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Intermediate metabolism in normal pregnancy and in gestational diabetes
Abstract
Complex though integrated hormonal and metabolic changes characterize pregnancy. In the face of progressive decline in insulin action, glucose homeostasis is maintained through a compensatory increase in insulin secretion. This switches energy production from carbohydrates to lipids, making glucose readily available to the fetus. This precise and entangled hormonal and metabolic condition can, however, be disrupted and diabetic hyperglycemia can develop (gestational diabetes). The increase in plasma glucose level is believed to confer significant risk of complications to both the mother and the fetus and the newborn. Moreover, exposition of fetal tissues to the diabetic maternal environment can translate into an increased risk for development of diabetes and/or the metabolic syndrome in the adult life. In women with previous gestational diabetes, the risk of developing type 2 diabetes is greatly enhanced, to the point that GDM represents an early stage in the natural history of type 2 diabetes. In these women, accurate follow-up and prevention strategies are needed to reduce the subsequent development of overt diabetes. This paper will review current knowledge on the modifications occurring in normal pregnancy, while outlining the mechanisms. In this paper, we will review the changes of intermediary metabolism occurring during pregnancy. In particular, we will outline the mechanisms responsible for gestational diabetes; the link between these alterations and associated maternal and neonatal morbidity will be examined.
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“During early gestation, insulin sensitivity increases, promoting the uptake of glucose into adipose stores in preparation for the energy demands of later pregnancy [5].”
From The Pathophysiology of Gestational Diabetes Mellitus (2018) · cites this paper as [5]
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Habibi, N., Mousa, A., Tay, C. T., Khomami, M. B., Patten, R. K., Andraweera, P. H., Wassie, M., Vandersluys, J., Aflatounian, A., Bianco‐Miotto, T., et al. (2022) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.3532 · Cited by 53
Insulin therapy in pregnancy complicated by diabetes: are insulin analogs a new tool?
Lapolla, A., Dalfrà, M. G., & Fedele, D. (2005) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.551 · Cited by 51
“During the first trimester, insulin sensitivity is normal, but, as pregnancy progresses, a decrease in insulin sensitivity occurs, and, in late pregnancy, it falls by about 50% [11].”
BackgroundMetabolomics in gestational diabetes
Mao, X., Chen, X., Chen, C., Zhang, H., & Law, K. P. (2017) · Clinica Chimica Acta · doi:10.1016/j.cca.2017.10.019 · Cited by 53
Hocaoğlu, M., Demirer, S., Şentürk, H., Turgut, A., & Kömürcü-Bayrak, E. (2019) · Pregnancy Hypertension · doi:10.1016/j.preghy.2019.04.004 · Cited by 53
Avis, H. J., Hutten, B. A., Twickler, T. B., Kastelein, J. J. P., van der Post, J., Stalenhoef, A. F. H., & Vissers, M. N. (2009) · Current Opinion in Lipidology · doi:10.1097/mol.0b013e3283319127 · Cited by 52
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“These metabolic changes, culminating at the end of pregnancy, are essential for normal fetal nourishment, growth and development and adequate maternal metabolism [2].”
BackgroundNegrato, C. A., Jovanovič, L., Tambascia, M. A., Calderon, I. D. M. P., Geloneze, B., Días, A., & Rudge, M. V. C. (2008) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.815 · Cited by 50
“In the control group (normal 100 g OGTT and glycaemic profile), the HOMA-IR and HOMA-ß evolution confirm the typical elevation in insulin resistance that characterizes normal pregnancy accompanied by a compensatory hyperinsulinaemia that returns to normal levels 6 weeks after delivery [34].”
BackgroundLapolla, A., Dalfrà, M. G., Bonomo, M., Castiglioni, M. T., Cianni, G. D., Masin, M., Mion, E., Paleari, R., Schievano, C., Songini, M., et al. (2007) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2007.01.022 · Cited by 47
Self-citationYang, Y., Liu, L., Liu, B., Li, Q., Wang, Z., Fan, S.-Y., Wang, H., & Wang, L. (2018) · DNA and Cell Biology · doi:10.1089/dna.2017.4005 · Cited by 49
“The overall incidence of GDM is between 4% and 7%, with 2- to 20-fold higher risk in overweight and obese women (Di Cianni et al., 2003).”
BackgroundUse of glargine in pregnant women with type 1 diabetes mellitus: a case-control study
IMBERGAMO, M., AMATO, M., SCIORTINO, G., GAMBINA, M., ACCIDENTI, M., CRISCIMANNA, A., GIORDANO, C., & GALLUZZO, A. (2008) · Clinical Therapeutics · doi:10.1016/j.clinthera.2008.08.013 · Cited by 46
Maternal Arsenic Exposure and Gestational Diabetes: A Systematic Review and Meta-Analysis
Salmeri, N., Villanacci, R., Ottolina, J., Bartiromo, L., Cavoretto, P. I., Dolci, C., Lembo, R., Schimberni, M., Valsecchi, L., Viganò, P., et al. (2020) · Nutrients · doi:10.3390/nu12103094 · Cited by 45
“In normal pregnancy, insulin sensitivity physiologically changes depending on gestational age; in early gestation, the sensitivity increases, promoting glucose uptake in adipocytes in order to store energy for later pregnancy [48].”
BackgroundZhang, R., Zhang, X., Xing, B., Zhao, J., Zhang, P., Shi, D., & Yang, F. (2019) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-019-0522-7 · Cited by 46
“The decreased insulin secretion and the enhanced insulin-resistant state disturb the maternal insulin balance then trigger the maternal glucose intolerance and promote the pathogenesis of GDM [27].”
BackgroundRole of ferroptosis in pregnancy related diseases and its therapeutic potential
Xu, J., Zhou, F., Wang, X., & Mo, C. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1083838 · Cited by 45
Proximity to Delivery Alters Insulin Sensitivity and Glucose Metabolism in Pregnant Mice
Musiał, B., Fernandez‐Twinn, D. S., Vaughan, O. R., Ozanne, S. E., Voshol, P. J., Sferruzzi-Perri, A. N., & Fowden, A. L. (2016) · Diabetes · doi:10.2337/db15-1531 · Cited by 44
“In humans and rats, early pregnancy is a period of lipid accumulation and unchanged or increased insulin sensitivity, whereas later pregnancy is characterized by lipid mobilization and insulin resistance, common features of overt type 2 diabetes (1,2,5,6).”
Lu, S., Wang, J., Kakongoma, N., Hua, W., Xu, J., Wang, Y., He, S., Gu, H., Shi, J., & Hu, W. (2022) · Clinical Epigenetics · doi:10.1186/s13148-022-01289-5 · Cited by 45
Dynamic efficiency of the human intestinal microbiota
Candela, M., Biagi, E., Turroni, S., Maccaferri, S., Figini, P., & Brigidi, P. (2013) · Critical Reviews in Microbiology · doi:10.3109/1040841x.2013.813900 · Cited by 45
Lapolla, A., Amaro, F., Bruttomesso, D., Bartolo, P. D., Grassi, G., Maffeis, C., Purrello, F., & Tumini, S. (2020) · Nutrition Metabolism and Cardiovascular Diseases · doi:10.1016/j.numecd.2020.06.006 · Cited by 42
Cianni, G. D., Ghio, A., Resi, V., & Volpe, L. (2010) · Women s Health · doi:10.2217/whe.09.76 · Cited by 43
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Self-citationPregnancy to postpartum transition of serum metabolites in women with gestational diabetes
Chorell, E., Andersson-Hall, U. K., Gustavsson, C., Berntorp, K. E., Puhkala, J., Luoto, R. M., Olsson, T., & Holmäng, A. B. (2017) · Metabolism · doi:10.1016/j.metabol.2016.12.018 · Cited by 40
“or postpartum T2DM [3, 5] has not been successful.”
BackgroundInfluentialOrtega, M. A., Fraile‐Μartinez, O., Montero, C. G., Paradela, A., Sánchez-Gil, M. A., Rodriguez-Martín, S., León-Luis, J. A. D., Pereda-Cerquella, C., Buján, J., Guijarro, L. G., et al. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.1060850 · Cited by 43
Guidelines for assessing maternal cardiovascular physiology during pregnancy and postpartum
Collins, H. E., Alexander, B. T., Care, A. S., Davenport, M. H., Davidge, S. T., Eghbali, M., Giussani, D. A., Hoes, M. F., Julian, C. G., LaVoie, H. A., et al. (2024) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00055.2024 · Cited by 46
Watkins, O. C., Yong, H. E. J., Sharma, N., & Chan, S. (2020) · Critical Reviews in Food Science and Nutrition · doi:10.1080/10408398.2020.1845604 · Cited by 40
“Pregnancy is characterized by substantial and complex changes in glycemic and lipidomic regulation, brought about by signals released by the fetal-placental unit (Di Cianni et al. 2003).”
BackgroundFetomaternal Expression of Glucose Transporters (GLUTs)—Biochemical, Cellular and Clinical Aspects
Sibiak, R., Ożegowska, K., Wender-Ożegowska, E., Gutaj, P., Mozdziak, P. E., & Kempisty, B. (2022) · Nutrients · doi:10.3390/nu14102025 · Cited by 47
Fraticelli, F., Celentano, C., Zecca, I. A., Di Vieste, G., Pintaudi, B., Liberati, M., Franzago, M., Di Nicola, M., & Vitacolonna, E. (2018) · Acta Diabetologica · doi:10.1007/s00592-018-1157-4 · Cited by 39
Gestational diabetes mellitus in association with macrosomia in Iran: a meta-analysis
Tabrizi, R., Asemi, Z., Lankarani, K. B., Akbari, M., Khatibi, S. R., Naghibzadeh‐Tahami, A., Sanjari, M., Alizadeh, H., Afshari, M., Khodadost, M., et al. (2019) · Journal of Diabetes & Metabolic Disorders · doi:10.1007/s40200-019-00388-0 · Cited by 37
Low-Carbohydrate Diets for Gestational Diabetes
Farabi, S. S., & Hernandez, T. L. (2019) · Nutrients · doi:10.3390/nu11081737 · Cited by 37
“The blunted insulin secretion resulted in insulin levels inadequate to suppress lipolysis and drove elevated FFA over 24 h [93].”
BackgroundInfluentialAssociation Between Insulin Resistance, Glucose Intolerance, and Hypertension in Pregnancy
Negrato, C. A., Jovanovič, L., Tambascia, M. A., Geloneze, B., Días, A., Calderon, I. D. M. P., & Rudge, M. V. C. (2008) · Metabolic Syndrome and Related Disorders · doi:10.1089/met.2008.0043 · Cited by 39
“14,15 Some conditions that are associated with insulin resistance, like obesity 16 and gestational diabetes, 17–19 may be risk factors for the occurrence of hypertension in pregnancy.”
Maghbooli, Z., Hossein‐Nezhad, A., Mirzaei, K., Karimi, F., Besharati, A., Omidfar, K., & Larijani, B. A. (2009) · Reproductive Sciences · doi:10.1177/1933719109351097 · Cited by 39
“In recent experiment, stimulation with RBP4 in the wild-type rodent was leaded to insulin resistance and glucose intolerance.21 However, correlation between RBP4 concentrations and insulin resistance remains controversial.22-24 In some study, RBP4 concentrations were elevated in people with obesity, impaired glucose t…”
BackgroundInfluentialKunysz, M., Mora-Janiszewska, O., & Darmochwał-Kolarz, D. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094693 · Cited by 37
“In early gestation, insulin sensitivity increases, promoting the uptake and storage of glucose to meet the energy demands of later pregnancy [11].”
BackgroundThyroid dysfunction during gestation and gestational diabetes mellitus: a complex relationship
Pinto, S., Croce, L., Lea, C., Cosson, E., & Rotondi, M. (2023) · Journal of Endocrinological Investigation · doi:10.1007/s40618-023-02079-3 · Cited by 39
Metadata
- Authors
- Di Cianni, G., Miccoli, R., Volpe, L., Lencioni, C., & Del Prato, S.
- Affiliations
- University of Pisa (IT)
- ORCID
- Miccoli, R.
- Venue
- Diabetes/Metabolism Research and Reviews
- Publisher
- Wiley
- Published
- 2003-07
- Volume
- 19
- Issue
- 4
- Pages
- 259-270
- ISSN
- 1520-7552 (ISSN-L)
- 1520-7560
- OpenAlex
- W2129752055
- Cited by
- 406
- References
- 129
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 26 · 2023: 29 · 2022: 30 · 2021: 44 · 2020: 40 · 2019: 24 · 2018: 26 · 2017: 18 · 2016: 21 · 2015: 14 · 2014: 12 · 2013: 10 · 2012: 12
- FWCI
- 1.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Diabetes/Metabolism Research and Reviews (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Gestational Diabetes Research and Management
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
- Keywords
- gestational diabetes mellitus, intermediary metabolism, pregnancy, glucose homeostasis, insulin resistance, insulin secretion, maternal hyperglycemia, type 2 diabetes risk, metabolic syndrome, maternal and neonatal morbidity, postpartum follow-up
- MeSH terms
- Female, Glucose, Homeostasis, Hormones, Humans, Insulin, Pregnancy, Reference Values, Diabetes, Gestational
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