diabetic dyslipidemia. Metabolism 2014; 63(12): 1469-79.
[175]
Mikhailidis DP, Elisaf M, Rizzo M, et al. European panel on low density lipoprotein (LDL) subclasses: A statement on the pathophysiology, atherogenicity and clinical significance of LDL subclasses: executive summary. Curr Vasc Pharmacol 2011; 9(5): 531-2.
[176]
Mikhailidis DP, Elisaf M, Rizzo M, et al. European panel on low density lipoprotein (LDL) subclasses: A statement on the pathophysiology, atherogenicity and clinical significance of LDL subclasses. Curr Vasc Pharmacol 2011; 9(5): 533-71.
[177]
Nolan CJ, Riley SF, Sheedy MT, Walstab JE, Beischer NA. Maternal serum triglyceride, glucose tolerance, and neonatal birth weight ratio in pregnancy. Diabetes Care 1995; 18(12): 1550-6.
[178]
Li Q, Wu X, Yang S, Xie M, Shi L. Association of dietary habits with gestational diabetes mellitus among Cantonese women. Nan Fang Yi Ke Da Xue Xue Bao 2015; 35(5): 772-6.
[179]
Skryten A, Johnson P, Samsioe G, Gustafson A. Studies in diabetic pregnancy. I. Serum lipids. Acta Obstet Gynecol Scand 1976; 55(3): 211-5.
[180]
Bao W, Dar S, Zhu Y, et al. Plasma concentrations of lipids during pregnancy and the risk of gestational diabetes mellitus: A longitudinal study. J Diabetes 2018; 10(6): 487-95.
[181]
Wang C, Zhu W, Wei Y, et al. The predictive effects of early pregnancy lipid profiles and fasting glucose on the risk of gestational diabetes mellitus stratified by body mass index. J Diabetes Res 2016; 2016: 3013567.
[182]
Paradisi G, Ianniello F, Tomei C, et al. Longitudinal changes of adiponectin, carbohydrate and lipid metabolism in pregnant women at high risk for gestational diabetes. Gynecol Endocrinol 2010; 26(7): 539-45.
[183]
Shelley-Jones DC, Wein P, Nolan C, Beischer NA. Why do Asian-born women have a higher incidence of gestational diabetes? An analysis of racial differences in body habitus, lipid metabolism and the serum insulin response to an oral glucose load. Aust N Z J Obstet Gynaecol 1993; 33(2): 114-8.
[184]
Tsai P-J, Yu C-H, Hsu S-P, et al. Maternal plasma adiponectin concentrations at 24 to 31 weeks of gestation: negative association with gestational diabetes mellitus. Nutrition 2005; 21(11-12): 1095-9.
[185]
Wang D, Xu S, Chen H, Zhong L, Wang Z. The associations between triglyceride to high-density lipoprotein cholesterol ratios and the risks of gestational diabetes mellitus and large-for-gestational-age infant. Clin Endocrinol (Oxf) 2015; 83(4): 490-7.
[186]
Couch SC, Philipson EH, Bendel RB, Pujda LM, Milvae RA, Lammi-Keefe CJ. Elevated lipoprotein lipids and gestational hormones in women with diet-treated gestational diabetes mellitus compared to healthy pregnant controls. J Diabetes Complications 1998; 12(1): 1-9.
[187]
Maple-Brown L, Ye C, Hanley AJ, et al. Maternal pregravid weight is the primary determinant of serum leptin and its metabolic associations in pregnancy, irrespective of gestational glucose tolerance status. J Clin Endocrinol Metab 2012; 97(11): 4148-55.
[188]
Whyte K, Kelly H, O’Dwyer V, Gibbs M, O’Higgins A, Turner MJ. Offspring birth weight and maternal fasting lipids in women screened for gestational diabetes mellitus (GDM). Eur J Obstet Gynecol Reprod Biol 2013; 170(1): 67-70.
[189]
McGrowder D, Grant K, Irving R, et al. Lipid profile and clinical characteristics of women with gestational diabetes mellitus and preeclampsia. J Med Biochem 2009; 28(2): 72-81.
[190]
Liu B, Geng H, Yang J, et al. Early pregnancy fasting plasma glucose and lipid concentrations in pregnancy and association to offspring size: A retrospective cohort study. BMC Pregnancy Childbirth 2016; 16: 56.
[191]
Liu B, Deng S, Xu Y, Yang J, Geng H, Wang Z. Association between maternal and umbilical cord serum dipeptidyl peptidase IV in pregnant women with and without gestational diabetes mellitus. J Obstet Gynaecol Res 2016; 42(5): 505-10. b
[192]
Warth MR, Knopp RH. Lipid metabolism in pregnancy. Interactions of diabetes, body weight, age, and high carbohydrate diet. Diabetes 1977; 26(11): 1056-62.
[193]
Cowett RM, Carr SR, Ogburn PLJ. Lipid tolerance testing in pregnancy. Diabetes Care 1993; 16(1): 51-6.
[194]
He B, Li S, Wang W, Han P. Maternal serum lipid at 36-42 weeks’ gestation and their relationship to newborn weight in pregnant women with gestational diabetes mellitus and type 1 and type 2 diabetes mellitus. Zhonghua Fu Chan Ke Za Zhi 2004; 39(10): 675-7.
[195]
Kale SD, Kulkarni SR, Lubree HG, et al. Characteristics of gestational diabetic mothers and their babies in an Indian diabetes clinic. J Assoc Physicians India 2005; 53: 857-63.

Rights & Permissions Print Cite
Article Metrics
60
6
1
© 2024 Bentham Science Publishers | Privacy Policy