Effects of Dietary and Physical Activity Intervention during Pregnancy on Circulating Leptin and Adiponectin Levels

Abstract

Objective: We investigated whether lifestyle intervention during pregnancy modifies pregnancy leptin and adiponectin levels, adipokines and their association with body mass index (BMI). Methods: Of the 126 pregnant nulliparous women recruited, 43 in the intervention and 56 in the control group completed the study. Blood samples were collected on gestation weeks 8 - 10 (baseline) and weeks 36 - 38 (end of the intervention). Statistical analyses included group-based correlations between adipokines, pre-pregnancy BMI and gestational weight gain and covariance analysis including all confounding factors. Results: Pre-pregnancy BMI correlated with baseline (p = 0.023 and p = 0.079) and end leptin levels (p = 0.128 and p < 0.001). Similarly, gestational weight gain correlated with both baseline (p = 0.009 and p = 0.046) and end leptin levels (p = 0.065 and p = 0.011). BMI at the end of pregnancy correlated with the end leptin levels, but the correlation was weaker in the control (p = 0.043) than intervention women (p < 0.001). Control women having the highest pre-pregnancy BMI tended to exhibit the lowest increase in leptin levels during pregnancy (p = 0.10), whilst in the intervention group, women who had the highest pre-pregnancy BMI exhibited the highest increase in pregnancy leptin (p = 0.058). In covariance analysis including all covariates change in leptin was associated with gestational weight gain (p = 0.036), but change in adiponectin was not (p = 0.93). Conclusions: In contrast to the control group, women in the life-style intervention group exhibited a stronger association between gestational weight gain and leptin levels, indicating that they maintained insulin sensitivity.

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L. Hilakivi-Clarke, S. Assis, J. Raitanen and R. Luoto, "Effects of Dietary and Physical Activity Intervention during Pregnancy on Circulating Leptin and Adiponectin Levels," Food and Nutrition Sciences, Vol. 3 No. 4, 2012, pp. 556-567. doi: 10.4236/fns.2012.34078.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Institute of Medicine, “Weight Gain during Pregnancy: Reexamining the Guidelines,” National Academies, Washington DC, 2009.
[2] R. Artal, C. J. Lockwood and H. L. Brown, “Weight Gain Recommendations in Pregnancy and the Obesity Epidemic,” Obstetrics & Gynecology, Vol. 115, No. 1, 2010, pp. 152-155. doi:10.1097/AOG.0b013e3181c51908
[3] S. S. Huda, L. E. Brodie and N. Sattar, “Obesity in Pregnancy: Prevalence and Metabolic Consequences,” Seminars in Fetal and Neonatal Medicine, Vol. 15, No. 2, 2010, pp. 70-76. doi:10.1016/j.siny.2009.09.006
[4] A. M. Siega-Riz, M. Viswanathan, M. K. Moos, A. Deierlein, S. Mumford, J. Knaack, P. Thieda, L. J. Lux and K. N. Lohr, “A Systematic Review of Outcomes of Maternal Weight Gain According to the Institute of Medicine Recommendations: Birthweight, Fetal Growth, and Postpartum Weight Retention,” American Journal of Obstetrics and Gynecology, Vol. 201, No. 4, 2009, pp. 339-314. doi:10.1016/j.ajog.2009.07.002
[5] K. Shankar, A. Harrell, X. Liu, J. M. Gilchrist, M. J. Ronis and T. M. Badger, “Maternal Obesity at Conception Programs Obesity in the Offspring,” American Journal of Physiology—Regulatory, Integrative and Comparative Physiology, Vol. 294, No. 2, 2009, pp. R528-R538. doi:10.1152/ajpregu.00316.2007
[6] S. M. Nelson, P. Matthews and L. Poston, “Maternal Metabolism and Obesity: Modifiable Determinants of Pregnancy Outcome,” Human Reproduction Update, Vol. 16, No. 3, 2009, pp. 255-275.
[7] J. C. King, “Maternal Obesity, Metabolism, and Pregnancy Outcomes,” Annual Review of Nutrition, Vol. 26, 2006, pp. 271-291. doi:10.1146/annurev.nutr.24.012003.132249
[8] T. I. Kinnunen, M. Pasanen, M. Aittasalo, M. Fogelholm, L. Hilakivi-Clarke, E. Weiderpass and R. Luoto, “Preventing Excessive Weight Gain during Pregnancy—A Controlled Trial in Primary Health Care,” European Journal of Clinical Nutrition, Vol. 61, No. 7, 2007, pp. 884-891. doi:10.1038/sj.ejcn.1602602
[9] Y. B. Kim, S. Uotani, D. D. Pierroz, J. S. Flier and B. B. Kahn, “In Vivo Administration of Leptin Activates Signal Transduction Directly in Insulin-Sensitive Tissues: Overlapping But Distinct Pathways from Insulin,” Endocrinology, Vol. 141, No. 7, 2000, pp. 2328-2339. doi:10.1210/en.141.7.2328
[10] B. O. Yildiz and I. C. Haznedaroglu, “Rethinking Leptin and Insulin Action: Therapeutic Opportunities for Diabetes,” The International Journal of Biochemistry & Cell Biology, Vol. 38, No. 5-6, 2006, pp. 820-830. doi:10.1016/j.biocel.2005.09.013
[11] M. Matsubara, S. Maruoka and S. Katayose, “Inverse Relationship between Plasma Adiponectin and Leptin Concentrations in Normal-Weight and Obese Women,” European Journal of Endocrinology, Vol. 147, No. 2, 2002, pp. 173-180. doi:10.1530/eje.0.1470173
[12] J. Jurimae, T. Jurimae, S. Ring-Dimitriou, L. M. LeMura, P. J. Arciero and S. P. von Duvillard, “Plasma Adiponectin and Insulin Sensitivity in Overweight and Normal-Weight Middle-Aged Premenopausal Women,” Metabolism, Vol. 58, No. 5, 2009, pp. 638-643. doi:10.1016/j.metabol.2008.12.009
[13] Y. Zhang, R. Proenca, M. Maffei, M. Barone, L. Leopold and J. M. Friedman, “Positional Cloning of the Mouse Obese Gene and Its Human Homologue,” Nature, Vol. 372, No. 6505, 1994, pp. 425-432. doi:10.1038/372425a0
[14] M. Fasshauer, J. Klein, S. Neumann, M. Eszlinger and R. Paschke, “Hormonal Regulation of Adiponectin Gene Expression in 3T3-L1 Adipocytes,” Biochemical and Biophysical Research Communications, Vol. 290, No. 3, 2002, pp. 1084-1089. doi:10.1006/bbrc.2001.6307
[15] I. Kowalska, M. Straczkowski, A. Nikolajuk, A. Krukowska, I. Kinalska and M. Gorska, “Plasma Adiponectin Concentration and Tumor Necrosis Factor-Alpha System Activity in Lean Non-Diabetic Offspring of Type 2 Diabetic Subjects,” European Journal of Endocrinology, Vol. 154, No. 2, 2006, pp. 319-324. doi:10.1530/eje.1.02084
[16] R. M. Blumer, S. N. van der Crabben, M. E. Stegenga, M. V. V. Tanck, M. T. Ackermans, E. Endert, P. T. van der and H. P. Sauerwein, “Hyperglycemia Prevents the Suppressive Effect of Hyperinsulinemia on Plasma Adiponectin Levels in Healthy Humans,” American Journal of Physiology—Endocrinology and Metabolism, Vol. 295, No. 3, 2008, pp. E613-E617. doi:10.1152/ajpendo.90288.2008
[17] S. Mazaki-Tovi, H. Kanety, C. Pariente, R. Hemi, A. Wiser, E. Schiff and E. Sivan, “Maternal Serum Adiponectin Levels during Human Pregnancy,” Journal of Perinatology, Vol. 27, No. 2, 2007, pp. 77-81. doi:10.1038/sj.jp.7211639
[18] I. Hendler, S. C. Blackwell, S. H. Mehta, J. E. Whitty, E. Russell, Y. Sorokin and D. B. Cotton, “The Levels of Leptin, Adiponectin, and Resistin in Normal Weight, Overweight, and Obese Pregnant Women with and without Preeclampsia,” American Journal of Obstetrics and Gynecology, Vol. 193, No. 3, 2005, pp. 979-983.
[19] J. M. Gomez, F. J. Maravall, N. Gomez, M. A. Navarro, R. Casamitjana and J. Soler, “Interactions between Serum Leptin, the Insulin-Like Growth Factor-I System, and Sex, Age, Anthropometric and Body Composition Variables in a Healthy Population Randomly Selected,” Clinical Endocrinology, Vol. 58, No. 2, 2003, pp. 213-219. doi:10.1046/j.1365-2265.2003.01698.x
[20] J. M. Friedman and J. L. Halaas, “Leptin and the Regulation of Body Weight in Mammals,” Nature, Vol. 395, No. 6704, 1998, pp. 763-770. doi:10.1038/27376
[21] L. Hardie, P. Trayhurn, D. Abramovich and P. Fowler, “Circulating Leptin in Women: A Longitudinal Study in the Menstrual Cycle and during Pregnancy,” Clinical Endocrinology, Vol. 47, No. 1, 1997, pp. 101-106. doi:10.1046/j.1365-2265.1997.2441017.x
[22] C. Schubring, P. Englaro, T. Siebler, W. F. Blum, T. Demirakca, J. Kratzsch and W. Kiess, “Longitudinal Analysis of Maternal Serum Leptin Levels during Pregnancy, at Birth and up to Six Weeks after Birth: Relation to Body Mass Index, Skinfolds, Sex Steroids and Umbilical Cord Blood Leptin Levels,” Hormone Research, Vol. 50, No. 5, 1998, pp. 276-283. doi:10.1159/000023290
[23] T. P. Stein, T. O. Scholl and M. D. Schluter, C. M. Schroeder, “Plasma Leptin Influences Gestational Weight Gain and Postpartum Weight Retention,” The American Journal of Clinical Nutrition, Vol. 68, No. 6, 1998, pp. 1236-1240.
[24] T. Tamura, R. L. Goldenberg, K. E. Johnston and S. P. Cliver, “Serum Leptin Concentrations during Pregnancy and Their Relationship to Fetal Growth,” Obstetrics & Gynecology, Vol. 91, No. 3, 1998, pp. 389-395. doi:10.1016/S0029-7844(97)00670-4
[25] A. Festa, N. Shnawa, W. Krugluger, P. Hopmeier, G. Schernthaner and S. M. Haffner, “Relative Hypoleptinaemia in Women with Mild Gestational Diabetes Mellitus,” Diabetic Medicine, Vol. 16, No. 8, 1999, pp. 656662. doi:10.1046/j.1464-5491.1999.00122.x
[26] R. Mukherjea, T. W. Castonguay, L. W. Douglass and P. Moser-Veillon, “Elevated Leptin Concentrations in Pregnancy and Lactation: Possible Role as a Modulator of Substrate Utilization,” Life Sciences, Vol. 65, No. 11, 1999, pp. 1183-1193. doi:10.1016/S0024-3205(99)00352-5
[27] J. L. Halaas, K. S. Gajiwala, M. Maffei, S. L. Cohen, B. T. Chait, D. Rabinowitz, R. L. Lallone, S. K. Burley and J. M. Friedman, “Weight-Reducing Effects of the Plasma Protein Encoded by the Obese Gene,” Science, Vol. 269, No. 5223, 1995, pp. 543-546. doi:10.1126/science.7624777
[28] R. L. Leibel, M. Rosenbaum and J. Hirsch, “Changes in Energy Expenditure Resulting from Altered Body Weight,” The New England Journal of Medicine, Vol. 332, No. 10, 1995, pp. 621-628. doi:10.1056/NEJM199503093321001
[29] T. Kusakabe, H. Tanioka, K. Ebihara, M. Hirata, L. Miyamoto, F. Miyanaga, H. Hige, D. Aotani, T. Fujisawa, H. Masuzaki, K. Hosoda and K. Nakao, “Beneficial Effects of Leptin on Glycaemic and Lipid Control in a Mouse Model of Type 2 Diabetes with Increased Adiposity Induced by Streptozotocin and a High-Fat Diet,” Diabetologia, Vol. 47, No. 10, 2009, pp. 1838-1846.
[30] P. J. Scarpace and Y. Zhang, “Leptin Resistance: A Prediposing Factor for Diet-Induced Obesity,” American Journal of Physiology—Regulatory, Integrative Comparative Physiology, Vol. 296, No. 3, 2009, pp. R493-R500. doi:10.1152/ajpregu.90669.2008
[31] E. Sivan, P. G. Whittaker, D. Sinha, C. J. Homko, M. Lin, E. A. Reece and G. Boden, “Leptin in Human Pregnancy: The Relationship with Gestational Hormones,” American Journal of Obstetrics and Gynecology, Vol. 179, No. 5, 1998, pp. 1128-1132. doi:10.1016/S0002-9378(98)70118-8
[32] S. M. Stock, E. M. Sande and K. A. Bremme, “Leptin Levels Vary Significantly during the Menstrual Cycle, Pregnancy, and in Vitro Fertilization Treatment: Possible Relation to Estradiol,” Fertility and Sterility, Vol. 72, No. 4, 1999, pp. 657-662. doi:10.1016/S0015-0282(99)00321-0
[33] N. F. Butte, J. M. Hopkinson and M. A. Nicolson, “Leptin in Human Reproduction: Serum Leptin Levels in Pregnant and Lactating Women,” The Journal of Clinical Endocrinology & Metabolism, Vol. 82, No. 2, 1997, pp. 585-589. doi:10.1210/jc.82.2.585
[34] S. R. Ladyman, R. A. Augustine and D. R. Grattan, “Hormone Interactions Regulating Energy Balance during Pregnancy,” Journal of Neuroendocrinology, Vol. 22, No. 7, 2010, pp. 805-817.
[35] D. R. Grattan, S. R. Ladyman and R. A. Augustine, “Hormonal Induction of Leptin Resistance during Pregnancy,” Physiology & Behavior, Vol. 91, No. 4, 2007, pp. 366374. doi:10.1016/j.physbeh.2007.04.005
[36] R. A. Augustine, S. R. Ladyman and D. R. Grattan, “From Feeding One to Feeding Many: Hormone-Induced Changes in Bodyweight Homeostasis during Pregnancy,” The Journal of Physiology, Vol. 586, No. 2, 2008, pp. 387-397. doi:10.1113/jphysiol.2007.146316
[37] J. P. Kirwan, S. Hauguel-De Mouzon, J. Lepercq, J. C. Challier, L. Huston-Presley, J. E. Friedman, S. C. Kalhan and P. M. Catalano, “TNF-Alpha Is a Predictor of Insulin Resistance in Human Pregnancy,” Diabetes, Vol. 51, No. 7, 2002, pp. 2207-2213. doi:10.2337/diabetes.51.7.2207
[38] Z. Maghbooli, A. Hossein-Nezhad, M. Rahmani, A. R. Shafaei and B. Larijani, “Relationship between Leptin Concentration and Insulin Resistance,” Hormone and Metabolic Research, Vol. 39, No. 12, 2007, pp. 903-907. doi:10.1055/s-2007-992812
[39] J. M. Ategbo, O. Grissa, A. Yessoufou, A. Hichami, K. L. Dramane, K. Moutairou, A. Miled, A. Grissa, M. Jerbi, Z. Tabka and N. A. Khan, “Modulation of Adipokines and Cytokines in Gestational Diabetes and Macrosomia,” The Journal of Clinical Endocrinology & Metabolism, Vol. 91, No. 10, 2006, pp. 4137-4143. doi:10.1210/jc.2006-0980
[40] K. A. McLachlan, D. O’Neal, A. Jenkins and F. P. Alford, “Do Adiponectin, TNFalpha, Leptin and CRP Relate to Insulin Resistance in Pregnancy? Studies in Women with and without Gestational Diabetes, during and after Pregnancy,” Diabetes/Metabolism Research and Reviews, Vol. 22, No. 2, 2006, pp. 131-138. doi:10.1002/dmrr.591
[41] H. Yamashita, J. Shao, T. Ishizuka, P. J. Klepcyk, P. Muhlenkamp, L. Qiao, N. Hoggard and J. E. Friedman, “Leptin Administration Prevents Spontaneous Gestational Diabetes in Heterozygous Lepr(db/+) Mice: Effects on Placental Leptin and Fetal Growth,” Endocrinology, Vol. 142, No. 7, 2001, pp. 2888-2897. doi:10.1210/en.142.7.2888
[42] R. Saucedo, A. Zarate, L. Basurto, M. Hernandez, E. Puello, R. Galvan and S. Campos, “Relationship between Circulating Adipokines and Insulin Resistance during Pregnancy and Postpartum in Women with Gestational Diabetes,” Archives of Medical Research, Vol. 42, No. 4, 2011, pp. 318-323. doi:10.1016/j.arcmed.2011.06.009
[43] T. Kadowaki, T. Yamauchi, N. Kubota, K. Hara, K. Ueki and K. Tobe, “Adiponectin and Adiponectin Receptors in Insulin Resistance, Diabetes, and the Metabolic Syndrome,” The Journal of Clinical Investigation, Vol. 116, No. 7, 2006, pp. 1784-1792. doi:10.1172/JCI29126
[44] A. H. Berg, T. P. Combs and P. E. Scherer, “ACRP30/ Adiponectin: An Adipokine Regulating Glucose and Lipid Metabolism,” Trends in Endocrinology & Metabolism, Vol. 13, No. 2, 2002, pp. 84-89. doi:10.1016/S1043-2760(01)00524-0
[45] T. Kadowaki, T. Yamauchi, N. Kubota, K. Hara and K. Ueki, “Adiponectin and Adiponectin Receptors in Obesity-Linked Insulin Resistance,” Novartis Foundation Symposium, Vol. 286, 2007, pp. 164-176. doi:10.1002/9780470985571.ch15
[46] K. J. Mather, T. Funahashi, Y. Matsuzawa, S. Edelstein, G. A. Bray, S. E. Kahn, J. Crandall, S. Marcovina, B. Goldstein and R. Goldberg, “Adiponectin, Change in Adiponectin, and Progression to Diabetes in the Diabetes Prevention Program,” Diabetes, Vol. 57, No. 4, 2008, pp. 980-986. doi:10.2337/db07-1419
[47] A. E. Altinova, F. Toruner, N. Bozkurt, N. Bukan, A. Karakoc, I. Yetkin, G. Ayvaz, N. Cakir and M. Arslan, “Circulating Concentrations of Adiponectin and Tumor Necrosis Factor-Alpha in Gestational Diabetes Mellitus,” Gynecological Endocrinology, Vol. 23, No. 3, 2007, pp. 161-165. doi:10.1080/09513590701227960
[48] P. M. Catalano, M. Hoegh, J. Minium, L. Huston-Presley, S. Bernard, S. Kalhan and S. Hauguel-De Mouzon, “Adiponectin in Human Pregnancy: Implications for Regulation of Glucose and Lipid Metabolism,” Diabetologia, Vol. 49, No. 7, 2006, pp. 1677-1685. doi:10.1007/s00125-006-0264-x
[49] S. Soheilykhah, M. Mohammadi, M. Mojibian, S. Rahimi-Saghand, M. Rashidi, H. Hadinedoushan and M. fkhami-Ardekani, “Maternal Serum Adiponectin Concentration in Gestational Diabetes,” Gynecological Endocrinology, Vol. 25, No. 9, 2009, pp. 593-596. doi:10.1080/09513590902972109
[50] S. Weerakiet, K. Lertnarkorn, P. Panburana, S. Pitakitronakorn, K. Vesathada and S. Wansumrith, “Can Adiponectin Predict Gestational Diabetes?” Gynecological Endocrinology, Vol. 22, No. 7, 2006, pp. 362-368. doi:10.1080/09513590600818919
[51] Suositukset, “Seulontatutkimukset ja Yhteistyo Aitiyshuollossa,” Gummerus, Jyvaskyla, 1999.
[52] Institute of Medicine, “Nutrition during Pregnancy, Weight Gain and Nutrient Supplements,” National Academic Press, Washington DC, 1990.
[53] K. Cseh, E. Baranyi, Z. Melczer, E. Kaszas, E. Palik and G. Winkler, “Plasma Adiponectin and Pregnancy-Induced Insulin Resistance,” Diabetes Care, Vol. 27, No. 1, 2004, pp. 274-275. doi:10.2337/diacare.27.1.274
[54] R. Luoto, T. I. Kinnunen, M. Aittasalo, P. Kolu, J. Raitanen, K. Ojala, K. Mansikkamaki, S. Lamberg, T. Vasankari, T. Komulainen and S. Tulokas, “Primary Prevention of Gestational Diabetes Mellitus and Large-for-Gestational-Age Newborns by Lifestyle Counseling: A ClusterRandomized Controlled Trial,” PLoS Medicine, Vol. 8, No. 5, 2011, p. e1001036. doi:10.1371/journal.pmed.1001036
[55] A. Lagiou, P. Lagiou, D. S. Vassilarou, M. Stoikidou and D. Trichopoulos, “Comparison of Age at First Full-Term Pregnancy between Women with Breast Cancer and Women with Benign Breast Diseases,” International Journal of Cancer, Vol. 107, No. 5, 2003, pp. 817-821. doi:10.1002/ijc.11476
[56] G. K. Ong, J. K. Hamilton, M. Sermer, P. W. Connelly, G. Maguire, B. Zinman, A. J. Hanley and R. Retnakaran, “Maternal Serum Adiponectin and Infant Birthweight: The Role of Adiponectin Isoform Distribution,” Clinical Endocrinology, Vol. 67, No. 1, 2007, pp. 108-114. doi:10.1111/j.1365-2265.2007.02846.x
[57] F. S. Al Atawi, M. H. Addar, A. S. Warsy and Z. A. Babay, “Leptin Concentration during Different Trimesters of Pregnancy and Its Relation to Other Pregnancy Hormones,” Saudi Medical Journal, Vol. 25, No. 11, 2004, pp. 1617-1622.
[58] A. Kautzky-Willer, G. Pacini, A. Tura, C. Bieglmayer, B. Schneider, B. Ludvik, R. Prager and W. Waldhausl, “Increased Plasma Leptin in Gestational Diabetes,” Diabetologia, Vol. l 44, No. 2, 2001, pp. 164-172.
[59] J. Fuglsang, C. Skjaerbaek, J. Frystyk, A. Flyvbjerg and P. Ovesen, “A Longitudinal Study of Serum Adiponectin during Normal Pregnancy,” BJOG, Vol. 113, No. 1, 2006, pp. 110-113. doi:10.1111/j.1471-0528.2005.00792.x
[60] B. Eriksson, M. Lof, H. Olausson and E. Forsum, “Body Fat, Insulin Resistance, Energy Expenditure and Serum Concentrations of Leptin, Adiponectin and Resistin before, during and after Pregnancy in Healthy Swedish Women,” British Journal of Nutrition, Vol. 103, No. 1, 2010, pp. 50-57. doi:10.1017/S0007114509991371
[61] R. Retnakaran, Y. Qi, P. W. Connelly, M. Sermer, A. J. Hanley and B. Zinman, “Low Adiponectin Concentration during Pregnancy Predicts Postpartum Insulin Resistance, Beta Cell Dysfunction and Fasting Glycaemia,” Diabetologia, Vol. 53, No. 2, 2009, pp. 268-276.
[62] J. K. Nien, S. Mazaki-Tovi, R. Romero, O. Erez, J. P. Kusanovic, F. Gotsch, B. L. Pineles, R. Gomez, S. Edwin, M. Mazor, J. Espinoza, B. H. Yoon and S. S. Hassan, “Plasma Adiponectin Concentrations in Non-Pregnant, Normal and Overweight Pregnant Women,” Journal of Perinatal Medicine, Vol. 35, No. 6, 2007, pp. 522-531. doi:10.1515/JPM.2007.123

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