Gestational diabetes mellitus as a risk factor for neuropsychiatric pathology in offspring

Abstract

This review article summarizes current ideas about gestational diabetes mellitus as an independent risk factor for long-term neuropsychiatric morbidity in offspring. Herein, we describe the genetic programming patterns of morphofunctional brain development during intrauterine life, which provide the basis for short- and long-term functions of the central nervous system. The results of experimental and clinical studies are presented that explain the pathophysiological mechanisms of the harmful effects on the fetal brain of hyperglycemia, hyperinsulinemia, hyperlepthyremia, oxidative stress, and systemic inflammation in the mother with pregnancy complicated by diabetes mellitus. We also discuss structural brain abnormalities and neuropsychiatric consequences. The article substantiates the need for the prevention of neuropsychiatric diseases in the offspring of women with obesity and other concomitant pathology at the stage of family planning, and at the onset of pregnancy, the expediency of early screening, treatment of gestational diabetes mellitus and neuroprotection in the perinatal period of the child’s life.

Keywords

gestational diabetes mellitus / fetus / brain / neuropsychiatric pathology

References

[1] Wang H, Li N, Chivese T, Werfalli M, et al; IDF Diabetes Atlas Committee Hyperglycaemia in Pregnancy Special Interest Group. IDF Diabetes atlas: estimation of global and regional gestational diabetes mellitus prevalence for 2021 by International Association of Diabetes in Pregnancy Study Group’s Criteria. Diabetes Res Clin Pract. 2022;183. doi: 10.1016/j.diabres.2021.109050

[2] Wang H., Li N., Chivese T., et al; IDF Diabetes Atlas Committee Hyperglycaemia in Pregnancy Special Interest Group. IDF diabetes atlas: estimation of global and regional gestational diabetes mellitus prevalence for 2021 by international association of diabetes in pregnancy study group’s criteria // Diabetes Res Clin Pract. 2022. Vol. 183. doi: 10.1016/j.diabres.2021.109050

[3] Shevtsova GO, Moiseeva KE, Berezkina EN, et al. Some results of the assessment of morbidity of gestation diabetes mellitus. Medicine and health care organization. 2020;4(1):29–34. EDN: WSCZUA

[4] Шевцова О.Г., Моисеева К.Е., Березкина Е.Н., и др. Некоторые результаты оценки заболеваемости гестационным сахарным диабетом // Медицина и организация здравоохранения. 2020. Т. 4, № 1. С. 29–34. EDN: WSCZUA

[5] Epishkina-Minina AA, Khamoshina MB, Grabovsky VM, et al. Gestational diabetes mellitus: current state of the problem. Obstetrics and Gynecology: News, Opinions, Training. 2018;6(S3):23–29. EDN: BTDAXY doi: 10.24411/2303-9698-2018-13903

[6] Епишкина-Минина А.А., Хамошина М.Б., Грабовский В.М., и др. Гестационный сахарный диабет: современное состояние проблемы // Акушерство и гинекология: новости, мнения, обучение. 2018. Т. 6, № S3. C. 23–29. EDN: BTDAXY doi: 10.24411/2303-9698-2018-13903

[7] Rodolaki K, Pergialiotis V, Iakovidou N, et al. The impact of maternal diabetes on the future health and neurodevelopment of the offspring: a review of the evidence. Front Endocrinol. 2023;14. doi: 10.3389/fendo.2023.1125628

[8] Rodolaki K., Pergialiotis V., Iakovidou N., et al. The impact of maternal diabetes on the future health and neurodevelopment of the offspring: a review of the evidence // Front Endocrinol. 2023. Vol. 14. doi: 10.3389/fendo.2023.1125628

[9] Evsyukova II. The impact of maternal obesity and diabetes on fetal brain development (mechanisms and prevention). Journal of Obstetrics and Women’s Diseases. 2020;69(3):33–38. EDN: WPVJWB doi: 10.17816/JOWD69333-38

[10] Евсюкова И.И. Влияние ожирения и сахарного диабета матери на развитие мозга ребенка (механизмы и профилактика) // Журнал акушерства и женских болезней. 2020. Т. 69, № 3. C. 33–38. EDN: WPVJWB doi: 10.17816/JOWD69333-38

[11] Nahum Sacks K, Friger M, Shoham-Vardi I, et al. Prenatal exposure to gestational diabetes mellitus as an independent risk factor for long-term neuropsychiatric morbidity of the offspring. Am J Obstet Gynecol. 2016;215(3):380.e1–380.e3807. doi: 10.1016/j.ajog.2016.03.030

[12] Nahum Sacks K., Friger M., Shoham-Vardi I., et al. Prenatal exposure to gestational diabetes mellitus as an independent risk factor for long-term neuropsychiatric morbidity of the offspring // Am J Obstet Gynecol. 2016. Vol. 215, N. 3. P. 380.e1–380.e3807. doi: 10.1016/j.ajog.2016.03.030

[13] Miroshnik EV, Ryumina II, Orbu AM., et al. The phenotype of a newborn with diabetic fetopathy. Neonatologiya: novosti, mneniya, obuchenie. 2020;8(4):28–32. EDN: OLVBZP doi: 10.33029/2308-2402-2020-8-4-28-32

[14] Мирошник Е.В., Рюмина И.И., Орбу А.М., и др. Фенотип новорожденного с диабетической фетопатией // Неонатология: новости, мнения, обучение. 2020. Т. 8, № 4. С. 28–32. EDN: OLVBZP doi: 10.33029/2308-2402-2020-8-4-28-32

[15] Eletri L, Mitanchez D. How do the different types of maternal diabetes during pregnancy influence offspring outcomes? Nutrients. 2022;14(18):3870. doi: 10.3390/nu14183870

[16] Eletri L., Mitanchez D. How do the different types of maternal diabetes during pregnancy influence offspring outcomes? // Nutrients. 2022. Vol. 14, N. 18. doi: 10.3390/nu14183870

[17] Perna R, Loughan AR, Le J, et al. Gestational diabetes: long-term central nervous system developmental and cognitive sequelae. Appl Neuropsychol Child. 2015;4(3):217–220. doi: 10.1080/21622965.2013.874951

[18] Perna R., Loughan A.R., Le J., et al. Gestational diabetes: long-term central nervous system developmental and cognitive sequelae // Appl Neuropsychol Child. 2015. Vol. 4, N. 3. P. 217–220. doi: 10.1080/21622965.2013.874951

[19] Nomura Y, Marks DJ, Grossman B, et al. Exposure to gestational diabetes mellitus and low socioeconomic status: effects on neurocognitive development and risk of attention-deficit/hyperactivity disorder in offspring. Arch Pediatr Adolesc Med. 2012;166(4):337–343. doi: 10.1001/archpediatrics.2011.784

[20] Nomura Y., Marks D.J., Grossman B. Exposure to gestational diabetes mellitus and low socioeconomic status: effects on neurocognitive development and risk of attention-deficit/hyperactivity disorder in offspring // Arch Pediatr Adoles Med. 2012. Vol. 166, N. 4. P. 337–343. doi: 10.1001/archpediatrics.2011.784

[21] Cai S, Qiu A, Broekman BF, et al. The influence of gestational diabetes on neurodevelopment of children in the first two years of life: a prospective study. PLoS One. 2016;11(9). doi: 10.1371/journal.pone.0162113

[22] Cai S., Qiu A., Broekman B.F., et al. The influence of gestational diabetes on neurodevelopment of children in the first two years of life: a prospective study // PLoS ONE. 2016.Vol. 11, N. 9. doi: 10.1371/journal.pone.0162113

[23] Dionne G, Boivin M, Séguin JR, et al. Gestational diabetes hinders language development in offspring. Pediatrics. 2008;122(5):e1073–e1079. doi: 10.1542/peds.2007-3028

[24] Dionne G., Boivin M., Seguin J.R., et al. Gestational diabetes hinders language development in offspring // Pediatrics. 2008. Vol. 122, N. 5. P. e1073–1079. doi: 10.1542/peds.2007-3028

[25] Nikitina IL, Konoplya IS, Polyanskaya AA, et al. Characterization of psychological and physical development in children of gestation diabetes pregnancies. Medical Council. 2017;(9):14–20. EDN: ZCIRJX doi: 10.21518/2079-701X-2017-9-14-20

[26] Никитина И.Л., Конопля И.С., Полянская А.А., и др. Характеристика физического и психомоторного развития детей, рожденных от матерей с гестационным сахарным диабетом // Медицинский совет. 2017. № 9. C. 14–20. EDN: ZCIRJX doi: 10.21518/2079-701X-2017-9-14-20

[27] Alves JM, Smith A, Chow T, et al. Prenatal exposure to gestational diabetes mellitus is associated with mental health outcomes and physical activity has a modifying role. Res Sq. 2023. doi: 10.21203/rs.3.rs-3290222/v1

[28] Alves J.M., Smith A., Chow T., et al. Prenatal exposure to gestational diabetes mellitus is associated with mental health outcomes and physical activity has a modifying role // Res Square. 2023. Vol. 29. doi: 10.21203/rs.3.rs-3290222/v1

[29] Zhao L, Li X, Liu G, et al. The association of maternal diabetes with attention deficit and hyperactivity disorder in offspring: a meta-analysis. Neuropsychiatr Dis Treat. 2019;15:675–684. doi: 10.2147/NDT.S189200

[30] Zhao L., Li X., Liu G., et al. The association of maternal diabetes with attention deficit and hyperactivity disorder in offspring: a meta-analysis // Neuropsychiatr Dis Treat. 2019. Vol. 15. P. 675–684. doi: 10.2147/NDT.S189200

[31] Schmitt J, Romanos M. Prenatal and perinatal risk factors for attention-deficit/hyperactivity disorder. Arch Pediatr Adolesc Med. 2012;166(11):1074–1075. doi: 10.1001/archpediatrics.2012.1078

[32] Schmitt J., Romanos M. Prenatal and perinatal risk factors for attention-deficit/hyperactivity disorder // Arch Pediatr Adolesc Med. 2012. Vol. 166, N. 11. P. 1074–1075. doi: 10.1001/archpediatrics.2012.1078

[33] Xiang AH, Wang X, Martinez MP, et al. Association of maternal diabetes with autism in offspring. JAMA. 2015;313(14):1425–1434. doi: 10.1001/jama.2015.2707

[34] Xiang A.H., Wang X., Martinez M.P., et al. Association of maternal diabetes with autism in offspring // JAMA. 2015. Vol. 313, N. 14. P. 1425–1434. doi: 10.1001/jama.2015.2707

[35] Wan H, Zhang C, Li H, et al. Association of maternal diabetes with autism spectrum disorders in offspring: a systemic review and meta-analysis. Medicine (Baltimore). 2018;97(2). doi: 10.1097/MD.0000000000009438

[36] Wan H., Zhang C., Li H., et al. Association of maternal diabetes with autism spectrum disorders in offspring // Medicine. 2018. Vol. 97, N. 2. doi: 10.1097/MD.0000000000009438

[37] Cannon M, Jones PB, Murray RM. Obstetric complications and schizophrenia: historical and meta-analytic review. Am J Psychiatry. 2002;159(7):1080–1092. doi: 10.1176/appi.ajp.159.7.1080

[38] Cannon M., Jones P.B., Murray R.M. Obstetric complications and schizophrenia: historical and meta-analytic review // Am J Psychiatry. 2002. Vol. 159, N. 7. P. 1080–1092. doi: 10.1176/appi.ajp.159.7.1080

[39] Van Lieshout RJ, Voruganti LP. Diabetes mellitus during pregnancy and increased risk of schizophrenia in offspring: a review of the evidence and putative mechanisms. J Psychiatry Neurosci. 2008;33(5):395–404.

[40] Van Lieshout R.J., Voruganti L.P. Diabetes mellitus during pregnancy and increased risk of schizophrenia in offspring: a review of the evidence and putative mechanisms // J Psychiatry Neurosci. 2008. Vol. 33, N. 5. P. 395–404.

[41] Nogueira Avelar E Silva R, Yu Y, Liew Z, et al. Associations of maternal diabetes during pregnancy with psychiatric disorders in offspring during the first 4 decades of life in a population-based danish birth cohort. JAMA Netw Open. 2021;4(10). doi: 10.1001/jamanetworkopen.2021.28005

[42] Silva R.N.A., Yu Y., Liew Z., et al. Associations of maternal diabetes during pregnancy with psychiatric disorders in offspring during the first 4 decades of life in a population-based danish birth cohort // JAMA Netw Open. 2021. Vol. 4, N. 10. doi: 10.1001/jamanetworkopen.2021.28005

[43] Kong L, Nilsson IAK, Brismar K, et al. Associations of different types of maternal diabetes and body mass index with offspring psychiatric disorders. JAMA Netw Open. 2020;3(2). doi: 10.1001/jamanetworkopen.2019.20787

[44] Kong L., Nilsson I.A., Brismar K., et al. Associations of different types of maternal diabetes and body mass index with offspring psychiatric disorders // JAMA Netw Open. 2020. Vol. 3, N. 2. doi: 10.1001/jamanetworkopen.2019.20787

[45] Perrone S, Grassi F, Caporilli C, et al. Brain damage in preterm and full-term neonates: serum biomarkers for the early diagnosis and intervention. Antioxidants (Basel). 2023;12(2):309. doi: 10.3390/antiox12020309

[46] Perrone S., Grassi F., Caporilli C., et al. Brain damage in preterm and full-term neonates: serum biomarkers for the early diagnosis and intervention // Antioxidants (Basel). 2023. Vol. 12, N. 2. P. 309. doi: 10.3390/antiox12020309

[47] Protsenko EV, Vasil’eva ME, Peretyatko LP, et al. Morphological changes in ventricular germinal zone and neocortex of the cerebral hemispheres in human fetuses and newborns on weeks 22–40 of prenatal development. Ontogenesis. 2014;45(5):349–354. EDN: SLIVLF doi: 10.7868/S047514050073

[48] Проценко Е.В., Васильева М.Е., Перетятко Л.П., и др. Морфологические изменения вентрикулярной герминативной зоны и неокортекса больших полушарий головного мозга у плодов человека и новорожденных с 22-й по 40-ю недели пренатального онтогенеза // Онтогенез. 2014. Т. 45, № 5. С. 349–354. EDN: SLIVLF doi: 10.7868/S047514050073

[49] Oka Y, Sato M, Chou SJ. Editorial: the earliest-born cortical neurons as multi-tasking pioneers: expanding roles for subplate neurons in cerebral cortex organization and function, volume II. Front Neuroanat. 2023;17. doi: 10.3389/fnana.2023.1211678

[50] Oka Y., Sato M., Chou S-J. Editorial: the earliest-born cortical neurons as multi-tasking pioneers: expanding roles for subplate neurons in cerebral cortex organization and function, volume II // Front Neuroanat. 2023. Vol. 17. doi: 10.3389/fnana.2023.1211678.

[51] Wilson S, Pietsch M, Cordero-Grande L, et al. Spatiotemporal tissue maturation of thalamocortical pathways in the human fetal brain. Elife. 2023;12. doi: 10.7554/eLife.83727

[52] Wilson S., Pietsch M., Cordero-Grande L., et al. Spatiotemporal tissue maturation of thalamocortical pathways in the human fetal brain // Elife. 2023. Vol.12. doi: 10.7554/eLife.83727

[53] Inder TE, Volpe JJ, Anderson PJ. Defining the neurologic consequences of preterm birth. N Engl J Med. 2023;389(5):441–453. doi: 10.1056/NEJMra2303347

[54] Inder T.E., Volpe J.J., Anderson P.J. Defining the neurologic consequences of preterm birth // N Engl J Med. 2023. Vol. 389, N. 5. P. 441–453. doi: 10.1056/NEJMra2303347

[55] Alhajeri MM, Alkhanjari RR, Hodeify R, et al. Neurotransmitters, neuropeptides and calcium in oocyte maturation and early development. Front Cell Dev Biol. 2022;10. doi: 10.3389/fcell.2022.980219

[56] Alhajeri M.M., Alkhanjari R.R., Hodeify R., et al. Neurotransmitters, neuropeptides and calcium in oocyte maturation and early development // Front Cell Dev Biol. 2022. Vol. 10. doi: 10.3389/fcell.2022.980219

[57] Xing L, Huttner WB. Neurotransmitters as modulators of neural progenitor cell proliferation during mammalian neocortex development. Front Cell Dev Biol. 2020;8:391. doi: 10.3389/fcell.2020.00391

[58] Xing L., Huttner W.B. Neurotransmitters as modulators of neural progenitor cell proliferation during mammalian neocortex development // Front Cell Dev Biol. 2020. Vol. 26, N. 8. P. 391. doi: 10.3389/fcell.2020.00391

[59] Kolk SM, Rakic P. Development of prefrontal cortex. Neuropsychopharmacology. 2022;47(1):41–57. doi: 10.1038/s41386-021-01137-9

[60] Kolk S.M., Rakic P. Development of prefrontal cortex // Neuropsychopharmacology. 2022. Vol. 47, N. 1. P. 41–57. doi: 10.1038/s41386-021-01137-9

[61] Brummelte S, Mc Glanaghy E, Bonnin A, et al. Developmental changes in serotonin signaling: Implications for early brain function, behavior and adaptation. Neuroscience. 2017;342:212–231. doi: 10.1016/j.neuroscience.2016.02.037

[62] Brummelte S., Mc Glanaghy E., Bonnin A., et al. Developmental changes in serotonin signaling: Implications for early brain function, behavior and adaptation // Neuroscience. 2017. Vol. 342. P. 212–231. doi: 10.1016/j.neuroscience.2016.02.037.

[63] Herlenius E, Lagercrantz H. Neurotransmitters and neuromodulators during early human development. Early Hum Dev. 2001;65(1):21–37. doi: 10.1016/s0378-3782(01)00189-x

[64] Herlenius E., Lagercrantz H. Neurotransmitters and neuromodulators during early human development // Early Hum Dev. 2001. Vol. 65, N. 1. P. 21–37. doi: 10.1016/s0378-3782(01)00189-x

[65] Evsyukova II. Molecular mechanisms of the functioning system mother-placenta-fetus in women with obesity and gestational diabetes mellitus. Molekulyarnaya Meditsina (Molecular medicine). 2020;18(1):11–15. EDN: ORKJZD doi: 10.29296/24999490-2020-01-02

[66] Евсюкова И.И. Молекулярные механизмы функционирования системы «мать – плацента – плод» при ожирении и гестационном сахарном диабете // Молекулярная медицина. 2020. Т. 18, № 1. С. 11–15. EDN: ORKJZD doi: 10.29296/24999490-2020-01-02

[67] Carrasco-Wong I, Moller A, Giachini FR, et al. Placental structure in gestational diabetes mellitus. Biochim Biophys Acta Mol Basis Dis. 2020;1866(2). doi: 10.1016/j.bbadis.2019.165535

[68] Carrasco-Wonga I., Mollerb A., Giachinic F.R., et al. Placental structure in gestational diabetes mellitus // Biochim Biophys Acta Mol Basis Dis. 2020.Vol. 1866, N. 2. doi: 10.1016/j.bbadis.2019.165535

[69] Bedell S, Hutson J, de Vrijer B, et al. Effects of maternal obesity and gestational diabetes mellitus on the placenta: current knowledge and targets for therapeutic interventions. Curr Vasc Pharmacol. 2021;19(2):176–192. doi: 10.2174/1570161118666200616144512

[70] Bedell S., Hutson J., de Vrijer B., et al. Effects of maternal obesity and gestational diabetes mellitus on the placenta: current knowledge and targets for therapeutic interventions // Curr Vasc Pharmacol. 2021. Vol. 19, N. 2. P. 176–192. doi: 10.2174/1570161118666200616144512

[71] Xuan DS, Zhao X, Liu YC, et al. Brain development in infants of mothers with gestational diabetes mellitus: a diffusion tensor imaging study. J Comput Assist Tomogr. 2020;44(6):947–952. doi: 10.1097/RCT.0000000000001110

[72] Xuan D-S., Zhao X., Liu Y-C., et al. Brain development in infants of mothers with gestational diabetes mellitus: a diffusion tensor imaging // J Comput Assist Tomogr. 2020. Vol. 44, N. 6. P. 947–952. doi: 10.1097/RCT.0000000000001110

[73] You L, Deng Y, Li D, et al. GLP-1 rescued gestational diabetes mellitus-induced suppression of fetal thalamus development. J Biochem Mol Toxicol. 2023;37(2). doi: 10.1002/jbt.23258

[74] You L., Deng Y., Li D. et al. GLP-1 rescued gestational diabetes mellitus-induced suppression of fetal thalamus development // J Biochem Mol Toxicol. 2023. Vol. 37, N. 2. doi: 10.1002/jbt.23258

[75] Ekin A, Sever B. Changes in fetal intracranial anatomy during maternal pregestational and gestational diabetes. J Obstet Gynaecol Res. 2023;49(2):587–596. doi: 10.1111/jog.15502

[76] Ekin A., Sever B. Changes in fetal intracranial anatomy during maternal pregestational and gestational diabetes // J Obstet Gynaecol Res. 2023. Vol. 49, N. 2. P. 587–596. doi: 10.1111/jog.15502

[77] Ruth Gründahl F, Hammer K, Braun J, et al. Fetal brain development in diabetic pregnancies and normal controls. J Perinat Med. 2018;46(7):797–803. doi: 10.1515/jpm-2017-0341

[78] Gründahl F.R., Hammer K., Braun J., et al. Fetal brain development in diabetic pregnancies and normal controls // J Perinat Med. 2018. Vol. 46, N. 7. P. 797–803. doi: 10.1515/jpm-2017-0341

[79] Jing YH, Song YF, Yao YM, et al. Retardation of fetal dendritic development induced by gestational hyperglycemia is associated with brain insulin/IGF-I signals. Int J Dev Neurosci. 2014;37:15–20. doi: 10.1016/j.ijdevneu.2014.06.004

[80] Jing Y-H., Song Y-F., Yao Y-M., et al. Retardation of fetal dendritic development induced by gestational hyperglycemia is associated with brain insulin/IGF-I signals // Int J Dev Neurosci. 2014. Vol. 37. P. 15–20. doi: 10.1016/j.ijdevneu.2014.06.004

[81] Tinker SC, Gilboa SM, Moore CA, et al. National birth defects prevention study. specific birth defects in pregnancies of women with diabetes: national birth defects prevention study, 1997–2011. Am J Obstet Gynecol. 2020;222(2):176.e1–176.e11. doi: 10.1016/j.ajog.2019.08.028

[82] Tinker S.C., Gilboa S.M., Moore C.A., et al. Specific birth defects in pregnancies of women with diabetes: national birth defects prevention study, 1997–2011 // Am J Obstet Gynecol. 2020. Vol. 222, N 2. P. 176.e1–176.e11. doi: 10.1016/j.ajog.2019.08.028

[83] Cacciatore M, Grasso EA, Tripodi R, et al. Impact of glucose metabolism on the developing brain. Front Endocrinol (Lausanne). 2022;13. doi: 10.3389/fendo.2022.1047545

[84] Cacciatore M., Grasso E.A., Tripodi R., et al. Impact of glucose metabolism on the developing brain // Front Endocrinol. (Lausanne). 2022. Vol. 13. doi: 10.3389/fendo.2022.1047545

[85] Desoye G, Carter AM. Fetoplacental oxygen homeostasis in pregnancies with maternal diabetes mellitus and obesity. Nat Rev Endocrinol. 2022;18(10):593–607. doi: 10.1038/s41574-022-00717-z

[86] Desoye G., Carter A.M. Fetoplacental oxygen homeostasis in pregnancies with maternal diabetes mellitus and obesity // Nat Rev Endocrinol. 2022. Vol. 18, N. 10. P. 593–560. doi: 10.1038/s41574-022-00717-z

[87] Ornoy A, Becker M, Weinstein-Fudim L, et al. Diabetes during pregnancy: a maternal disease complicating the course of pregnancy with long-term deleterious effects on the offspring. A Clinical Review. Int J Mol Sci. 2021;22(6). doi: 10.3390/ijms22062965

[88] Ornoy A., Becker M., Weinstein-Fudim L., et al. Diabetes during pregnancy: a maternal disease complicating the course of pregnancy with long-term deleterious effects on the offspring. a clinical review // Int J Mol Sci. 2021. Vol. 22, N. 6. P. 2965. doi: 10.3390/ijms22062965

[89] Linares-Pineda T, Peña-Montero N, Fragoso-Bargas N, et al. Epigenetic marks associated with gestational diabetes mellitus across two time points during pregnancy. Clin Epigenetics. 2023;15(1):110. doi: 10.1186/s13148-023-01523-8

[90] Linares-Pineda T., Peña-Montero N., Fragoso-Bargas N. Epigenetic marks associated with gestational diabetes mellitus across two time points during pregnancy // Clin Epigen. 2023. Vol. 15, N. 1. P. 110. doi: 10.1186/s13148-023-01523-8

[91] Lehnen H, Zechner U, Haaf T. Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life. Mol Hum Reprod. 2013;19(7):415–422. doi: 10.1093/molehr/gat020

[92] Lehnen H., Zechner U., Haaf T. Epigenetics of gestational diabetes mellitus and offspring health: the time for action is in early stages of life // Mol Hum Reprod. 2013. Vol. 19, N. 7. P. 415–422. doi: 10.1093/molehr/gat020

[93] Hjort L, Novakovic B, Grunnet LG, et al. Diabetes in pregnancy and epigenetic mechanisms-how the first 9 months from conception might affect the child’s epigenome and later risk of disease. Lancet Diabetes Endocrinol. 2019;7(10):796–806. doi: 10.1016/S2213-8587(19)30078-6

[94] Hjort L., Novakovic B., Grunnet L.G., et al. Diabetes in pregnancy and epigenetic mechanisms — how the first 9 months from conception might affect the child’s epigenome and later risk of disease // Lancet Diabetes Endocrinol. 2019. Vol. 7, N. 10. P. 796–806. doi: 10.1016/S2213-8587(19)30078-6

[95] Haertle L, El Hajj N, Dittrich M, et al. Epigenetic signatures of gestational diabetes mellitus on cord blood methylation. Clin Epigenetics. 2017;9:28. doi: 10.1186/s13148-017-0329-3

[96] Haertle L., Hajj N.E., Dittrich M., et al. Epigenetic signatures of gestational diabetes mellitus on cord blood methylation // Clin Epigenetics. 2017. Vol. 27, N. 9. P. 28. doi: 10.1186/s13148-017-0329-3

[97] Sulyok E, Farkas B, Bodis J. Pathomechanisms of prenatally programmed adult diseases. Antioxidants (Basel). 2023;12(7):1354. doi: 10.3390/antiox12071354

[98] Sulyok E., Farkas B., Bodis J. Pathomechanisms of prenatally programmed adult diseases // Antioxidants. 2023. Vol. 12. P. 1354. doi: 10.3390/antiox12071354

[99] Aviel-Shekler K, Hamshawi Y, Sirhan W, et al. Gestational diabetes induces behavioral and brain gene transcription dysregulation in adult offspring. Transl Psychiatry. 2020;10(1):412. doi: 10.1038/s41398-020-01096-7

[100] Aviel-Shekler K., Hamshawi Y., Sirhan W., et al. Gestational diabetes induces behavioral and brain gene transcription dysregulation in adult offspring // Transl Psychiatry. 2020. Vol. 10, N. 1. P. 412. doi: 10.1038/s41398-020-01096-7

[101] Howe CG, Cox B, Fore R, et al. Maternal gestational diabetes mellitus and newborn dna methylation: findings from the pregnancy and childhood epigenetics consortium. Diabetes Care. 2020;43(1):98–105. doi: 10.2337/dc19-0524

[102] Howe C.G., Cox B., Fore R. et al. Maternal gestational diabetes mellitus and newborn DNA methylation: findings from the pregnancy and childhood epigenetics consortium // Diabetes Care. 2020. Vol. 43, N. 1. P. 98–105. doi: 10.2337/dc19-0524

[103] Camuso S, La Rosa P, Fiorenza MT, et al. Pleiotropic effects of BDNF on the cerebellum and hippocampus: Implications for neurodevelopmental disorders. Neurobiol Dis. 2022;163. doi: 10.1016/j.nbd.2021.105606

[104] Camuso S., La Rosa P., Fiorenza M.T., et al. Pleiotropic effects of BDNF on the cerebellum and hippocampus: implications for neurodevelopmental disorders // Neurobiol Dis. 2022. Vol. 163. doi: 10.1016/j.nbd.2021.105606

[105] Sardar R, Hami J, Soleimani M, et al. Maternal diabetes-induced alterations in the expression of brain-derived neurotrophic factor in the developing rat hippocampus. J Chem Neuroanat. 2021;114. doi: 10.1016/j.jchemneu.2021.101946

[106] Sardar R., Hami J., Soleimani M., et al. Maternal diabetes-induced alterations in the expression of brain-derived neurotrophic factor in the developing rat hippocampus // J Chem Neuroanat. 2021. Vol. 114. doi: 10.1016/j.jchemneu.2021.101946

[107] Briana DD, Papastavrou M, Boutsikou M, et al. Differential expression of cord blood neurotrophins in gestational diabetes: the impact of fetal growth abnormalities. J Matern Fetal Neonatal Med. 2018;31(3):278–283. doi: 10.1080/14767058.2017.1281907

[108] Briana D.D., Papastavrou M., Boutsikou M., et al. Differential expression of cord blood neurotrophins in gestational diabetes: the impact of fetal growth abnormalities // J Maternal-Fetal Neonatal Med. 2018. Vol. 31, N. 3. P. 278–283. doi: 10.1080/14767058.2017.1281907

[109] Piazza FV, Segabinazi E, de Meireles ALF, et al. Severe uncontrolled maternal hyperglycemia induces microsomia and neurodevelopment delay accompanied by apoptosis, cellular survival, and neuroinflammatory deregulation in rat offspring hippocampus. Cell Mol Neurobiol. 2019;39(3):401–414. doi: 10.1007/s10571-019-00658-8

[110] Piazza F.V., Segabinazi E., de Meireles A.L.F., et al. Severe uncontrolled maternal hyperglycemia induces microsomia and neurodevelopment delay accompanied by apoptosis, cellular survival, and neuroinflammatory deregulation in rat offspring hippocampus // Cell Mol Neurobiol. 2019. Vol. 39, N. 3. P. 401–414. doi: 10.1007/s10571-019-00658-8

[111] Han VX, Patel S, Jones HF, et al. Maternal immune activation and neuroinflammation in human neurodevelopmental disorders. Nat Rev Neurol. 2021;17(9):564–579. doi: 10.1038/s41582-021-00530-8

[112] Han V.X., Patel S., Jones H.F., et al. Maternal immune activation and neuroinflammation in human neurodevelopmental disorders // Nat Rev Neurol. 2021. Vol. 17, N. 9. P. 564–79. doi: 10.1038/s41582-021-00530-8

[113] Money KM, Barke TL, Serezani A, et al. Gestational diabetes exacerbates maternal immune activation effects in the developing brain. Mol Psychiatry. 2018;23(9):1920–1928. doi: 10.1038/mp.2017.191

[114] Money K.M., Barke T.L., Serezani A., et al. Gestational diabetes exacerbates maternal immune activation effects in the developing brain // Mol Psychiatry. 2018. Vol. 23, N. 9. P. 1920–1908. doi: 10.1038/mp.2017.191

[115] De Sousa RAL. Animal models of gestational diabetes: characteristics and consequences to the brain and behavior of the offspring. Metab Brain Dis. 2021;36(2):199–204. doi: 10.1007/s11011-020-00661-9

[116] De Sousa R.A.L. Animal models of gestational diabetes: characteristics and consequences to the brain and behavior of the offspring // Metab Brain Dis. 2021. Vol. 36, N. 2. P. 199–204. doi: 10.1007/s11011-020-00661-9

[117] Feldhaus B, Dietzel ID, Heumann R, et al. Effects of interferon-gamma and tumor necrosis factor-alpha on survival and differentiation of oligodendrocyte progenitors. J Soc Gynecol Investig. 2004;11(2):89–96. doi: 10.1016/j.jsgi.2003.08.004

[118] Feldhaus B., Dietzel I.D., Heumann R., et al. Effects ofinterferon-gamma and tumor necrosis factor-alpha on survival and differentiation of oligodendrocyte progenitors // J Soc Gynecol Invest. 2004. Vol. 11, N. 2. P. 89–96. doi: 10.1016/j.jsgi.2003.08.004

[119] Lee TH, Cheng KK, Hoo RL, et al. The novel perspectives of adipokines on brain health. Int J Mol Sci. 2019;20(22):5638. doi: 10.3390/ijms20225638

[120] Lee T.H., Cheng K.K., Hoo R.L., et al. The novel perspectives of adipokines on brain health // Int J Mol Sci. 2019. Vol. 20, N. 22. P. 5638. doi: 10.3390/ijms20225638

[121] Goines PE, Croen LA, Braunschweig D, et al. Increased midgestational IFN-γ, IL-4 and IL-5 in women bearing a child with autism: a case-control study. Mol Autism. 2011;2:13. doi: 10.1186/2040-2392-2-13

[122] Goines P.E., Croen L.A., Braunschweig D., et al. Increased midgestational IFN-gamma, IL-4 and IL-5 in women bearinga child with autism: a case-control study // Mol Autism. 2011. Vol. 2, N. 2. P. 13. doi: 10.1186/2040-2392-2-13

[123] Iwabuchi T, Takahashi N, Nishimura T, et al. Associations among maternal metabolic conditions, cord serum leptin levels, and autistic symptoms in children. Front Psychiatry. 2022;12. doi: 10.3389/fpsyt.2021.816196

[124] Iwabuchi T., Takahashi N., Nishimura T., et al. Associations among maternal metabolic conditions, cord serum leptin levels, and autistic symptoms in children // Front Psychiatry. 2022. Vol. 12. doi: 10.3389/fpsyt.2021.816196

[125] Babacheva E, Rallis D, Christou H, et al. Maternal diabetes and the role of neonatal reticulocyte hemoglobin content as a biomarker of iron status in the perinatal period. Front Endocrinol (Lausanne). 2022;13. doi: 10.3389/fendo.2022.1011897

[126] Babacheva E., Rallis D., Christou H., et al. Maternal diabetes and the role of neonatal reticulocyte hemoglobin content as a biomarker of iron status in the perinatal period // Front Endocrinol. 2022. Vol. 13. doi: 10.3389/fendo.2022.1011897

[127] Georgieff MK. Iron deficiency in pregnancy. Am J Obstet Gynecol. 2020;223(4):516–524. doi: 10.1016/j.ajog.2020.03.006

[128] Georgieff M.K. Iron deficiency in pregnancy // Am J Obstet Gynecol. 2020. Vol. 223, N. 4. P. 516–524. doi: 10.1016/j.ajog.2020.03.006

[129] Tran PV, Carlson ES, Fretham SJ, et al. Early-life iron deficiency anemia alters neurotrophic factor expression and hippocampal neuron differentiation in male rats. J Nutr. 2008;138(12):2495–2501. doi: 10.3945/jn.108.091553

[130] Tran P.V., Carlson E.S., Fretham S.J., et al. Early-life iron deficiency anemia alters neurotrophic factor expression and hippocampal neuron differentiation in male rats // J Nutr. 2008. Vol. 138, N. 12. P. 2495–501. doi: 10.3945/jn.108.091553

[131] He XJ, Dai RX, Tian CQ, et al. Neurodevelopmental outcome at 1 year in offspring of women with gestational diabetes mellitus. Gynecol Endocrinol. 2021;37(1):88–92. doi: 10.1080/09513590.2020.1754785

[132] He X.J., Dai R.X., Tian C.Q., et al. Neurodevelopmental outcome at 1 year in offspring of women with gestational diabetes mellitus // Gynecol Endocrinol. 2021. Vol. 37, N. 1. P. 88–92. doi: 10.1080/09513590.2020.1754785

[133] Devarshi PP, Grant RW, Ikonte CJ, et al. Maternal omega-3 nutrition, placental transfer and fetal brain development in gestational diabetes and preeclampsia. Nutrients. 2019;11(5):1107. doi: 10.3390/nu11051107

[134] Devarshi P.P., Grant R.W., Ikonte C.J., et al. Maternal omega-3 nutrition, placental transfer and fetal brain development in gestational diabetes and preeclampsia // Nutrients. 2019. Vol. 11, N. 5. P. 1107. doi: 10.3390/nu11051107

[135] Hai-Tao Y, Zhi-Heng G, Yi-Ru C, et al. Gestational diabetes mellitus decreased umbilical cord blood polyunsaturated fatty acids: a meta-analysis of observational studies. Prostaglandins Leukot Essent Fatty Acids. 2021;171. doi: 10.1016/j.plefa.2021.102318

[136] Hai-Tao Y., Zhi-Heng G., Yi-Ru C., et al. Gestational diabetes mellitus decreased umbilical cord blood polyunsaturated fatty acids: a meta-analysis of observational studies // Prostaglandins leukot Essen Fatty Acids. 2021. Vol. 171. doi: 10.1016/j.plefa.2021.102318

[137] Elshani B, Kotori V, Daci A. Role of omega-3 polyunsaturated fatty acids in gestational diabetes, maternal and fetal insights: current use and future directions. J Matern Fetal Neonatal Med. 2021;34(1):124–136. doi: 10.1080/14767058.2019.1593361

[138] Elshani B., Kotori V., Daci A. Role of omega-3 polyunsaturated fatty acids in gestational diabetes, maternal and fetal insights: current use and future directions // J Maternal-Fetal Neonatal Med. 2021. Vol. 34, N. 1. P. 124–136. doi: 10.1080/14767058.2019.1593361

[139] Titmuss A, D’Aprano A, Barzi F, et al. Hyperglycemia in pregnancy and developmental outcomes in children at 18-60 months of age: the PANDORA Wave 1 study. J Dev Orig Health Dis. 2022;13(6):695–705. doi: 10.1017/S2040174422000101

[140] Titmuss A., D’Aprano A., Barzi F., et al. Hyperglycemia in pregnancy and developmental outcomes in children at 18–60 months of age: the PANDORA wave 1 study // J Dev Orig Health Dis. 2022. Vol. 13, N. 6. P. 695–705. doi: 10.1017/S2040174422000101

[141] Torres-Espinola FJ, Berglund SK, García-Valdés LM, et al. Maternal obesity, overweight and gestational diabetes affect the offspring neurodevelopment at 6 and 18 months of age--a follow up from the PREOBE cohort. PLoS One. 2015;10(7). doi: 10.1371/journal.pone.0133010

[142] Torres-Espinola F.J., Berglund S.K., García-Valdés L.M., et al. Maternal obesity, overweight and gestational diabetes affect the offspring neurodevelopment at 6 and 18 months of age – a follow up from the PREOBE cohort // PloS One. 2015. Vol. 10, N. 7. doi: 10.1371/journal.pone.0133010

[143] Lackovic M., Milicic B., Mihajlovic S., et al. Gestational diabetes and risk assessment of adverse perinatal outcomes and newborns early motoric development. Medicina (Kaunas Lithuania). 2021;57(8):741. doi: 10.3390/medicina57080741

[144] Lackovic M., Milicic B., Mihajlovic S., et al. Gestational diabetes and risk assessment of adverse perinatal outcomes and newborns early motoric development // Medicina (Kaunas Lithuania). 2021. Vol. 57, N. 8. P. 741. doi: 10.3390/medicina57080741

[145] Arabiat D, Al Jabery M, Jenkins M, et al. Language abilities in children born to mothers diagnosed with diabetes: a systematic review and meta-analysis. Early Hum Dev. 2021;159. doi: 10.1016/j.earlhumdev.2021.105420

[146] Arabiat D., Al Jabery M., Jenkins M., et al. Language abilities in children born to mothers diagnosed with diabetes: a systematic review and meta-analysis // Early Hum Dev. 2021. Vol. 159. doi: 10.1016/j.earlhumdev.2021.105420

[147] Rowland J, Wilson CA. The association between gestational diabetes and ASD and ADHD: a systematic review and meta-analysis. Sci Rep. 2021;11(1):5136. doi: 10.1038/s41598-021-84573-3

[148] Rowland J., Wilson C.A. The association between gestational diabetes and ASD and ADHD: a systematic review and meta-analysis // Sci Rep. 2021. Vol. 11, N. 1. P. 5136. doi: 10.1038/s41598-021-84573-3

[149] Lin CH, Lin WD, Chou IC, et al. Infants of mothers with diabetes and subsequent attention deficit hyperactivity disorder: a retrospective cohort study. Front Pediatr. 2019;7:452. doi: 10.3389/fped.2019.00452

[150] Lin C.H., Lin W.D., Chou I.C., et al. Infants of mothers with diabetes and subsequent attention deficit hyperactivity disorder: a retrospective cohort study // Front Pediatr. 2019. Vol. 7. P. 452. doi: 10.3389/fped.2019.00452

[151] Lawrence RL, Wall CR, Bloomfield FH. Prevalence of gestational diabetes according to commonly used data sources: an observational study. BMC Pregnancy Childbirth. 2019;19(1):349. doi: 10.1186/s12884-019-2521-2

[152] Lawrence R.L., Wall C.R., Bloomfield F.H. Prevalence of gestational diabetes according to commonly used data sources: an observational study // BMC Pregnancy Childbirth. 2019. Vol. 19, N. 1. P. 349. doi: 10.1186/s12884-019-2521-2

[153] Evsyukova II. Maternal circadian rhythm and its implications for offspring health. Journal of Obstetrics and Women’s Diseases. 2022;71(4):95–105. EDN: RSKRUY doi: 10.17816/JOWD108049.

[154] Евсюкова И.И. Циркадный ритм матери и его значение для здоровья потомства // Журнал акушерства и женских болезней. 2022. Т. 71, № 4. С. 95–105. EDN: RSKRUY doi: 10.17816/JOWD108049

[155] Häusler S, Robertson NJ, Golhen K, et al. Melatonin as a therapy for preterm brain injury: what is the evidence? Antioxidants (Basel). 2023;12(8):1630. doi: 10.3390/antiox12081630

[156] Häusler S., Robertson N.J., Golhen K., et al. Melatonin as a therapy for preterm brain injury: what is the evidence? // Antioxidants. 2023. Vol. 12, N. 8. P. 1630. doi: 10.3390/antiox12081630

RIGHTS & PERMISSIONS

Eсо-Vector