Download PDF
Exp Clin Endocrinol Diabetes 2020; 128(12): 788-795
DOI: 10.1055/a-0824-6362
Article

Ultrasonographic Evaluation of Glycemic Control Effect on Placental Vascularization in Pregnancy with Type 1 Diabetes Mellitus

Zoltan Kozinszky
1   Department of Obstetrics and Gynecology, Blekinge Hospital, Karlskrona, Sweden
,
AbelT. Altorjay
2   Department of Obstetrics and Gynecology, University of Szeged, Szeged, Hungary
,
Andras Molnar
2   Department of Obstetrics and Gynecology, University of Szeged, Szeged, Hungary
,
Tibor Nyári
3   Department of Medical Physics and Informatics, University of Szeged, Szeged, Hungary
,
Sandor G. Vari
4   International Research and Innovation in Medicine Program, Cedars - Sinai Medical Center, Los Angeles, CA, USA
,
Gabor Nemeth
2   Department of Obstetrics and Gynecology, University of Szeged, Szeged, Hungary
,
Andrea Suranyi
2   Department of Obstetrics and Gynecology, University of Szeged, Szeged, Hungary
› Author Affiliations
› Further Information
Also available at
    Permissions and Reprints

Abstract

Aims The aim of our study was to assess the effect of glycemic control on placental vascularization in pregnancies complicated by type 1 diabetes mellitus (T1DM) and to compare dataset of optimal/suboptimal glycemic control to normal placental 3-dimensional power Doppler (3-DPD) indices in 2nd and 3rd trimester.

Methods Placental vascularization of pregnant women was prospectively evaluated by 3-DPD ((vascularization-index (VI); flow-index (FI); vascularization-flow-index (VFI)) ultrasound technique. The normal pregnancies (n=214) were compared to those complicated by T1DM (n=53) with optimal (HbA1C≤6%;≤ 42 mmol/mol) and suboptimal (HbA1C>6%;>42 mmol/mol) glycemic control.

Results Pregnancies complicated by T1DM expressed lower placental vascularization indices as compared with normal pregnancies (adjusted odds ratio (AOR) for VI:0.86; FI:0.94; VFI:0.76). Placental 3-DPD indices have a significant correlation with HbA1C and optimal glycemic control is associated with lower placental perfusion (AOR for VI:1.64; FI:1.13; VFI:2.34). Short-term adverse neonatal outcome was predicted by lower 3-DPD indices (AORVI:0.83, AORFI:0.93, AORVFI:0.66, p<0.05 for each index). Besides the glycemic control, the pregestational body mass index (BMI), had significant influences on placental perfusion.

Conclusions VI displayed the best screening ability for suboptimal glycemic control with a sensitivity of 90.9%. The suboptimal glycemic control has a direct deteriorating effect on placental vasculature. Therefore the ultrasound examination could be an adjunct diagnostic modality for pregnant women with T1DM.

Key words

glycemic control - placental vascularization - type 1 diabetes mellitus - 3-dimensional power Doppler indices - ultrasound


Publication History

Received: 18 September 2018
Received: 28 November 2018

Accepted: 18 December 2018

Article published online:
14 January 2019

© 2020. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 National Institute for Health and Care Excellenc. Diabetes in pregnancy Management of diabetes and its complications from preconception to the postnatal period. https://www.nice.org.uk/guidance/ng3/evidence/full-guideline-3784285 Accessed 18.08.02
    PubMed
  • 2 Middleton P, Crowther CA, Simmonds L. Different intensities of glycaemic control for pregnant women with pre-existing diabetes. Cochrane Database Syst Rev 2012; 8: CD008540
    PubMedGoogle Scholar
  • 3 Damm P, Mersebach H, Råstam J. et al. Poor pregnancy outcome in women with type 1 diabetes is predicted by elevated HbA1c and spikes of high glucose values in the third trimester. J Matern Fetal Neonatal Med 2014; 27: 149-154
    CrossrefPubMedGoogle Scholar
  • 4 Nielsen GL, Sørensen HT, Nielsen PH. et al. Glycosylated hemoglobin as predictor of adverse foetal outcome in type 1 diabetic pregnancies. Acta Diabetol 1997; 34: 217-222
    CrossrefPubMedGoogle Scholar
  • 5 Kitzmiller JL, Gavin LA, Gin GD. et al. Preconception care of diabetes. Glycemic control prevents congenital anomalies. JAMA 1991; 265: 731-736
    CrossrefPubMedGoogle Scholar
  • 6 American Diabetes Association. Management of diabetes in pregnancy. Diabetes Care 2015; 38 Supplement 1 S77-S79
    CrossrefPubMedGoogle Scholar
  • 7 Kitzmiller JL, Block JM, Brown FM. et al. Managing preexisting diabetes for pregnancy: Summary of evidence and consensus recommendations for care. Diabetes Care. 2008; 31: 1060-1079
    CrossrefPubMedGoogle Scholar
  • 8 Stewart ZA, Wilinska ME, Hartnell S. et al. Closed-loop insulin delivery during pregnancy in women with Type 1 Diabetes. N Engl J Med 2016; 375: 644-654
    CrossrefPubMedGoogle Scholar
  • 9 Skyler JS. Effects of glycemic control on diabetes complications and on the prevention of diabetes. Clin Diabetes 2004; 22: 162-166
    CrossrefPubMedGoogle Scholar
  • 10 Kaaja R. Vascular complications in diabetic pregnancy. Thromb Res 2011; 127 (Suppl. 03) S53-S55
    CrossrefPubMedGoogle Scholar
  • 11 Hirsch IB. Glycemic variability and diabetes complications: Does it matter? Of course it does!. Diabetes Care. 2015; 38: 1610-1614
    CrossrefPubMedGoogle Scholar
  • 12 Sommerfield AJ, Wilkinson IB, Webb DJ. et al. Vessel wall stiffness in type 1 diabetes and the central hemodynamic effects of acute hypoglycemia. Am J Physiol Endocrinol Metab 2007; 293: E1274-E1279
    CrossrefPubMedGoogle Scholar
  • 13 Zawiejska A, Wender-Ozegowska E, Brazert J. Microvascular complications are associated with low levels of maternal sE-selectin and sVCAM-1 in pregnancy complicated with pregestational diabetes mellitus. Diabetes Res Clin Pract 2010; 88: 164-170
    CrossrefPubMedGoogle Scholar
  • 14 Olszewska-Pazdrak B, Hein TW, Olszewska P. et al. Chronic hypoxia attenuates VEGF signaling and angiogenic responses by downregulation of KDR in human endothelial cells. Am J Physiol Cell Physiol 2009; 296: C1162-C1170
    CrossrefPubMedGoogle Scholar
  • 15 Mayhew TM. Enhanced fetoplacental angiogenesis in pre-gestational diabetes mellitus: the extra growth is exclusively longitudinal and not accompanied by microvascular remodelling. Diabetologia 2002; 45: 1434-1439
    CrossrefPubMedGoogle Scholar
  • 16 Boyd PA, Scott A, Keeling JW. Quantitative structural studies on placentas from pregnancies complicated by diabetes mellitus. Br J Obstet Gynaecol 1986; 93: 31-35
    CrossrefPubMedGoogle Scholar
  • 17 Nelson SM, Sattar N, Freeman DJ. et al. Inflammation and endothelial activation is evident at birth in offspring of mothers with type 1 diabetes. Diabetes 2007; 56: 2697-270
    CrossrefPubMedGoogle Scholar
  • 18 Higgins M, Felle P, Mooney EE. et al. Stereology of the placenta in type 1 and type 2 diabetes. Placenta 2011; 32: 564-569
    CrossrefPubMedGoogle Scholar
  • 19 Jirkovská M, Kucera T, Kaláb J. et al. The branching pattern of villous capillaries and structural changes of placental terminal villi in type 1 diabetes mellitus. Placenta 2012; 33: 343-351
    CrossrefPubMedGoogle Scholar
  • 20 Surányi A, Kozinszky Z, Molnár A. et al. Placental three-dimensional power Doppler indices in mid and late pregnancy complicated by gestational diabetes mellitus. Prenat Diagn 2013; 33: 952-958
    CrossrefPubMedGoogle Scholar
  • 21 Rizzo G, Capponi A, Pietrolucci ME. et al. First trimester placental volume and three dimensional power doppler ultrasonography in type I diabetic pregnancies. Prenat Diagn 2012; 32: 480-484
    CrossrefPubMedGoogle Scholar
  • 22 Gonzalez Gonzalez NL, Gonzalez Davila E, Castro A. et al. Effect of pregestational diabetes mellitus on first trimester placental characteristics: Three-dimensional placental volume and power Doppler indices. Placenta 2014; 35: 147-151
    CrossrefPubMedGoogle Scholar
  • 23 Mercé LT, Barco MJ, Bau S. Reproducibility of the study of placental vascularization by three-dimensional power Doppler. J Perinat Med 2004; 32: 228-233
    CrossrefPubMedGoogle Scholar
  • 24 Mercé LT, Barco MJ, Bau S. et al. Assessment of placental vascularisation by three-dimensional power Doppler “vascular biopsy” in normal pregnancies. Croat Med J 2005; 46: 765-771
    PubMedGoogle Scholar
  • 25 Tuuli MG, Houser M, Odibo L. et al. Validation of placental vascular sonobiopsy for obtaining representative placental vascular indices by three-dimensional power Doppler ultrasonography. Placenta 2010; 31: 192-196
    CrossrefPubMedGoogle Scholar
  • 26 de Paula CF, Ruano R, Campos JA. et al. Quantitative analysis of placental vasculature by three-dimensional power Doppler ultrasonography in normal pregnancies from 12–40 weeks of gestation. Placenta 2009; 30: 142-148
    CrossrefPubMedGoogle Scholar
  • 27 Pretorius DH, Nelson TR, Baergen RN. et al. Imaging of placental vasculature using three-dimensional ultrasound and color power Doppler: A preliminary study. Ultrasound Obstet Gynecol 1998; 12: 45-49
    CrossrefPubMedGoogle Scholar
  • 28 Hungarian Statistical Office: Demographic yearbook. (In Hungarian: Demográfiai évkönyv). Hungarian Statistical Office, Budapest 2011; Hungarian Statistical Office www.ksh.hu Accessed 18.01.02
    PubMed
  • 29 Hiden U, Froehlich J, Desoye G. Diabetes and the Placenta. Kay HH, Nelson DM, Wang Y. (editors) The Placenta: From Development to Disease, From Development to Disease. Wiley-Blackwell; Oxford, UK: 2011. Part I. (Chapter 30.) pp 228-230
    CrossrefGoogle Scholar
  • 30 Rampersad R, Cervar-Zivkovic M, Nelson MD. Development and anatomy of the human placenta. Kay HH, Nelson DM, Wang Y. (editors) The Placenta: From Development to Disease. Wiley-Blackwell; Oxford, UK: 2011. Part II. (Chapter 3.) pp 19-26
    Google Scholar
  • 31 HAPO Study Cooperative Research Group. Metzger BE, Lowe LP, Dyer AR. et al. Hyperglycemia and adverse pregnancy outcomes. N Engl J Med 2008; 358: 1991-2002
    Google Scholar
  • 32 Leach L. Placental vascular dysfunction in diabetic pregnancies. Microcirculation 2011; 18: 263-269
    CrossrefPubMedGoogle Scholar
  • 33 Saldeen P, Olofsson P, Laurini RN. Structural, functional and circulatory placental changes associated with impaired glucose metabolism. Eur J Obstet Gynecol Reprod Biol 2002; 105: 136-142
    CrossrefPubMedGoogle Scholar
  • 34 Maly A, Goshen G, Sela J. et al. Histomorphometric study of placental villi vascular volume in toxemia and diabetes. Hum Pathol 2005; 36: 1074-1079
    CrossrefPubMedGoogle Scholar
  • 35 Evers IM, Nikkels PG, Sikkema JM. et al. Placental pathology in women with Type 1 Diabetes and in a control group with normal and large-for-gestational-age infants. Placenta 2003; 24: 819-825
    CrossrefPubMedGoogle Scholar
  • 36 Visser GHA, Evers IM, Mello G. Management of macrosomic fetus. Hod H, Jovanovic L, Di Renzo GC, de Leiva A, Langer O. Textbook of Diabetes and Pregnancy. Second Edition CRC Press; USA: 2008. (Chapter 40) pp 304-307
    Google Scholar
  • 37 Reece EA, Sivan E, Francis G. et al. Pregnancy outcomes among women with and without diabetic microvascular disease (White's classes B to FR) versus non-diabetic controls. Am J Perinatol 1998; 15: 549-555
    Article in Thieme ConnectPubMedGoogle Scholar
  • 38 Higgins MF, Russell NM, Mooney EE. et al. Clinical and ultrasound features of placental maturation in pre-gestational diabetic pregnancy. Early Hum Dev 2012; 88: 817-821
    CrossrefPubMedGoogle Scholar