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Journal of Investigative Surgery

ISSN: 0894-1939 (Print) 1521-0553 (Online) Journal homepage: https://www.tandfonline.com/loi/iivs20

An Optimal Uterine Closure Technique for Better


Scar Healing and Avoiding Isthmocele in Cesarean
Section: A Randomized Controlled Study

Ziya Kalem, Aski Ellibes Kaya, Batuhan Bakırarar, Alper Basbug & Müberra
Namlı Kalem

To cite this article: Ziya Kalem, Aski Ellibes Kaya, Batuhan Bakırarar, Alper Basbug & Müberra
Namlı Kalem (2019): An Optimal Uterine Closure Technique for Better Scar Healing and Avoiding
Isthmocele in Cesarean Section: A Randomized Controlled Study, Journal of Investigative Surgery,
DOI: 10.1080/08941939.2019.1610530

To link to this article: https://doi.org/10.1080/08941939.2019.1610530

Published online: 09 May 2019.

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Journal of Investigative Surgery, 0: 1–9, 2019
Copyright # 2019 Taylor & Francis Group, LLC
ISSN: 0894-1939 print / 1521-0553 online
DOI: 10.1080/08941939.2019.1610530

ORIGINAL RESEARCH

An Optimal Uterine Closure Technique for Better Scar


Healing and Avoiding Isthmocele in Cesarean Section:
A Randomized Controlled Study
Ziya Kalem1, Aski Ellibes Kaya2, Batuhan Bakırarar3, Alper Basbug2 and
M€uberra Namlı Kalem4

1
Department of Obstetrics and Gynecology, Gurgan Clinic IVF and Women Health Center, Ankara, Turkey;
2
Department of Obstetrics and Gynecology, Duzce University, Duzce, Turkey; 3Department of Biostatistics, Ankara
University, Ankara, Turkey; 4Department of Obstetrics and Gynecology, Liv Hospital Ankara, Ankara, Turkey

ABSTRACT
Objective: The aim of this study is to compare the effects of two different uterine closure techniques, used
during cesarean section (CS) operations on isthmocele formation. Material and Methods: This prospective,
randomized, controlled study was performed on 138 patients in a university hospital between the dates
December 2016 and August 2017. Uterine closures were performed using the double-layer, far-far-near-near
(FFNN) unlocked technique, in the study group (n ¼ 70) and using a single-layer continuous locked (SLL)
technique in the control group (n ¼ 68). The presence of isthmocele, residual myometrial thickness (RMT),
postmenstrual spotting, dysmenorrhea, chronic pelvic pain and uterus position were evaluated in postopera-
tive sixth month. Results: Isthmocele formation was less frequent and RMT was greater in the study group
when compared to the control group (p < 0.001 and p < 0.001, respectively). Duration of operation, amount
of blood loss and additional hemostatic suture requirement were not significantly different between the two
groups (p ¼ 0.221, p ¼ 0.520 and p ¼ 0.930, respectively). Postmenstrual spotting was less common in FFNN
group, while the rates of chronic pelvic pain and dysmenorrhea were not significantly different between the
groups (p ¼ 0.002, p ¼ 0.205 and p ¼ 0.490, respectively). Conclusion: The findings of the present study demon-
strate that uterine closure using the FFNN technique is beneficial in terms of providing protection from isth-
mocele formation and ensuring sufficient RMT. This method has the potential to become the optimal
uterine closure technique, but the findings of the present study should be supported by large-scale studies
in the future.
Keywords: cesarean; isthmocele; suturing technique; residual myometrial thickness; scar healing; double-
layer suturing

INTRODUCTION contrast-enhanced sonohysterography in a random


population of women with a history of CS [2]. The
Isthmocele, which was first defined in 1995 by most common gynecologic problems associated with
Morris, is a uterine scar defect resulting from the isthmocele include menstrual spotting, dysmenor-
poor healing of an incision in the uterus [1]. In fact, rhea, dyspareunia, chronic pelvic pain and infertility
the frequency of niche occurrence varies in patients [3, 4], and there is also an increased risk of scar preg-
who have had a cesarean section (CS). While the rate nancy, placentation abnormalities and the develop-
of isthmocele detection in pelvic ultrasonographies ment of uterine ruptures in future pregnancies [5, 6].
varies between 6 and 36 percent, the range Considering the worldwide increase in rates of
is between 56 and 84 percent when using a CS operations, the current rate of isthmocele and

Address correspondence to M€ uberra Namlı Kalem, MD, Department of Obstetrics and Gynecology, Liv Hospital Ankara, Ankara,
Turkey. E-mail: muberranamli@hotmail.com

Color versions of one or more of the figures in the article can be found online at www.tandfonline.com/iivs.
Supplemental data for this article is available online at https://doi.org/10.1080/08941939.2019.1610530.

1
2 Z. Kalem et al.

associated complications should not be overlooked.


Although hysteroscopic and laparoscopic isthmocele
repair procedures have demonstrated high success
rates [7, 8], measures to prevent the formation of
isthmocele during CS operations should be the pri-
mary goal. The selected uterine closure technique is
considered to be the most important factor affecting
isthmocele formation [9, 10], although other factors
include close proximity of the uterine incision to the
cervix, the formation of adhesions, myometrial
ischemia and impaired wound healing [11, 12].
An optimal uterine closure technique should FIGURE 1. Schematic representation of far-far, near-near
ensure better scar healing, reduce the risk of isthmo- suture technique.
cele formation and also decrease risks related to the
most important long-term complications, including CS operation were also excluded from the study, as
placentation abnormalities and uterine rupture. We this is not appropriate for the investigated uterine
believe that the endometrial sparing double-layer closure technique.
unlocked suture technique – defined in 2012 by Babu In total, 138 patients included to the study were
and Magon as a continuous modified mattress suture randomized at a ratio of 1:1 and divided into two
– is the optimal technique for uterine closures. This groups using a computer system. A Pfannenstiel
technique ensures full-thickness decidua-to-decidua, incision was made and a Kerr incision was made on
myometrium-to-myometrium and serosa-to serosal the lower uterine segment of all patients. Following
approximation of the uterine cut margins and good a 2 cm transverse incision, the lower uterine segment
homeostasis. The method also eliminates the eversion was opened by cutting myometrium with scissors.
problems associated with single-layer sutures, vascu- In the control group, the uterine closure was carried
larization problems resulting from locking, and endo- out using a continuous single-layer locked closure
metrial inversion problems seen in sutures including technique. The suture passed from the junction of
the endometrium [13]. the endometrium and myometrium, and was locked
The present study was carried out to compare to enclose the complete myometrium and perime-
the modified mattress suture technique, which was trium, while the suture did not enclose the decidua
described by Babu and Magon as a uterine closure and the visceral peritoneum was not closed. The
technique for CS operations, with the conventional suturing technique used in the study group, as
single-layer locked technique, in terms of their shown in Figures 1 and 2, was the far-far-near-near
effects on isthmocele formation. (FFNN) continuous unlocked double-layer method,
carried out in a single step. The steps followed dur-
ing this suturing technique, which will be referred
MATERIALS AND METHODS to hereafter as FFNN, were as follows. First, a sin-
gle-suture was made to both ends of the incision
This prospective, randomized and controlled trial line; then, the needle was inserted starting 1 cm
was carried out to compare two different uterine away from the lower margin of the incision(x0) and
closure techniques used for CS operations, and coming out at the junction of the myometrium and
included 138 patients between December 2016 and decidua of the lower edge of the incision (z0) and
August 2017. The study was granted ethics commit- the myometrium was covered in a single-layer.
tee approval by the Duzce University Medical Afterwards, the needle was inserted at the junction
Faculty Ethics Committee, and all participants pro- of the decidua and myometrium of the upper edge
vided written informed consent. of the incision (z1), and came out 1 cm away from
The study inclusion criteria were as follows: the margin of the upper edge (x1) and the first loop
women aged between 18 and 40 years with a BMI of formed was kept at traction. In the next step, a
15.5–34.9, had a single pregnancy, were at more superficial bite was taken from the outer border of
than the 38th week of pregnancy and underwent CS the subperitoneal fascia and the outer myometrium
operation. The exclusion criteria were as follows: from the lower edge (y0), while the needle was fac-
presence of diabetes or hypertension, thrombophilia, ing the same direction the same transition was
a previous history of CS or other uterine surgeries, repeated on the cranial side (y1). While the assistant
has lower segment myoma (a congenital uterine was holding two loops, the first and the larger loop
abnormality), placental decollement or placenta pre- was pulled first and then the superficial loop was
via. Additionally, patients who were found to have pulled, thus the tissues were brought opposite to
very thin low segments (less than 0.5 cm) during the each other and while the assistant was maintaining

Journal of Investigative Surgery


3

FIGURE 2. Top view of tissue sutured by far-far, near-near


suture technique.

the traction of the thread the surgeon continued the


same process for the next bite. The next suture was
made leaving a 1–1.5 cm gap without locking. This
method (as required in any ideal surgical method)
allows the accurate opposite approximation of the
serosa, myometrium and decidual tissues. A full- FIGURE 3. Ultrasonographic appearance of isthmocele,
thickness approximation prevents the inversion or residual myometrial thickness and uterus position.
eversion of the tissue layers, while also preventing
the problem of insufficient vascularization due to patients’ age, BMI, previous pregnancies, number of
locking. Decidual tissues were not included in the births and dilation and curettage (D&C) was col-
suture in this patient group. Additionally, as the lected, and the cervical dilatation at the operation
serosal layers were approximated completely oppos- was also recorded for patients in labor. CS indica-
ite to each other, the visceral peritoneum was not tions, the duration of operation and any additional
closed either in the study or in the control group. suture requirements were noted. In order to calcu-
The parietal peritoneum was also not sutured in late the amount of blood loss, the difference
either of the groups. between the preoperative hemoglobin levels and the
During all of the CS procedures performed in levels measured at the postoperative 36th hour was
this study, uterine closure was carried out using calculated. All patients included to the study were
synthetic absorbable No:1 Polyglactin (Coated asked to return for a control visit six months after
VICRYLV R [polyglactin 910] Sutures, Ethicon, NJ, CS. During this visit, a clinical examination was
USA). All patients were given an intraoperative sin- made using a vaginal B-ultrasound (Voluson 730
gle dose of intravenous antibiotics (1 gram cefazolin) Expert; General Electric Healthcare, Solingen,
_
(Bilim Ilaç, Istanbul, Turkey). Germany) was obtained to determine the presence
During the follow-up of the patients, demo- of isthmocele, residual myometrial thickness (RMT)
graphical data were recorded and data on the and uterus position (Figure 3). One year after CS all

# 2019 Taylor & Francis Group, LLC


4 Z. Kalem et al.

patient were asked about the presence of dysmenor- Power analysis


rhea, postmenstrual spotting and chronic pelvic pain
by phone call. The power of the study was estimated to be 0.99 in
a power analysis performed using a Student T-Test
on a sample of 138 people at a significance level of
Statistical analysis 0.05, assuming the mean ± SD values of the Group
categories (Control-Case) for the RMT quantitative
All statistical analyses were performed using the variable were 5.09 ± 1.79 and 8.52 ± 2.82, respectively.
SPSS for Windows 11.5 software program (SPSS
Inc., Chicago, IL). Descriptive statistics were pre-
sented as mean ± SD and median (min-max) for
quantitative variables, and numerically (percentage) RESULTS
for qualitative parameters. For the quantitative vari-
ables, the potential significant differences between The study included 138 patients, including 70
the categories of the binary qualitative variables patients in the study group and 68 patients in the
were tested by a Mann-Whitney U-Test, as these control group. A flow diagram of the participants is
parameters did not meet the assumptions of normal given in Supplemental File 1. Demographical charac-
distribution. A chi-square test and a Fisher Exact teristics, operational data and postoperative findings
Test were used to test the relations between two cat- were evaluated and compared between the two
egorical variables. A linear regression analysis was groups, and the numerical data collected in this
carried out to investigate how a measured depend- study are presented in Table 1, while categorical
ent variable was affected by one or more independ- data are shown in Table 2, along with the compari-
ent variables, and to what extent the change in the sons of the two groups. The results revealed no stat-
dependent variable could be attributed to the inde- istically significant differences between the study
pendent variable(s). A multiple logistic regression groups in terms of demographical data, indications
was performed to ascertain the effects of one vari- for operation or operation-specific parameters. The
able or more than one variable together on the likeli- results of the postoperative evaluations showed that
hood that participants will develop isthmocele. A p RMT was found to be significantly statistically lower
value of 0.05 was considered statistically significant. and the rates of isthmocele development, and

TABLE 1. Demographical characteristics, operational data and postoperative findings (numeric data)

Groups
SLL suture (n ¼ 68) (Control) FFNN suture (n ¼ 70)
Median Median
Variables Mean ± SD (Min-Max) Mean ± SD (Min-Max) p Value

Age (year) 29.25 ± 6.27 29.00 28.94 ± 5.17 29.00 0.773


(19.00–40.00) (19.00–40.00)
BMI 26.04 ± 2.37 25.82 25.90 ± 2.28 25.87 0.735
(21.00–31.00) (21.32–30.59)
Gravida (n) 1.97 ± 1.55 1.00 1.36 ± 0.85 1.00 0.052
(1.00–6.00) (1.00–5.00)
Parity (n) 0.85 ± 1.20 0.00 0.30 ± 0.73 0.00 0.071
(0.00–4.00) (0.00–3.00)
D&C (n) 0.35 ± 0.79 0.00 0.19 ± 0.52 0.00 0.092
(0.00–5.00) (0.00–3.00)
Gestational weeks at delivery 38.50 ± 2.7 38.60 39.40 ± 3.6 39.10 0.646
(38.00–41.00) (38.00–41.00)
Birthweight (g) 3230.76 ± 506.24 3225.00 3260.26 ± 485.74 3276.50 0.785
(1525.00–4850.00) (1950.00–4920.00)
Cervical dilatation at operation (cm) 1.34 ± 1.79 0.00 0.84 ± 1.71 0.00 0.067
(0.00–7.00) (0.00–9.00)
Operative time (minute) 36.91 ± 6.23 35.00 35.71 ± 7.68 35.00 0.221
25.00–50.00) (25.00–55.00)
Blood loss (g/dL) 1.08 ± 0.63 1.00 1.01 ± 0.64 0.95 0.529
(Preoperative Hb-Postoperative Hb) (1.00–2.60) (0.00–2.70)
RMT (mm) 5.09 ± 1.79 5.05 8.52 ± 2.82 8.65 <0.001
(1.96–11.00) (2.30–13.10)

BMI, body mass index; RMT, residual myometrial thickness, D&C: dilatation-curettage.

Journal of Investigative Surgery


TABLE 2. Demographical characteristics, operational data and postoperative findings (categorical data)

Group
FFNN

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SLL (n ¼ 68) (Control) (n ¼ 70)
Variables n % n % p Value

CS indications Prolonged labor 11 14.3 7 9.7 0.123a


CPD 6 7.8 8 11.1
Pathological cardiotocography 12 15.6 7 9.7
Macrosomy 7 9.0 5 6.9
Breech presentation 9 11.7 2 2.8
Other malpresentations (transverse, oblique) 4 5.2 6 8.3
Maternal pelvic deformity 3 3.9 5 6.9
Primary genital herpes 2 2.6 4 5.6
Active vulvovaginal HPV lesions 2 2.6 7 9.7
Abnormal fetal Doppler 3 3.9 4 5.6
Others (maternal anxiety, acute appendicitis, maternal trauma, maternal cardiomyopathy) 9 11.7 15 20.8
Additional hemo- No 54 79.4 59 84.2 0.930a
static suture Yes 13 19.1 11 15.7
requirement
Isthmocele No 40 58.8 63 90.0 <0.001b
Yes 28 41.2 7 10.0
Postmenstrual No 53 77.9 67 95.7 0.002b
spotting Yes 15 22.1 3 4.3
Dysmenorrhea No 63 92.6 67 95.7 0.490a
Yes 5 7.4 3 4.3
Chronic pel- No 64 94.1 69 98.6 0.205a
vic pain Yes 4 5.9 1 1.4
Uterus position Anteverted 55 80.9 58 82.9 0.827b
Retroverted 13 19.1 12 17.1

CPD, cephalopelvic disproportion; HPV, human pappilloma virus.


a
Fisher exact test.
b
Chi-square test.
5
6 Z. Kalem et al.

TABLE 3. RMT (linear regression) when variables were introduced to the model one by one

95% Confidence Interval


Independent variables b S.E R 2
p Value Lower limit Upper limit

Group (FFNN) 3.043 0.404 0.347 <0.001 2.634 4.232


Parity 0.643 0.238 0.051 0.008 1.115 0.172
D&C 0.857 0.370 0.038 0.022 1.588 0.126
Cervical dilatation at operation 0.342 0.139 0.042 0.015 0.617 0.066
Uterine position (Anteversion) 0.124 0.649 0.001 0.848 1.407 1.158

RMT, residual myometrial thickness; FFNN, far-far, near-near technique.

TABLE 4. Isthmocele (logistic regression) – when all variables were introduced to the model one
by one

95% Confidence Interval


Independent variables (reference category) b S.E. OR p Value Lower limit Upper limit

Group (FFNN) 1.841 0.468 6.300 <0.001 2.515 15.779


Parity 0.203 0.179 1.225 0.258 0.862 1.740
D&C 0.496 0.284 1.641 0.081 0.941 2.863
Cervical dilatation at operation 0.201 0.104 1.222 0.054 0.997 1.498
Uterine position (retroversion) 1.500 0.466 4.481 <0.001 1.799 11.159

FFNN, far-far, near-near technique.

postmenstrual spotting were significantly higher in DISCUSSION


the controls than in the study group (Tables 1
and 2). In the present study, the rate of isthmocele develop-
None of the patients included in the study ment was found to be lower, and RMT was
developed uterine atony or endometritis. increased in the group in which the endometrial
A linear regression analysis was carried out to sparing, unlocked double-layer FFNN suture tech-
evaluate the factors potentially affecting the RMT of nique was used as the method of uterine closure
the patients (Table 3). RMT was seen to decrease as during a CS operation, when compared to the group
the number of parities and previous dilatation-curet- that underwent a single-layer locked closure tech-
tage (D&C) procedures increased, RMT also nique. The duration of operation, amount of blood
decreased when cervical dilatation was high during loss and additional hemostatic suture requirements
CS. A multiple linear regression model was found did not differ significantly between the groups.
to be RMT 5 5.533 1 3.264 * Group (FFNN) 1 While the rate of postmenstrual spotting was lower
(20.523) * D&C 1 (20.196) * Cervical Dilatation in the FFNN group, the rates of chronic pelvic pain
and the p values of the relevant variables were and dysmenorrhea were not significantly different
<0.001, 0.086 and 0.091, respectively. When these between the groups.
variables were incorporated into the model together, In a search of literature related to the potential
they accounted for 37.7 percent of the change in the etiologic factors associated with the development of
RMT variable. isthmocele, incomplete closure of the uterine wall
A multiple logistic regression analysis was car- comes to the fore as the most powerful hypothesis
ried out to ascertain the effects of group (FFNN), [12]. The most important feature of the uterine clos-
D&C and retroversion together on the likelihood of ure technique used in this study is that it allows a
isthmocele formation (Table 4). The logistic regres- complete opposite approximation of the tissue
sion model was found to be statistically significant layers, which is a primary surgical principle [14].
(p < 0.001), explaining 31.3 percent (Nagelkerke R2) The endometrium–myometrium junction is passed
of the variance in isthmocele, and correctly classify- and a superficial bite is taken from the serosal sur-
ing 74.5 percent of cases. The control group (SLL) face in this method, after which, a complete layer is
was 6.89 times more likely to develop isthmocele passed in the myometrium and the layers are
than the FFNN group, and the retroverted uterine approximated opposite to each other. In this way,
position was 6.57 times more likely to be associated the endometrium and perimetrium are also located
with isthmocele than uterine anteversion. The completely opposite to each other.
increasing number of D&C was associated with an The benefits of single- or double-layer closures
increased likelihood of developing isthmocele. of the uterus are also a matter of debate in literature

Journal of Investigative Surgery


7

[2]. In a recently published meta-analysis [15] and a uterus closure [12, 27]. The eversion of myometrium
prospective cohort study reported by Vikhareva to serosa increases the possibility of adhesions, and
Osser and Valentin [16], no difference was found in its inversion into the cavity results in postoperative
terms of the formation of cesarean scar defects endometrial defects [28]. The invasion of endomet-
between single- or double-layer closures of the ute- rium into the myometrium also facilitates the devel-
rus. However, the double-layer closure method is opment of adenomyosis [29], and all such events
currently recommended by certain teams for the contribute to niche formation. With this in mind,
prevention of the formation of isthmocele [17–19]. In particular attention was paid to this issue in both
the present study, a double-layer technique was suturing groups in the present study, and the sur-
used in the group with a lower rate of isthmocele geon was particularly careful to ensure the opposite
development, leading us to believe that the double- approximation of the tissues in the control group,
layer technique is more effective in ensuring the sta- whereas the FFNN method already eliminates the
bilization of the myometrium, which is both thick possibility of inversion and eversion.
and dynamic due to its contractility. In the present study, a multiple regression ana-
There have been reports in literature suggesting lysis was carried out to evaluate the factors affecting
that the endometrium should be incorporated into isthmocele development other than the uterine clos-
the suture to prevent uterine scar defects, and the ure technique. A previous history of D&C was
full-thickness suture method ensures better wound found to increase the risk of isthmocele, while ute-
healing [17, 20]. We, on the other hand, believe that rus retroversion was also accompanied by an
full-layer suturing of the uterus including the endo- increased rate of isthmocele formation. A further
metrium may lead to a weaker scar healing, since it regression analysis carried out to investigate the fac-
will cause a decidual inclusion in the scar tissue and tors affecting RMT indicated that increased cervical
facilitate the formation of a niche. For this reason, dilatation during CS, having a previous history of
we did not include the deciduas in the suture in childbirth and D&C were found to be associated
either the study or control groups, and there are a with a lower RMT. There are also studies in litera-
number of reports in the literature to support this ture that report that the number of previous births
[21–23]. In several animal experiments, Poidevin and history of D&C reduces RMT and increases the
demonstrated that suturing the complete thickness possibility of cesarean scar defects [2, 12]. Similarly,
of the uterus, including the endometrium, led to increased cervical dilatation at the time of the CS
inclusions of endometrial tissue in the scar, resulting operation was listed among the risk factors for
in scar defects several weeks or months later [24]. incomplete healing of uterine incisions in literature
Among the previous studies in the literature [16, 30].
comparing locked and unlocked suture techniques This is the first prospective randomized con-
for uterine closure, Ceci et al. [25] identified no sig- trolled study in literature to compare the rate of
nificant difference between the two techniques in isthmocele formation and RMT between the single-
terms of scar defects, whereas Yasmin et al. [26] layer locked closure technique and the FFNN tech-
nique, which we believe is the optimal uterine clos-
reported higher RMT in the unlocked group.
ure technique in CS operations. In the present
Roberge et al. [18] also found that the closure of ute-
study, all operations were performed by the same
rus by the locked suture technique reduced RMT,
surgeon, in both study and control group, to avoid
and concluded:
any potential differences that may occur due to the
surgical techniques of different surgeons, which is a
It is possible that the locked suture, by being
more hemostatic, can cause a strangulation of the factor that enriches the power of this study. The crit-
scar tissue and leads to weaker healing. It is also ical limitation of this study is the single-layer suture
possible that the weakness of the scar in the technique of the control group. It would be more
locked suture is secondary to the fact that this appropriate study design to compare patients with
technique is usually performed with inclusion of continuous unlocked double-layer suture as the con-
the inner part of the uterine wall (decidua/ trol group and patients with FFNN suture as the
endometrium) in the scar tissue. study group. The other limitations of this study is
the absence of subgroups, and a comparison of both
According to a recent systematic review, only suture techniques between subgroups such as endo-
the “locked” single-layer closure was associated metrium included-excluded, and peritoneum
with uterine rupture [23]. Similarly, we also believe sutured-non-sutured would increase the value of
that the locked suture technique should not be used this study.
for uterine closure in CS. FFNN technique prevents istmocele develop-
One of the factors impairing scar healing after a ment and contributes more RMT because this tech-
CS operation is tissue inversion and eversion during nique provides complete approximation of the tissue

# 2019 Taylor & Francis Group, LLC


8 Z. Kalem et al.

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