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doi:10.1111/jog.14243 J. Obstet. Gynaecol. Res.

2020

Efficacy of intraoperative wireless ultrasonography for


uterine incision among patients with adherence findings
in placenta previa

Min J. Choi , Chan M. Lim, Dahoe Jeong, Hae-Rin Jeon, Kyung J. Cho and Suk Y. Kim
Department of Obstetrics and Gynecology, Gachon University Gil Medical Center, Incheon, Korea

Abstract
Aim: We evaluated the effectiveness of intraoperative wireless ultrasonography in determining the location
of uterine incision during cesarean delivery in patients with placenta previa who have sonographic adher-
ence findings in order to assess intraoperative blood loss and maternal morbidity.
Methods: A prospective study using wireless sonography, including 15 patients with previa, was conducted
among women with singleton pregnancies who delivered by cesarean section between August 1, 2017, and
August 30, 2019. Retrospective study for the control group included 32 patients with placenta previa who
underwent cesarean section between January 1, 2016, and July 31, 2017, without wireless sonography.
Patients with previa who had adherence findings in prenatal sonography were included in both groups.
Logistic regression was used to identify the association between massive intraoperative bleeding loss and
use of wireless ultrasound sonography.
Results: Intraoperative blood loss was significantly reduced in the study group compared to that in the con-
trol group (P = 0.009). The hospital stay was significantly shorter in the study group compared to the control
group (5 days vs 6 days, P < 0.001). The use of intraoperative wireless sonography (P = 0.01) had a signifi-
cant association with massive intraoperative hemorrhage in multivariable analysis.
Conclusion: Our study is the first study to apply a wireless ultrasound sonography device in women with
placenta previa during cesarean section to examine maternal morbidity. This latest wireless ultrasound
sonography device is advantageous for uterine incision guidance in women with placenta previa and
improves maternal morbidity by reducing intraoperative hemorrhage.
Key words: intraoperative hemorrhage, intraoperative sonography, placenta previa, uterine incision.
wireless ultrasonography.

Introduction lead to an increase in maternal and neonatal morbid-


ity and mortality.2–4 The study by Gibbins et al.
Placenta previa is defined as the placenta implanted reported that the maternal mortality ratio is increased
in the lower uterine segment, either over or near the approximately threefold for women with placenta
internal cervical os.1 The incidence of placenta previa previa.5
has risen over the past 30 years, with an average inci- For practical reasons, patients with placenta previa
dence of 0.3%–0.5%.2 Obstetricians should be aware undergo cesarean delivery and have a risk of massive
of the possibility of antepartum, intrapartum and bleeding during the operation.6 Massive intraoperative
post-partum hemorrhage, which can subsequently hemorrhage is related to the location of the placenta,

Received: October 17 2019.


Accepted: March 7 2020.
Correspondence: Professor Suk Y. Kim, Department of Obstetrics and Gynecology, Gachon University Gil Medical Center,
21 Namdong-daero 774beon-gil, Namdong-gu, Incheon 21565, Korea. Email: ksyob@gilhospital.com

© 2020 Japan Society of Obstetrics and Gynecology 1


M. J. Choi et al.

as well as surgical procedures, such as uterine incision, the internal cervical ostium to the placental edge of
and the placental separation site due to placenta the anterior wall than that of the posterior wall.9 We
adherence.3,7 also included posterior placental previa defined if the
In patients with placenta previa, it is necessary to distance from the internal cervical ostium to the pla-
check these conditions and perform imaging studies, cental edge was longer in the uterine posterior wall
such as ultrasound sonography or magnetic resonance than in the anterior wall. In other words, even though
imaging (MRI), before cesarean delivery in order to it is posterior placentation, placenta covers some part
precisely determine the best location for uterine inci- of anterior wall as well. Therefore, we believe that
sion. Placental injury by an inappropriate uterine inci- mobile wireless sonography would be also helpful to
sion can lead to massive maternal blood loss and fetal find clear vision of placenta edge to avoid transpla-
injury during cesarean section.7 Fan et al. conducted cental incision in posterior placenta previa.
cesarean section with ultrasound sonography to deter- Uterine incision was made either low transverse or
mine the placental position, and designed the uterine body transverse depending on the placentation. The
incision before delivery.8 We believe that it is more body transverse incision was 2–3 cm upper apart
effective to localize the placental position and mark from the conventional low transverse incision since it
the location of the uterine incision directly on the was inevitable to make a body transverse uterine inci-
uterus ahead of delivery by recently developed wire- sion to avoid a transplacental approach.
less mobile ultrasonography (US) in operation field Medical records were reviewed in order to collect
rather than transecting the placenta. data on maternal, neonatal and operative characteris-
Therefore, the aim of the present study was to eval- tics, including the volume of blood loss, transfusion
uate the effectiveness of intraoperative wireless US for rate, operative duration, hospitalization days and neo-
determining the best location for uterine incision dur- natal Apgar scores. The exclusion criteria were multi-
ing cesarean delivery in patients with placenta previa ple pregnancy, placental abruption, uterine rupture,
in order to assess intraoperative blood loss and intrauterine fetal death, intrauterine infection, pre-
reduce maternal morbidity. eclampsia, diabetes mellitus (including gestational
diabetes mellitus), intrauterine fetal death and hema-
tologic disorders. All patients in the study group pro-
Methods vided informed consent.
Sonographic assessment with a wireless mobile US
A prospective study using wireless sonography, device and a tablet PC (SONON, 300L, Healcerion Inc.,
including 15 patients with previa, was conducted Seoul, South Korea) was performed in real-time scan-
among women with singleton pregnancies who deliv- ning directly on the uterus to check fetal presentation
ered by cesarean section at our institute, a tertiary and placentation during cesarean section (Fig. 1). This
university center between August 1, 2017, and August wireless US device uses wireless signals to transfer
30, 2019. Patients with previa who had sonographic images to a display system that shows the images in
adherence findings were included in the study group. real time. The sonography probe was covered with an
Patients with placenta previa who also had adherence aseptic plastic coverage and connected to a portable
findings in prenatal sonography and underwent tablet via Bluetooth (Fig. 2). Since the sonography
cesarean section between January 1, 2016, and July device is connected to a tablet PC, the operator can
31, 2017, were included in the control group before check fetal presentation and find the nearest placental
we adopted up-to-date wireless mobile US. The study edge for uterine incision directly on the uterus (Fig. 3).
was approved by the Institutional Review Board, an Captured images were saved and collected on the tab-
ethics committee (assigned number: GDIRB2017-201). let. For the control group, the determination of uterine
In the present study, we reviewed the types of pla- incision was dependent on the operator’s experience
centa previa (complete, partial or marginal placenta with prenatal sonographic findings.
previa), the position of placental attachment (anterior Demographic and obstetric characteristics included
or posterior wall attachment) and sonographic adher- maternal age, gestational age at delivery, parity, type of
ence findings, such as placental lacunae, lack of a previa (total or low-lying), position of the placenta
clear zone, sponge-like appearance of the cervical wall (anterior or posterior), number of previous cesarean sec-
and bladder wall disruption. Anterior placentation tions and preoperative serum hemoglobin level. Mater-
with previa was defined by a longer distance from nal morbidity was assessed by several indicators

2 © 2020 Japan Society of Obstetrics and Gynecology


Wireless sonography and placenta previa

Figure 1 (a) Wireless mobile ultrasonography (SONON 300L) and (b) tablet PC.

including total amount of intraoperative bleeding loss, Mann–Whitney test or Student t-test, as appropriate.
intraoperative transfusion rate, transfusion unit of Percentages were compared using Fisher’s exact test or
packed red blood cell, post hemoglobin, hemoglobin Pearson’s chi-square test. Gestational age converted to
changes between preoperation and postoperation, decimal scale was used. In addition, the association
requirement for additional procedures (uterine artery between clinical characteristics and intraoperative hem-
embolization or hysterectomy), duration of hospitaliza- orrhage was analyzed using univariable and multivari-
tion, post-partum fever higher than 38 C and serum C- able logistic regression analysis, respectively. A P-value
reactive protein level. less than 0.05 was considered statistically significant.
Data were also collected regarding duration of the
operation (min), neonatal injury and neonatal Apgar
scores. The operation time was measured from the Results
time of skin incision to the time of skin closure. The
intraoperative bleeding loss was also measured dur- The maternal and obstetric characteristics are shown
ing the operation; 1 min and 5 min Apgar scores of in Table 1. There were no significant differences
less than 7 were assessed for neonatal morbidity. In between the two groups in terms of patient character-
the present study, we defined intraoperative hemor- istics. Overall, the median maternal age was 35 for
rhage if the total blood loss during the operation was the study group and 33.5 years old for the control
more than 1000 mL. group. In the study group, 11 (73.3%) patients had
Statistical analysis was performed via IBM SPSS statis- complete placenta previa, and in the control group,
tics version 22 and presented as the median and inter- 25 (78.1%) had complete placenta previa. The median
quartile range. Continuous data were analyzed using gestational age at delivery, rate of previous cesarean

Figure 2 Wireless mobile ultrasonography with an aseptic coverage.

© 2020 Japan Society of Obstetrics and Gynecology 3


M. J. Choi et al.

Figure 3 (a) Mapping of uterine incision site and (b) localization of uterine incisional site in edge of placenta.

section and the rate of placental position (anterior 20%) required intraoperative transfusion in the study
position and posterior position) were also similar group than in the control group (37.5%). In addition,
between the two groups. only one patient in the control group underwent post-
The maternal outcomes regarding intraoperative partum hysterectomy, while no patients in the study
hemorrhage and neonatal morbidity are compared group underwent post-partum hysterectomy. Moreover,
between the two groups in Table 2. We found that the two patients had a postoperative fever (6.3%). The pre-
intraoperative blood loss in the study group was signifi- sent study found no significant differences in fetal
cantly reduced in the study group compared to the con- injury rates and neonatal outcomes between groups.
trol group (750 mL vs 1000 mL, respectively; P = 0.009). Table 3 shows the results of univariable and multivar-
In addition, the duration of hospital stay was signifi- iable logistic regression analyses performed to assess
cantly shorter in the study group compared to the the association between massive intraoperative bleeding
patients who underwent cesarean section without wire- loss and potential variables. Only the use of wireless
less sonographic study (5 days vs 6 days, P < 0.001). mobile US was significantly associated with massive
Although there was no significant difference between intraoperative hemorrhage in univariate analysis (odds
the two groups, it was shown that fewer patients (n = 3, ratio [OR]: 0.249, 95% confidence interval [CI]:

4 © 2020 Japan Society of Obstetrics and Gynecology


Wireless sonography and placenta previa

Table 1 Characteristics of patients with sonographic adherence findings in placenta previa (n = 47)†
Characteristic Wireless sonography Wireless sonography P-value
(+) (n = 15) (−) (n = 32)
Maternal age (years), median 35 (31–37) 33.5 (31.50–35.75) 0.395
Parity, n (%)
0 8 (53.3) 18 (56.3)
1 5 (33.3) 9 (28.1) 0.979
2 2 (13.3) 5 (15.6)
Gestational weeks at delivery 37.9 (35.5–38.4) 37.2 (32.07–38.30) 0.417
Types of previa, n (%)
Complete 11 (73.3) 25 (78.1) 0.725
Low-lying 4(26.7) 7 (21.9)
Number of previous cesareans, n (%)
0 11 (73.3) 25 (76.6) 0.725
1 4 (26.7) 7 (21.9)
Position of placenta
Anterior 6 (40) 8 (25) 0.295
Posterior 9 (60) 24 (75)
Preoperative serum hemoglobin level (g/L) 11.7 (11.1–12.4) 12 (11.50–12.60) 0.223
†Values are given as number (percentage) or median (interquartile range).

0.07–0.95, P = 0.043). However, the use of both It is well known that the following factors are likely
intraoperative wireless sonography (OR: 0.065, 95% CI: to increase incidence of massive hemorrhage: anterior
0.01–0.52, P = 0.01) and previous cesarean section (OR: placentation, presence of antenatal ultrasonic placen-
7.527, 95% CI: 1.161–48.80, P = 0.034) were revealed to tal adherence findings, cesarean section history and a
have a significant association with massive transplacental approach.3,6,10 In women with one or
intraoperative hemorrhage in multivariable analysis. more of these conditions, obstetricians should prepare
to encounter profuse bleeding during the cesarean
section.11–13
Discussion In order to reduce intraoperative bleeding loss,
Verspyck et al. compared maternal outcomes between
The present study demonstrated that intraoperative transection of the placenta and avoiding incision of the
wireless ultrasound sonography can effectively iden- anterior placenta by sonographic localization of the pla-
tify the location for uterine incision, thereby reducing centa among patients with anterior placenta previa.
intraoperative hemorrhage in women with placenta They found that the loss of intraoperative hemoglobin
previa in whom placenta accrete cannot be ruled out count and the frequency of maternal blood transfusion
via prenatal sonography. during or after cesarean section were significantly

Table 2 Clinical outcomes in patients with placenta previa (n = 47)


Characteristic Wireless sonography Wireless sonography P-value
(+) (n = 15) (−) (n = 32)
Operation time (min) 70 (65–100) 80 (66.25–93.75) 0.828
Intraoperative blood loss (mL) 750 (500–1000) 1000 (762.5–1175) 0.009*
Intraoperative transfusion rate (%) 3 (20) 12 (37.5) 0.321
Hospitalization (days) 5 (5–6) 6 (6) <0.001*
Postoperative uterine artery embolization, n (%) 1 (6.7) 1 (3.1) 0.541
Hysterectomy, n (%) 0 (0) 1 (3.1) 0.999
Postoperative serum hemoglobin level (g/L) 9.4 (8.6–10.2) 9.8 (8.73–10.48) 0.833
Changes in hemoglobin (g/dL) 2.2 (1.5–2.6) 2.4 (1.50–2.35) 0.504
Postoperative CRP level (mg/dL) 6.91 (3.50–8.45) 6.1 (3.42–7.03) 0.228
Postoperative fever, n (%) 0 2 (6.3) 0.999
Birth weight (g) 2960 (2614–3040) 2727 (1730.0–3087.5) 0.283
1-min Apgar score (<7) 1 (6.7%) 2 (6.3) 0.999
5-min Apgar score (<7) 0 0
*p < 0.05. and CRP, C-reactive protein.

© 2020 Japan Society of Obstetrics and Gynecology 5


M. J. Choi et al.

Table 3 Logistic regression model to assess association between intraoperative massive hemorrhage and potential
variables
Characteristic Univariable analysis, P-value Multivariable analysis, P-value
odds ratio (95% CI) odds ratio (95% CI)
Wireless sonography 0.249 (0.065–0.954) 0.043* 0.065 (0.008–0.524) 0.01*
Previous cesarean section 3.733 (0.847–16.452) 0.082 7.527 (1.161–48.799) 0.034*
Anterior placenta 2.443 (0.670–8.901) 0.176 4.487 (0.863–23.322) 0.074
Previa totalis 1.2 (0.310–4.651) 0.792 0.845 (0.152–4.692) 0.847
Prehemoglobin 0.906 (0.503–1.631) 0.742 0.511 (0.234–1.118) 0.093
Gestational age at delivery 0.944 (0.787–1.133) 0.535 1.157 (0.905–1.479) 0.246
*p < 0.05. and CI, confidence interval.

reduced.14 They recommended that determining the at the placenta; this may be considered to lead to
location of the placenta with US before delivery could more incisional site bleeding since the uterine body is
be useful technique for precise uterine incision to avoid thicker than the lower uterine segment.3 However,
transect placenta. using intraoperative sonography, Kotsuji et al. demon-
There are several other studies that use ultrasound strated the feasibility and safety of transverse fundal
sonography or other imaging, such as MRI, to localize incision in women with placenta previa, in whom pla-
uterine incision in order to avoid rapid transecting pla- centa accrete could not be ruled out.11 They stated
centa and reduce intraoperative hemorrhage. Indeed, that performing transverse fundal incision, compared
Frank et al. conducted mapping of the placenta location to conventional low transverse incision transecting
with real-time sonography to decide the incision site the placenta, in patients with anterior placenta previa
and type.4 They found that patients with paraplacental and possible placenta accrete led to less blood loss
incision had reduced maternal morbidity with during cesarean section, as well as a clear visualiza-
decreased intraoperative blood loss while patients with tion of the operation field.11 The present study
conventional transplacental incision required transfu- showed that total amount of intraoperative bleeding
sion.4 Furthermore, Cao et al. reported that three- loss was significantly reduced even though a study
dimensional (3D) MRI provided accurate guidance for group had more patients with anterior placentation
uterine incision in placenta previa, and avoided placen- about 40% than a control group, 25%. We believe that
tal injury during cesarean section. They found that it demonstrates the operative usefulness of the wire-
patients with previa who underwent 3D MRI modeling less US in placenta previa, since the result was led by
for uterine incision guide had less intraoperative blood avoiding transplacental incision with wireless sonog-
loss and a shorter operative time compared to the con- raphy although body incision can increase blood loss.
trol group. Moreover, the transfusion frequency was As well as the reduction in intraoperative hemor-
also significantly reduced in the 3D MRI study.7 rhage and shorter hospitalization stay, a further sig-
Consistent with the abovementioned studies, the pre- nificant advantage of this procedure is that the
sent study showed that mapping uterine incision by operator is able to identify the placental margin more
intraoperative wireless US led to significantly reduced accurately, comforting operators to make uterine inci-
intraoperative blood loss compared with patients who sion with less surgical site bleeding in a relaxed con-
underwent cesarean procedures with random uterine dition. Wireless US is a cost-effective, safe and simple
incision (750 mL vs 1000 mL, respectively; P = 0.009). In device that can be adapted by obstetricians and
addition, the results showed that performing cesarean applied successfully when compared to MRI examina-
section using the new procedure is associated with less tion. Furthermore, it only requires a short time for
intraoperative hemorrhage based on the data from our setup and is easy to manage. Importantly, wireless
statistical analysis. It would seem that intraoperative US accurately reflects the state of the placenta at the
wireless US provides the physician with the exact pla- time of delivery; this included the location of vessels,
centa location and helps to make a precise uterine inci- placental location and fetal presentation.
sion, leading to reduced incisional site bleeding; thus, The present study is the first study to apply a wire-
decreasing the intraoperative bleeding loss. less US device in women with placenta previa during
Body or fundal transverse uterine incision in ante- cesarean section. Wireless mobile US has poor image
rior placenta previa was inevitable to avoid incision quality and visual angle compared to conventional

6 © 2020 Japan Society of Obstetrics and Gynecology


Wireless sonography and placenta previa

US. However, an important aspect of the mobile US is 2. Kollmann M, Gaulhofer J, Lang U, Klaritsch P. Placenta
the portability and easiness of handling in a more praevia: Incidence, risk factors and outcome. J Matern Fetal
Neonatal Med 2016; 29: 1395–1398.
convenient way. With these reasons, it is applied to
3. Baba Y, Matsubara S, Ohkuchi A et al. Anterior placentation
various cases in other fields as well. For examples, it as a risk factor for massive hemorrhage during cesarean
provides more accurate needle placement in all body section in patients with placenta previa. J Obstet Gynaecol Res
joints, guide a biopsy needle and arterial line inser- 2014; 40: 1243–1248.
tion, finding vessels prior to injection and other 4. Frank H, Boehm M, Arthur C, Fleischer MD, Jeffrey M,
Barrett MD. Sonographic placental localization in the deter-
interventions.
mination of the site of uterine incision for placenta previa.
In terms of the study limitations, the sample size J Ultrasound Med 1982; 1: 311–314.
was small (n = 47), and the study was conducted in a 5. Gibbins KJ, Einerson BD, Varner MW, Silver RM. Placenta
single center. Therefore, a multicenter prospective previa and maternal hemorrhagic morbidity. J Matern Fetal
randomized clinical study regarding criteria for appli- Med 2017; 31: 494–499.
6. Hasegawa J, Nakamura M, Hamada S et al. Prediction of
cation of the device should be conducted in the
hemorrhage in placenta previa. Taiwan J Obstet Gynecol 2012;
future. 51: 3–6.
In conclusion, we suggest that the wireless US 7. Cao Y, Wei Y, Yu Y, Wang Z. Safety and efficacy of a novel
mobile device is advantageous for uterine incision three-dimensional magnetic resonance imaging model for
guidance in women with placenta previa and uterine incision in placenta previa. Int J Gynaecol Obstet 2017;
139: 336–341.
improves maternal morbidity as a result of reducing
8. Fan D, Wu S, Ye S et al. Random placenta margin incision
intraoperative hemorrhage. for control hemorrhage during cesarean delivery compli-
cated by complete placenta previa: A prospective cohort
study. J Matern Fetal Neonatal Med 2019; 32: 3054–3061.
9. Jing L, Wei G, Mengfan S, Yanyan H. Effect of site of placen-
Acknowledgments tation on pregnancy outcomes in patients with placenta
previa. PLoS One 2018; 13: e0200252.
This research was partly supported by the Gachon Uni- 10. Hasegawa J, Matsuoka R, Ichizuka K et al. Predisposing fac-
versity Gil Medical Center (Grant number: FRD2015-02) tors for massive hemorrhage during cesarean section in
and the Next-Generation Medical Device Development patients with placenta previa. Ultrasound Obstet Gynecol
Printogram for Newly-Created Market of the National 2009; 34: 80–84.
11. Kotsuji F, Nishijima K, Kurokawa T et al. Transverse uterine
Research Foundation (NRF) funded by the Korean Gov-
fundal incision for placenta praevia with accreta, involving
ernment, MSIP (No. 2015M3D5A1065907). the entire anterior uterine wall: A case series. BJOG 2013;
120: 1144–1149.
12. Nishida R, Yamada T, Akaishi R et al. Usefulness of trans-
Disclosure verse fundal incision method of cesarean section for women
with placentas widely covering the entire anterior uterine
wall. J Obstet Gynaecol Res 2013; 39: 91–95.
None declared.
13. Silver RM. Abnormal placentation: Placenta previa, vasa
previa, and placenta accreta. Obstet Gynecol 2015; 126:
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© 2020 Japan Society of Obstetrics and Gynecology 7

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