Journal of Obstetrics and Gynaecology

ISSN: 0144-3615 (Print) 1364-6893 (Online) Journal homepage: http://www.tandfonline.com/loi/ijog20

Shear wave elastography of the placenta in

patients with gestational diabetes mellitus

Mehmet Aytac Yuksel, Fahrettin Kilic, Yasemin Kayadibi, Ebru Alici

Davutoglu, Metehan Imamoglu, Selim Bakan, Ismail Mihmanli, Fatih
Kantarci & Riza Madazli

To cite this article: Mehmet Aytac Yuksel, Fahrettin Kilic, Yasemin Kayadibi, Ebru Alici
Davutoglu, Metehan Imamoglu, Selim Bakan, Ismail Mihmanli, Fatih Kantarci & Riza Madazli
(2016): Shear wave elastography of the placenta in patients with gestational diabetes mellitus,
Journal of Obstetrics and Gynaecology, DOI: 10.3109/01443615.2015.1110120

To link to this article: http://dx.doi.org/10.3109/01443615.2015.1110120

Published online: 25 Mar 2016.

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Download by: [RMIT University Library] Date: 09 April 2016, At: 04:53
 Journal of Obstetrics and Gynaecology, 2015; Early Online: 1–4
ß 2015 Taylor & Francis
ISSN 0144-3615 print/ISSN 1364-6893 online
DOI: 10.3109/01443615.2015.1110120
ORIGINAL ARTICLE
Shear wave elastography of the placenta in patients with gestational
diabetes mellitus
Mehmet Aytac Yuksel1, Fahrettin Kilic2, Yasemin Kayadibi2, Ebru Alici Davutoglu1, Metehan Imamoglu1,
Selim Bakan2, Ismail Mihmanli2, Fatih Kantarci2 & Riza Madazli1
1
Department of Obstetrics and Gynecology, Cerrahpasa School of Medicine, Istanbul University, Istanbul, Turkey and 2Department of
Radiology, Cerrahpasa School of Medicine, Istanbul University, Istanbul, Turkey
To evaluate placental elasticty in women with gestational
diabetes mellitus (GDM) and non-diabetic controls. Thirty-three
Downloaded by [RMIT University Library] at 04:53 09 April 2016
pregnant women with GDM according to the current criteria of
the American Diabetes Association and 43 healthy pregnant
women who were admitted to the antenatal clinic were
recruited for this case–control study. Elasticity values of both the
peripheral and the central parts of the placentas of the patients
in both groups were determined by shear wave elastography
(SWE) imaging. Mean elasticity values of both the central and
the peripheral part of the placentas were significantly higher in
GDM pregnancies (p50.001). No difference was observed in the
mean elasticity values of the central and the peripheral part of
the placentas in two groups (p40.05). SWE imaging technology
might provide a quantitative assessment of the morphological
pathologies of placentas in pregnant women with GDM.
Keywords: Shear wave elastography, gestational diabetes mellitus,
placental elasticity, placental morphology, high-risk pregnancy
Introduction
Gestational diabetes mellitus (GDM) is defined as a glucose
intolerance of varying severity with onset or first recognition
during pregnancy (Metzger 1991). It complicates approximately
1–10% of pregnancies and is associated with significant foetal
complications and morbidity, which include macrosomia, birth
trauma, neonatal hypoglycemia, respiratory distress syndrome
and maternal long-term risk of developing type 2 diabetes
mellitus (Kim et al. 2002; Nordin et al. 2006).
The placenta is the essential link between mother and the
developing fetus and placental disease can affect foetal outcome.
Placentas of diabetic patients have been shown to present a
variety of significant histological structural changes. Classical
morphologic investigations of placental structure in diabetic
pregnancies have shown a varying degree of changes in the
syncytiotrophoblast, cytotrophoblast, trophoblastic basement
membrane and foetal vessels (Evers et al. 2003; Jauniaux and
Burton 2006).
Although there are relatively few studies for GDM, placental
structural abnormalities have been reported to be similar with
pre-existing diabetes mellitus (Jones and Fox 1976). In diabetic
patients, the surface area on the peripheral zone of the villous
tree is especially enlarged. The diffusion space between the
Correspondence: Mehmet Aytac Yuksel, MD, Department of Obstetrics and Gynecology, Cerrahpasa School of Medicine, Istanbul University,
Kocamustafapasa, Istanbul, Turkey. Tel: +90 532 601 60 58. E-mail: maytacyuksel@gmail.com
maternal and foetal vessels is also increased due to the thickening
of the trophoblastic basement membrane by large amounts of
collagen, predominantly type IV (Leushner et al. 1986). In
clinical practice, it is not easy to define the morphological
changes on routine sonographic examination, since they are
genarally insidious (Pathak et al. 2011).
Shear wave elastography (SWE) is a novel ultrasonographic
technique used to obtain elasticity information that ought to
represent the constituent of soft tissues. Application of this
technique in obstetrics has recently been documented. Studies
conserning placentas of preeclamptic patients have been reported
(Cimsit et al. 2015a, 2015b; Kilic et al. 2015). SWE has identical
ultrasound safety considerations to Doppler imaging, which is
considered safe for use during pregnancy within American
Institute for Ultrasound in Medicine (AIUM) limits (Bamber
et al. 2013). To the best of our knowledge, the application of
SWE for the evaluation of the placenta in GDM has not been
studied previously. The aim of our study was to utilise SWE to
determine the values of placental elasticity in women with or
without GDM.
Materials and methods
This was a case–control study with institutional ethics approval
performed between January 2013 and November 2013 at the
Cerrahpasa Medical Faculty Departments of Obstetrics and
Gynecology and Radiology. Forty-three women with normal
pregnancy and thirty-three women with GDM were recruited.
Gestational age was confirmed in all pregnant women by a
routine ultrasonographic examination performed during the first
trimester of gestation. All women were non-smokers and none
was administered any antenatal medications except anti-anemic
drugs. Exclusion criteria for all subjects were taking medication,
smoking, high blood pressure, and family history of diabetes
mellitus for the control group.
Insulin resistance was estimated by HOMA-IR (homoeostasis
model assessment-insulin resistance) (Matthews et al. 1985).
Body mass index (BMI) was obtained during the performance of
SWE. Women with GDM were diagnosed according to the
Carpenter–Coustan criteria; the 50-g glucose screening test was
carried out independent of the time of day or any previous meals
at about 24-week gestation (Carpenter and Coustan 1982). An
oral glucose tolerance test was recommended to all patients
 2 M. A. Yuksel et al.

whose 1-hour test result equaled or exceeded 140 mg/dl
(7.8 mmol/l). A diagnosis of GDM is made if at least 2 abnormal
values are met: fasting  95 mg/dl (5.3 mmol/l); 1 h, 180 mg/dl
(10.0 mmol/l); 2 h, 155 mg/dl (8.6 mmol/l); 3 h, 140 mg/dl
(7.8 mmol/l). Women diagnosed with gestational diabetes were
seen weekly and treatment consisted of dietary treatment (energy
goals of 35 kcal/kg of ideal body weight), adapted to allow
0.2–0.5 kg weight gain per week. Nutrition therapy was
combined with insulin based on the patient’s ability to achieve
glycemic control within 0–2 weeks. Insulin therapy was initiated
if blood glucose readings remained above target levels
[5.8 mmol/l (105 mg/dl) before meals and 7.1 mmol/l
(130 mg/dl) 2 h after meals] and was adjusted by the patient on
a daily basis based on a protocol using their self-monitored blood
glucose levels 3–4 times per day. Timing of delivery was based
primarily on obstetric indications.
Sonoelastography examination was performed with a shear
wave capable device supported with 1–6 MHz curved array
transducer (SuperSonic Imagine, Aix en Provence, France) in the
supine position. Sagittal imaging planes in the nearest part with a
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the umblical cord inserts) and peripheral parts of the placenta.
Region of interest (ROI, QBOX) tool which was fixed to 5mm
diameter was placed on the stiffest area on the color map, only
one ROI was used for each central and periphearal part of the
placenta. Shear modulus data (in kilopascals, kPA) automatically
displayed for all ROI. The measured mean elasticity data and
standard deviations within each ROI were used for statistical
analysis.
Statistical analysis
All analyses were performed using the Statistical Package for the
Social Sciences (SPSS) software version 18.0 (Chicago, IL).
Kolmogorov–Smirnov test was used assess normality of distri-
bution of variables. Data were presented as mean ± standard
deviation. Mean values between the groups were compared by
Student’s t-test. Comparison between groups was performed
using the Mann–Whitney U test or independent samples t-test.
The elastic modulus of the placental centre and the edge were
compared using a paired t-test. Spearman’s correlation coeffi-

perpendicular view of placenta were used. Before acquisitions,

patients were asked to breathe slightly. Elastogram images were
displayed as an overlay in dual mode with gray-scale images
simultaneously. A rectangular adjustable electronic box was used
for SWE examinations in the elastogram screen. During the
examination care was taken to avoid placing the box on vascular
tissues and heterogenous parts of the placenta. The adjustable
box displayed the tissue stiffness in the placenta (Figure 1).
Elastograms were captured from central (2 cm away from where
cient was used to determine the relationship between the
variables.
Results
General characteristics of the study population are shown in
Table I. The women were comparable with regard to maternal
age, parity, BMI, gestational age at delivery, birth weight and

Figure 1. Shear wave elastography image and corresponding two-dimensional images of placenta .The rectangle box represent the stiffed area and ROI is
placed in the denser area.
 Elastography in pregnancy with GDM 3

placental weight. There was no perinatal mortality and no
malformations were found in the neonates. All gestational
diabetic mothers were well controlled in glucose and glycated
hemoglobin levels.
Radiological scores of SWE are presented in Table II. The
mean elasticity values in the central and the peripheral part of the
placentas were 10.63 ± 5.97 and 10.67 ± 7.41 kPa respectively for
women with GDM. The mean elasticity values in the central and
the peripheral part of the placentas of controls were 5.47 ± 1.74
and 5.23 ± 1.31 kPa respectively. No statistically significant
difference was found between the mean elasticity values of the
central part placenta and the peripheral part placenta within each
group (p40.05). Women with GDM had a significantly higher
mean elasticity value both in the central and the peripheral of
part of the placentas than controls (p50.001) (Table II).
Of the women with GDM, 13 had insulin therapy and 20 were
treated with diet alone. The mean elasticity values in the central
and the peripheral part placenta of GDM treated with insulin
were 11.10 ± 5.17 kPa and 11.16 ± 8.54 kPa, and with diet alone
were 9.91 ± 9.19 kPa and 10.29 ± 6.62 kPa respectively. There was
Downloaded by [RMIT University Library] at 04:53 09 April 2016
provides a reliable basis for identifying and diagnosing diseases
(Berg et al. 2012; Sporea and Sirli 2012, Botanlioglu et al. 2013;
Monpeyssen et al. 2013). Since the placenta is one of the most
important parenchymal organs in obstetrics, we investigated
placental elasticity using SWE technology as a preliminary study
for future clinical use of this method.
The major conclusion of the present study is that the mean
placental elasticity value measured in women with GDM was
higher compared to healthy pregnant women. Women with
GDM had placentas with higher elasticity modulus. We have also
observed that there was no difference between the periphreal and
central areas in terms of mean placental elasticity values. Li et al.
have also reported that there was no significant difference
between the edge and central areas of normal pregnancy
placental elastic modulus (Li et al. 2012). These findings indicate
that placental centre and periphery can both represent the
placental elasticity.
Most authors have reported the presence of focal fibrinoid
necrosis and a relative placental immaturity in diabetic
pregnancies. Moreover, detailed ultrastructural studies have

no statistically significant difference between these two groups documented the focal thickening of the villous trophoblastic
(p40.05). basement membrane and patchy focal syncytiotrophoblastic
The mean elasticity values in the central was not found to be necrosis with marked cytotrophoblastic hyperplasia (Jones and
associated with maternal age, gestational age, birth weight, Fox 1976; Jauniaux et al. 2006; Madazli et al. 2008; Salge et al.
HbA1c, fasting glucose, insulin levels (r ¼ 0.060, p ¼ 0.615; 2012). In a recent study, we have also demonstrated that the
r ¼ 0.140, p ¼ 0.241; r ¼ 0.097, p ¼ 0.458; r ¼ 0.091, p ¼ 0.566; presence of villous immaturity, chorangiosis and ischemia were
r ¼ 0.124, p ¼ 0.300; r ¼ 0.111, p ¼ 0.368; r ¼ 0.013, p ¼ 0.936, significantly increased in the placentas of women with GDM
respectively) (Table III). (Madazli et al. 2008). High mean placental elasticity observed in
the present study may be due to the placental pathologies that
have been observed in the diabetic pregnancies. However the
Discussion major limitation of our study is that we do not have the
Elasticity imaging technology has been used in clinical practice to histopathological examination of the placentas. Studies involving
evaluate the elasticity in parenchymal organs for over 10 years. placental histopatology and also pre-gestational diabetic preg-
The elasticity imaging of breast lesions, thyroid and other organs nancies are needed to improve our knowledge about the
diagnostic efficiency of the mentioned technique.
Some studies showed that the pathologic findings of the
Table I. General characteristics of the study population. diabetic placentas can still be detected even in cases with slightly
Control GDM p improved maternal glycemic control (Laurini et al. 1987; Desoye
Subjects, n 43 33
et al. 2002; Madazli et al. 2008). GDM patients enrolled in this
Maternal age, years 32.7 ± 5.6 30.6 ± 5.5 0.130 study had well-maintained glycemic profile and the results
Parity 1.8 ± 1.1 1.9 ± 1.2 0.787 revealed no significant difference in the elasticity of the placentas
Gestatinal age at SWE, weeks 30.5 ± 3.7 30.5 ± 3.4 0.926 between the patients with GDM treated with insulin and diet.
BMI 28.2 ± 3.2 28.4 ± 2.1 0.697 Sugitani et al. measured the elasticity of placentas of
HbA1c, % 5.1 ± 0.3 5.9 ± 1.6 0.030
HOMA-IR 1.5 ± 0.5 2.7 ± 1.6 0.000* hypertensive and foetal growth restriction (FGR) pregnancies
Gestational age at delivery, weeks 38.7 ± 1.1 38.8 ± 0.7 0.543 ex vivo and reported significantly higher elasticity values of
Birth weight, g 3287 ± 366 3476 ± 504 0.114 central part of placentas in intrauterine growth restricted and
APGAR 5th 9.1 ± 1.1 9.08 ± 0.7 0.179 hypertensive pregnancies (Sugitani et al. 2013). They speculated
Placental weight, g 523 ± 7.7 528 ± 9.9 0.170
that the increased elasticity values in this group of pregnancies
Figures are mean ± SD unless otherwise indicated. might be due to the placental histological pathologies observed in
BMI, body mass index; HOMA-IR, homeostatic model assessment of insulin
resistance; SWE, shear wave elastography.
such pregnancies. Although the mentioned study was ex vivo in
*Statistically significant at p50.05.

Table III. Correlations between mean elasticity values in the central and all
the other parameters in whole groups.
r p
Table II. The shear wave velocity of the placenta in women diagnosed with
Maternal age 0.060 0.615
gestational diabetes and normal controls.
Gestatinal age at SWE (week) 0.140 0.241
GDM Control p Birth weight (g) 0.097 0.458
HbA1c (%) 0.091 0.566
Subjects, n 33 43 Fasting glucose (mg/dl) 0.124 0.300
Mean elasticity of central part 10.63 ± 5.97 5.47 ± 1.74 0.000 Insulin (mU/l) 0.111 0.368
of placenta (kPa)
Mean elasticity of peripheral part 10.67 ± 7.41 5.23 ± 1.31 0.001 BMI, body mass index; HOMA-IR, homeostatic model assessment of insulin
of placenta (kPa) resistance.

Figures are mean ± SD.

 4 M. A. Yuksel et al.
nature, it highlights the ability of SWE examination of the
placentas in pathological conditions. In recent studies, Kilic et al.
(2015) and Cimsit et al. (2015a) have demonstrated that in vivo
stiffness of the placentas were significantly higher in patients
with preeclampsia than controls.
Conclusion
This is the first report on the in vivo quantization of elasticity of
placentas in gestational diabetes. It brings new insights into
imaging of the placentas in GDM with application of shear wave
imaging. Taking into consideration of the limitations of the
present study, SWE imaging might indirectly provide informa-
tion of the morphological pathologies of placentas with gesta-
tional diabetes. Therefore, with the help of further elaborately
designed studies, the utilisation of SWE might be helpfull in the
managemet of GDM.
Declaration of interest: We state explicitly that there are no
conflicts of interest in connection with this article.
Downloaded by [RMIT University Library] at 04:53 09 April 2016
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