Archives of Gynecology and Obstetrics

https://doi.org/10.1007/s00404-024-07417-1

GENERAL GYNECOLOGY

The association of endometrial closure during cesarean section

to the risk of developing uterine scar defect: a randomized control trial
Aya Mohr‑Sasson1,2 · Elias Castel1,2 · Tal Dadon1 · Ariel Brandt1 · Roie Etinger1 · Adiel Cohen1 · Michal Zajicek1,2 ·
Jigal Haas1,2 · Roy Mashiach1,2

Received: 17 December 2023 / Accepted: 4 February 2024

© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2024

Abstract
Purpose The surgical technique for uterine closure following cesarean section influences the healing of the cesarean scar;
however, there is still no consensus on the optimal technique regarding the closure of the endometrium layer. The aim of
this study was to compare the effect of closure versus non-closure of the endometrium during cesarean section on the risk
to develop uterine scar defect and associated symptoms.
Methods A randomized prospective study was conducted of women undergoing first elective cesarean section at a single
tertiary medical center. Exclusion criteria included previous uterine scar, preterm delivery and dysmorphic uterus. Women
were randomized for endometrial layer closure versus non-closure. Six months following surgery, women were invited to
the ambulatory gynecological clinic for follow-up visit. 2-D transvaginal ultrasound examination was performed to evaluate
the cesarean scar characteristics. In addition, women were evaluated for symptoms that might be associated with uterine
scar defect. Primary outcome was defined as the residual myometrial thickness (RMT) at the uterine cesarean scar. Data are
presented as median and interquartile range.
Results 130 women were recruited to the study, of them follow-up was achieved in 113 (86.9%). 61 (54%) vs. 52 (46%) of the
women were included in the endometrial closure vs. non-closure groups, respectively. Groups were comparable for patient's
demographic, clinical characteristics and follow-up time for postoperative evaluation. Median RMT was 5.3 (3.0–7.7) vs. 4.6
(3.0–6.5) mm for the endometrial closure and non-closure groups, respectively (p = 0.38). Substantially low RMT (< 2.5 mm)
was measured in four (6.6%) women in the endometrial closure group and three (5.8%) of the women in the non-closure
group (p = 0.86). All other uterine scar sonographic measurements, as well as dysmenorrhea, pelvic pain and intermenstrual
bleeding rates were comparable between the groups.
Conclusion Closure versus non-closure of the endometrial layer during cesarean uterine incision repair has no significant
difference in cesarean scar characteristics and symptom rates at 6 months follow-up.

Keywords Endometrial layer · Cesarean scar defect · Residual myometrial thickness · Dysmenorrhea · Dysmenorrhea ·
Intermenstrual bleeding

What does this study add to the clinical work

Closure versus non closure of the endometrial layer
of the uterine incision during Cesarean delivery is
associated with similar Cesarean scar characteristics
and symptomatic rates.

* Aya Mohr‑Sasson
Mohraya@gmail.com
1
Department of Obstetrics and Gynecology, Sheba Medical
Center, 5265601 Tel‑Hashomer, Israel
2
Sackler School of Medicine, Tel-Aviv University, Tel‑Aviv,
Israel

Vol.:(0123456789)

Introduction
Cesarean section (CS) is the most common major operation
performed in women worldwide with progressively rising
incidence [1]. Consequently, long-term adverse events due
to uterine scar defect (niche) have been increasing [2, 3].
Common gynecological complaints include chronic pelvic
pain, dyspareunia, dysmenorrhea and post-menstrual
spotting [2, 4]. Recent studies have found association
between the presence of niche and infertility [5–7].
Obstetric complications seem to be increasing such as
cesarean scar pregnancy (CSP), placenta previa, placenta
accreta, scar dehiscence and uterine rupture, all associated
with major maternal morbidity and even mortality [8–11].
Shiber et al. [12] reported outcomes of 60 women with
cesarean scar pregnancy diagnosed during a period of 25
years. Abnormal uterine scar and abnormal placentation
were noted in 10.5 and 26.3%, respectively. The presence
of niche was associated as a risk factor for future uterine
rupture during trial of labor after cesarean (TOLAC) as
reported by Cohen et al. [10].
Surgical treatments have been recommended when
uterine scar defect is diagnosed in symptomatic women.
Fig. 1  Niche measurements. R residual myometrial thickness (RMT), A adjacent myometrial thickness (AMT), D depth, L length
Archives of Gynecology and Obstetrics
The surgical approach is decided based on the residual
myometrial thickness (RMT) above the area of the uterine
scar (Fig. 1) and includes hysteroscopy and laparoscopy.
A systematic review found an improvement in abnormal
uterine bleeding, secondary infertility and pain following
uterine scar repair [13]. Similarly, good pregnancy
outcomes were reported in a study conducted by
Goldenberg et al. [14] in women with mean RMT < 2 mm
that had been repaired.
Given the association between uterine scar defect and
gynecological symptoms, obstetric complications and infer-
tility, it is important to elucidate the etiology to develop
preventive strategies [15]. Risk factors that have been asso-
ciated include: single-layer myometrium closure, multiple
CSs and uterine retroflexion [16]. Nevertheless, surgical
technique of uterine incision closure seems to be the most
important determinant for defect formation. It is proposed
that continuous, non-locking absorbable sutures in two lay-
ers, without including much of the endometrial layer and
without tight pulling of sutures, are likely to result in good
healing of the uterine scar [8]; however, data is limited. The
aim of this prospective randomized study is to evaluate spe-
cifically the influence of inclusion (closure) versus exclusion
(non-closure) of the endometrial layer during suturing the
Archives of Gynecology and Obstetrics
uterine incision on the risk to develop uterine scar defect and
associated symptoms.
Material and methods
This is a prospective randomized single blinded study
conducted at a single university-affiliated tertiary medical
center. All women at term (≥ 37 weeks of gestation) visiting
the preoperation clinic for planned elective cesarean section
with singleton pregnancy were offered to participate in the
study. Women with previous uterine scar, multiple gestation,
thrombophilia, dysmorphic uterus or connective tissue disor-
der were excluded. After signing informed consent, women
were block randomized into one of two groups based on
the order they were recruited: A—uterine incision repair in
double layer including suturing of the endometrial layer (odd
numbers), B—uterine incision repair in double layer exclud-
ing the endometrial layer (even numbers). Women were
blinded to the randomization arm they were allocated to.
All operation was performed by a single highly skilled
obstetrician. All other stages of operations were similar in
both of the groups including: low segment uterine incision,
delivery of the fetus and the placenta and uterine revision
to verify no retained products of conception. Uterine repair
was done in all cases intra-abdominally. Stratafix thread
suture was used for the hysterotomy repair that was done
in continuous non-locking fashion in two layers. The first
layer included approximation of the endometrium in addi-
tion to myometrium in women who were randomized to
include the endometrium (Group A). Imbrication was done
in the second layer in both of the groups. Demographics,
clinical characteristics, operative and postoperative data
were collected from the women’s medical files. Operative
information included: operation duration from anesthesia
until abdominal closure, estimated blood loss reported by
the surgeon and operation complications (anesthesia, bleed-
ing, adjacent organ damage). Postoperative complications
included hemorrhage, infection (urinary tract, pulmonary,
endometritis), vascular thromboembolic event and ileus.
Six months following surgery, all women were invited
to the ambulatory gynecological clinic for follow-up visit.
When possible, the timing was scheduled for the early mid
follicular stage, as uterine scar is better demonstrated on
ultrasound examination [17]. During the follow-up visit,
women were asked to report any new symptoms since
delivery that might be associated with uterine scar defect,
including: (1) heavy menstrual bleeding since the operation
(defined by the American College of Obstetrician and Gyne-
cology as any of the following: bleeding that lasts more than
7 days; bleeding that soaks through one or more tampons or
pads every hour for several hours; need to wear more than
one pad at a time to control menstruation; changing pads
or tampons during the night; or menstrual flow with blood
clots) [18] (menorrhagia); (2) intermenstrual spotting; (3)
pain during intercourse (dyspareunia); or (4) pelvic pain.
In addition, a transvaginal 2-D ultrasound examination tar-
geted to assess the uterus and the uterine niche characteris-
tics was performed. Uterine niche measurement was done in
the transverse plane for the evaluation of the largest width of
the niche. The sagittal plane was used for the measurements
of the length at the base, depth from the base to the myome-
trium above, residual myometrial thickness (RMT) above
the area of the deficit and adjacent myometrial thickness
(AMT) at the area approximate to the niche with full myo-
metrial thickness (Fig. 1). The severity of the niche was also
estimated by both the proportion between the residual to the
adjacent myometrial thickness (RMT/AMT). The research
team member performing the transvaginal examination was
blinded to the randomization of the women. The primary
outcome was defined as the presence of substantial niche. As
the definition varies between studies [17, 19, 20], we defined
it as RMT below 2.5 mm on follow-up visit, the value that is
considered substantial in our medical center.
Secondary outcomes included operation time, intraopera-
tive and postoperative complication rates, difference in uter-
ine characteristics postoperation and change in symptoms
associated with the presence of uterine scar defect.
The study protocol was approved by the “Sheba Medical
Center” Review Board (ID 5822-18-SMC) and was regis-
tered at the National Institutes of Health (NCT03851003)
on Feb 22, 2019. The first patient was recruited on May
10th 2019.
Statistical analysis
The normality of the data was tested using the Shap-
iro–Wilk or Kolmogorov–Smirnov tests. Comparison
between unrelated variables was conducted by Student’s t
test or Mann–Whitney U test, as appropriate. Data are pre-
sented as median and interquartile range. The Chi-square
and Fisher’s exact tests were used for comparison between
categorical variables. Logistic multivariate regression analy-
sis was used to determine which factors were significantly
and independently associated with RMT < 2.5 mm including
women’s age, parity, endometrial layer closure versus non-
closure group and the presence of symptoms. Significance
was accepted at p < 0.05. Statistical analyses were conducted
using the IBM Statistical Package for the Social Sciences
(IBM SPSS v.22; IBM Corporation Inc, Armonk, NY, USA).
The sample size calculations were based on Bamberg
et al. [21] randomized control prospective study compar-
ing single- (n = 149) to double-layer closure (n = 129) of
the cesarean hysterotomy, as no previous studies addressed
specifically the endometrial layer. RMT evaluated by
transvaginal ultrasound at 6–24 months follow-up was

4.1 ± 2.9SD mm for the single-layer group that was assumed
to be parallel to closure without the endometrial layer and
5.7 ± 1.7SD mm that assumed to be parallel to closure
including the endometrial layer. To achieve an 80% power
with a two-sided alpha of 0.05, we needed to enroll 48 in
each arm. We aimed to enroll 62 patients in each arm taking
under consideration 30% (n = 27) lost to follow-up.
Results
130 women were recruited for the study, of them follow-up
was achieved in 113 (86.9%) (Fig. 2). 61 (54%) vs. 52 (46%)
of the women were included in the endometrial closure vs.
non-closure groups, respectively.
The women’s demographic and clinical characteristics are
presented in Table 1. Median age, body mass index (BMI)
and parity were comparable between the groups. Follow-up
time for postoperative evaluation was 280 (228–380) and
295 (215–444) days for the closure and non-closure groups,
respectively (p = 0.86).
Table 2 presents the uterine and uterine scar charac-
teristics on transvaginal ultrasound examination. Uterine
measurements were all comparable between the groups.
Fig. 2  Study population
Archives of Gynecology and Obstetrics
Endometrial layer was found significantly thicker in the
non-closure group compared to the closure group [4.5
(3.1–6.4) vs. 3.1 (2.0–4.5) mm; p = 0.03]. Interestingly, the
median residual myometrial thickness was found to be lower
in the non-closure vs. the closure group [4.6 (3.0–6.5) vs.
5.3(3.0–7.7) mm; p = 0.38].
To date, there are no guidelines for a specific measure-
ment that is considered superior to define uterine scar defect.
Some studies define uterine scar defect when the proportion
is lower than 0.5 [22]. In our study, both groups had a pro-
portion between RMT/AMT lower than 0.5, with the non-
closure of endometrial layer measuring lower values than
the closure group [0.36 (0.19–0.55) vs 0.46 (0.27–0.61)].
This difference was not statistically significant (0.26). We,
like other teams, base our treatment on the RMT cutoff
of 2.5 mm (larger symptomatic uterine scar defects with
RMT < 2.5 mm is treated laparoscopically and smaller with
RMT > 2.5 mm hysteroscopically). Substantially low RMT
(< 2.5 mm) was measured in four (6.6%) and three (5.8%) of
the women, in the closure versus non-closure groups, respec-
tively (p = 0.86).
The rates of symptoms associated with uterine scar
defects reported on follow-up visit by the women are
described in Table 3. No statistically significant difference
Archives of Gynecology and Obstetrics

Table 1  Women’s demographic Endometrial closure Endometrial non-closure P value

and clinical characteristics (n = 61) (n = 52)

Age (years) 32 (31–34) 31 (29–33) 0.52

BMI (kg/m2) 28 (26–31) 29 (26–35) 0.31
Gravidity 2 (1–3) 2 (1–3) 0.24
Parity 1 (1–2) 1 (1–2) 0.90
Gestational week 38.3 (38.1–38.5) 38.3 (37.1–39.5) 0.64
Cervical dilatation 1 (1–1) 1 (1–1) 0.75
Pelvic station 4 (3–4) 4 (3–4) 0.72
Fetal weight 3171 (2778–3625) 3085 (2849–3359) 0.32
Estimated blood loss (ml) 500 (500–600) 500 (500–700) 0.48
Breastfeedinga 5 (8) 2 (4) 0.74
Time from surgery (days) 280 (228–380) 295 (215–444) 0.86

BMI—body mass index

Data are presented as median and Interquartile range
a
Data are presented as n (%)

Table 2  Uterine ultrasound Endometrial closure Endometrial non-closure P value

characteristics (n = 61) (n = 52)

Uterine length 52 (47–59) 59 (52–65) 0.16

Uterine height 35 (33–41) 40 (32–44) 0.38
Uterine width 49 (44–52) 50 (45–59) 0.25
Endometrial thickness 3.1 (2.0–4.5) 4.5 (3.1–6.4) 0.03
Niche length 6.3 (4.6–8.4) 4.9 (4.1–7.6) 0.23
Niche depth 3.3 (2.8–4.6) 4.0 (3.0–4.8) 0.46
Niche width 5.8 (4.0–6.4) 4.5 (3.6–7.6) 0.75
AMT 12.3 (10.7–14.3) 14.6 (11.2–16.7) 0.13
RMT 5.3 (3.0–7.7) 4.6 (3.0–6.5) 0.38
RMT/AMT 0.5 (0.3–0.6) 0.4 (0.2–0.5) 0.26
RMT < 2.5MMa 4.0 (6.6%) 3 (5.8%) 0.86

Residual myometrial thickness—RMT, adjacent myometrial thickness—AMT, endometrial scar defect

(niche)
Data are presented as median and Interquartile range
a
Data are presented as n (%)

Table 3  Symptoms associated with uterine scar defect was found in any of the reported symptoms including the
Endometrial Endometrial P value total symptomatic rate as a composite outcome including:
closure non-closure intermenstrual spotting, menorrhagia, dyspareunia and
(n = 61) (n = 52) pelvic pain. While comparing the uterine scar measurement
between the symptomatic and asymptomatic women, RMT
Intermenstrual spotting 2 (3.3) 0 (0) 0.23
was the only measurement that was found to be significantly
Menorrhagia 7 (11.4) 4 (7.7) 0.85
reduced in the presence of symptoms (Table 4).
Dyspareunia 2 (3.3) 3 (5.8) 0.31
To evaluate the factors associated with RMT < 2.5 mm,
Pelvic pain 3 (4.9) 6 (11.5) 0.50
a logistic regression analysis was performed including
Symptomatic—total 8 (13.1) 7 (13.5) 0.96
women’s age, parity, endometrial layer closure versus
Data are presented as n (%) non-closure group and the presence of symptoms. None

Table 4  Uterine ultrasound characteristics based on the presence of
symptoms
Symptomatic Non-symptomatic P value
(n = 14) (n = 33)
Niche length 7.25 (5.20–8.63) 5.60 (4.20–7.50) 0.09
Niche depth 4.30 (3.10–4.67) 3.40 (2.80–4.30) 0.34
AMT 13.70 (10.20–14.55) 13.00 (10.80–16.55) 0.60
RMT 4.2 (2.75–6.10) 6.95 (5.23–9.13) 0.006
Residual myometrial thickness—RMT, adjacent myometrial thick-
ness—AMT, endometrial scar defect (niche)
Data are presented as median and Interquartile range
of the parameters were associated with the RMT < 2.5 mm
(Supplement 1). Similarly, no association was found between
the presence of symptoms as a composite outcome and the
age, parity, gestational week at delivery and endometrial
layer closure versus non-closure group (Supplement 2).
Discussion
Principal findings
The principal findings of the study are: (1) closure versus
non-closure of the endometrial layer of the uterine incision
following cesarean section is associated with similar cesar-
ean scar characteristics; (2) endometrial layer was signifi-
cantly thicker in the non-closure compared to the closure
group (p = 0.03); (3) closure technique was not associated
with the presence of symptoms associated with uterine scar
defect.
Clinical implications
The importance to elucidate the risk factors associated with
the development of uterine scar defect cannot be overem-
phasized due to the known long-term morbidity including
gynecological symptoms, obstetric complications and poten-
tially infertility [15, 16].
Specific interest in surgery-related factors has grown
since those could be modified and serve as a potential strat-
egy to reduce the prevalence of uterine scar defect [23].
Low uterine incision during CS, an incomplete closure of
the uterine wall due to single-layer closure, endometrial sav-
ing closure technique or use of locking sutures have all been
associated with surgical risk factors [15, 24, 25]. In addition,
surgical acts that are associated with adhesion formation
including non-closure of peritoneum, inadequate hemostasis,
applied sutures and the use of adhesion barriers have also
been suggested [26].
Abnormal uterine bleeding (AUB) patterns are
considered the most common symptoms that are strongly
Archives of Gynecology and Obstetrics
and consistently associated with the presence of uterine
scar defect [27]. Study on symptomatic patients with AUB
that underwent surgical excision of the uterine scar revealed
histopathologic characteristic findings that mostly included
fibrosis, necrotic tissue, endometriosis, adenomyosis and
inflammatory infiltrate [27]. These changes most probably
can be attributed to improper approximation and abnormal
healing process of the endometrial layer [27, 28]. Although
in the past, avoiding the inclusion of the endometrial
layer into the uterine wall was considered the appropriate
technique while closing the hysterotomy during a cesarean
section, as newer closure techniques were introduced, the
importance of this practice has gradually lost its importance
[29, 30].
The impact of the endometrium on scar strength and
integrity has been studied in animal and human models
[15]. However, to date, studies addressing the endometrial
layer during incision closure following cesarean section are
limited and inconclusive. Antoine et al. [29] compared the
prevalence of residual uterine scar defect in the nongravid
uterus following first CS by saline infusion sonohystero-
gram. 25 women were compared to 20 women following
endometrium-free and routine non-endometrium-free hys-
terotomy closure techniques, respectively. A clinically sig-
nificant defect was six times higher in the non-endometrial
closure group. Therefore, they concluded that exclusion of
the endometrium at uterine closure reduces the development
of significant scar defects [29]. A randomized control trial
conducted by Tahermanesh [31] et al. allocated 34 vs. 38
women to closure in single layer excluding the endometrium
and to double-layer closure including the endometrium,
respectively. Large uterine scar defect, defined as more than
50% involvement (RMT/AMT), was significantly more com-
mon in the double-layer endometrial closure group [1 (2.9%)
vs. 9 (23.7%); p = 0.01]. In contrast to these studies, a recent
meta-analysis including six trials published by Genovese
et al. [32] supported the superiority of the double-layer clo-
sure over the single layer, with recommendation to include
the decidua in the first layer and overlap the first with the
second layer. Our study revealed no difference in the rate of
subsequent cesarean scar defect between hysterotomy closed
with and without the endometrial layer. A trend for larger
uterine scar depth and reduced RMT and RMT/AMT pro-
portion were found in the non-endometrial closure; however,
none of the measurements reached statistical significance.
The endometrial layer thickness was higher in the non-
endometrial closure group compared to the endometrial clo-
sure group (median 4.5 vs. 3.1 mm). This difference reached
significance (p = 0.03). The possible proposed explanation
to this observation might be due to improved aligning of
both edges of the incision. As the endometrium is primarily
not included in the suture, it is less likely to be entrapped
in the myometrial layer and therefore leads to better healing
Archives of Gynecology and Obstetrics
process. However, despite the differences in the endometrial
layer thickness between the groups, no significant differ-
ences were found in the uterine scar defect measurements.
Our study found lower RMT in the symptomatic group.
This finding is in concordance with previous studies [17].
However, while comparing closure techniques, there were
no differences in symptom rate (Table 3). Moreover, logistic
regression analysis for the presence of symptoms associated
with uterine scar defect did find the closure technique to be
statistically significant.
Strength and limitations
To the best of our knowledge, this is the first prospective
randomized study evaluating the association of endometrial
suturing with the risk of developing uterine scar defect. The
study findings have high reliability due to the prospective
design, randomization of the women and the high follow-
up rate (86.9%). In addition, all operations were performed
using the same technique by the same surgeon, minimizing
confounders that might have influenced the study results.
Finally, evaluation of the uterine scar was completed using
the objective parameters in addition to a questionnaire
assessing possible symptoms associated with uterine scar
defect.
The limitations of this study also need to be acknowl-
edged. As all operations were done by highly skilled obstet-
ric surgeons and uterine suturing was done with Staratafix
suture only, generalization of the study findings is limited.
Moreover, the definition of substantial uterine scar defect
still differs between clinicians and is not yet unified by
guidelines; however, the implication of the study conclu-
sions might be debated.
Conclusions
As cesarean section is one of the most common surgeries
worldwide with elevating rates, it is important to acknowl-
edge the potential long-term consequences of abnormal
uterine incision healing and to recognize the risk factors
associated with them. In the present study, we found that
closure versus non-closure of the endometrial layer during
cesarean uterine incision repair has no significant differ-
ence in cesarean scar characteristics and symptom rates at
6 months follow-up. The study findings support both tech-
niques that are currently done based on the surgeon’s prefer-
ence. This information should be of value to physicians and
patients alike.
Supplementary Information The online version contains
supplementary material available at https:// ​ d oi. ​ o rg/ ​ 1 0. ​ 1 007/​
s00404-​024-​07417-1.
Acknowledgements N/A.
Author contributions AMS: conception and design, or acquisition
of data, analysis and interpretation of data, statistical analysis. EC:
surgeon performing the procedures, acquisition of data, reviewing
­manuscript. TD: acquisition of data. AB: acquisition of data. RE: acqui-
sition of data. AC: acquisition of data. MZ: conception and design,
analysis and interpretation of data. JH: conception and design, analysis
and interpretation of data. RM: conception and design, writing, editing.
Funding The study was supported by Sheba Medical Center institu-
tional sources.
Declarations
Conflict of interest The authors report no conflict of interest.
Ethical approval The study protocol was approved by the “Sheba
Medical Center” Review Board (ID 5822–18-SMC) and was registered
at the National Institutes of Health (NCT03851003) on Feb 22, 2019.
Consent to participate All participants gave their informed written
consent to participate in the study.
Consent for publication All authors gave consent for publication.
Data availability Data will be available upon request.
Code availability N/A.
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