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Ultrasound Evaluation of the Uterine Scar

After Cesarean Delivery


A Randomized Controlled Trial of One- and Two-Layer Closure
Benjamin D. Hamar, MD, Shelley B. Saber, MD, Michael Cackovic, MD, Lissa K. Magloire, MD,
Christian M. Pettker, MD, Sonya S. Abdel-Razeq, MD, Victor A. Rosenberg, MD,
Irina A. Buhimschi, and Catalin S. Buhimschi, MD

OBJECTIVE: To survey the uterine scar thickness by ultra- CONCLUSION: The process of uterine scar remodeling
sonography in women randomly assigned to one- or two- can be successfully monitored by ultrasonography. Uter-
layer hysterotomy closure after primary cesarean delivery. ine scar thickness diminishes progressively after both
METHODS: This was a randomized, blinded trial of uter- one- or two-layer closure but does not vary with mode of
ine scar closure with ultrasonographic follow-up. Thirty hysterotomy closure. The uterine scar thickness remains
consecutive patients undergoing primary cesarean deliv- increased even at 6 weeks post partum, suggesting that
the process of uterine scar remodeling extends beyond
ery were enrolled and randomly assigned to one- or
the traditional postpartum period.
two-layer closure of the hysterotomy. Ultrasound surveil-
lance of the uterine scar thickness was performed at CLINCAL TRIAL REGISTRATION: ClinicalTrials.gov, www.
baseline (before surgery) and 48 hours, 2 weeks, and 6 clinicaltrials.gov, NCT00224250
(Obstet Gynecol 2007;110:808–13)
weeks post partum.
LEVEL OF EVIDENCE: I
RESULTS: Patient compliance with the postpartum sur-
veillance protocol was 90%, and the uterine scar was
visualized in 99% of attempted ultrasonographic exami-
nations. There were no differences between groups at
baseline or at any of the follow-up evaluations. An initial
C esarean delivery has become more common,
with primary cesarean delivery rates increasing
from 21.2% in 1996 to 27.1% in 2003.1 Over the same
5- to 6-fold increase in uterine scar thickness was ob- interval, vaginal birth after cesarean birth has de-
served, followed by a gradual decrease with the 6-week
creased from 28.3% to 10.6%.1 This decrease may be
measurements still thicker than baseline. Repeated mea-
attributed to concerns regarding the risks during trials
sures analysis of variance showed significant variation
across time points starting either at baseline (P<.001) or
of labor, such as uterine rupture, estimated to occur in
at 48 hour postoperatively (P<.001), but this variation did 0.3– 4.0% of pregnancies with history of cesarean
not depend on closure type (Pⴝ.79 for all visits and Pⴝ.81 delivery.2–7 The risk for poor obstetric outcome in a
beginning with 48-hour postoperative time point). subsequent pregnancy has been shown to be related
to surgical technique, with classical cesarean delivery
having the highest risk for rupture and lower segment
From the Yale School of Medicine, Department of Obstetrics, Gynecology, and
Reproductive Biology, New Haven, Connecticut. incisions having a lower risk.8
Initially presented at the Society for Maternal–Fetal Medicine 27th Annual
Currently, a low-transverse incision is the pre-
Meeting, February 5–10, 2007, San Francisco, California. ferred method of hysterotomy during cesarean deliv-
The authors thank Jim Dziura, PhD, of Yale University for his assistance with ery. This incision has traditionally been repaired with
part of the statistical analysis. a two-layer closure, although a one-layer closure has
Corresponding author: Benjamin Hamar, MD, Beth Israel-Deaconess Medical been shown to be as effective for surgical closure and
Center, 330 Brookline Avenue, Boston, MA 02215; e-mail: bhamar@bidmc. hemostasis,9 with the advantages of shorter operative
harvard.edu.
time, decreased blood loss, lower rates of endometri-
Financial Disclosure
The authors have no potential conflicts of interest to disclose.
tis, and shorter hospital stay.10 A one-layer closure
usually involves a single continuous, locking layer of
© 2007 by The American College of Obstetricians and Gynecologists. Published
by Lippincott Williams & Wilkins. absorbable suture. A two-layer closure typically adds
ISSN: 0029-7844/07 an imbricating layer of absorbable suture. Substantial

808 VOL. 110, NO. 4, OCTOBER 2007 OBSTETRICS & GYNECOLOGY


research effort has attempted to estimate whether their hysterotomy closed in one layer with a running,
one- or two-layer closure provides better outcomes locking suture of 0-Polysorb (coated, braided glycolide/
and a lower risk for uterine rupture in subsequent lactide polymer; U.S. Surgical, Norwalk, CT).
pregnancies.10 –13 Several studies have shown an in- Patients randomly assigned to a two-layer closure
crease in uterine scar disruption for one-layer clo- had an initial closure identical to the one-layer closure
sure10,13 while others have shown no effect.11,12 Impor- as above. An additional layer of 0-Polysorb suture was
tantly these research efforts have been limited by their used to imbricate the first layer in a continuous,
retrospective nature and the biases inherent in study- nonlocking suture.
ing surgical technique with these methods. All closures were performed by one of the inves-
To assess the risk of uterine rupture in a subse- tigators according to a study protocol. For each
quent pregnancy, researchers have used ultrasonog- patient, additional hemostatic sutures were placed at
raphy in the evaluation of the uterine scar in the the discretion of the operating physician, and the
second14 and third trimesters15–18 as well as the post- number of additional sutures was recorded. Also
partum period.19 It has generally been found that the recorded prospectively were labor at time of cesarean
thicker the uterine scar the lower the rate of complica- delivery, clinical chorioamnionitis or endometritis as
tions.14 –16,18,19 One may postulate that a thicker scar is assessed by the treating physician, estimated blood
stronger, and thus performs better, than a thinner one. loss at surgery, hematocrit change (preoperative mi-
Whether thickness of the uterine scar varies with the nus 24 hours postoperative), duration of surgery, birth
technique used at the time of hysterotomy closure is weight, sex of newborn, and whether the mother was
an unexplored question. breastfeeding. All patients received a single dose of a
Our hypothesis is that uterine scar thickness is
first-generation cephalosporin antibiotic (or equiva-
unaffected by the type of hysterotomy closure (one-
lent if penicillin allergic) at umbilical cord clamping
versus two-layer). We performed a randomized trial
per hospital protocol.
of hysterotomy closure at primary cesarean delivery
Patients had an evaluation of the lower uterine
using one- versus two-layer technique, with a prospec-
segment immediately preoperative (baseline) and
tive blinded ultrasonographic follow-up of the uterine
then follow-up measurements at 48 hours, 2 weeks,
scar.
and 6 weeks postoperatively according to a study
MATERIALS AND METHODS protocol. Baseline measurements were obtained by
Patients were identified as potential study subjects if measuring the myometrial thickness in the midsagittal
they were to have a term primary cesarean delivery at plane by transabdominal ultrasonography at a point
term at Yale-New Haven Hospital between January below the reflection of the bladder in a technique
2005 and June 2006. Patients were approached for described by Buhimschi et al20 and illustrated in
participation if their delivery was a scheduled primary Figure 1. Previously published reports have shown
cesarean delivery or a nonemergent cesarean delivery that the lower uterine segment thickness measured by
in labor. Exclusion criteria were multiple gestations, a ultrasonography is not altered by labor status.20 Post-
pain score greater than 4 out of 10, abnormalities of operative evaluation of the uterine incision involved
fetal heart rate (variable or late decelerations), prior identifying the uterine scar as described by Koutsoug-
uterine surgery, hydramnios, uterine malformation, eras et al19 and measuring the scar in the midsagittal
maternal diabetes, connective tissue disorders, and plane perpendicular to the uterine wall by transab-
non-English language. Before initiation of the study, dominal or transvaginal approach. The scar was
random allocation was performed using premade identified by a discontinuity in the architecture of the
allocation cards (N⫽30), specifying “one-layer” or uterus in the midsagittal plane and was manifest by
“two-layer,” sorted in blocks of 10 and placed into either a hyperechoic or hypoechoic line perpendicu-
sequentially numbered, sealed, opaque envelopes. lar to the wall of the uterus. A transabdominal ap-
After obtaining written consent and confirming entry proach was attempted, but if the scar was poorly
into the study, each patient was assigned a treatment visualized, transvaginal ultrasonography was used.
group by selection of the next consecutive envelope. Measurements were done by one of the investigators
The group allocation was revealed to the surgeon (B.D.H., S.B.S., or C.S.B.) who were blinded to the
during the surgery just before the hysterotomy repair. allocation group for hysterotomy closure. Previous
The Yale Human Investigation Committee ap- studies by our group have validated the interobserver
proved the research protocol and consent process. and intraobserver variability of these measurements
Patients randomly assigned to one-layer closure had taken by this method.20

VOL. 110, NO. 4, OCTOBER 2007 Hamar et al Ultrasonography of Uterine Scar After Cesarean 809
Fig. 1. Measurement of the preoperative myometrial thick-
ness by ultrasonography in the midsagittal plane. B, blad-
der; F, fetus in amniotic cavity.
Hamar. Ultrasonography of the Uterine Scar After Cesarean.
Obstet Gynecol 2007.

Measurements were carried out using GE Logiq 3


or GE Voluson 730 ultrasound machine (GE Health-
care, Chalfont St. Giles, United Kingdom) using a 3-
to 5-MHz or 4- to 7-MHz transabdominal transducer
or a 5- to 9-MHz transvaginal transducer as necessary.
A sample size calculation was performed to esti-
mate the required number of participants. Based on
available data,20 to detect a 10% difference in myome-
trial thickness between groups or between study periods
with 80% power and ␣⫽0.05, it was anticipated that 30
subjects (15 per closure group) would be required.
Data were tested for normality using the Kolmog-
orov-Smirnov method and reported as either mean
and 95% confidence interval (CI) (for normally dis-
tributed data) or as median and interquartile range
(IQR) (for skewed data). Comparisons between two
groups were performed using Student t tests or Mann-
Whitney rank sum tests as appropriate. Two-tailed Fig. 2. Flow diagram of the recruitment and follow-up of the
analysis was performed in all cases. Multiple compar- study population.
ison procedures were performed using repeated mea- Hamar. Ultrasonography of the Uterine Scar After Cesarean.
Obstet Gynecol 2007.
sures analysis of variance followed by Tukey or
Dunn’s post hoc comparisons as appropriate. Propor-
tions were compared with ␹2 or Fisher exact test as RESULTS
appropriate. Statistical analyses was performed using Thirty patients were recruited and randomly assigned
SPSS 11.0.4 (SPSS, Inc, Chicago, IL). Sample size and to one- or two-layer closure (15 per group, Fig. 2).
power analysis calculations were performed using Demographic data revealed that the women in the
JMP 5.0 (SAS Institute, Inc, Chicago, IL). Throughout one-layer group were significantly older, but that
our analyses, we considered a P value ⬍.05 to indicate there were no other significant demographic differ-
statistical significance, and all analyses were based on ences between groups (Table 1).
an intention-to-treat. All patients had the allocated closure. In 8 (53%)

810 Hamar et al Ultrasonography of Uterine Scar After Cesarean OBSTETRICS & GYNECOLOGY
Table 1. Demographic and Clinical Characteristics of Women (at Enrollment)
One-Layer Two-Layer
Closure (nⴝ15) Closure (nⴝ15) P
Age (y)* 30⫾7 25⫾7 .02
Gravidity† 2 (1–3) 1 (1–3) .63
Parity† 0 (0–1) 0 (0–1) .32
Nulliparity‡ 11 (73) 8 (53) .26
Gestational age (wk)* 39.3⫾0.5 38.6⫾0.9 .12
Contraindication to vaginal delivery‡ 10 (67) 8 (53) .46
Labor at time of delivery‡ 5 (33) 8 (53) .27
* Data presented as mean⫾standard deviation and analyzed with Student t test.

Data presented as median (interquartile range) and analyzed with Mann-Whitney U Test.

Data presented as n (%) and analyzed with ␹2 and Fisher exact tests where appropriate.

of the one-layer closure cases, the surgeon deemed it pared with two-layer: 14.1 [11.4 –16.8] mm, P⫽.61). For
necessary to use additional hemostatic sutures com- both closure techniques, there was an initial 5- to 6-fold
pared with 4 (27%) of the two-layer closure group increase in scar thickness at 48 hours postpartum
(P⫽.14). There were no significant differences seen in (P⬍.001) compared with the preoperative myometrial
estimated blood loss, hematocrit change, operative thickness. This initial increase was followed by a gradual
time, or other intraoperative data (Table 2). There reduction in thickness of the scar site. However, we
were no intraoperative complications in either group. found that, even at 6 weeks post partum, the uterine wall
In all, 90% of follow-up visits were kept and the at the site of the scar was significantly thicker than before
uterine scar was visualized in 99% of the visits (repre- surgery, irrespective of the closure technique.
sentative image in Figure 3). Repeated measures analy-
sis of variance, showed significant variation across time DISCUSSION
points compared with either lower segment thickness at Our results demonstrate that, in the immediate post-
baseline (P⬍.001) or with scar thickness at 48 hours operative period, it is possible to follow the progres-
postoperatively (P⬍.001), but that this variation did not sion of scar morphology by ultrasonography. In
depend on closure type (P⫽.79 for all visits and P⫽.81 women who have primary cesarean delivery, there is
beginning with 48 hour postoperative time point) (Fig. an immediate increase in the thickness of the
4). Within each measurement set, the thickness of the uterine scar compared with the preoperative myo-
lower segment and scar showed no differences between metrial thickness, and then a gradual decrease as
groups at baseline (median [95% CI], one-layer: 4.9 the scar is remodeled. These changes in the scar
[3.9 – 6.0] mm compared with two-layer: 4.9 [4.5–5.4] thickness are independent of the method of closure
mm, P⫽.97), at 48 hours (one-layer: 25.4 [21.2–29.7] (one- compared with two-layer) and confirm our
mm compared with two-layer: 30.3 [27.5–33.0] mm, original hypothesis.
P⫽.09), at 2 weeks (one-layer: 17.1 [15.3–19.0] mm Prior efforts with ultrasound evaluation of the
compared with two-layer: 16.6 [14.8 –18.4] mm, P⫽.75), uterine scar have focused on antepartum assessment,
or at 6 weeks (one-layer: 13.0 [10.8 –15.3] mm com- and less on postpartum evaluation of the hysterotomy

Table 2. Operative Characteristics and Birth Outcomes


One-Layer Two-Layer
Closure (nⴝ15) Closure (nⴝ15) P
Clinical chorioamnionitis* 3 (20) 6 (40) .43
Additional sutures necessary* 8 (53) 4 (27) .14
Estimated blood loss (mL)† 616⫾130 613⫾154 .95
Change in hematocrit over 24 h (%)† 5.3⫾2.6 5.5⫾2.4 .92
Time in operating room (min)† 55⫾15 58⫾12 .56
Birth weight (g)† 3,352⫾753 3,442⫾430 .70
Male infant* 9 (60) 6 (40) .27
Breastfed infant* 8 (53) 6 (40) .46
Measurement by transabdominal approach* 45 (83) 45 (85) .82
* Data presented as n (%) and analyzed with ␹2 and Fisher exact tests where appropriate.

Data presented as mean⫾standard deviation and analyzed with Student t test.

VOL. 110, NO. 4, OCTOBER 2007 Hamar et al Ultrasonography of Uterine Scar After Cesarean 811
ean delivery.22 Other investigators have found that
antepartum uterine scar thickness inversely corre-
lates with risk of intrapartum rupture,16 and that
antepartum assessment can predict term intrapar-
tum uterine rupture with a high degree of accura-
cy.18 The technique of antepartum evaluation of the
myometrium20 and postpartum evaluation of the
uterine scar14,19 have been described. Our study was
designed to determine if uterine closure technique
has an effect on subsequent measurement of the
uterine scar by ultrasonography.
Initial reports with one- compared with two-layer
closures focused on intraoperative and immediate
postoperative outcomes and found them to be equiv-
alent.9 A follow-up study found equivalent outcomes
in the subset of women who had a subsequent preg-
Fig. 3. Ultrasound follow-up of the uterine scar at 6 weeks nancy and a trial of labor.12 Durnwald and Mercer10
cesarean delivery by transabdominal approach. B, bladder; performed a retrospective analysis of women with a
U, uterus. The scar is between the two arrows. prior primary cesarean delivery. No difference was
Hamar. Ultrasonography of the Uterine Scar After Cesarean.
Obstet Gynecol 2007.
found in rates of uterine rupture although there was
an increase in “uterine windows” at cesarean delivery
in women with a prior one-layer closure. Bujold et al13
performed a chart review of women undergoing a
trial of labor at their institution with a history of a
prior cesarean delivery. A significant increase in the
odds ratio for uterine rupture was seen in women with
a prior single-layer closure. These studies provide
important information but nonetheless are limited by
their retrospective design and unknown confounders
affecting the decisions for initial closure and subse-
quent trials of labor,10,12,13 the interpregnancy interval
on healing, and recent changes in practice patterns.13
Additionally, confounders such as operator technique
and other intraoperative factors could not be taken
into account. In contrast, we randomized allocation to
scar closure and evaluated the effect postoperatively.
Confounding variables were thus minimized by
randomization.
In the context of prior studies and our current
understanding of the relationship between scar thick-
ness and wound strength, our data suggest that it may
Fig. 4. Graph of mean uterine (baseline) and scar (48 hours, not matter which closure type is used at the time of
2 weeks, and 6 weeks) thickness by closure type. Data closure of a low-transverse uterine incision after ce-
presented as mean (mm) with 95% confidence intervals sarean delivery. Further work is needed to determine
(CI).
if our findings of equivalent scar thickness persist and
Hamar. Ultrasonography of the Uterine Scar After Cesarean.
Obstet Gynecol 2007. whether the postoperative scar thickness is predictive
of future uterine disruption.
Post hoc sample size calculations were performed
incision repair stratified by closure technique. For to determine the number of patients needed to
example, investigators have elucidated the natural achieve statistical significance for the differences we
history of scar thickness in women with a prior uterine observed in our trial. We used the same parameters
scar21 and found a correlation between ultrasono- used in the sample size calculation for this study
graphic and clinically determined thickness at cesar- (power⫽80%, ␣⫽0.05). Total sample sizes (both one-

812 Hamar et al Ultrasonography of Uterine Scar After Cesarean OBSTETRICS & GYNECOLOGY
and two-layer groups) varied from 1,696 patients for 7. Flamm BL, Lim OW, Jones C, Fallon D, Newman LA, Mantis
JK. Vaginal birth after cesarean section: results of a multicenter
the 2-week measurements to 9,522 patients for the
study. Am J Obstet Gynecol 1988;158:1079–84.
48-hour measurements.
8. Halperin ME, Moore DC, Hannah WJ. Classical versus low-
Although our sample size was small, significant segment transverse incision for preterm caesarean section:
results were obtained regarding the thickness of the maternal complications and outcome of subsequent pregnan-
scar over the study interval. No significant differences cies. Br J Obstet Gynaecol 1988;95:990–6.
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closure: one versus two layers. Am J Obstet Gynecol 1992;167
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need to be obtained to show significant differences 10. Durnwald C, Mercer B. Uterine rupture, perioperative and
between closure types. It is unclear how long the perinatal morbidity after single-layer and double-layer closure
uterus takes to complete its remodeling, and it is at cesarean delivery. Am J Obstet Gynecol 2003;189:925–9.
possible that significant differences between closure 11. Tucker JM, Hauth JC, Hodgkins P, Owen J, Winkler CL. Trial
of labor after a one- or two-layer closure of a low transverse
types could appear at longer time intervals. A prior uterine incision. Am J Obstet Gynecol 1993;168:545–6.
study using magnetic resonance imaging suggests that 12. Chapman SJ, Owen J, Hauth JC. One- versus two-layer closure
the remodeling may not be complete up to 6 months of a low transverse cesarean: the next pregnancy. Obstet
after surgery.24 In our study, the closure groups ap- Gynecol 1997;89:16–8.
peared to follow the same path in the change in 13. Bujold E, Bujold C, Hamilton EF, Harel F, Gauthier RJ. The
thickness over the follow-up interval, and it is unlikely impact of a single-layer or double-layer closure on uterine
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that differences would appear between closure types
14. Sambaziotis H, Conway C, Figueroa R, Elimian A, Garry D.
at a later time point. Additional studies focused on the Second-trimester sonographic comparison of the lower uterine
correlation between closure technique, scar thickness, segment in pregnant women with and without a previous
the interpregnancy interval, and future long-term cesarean delivery. J Ultrasound Med 23:907–11, 2004; quiz
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