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European Journal of Obstetrics & Gynecology and Reproductive Biology 179 (2014) 125129

Contents lists available at ScienceDirect

European Journal of Obstetrics & Gynecology and


Reproductive Biology
journal homepage: www.elsevier.com/locate/ejogrb

Successful treatment of cervical incompetence using a modied


laparoscopic cervical cerclage technique: a cohort study
Lu Luo, Shu-qin Chen 1, Hong-ye Jiang, Gang Niu, Qiong Wang, Shu-zhong Yao *
Department of Obstetrics and Gynecology, the First Afliated Hospital of Sun Yat-sen University, Guangdong Provincial Key Laboratory of Reproductive
Medicine, Guangzhou, Guangdong, PR China

A B S T R A C T

Article history:
Received 10 July 2013
Received in revised form 14 February 2014
Accepted 23 May 2014

Objective: We introduce a modied surgical method for laparoscopic cervical cerclage (LCC) and compare
the operative data and obstetric outcomes to those obtained by traditional vaginal cerclage (TVC).
Study design: This is a prospective cohort study in a university-afliated hospital from August 2008
through February 2013. Nineteen patients treated by LCC were prospectively monitored and the
treatment outcomes were compared to a control group consisted of 25 patients that were retrospectively
studied and treated with TVC using traditional McDonald suture. Laparoscopic cervical cerclage was
performed with Mersilene tape and a modied surgical technique. Perioperative complications and
obstetric outcomes were compared between LCC and TVC treatment groups.
Results: No perioperative complications occurred during LCC treatment. Of the 19 LCC patients, 15 (78.9%)
became pregnant during the study period. The fetal salvage rate was 92.3% (12/13) and no adverse events
were encountered. The mean gestational age in LCC group was 36.4 weeks, and it was 17.4 weeks longer
than their previous pregnancy age, which was signicantly higher than obtained by TVC.
Conclusion: This modied technique for laparoscopic cervical cerclage demonstrates good obstetric
outcomes with low risk of adverse events, which may provide a reasonable alternative to achieve
pregnancy success in patients with cervical incompetence.
2014 Elsevier Ireland Ltd. All rights reserved.

Introduction

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Keywords:
Cervical cerclage
Laparoscopy
Vaginal cerclage
Cervical incompetence

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A R T I C L E I N F O

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Cervical incompetence is dened as the inability to retain an


intrauterine pregnancy to full term due to structural or
functional insufciency of the cervix [1]. It occurs in 0.5%1%
of all pregnancies and has a recurrence risk of up to 30% [2]. The
traditional vaginal approach of cervical cerclage during mid-term
pregnancy [3] has been used for several decades and is effective
for most patients. However, a small minority are not successfully
treated by the transvaginal approach. For example, patients with
anatomically deformed, deeply lacerated, or severely scarred
cervices from previous failed vaginal cerclage cannot be treated
by placement of a transvaginal suture. In 1965, transabdominal
cervical cerclage was rst described [4], and subsequent studies
reported successful results in patients for whom a vaginal
approach was deemed impossible. In recent years, a laparoscopic
cervical cerclage approach was described in several case series,

* Corresponding author at: 58 Zhongshan Er Road, Guangzhou, Guangdong


510080, PR China. Tel: +86 13602834127.
E-mail addresses: yszlfy@163.com, gzluolu@163.com (S.-z. Yao).
1
These authors contributed equally to this study.

and results compared favorably to the traditional laparotomy


approach [5].
The present study reports a series of cervical incompetence
cases treated by laparoscopic cervical cerclage (LCC) using a
modied surgical technique which is easy-operating, minimal
invasive and highly effective. Operative details and obstetric
outcomes were compared with those obtained using traditional
vaginal cerclage (TVC).
Materials and methods
A prospective observational cohort study was conducted from
August 2008 through February 2013 at the First Afliated Hospital
of Sun Yat-sen University (Guangzhou, China). The study was
approved by the institutional ethics board and informed written
consent was obtained from all patients. The indications for
laparoscopic cerclage included a history of cervical incompetence/insufciency, with or without congenital short cervix or
traumatic/surgical damage rendering the vaginal approach
difcult or previous failed transvaginal cerclage. Nineteen
patients were selected for LCC and were prospectively monitored
for perioperative and postoperative complications, conception
success, and successful delivery. We performed a parallel

http://dx.doi.org/10.1016/j.ejogrb.2014.05.032
0301-2115/ 2014 Elsevier Ireland Ltd. All rights reserved.

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L. Luo et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 179 (2014) 125129

Table 1
Patient demographics.
Demographic

LC groupa (n = 19)

VC groupb (n = 25)

Maternal age at cerclage (y, [median, range])


No. of prior T2c loss (median, range)
No. of preterm labor< 34 w (median, range)
Patients with prior failed vaginal cerclage (%)
No. of prior failed vaginal cerclage (median, range)
Prior gestational age (for pregnancies continued beyond the rst trimester [median, range])
Patients with cervical abnormality (laceration at delivery)
Patients with prior cone biopsy (%)

31 (2735)
2.5 (15)
0
n = 11 (57.8%)
1 (02)
21 (1627)
n = 4 (21.1%)
n = 1 (5.3%)

32 (2841)
2 (03)
0.24 (02)
n = 3 (12%)
0.08 (01)
23 (1730)
n=0
n=0

Note: There were no signicant differences of demographics between the two groups.
a
LC group, laparoscopic group.
b
VC group, vaginal group.
c
T2, second trimester.

Surgical preparation

retrospective analysis of 25 patients treated by TVC during the


same period. For TVC group, all patients were clinically diagnosed
with incompetent cervix before pregnancy and were treated with
prophylactic TVC using traditional McDonald suture in the second
trimester of pregnancy. The demographic data of the two
treatment groups is shown in Table 1.

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Preoperative preparations were similar to those of other


laparoscopic surgeries. The patient was prepared in the dorsal
lithotomy position with a urinary catheter in situ. A transcervical
uterine manipulator was used to facilitate uterine manipulation. A 3port operative laparoscopy system was used. Initial abdominal entry
is achieved through the closed Veress technique at the umbilicus.
Abdominal insufation was maintained at 1215 mmHg using CO2.
Step 1: development of the paravesical and vesicouterine spaces.
The vesicouterine peritoneum was incised using monopolar
forceps and a combination of sharp and blunt dissection. The

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Technique description

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For LCC group, prophylactic laparoscopic cerclage was performed as an interval procedure before pregnancy. The cerclages
were all placed in the same fashion by one surgeon.

Fig. 1. Intraoperative photographs illustrating the modied laparoscopic cervical cerclage method. (A) Step 1: Create paravesical and vesicouterine spaces. (B and C) Step 2:
Identify the contours of the uterine vessels on both sides of the uterine isthmus. (DG) Step 3: Place the Mersilene tape around the cervicourerine junction using a direct
suture technique. (H) Step 4: Ensure that the tape had not passed through the cervical canal by hysteroscopy. (I) Step 5: Tie the tape posteriorly with an intracorporeal knot.

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L. Luo et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 179 (2014) 125129
Table 2
Perioperative data.
Variable (median, range)

LC group
(n = 19)

VC group (n = 25)

Duration of surgery (min)


Blood loss during surgery (mL)
Hospital stay after surgery (days)
Patients with perioperative complications
(%)

29 (2055)
26 (2050)
2 (23)
n=0

18 (1035)
10 (015)
2.5 (24)
n = 1 (4%)

Note: There were no signicant differences of demographics between the two


groups.

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attempt conception immediately after surgery. The ideograph of


the surgery is shown in Fig. 2 and the surgical steps are shown in
Fig. 1AI.
The control group was treated by prophylactic traditional
McDonald vaginal cerclage with 5-mm Mersilene band during the
second trimester of pregnancy. In order to reveal fetal congenital
deformity, three dimensional ultrasonography was performed
during 1722 weeks of preganancy before surgery. The mean
pregnancy age of cerclage was 19.9 (17.022.6) weeks.

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Results

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Surgeries were successfully performed in all patients in both


the LCC and TVC treatment groups. There were no signicant
differences in the perioperative data between the two groups
although the duration of surgery seems slightly longer and blood
loss seems slightly more in LCC group (Table 2). In the laparoscopic
group, no patient required laparotomy, and no perioperative
complications occurred, such as uterine vessel bleeding, adjacent
organ damage or perioperative infection. In the TVC group, two
patients experienced postoperative pregnancy loss due to premature rupture of membranes one week after surgery.
The details of obstetric outcomes are presented in Tables 3 and
4. Fifteen of the patients undergoing LCC conceived during the
course of our study, while four were not yet pregnant, possibly due
to the short interval after surgery. One patient was still at her 18
weeks of gestation at writing, and was excluded in the following
analyses. The overall fetal salvage rate was dened as the number
of perinatal survival per number of pregnancies lasted more than
12 weeks of gestation.
In successful cases, we determined the gestational age at the
time of delivery. In the LCC group, there were 12 living children out
of 13 pregnancies for a 92.3% perinatal survival rate. All these
infants were discharged with their parents. In the TVC group, there
were 22 living children out of 25 pregnancies (88% perinatal
survival, all discharged with parents but one had sequelae of
prematurity). The mean gestational age for pregnancies beyond
the 1st trimester in the two groups were 36.4 and 34.7 weeks
respectively, which showed no statistically differences although
delivery age in LCC group seems longer. However, in LCC group, the
mean delivery age was 17.4 weeks longer than the previous

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bladder was retracted away from the lower uterine segment and
anterior cervix to create a vesicouterine space.
Step 2: identication of the contour of uterine vessels.
In step 2, the uterine vessels were identied. Incision of the
peritoneum was extended and the anterior leaf of the broad
ligament was opened. The contour of the uterine vessels were
identied on both sides of the uterine isthmus. Up to date
references, the standard step of cervico-isthmic cervical cerclage is
creation of broad ligament peritoneal window [6]. The posterior
peritoneum should be opened to create a window in the broad
ligament, which allows for caudal displacement of the ureters,
identication of the uterine vessels, and a space for a needle to be
passed through into the cervix. In our study, this step was
modied. Since we could clearly see the contours of the uterine
vessels, it was unnecessary to open a window in the broad
ligament.
Step 3: placement of suture material.
We used a 5-mm Mersilene tape with straight needle for direct
suture. To avoid uterine vessel and ureter damage, the straight
needle was carefully inserted into the exposed anterior surface of
the cervix on the right side at the level of the cervico-isthmic
junction and medially to the uterine vessels but not into the broad
ligament. The needle was passed through the muscular layer of
the cervix, with a small piece of cervical tissue remaining outside
the noose. The tape was passed in the anterior to posterior
direction, and the needle withdrawn from the posterior surface of
the cervix on the same side. In a similar fashion, the straight
needle was inserted in the anterior surface of the cervix on the left
side and passed in the anterior to posterior direction through the
muscular layer.
Step 4: hysteroscopy check and cerclage knot secured.
After placing the tape around the internal os, a hysteroscopy
check was conducted to ensure that the tape had not passed
through the cervical canal. The knot was rmly tied on the
posterior side to avoid potential bladder irritation. The tension of
the noose can be adjusted over a transcervical 6# Hegar dilator. The
visceral peritoneum was left unclosed.
At the conclusion of the procedure, the laparoscopic ports are
removed, the gas evacuated, and the abdominal wall and skin are
repaired in the usual fashion. A single dose of antibiotics was
administered perioperatively. All patients were encouraged to

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Table 3
Main outcome of LC group patients.

Fig. 2. Schematic chart of laparoscopic cervical cerclage insertion using our


modied surgical method.

Variable

LC group

Not pregnant
Still being pregnant
T1b loss
T2c loss
Preterm labor
Full-term labor

n = 4a
n=4
n=1
n=1
n=1
n=8

a
Three patients were not intent to be pregnant yet, one was with male-factor
infertility.
b
T1, rst trimester.
c
T2, second trimester.

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L. Luo et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 179 (2014) 125129

Table 4
Comparison of details of obstetric outcomes.
Variable

LC group (n = 10)

VC group (n = 25)

P value

No. of fetal loss in the second trimester (%)


No. of preterm labor (%)
No. of full-term labor (%)
Gestational age for patients beyond 1st trimestera
Gestational age for full-term labor
No. of neonatal department admissions (%)
No. of neonatal death (%)
No. with long-term sequelae of prematurity (%)
Weeks of pregnancy gained (w [median, range])a
No. of living children
Fetal salvage rate (for pregnancy continued beyond the rst trimester) (%)

n = 1 (10%)
n = 1 (10%)
n = 8 (80%)
38 (2039)
38.1 (n = 8)
n = 1 (10%)
n=0
n=0
16.5 (123)
n=9
90%

n = 2 (8%)
n = 7 (28%)
n = 16 (64%)
35 (27.637.7)
38 (n = 16)
n = 9 (36%)
n = 2 (8%)
n = 1(4%, retinopathy)
11 (2.629)
n = 22
88%

NS
NS
NS
0.005
NS
NS
NS
NS
0.039

NS

Note: NS = not signicant.


a
Values are median (range).

damage to surrounding viscera was also higher in TAC. Moreover, if


it is done before pregnancy, postoperative pelvic adhesion could
lead to secondary infertility. As a result, the indications for this
more invasive approach have generally been limited to the strictly
selected group described above.
In order to reduce the operative morbidity, laparoscopic
approach of cervicoisthmic cerclage placement has recently been
developed. In several single case reports and small case series,
preliminary results suggest that the risk of complications and
obstetric outcomes compare favorably with the laparotomy
approach [5,7,8,9]. We performed a systematic literature search
of PubMed, EMBASE, and the Cochrane database for studies on the
laparoscopic approach. Sixteen studies in English encompassing
136 patients (Table 5) yielded a mean fetal survival rate of 81.6%
(75100%, n = 130) and an operative complication rate of 6% (0
10.7%, n = 136). The main perioperative complications included
excessive blood loss due to uterine vessel damage, damage to the
ureters, cystotomy, conversion to laparotomy due to surgical
invisibility (which occurs more frequently in pregnant patients),
perioperative pregnancy loss, and ruptured fetal membranes.
Whittle et al. [5] reported the largest sample (65-patient) cohort
study of laparoscopic cervical cerclage to date with fetal survival
rate of 80% and 10.7% of perioperative complication rate.
In the present study, we described a modied surgical method
for laparoscopic abdominal cerclage to avoid many complications
associated with previous techniques. Instead of creating windows
in broad ligament peritoneal membranes, we directly inserted the

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delivery age, while in TVC group, this number was 11 weeks, which
made a statistically differences between the two groups (p = 0.039).
Only one LCC patient experienced premature rupture of the
membrane (at 20 weeks) and the fetus was aborted vaginally after
removing the cerclage by mini-laparotomy. Other viable pregnancies in LCC group were delivered by caesarean section. The cervical
sutures were left in situ at the time of caesarean section. In TVC
group, the sutures were removed at 37 weeks of gestation or with
the onset of labor if earlier, and the patients were allowed to
deliver as appropriate.

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Cervical incompetence is traditionally treated with a TVC


during the late rst trimester or early second trimester of
pregnancy. However, TVC fails in a part of patients due to
extremely short, deformed, and/or scarred cervices. A transabdominal approach for cervical cerclage was indicated in the
select group of patients with a cervix that is too short or scarred for
a TVC or who have previously failed a TVC. Different from the TVC,
the cerclage was placed at the level of the cervicoisthmic junction
in transabdominal cerclage, which theoretically made the cervix
more strengthened to act as the barrier against intrauterine
pressure during gestation. Some studies have shown better results
of TAC than TVC, with higher perinatal survival rate. However, the
surgery technique itself was more complex, and the rate of serious
operative complications such as the need for transfusion or

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Discussion

Table 5
Cumulative results of cervico-isthmic cerclage placed by laparoscopy.
Cerclage by laparotomy:
study and year

Patient
no.

The timing of surgery

Patient no.
conceived

Pregnancy
no.

Intraoperative
complication rate (%)

Fetal survival
rate (%)

Average gestational age


at birth

Lesser KB et al., 1998


Mingione MJ et al., 2003
Cho CH, et al., 2003
Gallot D et al., 2003
Ghomi A et al., 2006
Aboujaoude R et al., 2007

1
11
20
3
1
1

Duriung pregnancy
Before pregnancy
During pregnancy
Before pregnancy
Before pregnancy
During pregnancy

10

2
1

0
9
0
0
0
0

100
83
95
100
100
Not reported

Not reported
37.1
36.2
38
38.4
Not reported

Agdi M et al., 2008


Reid GD et al., 2008
Liddell HS and Lo C., 2008
Whittle WL et al., 2009
Fechner AJ et al., 2009
Carter JF et al., 2009

1
3
11
65
1
12

10
26, n = 34

12

0
0
0
10.7
0
0

Not reported
100
80
100
75

Not reported
Not reported
35.8
37
Not reported

Pereira RM et al., 2009


Pawowicz P et al., 2009

1
2

Before pregnancy
During pregnancy
Before pregnancy
34 not pregnant, 31 pregnant
Pregnant
5 during pregnancy and 7
before pregnancy
Before pregnancy
Before pregnancy

1
12
21
2
1
Not
reported
1
3
10
67
1
12

0
0

100
Not reported

38
Not reported

Murray A et al., 2011


DaCosta V et al., 2011
Total
Current study

1
3
137
19

Before pregnancy
Before pregnancy

Before pregnancy

1
2
68
15

2
Not
reported
1
2
136
15

Not reported
0
6, n = 136
0

100
100
81.6, n = 130
92.9

28
37
36, n = 103
38.2

1
2

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be neglected. In our series, to ensure postoperative fertility and to


facilitate embryo discharge in case of miscarriage during the rst
and early second trimester, we placed a 6# Hegar dilator
transcervically when tying the knot as reported by Whittle et al.
and others [5,10]. The fertility rate was not affected postoperatively, and fetal tissue could be discharged in our case of early
miscarriage.
One possible limitation of our study is that the experimental
group and the control group are not perfectly matched. As an
experimental group, the LCC group is a prospective (cohort) group
and the control group is a retrospective group (TVC). The
comparisons between these two groups are not perfectly
comparable and effective. In addition, it would be even better if
there is one more control group of transabdominal cervical
cerclage, so that it will be better to show the efcacy of these three
different surgical methods. Randomized controlled trials with
large sample are needed to further conrm the safety, practicability and effectiveness of this modied LCC approach, and to conrm
the idea of its expanded indications.
In conclusion, our modied method for laparoscopic cerclage
demonstrates good obstetric outcomes with low risk of adverse
events. This cerclage method may provide a reasonable alternative
to achieve pregnancy success in patients with cervical incompetence.

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Conict of interest

None of the authors have commercial, proprietary, or nancial


interests in the products or companies mentioned in this article.
Further, there are no disclosures to report for this paper.

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straight needle into the anterior surface of the cervix on one side
with a small piece of cervical tissue remaining outside the noose to
decrease the possibility of damage to the uterine vessels and
ureters, excessive blood loss, and compression of the uterine
vessels. The surgical duration was relatively short and blood loss
was minimal, with a 0% perioperative complication rate up to now.
In our series, patients in the LCC group achieved satised results
in obstetric outcomes. The fetal survival rate in the LCC group was
as high as 92.3% with a mean gestational age of 36.4 weeks, and
weeks gained for the gestational age to previous pregnancies was
17.4 weeks. No long-term sequelae of prematurity happened.
These results are in accordance with past studies (Table 5)
demonstrating a total fetal survival rate after laparoscopic
abdominal cerclage of 81.6% (75100%, n = 130) and an average
gestational age at birth of 36 weeks (n = 103), which was reported
to be better than the TVC approach. However, limited to the small
case number, fetal salvage rate and mean gestational age in the
present study were similar between the two groups. Only weeks
gained for the gestational age to previous pregnancies showed
statistically superiority in LCC group.
To sum up, our results showed that this modied approach
maintained the strong point of TAC to placement of a cervicoisthmic cerclage at the level of the cervicoisthmic junction, while it
simplied the surgical steps to be much easier to master by most
gynecologist and it further reduced the operative morbidity to be
as minimal invasive as TVC. Based on our results, this modied LCC
method is safe and probably more effective, and its indications can
be extended to those of traditional transvaginal cerclage. Some
may argue that LCC have obvious disadvantages including the need
of another laparoscopic surgery or laparotomy to remove the tape
once second-trimester miscarriage or intrauterine fetal death
happens, and the delivery mode for full-term or premature
delivery can only be cesarean section. However, for the high risk
patients who have experienced painful recurrent fetal losses and
strongly demand for a baby to take home, it is worth the risk of
another laparoscopic surgery or mini-laparotomy for a probably
better obstetric result. Meanwhile, cesarean section seems to be
minor drawback for these patients given their complex and
difcult obstetric history.
Another controversial point is the optimal time for cerclage
surgery. Most studies reported that the timing of cerclage
placement did not inuence the gestational age at delivery,
although cerclage failure did occur more often when inserted
during pregnancy [5,9]. In our study, all patients underwent the
modied LCC surgery before pregnancy. We believe cerclage
insertion should be avoided during pregnancy for the following
reasons. First, the pelvic cavity and the uterus are more congested
during pregnancy and surgeries during pregnancy can lead to
excessive bleeding. Second, since the gravid uterus is enlarged, the
surgical visibility is relatively poor and transcervical uterine
manipulators cannot be used, so cerclage placement is a greater
challenge for surgeons. Third, postoperative rupture of membranes
and fetal loss are still possible following transabdominal cervical
cerclage; if conducted before pregnancy, such considerations can

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