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Published in: Acta Diabetologica 4/2019

01-04-2019 | Obesity | Original Article

Impact of maternal BMI and gestational diabetes mellitus on maternal and cord blood metabolome: results from the PREOBE cohort study

Authors: Engy Shokry, Linda Marchioro, Olaf Uhl, Mercedes G. Bermúdez, Jose Antonio García-Santos, Mª Teresa Segura, Cristina Campoy, Berthold Koletzko

Published in: Acta Diabetologica | Issue 4/2019

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Abstract

Aims

Maternal obesity and gestational diabetes mellitus (GDM) were frequently reported to be risk factors for obesity and diabetes in offspring. Our goal was to study the impact of maternal prepregnancy BMI (pBMI) and GDM on both maternal and cord blood metabolic profiles.

Methods

We used LC–MS/MS to measure 201 metabolites comprising phospholipids (PL), amino acids, non-esterified fatty acids (NEFA), organic acids, acyl carnitines (AC), and Krebs cycle metabolites in maternal plasma at delivery and cord plasma obtained from 325 PREOBE study participants.

Results

Several metabolites were associated with pBMI/GDM in both maternal and cord blood (p < 0.05), while others were specific to either blood sources. BMI was positively associated with leucine, isoleucine, and inflammation markers in both mother and offspring, while β-hydroxybutyric acid was positively associated only in cord blood. GDM showed elevated levels of sum of hexoses, a characteristic finding in both maternal and cord blood. Uniquely in cord blood of offspring born to GDM mothers, free carnitine was significantly lower with the same tendency observed for AC, long-chain NEFA, PL, specific Krebs cycle metabolites, and β-oxidation markers.

Conclusions

Maternal BMI and GDM are associated with maternal and cord blood metabolites supporting the hypothesis of transgenerational cycle of obesity and diabetes.
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Literature
1.
go back to reference NCD Risk Factor Collaboration (2017) Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet 390(10113):2627–2642CrossRef NCD Risk Factor Collaboration (2017) Worldwide trends in body-mass index, underweight, overweight, and obesity from 1975 to 2016: a pooled analysis of 2416 population-based measurement studies in 128·9 million children, adolescents, and adults. Lancet 390(10113):2627–2642CrossRef
2.
go back to reference Huvinen E, Eriksson JG, Stach-Lempinen B, Tiitinen A, Koivusalo SB (2018) Heterogeneity of gestational diabetes (GDM) and challenges in developing a GDM risk score. Acta Diabetol 55(12):1251–1259CrossRefPubMed Huvinen E, Eriksson JG, Stach-Lempinen B, Tiitinen A, Koivusalo SB (2018) Heterogeneity of gestational diabetes (GDM) and challenges in developing a GDM risk score. Acta Diabetol 55(12):1251–1259CrossRefPubMed
3.
go back to reference Huvinen E, Eriksson JG, Koivusalo SB, Grotenfelt N, Tiitinen A, Stach-Lempinen B (2018) Heterogeneity of gestational diabetes (GDM) and long-term risk of diabetes and metabolic syndrome: findings from the RADIEL study follow-up. Acta Diabetol 55(12):1251–1259CrossRefPubMed Huvinen E, Eriksson JG, Koivusalo SB, Grotenfelt N, Tiitinen A, Stach-Lempinen B (2018) Heterogeneity of gestational diabetes (GDM) and long-term risk of diabetes and metabolic syndrome: findings from the RADIEL study follow-up. Acta Diabetol 55(12):1251–1259CrossRefPubMed
4.
go back to reference Lowe WL Jr, Bain JR, Nodzenski M (2017) Maternal BMI and glycemia impact the fetal metabolome. Diabet Care 40:902–910CrossRef Lowe WL Jr, Bain JR, Nodzenski M (2017) Maternal BMI and glycemia impact the fetal metabolome. Diabet Care 40:902–910CrossRef
5.
go back to reference Kaaja R, Rönnemaa T (2008) Gestational diabetes: pathogenesis and consequences to mother and offspring. Rev Diab Stud 5(4):194–202CrossRef Kaaja R, Rönnemaa T (2008) Gestational diabetes: pathogenesis and consequences to mother and offspring. Rev Diab Stud 5(4):194–202CrossRef
6.
go back to reference Pintaudi B, Fresa R, Dalfrà M, Dodesini AR, Vitacolonna E, Tumminia A, Sciacca L, Lencioni C, Marcone T, Lucisano G, Nicolucci A, Bonomo M, Napoli A, STRONG Study Collaborators (2018) The risk stratification of adverse neonatal outcomes in women with gestational diabetes (STRONG) study. Acta Diabetol 55(12):1261–1273CrossRefPubMed Pintaudi B, Fresa R, Dalfrà M, Dodesini AR, Vitacolonna E, Tumminia A, Sciacca L, Lencioni C, Marcone T, Lucisano G, Nicolucci A, Bonomo M, Napoli A, STRONG Study Collaborators (2018) The risk stratification of adverse neonatal outcomes in women with gestational diabetes (STRONG) study. Acta Diabetol 55(12):1261–1273CrossRefPubMed
7.
go back to reference Leybovitz-Haleluya N, Wainstock T, Landau D, Sheiner E (2018) Maternal gestational diabetes mellitus and the risk of subsequent pediatric cardiovascular diseases of the offspring: a population-based cohort study with up to 18 years of follow up. Acta Diabetol 55(10):1037–1042CrossRefPubMed Leybovitz-Haleluya N, Wainstock T, Landau D, Sheiner E (2018) Maternal gestational diabetes mellitus and the risk of subsequent pediatric cardiovascular diseases of the offspring: a population-based cohort study with up to 18 years of follow up. Acta Diabetol 55(10):1037–1042CrossRefPubMed
8.
go back to reference Berglund SK, García-Valdés L, Torres-Espinola FJ, Segura MT, Martínez-Zaldívar C, Aguilar MJ, Agil A, Lorente JA, Florido J, Padilla C, Altmäe S, Marcos A, López-Sabater MC, Campoy C, PREOBE Team (2016) Maternal, fetal and perinatal alterations associated with obesity, overweight and gestational diabetes: an observational cohort study (PREOBE). BMC Public Health 16:207CrossRefPubMedPubMedCentral Berglund SK, García-Valdés L, Torres-Espinola FJ, Segura MT, Martínez-Zaldívar C, Aguilar MJ, Agil A, Lorente JA, Florido J, Padilla C, Altmäe S, Marcos A, López-Sabater MC, Campoy C, PREOBE Team (2016) Maternal, fetal and perinatal alterations associated with obesity, overweight and gestational diabetes: an observational cohort study (PREOBE). BMC Public Health 16:207CrossRefPubMedPubMedCentral
9.
go back to reference International Association of Diabetes and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, Damm P, Dyer AR, Leiva A, Hod M, Kitzmiler JL, Lowe LP, McIntyre HD, Oats JJ, Omori Y, Schmidt MI (2010) International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 33(3): 676–682CrossRefPubMedCentral International Association of Diabetes and Pregnancy Study Groups Consensus Panel, Metzger BE, Gabbe SG, Persson B, Buchanan TA, Catalano PA, Damm P, Dyer AR, Leiva A, Hod M, Kitzmiler JL, Lowe LP, McIntyre HD, Oats JJ, Omori Y, Schmidt MI (2010) International association of diabetes and pregnancy study groups recommendations on the diagnosis and classification of hyperglycemia in pregnancy. Diabetes Care 33(3): 676–682CrossRefPubMedCentral
10.
go back to reference Hellmuth C, Weber M, Koletzko B, Peissner W (2012) Nonesterified fatty acid determination for functional lipidomics. Comprehensive ultrahigh performance liquid chromatography–tandem mass spectrometry quantitation, qualification, and parameter prediction. Anal Chem 84:1483–1490CrossRefPubMed Hellmuth C, Weber M, Koletzko B, Peissner W (2012) Nonesterified fatty acid determination for functional lipidomics. Comprehensive ultrahigh performance liquid chromatography–tandem mass spectrometry quantitation, qualification, and parameter prediction. Anal Chem 84:1483–1490CrossRefPubMed
11.
go back to reference Rauschert S, Uhl O, Koletzko B, Kirchberg F, Mori TA, Huang RC, Beilin LJ, Hellmuth C, Oddy WH (2016) Lipidomics reveals associations of phospholipids with obesity and insulin resistance in young adults. J Clin Endocrinol Metab 101:871–879CrossRefPubMed Rauschert S, Uhl O, Koletzko B, Kirchberg F, Mori TA, Huang RC, Beilin LJ, Hellmuth C, Oddy WH (2016) Lipidomics reveals associations of phospholipids with obesity and insulin resistance in young adults. J Clin Endocrinol Metab 101:871–879CrossRefPubMed
12.
go back to reference Harder U, Koletzko B, Peissner W (2011) Quantification of 22 plasma amino acids combining derivatization and ion-pair LC–MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 879:495–504CrossRefPubMed Harder U, Koletzko B, Peissner W (2011) Quantification of 22 plasma amino acids combining derivatization and ion-pair LC–MS/MS. J Chromatogr B Analyt Technol Biomed Life Sci 879:495–504CrossRefPubMed
13.
go back to reference Maeba R, Hara H (2012) Serum choline plasmalogen is a reliable biomarker for atherogenic status. In: Squeri A (ed) Coronary artery disease—new insights and novel approaches. InTech, Rijeka, pp 243–260 Maeba R, Hara H (2012) Serum choline plasmalogen is a reliable biomarker for atherogenic status. In: Squeri A (ed) Coronary artery disease—new insights and novel approaches. InTech, Rijeka, pp 243–260
14.
go back to reference Zhang W, Sun G, Aitken D, Likhodii S, Liu M, Martin G, Furey A, Randell E, Rahman P, Jones G, Zhai G (2016) Lysophosphatidylcholines to phosphatidylcholines ratio predicts advanced knee osteoarthritis. Rheumatol 55(9):1566–1574CrossRef Zhang W, Sun G, Aitken D, Likhodii S, Liu M, Martin G, Furey A, Randell E, Rahman P, Jones G, Zhai G (2016) Lysophosphatidylcholines to phosphatidylcholines ratio predicts advanced knee osteoarthritis. Rheumatol 55(9):1566–1574CrossRef
15.
go back to reference Pickens CA, Vazquez AI, Daniel Jones A, Fenton JI (2017) Obesity, adipokines, and C-peptide are associated with distinct plasma and phospholipid profiles in adult males, an untargeted lipidomic approach. Sci Rep 7:6335CrossRefPubMedPubMedCentral Pickens CA, Vazquez AI, Daniel Jones A, Fenton JI (2017) Obesity, adipokines, and C-peptide are associated with distinct plasma and phospholipid profiles in adult males, an untargeted lipidomic approach. Sci Rep 7:6335CrossRefPubMedPubMedCentral
16.
go back to reference Kirchberg FF, Brandt S, Moß A, Peissner W, Koenig W, Rothenbacher D, Brenner H, Koletzko B, Hellmuth C, Wabitsch M (2017) Metabolomics reveals an entanglement of fasting leptin concentrations with fatty acid oxidation and gluconeogenesis in healthy children. PLoS One 12(8):e0183185CrossRefPubMedPubMedCentral Kirchberg FF, Brandt S, Moß A, Peissner W, Koenig W, Rothenbacher D, Brenner H, Koletzko B, Hellmuth C, Wabitsch M (2017) Metabolomics reveals an entanglement of fasting leptin concentrations with fatty acid oxidation and gluconeogenesis in healthy children. PLoS One 12(8):e0183185CrossRefPubMedPubMedCentral
17.
go back to reference Sampath H, Ntambi JM (2008) Role of stearoyl-CoA desaturase in human metabolic disease. Future Lipidol 3:163–173CrossRef Sampath H, Ntambi JM (2008) Role of stearoyl-CoA desaturase in human metabolic disease. Future Lipidol 3:163–173CrossRef
18.
go back to reference Myatt L, Powell T, Brown L et al (2010) Part I. nutritional regulation and requirements for pregnancy and fetal growth. In: Symonds ME, Ramsay M (eds) Maternal–fetal nutrition during pregnancy and lactation. Cambridge University Press, Cambridge, p 16 Myatt L, Powell T, Brown L et al (2010) Part I. nutritional regulation and requirements for pregnancy and fetal growth. In: Symonds ME, Ramsay M (eds) Maternal–fetal nutrition during pregnancy and lactation. Cambridge University Press, Cambridge, p 16
19.
go back to reference Butte NF, Liu Y, Zakeri IF, Mohney RP, Mehta N, Voruganti VS, Göring H, Cole SA, Comuzzie AG (2015) Global metabolomic profiling targeting childhood obesity in the Hispanic population. Am J Clin Nutr 102(2):256–267CrossRefPubMedPubMedCentral Butte NF, Liu Y, Zakeri IF, Mohney RP, Mehta N, Voruganti VS, Göring H, Cole SA, Comuzzie AG (2015) Global metabolomic profiling targeting childhood obesity in the Hispanic population. Am J Clin Nutr 102(2):256–267CrossRefPubMedPubMedCentral
21.
go back to reference Sandler V, Reisetter AC, Bain JR, Muehlbauer MJ, Nodzenski M, Stevens RD, Ilkayeva O, Lowe LP, Metzger BE, Newgard CB, Scholtens DM, Lowe WL Jr, HAPO Study Cooperative Research Group (2017) Association of maternal BMI and insulin resistance with the maternal metabolome and newborn outcomes. Diabetologia 60:518–530CrossRefPubMed Sandler V, Reisetter AC, Bain JR, Muehlbauer MJ, Nodzenski M, Stevens RD, Ilkayeva O, Lowe LP, Metzger BE, Newgard CB, Scholtens DM, Lowe WL Jr, HAPO Study Cooperative Research Group (2017) Association of maternal BMI and insulin resistance with the maternal metabolome and newborn outcomes. Diabetologia 60:518–530CrossRefPubMed
22.
go back to reference Jansson N, Rosario FJ, Gaccioli F, Lager S, Jones HN, Roos S, Jansson T, Powell TL (2013) Activation of placental mtor signaling and amino acid transporters in obese women giving birth to large babies. J Clin Endocrinol Metab 98:105–113CrossRefPubMed Jansson N, Rosario FJ, Gaccioli F, Lager S, Jones HN, Roos S, Jansson T, Powell TL (2013) Activation of placental mtor signaling and amino acid transporters in obese women giving birth to large babies. J Clin Endocrinol Metab 98:105–113CrossRefPubMed
23.
go back to reference Lindsay KL, Hellmuth C, Uhl O, Buss C, Wadhwa PD, Koletzko B, Entringer S (2015) Longitudinal metabolomic profiling of amino acids and lipids across healthy pregnancy. PLoS One 10:e0145794CrossRefPubMedPubMedCentral Lindsay KL, Hellmuth C, Uhl O, Buss C, Wadhwa PD, Koletzko B, Entringer S (2015) Longitudinal metabolomic profiling of amino acids and lipids across healthy pregnancy. PLoS One 10:e0145794CrossRefPubMedPubMedCentral
24.
go back to reference Marseglia L, Manti S, D’Angelo G, Nicotera A, Parisi E, Di Rosa G, Gitto E, Arrigo T (2015) Oxidative stress in obesity: a critical component in human diseases. Int J Mol Sci 16:378–400CrossRef Marseglia L, Manti S, D’Angelo G, Nicotera A, Parisi E, Di Rosa G, Gitto E, Arrigo T (2015) Oxidative stress in obesity: a critical component in human diseases. Int J Mol Sci 16:378–400CrossRef
25.
go back to reference Zeitoun-Ghandour S, Leszczyszyn OI, Blindauer CA, Geier FM, Bundy JG, Stürzenbaum SR (2011) C. elegans metallothioneins: response to and defence against ROS toxicity. Mol Biosyst 7(8):2397–2406CrossRefPubMed Zeitoun-Ghandour S, Leszczyszyn OI, Blindauer CA, Geier FM, Bundy JG, Stürzenbaum SR (2011) C. elegans metallothioneins: response to and defence against ROS toxicity. Mol Biosyst 7(8):2397–2406CrossRefPubMed
26.
go back to reference Gao X, Zhang W, Yongbo W, Pedram P, Cahill F, Zhai G, Randell EW, Gulliver WP, Sun G (2016) Serum metabolic biomarkers distinguish metabolically healthy peripherally obese from unhealthy centrally obese individuals. Nutr Metab 13:33CrossRef Gao X, Zhang W, Yongbo W, Pedram P, Cahill F, Zhai G, Randell EW, Gulliver WP, Sun G (2016) Serum metabolic biomarkers distinguish metabolically healthy peripherally obese from unhealthy centrally obese individuals. Nutr Metab 13:33CrossRef
27.
go back to reference Kim JY, Park JY, Kim OY, Ham BM, Kim HJ, Kwon DY, Jang Y, Lee JH (2010) Metabolic profiling of plasma in overweight/obese and lean men using ultra performance liquid chromatography and Q-TOF mass spectrometry (UPLC-Q-TOF MS). J Proteome Res 9:4368–4375CrossRefPubMed Kim JY, Park JY, Kim OY, Ham BM, Kim HJ, Kwon DY, Jang Y, Lee JH (2010) Metabolic profiling of plasma in overweight/obese and lean men using ultra performance liquid chromatography and Q-TOF mass spectrometry (UPLC-Q-TOF MS). J Proteome Res 9:4368–4375CrossRefPubMed
28.
go back to reference Dudzik D, Zorawski M, Skotnicki M, Zarzycki W, Kozlowska G, Bibik-Malinowska K, Vallejo M, García A, Barbas C, Ramos MP (2014) Metabolic fingerprint of gestational diabetes mellitus. J Proteom 103:57–71CrossRef Dudzik D, Zorawski M, Skotnicki M, Zarzycki W, Kozlowska G, Bibik-Malinowska K, Vallejo M, García A, Barbas C, Ramos MP (2014) Metabolic fingerprint of gestational diabetes mellitus. J Proteom 103:57–71CrossRef
29.
go back to reference Curcic S, Holzer M, Pasterk L, Knuplez E, Eichmann TO, Frank S, Zimmermann R, Schicho R, Heinemann A, Marsche G (2017) Secretory phospholipase A2 modifed HDL rapidly and potently suppresses platelet activation. Sci Rep 7:8030CrossRefPubMedPubMedCentral Curcic S, Holzer M, Pasterk L, Knuplez E, Eichmann TO, Frank S, Zimmermann R, Schicho R, Heinemann A, Marsche G (2017) Secretory phospholipase A2 modifed HDL rapidly and potently suppresses platelet activation. Sci Rep 7:8030CrossRefPubMedPubMedCentral
30.
go back to reference Hellmuth C, Lindsay KL, Uhl O (2017) Association of maternal prepregnancy BMI with metabolomic profile across gestation. Int J Obes (Lond) 41(1):159–169CrossRef Hellmuth C, Lindsay KL, Uhl O (2017) Association of maternal prepregnancy BMI with metabolomic profile across gestation. Int J Obes (Lond) 41(1):159–169CrossRef
31.
go back to reference Herrera E (2002) Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocrine 19(1):43–55CrossRefPubMed Herrera E (2002) Lipid metabolism in pregnancy and its consequences in the fetus and newborn. Endocrine 19(1):43–55CrossRefPubMed
32.
go back to reference Scholtens DM, Muehlbauer MJ, Daya NR, Stevens RD, Dyer AR, Lowe LP, Metzger BE, Newgard CB, Bain JR, Lowe WL Jr, HAPO Study Cooperative Research Group (2014) Metabolomics reveals broad-scale metabolic perturbations in hyperglycemic mothers during pregnancy. Diabetes Care 37(1):158–166CrossRefPubMed Scholtens DM, Muehlbauer MJ, Daya NR, Stevens RD, Dyer AR, Lowe LP, Metzger BE, Newgard CB, Bain JR, Lowe WL Jr, HAPO Study Cooperative Research Group (2014) Metabolomics reveals broad-scale metabolic perturbations in hyperglycemic mothers during pregnancy. Diabetes Care 37(1):158–166CrossRefPubMed
33.
34.
go back to reference Gaither K, Quraishi AN, Illsley NP (1999) Diabetes alters the expression and activity of the human placental GLUT1 glucose transporter. J Clin Endocrinol Metab 84:695–701PubMed Gaither K, Quraishi AN, Illsley NP (1999) Diabetes alters the expression and activity of the human placental GLUT1 glucose transporter. J Clin Endocrinol Metab 84:695–701PubMed
35.
go back to reference Obeid R, Herrmann W (2009) Homocysteine and lipids: S-adenosyl methionine as a key intermediate. FEBS Lett 583:1215–1225CrossRefPubMed Obeid R, Herrmann W (2009) Homocysteine and lipids: S-adenosyl methionine as a key intermediate. FEBS Lett 583:1215–1225CrossRefPubMed
36.
go back to reference Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, Mason A, Vance DE (2006) The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab 3(5):321–331CrossRefPubMed Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, Mason A, Vance DE (2006) The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab 3(5):321–331CrossRefPubMed
37.
go back to reference Braverman NE, Moser AB (2012) Review Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 1822(9):1442–1452CrossRefPubMed Braverman NE, Moser AB (2012) Review Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta 1822(9):1442–1452CrossRefPubMed
38.
go back to reference Allalou A, Nalla A, Prentice KJ (2016) A predictive metabolic signature for the transition from gestational diabetes mellitus to type 2 diabetes. Diabetes 65:2529–2539CrossRefPubMedPubMedCentral Allalou A, Nalla A, Prentice KJ (2016) A predictive metabolic signature for the transition from gestational diabetes mellitus to type 2 diabetes. Diabetes 65:2529–2539CrossRefPubMedPubMedCentral
39.
go back to reference Evangeliou A, Gourgiotis D, Kragianni C, Markouri M, Anogianaki N, Mamoulakis D, Maropoulos G, Tsakalidis C, Frentzayias A, Nicolaidou P (2010) Carnitine status and lactate increase in patients with type I juvenile diabetes. Minerva Pediatr 62(6):551–557PubMed Evangeliou A, Gourgiotis D, Kragianni C, Markouri M, Anogianaki N, Mamoulakis D, Maropoulos G, Tsakalidis C, Frentzayias A, Nicolaidou P (2010) Carnitine status and lactate increase in patients with type I juvenile diabetes. Minerva Pediatr 62(6):551–557PubMed
40.
go back to reference Pappa KI, Anagnou NP, Salamalekis E, Bikouvarakis S, Maropoulos G, Anogianaki N, Evangeliou A, Koumantakis E (2005) Gestational diabetes exhibits lack of carnitine deficiency despite relatively low carnitine levels and alterations in ketogenesis. J Matern Fetal Neonatal Med 17:63–68CrossRefPubMed Pappa KI, Anagnou NP, Salamalekis E, Bikouvarakis S, Maropoulos G, Anogianaki N, Evangeliou A, Koumantakis E (2005) Gestational diabetes exhibits lack of carnitine deficiency despite relatively low carnitine levels and alterations in ketogenesis. J Matern Fetal Neonatal Med 17:63–68CrossRefPubMed
41.
go back to reference Agakidou E, Diamanti E, Papoulidis I, Papakonstantinou E, Stergioudas I, Sarafidis K, Drossou V, Evangeliou A (2013) Effect of gestational diabetes on circulating levels of maternal and neonatal carnitine. J Diabetes Metab 4:250CrossRef Agakidou E, Diamanti E, Papoulidis I, Papakonstantinou E, Stergioudas I, Sarafidis K, Drossou V, Evangeliou A (2013) Effect of gestational diabetes on circulating levels of maternal and neonatal carnitine. J Diabetes Metab 4:250CrossRef
42.
go back to reference Visiedo F, Bugatto F, Sanchez V, Cozar-Castellano I, Bartha JL, Perdomo G (2013) High glucose levels reduce fatty acid oxidation and increase triglyceride accumulation in human placenta. Am J Physiol Endocrinol Metab 305:E205–E212CrossRefPubMed Visiedo F, Bugatto F, Sanchez V, Cozar-Castellano I, Bartha JL, Perdomo G (2013) High glucose levels reduce fatty acid oxidation and increase triglyceride accumulation in human placenta. Am J Physiol Endocrinol Metab 305:E205–E212CrossRefPubMed
43.
go back to reference Lackey DE, Lynch CJ, Olson KC, Mostaedi R, Ali M, Smith WH, Karpe F, Humphreys S, Bedinger DH, Dunn TN, Thomas AP, Oort PJ, Kieffer DA, Amin R, Bettaieb A, Haj FG, Permana P, Anthony TG, Adams SH (2013) Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am J Physiol Endocrinol Metab 304:E1175–E1187CrossRefPubMedPubMedCentral Lackey DE, Lynch CJ, Olson KC, Mostaedi R, Ali M, Smith WH, Karpe F, Humphreys S, Bedinger DH, Dunn TN, Thomas AP, Oort PJ, Kieffer DA, Amin R, Bettaieb A, Haj FG, Permana P, Anthony TG, Adams SH (2013) Regulation of adipose branched-chain amino acid catabolism enzyme expression and cross-adipose amino acid flux in human obesity. Am J Physiol Endocrinol Metab 304:E1175–E1187CrossRefPubMedPubMedCentral
44.
go back to reference Crawford SO, Hoogeveen RC, Brancati FL, Astor BC, Ballantyne CM, Schmidt MI, Young JF (2010) Association of blood lactate with type 2 diabetes: the Atherosclerosis Risk in Communities Carotid MRI Study. Int J Epidemiol 39(6):1647–1655CrossRefPubMedPubMedCentral Crawford SO, Hoogeveen RC, Brancati FL, Astor BC, Ballantyne CM, Schmidt MI, Young JF (2010) Association of blood lactate with type 2 diabetes: the Atherosclerosis Risk in Communities Carotid MRI Study. Int J Epidemiol 39(6):1647–1655CrossRefPubMedPubMedCentral
45.
go back to reference Wu Y, Dong Y, Atefi M, Liu Y, Elshimali Y, Vadgama JV (2016) Lactate, a neglected factor for diabetes and cancer interaction. Mediators Inflamm 2016:6456018 Wu Y, Dong Y, Atefi M, Liu Y, Elshimali Y, Vadgama JV (2016) Lactate, a neglected factor for diabetes and cancer interaction. Mediators Inflamm 2016:6456018
Metadata
Title
Impact of maternal BMI and gestational diabetes mellitus on maternal and cord blood metabolome: results from the PREOBE cohort study
Authors
Engy Shokry
Linda Marchioro
Olaf Uhl
Mercedes G. Bermúdez
Jose Antonio García-Santos
Mª Teresa Segura
Cristina Campoy
Berthold Koletzko
Publication date
01-04-2019
Publisher
Springer Milan
Published in
Acta Diabetologica / Issue 4/2019
Print ISSN: 0940-5429
Electronic ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-019-01291-z

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