Addition of Cervical Elastography May Increase Preterm Delivery Prediction Performance in Pregnant Women with Short Cervix: a Prospective Study

Abstract

Background
We investigated whether there is a difference in elastographic parameters between pregnancies with and without spontaneous preterm delivery (sPTD) in women with a short cervix (≤ 25 mm), and examined the ability of elastographic parameters to predict sPTD in those women.

Methods
E-CervixTM (WS80A; Samsung Medison, Seoul, Korea) elastography was used to examine the cervical strain. Elastographic parameters were compared between pregnancies with and without sPTD. Diagnostic performance of elastographic parameters to predict sPTD ≤ 37 weeks, both alone and in combination with other parameters, was compared with that of cervical length (CL) using area under receiver operating characteristic curve (AUC) analysis.

Results
A total of 130 women were included. Median gestational age (GA) at examination was 24.4 weeks (interquartile range, 21.4–28.9), and the prevalence of sPTD was 20.0% (26/130). Both the elastographic parameters and CL did not show statistical difference between those with and without sPTD. However, when only patients with CL ≥ 1.5 cm (n = 110) were included in the analysis, there was a significant difference between two groups in elasticity contrast index (ECI) within 0.5/1.0/1.5 cm from the cervical canal (P < 0.05) which is one of elastographic parameters generated by E-Cervix. When AUC analysis was performed in women with CL ≥ 1.5 cm, the combination of parameters (CL + pre-pregnancy body mass index + GA at exam + ECI within 0.5/1.0/1.5 cm) showed a significantly higher AUC than CL alone (P < 0.05).

Conclusion
An addition of cervical elastography may improve the ability to predict sPTD in women with a short CL between 1.5 and 2.5 cm.

Full text

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ABSTRACT
Background: We investigated whether there is a dierence in elastographic parameters
between pregnancies with and without spontaneous preterm delivery (sPTD) in women with
a short cervix (≤ 25 mm), and examined the ability of elastographic parameters to predict
sPTD in those women.
Methods: E-CervixTM (WS80A; Samsung Medison, Seoul, Korea) elastography was used to
examine the cervical strain. Elastographic parameters were compared between pregnancies
with and without sPTD. Diagnostic performance of elastographic parameters to predict sPTD
≤ 37 weeks, both alone and in combination with other parameters, was compared with that of
cervical length (CL) using area under receiver operating characteristic curve (AUC) analysis.
Results: A total of 130 women were included. Median gestational age (GA) at examination was
24.4 weeks (interquartile range, 21.4–28.9), and the prevalence of sPTD was 20.0% (26/130).
Both the elastographic parameters and CL did not show statistical dierence between those
with and without sPTD. However, when only patients with CL ≥ 1.5 cm (n = 110) were included
in the analysis, there was a signicant dierence between two groups in elasticity contrast index
(ECI) within 0.5/1.0/1.5 cm from the cervical canal (
P
< 0.05) which is one of elastographic
parameters generated by E-Cer vix. When AUC analysis was performed in women with CL ≥ 1.5
J Korean Med Sci. 2019 Mar 11;34(9):e68
https://doi.org/10.3346/jkms.2019.34.e68
eISSN 1598-6357·pISSN 1011-8934
Original Article
Received: Oct 24, 2018
Accepted: Feb 15, 2019
Address for Correspondence:
Soo-young Oh, MD, PhD
Department of Obstetrics and Gynecology,
Samsung Medical Center, Sungkyunkwan
University School of Medicine, 81 Irwon-ro,
Gangnam-gu, Seoul 06351, Korea.
E-mail: ohsymd@skku.edu
*Present address: Department of Obstetrics
and Gynecology, CHA Gangnam Medical
Center, CHA University School of Medicine,
Seoul, Korea
© 2019 The Korean Academy of Medical
Sciences.
This is an Open Access article distributed
under the terms of the Creative Commons
Attribution Non-Commercial License (https://
creativecommons.org/licenses/by-nc/4.0/)
which permits unrestricted non-commercial
use, distribution, and reproduction in any
medium, provided the original work is properly
cited.
ORCID iDs
Hyun Soo Park
https://orcid.org/0000-0002-7873-3234
Hayan Kwon
https://orcid.org/0000-0002-5195-7270
Dong Wook Kwak
https://orcid.org/0000-0003-2447-561X
Moon Young Kim
https://orcid.org/0000-0001-8881-2027
Hyun-Joo Seol
https://orcid.org/0000-0003-0303-7813
Joon-Seok Hong
https://orcid.org/0000-0002-3832-8445
Hyun Soo Park ,1 Hayan Kwon ,1 Dong Wook Kwak ,2,3 Moon Young Kim ,2,*
Hyun-Joo Seol ,4 Joon-Seok Hong ,5 Jae-Yoon Shim ,6 Sae-Kyung Choi ,7
Han-Sung Hwang ,8 Min Jeong Oh ,9 Geum Joon Cho ,9 Kunwoo Kim ,10
Soo-young Oh ,11 and Korean Society of Ultrasound in Obstetrics and
Gynecology Research Group
1Department of Obstetrics and Gynecology, Dongguk University Ilsan Hospital, Goyang, Korea
2
Department of Obstetrics and Gynecology, Cheil General Hospital and Women's Healthcare Center,
Dankook University College of Medicine, Seoul, Korea
3
Department of Obstetrics and Gynecology, Ajou University Hospotal, Ajou University School of Medicine,
Suwon, Korea
4
Department of Obstetrics and Gynecology, Kyung Hee University Hospital at Gangdong, Kyung Hee
University School of Medicine, Seoul, Korea
5Department of Obstetrics and Gynecology, Seoul National University Bundang Hospital, Seongnam, Korea
6
Department of Obstetrics and Gynecology, Asan Medical Center, University of Ulsan College of Medicine,
Seoul, Korea
7
Department of Obstetrics and Gynecology, The Catholic University of Korea Incheon St. Mary's Hospital,
The Catholic University of Korea College of Medicine, Seoul, Korea
8
Department of Obstetrics and Gynecology, Konkuk University Medical Center, Konkuk University School of
Medicine, Seoul, Korea
9
Department of Obstetrics and Gynecology, Korea University Guro Hospital, Korea University College of
Medicine, Seoul, Korea
10Department of Obstetrics and Gynecology, Hamchoon Women's Clinic, Seoul, Korea
11
Department of Obstetrics and Gynecology, Samsung Medical Center, Sungkyunkwan University School of
Medicine, Seoul, Korea
Addition of Cervical Elastography May
Increase Preterm Delivery Prediction
Performance in Pregnant Women with
Short Cervix: a Prospective Study
Obstetrics & Gynecology
Provisional
Provisional

Jae-Yoon Shim
https://orcid.org/0000-0003-1881-8436
Sae-Kyung Choi
https://orcid.org/0000-0001-6264-4256
Han-Sung Hwang
https://orcid.org/0000-0003-0622-0701
Min Jeong Oh
https://orcid.org/0000-0002-3130-2728
Geum Joon Cho
https://orcid.org/0000-0001-6761-0944
Kunwoo Kim
https://orcid.org/0000-0002-2272-5665
Soo-young Oh
https://orcid.org/0000-0003-3002-0048
Presentation
The data in this article were presented at
the 27th World Congress on Ultrasound in
Obstetrics and Gynecology which was held in
Vienna, Austria, on September 15–19, 2017.
Funding
The work was funded (2015) by Samsung
Medison Company (Seoul, Korea).
Disclosure
The authors have no potential conflicts of
interest to disclose.
Author Contributions
Conceptualization: Kwak DW, Kim MY, Oh SY.
Data curation: Park HS, Kwon H, Kwak DW,
Kim MY, Seol HJ, Hong JS, Shim JY, Choi SK,
Hwang HS, Oh MJ, Cho GJ, Kim K, Oh SY.
Formal analysis: Park HS, Oh SY. Methodology:
Kwak DW, Seol HJ, Hong JS, Choi SK, Hwang
HS, Kim K, Oh SY. Validation: Park HS, Kwon
H, Kwak DW, Kim MY, Seol HJ, Hong JS, Shim
JY, Choi SK, Hwang HS, Oh MJ, Cho GJ, Kim K,
Oh SY. Writing - original draft: Park HS, Kwon
H, Oh SY. Writing - review & editing: Park HS,
Oh SY.
cm, the combination of parameters (CL + pre-pregnancy body mass index + GA at exam + ECI
within 0.5/1.0/1.5 cm) showed a signicantly higher AUC than CL alone (
P
< 0.05).
Conclusion: An addition of cervical elastography may improve the ability to predict sPTD in
women with a short CL between 1.5 and 2.5 cm.
Keywords: Short Cervix; Elastography; Strain; Preterm Delivery; Ultrasonography; Pregnancy
INTRODUCTION
Preterm delivery is a leading cause of neonatal morbidity and mortality and accounts for
about 10% of all births worldwide.1 Despite low birth rate, the rate of preterm birth in Korea
has steadily been increasing up to 7.3% and about 30,000 neonates were delivered at less than
37 weeks of gestation in 2016.2 Although previous preterm birth history increases recurrent
preterm birth,3 about 90% of pregnant women experience preterm birth without any history
of preterm birth. Therefore, proper prediction of preterm birth is of utmost important.
Ever since a study reported an association between short cervical length (CL) and subsequent
preterm birth,4 CL measurement during pregnancy has been one of the most frequently
performed ultrasound procedures in prediction of spontaneous preterm birth, both in low
and high-risk pregnancies.5,6 However, the actual rate of preterm birth varies depending on
the risk status of the pregnancy with short CL. For instance, in primiparas with a short CL (≤
2.5 cm) without prior preterm delivery (low-risk), the actual preterm birth ranges only from
14% to 16.2%.7,8 On the other hand, a short CL in high risk pregnancy is associated with
substantially increased risk of preterm delivery, ranging from 44% to 55%.9,10 Despite such
increase, it is clear that the rate of preterm birth is not perfectly predicted by CL measurement,
given that preterm birth actually occurred in less than half of the patients in both groups. A
Korean cohort study including 3,296 consecutive women with a singleton pregnancy who
underwent routine CL measurement between 20 and 24 weeks also proved that the actual
preterm birth rate (< 34 weeks) was only 26% among women with short CL (≤ 2.5 cm).11
Ultrasound elastography which assesses the biochemical and mechanical properties of a
tissue has emerged as a promising ancillary tool to conventional ultrasound. There are two
types of elastography used in clinical practice: strain and shear wave elastography. Strain
elastography is based on the measurement of tissue displacement under compression,
either extrinsic or intrinsic. It is based on the principle that so parts of the tissue deform
more than harder parts under compression.12 In contrast, shear wave elastography involves
displacing tissue with a high-frequency ultrasound pulse generated by ultrasound scanner
and subsequent monitoring of the propagation of shear wave, which is orthogonal to the
direction of tissue displacement.13 The property of shear wave—that it moves faster in stier
and slower in soer tissue—enables us to quantify tissue stiness or soness.
Since elastography is considered to measure the mechanical properties of the cervix, several
researchers actively studied cervical elastography during pregnancy in relation to preterm
birth and labor induction, either by using strain or shear wave elastography.14-27 However,
most studies include all women with various CLs without limiting it to a certain range, which
may not fully test the utility of elastographic parameters specically within the high-risk
patients with short CL.
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Given such background, we designed a multicenter prospective study in which cervical
elastography was performed in women with short CL (≤ 2.5 cm). The objective of this study
was to investigate; 1) whether there is a dierence in elastographic parameters between
pregnancies with and without spontaneous preterm delivery (sPTD) and 2) the ability of
elastographic parameters to predict sPTD in pregnancies with a short cervix (≤ 25 mm).
METHODS
Subjects
Pregnant women with CL ≤ 25 mm between 16 and 32 weeks of gestation were enrolled from
nine institutions between July 2015 and May 2017. The sPTD was dened as a birth before 37
completed weeks of gestation, due either to preterm labor or to preterm premature rupture
of membranes. Cervical elastography was performed simultaneously with CL measurement,
which was performed upon each clinician’s judgement. Multiple pregnancies, placenta
previa, abruptio placentae, and pregnancies using tocolytics or with cerclage before CL
measurements were excluded from the study. Pregnancy outcomes as well as demographic
and obstetric parameters were collected.
CL and elastographic measurements
CL was measured with vaginal ultrasound (WS80A Ultrasound System; Samsung Medison,
Seoul, Korea), which uses 6-MHz transvaginal probe with a standard CL measurement
protocol previously described (Fig. 1A).28 Aer measuring the CL, elastography was
performed three times in the same plane with the same transvaginal probe using the
E-CervixTM system (Samsung Medison), a quantication tool to measure the stiness of
the cervix using elastography. While collecting the data, patients are allowed to breathe
normally and the operator does not apply pressure to the cervix, a technique used in the study
of Swiatkowska-Freund and Preis.23 We avoided measurements when fetuses were moving,
especially when they were in non-cephalic presentation for consistent results. Participating
examiners were instructed to follow the standardized measuring methods before the start
of the study. The E-Cervix system uses minute internal organ movements from compression
sources including vessel pulsation and respiratory movement.
The technical process of collecting data is depicted in Fig. 2A, which essentially tracks
2-dimensional tissue deformation. Specically, the stiness of the cervical tissue is
estimated using strain variation through multiple frames, only when the probe is steady.
The steadiness of the probe is controlled by motion bars in the monitor screen, precluding
any gross movement such as active fetal activity from disturbing the steadiness. Only when
the probe movements are within the pre-determined range, all motion bars turn green
and strain values are acquired, which accordingly produces an elastography image. In this
process, E-Cervix performs 2-dimensional speckle tracking on a sliding buer of acquired
image frames normally covering at least several seconds. The strain calculated from multi-
frame images is visually converted to the stiness of each point in the cervix (Fig. 2B). Aer
collecting acquisition from adequate frames of strain elastography images, the strain values
were displayed in spectrum of colors from blue (so) to red (hard) in the monitor along with
the 2-dimensional ultrasound image. The operator denes region of interest (ROI) using
pre-dened selection tool built in ultrasound machine (Fig. 1B and C). First, operator lines
cervical canal by selecting 2- or 4- points between internal and external os of cervix. When
cervical canal is dened, the green points are automatically marked from the selected cervical
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canal. Aer the operator adjusts green points to dene entire cer vical area, each yellow point
is displayed at every 0.5 cm from cervical canal and used when the parameters such as strain
mean level, elasticity contrast index (ECI), and hardness ratio within 0.5/1.0/1.5 cm from the
cervical canal are calculated. When there was a funneling in the cervix, the operator adjusted
ROI to include as much cervix as possible while trying to avoid fetus or amniotic uid near
the cervix using funnel shaped ROI.
From those elastography images, multiple parameters are generated by E-Cervix (Table 1).
Detailed qualitative denitions of each parameter are as follows. Strain mean levels are average
strain values in the ROI, which are standardized in a range between 0 (hard) and 1 (so).
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A
B
C
D1 1.73 cm
1 cm
0.5 cm
1 cm
1.5 cm
1 cm
Fig. 1. Measurements and ROI definitions in elastography images. (A) CL measurement using 6-MHz transvaginal
probe in B-mode ultrasonography. Measurement areas of E-Cervix. (B) Strain values of the IOS and EOS are
measured using a 1-cm radius from IOS, and EOS, respectively. (C) Values of strain mean, hardness ratio, and
ECI are measured from within 0.5/1.0/1.5 cm area of the cervical canal. The patient agreed to publication of the
elastography image of the uterine cervix.
ROI = regions of interest, CL = cervical length, IOS = internal os of cervix, EOS = external os of cervix, ECI =
elasticity contrast index.
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ECI, an average contrast index of the pixels within the ROI, represents how heterogeneous
or homogeneous the object is within the ROI box. All the pixels in the ROI are graded on a
ten-point scale between 0 and 9. The dierence of the points between neighboring pixels is
converted to a number ranging between 0 and 81, which are ECI value of individual pixel. The
overall ECI is the average of the individual pixel contrast index. Hardness ratio is the percent
of upper 30 percent of red (hard) pixel area divided by total pixel area within the ROI and
represents how much area is occupied by hard pixels in the ROI. Only the strain means of the
internal and external os and their ratio were presented on the screen of the elastography during
the exam, and thus other elastographic parameters were blinded to all clinicians until delivery.
Statistical analysis
Maternal baseline and obstetric parameters and outcomes were compared between
patients with and without sPTD using χ2 test, Fisher's exact test, and Mann-Whitney U test.
Frequencies, medians, and interquartile ranges (IQRs) were calculated and compared between
groups. To evaluate the ability of a parameter or combinations of parameters to predict
sPTD, the areas under the receiver operating characteristic curve (AUC) were calculated and
compared. Logistic regression analysis was used to calculate and compare AUC when multiple
parameters were put in the prediction model. We used c-statistics of the logistic regression
model. The c
-
statistic, or concordance statistic is a measure of the discriminatory power
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Start
Have all frames been acquired?
Strain calculation
Producing elastography image
No
A
Yes
Calculating representative 2 dimensional
displacement using internal pressure source
Is probe steady enough?
B
Fig. 2. E-Cervix elastography image generation processes. (A) Flow diagram of E-Cervix elastography measurements. (B) E-Cervix elastography image generation
by multiple frames.
Table 1. Selected E-Cervix parameters
Measurement parameter Description
IOS strain mean level Standardized strain mean level in 1 cm circle of IOS, value range: 0 (hard)–1 (soft)
EOS strain mean level Standardized strain mean level in 1 cm circle of EOS, value range: 0 (hard)–1 (soft)
Ratio (IOS/EOS) IOS strain level/EOS strain level
Strain mean level within 0.5/1.0/1.5 cm
from the cervical canal
Strain mean level within 0.5/1.0/1.5 cm area from the cervical canal in ROI, value range: 0 (hard)–1 (soft)
ECI within 0.5/1.0/1.5 cm from the
cervical canal
ECI score within 0.5/1.0/1.5 cm area from the cervical canal in ROI, value range: 0 (homogeneity)–81 (heterogeneity)
Hardness ratio within 0.5/1.0/1.5 cm
from the cervical canal
30-Percentile hardness area ratio within 0.5/1.0/1.5 cm from the cervical canal in ROI, value range: 0% (soft)–100% (hard)
IOS = internal os of cervix, EOS = external os of cervix, ROI = region of interest, ECI = elasticity contrast index.
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of a predictive model, and is equivalent to AUC.29 A
P
value less than 0.05 was considered
signicant. STATA 14.0 (StataCorp, College Station, TX, USA) was used in statistical analyses.
Ethics statement
The study protocol was reviewed and approved by the Institutional Review Board (IRB)
in each participating hospital (IRB No. Asan Medical Center 2015-0800, Cheil General
Hospital CGH-IRB-2015-6, Dongguk University Ilsan Hospital 2015-42, Seoul St. Mary's
Hospital KC15OIMI0289, Kyung Hee University Hospital at Gangdong 2015-05-006,
Konkuk University Medical Center 1040044, Korea University Guro Hospital 2015GR0300,
Samsung Medical Center 2015-04-014-002, and Seoul National University Bundang Hospital
B-1505/297-002) and written informed consents were collected from all subjects. The patient
agreed to publication of the elastography image of the uterine cervix.
RESULTS
A total of 130 subjects were included in the analysis. Median gestational age (GA) at
examination was 24.4 weeks IQR, 21.4–28.9), and the prevalence of sPTD was 20.0%
(26/130). Table 2 lists the maternal and sonographic characteristics of these subjects, which
incorporates the selected E-Cervix parameters previously described in Table 1. Among all
the characteristics, pre-pregnancy body mass index (BMI) and funneling were signicantly
dierent between those with and without sPTD (
P
< 0.05). On the other hand, the ECI
scores within 1.0 and 1.5 cm from the cervical canal, one of the E-Cervix parameters,
were marginally dierent (
P
values of 0.067 and 0.056, respectively). All other maternal
or sonographic characteristics including CL were not dierent between women with and
without sPTD. The clinical courses aer CL examination are presented in Table 3. According
to the data, exam to delivery interval, GA at delivery, birth weight, and neonatal intensive
care unit (NICU) admission were dierent between two groups (
P
< 0.001). The frequency of
progesterone treatment was also signicantly dierent between two groups.
Next, we divided our original subjects into two groups: patients with CL < 1.5 cm, and
those with CL ≥ 1.5 cm. This division was to investigate whether there is any dierence in
elastographic parameters in relation to CL—whether the patient's cervix is moderately short
or severely short. In patients with CL < 1.5 cm, there was no dierence between patients with
and without sPTD in terms of E-Cervix parameters (data not shown). However, when subjects
were limited to CL ≥ 1.5 cm, patients with sPTD showed signicantly higher ECI scores
within 0.5/1.0/1.5 cm from the cervical canal, compared to those without sPTD (Table 4).
In subjects with CL ≥ 1.5 cm, we calculated the AUC of dierent models in predicting sPTD.
These models included CL, GA at CL exam, pre-pregnancy BMI, and ECI score within
0.5/1.0/1.5 cm from the cervical canal, both individually and in combination. Then, we
compared all the AUCs with that of CL alone (Table 5). According to the results, none of the
individual parameters showed better AUCs than CL alone. However, combination of CL, GA
at CL exam, and pre-pregnancy BMI showed better AUC than CL alone (
P
< 0.05), and an
addition of ECI score within 0.5/1.0/1.5 cm from the cervical canal signicantly increased the
predicting ability of the models up to an AUC of 0.8256 (Fig. 3).
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DISCUSSION
Strain elastography can be done either by manual compression applied to the target tissue
(external compression) or by internally generated ne vibration by organ motion such as
adjacent arterial pulsation and breathing (internal or in vivo compression).30 Strain values
from external compression can be more operator-dependent than those from intrinsic
compression.12 We used in vivo compression method with a soware named E-CervixTM
which acquires data for three seconds and collects strain data from 51 frames of images.
We previously demonstrated that the reproducibility of these elastographic parameters is in
moderate to substantial agreement in terms of intra- and inter-observer variance including 90
singleton pregnant women between 16 weeks and 32 weeks.31 Shear wave elastography, which
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Table 2. Maternal baseline characteristics and sonographic findings
Variables No sPTD (n = 104) sPTD (n = 26) P value
Age, yr 33.90 (31.00–36.00) 32.20 (30.00–36.00) 0.597
Multiparity 68 (65.4) 14 (53.8) 0.364
Prior sPTD 10 (9.6) 5 (19.2) 0.179
Prepregnancy BMI, kg/m220.99 (19.34–22.69) 19.33 (18.33–21.35) 0.009
DM 2 (1.9) 1 (3.8) 0.491
HTN 0 (0.0) 1 (3.8) 0.200
Smoking 1 (1.0) 0 (0.0) 1.000
GA at exam, wk 24.71 (21.86–29.14) 23.14 (20.86–27.14) 0.131
CL, cm 2.10 (1.81–2.30) 1.83 (1.34–2.30) 0.148
Funneling 19 (18.3) 12 (46.2) 0.005
IOS strain 0.30 (0.23–0.37) 0.29 (0.25–0.36) 0.965
EOS strain 0.34 (0.26–0.39) 0.32 (0.24–0.44) 1.000
IOS/EOS 0.88 (0.76–1.03) 0.89 (0.81–0.99) 0.864
Strain mean level within 0.5 cm 0.32 (0.25–0.40) 0.31 (0.27–0.41) 0.723
Strain mean level within 1.0 cm 0.31 (0.25–0.39) 0.31 (0.24–0.39) 0.930
Strain mean level within 1.5 cm 0.33 (0.27–0.40) 0.32 (0.26–0.41) 0.894
ECI within 0.5 cm 5.68 (3.96–7.38) 6.21 (4.57–8.91) 0.206
ECI within 1.0 cm 4.85 (3.35–5.95) 5.50 (4.07–7.78) 0.0 67
ECI within 1.5 cm 4.30 (3.11–5.14) 5.09 (3.70–6.95) 0.056
Hardness ratio within 0.5 cm 56.37 (41.96–71.22) 57.19 (37.23–65.72) 0.773
Hardness ratio within 1.0 cm 57.63 (44.73–71.58) 57.42 (40.44–72.87) 0.961
Hardness ratio within 1.5 cm 52.88 (41.55–66.00) 58.13 (38.50–68.58) 0.868
Data are presented as the median (interquartile range) or number (%).
P values less than 0.05 are shown in bold.
sPTD = spontaneous preterm delivery, BMI = body mass index, DM = diabetes mellitus, HTN = hypertension, GA
= gestational age, CL = cervical length, IOS = internal os of cervix, EOS = external os of cervix, ECI = elasticity
contrast index.
Table 3. Clinical course after CL examination including elastography and delivery outcome
Variables No sPTD (n = 104) sPTD (n = 26) P value
Cerclage after CL exam 7 (6.7) 5 (19.2) 0.063
Tocolytics after CL exam 3 (2.9) 3 (11.5) 0.094
Progesterone after CL exam 79 (76.0) 25 (96.2) 0.026
GDM 9 (8.7) 6 (23.1) 0.079
Preeclampsia 3 (3.0) 1 (4.0) 1.000
Exam to delivery interval, day 97.0 (65.5–120.5) 64.50 (39.75–74.75) < 0.001
GA at delivery, wk 38.71 (38.14–39.57) 33.36 (31.04–35.93) < 0.001
Cesarean delivery 30 (29.1) 10 (38.5) 0.355
Gender, men 56 (55.4) 11 (45.8) 0.496
Birth weight, g 3,280 (3,050–3,490) 1,915 (1,562–2,645) < 0.001
NICU admission 3 (2.9) 16 (61.5) < 0.001
Data are presented as the median (interquartile range) or number (%).
P values less than 0.05 are shown in bold.
CL = cervical length, sPTD = spontaneous preterm delivery, GDM = gestational diabetes, GA = gestational age,
NICU = neonatal intensive care unit.
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uses focused ultrasound beam displacing the target tissue and measures shear wave speed
radiating outward, have advantages of being less operator dependent32 and more frequently
applied to the elastography imaging of liver in clinical practice.33 However, since shear wave
estimation is based on the assumption of tissue homogeneity within the target ROI,13 it
was noted that anisotropic, heterogeneous and relatively small organ with microstructural
complexity imposes the cervix tissue less suitable for shear wave elastography than larger
isotropic organs such as liver.32 Intra- and inter reproducibility was presented from small
number of pregnant patients (n = 8) in shear wave measurements of cervix in which the
Aixplorer ultrasound system (SuperSonic Imagine, Aix-en-Provence, France) was applied.19
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Table 4. Comparison of E-Cervix parameters in subjects with CL ≥ 1.5 cm
Variables No sPTD (n = 93) sPTD (n = 17) P value
Age, yr 33.00 (31.00–35.00) 32.00 (30.00–35.00) 0.372
Multiparity 60 (64.5) 8 (47.1) 0.186
Prior sPTD 8 (8.6) 2 (11.8) 0.651
Prepregnancy BMI, kg/m220.91 (19.36–22.70) 19.26 (18.26–20.03) 0.017
DM 1 (1.1) 0 (0.0) 1.000
HTN 0 (0.0) 1 (5.9) 0.155
Smoking 1 (1.1) 0 (0.0) 1.000
GA at exam, wk 24.43 (21.43–29.00) 22.71 (20.29–24.00) 0.027
CL, cm 2.12 (1.95–2.32) 2.20 (1.84–2.38) 0.593
Funneling 13 (14.0) 4 (23.5) 0.296
IOS strain 0.28 (0.22–0.37) 0.30 (0.24–0.36) 0.753
EOS strain 0.33 (0.26–0.39) 0.36 (0.25–0.47) 0.442
IOS/EOS 0.89 (0.75–1.03) 0.85 (0.76–0.96) 0.492
Strain mean level within 0.5 cm 0.31 (0.24–0.39) 0.36 (0.27–0.44) 0.284
Strain mean level within 1.0 cm 0.31 (0.24–0.38) 0.32 (0.24–0.43) 0.614
Strain mean level within 1.5 cm 0.33 (0.27–0.40) 0.33 (0.27–0.42) 0.849
ECI within 0.5 cm 5.24 (3.72–6.70)] 7.39 (5.08–9.16) 0.023
ECI within 1.0 cm 4.73 (3.20–5.61) 6.26 (4.00–7.81) 0.011
ECI within 1.5 cm 4.20 (3.00–5.04) 5.76 (3.93–6.96) 0.009
Hardness ratio within 0.5 cm 57.29 (44.32–72.21) 50.14 (35.06–65.81) 0.376
Hardness ratio within 1.0 cm 59.02 (45.28–72.06) 56.06 (37.78–73.05) 0.7 85
Hardness ratio within 1.5 cm 54.48 (41.37–66.77) 55.84 (37.85–68.65) 0.954
Data are presented as the median (interquartile range) or number (%).
P values less than 0.05 are shown in bold.
sPTD = spontaneous preterm delivery, BMI = body mass index, DM = diabetes mellitus, HTN = hypertension, GA
= gestational age, CL = cervical length, IOS = internal os of cervix, EOS = external os of cervix, ECI = elasticity
contrast index.
Table 5. Comparison of AUCs between CL and other models for the prediction of sPTD (< 37 weeks) in subjects
with CL ≥ 1.5 cm (n = 110)
Variables AUC P valuea
CL 0.5411 -
ECI within 0.5 cm 0.6743 0.286
ECI within 1.0 cm 0.6948 0.216
ECI within 1.5 cm 0.6996 0.213
GA at CL 0.6698 0.172
PreBMI, kg/m20.6842 0.113
CL + ECI within 0.5 cm 0.6812 0.155
CL + ECI within 1.0 cm 0.7008 0.115
CL + ECI within 1.5 cm 0.7034 0.119
CL + GA at CL + preBMI 0.7153 0.047
CL + GA at CL + preBMI + ECI within 0.5 cm 0.7958 0.003
CL + GA at CL + preBMI + ECI within 1.0 cm 0.8256 < 0.001
CL + GA at CL + preBMI + ECI within 1.5 cm 0.8201 < 0.001
P values less than 0.05 are shown in bold.
AUC = area under receiver operating characteristic curve, CL = cervical length, ECI = elasticity contrast index, GA
at CL = gestational age at cervical length measurement, preBMI = pre-pregnancy body mass index.
aComparison between CL alone and other models.
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At current stage, the clinical application to cervix either by strain elastography (manual or
internal compression) or by shear wave elastography needs to provide reproducibility data
and requires further validation with larger study population.
Our study demonstrated that there was no dierence between pregnancies with and without
sPTD in terms of both the elastographic parameters and CL. However, aer analyzing the
subgroup of women whose CL were between 1.5 and 2.5 cm, there was a signicant dierence
in ECI scores within 0.5/1.0/1.5 cm from the cervical canal. Our data also suggested that a
combination of multiple parameters including both the E-cervix parameters and CL may help
predict sPTD in women with a moderately short CL.
As a response to the limitation of CL measurement in predicting preterm delivery, cervical
elastography has recently been recognized as an important research agenda, possibly as
a better prediction tool for preterm birth.34 Various studies began to test this technology,
targeting both low- and high-risk population (Table 6). Studies that analyzed the low-risk
population have collectively suggested that the strain value in the internal os or anterior
cervical lip is associated with sPTD. Studies targeting the high-risk population showed
similar diagnostic performances as our own study in terms of AUC analysis. A study by
Woźniak et al.27 including 109 women with a short CL (≤ 2.5 cm) demonstrated that a red
color (so) strain in the internal os showed an AUC of 0.84 for elastography and 0.68 for
CL in prediction of preterm birth. In addition, von Schöning et al.25 revealed that the mean
proportion of the sti area within the ROI showed an AUC of 0.711 for elastographic ndings
and 0.604 for CL in predicting sPTD in women with preterm labor at 23–34 weeks. Despite
such similarities, most of these studies used semi-quantitative method in elastographic
assessment only using colors.
In our study, we compared multiple elastographic parameters including strain mean level,
ECI, and hardness ratio. Among these parameters, the ECI score was found to be crucial in
our study population. The ECI score was originally introduced as a semi-quantitative score for
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0
0
0.50 0.750.25 1.00
1.00
0.75
0.50
0.25
Sensitivity
1-Specificity
AUC = 0.749
Cuf-off probability = 0.197
Fig. 3. Receiver operating characteristic curve using the predicted probability calculated from the logistic
regression model using CL, pre-pregnancy BMI, GA at CL measurement, and parameters of ECI within 1.5 cm from
the cervical canal.
AUC = area under receiver operating characteristic curve, BMI = body mass index, CL = cervical length, GA at CL =
gestational age at cervical length measurement, ECI = elasticity contrast index.
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Table 6. Summary of studies predicting spontaneous preterm birth using elastography
Year Study Design Risk group Total Prevalence of
sPTD
Ultrasound
system
Compression ROI Assessment of
elastography
Comparison Results
2014 Köbbing
et al.18
Prospective
cohort study
Low-risk
(11–36 wk)
182 17 (11.9) Toshiba
Aplio XG
External
(manually)
Four circular
ROIs in anterior
lip of cervix
Strain measurements
using TDI-Q software
Strain ratio (endo/midcx)
between preterm and term
delivery groups
Strain ratio R selective
was identified as the best
predictor of sPTD
2014 Wozniak
et al.26
Prospective
observational
study
Low-risk
(18–22 wk)
333 45 (8.2) Samsung
Medison V20
Internal
(patients'
breathing,
arterial
pulsation)
IOS Subjective IOS color
assessment: red (soft),
yellow (medium soft),
blue (medium hard),
purple (hard)
Frequency of preterm
deliveries in various
categories of IOS
assessment
sPTD < 37 weeks were
higher in the red and
yellow groups
2015 Hernandez-
Andrade
et al.16
Cross-
sectional
study
Low-risk
(11–28 wk)
566 35 (10.5) Hitachi Hi
Vision
External
(manually)
Circular
endocervical
area in the IOS
The percentage of
tissue displacement
or deformation that
resulted during the
manual application of
oscillatory pressure
IOS endocervical strain
among sPTD ≤ 34, < 37
weeks, and term delivery
groups
Strain in the 3rd and
4th quartiles in IOS has
increased risk of sPTD
≤ 34, < 37 weeks
2015 Sabiani
et al.22
Prospective
longitudinal
study
Low-risk
(exam in each
trimester)
72 9 (12.5) Hitachi Hi
Vision
External
(manually)
1 cm2 at anterior
and posterior lip
EI = E ant. Lip/(E ant.
Lip + E post. Lip)
Unfavorable outcome
(PTD, PPROM, Em cerclage)
between low and high
EI groups
Low EI was associated
with unfavorable
outcomes
2014 Swiatkowska-
Freund
et al.24
Not stated High-risk
(preterm
uterine
contractions
at 22–36 wk)
44 21 (47.7) Samsung
Medison V10
Internal
(patients'
breathing,
arterial
pulsation)
A circle of 5 mm
in diameter was
placed in each of
five regions
Elastography index,
five-step (0–4) color
scale in anterior.wall,
posterior wall, IOS,
EOS and cervical canal
Correlation between EI for
different parts of the cx
and risk of sPTD, and time
from exam to delivery
Significant correlation
between EI of IOS and
time from exam to
delivery and also risk of
sPTD
2015 von Schöning
et al.25
Prospective
cohort study
High-risk
(preterm
labor at
23–34 wk)
64 25 (39.1) Hitachi
Hi Vision
Preirus
No
additional
pressure
Rectangular
ROI including
the cervix and
cervical canal
Color scale: blue
(stiff), green (average),
red (deformable)
Correlation between stiff
tissue and preterm birth
The mean proportion of
the blue area correlated
significantly with preterm
birth
2015 Woźniak
et al.27
Prospective
observational
study
High-risk
(CL ≤ 25 mm
at 18–22 wk)
109 45 (41.3) Samsung
Medison V20
Internal
(patients'
breathing,
arterial
pulsation)
IOS Subjective IOS color
assessment: red (soft),
yellow (medium soft),
blue (medium hard),
purple (hard)
Percentage of PTDs in
various categories of
elastographic cervical
assessment
The number of PTDs was
significantly higher in the
red group, than in the
blue and purple groups
2015 Muller
et al.19
Cross-
sectional
study
High-risk
(preterm
uterine
contraction
at 24–35 wk)/
control group
81/110 10 (12)/
5 (4.3)
Aixplorer
SuperSonic
Imagine
Acoustic
radiation
force impulse
(shear wave)
A circle of 8 mm
in diameter was
placed in lower
anterior part of
the cervix
Shear wave speed Shear wave speed in
preterm labor or preterm
birth (compared to control)
Shear wave speed was
significantly reduced in
patients diagnosed with
pre-term labor and in
patients who actually
delivered preterm
2018 Agarwal
et al.14
Prospective
observational
study
High-risk
(preterm
uterine
contractions
at 28–37 wk)
34 14 (41.2) Siemens
Healthcare
Acuson
S2000
Acoustic
radiation
force impulse
(shear wave)
Rectangular ROI
(10 × 6mm sized)
was placed on
the anterior wall
of the internal os
5 color EI and shear
wave velocity
EI and shear wave speed
between preterm and term
birth group
Significant higher EI and
lower shear wave speed
was observed in preterm
birth compared to term
birth group
Data are presented as number (%).
sPTD = spontaneous preterm delivery, ROI = region of interest, IOS = internal os, EI = elastography index, EOS = external os of cervix, EI = elasticity index, PTD = preterm delivery.
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assessing mass in thyroid ultrasonography.35 In addition, it was shown to discriminate benign
from malignant lesions in the parotid gland, performing an adjunctive role in enhancing the
diagnostic performance of gray-scale ultrasound.36 ECI scores are calculated from the strain
map to quantify the local stiness contrast within a nodule or ROI.35 For example, if there are
mainly red (hard) pixels or pixels with a color close to red (hard) in the ROI, the contrast of
the color in the ROI is small, and the ECI value will accordingly be small. On the other hand, if
there is an equal mixture of red (hard) and purple (so), the contrast of the color in the ROI is
high and the ECI score will be larger. It is the same with purple (so) pixels.
It is noteworthy that we performed subgroup analysis aer excluding women with a severely
short CL (< 1.5 cm) who account for about 15% of our initial study population. The rationale
behind this division is that in a study including patients with an asymptomatic short cervix
less than or equal to 1.5 cm, nearly a fourth of patients have intra-amniotic infection/
inammation and 40% of them delivered within 1 week from amniocentesis. Hence,
patients with severely short cervix are less likely to benet from screening and prophylactic
administration of progesterone.37,38 A recent meta-analysis of individual patient data was
also consistent with this.39 In our study, there was no signicant dierence in the ECI score
between the preterm and term delivery groups of women with CL ≤ 1.5cm. Therefore, the
diagnostic performance of ECI in the prediction of sPTD was limited to women with a
short CL between 1.5 and 2.5 cm. Our interpretation of this data is based on the fact that
the mechanical changes in the composition of the cervix are closely related to the ripening
process. Indeed, cervical ripening was proved to be associated with in vivo change in the
elasticity of the cervix in the animal model.40 The biochemical change associated with a short
CL such as the decreased collagen and increased water concentration should already be far
advanced in the subgroup with CL less than 1.5 cm. Therefore, the cervix has already become
homogenous in terms of biochemical composition in this subgroup, precluding the use of
the ECI score to dierentiate subsequent preterm delivery from term delivery. Given that
the actual preterm birth rate is about 45% in women with CL ≤ 1.5 cm, cervical elastography
may not convey additional information in these women with severely short cervix. Instead,
women with CL between 1.5 and 2.5 cm, in whom preterm births occurred in about 16%
in our study population, can benet from cervical elastography. As we have very small
number (n = 17) of patients with sPTD in patients with CL between 1.5 and 2.5 cm, there is a
possibility of overtting in the prediction model. A larger study looking into the usefulness of
E-Cervix elastography will help address the issue, which is under way.
ACKNOWLEDGMENT
The ultrasound machines (WS80A Ultrasound System with E-Cervix function) were provided
by Samsung Medison Company (Seoul, Korea) to four institutions during the study period.
We thank Dr. Eun Jeong Choi, Dr. Yoo Min Kim and Dr. Mina Kim for their invaluable
contributions in patient enrollment and data acquisition for this study. We also thank former
KSUOG presidents, Professor Sa Jin Kim (The Catholic University of Korea, College of
Medicine) and Professor Joong Shin Park (Seoul National University College of Medicine) for
their warm supports during the study period.
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PUBMED | CROSSREF
14/14
https://jkms.org https://doi.org/10.3346/jkms.2019.34.e68
Cervical Elastography in Short Cervix
Provisional
Provisional