Expert Reviews

ajog.org

OBSTETRICS

Adhesion prevention after cesarean delivery: evidence, and

lack of it
Asnat Walfisch, MD; Ron Beloosesky, MD; Alon Shrim, MD; Mordechai Hallak, MD

In spite of the recognized occurrence of cesarean-attributable adhesions, its clinical

significance is uncertain. The presence of adhesions during a repeat cesarean section
can make fetal extraction lengthy and the procedure challenging and may increase the
risk of injury to adjacent organs. Two methods for adhesion prevention are discussed,
peritoneal closure and use of adhesion barriers. Peritoneal closure appears to be safe in
the short term. In the long term, conflicting evidence arise from reviewing the literature
for possible adhesion reduction benefits. A systematic review of the literature on the use
of adhesion barriers in the context of cesarean section yielded only a few studies, most of
which are lacking in methodology. For now, it appears that the available evidence does
not support the routine use of adhesion barriers during cesarean delivery.
Key words: adhesion barriers, pelvic adhesions, peritoneal closure, repeat cesarean
section

esarean delivery is the most common surgical procedure for

women in the United States with more
than 1.3 million cesarean surgeries performed every year. When the US national
rate of cesarean delivery was rst
measured in 1965, it was as low as 4.5%.1
Much has changed since then,2-5 and
among 19 industrialized countries that
provided data to the Organization for
Economic Cooperation and Development in 2011, cesarean rates ranged
from a low of 15% for Iceland to a
high of 38% for Italy.5 Of the 1.3 million
cesarean surgeries performed every year
in the United States, approximately one
third are repeat operations because more

From the Department of Obstetrics and

Gynecology, Hillel Yaffe Medical Center, Hadera,
Israel (all authors), and The Bruce and Ruth
Rappaport Faculty of Medicine, Technion, Israel
Institute of Technology, Haifa, Israel (all authors).
Received May 15, 2014; accepted May 20,
2014.
This study was not funded.
The authors report no conict of interests.
Reprints not available from the authors.
0002-9378/$36.00
2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.ajog.2014.05.027

than 90% of the women who undergo

1 cesarean delivery (CD) have a repeat
procedure in subsequent pregnancies.6

Adhesion formation
Adhesions are abnormal brous connections between 2 anatomically different
surfaces, as a part of a disordered healing
process.7 Postoperative adhesions are a
natural consequence of surgical tissue
trauma and healing and develop, transiently or permanently, each time the
abdomen is entered. Normal peritoneal
healing lasts 5-8 days on average and involves a combination of brosis, brinolysis, and mesothelial regeneration.8,9
It is the suppression of the normal
brinolysis process that leads to a
cascade resulting in adhesion formation
(Figure 1). Although the likelihood of
adhesion formation in an individual
patient is hard to estimate, the peritoneal inammatory status seems to be a
crucial factor in determining the duration and extent of the imbalance between brin formation and lysis. Factors
that appear to inuence the rate of
adhesion formation include infection,
tissue ischemia, degree of tissue devascularization and manipulation, and
surgical technique.

446 American Journal of Obstetrics & Gynecology NOVEMBER 2014

Rates and impact of adhesions after

cesarean delivery
As expected, the more often the
abdomen is entered, the more extensive
and dense adhesions may be encountered. The reported prevalence of adhesions is 12-46% of women at their
second cesarean and 26-75% of women
during their third cesarean.10-14 The
signicant variation in reported rates
of postcesarean adhesions is probably
related to the different adhesion-grading
systems used in different institutions.
Recently Tulandi and Lyell15 proposed a
standardized classication system for
adhesion location, extent, and consistency
following CD. The authors suggest a
point system, with the scores from
multiple sites being additive. The use of
this classication system may assist
mainly in the future research of the
possible benets attributed to the different adhesion prevention methods.
Although signicant variation exists in
reported adhesion rates following cesarean section, these rates appear to be lower
than those reported following gynecological laparotomies.16 Some authors
believe this may be due to anatomical
considerations as well as the unique nature of cesarean section.16,17 In a routine
cesarean section, the bowel is usually
not directly handled and the operative
eld focuses on the anterior aspect of
the gravid uterus. This is in contrast to
gynecological surgery, in which the
ovaries, fallopian tubes, pouch of Douglas, and bowel (all often involved in
adhesion-related disease) are commonly
encountered.
In addition, amniotic uid is rich in
factors that augment brinolysis, and
spillage of the uid into the abdominal
cavity may assist in brin clearance.16,17
Usually, 2 anatomical areas are of
concern in adhesion formation following CD: between the uterine incision
and the bladder ap and between the

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parietal peritoneum and surrounding
structures (uterine incision/bladder ap/
abdominal wall). Most authors agree
that adhesions involving the bladder,
which potentially carry a higher morbidity, are less frequent (7-35% of repeat
CS cases) than those involving the abdominal wall (27-77% of repeat CS
cases).10,13,18
In spite of the recognized association,
the clinical signicance of cesarean
attributable adhesions is uncertain for
both mother and child. Focusing on
immediate consequences, the presence
of dense adhesions can make the surgical
procedure and fetal extraction more
time consuming and challenging and
may increase the risk of bowel or bladder
injury and excessive blood loss.12,13,19-21
In one study, the reported delay in fetal
extraction was 5.6 minutes with 1 previous CD and 18.1 minutes with 3 previous CDs.13 The time to infant delivery
and risk of surgical complexity during
repeat CD are of critical concern,
particularly in emergency cases.
In the long term, postoperative adhesions may be a cause of small bowel
obstruction. However, specically following CD, rates appear to be small. The
reported rate of bowel obstruction
following 1 CD is 0.5 per 1000 and 9 per
1000 after 3 CDs.22-24 In a large Swedish
nested case-control study, with more
than 900,000 women investigated, the
odds ratio for bowel obstruction following cesarean delivery (compared with
vaginal delivery) was a modest 2.0 and
the number of cases of CD needed to
cause one case of adhesions or intestinal
obstruction (number needed to harm)
was as high as 360.22
Pelvic adhesions may also distort tubal
anatomy and lead to infertility. Nevertheless, there is no strong evidence supporting a causal relationship between a
cesarean delivery in the rst pregnancy
and subsequent subfertility.25

Methods for adhesion prevention or

reduction
Data related to short- and long-term
morbidities with post-CD adhesions
are emerging. These are concerning in
light of the growing CD rates worldwide.
Accordingly, obstetrical practices are

Obstetrics
increasingly considering adhesion reduction strategies. In part, strategies focus
on efforts to reduce the rates of primary
CD.26 In parallel, the availability of
different adhesion prevention strategies
has also built support for a more proactive strategy to reduce the risk in patients
undergoing repeat CDs. Some data exist
on different surgical techniques and the
potential benet of future adhesion
reduction, including bladder ap formation, single- vs double-layer closure of the
uterine scar, and evaluation of the Misgav
Ladach technique.27-30 In this review, we
address the 2 most commonly studied
interventions in this context: peritoneal
closure and adhesion barriers.

Peritoneal closure
Historically, both visceral (uterovesical
fold) and parietal peritoneum were surgically closed during CD. This strategy
was gradually abandoned because studies
have shown that peritoneal nonclosure
results in some short-term benets such
as shorter operative time, reduced analgesic requirements, and reduced hospitalization length.31-36
Two large and well-designed randomized controlled trials were published
in the last 4 years evaluating different
aspects of the surgical techniques used
in CDs. In the Caesarean section surgical techniques: a randomized factorial
trial,37 3033 women undergoing CD
were randomly assigned to alternative
surgical techniques including closure vs
nonclosure of the pelvic peritoneum.
There were no differences in any of the
short-term outcomes evaluated and no
signicant adverse effects of any of the
alternative techniques used in the trial.
In the second and even larger
Caesarean section surgical techniques
(CORONIS): a fractional, factorial, unmasked, randomised controlled trial,38
closure vs nonclosure of the peritoneum
(pelvic and parietal) was assessed among
other surgical aspects of CD. Here almost
16,000 women underwent randomization and, again, there were no statistically
signicant differences within any of the
intervention pairs for the different shortterm outcomes.
The inevitable conclusion from these
strong data is that short-term morbidity

Expert Reviews

should not serve as a factor in the decision of whether to close the peritoneum.
Thus, the focus should shift to the
question of potential long-term benets
of this technique and particularly their
adhesion reduction potential. On the
one hand, peritoneal closure may potentially enhance adhesion formation by
causing tissue damage and necrosis as
well as foreign body reaction to the
suture material. On the other hand,
leaving the peritoneal cavity open may
result in the adherence of the large uterus
to the anterior abdominal wall.
In addition, women after cesarean
section are encouraged to early mobilization; thus, the left-open peritoneum
can no longer isolate omentum and
bowel from the healing uterus, fascia,
and rectus abdominis. Two relatively
recent, systematic reviews evaluated the
association between peritoneal closure
and adhesion formation in subsequent
pregnancies.39,40 One reviewed randomized controlled trials (RCTs) and
the second, retrospective studies. Both
concluded that nonclosure of the peritoneum during cesarean section is associated with more adhesion formation.
However, all the authors agreed that
more RCTs of higher quality and larger
size were needed for more robust
conclusions.
Subsequent to these meta-analyses, a
large, well-designed trial randomly
assigned 533 women during their primary cesarean to peritoneal nonclosure
or closure. The authors found no signicant difference between the groups
in the proportion of patients with adhesions at any site and in time from
incision to delivery during a repeat CD
(n 97 repeat CDs).41 This clinical trial
had multiple methodological strengths
including its primary objective being to
examine adhesion formation in a repeat
CD, use of an adhesion scoring system,
exclusion of patients who had had prior
pelvic or abdominal surgery, use of a
standard technique for performing the
CD, and blinding of the surgeon performing the repeat cesarean to patient
allocation. Its main weakness lies in the
sample size of repeat CDs. The authors
admit the study was powered to identify
a large difference (50%) in adhesion rate

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447

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FIGURE 1

Pathogenesis of postoperative adhesion formation

Walsch. Adhesion prevention post CD. Am J Obstet Gynecol 2014.

and could not exclude smaller, yet possibly clinically meaningful, differences.
To summarize this part, peritoneal
closure is a safe surgical technique, which
probably carries no signicant shortterm hazards for the mother, based on
large and well-designed RCTs. As for longterm benets and reduction in adhesion formation, conicting results arise
from reviewing the literature. However,
this conict may resolve once the large
Caesarean Section Surgical Techniques: A
Randomized Factorial Trial andCaesarean
section surgical techniques (CORONIS):
a fractional, factorial, unmasked, randomised controlled trials42 publish their
long-term results, in due time.

Adhesion barriers
The risk of adhesion formation following CD may further be lowered
through the use of certain commercial

products. Some of these antiadhesives

provide a barrier between raw surfaces,
which mechanically prevent adhesion
formation while reperitonealization and
healing take place. The product is then
reabsorbed within a few days. An ideal
adhesion barrier should provide effective
tissue separation, have a long half-life
(more than critical 5-8 days of peritoneal healing), be absorbed with a minimal inammatory response, and remain
active in the presence of blood. All this
should occur without compromising
wound healing and promoting bacterial
growth.
Several synthetic agents of differing
chemical composition exist. Examples of
such commercially available barriers,
which are used by some in the context of
CD, include Gynecare Interceed (TC7oxidized regenerated cellulose; Ethicon,
Blue Ash, OH) and Sepralm (sodium

448 American Journal of Obstetrics & Gynecology NOVEMBER 2014

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hyaluronate and carboxymethylcellulose
lm; Sano-Aventis, Bridgewater, NJ).
Both are approved by the Food and Durg
Administration in the United States.
A Cochrane review published in
2008,43 entitled Barrier agents for adhesion prevention after gynaecological
surgery, concluded that some absorbable
adhesion barriers reduce the incidence
of adhesion formation following laparoscopy and laparotomy. However, no
conclusion was drawn regarding CDs
in particular because there were no
published RCTs. To identify all available
data related to the efcacy of the use of
adhesion barriers during CD, we have
conducted a systematic search of the
literature. The search was conducted
based on a prospectively prepared protocol, using the Preferred Reporting
Items for Systematic reviews and MetaAnalyses guidelines.44

Literature search
Searches were conducted in the following
databases (all from inception to May
2014): MEDLINE(R) using the OvidSP
interface and PUBMED, Web of Science
(CORE and ALL DATABASES), SCOPUS
and its Secondary Documents, The
Cochrane Central Register of Controlled
Trials (CENTRAL), Cochrane Database
of Systematic Reviews, and relevant conference proceedings, hand searched. The
reference lists of all the related systematic
reviews and guidelines as well as included
studies were searched for possible additional studies.
A search strategy was developed
based on the MEDLINE database
subject headings and the used for synonyms listed in the scope notes for the
terms, cesarean section, adhesions, barriers, Interceed, oxidized regenerated
cellulose, Sepralm (Sano-Aventis),
carboxymethylcellulose lm, Gore-tex
(W. L. Gore and Associates, Newark,
DE), and brin sheet in different combinations. No language restrictions were
applied. Studies were included if they
were RCTs, nonrandomized controlled
clinical trials, prospective and retrospective cohort studies, and case-control
studies. Animal studies, case reports and
case series, reviews, and editorials were
not included. Abstracts of studies were

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excluded if the full article was not
published.
Types of participants in included
studies had to be women in which any
kind of an adhesion barrier had been
used during a cesarean delivery and who
underwent at least 1 additional cesarean
delivery in which any assessment (direct
or indirect) of intraabdominal or pelvic
adhesions had been performed. The
outcome measures were the assessment
of the presence and severity of intraabdominal and pelvic adhesions during a
repeat cesarean delivery or their consequences. Titles and abstracts were
reviewed for possible exclusion by 1
reviewer (A.W.). The full-text articles
were reviewed by all 4 authors for suitability for inclusion.

Study quality grading

Quality assessment of individual
studies was performed using the 3
category summary grading system (A,
B, or C) suggested by Ip et al.45 Their
system denes a generic grading system that is applicable to any type of
study design including randomized
controlled trials, cohort, and casecontrol studies as mentioned in the
following text.
A (good)
This includes a study that adheres
mostly to the commonly held concepts of high quality including the
following: a clear description of the
population, setting, interventions, and
comparison groups; a clear description
of the comparison groups; an appropriate measurement of outcomes; appropriate statistical and analytical
methods and reporting; no reporting
errors; less than 20% dropout; clear
reporting of dropouts; and appropriate
consideration and adjustment for potential confounders.
B (fair/moderate)
These studies do not meet all the criteria
in category A because they have some
deciencies but none of which are likely
to cause major biases. The study may
have suboptimal adjustment for potential confounders. The study may also
be missing information, making it

Expert Reviews

FIGURE 2

Search flow
163 publicaons idened
using the search terms,
bibliographies, abstracts and
proceedings

150 excluded aer screening tles and/or abstracts

13 retrieved for a detailed evaluaon

7 from electronic search
4 from reference lists
2 from conference proceedings

6 excluded aer a detailed evaluaon

4 abstracts (full study not published) excluded

3 publicaons idened:
0 RCTs
3 prospecve/retrospecve cohorts
RCTs, randomized controlled trials.
Walsch. Adhesion prevention post CD. Am J Obstet Gynecol 2014.

difcult to assess limitations and potential problems.

C (poor)
Category C studies either did not
consider potential confounders or did
not adjust for them appropriately. These
studies may have serious shortcomings
in design, analysis, or reporting; or have
large amounts of missing information or
discrepancies in reporting.
Data extraction
Extracted data were compiled in an evidence table. The table includes a
description of the studies that addressed
the key question according to the inclusion/exclusion criteria. The table provides information about study design,

target population and sample size,

description of the adhesion barrier used,
method used for assessment of adhesions, summary of the results, and study
quality grading according to the scale
described above.45

Results and comment for the

systematic literature search
The search ow is described in Figure 2.
Following exclusion of studies published
as abstracts only, we were able to identify
3 studies46-48 with a total of 328 women
in the intervention group and 353 in the
control group. In general, it appears that
data related to the use of adhesion barriers during CDs are scarce and methodologically lacking (Table). Two of the
3 studies identied had small sample

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449

As a surrogate for adhesion

grading, the primary outcome was
time from skin incision to neonate
delivery. Also assessed total
operative time and rates of
selected complications.

No significant difference in
any of the assessed outcomes

ajog.org

450 American Journal of Obstetrics & Gynecology NOVEMBER 2014

Walsch. Adhesion prevention post CD. Am J Obstet Gynecol 2014.

CD, caesarean delivery.

Interceed; Ethicon, Blue Ash, OH. Seprafilm; Sanofi-Aventis, Bridgewater, NJ.

Seprafilm
248/269
2014
Edwards et al48

Retrospective
cohort

B
Significantly fewer adhesions
in barrier group (26% vs 78%,
P .01)
Locally developed: grade 0
(no adhesions) up to grade 3
(severe adhesions)
Interceed
53/59
Retrospective
cohort
2011
Chapa et al47

Obstetrics

Significantly fewer adhesions

in barrier group (7.4% vs 48%,
P .001)
Not specified
Seprafilm
27/25
Prospective
cohort
Fushiki et al

Reference

46

2005

Study type

Number of participants
evaluated during repeat
CD (intervention/control)
Year of
publication

Data related to the use of adhesion barriers during CDs

TABLE

Type of
intervention

Method used for adhesion

assessment

Results

Quality grading

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sizes and none were randomized. Two of

the studies,46,47 with smaller sample
sizes, showed reduced adhesion rates in
the intervention group, and 1 study, with
a signicantly larger sample size, showed
no difference between the groups.48
In all 3 studies, no clear indications
were described as to the considerations
used for placing the adhesion barrier in
some patients but not in others during
the primary CD, and the decision was
usually per the discretion of the managing physician.48
The largest study to date, published by
Edwards et al,48 is a retrospective cohort
study with patients assessed during a
repeat CD. Because this was a retrospective study, the authors chose the time
from skin incision to the neonate delivery
at repeat cesarean delivery as their primary outcome and as a surrogate for the
presence and severity of adhesions. The
authors also assessed total operative time
and rates of surgical complications. Data
on the presence of adhesions were available in about 70% of the study population. There were 248 women in the
intervention group and 269 controls. No
differences were found between groups
in both incision to delivery interval (6.1
minutes vs 5.8 minutes, P .25) and total
operative time (31.2 minutes vs 31.8
minutes, P .56). Surgical complications
and the presence of adhesions did not
differ as well. The authors were . unable to demonstrate any advantage to
placement of the carboxymethylcellulose
adhesion barrier at the time of primary
cesarean delivery.48
The second largest study published to
date by Chapa et al47 is a retrospective
cohort with 112 patients assessed during
a repeat CD. In this cohort, with barrier
used during the primary CD (Interceed),
patients had an adhesion rate of 26%
(14 of 53) vs 78% (46 of 59) in the
nonbarrier group (P .011). Patients in
the nonbarrier group had a longer incision to delivery interval, with a mean of
an additional 5 minutes, and were more
likely to suffer from excessive blood loss.
The study suffers from multiple methodological aws including, primarily, its
retrospective design with the inherent
selection bias as well as a relatively small
sample size.

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The third study, by Fushiki et al,46
suffers from multiple limitations including small sample size, lack of randomization, and lack of blinding to
group assignment. Additionally, the study
design allowed for the possibility that the
27 women in the Sepralm group represent a biased sample of the total number
of women who had an adhesion barrier
placed.
Except for 1 RCT identied in the
search as an abstract only (and thus
excluded), no RCTs are likely to be
published soon because the currently
registered trials on clinicaltrials.gov have
not yet begun enrolling patients or have
terminated enrollment before reaching
the target sample size.49-51 For now, it
appears that the available evidence does
not support routine use of adhesion
barriers during CD.

Cost-effectiveness
No study has addressed the issue of costeffectiveness of adhesion barrier use in
the context of CD. One study evaluated
the cost-effectiveness of an antiadhesive
in patients undergoing radical hysterectomy and pelvic lymphadenectomy, a
clearly more morbid surgery than CD.52
The authors calculated the antiadhesive
to be cost effective only when the incidence of small bowel obstruction
following surgery was at least 2.4%, a
much higher incidence than the reported incidence of 0.5-9 bowel obstructions per 1000 CDs. Additionally,
it appears that 2000 women would need
to have an adhesion barrier placed
during their cesarean to avoid 1 bowel
obstruction.53
Of note is the fact that the most feared
and serious maternal complications
associated with repeat CD is not pelvic
adhesions but, rather, placenta accreta,
which is probably unrelated to pelvic
adhesions. Thus, neither peritoneal
closure nor the use of adhesion barriers
is likely to have any effect on the occurrence of placenta accreta.
Conclusion
The issues of repeat CD and its associated
risks for both mother and child continue
to burden the clinicians and are likely to
increase in light of the ever-increasing

CD rates. In an effort to reduce occurrence of pelvic adhesions encountered

during repeat CDs, 2 main strategies are
currently available, both lacking in supporting evidence. Peritoneal closure is
supported by a strong evidence of its
short-term safety. However, only inadequate and conicting evidence of its longterm efcacy in adhesion prevention is
currently available. The routine use of
adhesion barriers during CD is costly and
is not supported by high-quality research.
The need for well-designed randomized
controlled trials, directly addressing this
issue, persists.
It seems that none of the currently
available methods for adhesion prevention can replace good surgical technique
with meticulous hemostasis, gentle tissue handling, adequate irrigation, and
careful use of energy sources. Women
considering CD need to be informed of
the risks and implications of future pelvic adhesions and increased morbidity
with higher-order cesarean deliveries. ACKNOWLEDGMENT
We are grateful to Ms Margie Serling Cohn, head
librarian at the Alfred Goldschmidt Medical Sciences Library of the Technion Institute of Technology, for the systematic literature search.

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