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Role of Ultrasonography in Pregnancies Complicated by Gestational Diabetes

A Review

Sinno, Sara S. Hamze; Nassar, Anwar H.*

Section Editor(s): Pan, Yang; Shi, Dan-Dan

doi: 10.1097/FM9.0000000000000013
Review
Open

This review is to better clarify the role of ultrasonography during pregnancies complicated with gestational diabetes mellitus (GDM). It will focus on the effect of GDM on pregnancy, and the use of ultrasound modality to estimate fetal size and accordingly the mode of delivery. It will also shed light on how this technology can be used to improve our understanding of the pathophysiology of this diagnosis and hopefully improve the maternal-fetal outcome.

Department of Obstetrics and Gynecology, American University of Beirut Medical Center, Beirut 1107 2020, Lebanon.

Corresponding author: Prof. Anwar H. Nassar, Department of Obstetrics and Gynecology, American University of Beirut Medical Center, P.O. Box: 113-6044/B36, Beirut 1107 2020, Lebanon. E-mail: an21@aub.edu.lb

Received April 4, 2019

Online date: October 15, 2019

This is an open access article distributed under the terms of the Creative Commons Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal. http://creativecommons.org/licenses/by-nc-nd/4.0

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Introduction

Diabetes is one of the most common diseases that can have debilitating complications if not managed promptly especially in the context of the pregnancy. It was estimated by Wier et al., that around 6% of the pregnancies in the United States are affected by gestational diabetes mellitus (GDM).1 One of the physiologic changes in pregnancy is associated with proliferation of the beta cell of the pancreas that leads to a surge of insulin in fasting and postprandial states; however, in the last trimester the placenta secretes hormones that increase insulin resistance.2 Therefore, gestational diabetes is a state of glucose intolerance where beta cells during pregnancy cannot compensate for the insulin resistance.2 This state can compromise maternal-fetal outcome and increase the risk of complications during the pregnancy.3 Women, previously known to have GDM, are at a higher risk of developing it in subsequent pregnancies and even type 2 diabetes mellitus later in life.4–6 According to American College of Obstetricians and Gynecologists (ACOG), U.S. Preventive Services Task Force recommends GDM screening at or after 24 weeks of gestation (level B evidence) using the 50g nonfasting glucose challenge test, while women at increased risk of diabetes (family history of diabetes mellitus, ethnicity, and hypertension) are to be tested at the first antenatal visit.7 GDM is diagnosed by oral glucose tolerance test (OGTT) a 100 g fasting test for those with positive screening (>130–140 mg/dL).8 Another screening method is a one-step 75 g 2-hour fasting OGTT.8

Due to the increased risk of complications that may arise from GDM, that can range from hypertension to fetal growth changes, ultrasonography has been used to guide the management of GDM. In this review, the objective is to understand the importance of ultrasonography and its contribution in understanding and managing GDM.

Ultrasonography can be utilized to:

  • Monitor fetal growth and predict estimated fetal weight in pregnancies complicated with GDM.
  • Detect congenital abnormalities.
  • Monitor placental changes and possibly predict GDM at early stages of pregnancy.
  • Decide on the mode of delivery to avoid potential delivery complications as a result of GDM.
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Role in monitoring fetal growth

The use of ultrasonography in pregnancies complicated with GDM can vary according to clinical practice. Actually, it was suggested by ACOG that obstetricians usually begin fetal surveillance in females who require pharmacologic intervention to control GDM or have uncontrolled GDM at week 32 of gestation.7 However, this timing varies with presence of different factors that can increase risk of adverse pregnancy outcomes.7 In 2013, ACOG recommended antenatal follow up according to the local pattern of practice.9 Follow-up can include “twice weekly non-stress tests or weekly modified biophysical profiles starting 32–34 weeks of gestation”.9 Usually, one of the feared complications is fetal macrosomia due to the state of induced hyperinsulinemia in the fetus. Fetal macrosomia is commonly defined as more than or equal to 4000 g,10 or an estimated weight exceeding the 90th percentile in females with GDM.11 It is associated with increased risk for shoulder dystocia, brachial plexus injury, and trauma to the perineal area.12 Therefore, physicians monitor fetal growth sonographically starting 32–34 weeks of gestation. A strict guide for the routine surveillance in pregnancies complicated by GDM is not available due to the lack of large studies that correlate accelerated fetal growth with incidence of large for gestational age infants (LGA).13 The most commonly used parameters to estimate fetal weight are the measurement of the head circumference, biparietal diameter, abdominal circumference, and femur length.14 Additionally, the difference between estimated fetal weight and the actual weight is accentuated in pregnancies complicated with diabetes. The latter tends to affect the fat distribution in the fetus in an asymmetrical manner affecting mostly the abdominal girth.14 In a retrospective cohort study by Scifres et al., it was found that among women with ultrasound diagnosis of LGA fetuses, only 56 of 248 (22.6%) delivered LGA neonates.15 Therefore, it was found that ultrasonography significantly overestimated LGA in pregnancies complicated with GDM. In addition, it was noted that the diagnosis of LGA was associated with increased cesarean deliveries irrespective of the actual fetal weight.15

For better estimation of fetal birth weight, Liu et al. suggested to use fetal hemodynamic indices in late pregnancy to predict fetal birth weight in pregnancies complicated by GDM.16 The study included 271 pregnant women, 147 of whom had GDM and 124 controls. Fetal hemodynamic indices used in this study included systolic/diastolic (S/D) ratio, resistance index (RI) , pulsatility index (PI) of the umbilical artery (UA), middle cerebral artery (MCA), and renal artery using color Doppler ultrasonography.16 The indices in the two groups of women were compared at an average gestational age of 38 weeks and were found to be significantly different (P < 0.05).16 It was observed that pregnant women with GDM had lower UA and MCA indices than the control, but higher renal artery indices. Also, a negative correlation was found between UA and MCA with birth weight, head circumference, and abdominal circumference. This suggests that these indices can play an important role in estimating birth weight and avoiding respective complications arising from macrosomia.16

Additionally, in a prospective study done on 331 pregnant women who had their fetal liver length (FLL) measured by ultrasonography at 23 weeks of gestation followed by 100 g OGTT, it was found that FLL is correlated with the result of OGTT at 24 weeks of gestation.17 Accordingly, it was suggested that FLL can be used to detect GDM in women with high-risk profile.17 However, the best earliest time to predict the risk of diabetes is still unclear since follow up is one of the limitations in this study.

As a result, it can be concluded that the role ultrasonography in estimating fetal weight lies mostly in excluding the diagnosis of macrosomia that can help rule out maternal complications during delivery.14 Over diagnosis of fetal macrosomia by ultrasonography can actually increase the incidence of unnecessary cesarean deliveries and labor abnormalities independent of the actual weight. On that note, ultrasound-derived fetal weight estimates alone are not enough to decide the mode of delivery. It requires a full clinical assessment of the pelvic structure, pre-existing risk factors for macrosomia in addition to sonographic findings to reach a decision on how to manage the delivery and monitor the fetal growth.18

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Detecting congenital abnormalities

It is well established that pregestational diabetes (PGDM) is associated with increased risk of congenital malformations.19 It was found that in diabetic pregnancies, the rate of significant congenital malformations ranges between 6%–10%.20 However, in a meta-analysis of 21 cohort studies, it was found that GDM and PGDM may be associated with increased major congenital malformations [relative risks (RR): 2.44 and RR:1.11, respectively].21 It was noted that there is only a slight increase in the risk of congenital anomalies in women with GDM and a much higher risk in PGDM.21 GDM can affect any of the systems but most common malformations are those affecting the cardiovascular and nervous system.22

Ultrasonography as early as 11–14 weeks of gestation, can allow identification of some congenital malformation.23 Detection of other malformations might need to be confirmed later at 20–22 weeks of gestation.23 There are new advanced imaging techniques such as tissue harmonic imaging and targeted echocardiography that provide higher resolution than routine ultrasonography to allow more accurate diagnosis.24,25 Fetal ultrasonography can also guide physicians to check the need for early pharmacologic intervention to control maternal hyperglycemia.26

Congenital heart diseases are responsible for around 50% of perinatal mortality and morbidity. The detection rate for congenital heart diseases ranges between 35% and 86%.27 This rate is attributed to the heart activity and consequent difficulty in obtaining the proper views.28 Different modalities are present to detect various cardiac fetal anomalies. One of the modalities used is the four-chamber view for screening congenital abnormalities. However, Chaoui explained that four-chamber view ultrasonography performs poorly and can miss fetal anomalies. He suggested fetal echocardiography to be performed in order to improve diagnostic accuracy especially in regard to screening for outflow tract abnormalities.29 This was also supported by Albert et al., who proposed that fetal echocardiography has higher accuracy for cardiac malformations than four-chamber view ultrasonography (92% vs. 33%).20 Another technique that can be used to detect congenital cardiac abnormality is three-dimensional and four-dimensional based spatial-temporal imaging correlation in fetal echocardiography which is based on creating adequate volume to allow the assessment of the fetal heart from four-chamber view level to the aortic outflow and pulmonary tract.19,30 However, despite the outflow tract examination, it was found by DeVore et al. that only 13.7% of heart defects were detected in over 92,000 pregnancies.19

As for neural tube defects, they are more likely to occur in diabetic pregnancy (incidence of 20/1000) compared with general population (2/1000) with anencephaly and caudal regression syndrome being the most common associations.23 These anomalies are usually detected accurately early in pregnancy during the end of first trimester and beginning of the second.19

Further studies are still required to assess the direct correlation of between PGDM and congenital fetal anomalies to understand the effect of hyperglycemia on fetal embryopathy. However, ultrasonography can potentially allow early diagnosis of these abnormalities and thus affect the course of management of the complicated pregnancy.23

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Monitoring placental changes

GDM has been suggested to be associated with increased risk of maternal and fetal complications. Also, placental changes in pregnancy can predict possible complications.31 In a case-control study among 39 singleton pregnancies, placental volume was found to be inversely correlated with UA PI, RI, and S/D ratio.32 In addition, the placental volume significantly increases in pregnancies with GDM. However, a main limitation to this study is the small sample size.32 On the contrary, a similarly small case-control study including 28 women has shown a correlation between maternal diabetes and increased terminal villous volume along with the length of the capillaries without effect on the placental volume.33 This conclusion supports the thought that placental development tells us more about how healthy a pregnancy course is. As suggested by Edu et al., the enlarged placental size on ultrasonography during weeks 24–28 of gestation may be potentially utilized to predict and support the necessity to screen for GDM, even though other maternal factors can affect the placental changes occurring.34

A new insight on the use of ultrasonography to study placental changes was addressed in a quite recent prospective control study of 155 women that compared the changes in vascular indices in first and second trimester in pregnancies complicated with GDM.35 It concluded that placental vascular indices calculated using Doppler ultrasonography early in pregnancy (first trimester) can actually give an insight to the possibility of developing GDM.35 In this study, placental vascular indices including, vascularization index (VI), flow index (FI), vascularization flow index (VFI) in addition to placental volume and uterine artery PI were obtained during the first and second trimesters using Virtual Organ Computer-aided Analysis imaging software.35 The study suggested that changes in VI and VFI, at as early as first and second trimester, occurs before clinical diagnosis. It showed that VI and VFI, unlike FI and uterine PI that showed no difference from controls, were significantly lower in patients with GDM during that period of time in pregnancy.35 This conclusion is supported by Desoye et al., who suggested that the placentae in diabetic pregnancies have increased levels of thromboxane and tumor necrosis factor alfa leading to vasoconstriction that can explain the decrease in VI and VFI.36 As for FI, it remains relatively unchanged between both groups since it does not represent the amount of vascularization but rather the power of the flow.37

This new theory suggests that three-dimensional Doppler ultrasonography can be used early in pregnancy to predict the possibility of developing GDM by understanding placental vascularization early in pregnancy instead of emphasizing on placental volume as previously suggested in the literature.36 This conclusion may allow better management, earlier intervention, and eventually improved pregnancy outcomes.

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Predicting pregnancy outcomes

Diagnosis of GDM and the proper management of the condition can decrease the risk of maternal-fetal complications. As the glucose crosses to the fetus from a mother with GDM, it induces a state of fetal hyperinsulinism which contributes to fetal macrosomia.38 Despite this proposed pathophysiology, it was found that such increased birth weight in pregnancies complicated with gestational diabetes was actually low (1.1%) in a cohort of 1344 women with GDM.39 Fetal macrosomia significantly increases the risk of fetal death and maternal obstetrical complications including trauma during the delivery, shoulder dystocia, and asphyxia with difficult delivery in addition to an increased risk of cesarean deliveries.10 The role of ultrasonography in monitoring fetal weight and improving pregnancy outcome has been addressed, but still requires further improvement to detect LGA fetus.40

In pregnancies that are not complicated with GDM, it was found that the risk for cesarean delivery was positively correlated with having an ultrasound-based estimated fetal weight.41 On another hand, in pregnancies complicated with GDM, the effect of ultrasonographic diagnosis on mode of delivery remains unclear. In a retrospective cohort study by Little et al., women with ultrasound-estimated fetal weight 1 month before delivery were 44% more likely to be delivered by cesarean section.13

This was supported by a more recent retrospective cohort study conducted by Scifres et al., of 248 women with LGA fetus and 655 women with a non-LGA fetus, ultrasonography was associated with increased risk for cesarean deliveries independent of birth weight [odds ratio (OR): 3.13, confidence interval (CI): 2.10–4.67 with P < 0.001] even after excluding potentially confounding factors including body mass index, category, race, hypertensive disorders of pregnancy, chronic hypertension, and nulliparity.15 Ultrasonography can significantly overestimate the fetal weight and thus allows for falsely categorized LGA fetus.15 A diagnosis of LGA via ultrasonography was associated with tripling the risk of cesarean delivery15 Therefore, “ultrasound estimated fetal weight near term represents a modifiable risk factor that physicians can target.”13

The rate of cesarean deliveries has been increasing significantly in the past few years to reach 32.3% in the United States.42 However, it should be noted that ultrasonography detects estimated fetal weight with up to 10% inaccuracy.43

One of the feared complications of macrosomia or LGA fetuses is shoulder dystocia and can reach up to 10% in diabetic mothers.44 As previously described, the higher rates of shoulder dystocia witnessed in fetuses of diabetic mothers can be attributed to the asymmetrical fat redistribution in these fetuses. In a prospective study by Conway et al., diabetic pregnant females having ultrasound-estimated fetal weight more than 4.25 kg or exceeding 90th percentile but less than 4.25 kg at 37–38 weeks of gestation underwent induction of labor or elective cesarean delivery, respectively.41 As a result, there was an associated decrease in the risk of shoulder dystocia complication when these ultrasonographic cut-offs were used as an indication for elective delivery.44 However, shoulder dystocia can still occur in neonates with birth weight <4000 g showing that ultrasonography cannot fully detect those at risk of this complication.15 Therefore, the use of ultrasonography as a tool to avoid complications like shoulder dystocia is still controversial especially with the overestimation of fetal weight in sonographic measurements.

Future studies are required to categorize pregnancies complicated with GDM as low risk for macrosomia or LGA where routine ultrasonographic follow up will dictate unnecessary measures that outweigh the benefit. Until then, proper patient counseling is recommended in the context of over diagnosing macrosomia or LGA in pregnancies with GDM and its associated increased risk of cesarean delivery and respective maternal morbidities.

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Conclusions

The prevalence of GDM has been increasing over the past decade.45 Screening of GDM is usually conducted at around 24 weeks of gestation and is necessary to manage the condition to avoid further maternal-fetal complications. The role of ultrasonography in monitoring patients with GDM remains controversial. It allows physicians to estimate the fetal weight and growth which can offer physicians the ability to choose the favorable method of delivery, whether induction or cesarean delivery. Keeping in mind that ultrasonography can overestimate the fetal weight and might increase risk of cesarean delivery in current and future pregnancies, patients should be counseled about the inaccuracy and the risk of its repercussions.41 Ultrasonography can, potentially, detect developmental abnormalities and placental changes early in pregnancy allowing physicians to predict possibility of developing gestational diabetes ahead of time and allow better management and early course of action to avoid any complications.36

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Funding

None.

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Author Contributions

Sara S. Hamze Sinno conceived the idea and helped with the writing up and editing of the article. Anwar H. Nassar led the preparation of the article, including writing and editing.

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Conflicts of Interest

None.

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References

[1]. Wier LM, Witt E, Burgess J, et al Hospitalizations Related to Diabetes in Pregnancy, 2008: Statistical Brief #102. Healthcare Cost and Utilization Project (HCUP) Statistical Briefs [Internet]. Rockville (MD): Agency for Healthcare Research and Quality (US); 2010.
[2]. Butte NF. Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus. Am J Clin Nutr 2000;71(5 Suppl):1256s–1261s. doi: 10.1093/ajcn/71.5.1256s.
[3]. Kautzky-Willer A, Harreiter J, Bancher-Todesca D, et al Gestational diabetes mellitus. Wien Klin Wochenschr 2016;128(Suppl 2):S103–S112. doi: 10.1007/s00508-015-0941-1.
[4]. Kjos SL, Buchanan TA, Greenspoon JS, et al Gestational diabetes mellitus: the prevalence of glucose intolerance and diabetes mellitus in the first two months post partum. Am J Obstet Gynecol 1990;163(1 Pt 1):93–98. doi: 10.1016/s0002-9378(11)90676-0.
[5]. MacNeill S, Dodds L, Hamilton DC, et al Rates and risk factors for recurrence of gestational diabetes. Diabetes Care 2001;24(4):659–662. doi: 10.2337/diacare.24.4.659.
[6]. Moses RG. The recurrence rate of gestational diabetes in subsequent pregnancies. Diabetes Care 1996;19(12):1348–1350. doi: 10.2337/diacare.19.12.1348.
[7]. ACOG practice bulletin no. 190: gestational diabetes mellitus. Obstet Gynecol 2018;131(2):e49–e64. doi: 10.1097/AOG.0000000000002501.
[8]. Moyer VA. Screening for gestational diabetes mellitus: U.S. Preventive Services Task Force recommendation statement. Ann Intern Med 2014;160(6):414–420. doi: 10.7326/M13-2905.
[9]. Practice bulletin No. 137: gestational diabetes mellitus. Obstet Gynecol 2013;122(2 Pt 1):406–416. doi: 10.1097/01.AOG.0000433006.09219.f1.
[10]. Araujo Junior E, Peixoto AB, Zamarian AC, et al Macrosomia. Best Pract Res Clin Obstet Gynaecol 2017;38:83–96. doi: 10.1016/j.bpobgyn.2016.08.003.
[11]. Gardosi J, Francis A. A customized standard to assess fetal growth in a US population. Am J Obstet Gynecol 2009;201(1):25.e21–e27. doi: 10.1016/j.ajog.2009.04.035.
[12]. Garrison A. Screening, diagnosis, and management of gestational diabetes mellitus. Am Fam Physician 2015;91(7):460–467.
[13]. Little SE, Edlow AG, Thomas AM, et al Estimated fetal weight by ultrasound: a modifiable risk factor for cesarean delivery? Am J Obstet Gynecol 2012;207(4):309.e1–e6. doi: 10.1016/j.ajog.2012.06.065.
[14]. ACOG practice bulletin no. 173: fetal macrosomia. Obstet Gynecol 2016;128(5):e195–e209. doi: 10.1097/AOG.0000000000001767.
[15]. Scifres CM, Feghali M, Dumont T, et al Large-for-gestational-age ultrasound diagnosis and risk for cesarean delivery in women with gestational diabetes mellitus. Obstet Gynecol 2015;126(5):978–986. doi: 10.1097/AOG.0000000000001097.
[16]. Liu F, Liu Y, Lai YP, et al Fetal hemodynamics and fetal growth indices by ultrasound in late pregnancy and birth weight in gestational diabetes mellitus. Chin Med J (Engl) 2016;129(17):2109–2114. doi: 10.4103/0366-6999.189057.
[17]. Perovic M, Gojnic M, Arsic B, et al Relationship between mid-trimester ultrasound fetal liver length measurements and gestational diabetes mellitus. J Diabetes 2015;7(4):497–505. doi: 10.1111/1753-0407.12207.
[18]. Ben-Haroush A, Yogev Y, Hod M. Fetal weight estimation in diabetic pregnancies and suspected fetal macrosomia. J Perinat Med 2004;32(2):113–121. doi: 10.1515/JPM.2004.021.
[19]. Ahmed B, Abushama M, Khraisheh M, et al Role of ultrasound in the management of diabetes in pregnancy. J Matern Fetal Neonatal Med 2015;28(15):1856–1863. doi: 10.3109/14767058.2014.971745.
[20]. Albert TJ, Landon MB, Wheller JJ, et al Prenatal detection of fetal anomalies in pregnancies complicated by insulin-dependent diabetes mellitus. Am J Obstet Gynecol 1996;174(5):1424–1428. doi: 10.1016/s0002-9378(96)70583-5.
[21]. Zhao E, Zhang Y, Zeng X, et al Association between maternal diabetes mellitus and the risk of congenital malformations: a meta-analysis of cohort studies. Drug Discov Ther 2015;9(4):274–281. doi: 10.5582/ddt.2015.01044.
[22]. Ornoy A, Reece EA, Pavlinkova G, et al Effect of maternal diabetes on the embryo, fetus, and children: congenital anomalies, genetic and epigenetic changes and developmental outcomes. Birth Defects Res C Embryo Today 2015;105(1):53–72. doi: 10.1002/bdrc.21090.
[23]. Bano S, Chaudhary V, Kalra S. The diabetic pregnancy: an ultrasonographic perspective. J Pak Med Assoc 2016;66(9 Suppl 1):S26–S29.
[24]. Langer O. Ultrasound biometry evolves in the management of diabetes in pregnancy. Ultrasound Obstet Gynecol 2005;26(6):585–595. doi: 10.1002/uog.2615.
[25]. Wong SF, Chan FY, Cincotta RB, et al Routine ultrasound screening in diabetic pregnancies. Ultrasound Obstet Gynecol 2002;19(2):171–176. doi: 10.1046/j.0960-7692.2001.00560.x.
[26]. Rossi G, Somigliana E, Moschetta M, et al Adequate timing of fetal ultrasound to guide metabolic therapy in mild gestational diabetes mellitus. Results from a randomized study. Acta Obstet Gynecol Scand 2000;79(8):649–654.
[27]. Randall P, Brealey S, Hahn S, et al Accuracy of fetal echocardiography in the routine detection of congenital heart disease among unselected and low risk populations: a systematic review. BJOG 2005;112(1):24–30. doi: 10.1111/j.1471-0528.2004.00295.x.
[28]. DeVore GR, Falkensammer P, Sklansky MS, et al Spatio-temporal image correlation (STIC): new technology for evaluation of the fetal heart. Ultrasound Obstet Gynecol 2003;22(4):380–387. doi: 10.1002/uog.217.
[29]. Chaoui R. The four-chamber view: four reasons why it seems to fail in screening for cardiac abnormalities and suggestions to improve detection rate. Ultrasound Obstet Gynecol 2003;22(1):3–10. doi: 10.1002/uog.187.
[30]. Crane JP, LeFevre ML, Winborn RC, et al A randomized trial of prenatal ultrasonographic screening: impact on the detection, management, and outcome of anomalous fetuses. The RADIUS Study Group. Am J Obstet Gynecol 1994;171(2):392–399. doi: 10.1016/s0002-9378(94)70040-0.
[31]. Longtine MS, Nelson DM. Placental dysfunction and fetal programming: the importance of placental size, shape, histopathology, and molecular composition. Semin Reprod Med 2011;29(3):187–196. doi: 10.1055/s-0031-1275515.
[32]. Pala HG, Artunc-Ulkumen B, Koyuncu FM, et al Three-dimensional ultrasonographic placental volume in gestational diabetes mellitus. J Matern Fetal Neonatal Med 2016;29(4):610–614. doi: 10.3109/14767058.2015.1012066.
[33]. Higgins M, Felle P, Mooney EE, et al Stereology of the placenta in type 1 and type 2 diabetes. Placenta 2011;32(8):564–569. doi: 10.1016/j.placenta.2011.04.015.
[34]. Edu A, Teodorescu C, Dobjanschi CG, et al Placenta changes in pregnancy with gestational diabetes. Rom J Morphol Embryol 2016;57(2):507–512.
[35]. Wong CH, Chen CP, Sun FJ, et al Comparison of placental three-dimensional power Doppler indices and volume in the first and second trimesters of pregnancy complicated by gestational diabetes mellitus. J Matern Fetal Neonatal Med 2018;32(22):3784–3791. doi: 10.1080/14767058.2018.1472226.
[36]. Desoye G, Hauguel-de Mouzon S. The human placenta in gestational diabetes mellitus. The insulin and cytokine network. Diabetes Care 2007;30(Supplement 2):S120–S126. doi: 10.2337/dc07-s203.
[37]. Pairleitner H, Steiner H, Hasenoehrl G, et al Three-dimensional power Doppler sonography: imaging and quantifying blood flow and vascularization. Ultrasound Obstet Gynecol 1999;14(2):139–143. doi: 10.1046/j.1469-0705.1999.14020139.x.
[38]. Castillo-Castrejon M, Powell TL. Placental nutrient transport in gestational diabetic pregnancies. Front Endocrinol (Lausanne) 2017;8:306. doi: 10.3389/fendo.2017.00306.
[39]. Scifres C, Feghali M, Althouse AD, et al Adverse outcomes and potential targets for intervention in gestational diabetes and obesity. Obstet Gynecol 2015;126(2):316–325. doi: 10.1097/AOG.0000000000000928.
[40]. Humphries J, Reynolds D, Bell-Scarbrough L, et al Sonographic estimate of birth weight: relative accuracy of sonographers versus maternal-fetal medicine specialists. J Matern Fetal Neonatal Med 2002;11(2):108–112. doi: 10.1080/jmf.11.2.108.112.
[41]. Conway DL, Langer O. Elective delivery of infants with macrosomia in diabetic women: reduced shoulder dystocia versus increased cesarean deliveries. Am J Obstet Gynecol 1998;178(5):922–925. doi: 10.1016/s0002-9378(98)70524-1.
[42]. Martin JA, Hamilton BE, Sutton PD, et al Births: final data for 2008. Natl Vital Stat Rep 2010;59(1):3–71.
[43]. ACOG practice bulletin no. 101: ultrasonography in pregnancy. Obstet Gynecol 2009;113(2 Pt 1):451–461. doi: 10.1097/AOG.0b013e31819930b0.
[44]. Elliott JP, Garite TJ, Freeman RK, et al Ultrasonic prediction of fetal macrosomia in diabetic patients. Obstet Gynecol 1982;60(2):159–162.
[45]. Melchior H, Kurch-Bek D, Mund M. The prevalence of gestational diabetes. Dtsch Arztebl Int 2017;114(24):412–418. doi: 10.3238/arztebl.2017.0412.
Keywords:

Ultrasonography; Diabetes, gestational; Fetal weight

© 2019 by Lippincott Williams & Wilkins, Inc.