Adaptation of the cardiovascular system of infants born by mothers with diabetes mellitus
https://doi.org/10.29235/1814-6023-2021-18-1-94-108
Abstract
It is known, that diabetes mellitus has a significant impact on the growth and development of the fetus. Hyperglycemia during pregnancy increases significantly the incidence of congenital malformations, perinatal morbidity and neonatal mortality. Over the past decades has been a steady increase in the prevalence of diabetes mellitus both in the general population and among pregnant women. In this regard, the study of the influence of diabetes mellitus in the mother on the condition of the fetus and newborn is today a relevant problem of obstetric-gynecological, neonatological and pediatric services. Hyperglycemia during pregnancy has the greatest effect on the fetal cardiovascular system. Diabetes mellitus of the mother causes an increase in the frequency of congenital heart defects in the newborn, myocardial hypertrophy, as well as various functional disorders of the cardiovascular system.
This review mainly discusses the pathogenetic aspects and molecular mechanisms of the effect of hyperglycemia on the development of the fetal heart, provides an assessment of clinical, echocardiographic and some laboratory changes in the functioning of the cardiovascular system in newborns from mothers with diabetes mellitus, and also systematizes data on the relationship between maternal diabetes and the risks of cardiovascular disease in their children in the long term.
About the Authors
V. A. PrylutskayaBelarus
Verаnika A. Prylutskaya – Ph. D. (Med.), Associate Professor
83, Dzerzhinski Ave., 220116, Minsk, Republic of Belarus
A. V. Sukalo
Belarus
Alexander V. Sukalo – Academician, D. Sc. (Med.), Professor, Head of the Department
83, Dzerzhinski Ave., 220116, Minsk, Republic of Belarus
T. A. Derkach
Belarus
Tatsiana A. Dzerkach – Сlinical resident
83, Dzerzhinski Ave., 220116, Minsk, Republic of Belarus
References
1. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care, 2014, vol. 37, suppl. 1, рр. 81–90. https://doi.org/10.2337/dc14-S081
2. Jones L. V. Techniques of monitoring blood glucose during pregnancy for women with pre-existing diabetes. Cochrane Database of Systematic Reviews, 2019. Available at: https://doi.org/10.1002/14651858.CD009613.pub4/ (accessed 18 October 2020).
3. Macintosh М. C. M., Fleming K. M., Bailey J. A., Doyle P., Modder J., Acolet D., Golightly S., Miller A. Perinatal mortality and congenital anomalies in babies of women with type 1 or type 2 diabetes in England, Wales, and Northern Ireland: populationbased study. BMJ, 2006, vol. 333, no. 7560, art. 177. https://doi.org/10.1136/bmj.38856.692986.AE
4. Roglic G. WHO Global report on diabetes: а summary. World Health Organization. Available at: https://www.ijncd.org/text.asp?2016/1/1/3/184853/ (accessed 18 October 2020).
5. Feig D., Hwee J., Shah B. R., Booth G. L., Bierman A. S., LipscombeL. L. Trends in incidence of diabetes in pregnancy and serious perinatal outcomes: a large, population-based study in Ontario, Canada, 1996–2010. Diabetes Care, 2014, vol. 37, no. 6, рр. 1590–1596. https://doi.org/10.2337/dc13-2717
6. Ferrara A. Increasing prevalence of gestational diabetes mellitus: a public health perspective. Diabetes Care, 2007, vol. 30, suppl. 2, рр. S141–S146. https://doi.org/10.2337/dc07-s206
7. Albrecht S. S., Kuklina E. V., Bansil P., Jamieson D. J., Whiteman M. K., Kourtis A. P., Posner S. F., Callaghan W. M. Diabetes trends among delivery hospitalizations in the U. S., 1994–2004. Diabetes Care, 2010, vol. 33, no. 4, рр. 768–773. https://doi.org/10.2337/dc09-1801
8. Guariguata L., Linnenkamp U., Beagley J., Whiting D. R., Cho N. H. Global estimates of the prevalence of hyperglycaemia in pregnancy. Diabetes Research and Clinical Practice, 2014, vol. 103, no. 2, рр. 176–185. https://doi.org/10.1016/j.diabres.2013.11.003
9. Beyerlein A., von Kries R., Hummel M., Schiessl B., Giani G., Icks A. Improvement in pregnancy-related outcomes in the offspring of diabetic mothers in Bavaria, Germany, during 1987–2007. Diabetic Medicine, 2010, vol. 27, no. 12, рр. 1379–1384. https://doi.org/10.1111/j.1464-5491.2010.03109.x
10. Lipscombe L. L., Hux J. E. Trends in diabetes prevalence, incidence, and mortality in Ontario, Canada 1995–2005: a population-based study. Lancet, 2007, vol. 369, no. 9563, рр. 750–756. https://doi.org/10.1016/S0140-6736(07)60361-4
11. Balsells М., García-Patterson A., Gich I., Corcoy R. Maternal and fetal outcome in women with type 2 versus type 1 diabetes mellitus: a systematic review and metaanalysis. Journal of Clinical Endocrinology and Metabolism, 2009, vol. 94, no. 11, рр. 4284–4291. https://doi.org/10.1210/jc.2009-1231
12. Shand A. W., Bell J. C., McElduff A., Morris J., Roberts C. L. Outcomes of pregnancies in women with pre-gestational diabetes mellitus and gestational diabetes mellitus; a population-based study in New South Wales, Australia, 1998–2002. Diabetic Medicine, 2008, vol. 25, no. 6, рр. 708–715. https://doi.org/10.1111/j.1464-5491.2008.02431.x
13. Wren C. Cardiovascular malformations in infants of diabetic mothers. Heart, 2003, vol. 89, no. 10, рр. 1217–1220. https://doi.org/10.1136/heart.89.10.1217
14. Ray J. G., O’Brien T. E., Chan W. S. Preconception care and the risk of congenital anomalies in the offspring of women with diabetes mellitus: a meta-analysis. QJM, 2001, vol. 94, no. 8, рр. 435–444. https://doi.org/10.1093/qjmed/94.8.435
15. Vibeke А., van der Ploeg H. P., Cheung N. W., Huxley R. R., Bauman A. E. Socioeconomic correlation of the increasing trend in prevalence of gestational diabetes in large population of women between 1995–2005. Diabetes Care, 2008, vol. 31, no. 12, рр. 2288–2293. https://doi.org/10.2337/dc08-1038
16. Al-Biltagi М., Tolba O. A., Rowisha M. A., Mahfouz А., Elewa M. A. Speckle tracking and myocardial tissue imaging in infant of diabetic mother with gestational and pregestational diabetes. Pediatric Cardiology, 2015, vol. 36, no. 2, рр. 445–453. https://doi.org/10.1007/s00246-014-10330
17. Pauliks L. B. The effect of pregestational diabetes on fetal heart function. Diabetes Care, 2015, vol. 13, no. 1, рр. 67–74. https://doi.org/10.1586/14779072.2015.988141
18. Gibb А. А., Hill B. G. Metabolic coordination of physiological and pathological cardiac remodeling. Circulation Research, 2018, vol. 123, no. 1, рр. 107–128. https://doi.org/10.1161/CIRCRESAHA.118.312017
19. Maillet M., van Berlo J. H., Molkentin J. D. Molecular basis of physiological heart growth: fundamental concepts and new players. Nature Reviews Molecular Cell Biology, 2013, vol. 14, no. 1, рр. 38–48. https://doi.org/10.1038/nrm3495
20. Young M. E., McNulty P., Taegtmeyer H. Adaptation and maladaptation of the heart in diabetes: part II: potential mechanisms. Circulation, 2002, vol. 105, no. 15, рр. 1861–1870. https://doi.org/10.1161/01.cir.0000012467.61045.87
21. Eriksson U. J., Borg L. A. H. Diabetes and embryonic malformations. Role of substrate-induced free-oxygen radical production for dysmorphogenesis in cultured rat embryos. Diabetes, 1993, vol. 42, no. 3, рр. 411–419. https://doi.org/10.2337/diab.42.3.411
22. Kumar S. D., Dheen S. T., Tay S. S. Maternal diabetes induces congenital heart defects in mice by altering the expression of genes involved in cardiovascular development. Cardiovascular Diabetology, 2007, vol. 6, art. 34. https://doi.org/10.1186/1475-2840-6-34
23. Corrigan N., Brazil D. P., McAuliffe F. Fetal cardiac effects of maternal hyperglycemia during pregnancy. Birth Defects Research. Part A: Clinical and Molecular Teratology, 2009, vol. 85, no. 6, рр. 523–530. https://doi.org/10.1002/bdra.20567
24. Farrar D. Hyperglycemia in pregnancy: prevalence, impact, and management challenges. International Journal of Women’s Health, 2016, vol. 8, рр. 519–527. https://doi.org/10.2147/IJWH.S102117
25. Kulkarni A., Li L., Craft M., Nanda M., Lorenzo J. M., Danford D., Kutty S. Fetal myocardial deformation in maternal diabetes mellitus and obesity. Ultrasound in Obstetrics and Gynecology, 2017, vol. 49, no. 5, рр. 630–636. https://doi.org/10.1002/uog.15971
26. Schulze C., Drosatos K., Goldberg I. J. Lipid use and misuse by the heart. Circulation Research, 2016, vol. 118, no. 11, рр. 1736–1751. https://doi.org/10.1161/circresaha.116.306842
27. Cade W. T., Levy P., Tinius R., Patel M. D., Choudhry S., Holland M. R., Singh G. K., Cahill A. G. Markers of maternal and infant metabolism are associated with ventricular dysfunction in infants of obese women with type 2 diabetes. Pediatric Research, 2017, vol. 82, no. 5, рр. 768–775. https://doi.org/10.1038/pr.2017.140
28. Jensen M. D., Nielsen S. Insulin dose response analysis of free fatty acid kinetics. Metabolism, 2007, vol. 56, no. 1, рр. 68–76. https://doi.org/10.1016/j.metabol.2006.08.022
29. Higgins M., Auliffe F. Mc. A review of maternal and fetal growth factors in diabetic pregnancy. Current Diabetes Reviews, 2010, vol. 6, no. 2, рр. 116–125. https://doi.org/10.2174/157339910790909431
30. Paauw N. D., Stegeman R., de Vroede М., Termote J. U. M., Freund M. W., Breur J. M. P. J. Neonatal cardiac hypertrophy: the role of hyperinsulinism – a review of literature. European Journal of Pediatrics, 2020, vol. 179, no. 1, рр. 39–50. https://doi.org/10.1007/s00431-019-03521-6
31. Ullmo S., Vial Y., di Bernardo S., Roth-Kleiner M., Mivelaz Y., Sekarski N., Ruiz J., Meijboom E. J. Pathologic ventricular hypertrophy in the offspring of diabetic mothers: a retrospective study. European Heart Journal, 2007, vol. 28, no. 11, рр. 1319–1325. https://doi.org/10.1093/ eurheartj/ehl416
32. Oberhoffer R., Högel J., Stoz F., Kohne E., Lang D. Cardiac and extracardiac complications in infants of diabetic mothers and their relation to parameters of carbohydrate metabolism. European Journal of Pediatrics, 1997, vol. 156, no. 4, рр. 262–265. https://doi.org/10.1007/s004310050596
33. Russell N. E., Holloway P., Quinn S., Foley M., Kelehan P., McAuliffe F. Cardiomyopathy and cardiomegaly in stillborn infants of diabetic mothers. Pediatric and Developmental Pathology, 2008, vol. 11, no. 1, рр. 10–14. https://doi.org/10.2350/07-05-0277.1
34. Ivashkevich A. B. Characteristics of the state of the cardiovascular system in newborns from mothers with diabetes mellitus. Abstract of Ph. D. diss. Minsk, 2012. 20 p. (in Russian).
35. Lysenko S. N. Features of the formation of diabetic fetopathy: diagnosis and optimization of obstetric tactics. Abstract of Ph. D. diss. Moscow, 2019. 48 p. (in Russian).
36. Sobeih A. A., Sakr M. A., Abolmaaty R. K. Assessment of cardiac diastolic function in infants of diabetic mothers using tissue Doppler echocardiography. Egypt Pediatric Association Gaz, 2020, vol. 68, art. 10. https://doi.org/10.1186/s43054-020-00021-3
37. Zablah J. E., Gruber D., Stoffels G., Cabezas E. G., Hayes D. A. Subclinical decrease in myocardial function in asymptomatic infants of diabetic mothers: a tissue doppler study. Pediatric Cardiology, 2017, vol. 38, no. 4, рр. 801–806. https://doi.org/10.1007/s00246-017-1584-y
38. Al-Biltagi M., Tolba O. A., Rowisha M. A., Mahfouz A., Elewa M. A. Speckle tracking and myocardial tissue imaging in infant of diabetic mother with gestational and pregestational diabetes. Pediatric Cardiology, 2015, vol. 36, no. 2, рр. 445–453. https://doi.org/10.1007/s00246-014-1033-0
39. Kozák-Bárány A., Jokinen E., Kero P., Tuominen J., Rönnemaa T., Välimäki I. Impaired left ventricular diastolic function in newborn infants of mothers with pregestational or gestational diabetes with good glycemic control. Early Human Development, 2004, vol. 77, no. 1–2, рр. 13–22. https://doi.org/10.1016/j.earlhumdev.2003.11.006. PMID: 15113627
40. Korraa A., Ezzat M. H., Bastawy M., Aly H., El-Mazaryand A.-A., El-Aziz L. A. Cardiac troponin I levels and its relation to echocardiographic findings in infants of diabetic mothers. Italian Journal of Pediatrics, 2012, vol. 38, art. 39. https://doi.org/10.1186/1824-7288-38-39
41. De Lemos J. A., McGuire D. K., Drazner M. H. B-type natriuretic peptide in cardiovascular disease. Lancet, 2003, vol. 362, no. 9380, рр. 316–322. https://doi.org/10.1016/S0140-6736(03)13976-1
42. Russell N. E., Higgins M. F., Amaruso M., Foley M., McAuliffe F. M. Troponin T and pro-B-type natriuretic peptide in fetuses of type 1 diabetic mothers. Diabetes Care, 2009, vol. 32, no. 11, рр. 2050–2055. https://doi.org/10.2337/dc09-0552
43. Yu Yongfu, Arah O. A., Liew Z., Cnattingius S., Olsen J., Sørensen H. T. [et al.]. Maternal diabetes during pregnancy and early onset of cardiovascular disease in offspring: population based cohort study with 40 years of follow-up. BMJ, 2019, vol. 367, art. I6398. https://doi.org/10.1136/bmj.l6398
44. Sallam N. A., Palmgren V. A. C., Singh R. D., John C. M., Thompson J. A. Programming of vascular dysfunction in the intrauterine milieu of diabetic pregnancies. International Journal of Molecular Sciences, 2018, vol. 19, no. 11, art. 3665. https://doi.org/10.3390/ijms19113665
45. Dib A., Payen C., Bourreau J., Munier M., Grimaud L., Fajloun Z., Loufrani L., Henrion D., Fassot C. In utero exposure to maternal diabetes is associated with early abnormal vascular structure in offspring. Frontiers in Physiology, 2018, vol. 9, art. 350. https://doi.org/10.3389/fphys.2018.00350
Review
For citations:
Prylutskaya V.A., Sukalo A.V., Derkach T.A. Adaptation of the cardiovascular system of infants born by mothers with diabetes mellitus. Proceedings of the National Academy of Sciences of Belarus, Medical series. 2021;18(1):94-108. (In Russ.) https://doi.org/10.29235/1814-6023-2021-18-1-94-108