Original Research

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OBSTETRICS
1
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6 Q8 Stphanie Roberge, MSc; Suzanne Demers, MD; Mario Girard, RT; Olga Vikhareva, MD, PhD;
Stphanie Markey, MD; Nils Chaillet, PhD; Lynne Moore, PhD; Gatan Paris, MD;
7
Q1
Emmanuel Bujold, MD, MSc
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BACKGROUND: Incomplete healing of uterine scar after cesarean has 6 months after delivery. Secondary outcome was the RMT as a percentage
11
been associated with adverse gynecological and obstetrical outcomes. of the myometrial thickness above the scar (healing ratio). Intent-to-treat
12
Several studies reported that uterine closure at cesarean influences the analyses using Student t test were performed to compare each double13
healing of uterine scar and the risk of uterine rupture at subsequent layer technique to the single-layer closure, and P < .025 was consid14
pregnancies: the commonly used locked single-layer suture including the ered significant.
15
decidua being associated with a 4-fold increased risk of uterine rupture. RESULTS: Complete follow-up was obtained from 73 (90%) of the 81
16
participants. Compared to single-layer closure, double-layer closure with
However, data from randomized trials are lacking.
17
OBJECTIVE:
We
sought
to
evaluate
the
impact
of
3
techniques
of
unlocked first layer was associated with thicker RMT (3.8  1.6 mm vs 6.1
18
uterine
closure
after
cesarean
delivery
on
uterine
scar
healing.
 2.2 mm; P < .001) and greater healing ratio (54  20% vs 73  23%;
19
STUDY DESIGN: This was a 3-arm 1:1:1 randomized study in women P .004). In contrast, double-layer closure with locked first layer was not
20
with singleton pregnancies undergoing elective primary cesarean delivery significantly different than single-layer closure in either RMT (4.8  1.3;
21
at
38 weeks gestation. Closure of the uterine scar was carried out by P .032) or healing ratio (60  21%; P .287).
22
locked single layer including the decidua, double layer with locked first CONCLUSION: Double-layer closure with unlocked first layer is
23
layer including the decidua, or double layer with unlocked first layer associated with better uterine scar healing than locked single layer.
24
excluding the decidua. Primary outcome was residual myometrial thick25
ness (RMT) at the site of the scar, measured by transvaginal ultrasound Key words: cesarean, scar, uterine closure
26
27
28
Introduction
there is evidence from large retrospective the measurement of the remaining
29
Cesarean
delivery
is
carried
out
in
studies that the risk of uterine rupture myometrium thickness at the site of the
30
approximately
one
fourth
of
all
births
and placenta accreta is related to the uterine scar.7,15 Such a tool offers the
31
1-3
in developed countries.
Incomplete method of uterine closure.9,10 A meta- opportunity to evaluate the impact of
32
healing of the uterine scar after cesarean analysis including retrospective and uterine closure on scar healing.
33
The objective of this randomized
is a side effect with potential long-term prospective studies reported that locked
34
study
was to compare 2 types of doubleconsequences,
including
thinning
of
single-layer
closure,
compared
to
35
layer
closure
with the most commonly
the
myometrium
that
occurs
in
37-59%
double-layer
closure,
is
associated
with
a
36
4-6
used
method
of locked single-layer
of
cases.
4-fold
increase
in
risk
of
uterine
rupture
This
defect
has
been
associ37
9
closure
including
the decidua.16
in
a
subsequent
pregnancy.
ated
with
major
obstetrical
complicaProspective
38
tions, such as ectopic scar pregnancies, studies using ultrasound evaluation of
39
placenta accreta, and uterine rupture, as the scar favor an unlocked suture with Materials and Methods
40
well as numerous gynecological prob- exclusion of the decidua to optimize the Study design and participants
41
lems, including postmenstrual spotting, approximation of the tissues and their We performed a double-blind random42
dysmenorrhea, and pelvic pain.7
healing.9,11,12 However, at present, there ized controlled trial to compare 3 types
43
There is some evidence that the risk of is no consensus on the method of uterine of uterine closure (ratio 1:1:1). The
44
uterine scar defect is related to number closure following cesarean delivery in project was approved by the institutional
45
of previous cesarean deliveries and terms of use of 1 or 2 layers, locking review board of the hospital and
46
method of uterine closure.5,8 Similarly, or not of the rst layer, and whether registered at clinicaltrial.gov (NCT01
47
the decidua should be included or 860859). Participants were recruited
48
from March 2013 through June 2014, in
excluded.13,14
49
Cite this article as: Roberge S, Demers S, Girard M, et al.
Transvaginal ultrasound is a validated Quebec City, Quebec, Canada, during
50
Impact of uterine closure on residual myometrial thick- tool to evaluate uterine scars.15 Scar
their preoperative appointment where
51
ness after cesarean: a randomized controlled trial. Am J
defects are reported as niche, isth- they gave written informed consent. The
52
Obstet Gynecol 2015;volume;x.ex-x.ex.
mocele, or wedge and are related to study included women
18 years of age
53
0002-9378/$36.00
gynecological symptoms and uterine with singleton pregnancies undergoing
54
2015 Elsevier Inc. All rights reserved.
rupture in subsequent pregnancies.7 The an elective primary cesarean delivery
55
http://dx.doi.org/10.1016/j.ajog.2015.10.916
severity of the defect is quantied by at
38 weeks gestation. Exclusion

Impact of uterine closure on residual myometrial

thickness after cesarean: a randomized controlled trial

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Original Research
FIGURE 1

Types of uterine suture following cesarean delivery

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OBSTETRICS

A, Locked single-layer closure including decidua. B, Double-layer closure with first layer locked and
second layer unlocked and imbricating first layer. C, Double layer with first layer unlocked, excluding
decidua and including deeper part of myometrium. D, Second layer of double-layer closure, unlocked
and taking remaining part of myometrium, either subcuticular or over, depending on deepness of
suture.
Roberge et al. Impact of uterine closure after cesarean. Am J Obstet Gynecol 2015.

criteria were multiple pregnancies,

thrombophilia, mullerian anomalies,
previous cesarean or uterine scar, active
labor (with regular uterine contractions
and cervical dilatation
4 cm) at the
time of cesarean, body mass index (BMI)

35 kg/m2, placenta previa, or known

chronic inammatory disease.

Randomization and masking

Randomization was computer generated, supervised by a statistician using

167
3 blocks. At the time of the elective
168
cesarean delivery, a research assistant
169
gave the next sealed opaque and
170
consecutively numerated envelope
171
containing a description and an image of
172
the suture technique to the surgeon
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(Figure 1). Women were allocated to 1 of F1 174
the 3 groups: (1) single layer locked,
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including the decidua (controls)16;
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(2) double layer with the rst layer
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locked including the decidua and the
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second layer unlocked and imbricating
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the rst layer; and (3) double layer with
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the rst layer unlocked, excluding the
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decidua and including the deep part of
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the myometrium, and the second layer
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unlocked including the remaining part
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of the myometrium. All sutures had to be
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continuous using synthetic absorbable
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thread (polyglycolic acid, size: 0). The
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participant, the research nurse who
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collected postpartum information, the
189
sonographer who performed the ultra190
sound scan, the 2 external observers
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that analyzed the ultrasound images, and
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the person in charge of the database
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remained blinded to intervention
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allocation.
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Follow-up
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The following baseline characteristics
198
were collected: maternal age, BMI, pre199
vious vaginal birth, gestational age at
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delivery, and reason for the cesarean
201
delivery. A questionnaire was given
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to the surgeon after delivery for the
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following information: (1) need for
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additional suture; (2) whether or not
205
the vesicouterine and parietal perito206
neum were closed; and (3) duration of
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surgery. The following information was
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collected from the chart: birthweight,
209
estimated blood loss, and postpartum
210
endometritis.
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Considering that uterine scar healing
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is complete after a minimum of 6
213
months following delivery, each partici214
pant was invited for an ultrasound
215
examination of the uterine scar at be216
tween 6-12 months after the cesarean
217
delivery.17 At that appointment, she
218
answered a questionnaire administered
219
by a trained research nurse regarding
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potential postpartum complications.
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Thereafter, transvaginal ultrasound was
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performed by a trained sonographer to

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Original Research

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Trial profile.
Q9
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Roberge et al. Impact of uterine closure after cesarean. Am J Obstet Gynecol 2015.
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between uterine closures.18 Using a suture was realized correctly. The study
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Bonferroni correction for multiple was reported according to the Consoli309
comparisons, an alpha error of 0.025, dated Standards of Reporting Trials
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and a beta error of 0.20, we had to statement.19
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randomize a minimum of 72 partici312
pants. Considering a potential risk of Results
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10% of loss to follow-up, we intended to A total of 152 women were screened, 109
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randomize 81 patients. No interim were eligible for the study, and 81 agreed
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analysis was planned.
to participate and were randomized (27
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in each groups) (Figure 3). We observed F3 317
3 protocol violations: (1) 1 participant in
Analyses
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Statistical analyses were performed by the single layer group had a double-layer
319
intent-to-treat using software (SAS 9.3; closure with an unlocked rst layer; (2) 1
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SAS Institute Inc, Cary, NC). Compari- participant was 17 years old at the time
321
sons between each double-layer sub- of the cesarean; and (3) 1 participant was
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group to the control group were randomized at 36 6/7 weeks of gestation.
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conducted using Student t test for our Eight participants (10%), including the
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primary outcome and for other contin- one who did not receive the allocated
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uous variables presented as means with uterine closure and the 17-year-old pa326
SD. Comparison of proportions was tient, were lost to follow-up at the 6
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conducted using Fisher exact test. Using months postpartum visit: 2 participants
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Bonferroni adjustment for multiple (7.4%) were lost in the single-layer
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comparisons, a P value <.025 was locked group, 5 (18.5%) in the double330
considered signicant. Marginal power layer locked group, and 1 (3.7%) in the
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was calculated between groups for each double-layer unlocked group.
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comparison after loss to follow-up.
Complete follow-up for the primary
333
Revision of the patient charts was done outcome was obtained from 73 partici334
to assess compliance to assess if the pants (90%). Compliance to surgical Q3
FIGURE 3

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OBSTETRICS

Transvaginal ultrasound illustrating measurements of residual and total myometrial

thickness.
Roberge et al. Impact of uterine closure after cesarean. Am J
Obstet Gynecol 2015.

assess the uterine scar as previously

described.6 The following data were
collected: the position of the uterus
(anteverted or retroverted), residual
myometrial thickness (RMT), and total
myometrial thickness (TMT) above the
uterine scar (Figure 2). A video sequence
of the transvaginal ultrasound including
the entire low uterine segment by scanning from left to right was saved for
future measurement by 2 external observers blinded to the original measurement and blinded to the ndings of each
other.

Outcomes
Primary outcome was the mean RMT of
the 3 observers (1 sonographer and 2
external observers). In the case of a
discrepancy >1 mm between observers,
all of them reviewed the images and
measurements of the 3 observers to reach
a consensual RMT. Secondary outcomes
included: prevalence of severe scar defect
dened as the RMT <2.3 mm, mean
anterior TMT, healing ratio dened as
the RMT  100/TMT, mean operative
time, mean estimated blood loss at the
time of the cesarean, need for and
number of additional hemostatic sutures, and prevalence of postpartum
endometritis.

Sample size
Based on a previous report, we calculated the sample size to observe an estimated difference of 1.5 mm of RMT

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OBSTETRICS

TABLE 1

Baseline characteristics
Uterine closure
Single layer locked Double layer
Double layer
(controls), N 27 locked, N 27 unlocked, N 27

Characteristic
Age, y

30.8  4.0

Gestational age at delivery, wk

39.2  0.6

39.1  0.5

38.9  0.6

Body mass index, kg/m2

25.1  4.7

23.5  3.9

25.1  5.3

3350  379

Birthweight, g

31.1  6.4

3407  439

31.0  3.7

3236  465

Nulliparity

80.8

74.1

75.0

Previous vaginal birth

19.2

25.9

28.6

Noncephalic fetal presentation

92.3

93.3

85.7

Vesicouterine peritoneum closure

11.5

18.5

18.9

Parietal peritoneum closure

38.5

40.7

28.6

Breast-feeding

76.9

66.7

66.7

Values given as mean  SD or percent.

Roberge et al. Impact of uterine closure after cesarean. Am J Obstet Gynecol 2015.

technique was very good (96%). Marginal power between rst comparisons
(single-layer locked closure vs doublelayer closure with rst layer locked) was
99% and 63% for the second comparison (single layer locked vs double layer
unlocked excluding decidua). Baseline
characteristics, birthweight, and peritoneum closure was similar between
groups (Table 1).
We observed that a double layer with
an unlocked rst layer was associated
with a greater RMT than the singlelayer locked technique (P < .001).
While the association was statistically
nonsignicant, the RMT in the double
layer with a locked rst layer group was
greater than the locked single layer
group (P .032) with a limited marginal power (63%) related to the high
number of those lost to follow-up in
this group (n 5, 19%). Similarly, a
double layer with an unlocked rstlayer closure was associated with a
greater TMT and greater proportion of
healing ratios than the control group
but not the double layer with locked
rst layer (Table 2). No difference was
observed between the groups in terms
of severe uterine scar defect, need for
additional suture, estimated blood loss,
or operative time. No case of postpartum endometritis was reported.

Comment
Main findings of this study
The ndings of this randomized study
demonstrate that double-layer uterine
closure with a rst unlocked layer
excluding the decidua, compared to
locked single-layer closure including the
decidua, is associated with a greater
RMT, TMT, and healing ratio, suggesting
that this technique is associated with
better healing of the uterine scar. Similar
ndings were not observed with the
double layer with a locked rst layer
including the decidua, but the lack of
statistical power did not allow us to draw
a denitive conclusion. Finally, we
observed no difference for the need of
additional hemostatic suture between
single- and double-layer closure.

Comparison with results of

previous studies
Our results are consistent with those
from previous clinical trials suggesting a
benet of double-layer closure with an
unlocked rst layer separating or
excluding the decidua.18,20,21 Several
authors compared single-layer locked
suture to double layer with rst layer
locked and showed a signicant increase
in RMT and healing ratio, but stated
that locked double-layer closure presents
limited benets.20,22,23 In a similar

design, Yasmin et al18 compared 3 techniques: locked single layer; double

layer with the rst locked; and double
layer with interrupted rst layer.
They observed a signicantly thicker
RMT with the last technique but their
ndings were limited by the presence of
previous cesareans in all women and the
ultrasound performed before complete
uterine scar healing (6 weeks after
cesarean).18 In a quasirandomized trial,
Hayakawa et al21 compared interrupted
single layer including the decidua,
interrupted double layer with the rst
layer including the decidua, and continuous double layer with a rst unlocked
layer separating the inclusion of the
decidua, similar to the third technique
used in the current study. Their study
was also limited by the short delay before
ultrasound examination (1 month after
cesarean) but like us, they observed a
signicantly lower risk of a wedge defect
in the uterine scar with the third technique compared to the single layer (5.6%
vs 34%; odds ratio, 0.08; 95% condence
interval, 0.01e0.49). Sevket et al20
observed a greater RMT (9.95  1.94
mm vs 7.53  2.54 mm; P < .005) with
the double-layer, locked rst-layer technique compared to a locked single-layer
suture in a randomized controlled trial
including 36 women and hydrosonographic assessment of the uterine scar 6
months after cesarean. Interestingly, a
recent randomized controlled trial conducted in France observed no difference
in RMT between an unlocked singlelayer closure excluding the decidua and
a double-layer closure with a similar rst
layer (7.7 vs 7.3 mm).24 Finally, Turan
et al12 shown that a locked single-layer
suture was associated with a thinner
healing ratio than unlocked single-layer
suture (62% vs 76%; P < .001). All
together these trials suggest that exclusion of the decidua with a continuous
unlocked rst layer is associated with
optimal uterine scar healing.
Biologically, the use of an unlocked
suture could reduce the pressure and
the strength of the scar, causing less
strangulation of the tissue with less
interference with vascular supply.11,25
Moreover, it is also possible that
excluding or separating the decidua

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OBSTETRICS

Original Research

TABLE 2

Primary and secondary outcomes

Uterine closure
Single layer locked (controls),
N 25

Outcome
Residual myometrial thickness, mm
Thickness <2.3 mm
Total myometrial thickness, mm

Operative time, min

Need for additional sutureb

P value

.0317

6.09  2.21

.0002a

5/25 (20)

1/22 (4.5)

.1936

1/26 (3.8)

.0993

8.2  2.1

9.4  2.3

.0741

9.5  1.7

.0254

60  21
709  297.4

28  7.9

29  9.8

16/27 (59)

16/27 (59)

1.1  1.38

No. of additional sutureb

Double layer unlocked,

N 26

4.77  1.34

674  167.8

Estimated blood loss, mLb

P value

3.80  1.57

54  20

Healing ratio

Double layer locked,

N 22

1.0  0.96

.2866
.5969
.6730
1.0
.8166

73  23
722  142.3
28  6.1
16/27 (59)
1.1  1.15

.0036a
.2658
.8486
1.0
.9231

Values given as mean  SD or n/N (%).

Significant <.025; b Data available for all of 81 participants (27 in each group).
Roberge et al. Impact of uterine closure after cesarean. Am J Obstet Gynecol 2015.

when the suture is unlocked inuences

healing, inducing a better coaptation
(decidua to decidua and myometrium to
myometrium).11,25-27

Strengths and limitations of

the study
The strengths of our study include:
(1) homogeneity of the population,
represented by Caucasian participants
with similar socioeconomic status having a primary cesarean delivery, not in
labor, normal BMI, no diabetes, and
absence of previous uterine surgery;
(2) high follow-up; (3) uterine scar was
evaluated after a delay sufcient to
ensure complete healing and measurement of RMT and TMT by 3 independent observers who were blinded to
treatment allocation; and (4) high
compliance (96%) and low risk of bias
suggesting excellent internal validity.
The main limitation of the study is the
difference between groups in loss to
follow-up, leading to a low marginal
power for our comparison between single layer and double layer with a locked
rst layer and precluding clear conclusions about this comparison. Another
limitation is that RMT provides an indirect measure of uterine scar healing
and is only a surrogate outcome for the
prediction of uterine rupture or other
adverse outcomes related to uterine scar.
However, there is an important body of

evidence showing that ultrasonographic

scar defect and RMT are strongly correlated with such adverse outcomes, also
including menstrual disorders, infertility, or placental disorders.5,7,28-30 The
current trial did not have the power to
demonstrate differences in operative
time, need for additional sutures, or
blood loss among the 3 techniques. The
results are in agreement with literature
suggesting no difference between types
of closure for those outcomes.8,14,31,32
Few studies showed a signicant difference of 2-7 minutes of operative time of
single-layer technique compared to
double layer, but clinically, the advantages related to a better healing are
perhaps more important than a few
minutes less of operative time.33,34
Finally, our trial is limited to cesarean
performed in women before or in early
labor and we cannot extrapolate our
ndings to cesarean performed in
advanced labor. In that latter situation, it
is possible that such double-layer technique is not feasible or does not have the
same benets because of the very thin
myometrium of low uterine segment
that is typically observed in advanced
labor.

cesarean could improve uterine scar

healing and potentially lead to a reduction of severe obstetric complications
related to uterine scar defects. In Canada, a survey revealed that most surgeons
are currently using a locked closure.35
Since the conversion from one technique to another only requires minor
adjustment without extra costs, the
benets of using a double-layer uterine
closure with a rst unlocked layer
excluding the decidua far outweigh
the disadvantages.35 Combined with a
uterine scar evaluation during third
trimester, better scar healing would
allow more women to consider a vaginal
birth after cesarean without complications. Considering the great potential
of change for clinical practice, future
research should evaluate whether uterine
closure technique is as important in
women undergoing cesarean during
labor.
While the debate of the past few years
has been focused mainly on the number
of layers (single vs double), the current
study highlights the importance of other
features inuencing healing of the uterine scar such as including the decidua
and locking sutures.36
n

Implications for practice and

future research

References

Our results suggest that a small change in

the technique of uterine closure at

1. Blanchette H. The rising cesarean delivery

rate in America: what are the consequences?
Obstet Gynecol 2011;118:687-90.

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ajog.org

OBSTETRICS

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Author and article information

From the Departments of Social and Preventive Medicine
(Ms Roberge, and Drs Demers, Moore, and Bujold) and
Obstetrics and Gynecology (Drs Demers, Paris, and
Bujold, Mr Girard, and Ms Markey), Faculty of Medicine,
Universite Laval, Quebec, Quebec, Canada; Department
of Obstetrics and Gynecology, Malmo University Hospital,
Lund University, Malmo, Sweden (Dr Vikhareva); and
Department of Obstetrics and Gynecology, Universite de
Sherbrooke, Sherbrooke, Quebec, Canada (Dr Chaillet).
Received Sept. 24, 2015; revised Oct. 21, 2015;
accepted Oct. 23, 2015.
This study was supported by the Jeanne and JeanLouis Levesque Perinatal Research Chair at Universite
Laval, Quebec, Quebec, Canada. Dr Bujold holds a Q2
clinician scientist award and Ms Roberge and Ms Demers
hold a study award (Fond de recherche du Quebec e
Sante).
The authors report no conflict of interest.
Given as a short oral presentation at the 25th World
Congress on Ultrasound in Obstetrics and Gynecology,
Montreal, Quebec, Canada, Oct. 13, 2015.
Corresponding author: Emmanuel Bujold, MD, MSc.
emmanuel.bujold@crchul.ulaval.ca

1.e6 American Journal of Obstetrics & Gynecology MONTH 2015

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