Adiponectin in mother-and-child couple: is there a relation with materno-foetal transfer of nutrients, obesity and risk of type 2 diabetes?
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1 Adiponectin in mother-and-child couple: is there a relation with materno-foetal transfer of nutrients, obesity and risk of type 2 diabetes? Félix Ovono Abessolo 1, Jean Pierre Ngou-Mve-Ngou 2, John Mouba 3, Aude Mbang Bengone 1, Edouard Ngou-Milama 1 1Laboratoire de Biochimie Médicale, Département de Chimie-Biochimie, Biologie Cellulaire & Moléculaire, Faculté de Médecine, Université des Sciences de la Santé, Libreville, Gabon 2Fondation Jeanne Ebori, Service de Gynécologie, Libreville, Gabon 3Service de Pédiatrie, Hôpital Pédiatrique, Libreville, Gabon ABSTRACT To evaluate relationships between maternal and fetal adiponectin concentrations and lipoprotein and glycemic parameters in mother-and-child unity at birth, a study was performed with 90 women admitted in the delivery room after a free enlightened consent. Blood samples were taken simultaneously at delivery from mothers (peripheral venous) and newborns (umbilical cord) for glucose, cholesterol, triglyceride, and adiponectin determinations. Multiple correlations between different parameters were made. Adiponectin concentrations in cord blood were three times higher than in the mother s blood, while total, HDL and LDL cholesterol concentrations were higher in mothers. We demonstrated a slight inverse correlation between maternal adiponectin and gestational age (P=0.026) and between maternal adiponectin and concentrations of triglycerides in mothers (P=0.066). On the other hand, there were positive correlations between adiponectin concentrations, both in mothers and newborns, and LDL cholesterol concentrations in newborns (P= and P=0.028, respectively). We inferred that at the end of pregnancy the mother undergoes a situation of insulin resistance, with a decrease in adiponectin concentrations. This may cause the re-routing of her metabolites towards the fetus who under insulin sensitivity would use those metabolites for its metabolic needs. If maternal insulin resistance is higher because of obesity or diabetes, the fetus would receive more metabolites than necessary and would store them as long as its biosynthetic needs are met. This could lead to macrosomia at birth and to obesity afterwards. INTRODUCTION Obesity is defined as the presence of excessive amount of adipose tissue. It is a physiologic response to the environment, resulting from a positive energy balance. Its prevalence is globally increasing worldwide (1). It is associated with multiple metabolic disturbances, such as insulin resistance matched with hyperinsulinemia, type 2 diabetes (T2DM), dyslipidemia, hypertension, and cardiovascular disease. Most of people suffering from diabetes are obese and the worldwide increase of obesity during the last ten years has led to a 25% increase of T2DM prevalence (2). The common characteristic of diabetes and obesity is the insulin resistance (3). In the case of obesity, insulin resistance results from excessive energy intake with or without genetic predisposition factors. In the case of diabetes, insulin resistance results from genetic disorders and genes involved in insulin resistance have been identified. As far as insulin resistance is concerned, physiologic glucose blood concentrations are obtained through increasing insulin secretion, leading to hyperinsulinemia. Usually, insulin secretion as a compensatory response to excessive caloric intake is close to perfection, keeping glycemia at physiological concentrations. However, if the situation persists, increased excessive insulin secretion cannot be held for a long time. Indeed, insulin rate of secretion decreases and insulin plasmatic concentrations normalize and even fall to subnormal values; glucose intolerance then takes place and evolves to typical diabetes (3). To develop appropriate prevention strategies, it is fundamental to apprehend pathophysiologic mechanisms supporting the evolution from obesity to diabetes mellitus. In this regard, adiponectin, a cytokine produced by adipose tissue, is currently considered as the link between obesity and T2DM (4). Studies have shown that it decreases glucose intolerance and improves insulin sensitivity. In longitudinal studies, adiponectin concentrations increased with weight loss in Corrispondence to: Félix Ovono Abessolo, Laboratoire de Biochimie Médicale, Département de Chimie-Biochimie, Biologie Cellulaire & Moléculaire, Faculté de Médecine, Université des Sciences de la Santé, BP 4009 Libreville, Gabon. ovonab@yahoo.fr Ricevuto: Revisionato: Accettato: biochimica clinica, 2012, vol. 36, n
2 SCIENTIFIC PAPERS non-diabetic obese subjects and epidemiologic studies have shown an association between birth weight and adiponectin concentrations (5, 6). Here we studied the relationship between adiponectin and some biochemical parameters of the mother-and-child couple at birth to infer on materno-foetal transfer of nutrients and obesity predisposition. MATERIAL AND METHODS Type of study and setting This was a prospective and open study that took place from August 2009 to January The obstetric gynecology service s delivery room at the Libreville Medical Center and the Laboratory of Medical Biochemistry of the Libreville College of Medicine in Gabon, along with the Nutrigenetic Laboratory of Jussieu at Paris (France) were the sites that helped for the realization of this work. Population The study included women, admitted at the delivery room for labor, delivering a vivid baby through natural tract. Mothers and their newborn babies were recruited on a daily basis, including multigravida and multiparous mothers. Women were retained on the basis of complete antenatal check-up, absence of medication, and signature of free and enlightened consent. The work was carried out according to the Helsinki Declaration of 1975, as revised in We excluded women with infection reported by the parturient or recorded in the medical follow-up book, a positive retroviral serology, hypertension or diabetes history, and twin pregnancies. We looked for gestational diabetes after any recorded case of intolerance to glucose from glycemia measured between the 20 th and the 24 th week of amenorrhea. Sudden cases of hypertension occurring during pregnancy were defined by arterial systolic pressure 140 mmhg and/or arterial diastolic pressure 90 mmhg or by any increase of arterial pressure from baseline of at least 30 mmhg for systolic and 15 mmhg for diastolic. We also tested women for proteinuria using strip-test in order to rule out any case of preeclampsia. Blood sampling Mother s blood was taken by peripheral venous puncture at the elbow s plica (brachio-radial vein) after at least 8 h of fasting. In the newborn, umbilical cord blood was taken a few sec before the delivery. Blood samples were stored on ice and immediately sent to the laboratory after identification. Tubes were afterwards centrifuged at 3000 r.p.m. for 5 min and samples aliquoted. A fraction of each aliquoted serum was stored at -80 C and sent to the Nutrigenetic Laboratory at the Jussieu Hospital in Paris for adiponectin analyses. Biochemical analyses Total cholesterol, triglyceride, and glucose analyses were carried out using enzymatic methods. HDL cholesterol concentrations were measured after precipitation of apolipoprotein B-rich fractions using magnesium tungstate. LDL cholesterol concentrations were calculated using the Friedewald formula (7). We measured high MW adiponectin by ELISA (Daiichi Pure Chemical). The detection limit of the adiponectin assay was 0.40 mg/l. The intra- and interassay CV were <10% and <15%, respectively. All the measurements were performed in duplicate and the mean value was retained. Data analysis For our estimate, we used median values for quantitative variables and the frequency distribution for qualitative variables. Correlations were obtained with the Spearman s test and were considered significant for P <0.10. RESULTS We worked with a sampling of 90 mother-and-child couples. The parturient age varied between 17 and 43 years, with a median of 26 years. The median weight at the first trimester was 65 kg, with extreme values recorded at 40 and 107 kg. It corresponded to a median body mass index (BMI) of 24.3 kg/m 2. The weight gain during the pregnancy was 11 kg, with a minimum of 1 kg and a maximum of 28 kg. 50% of women had delivered at 39 weeks of amenorrhea. That term was inversely correlated to BMI and to the weight at the beginning of the pregnancy (r= and r= 0.481, respectively). 65% of the children were males. The median weight at birth was 3.12 kg, with extreme values at 2.60 and 4.86 kg. Other anthropometric parameters are summarized in Table 1. Table 2 displays biochemical parameters in mothers and children. The mother s glycemia was positively correlated to the maternal BMI (r=0.590, P=0.003), but inversely related to maternal weight gain during pregnancy (r= 0.460). Total cholesterol concentrations were not associated to the BMI (r=0.193, P=0.38). Whereas maternal HDL cholesterol concentration were found to be related to the weight before pregnancy (r=0.411, P=0.05), to the weight in the delivery room (r=0.441, P=0.035), and to the weight gain (r=0.395, P=0.06), this was not the case for LDL cholesterol. Mother s triglycerides were associated to the gestational age (r=0.524, P=0.013). The median value of adiponectin in mother s blood was 6.0 mg/l, with a maximum at 11.3 mg/l and a minimum at 3.2 mg/l. This parameter was not influenced by the majority of mother s morphological parameters (Table 3). However, maternal adiponectinemia was negatively associated to the gestational age (r= 0.463, P=0.026). It was the same with maternal triglyceridemia (P=0.066). We also found a slight positive association between maternal adiponectin and newborn LDL cholesterol concentrations (r=0.391, P=0.072). The glycemia in the cord blood was correlated to 236 biochimica clinica, 2012, vol. 36, n. 4
3 Table 1 Mother and newborn anthropometric parameters Variable Median 95% Confidence interval Mothers Age (years) Weight at first trimester (kg) Weight in delivering room (kg) Body mass index at first trimester (kg/m²) Gestational age (week) Systolic blood pressure (mmhg) Diastolic blood pressure (mmhg) Weight gain (kg) Height (cm) Newborns Weight (kg) Height (cm) Apgar score Table 2 Mother and newborn biochemical parameters (median and 95% confidence interval) Parameter Mothers Newborns Glycemia (mmol/l) 5.6 ( ) 4.4 ( ) Total cholesterol (mmol/l) 4.9 ( ) 1.5 ( ) HDL cholesterol (mmol/l) 1.4 ( ) 0.5 ( ) Triglycerides (mmol/l) 1.7 ( ) 0.5 ( ) LDL cholesterol (mmol/l) 2.6 ( ) 0.8 ( ) Adiponectin (mg/l) 6.0 ( ) 17.6 ( ) Table 3 Correlations of estimated parameters with mother adiponectin concentrations Parameter Correlation coefficient P Age Weight at first trimester Body mass index at first trimester Gestational age Mother triglyceride Mother LDL cholesterol Newborn weight Newborn HDL cholesterol Newborn LDL cholesterol the maternal one (r=0.782, P=0.0001). However, the relationship between newborn glycemia and the maternal BMI recorded at the onset of pregnancy was weak (r=0.407, P=0.05). Cord blood LDL cholesterol was negatively slightly correlated with women age (r= 0.432, P=0.05). Triglyceride concentrations were only associated to cord blood total cholesterol concentrations (r=0.577, P=0.0039). We observed a median value of adiponectin in cord blood of 17.6 mg/l. The hormone concentrations were negatively slightly correlated with the BMI (r= 0.373, P=0.080) and gestational age (r= 0.375, P=0.077). On the other hand, newborn adiponectin concentrations were closely related to newborn LDL cholesterol concentrations (r=0.467, P=0.028) (Table 4). biochimica clinica, 2012, vol. 36, n
4 SCIENTIFIC PAPERS Table 4 Correlations of estimated parameters with newborn adiponectin concentrations Parameter Correlation coefficient P Age Weight at first trimester Body mass index at first trimester Gestational age Mother glycemia Mother triglyceride Newborn weight Newborn glycemia Newborn total cholesterol Newborn LDL cholesterol Newborn HDL cholesterol DISCUSSION Adiponectin, a collagen-like plasma protein hormone secreted by adipocytes, has been suggested to play a causal role in the development of insulin resistance, obesity, and cardiovascular disease in adulthood (8). The aim of this work was to investigate adiponectin concentrations in both mothers and newborns in view to rely them with obesity predisposition. Accordingly, we explored the concentrations of adiponectin at birth in relationship with both mother and newborn physical and biochemical parameters. We found umbilical cord blood adiponectin concentrations approximately three times higher than in maternal blood. This difference suggests different levels of insulin sensitivity between mother and child at delivery, possibly leading to nutrient transfer from mother to child at the end of the pregnancy. In fact, during pregnancy, and mostly in the third trimester, a state of insulin resistance is gradually settled down, with an increase of blood glucose and free fatty acid concentrations. This drives an increase of maternal insulinemia (9). The newly acquired insulin resistance at the end of pregnancy is reflected in relatively lower maternal adiponectin concentrations, such as those we had recorded. The direct consequence of the insulin resistance would be the increase of glucose rate disposal for the fetus and placental metabolic needs. Adiponectin thus appears as a glycemia regulator in fetus by adjusting maternal insulin sensitivity. The positive correlation found between newborn glycemia and maternal BMI supports the evidence for a link between maternal obesity and carbohydrate intolerance and newborn glycemia increase. Free glucose utilization by the fetus or the placenta for their energetic needs requires an increase in insulin sensitivity with high adiponectin concentrations. Similar findings were described by other authors (10, 11). Such relationship is confirmed by the observed negative correlation between maternal adiponectin and the gestational age. In fact, the longer the pregnancy, the lower the maternal adiponectin, and the more the mother would experience insulin resistance with a high risk of gestational diabetes or hypertensive pathologies during pregnancy (12). The fetal origin of adiponectin in cord blood has been demonstrated (10). If the fetus receives an excess of nutrients, he will use them at first for its biosynthetic needs, then he will store the excess as an energetic reserve in the adipose tissue. The increasing volume of adipose tissue, with formation of mature adipocytes, will generate a negative feedback for adiponectin synthesis (13). We found a negative correlation between maternal adiponectin and triglycerides. In addition, a relationship between maternal and newborn adiponectin and LDL cholesterol in newborns was shown. These data disagree with those pubblished by Bansal et al. (10). However, relations observed in correlations studies can be explained as the fetus needs cholesterol for different biosyntheses and such need implies a mobilization of lipoproteins such as LDL. Besides, women at the end of the pregnancy do not need to accumulate triglycerides, but will rather convey cholesterol towards the fetus for synthesis. ACKNOWLEDGEMENTS Authors are grateful to adiponectin analysis. REFERENCES Dr. J.M. Lacorte for 1. Grant PJ. Obesity, diabetes and cardiovascular diseases: is the fat lady singing? Diab Vasc Dis Res 2006;3: Guerre-Millo M. Adipose tissue and adipokines: for better or worse. Diabetes Metab 2004;30: Unger RH. Weapons of lean body mass destruction: the role of ectopic lipids in the metabolic syndrome. Endocrinology 2003;144: Bastard JP, Maachi M, Lugathu C, et al. Recent advances in the relationship between obesity, inflammation and insulin resistance. Eur Cyt Net 2006;1: Weiss R. Fat distribution and storage: how much, where, 238 biochimica clinica, 2012, vol. 36, n. 4
5 and how? Eur J Endocrinol 2007;157: Cianfarani S, Martinez C, Maiorana A, et al. Adiponectin levels are reduced in children borned small for gestational age and are inversely related to postnatal catch-up growth. J Clin Endocrinol Metab 2004;89: Friedewald WT, Levy RI, Fredrickson DS. Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 1972;18: Kewano J, Arora R. The role of adiponectin in obesity, diabetes, and cardiovascular disease. J Cardiometab Syndr 2009;4: Buchanan TA, Xiang. Gestational diabetes mellitus. J Clin Invest 2005;115: Bansal N, Charlton-Menys V, Pemberton P, et al. Adiponectin in umbilical cord blood is inversely related to low-density lipoprotein cholesterol but not ethnicity. J Clin Endocrinol Metab 2006;91: Weryermann M, Beermann C, Brenner H, et al. Adiponectin and leptin in maternal serum, cord blood and breast milk. Clin Chem 2006;52: Thadhani R, Ecker JC, Mutter WP, et al. Insulin resistance and alterations in angiogenesis: additive insults that may lead to preeclampsia. Hypertension 2004;43: Kershaw EE, Flier JS. Adipose tissue as an endocrine organ. J Clin Endocrinol Metab 2004;89: biochimica clinica, 2012, vol. 36, n
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