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DOI: 10.1111/j.1471-0528.2010.02808.

x
Systematic review
www.bjog.org

Adhesion formation after previous caesarean


sectiona meta-analysis and systematic review
Z Shi,a,b* L Ma,b,c* Y Yang,b* H Wang,d A Schreiber,c X Li,b S Tai,d X Zhao,e J Teng,e L Zhang,e
W Lu,e Y An,e NR Alla,f T Cuig
a
Department of Chemistry, Temple University, Philadelphia, PA, USA b Department of Obstetrics and Gynaecology, Third Affiliated Hospital
of Sun Yat-sen University, Guangzhou, China c Health Science Center, Temple University, Philadelphia, PA, USA d Department of General
Surgery, Second Clinical College, Harbin Medical University, Harbin, China e Heilongjiang Academy of Traditional Chinese Medicine, Harbin,
China f Wistar Research Institute, University of Pennsylvania, Philadelphia, PA, USA g Childrens Hospital Boston, Boston, MA, USA
Correspondence: Dr Z Shi, Department of Chemistry, Temple University, 130 Beury Hall, 1901 N. 13th Street, Philadelphia, PA 19122, USA.
Email tua64317@temple.edu

Accepted 19 October 2010. Published Online 23 December 2010.

Background The optimal technique for performing caesarean Main results Thirty-three qualified studies including 4423 women
section with respect to minimising postoperative adhesions has were analysed. There were 406 adhesions among 571 women and
not been determined. 238 adhesions among 596 women in the Starks caesarean
section (also known as MisgavLadach method) group and
Objectives To evaluate adhesion formation for three common
modified Starks caesarean section group, respectively, with
caesarean section techniques in women undergoing repeat
pooled OR 4.69 (95% CI 3.326.62; P < 0.01, 12 studies); 1173
caesarean section surgeries.
adhesions among 1555 women and 1179 adhesions among 1625
Search strategy A database was constructed from Medline, women in Starks caesarean section group and classic lower-
EMBASE, Cochrane Library, National Science Digital Library, segment caesarean section group, respectively, with pooled odds
China Biological Medicine Database and through contact with ratio 1.28 (95% CI 0.971.68; P = 0.08, 21 studies); and 29
experts in this field from January 1990 to May 2010. adhesions from 102 women and 115 adhesions from 193 women
in modified Starks caesarean section group and classic lower-
Selection criteria Studies were included if they examined adhesion
segment caesarean section group, respectively, with pooled odds
formation in repeat caesarean sections as a primary objective,
ratio 0.28 (95% CI 0.100.82; P = 0.02, two studies).
delineated a clear study design, specified an adhesion scoring
system, and had sufficient patient exclusion criteria. Authors conclusions Closure of the peritoneum in modified
Starks caesarean section resulted in less adhesion formation and
Data collection and analysis We abstracted data regarding
should be recommended.
adhesion formation. The MantelHaenszel random-effects model
was employed for all analyses using odds ratio or inverse variance, Keywords Adhesion, caesarean section, postoperative.
along with 95% CI.

Please cite this paper as: Shi Z, Ma L, Yang Y, Wang H, Schreiber A, Li X, Tai S, Zhao X, Teng J, Zhang L, Lu W, An Y, Alla N, Cui T. Adhesion formation
after previous caesarean sectiona meta-analysis and systematic review. BJOG 2011;118:410422.

been debated by both caesarean section proponents and


Introduction
critics for several reasons.2,3 Many investigators and practi-
Caesarean section surgery has become one of the most tioners have argued that non-closure of the peritoneum has
common obstetric operations worldwide, accounting for more advantages and should be recommended,3 although it
over 27% of total deliveries over 2004/05 and 2007/08.1 does not restore the integrity of the abdominal anatomy.
The basic procedure has been modified over the years and Referring to data from large pools of women in rando-
improved through its extensive practice. However, issues mised control trials (RCTs), these advocates for non-clo-
such as closure or non-closure of the peritoneum have sure assert that it offers benefits both during surgery and
for short-term postoperative outcomes, such as operation
*These authors contributed equally to this paper. time, blood loss, analgesia requirement, febrile morbidity,

410 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology
Caesarean section techniques: under the cross-fire

return of bowel function, length of hospital stay and infec- section, with other abdominal or pelvic surgeries besides
tion. the previous caesarean section, with occurrences of post-
Nevertheless, because of the limited number of women operative fever or abdominal or pelvic infectious diseases,
in a small number of RCTs concerning long-term out- whose surgeries involved anti-adhesives, or whose previous
comes after caesarean section, it is difficult to draw sound caesarean section procedures were performed in hospitals
conclusions about whether or not to close the peritoneum. other than the hospitals where their repeat caesarean
Long-term issuessuch as abdominal adhesion formation sections were performed. We extracted data about study
found during repeat operations, chronic pelvic pain, and design and methods, patient inclusion and exclusion crite-
secondary infertility as the result of abdominal adhesions ria, clinical characteristics, procedure of previous caesarean
after previous caesarean section4have serious conse- section, description of adhesion, interval from skin inci-
quences, all of which have significant morbidity and high sion to delivery of the newborn, blood loss and complica-
healthcare costs.5,6 tions of the repeat caesarean section. According to
This meta-analysis, based on retrospective observational severity of adhesion, adhesion formation in different oper-
studies, compares adhesion formation detected in repeat ation groups was further evaluated in subgroups. Among
caesarean section procedures according to the different the three groups, standard surgical procedures were per-
techniques used in the previous surgeries, including Starks formed in the previous caesarean section. In the Starks
caesarean section (also known as MisgavLadach method),7 caesarean section, blunt separation of tissues along natural
modified Starks caesarean section, and classic lower-seg- tissue planes with a minimum of sharp dissection was
ment caesarean section, and determines the factors that performed; the transverse lower segment uterine incision
most greatly influence adhesion formation after primary was closed with one layer of continuous suture, and nei-
caesarean section. ther visceral nor parietal peritoneum was closed. In the
modified Starks caesarean section, both peritoneal layers
were closed with a continuous suture, and the other
Methods
procedural elements were exactly the same as in Starks
The MOOSE statement8 was referred to as a guideline for caesarean section. In the classic lower-segment caesarean
conducting this analysis. We searched Medline, EMBASE, section, more manoeuvres were performed, including
Cochrane Library, National Science Digital Library pushing down of the bladder to achieve greater exposure
(NSDL) and China Biological Medicine Database (CBM- of the uterine lower segment, closing the transverse lower
disc) for relevant observational studies (all retrospective). segment uterine incision with two layers of continuous
Queries included articles published from January 1990 to suture, and closure of both peritoneal layers (Table 1).10
May 2010 in English or Chinese peer-reviewed publica- There were several scoring systems measuring severity of
tions. Keywords employed were caesarean section (or sec- abdominal cavity adhesion, including those concerning
tion) and closure (or non-closure) and adhesion. We also infertility recommended by the American Fertility Society,11
hand-searched bibliographies of original studies, reviews
(including meta-analyses) and relevant conference
abstracts, and contacted some investigators directly. The Table 1. Major differences of the three caesarean sections
date last searched was 1 July 2010. Women included were procedures

divided into three groups according to the techniques in Starks Modified Classic
their previous caesarean section: Starks caesarean section, Starks lower-segment
modified Starks caesarean section, and classic lower-seg-
ment caesarean section. Skin incision Transverse Transverse Vertical
Two authors independently selected relevant studies, Subcutaneous tissue Blunt Blunt Sharp
assessed trial quality according to the STROBE statement9 division and (by hand) (by hand) (by cutting)
and preset the criteria described in the following text, peritoneum opening
then extracted data. Questionable studies were confirmed Dissection of No No Yes*
bladder off the uterus
or rejected after discussion with a third author. Studies
Suturing of uterus One layer One layer Two layers
that compared techniques during previous caesarean sec- Peritoneum closure Neither Both Both
tion concerning abdominal and pelvic adhesion formation (parietal or visceral)
were included. Studies were also required to have a clear Rectus muscle stitched No Yes Yes
study design and an adhesion scoring scale, as well as Operation time Shortest Longer Longest
procedure descriptions for the previous caesarean section
*Bladder was pushed down from the uterus before incision on the
techniques. Studies were rejected if they included women uterus.
who had adhesions found in the previous caesarean

2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology 411
Shi et al.

those concerning adhesive bowel obstruction,12 and those 86 cases in the Starks caesarean section group and 37 cases
concerning secondary adhesion after previous caesarean in the modified Starks caesarean section group, with a
section.13 We considered all the conditions and recon- pooled OR of 3.79 (95% CI 2.346.12, 12 studies, P < 0.01
structed a convenient scoring scale for all included studies for overall effect, with minimum heterogeneity, I2 = 0%).
(Tables S1S3). Concerning the interval from skin incision to delivery of
Statistical analyses were conducted using Review the newborn, there were 107 women in the Starks caesar-
Manager version 5.0 software (Cochrane Collaboration). ean section group and 97 women in the modified Starks
Pooled odds ratio (OR) or inverse variance (IV) and 95% caesarean section group, with an IV of 5.24 (95% CI )2.60
CI were determined by choice between the MantelHaens- to 13.08, two studies, P = 0.19 for overall effect, with very
zel fixed-effects or random-effects models, whichever was high heterogeneity, I2 = 98%, time measured in minutes,
most conservative14 (showing less efficacy, with a higher Figure 2). The above results showed a clear decrease in risk
P value, and the random-effects model qualified for this of adhesion formation after modified Starks caesarean
purpose) and shown in Forrest plot. Funnel plots were section.
applied to indicate publication bias. Statistical between-
study heterogeneity was assessed by I2 test15 and chi-square Starks caesarean section versus classic lower-seg-
test. Differences between subgroups were assessed on the ment caesarean section
basis of the chi-square statistic. For all the tests performed, There were 1173 cases of adhesion formation among 1555
statistical significance was achieved if the P value was <0.05 women who had undergone previous Starks caesarean sec-
(for overall effect of intervention) or <0.10 (for heterogene- tion, compared with 1179 cases of adhesion formation
ity test).14 among 1625 women who had undergone previous classic
lower-segment caesarean section, with pooled OR 1.28
(95% CI 0.971.68, 21 studies, P = 0.08 for overall effect,
Results
with medium heterogeneity, I2 = 33%). There were 502
Thirty-three qualified studies1648 were included for quanti- cases and 742 cases of grade 1 adhesion formation in the
tative analysis (12 studies investigating adhesion formation Starks caesarean section group and classic lower-segment
after Starks caesarean section versus modified Starks cae- caesarean section group, respectively, with a pooled OR of
sarean section during previous caesarean section; 21 studies 0.57 (95% CI 0.420.77, 21 studies, P < 0.01 for overall
examining adhesion formation comparing Starks caesarean effect, with medium heterogeneity, I2 = 65%). There were
section and classic lower-segment caesarean section; and 405 cases of grade 2 adhesion in the Starks caesarean sec-
two studies analysing the same indices comparing modified tion group and 350 such cases in the classic lower-segment
Starks caesarean section and classic lower segment caesar- caesarean section group, with a pooled OR of 1.78 (95%
ean section, characteristics in Table S1, selection process CI 1.053.00, 16 studies, P = 0.03 for overall effect, with
shown in Figure 1), including 4423 women. high heterogeneity, I2 = 78%). In the grade 3 adhesion
subgroup, there were 284 adhesion cases in the Starks cae-
Starks caesarean section versus modified Starks sarean section group and 87 cases in the classic lower-
caesarean section segment caesarean section group, with a pooled OR of
There were 406 cases of adhesion formation among 571 3.62 (95% CI 2.385.50, 20 studies, P < 0.01 for overall
women who had undergone previous Starks caesarean sec- effect, with medium heterogeneity, I2 = 38%). Concerning
tion compared with 238 cases of adhesion among 596 the interval from skin incision to opening of the perito-
women who had undergone previous modified Starks cae- neum, there were 680 women in the Starks caesarean sec-
sarean section, with pooled OR 4.69 (95% CI 3.326.62, 12 tion group and 657 women in the classic lower-segment
studies, P < 0.01 for overall effect, with moderate heteroge- caesarean section group, with an IV of 4.63 (3.705.56, five
neity, I2 = 34%). In the grade 1 adhesion formation com- studies, P < 0.01 for overall effect, with medium heteroge-
parison, there were 182 adhesions in the Starks caesarean neity, I2 = 72%). Concerning the interval from skin inci-
section group and 129 adhesions in the modified Starks sion to delivery of the newborn, there were 225 women in
caesarean section group, with a pooled OR of 1.70 (95% the Starks caesarean section group and 185 women in the
CI 1.282.25, 12 studies, P < 0.01 for overall effect, with classic lower-segment caesarean section group, with an IV
minimum heterogeneity, I2 = 0%). There were 138 grade 2 of 0.82 (95% CI )4.33 to 5.97, three studies, P = 0.75 for
adhesions in the Starks caesarean section group and 72 overall effect, with very high heterogeneity, I2 = 97%).
such cases in the modified Starks caesarean section group, With respect to blood loss during repeated caesarean sec-
with a pooled OR of 2.99 (95% CI 1.565.72, nine studies, tion from skin incision to opening of the peritoneum,
P < 0.01 for overall effect, with medium heterogeneity, there were 119 women in the Starks caesarean section
I2 = 63%). In the grade 3 adhesion comparison, there were group and 135 women in the classic lower-segment

412 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology
Caesarean section techniques: under the cross-fire

Records identified through primary database searching (n = 112)

Identification
Records after duplicates were
removed* (n = 111)

Screening
Records screened
(n = 111)
Review articles excluded (n = 6)

Full-text articles excluded:


Comparing adhesion condition during
Eligibility

obstetrical and gynecological operations


Full-text assessed for
eligibility (n = 105) (n = 20);
Classic lower segment transverse CS with
different abdominal incisions (n = 4);
Without excluding multiple abdominal or
pelvic operations, pelvic infectious
diseases, postoperative fever, or adhesion
found in primary CS (n = 12);
Comparing adhesion condition between
Included

first and second CS (n = 1);


Comparing inside and outside peritoneal
Studies included in
qualitative synthesis (n = 33) CS (n = 5);
Without adhesion scoring criteria (n = 27);
Prospective studies (n = 3).

Studies included in quantitative synthesis


(meta-analysis) (n = 33, with 4423 participants)

Secondary outcomes

Primary outcomes
Analysis

Interval from skin Complications


incision to delivery of Blood loss
in repeat CS
the newborn
Adhesion formation

Figure 1. Flow chart of selection process. Primary search: studies with a primary objective to examine adhesion formation after primary caesarean
section based on different tissue division and suture techniques were identified. *One study had duplicate publications in both English and Chinese.

caesarean section group, with an IV of 19.50 (95% CI Modified Starks caesarean section versus classic
17.8621.13, three studies, P < 0.01 for overall effect, with lower-segment caesarean section
minimum heterogeneity, I2 = 0%, blood volume measured There were 29 adhesions among 102 women who underwent
in millilitres, Figure 3). No study reported surgical compli- previous modified Starks caesarean section, and 115 adhe-
cations in repeat caesarean section involving bladder injury sions among 193 women who underwent previous classic
or lateral extension of uterine incision. The above results lower-segment caesarean section, with pooled OR being 0.28
showed a similar total adhesion formation after Starks cae- (95% CI 0.100.82, two studies, P = 0.02 for overall effect,
sarean section and classic lower-segment caesarean section. with high heterogeneity, I2 = 75%). There were 20 cases and
It also showed that there were fewer grade 1 adhesions but 71 cases of grade 1 adhesion formation in the modified
more grade 2 and grade 3 adhesions after Starks caesarean Starks caesarean section group and the classic lower segment
section, which was also reflected by more blood loss. caesarean section group, respectively, with a pooled OR of

2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology 413
Shi et al.

A Total adhesion
Starks Modified Starks Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2007 57 75 13 57 10.4% 10.72 [4.75, 24.20]
Chen 2008 25 32 28 40 7.3% 1.53 [0.52, 4.49]
Hamel 2007 23 30 13 32 7.0% 4.80 [1.60, 14.45]
Hao 2005 58 75 18 51 10.8% 6.25 [2.84, 13.76]
Kang 2007 35 46 16 46 9.1% 5.97 [2.40, 14.81]
Liang 2008 34 36 70 104 4.4% 8.26 [1.87, 36.41]
Nian 2008 32 58 21 55 11.4% 1.99 [0.94, 4.22]
Tian 2006 10 15 12 40 5.7% 4.67 [1.31, 16.60]
Wang 2007' 20 35 17 54 9.5% 2.90 [1.20, 7.01]
Wang 2008 14 42 4 42 6.1% 4.75 [1.41, 15.99]
Zhang 2006 57 75 18 50 10.9% 5.63 [2.57, 12.33]
Zhang 2009 41 52 8 25 7.3% 7.92 [2.71, 23.14]

Total (95% CI) 571 596 100.0% 4.69 [3.32, 6.62]


Total events 406 238
Heterogeneity: 2 = 0.12; 2 = 16.71, df = 11 (P = 0.12); I2 = 34%
0.01 0.1 1 10 100
Test for overall effect: Z = 8.80 (P < 0.00001) Favours Starks Favours modified Stark

B Funnel plot
0 SE(log[OR])

0.2

0.4

0.6

0.8

OR
1
0.01 0.1 1 10 100

C Grade 1 adhesion
Starks Modified Starks Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2007 10 75 8 57 8.0% 0.94 [0.35, 2.56]
Chen 2008 17 32 20 40 9.3% 1.13 [0.45, 2.87]
Hamel 2007 2 30 3 32 2.3% 0.69 [0.11, 4.45]
Hao 2005 33 75 14 51 13.7% 2.08 [0.97, 4.46]
Kang 2007 20 46 12 46 10.4% 2.18 [0.90, 5.25]
Liang 2008 10 36 13 104 9.2% 2.69 [1.06, 6.84]
Nian 2008 7 58 10 55 7.3% 0.62 [0.22, 1.76]
Tian 2006 8 15 10 40 5.2% 3.43 [0.99, 11.86]
Wang 2007' 14 35 16 54 10.1% 1.58 [0.65, 3.87]
Wang 2008 6 42 3 42 3.8% 2.17 [0.50, 9.31]
Zhang 2006 32 75 14 50 13.6% 1.91 [0.89, 4.13]
Zhang 2009 23 52 6 25 7.0% 2.51 [0.86, 7.31]

Total (95% CI) 571 596 100.0% 1.70 [1.28, 2.25]


Total events 182 129
Heterogeneity: 2 = 0.00; 2 = 10.03, df = 11 (P = 0.53); I2 = 0%
0.01 0.1 1 10 100
Test for overall effect: Z = 3.65 (P = 0.0003)
Favours Starks Favours modified Stark

Figure 2. Starks caesarean section versus modified Starks caesarean section: (A) total adhesions; (B) funnel plot; (C) grade 1 adhesions; (D) grade 2
adhesions; (E) grade 3 adhesions; (F) interval from skin incision to delivery of the newborn.

414 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology
Caesarean section techniques: under the cross-fire

D Grade 2 adhesion
Starks Modified Starks Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2007 30 75 4 57 11.9% 8.83 [2.89, 26.97]
Hamel 2007 15 30 9 32 12.4% 2.56 [0.89, 7.32]
Hao 2005 20 75 4 51 11.7% 4.27 [1.36, 13.39]
Kang 2007 12 46 4 46 11.1% 3.71 [1.10, 12.53]
Liang 2008 7 36 36 104 13.4% 0.46 [0.18, 1.14]
Nian 2008 15 58 8 55 13.1% 2.05 [0.79, 5.31]
Wang 2007' 4 35 1 54 5.8% 6.84 [0.73, 63.96]
Zhang 2006 20 75 4 50 11.7% 4.18 [1.33, 13.11]
Zhang 2009 15 52 2 25 8.9% 4.66 [0.98, 22.29]

Total (95% CI) 482 474 100.0% 2.99 [1.56, 5.72]


Total events 138 72
Heterogeneity: 2 = 0.60; 2 = 21.62, df = 8 (P = 0.006); I2 = 63%
0.01 0.1 1 10 100
Test for overall effect: Z = 3.31 (P = 0.0009) Favours Starks Favours modified Stark

E Grade 3 adhesion
Starks Modified Starks Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI

Chen 2007 17 75 1 57 5.5% 16.41 [2.11, 127.49]


Chen 2008 8 32 8 40 18.5% 1.33 [0.44, 4.06]
Hamel 2007 6 30 1 32 4.8% 7.75 [0.87, 68.77]
Hao 2005 5 75 0 51 2.7% 8.04 [0.43, 148.58]
Kang 2007 3 46 0 46 2.6% 7.48 [0.38, 149.08]
Liang 2008 17 36 21 104 35.0% 3.54 [1.57, 7.96]
Nian 2008 10 58 3 55 12.7% 3.61 [0.94, 13.91]
Tian 2006 2 15 2 40 5.4% 2.92 [0.37, 22.90]
Wang 2007' 2 35 0 54 2.4% 8.13 [0.38, 174.65]
Wang 2008 8 42 1 42 5.1% 9.65 [1.15, 81.02]
Zhang 2006 5 75 0 50 2.7% 7.88 [0.43, 145.73]
Zhang 2009 3 52 0 25 2.6% 3.61 [0.18, 72.54]

Total (95% CI) 571 596 100.0% 3.79 [2.34, 6.12]


Total events 86 37
Heterogeneity: 2 = 0.00; 2 = 7.84, df = 11 (P = 0.73); I2 = 0%
0.01 0.1 1 10 100
Test for overall effect: Z = 5.44 (P < 0.00001)
Favours Starks Favours modified Stark

F Interval from skin incision to delivery of the newborn


Starks CS Modified Starks CS Mean diffrence Mean diffrence
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% CI IV, Random, 95% CI
Chen 2007 19.7 3.1 75 10.5 2.4 57 50.5% 9.20 [8.26, 10.14]
Chen 2008 11.5 3.9 32 10.3 4.2 40 49.5% 1.20 [0.68, 3.08]

Total (95% CI) 107 97 100.0% 5.24 [2.60, 13.08]


Heterogeneity: 2 = 31.43; 2 = 55.87, df = 1 (P < 0.00001); I2 = 98%
100 50 0 50 100
Test for overall effect: Z = 1.31 (P = 0.19)
Favours Starks Favours modified Stark

Figure 2. (Continued)

0.44 (95% CI 0.250.79, two studies, P < 0.01 for overall were 57 women and 87 women in the modified Starks cae-
effect, with minimum heterogeneity, I2 = 0%). There were sarean section group and the classic lower-segment caesarean
eight cases of grade 2 adhesion in the modified Starks cae- section group, respectively, indicated by one study, with an
sarean section group and 33 such cases in the classic lower- IV of 4.30 (95% CI )5.17 to )3.43, P < 0.01, Figure 4).
segment caesarean section group, with a pooled OR of 0.55 These results showed fewer total and grade 1 adhesion for-
(95% CI 0.12, 2.45, two studies, P = 0.43 for overall effect, mations after modified Starks caesarean section, which was
with medium heterogeneity, I2 = 65%). In the grade 3 adhe- also shown by shorter operation duration.
sion comparison, there was one case in the modified Starks
caesarean section group and 11 cases in the classic lower-seg-
Discussion
ment caesarean section group, with a pooled OR of 0.26
(95% CI 0.051.52, two studies, P = 0.14 for overall effect, Adhesion is one of the most important postoperative
with minimum heterogeneity, I2 = 0%). With respect to complications. Occurrence of adhesions after caesarean sec-
interval from skin incision to delivery of the newborn, there tion could increase the duration of subsequent operations,

2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology 415
Shi et al.

A Total adhesion
Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI

Chen 2002 20 30 22 30 4.5% 0.73 [0.24, 2.21]


Chen 2007 39 75 33 87 9.2% 1.77 [0.95, 3.32]
Cheng 2005 5 34 12 42 4.2% 0.43 [0.13, 1.38]
Deng 2005 20 61 24 72 7.9% 0.98 [0.47, 2.01]
Ding 2006 20 32 27 52 6.1% 1.54 [0.63, 3.79]
Hong 2006 36 45 33 40 4.6% 0.85 [0.28, 2.54]
Huang 2007 482 482 482 482 Not estimable
Li 2005$ 34 46 17 36 5.8% 3.17 [1.25, 8.01]
Lin 2006 27 79 24 73 8.6% 1.06 [0.54, 2.08]
Liu 2007 35 62 20 50 7.5% 1.94 [0.91, 4.14]
Luo 2006 60 60 52 52 Not estimable
Niu 2006 14 20 13 20 3.4% 1.26 [0.33, 4.73]
Qu 2006 94 96 139 142 2.0% 1.01 [0.17, 6.19]
Ran 2004 3 29 9 40 3.1% 0.40 [0.10, 1.62]
Song 2008$ 63 79 26 40 6.5% 2.12 [0.91, 4.96]
Wang 2005 27 79 24 73 8.6% 1.06 [0.54, 2.08]
Wang 2007$ 35 35 53 55 0.8% 3.32 [0.15, 71.18]
Xu 2006 81 120 50 68 8.8% 0.75 [0.39, 1.45]
Yang 2005 24 24 28 28 Not estimable
Yu 2005 20 31 21 39 5.5% 1.56 [0.59, 4.10]
Zheng 2007 34 36 70 104 2.8% 8.26 [1.87, 36.41]

Total (95% CI) 1555 1625 100.0% 1.28 [0.97, 1.68]


Total events 1173 1179
Heterogeneity: 2 = 0.11; 2 = 25.35, df = 17 (P = 0.09); I2 = 33%
0.02 0.1 1 10 50
Test for overall effect: Z = 1.76 (P = 0.08)
Favours Starks Favours lower segment

B Funnel plot
0 SE(log[OR])

0.5

1.5

OR
2
0.01 0.1 1 10 100
Figure 3. Starks caesarean section versus classic lower-segment caesarean section: (A) total adhesions; (B) funnel plot; (C) grade 1 adhesions; (D)
grade 2 adhesions; (E) grade 3 adhesions; (F) interval from skin incision to delivery of the newborn; (G) interval from skin incision to delivery of the
newborn; (H) blood loss from skin incision to opening of peritoneum.

the incidence of injury to the intestines, bladder and ureter, treatment of adhesion complications.49 Adhesions are also
and increase bleeding. In a 10-year period, 5.7% of women considered a significant causative factor in secondary
who underwent caesarean section were admitted again for female infertility.50

416 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology
Caesarean section techniques: under the cross-fire

C Grade 1 adhesion
Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI

Chen 2002 16 30 18 30 4.3% 0.76 [0.27, 2.12]


Chen 2007 10 75 24 87 5.3% 0.40 [0.18, 0.91]
Cheng 2005 4 34 2 42 2.2% 2.67 [0.46, 15.53]
Deng 2005 14 61 15 72 5.2% 1.13 [0.50, 2.58]
Ding 2006 5 32 16 52 4.0% 0.42 [0.14, 1.28]
Hong 2006 33 45 33 40 4.2% 0.58 [0.20, 1.67]
Huang 2007 134 482 254 482 8.0% 0.35 [0.26, 0.45]
Li 2005$ 10 46 12 36 4.5% 0.56 [0.21, 1.49]
Lin 2006 15 79 20 73 5.5% 0.62 [0.29, 1.33]
Liu 2007 28 62 20 50 5.6% 1.24 [0.58, 2.63]
Luo 2006 15 60 30 52 5.3% 0.24 [0.11, 0.55]
Niu 2006 3 20 8 20 2.7% 0.26 [0.06, 1.21]
Qu 2006 52 96 116 142 6.5% 0.26 [0.15, 0.48]
Ran 2004 3 29 2 40 2.1% 2.19 [0.34, 14.05]
Song 2008$ 47 79 24 40 5.5% 0.98 [0.45, 2.13]
Wang 2005 15 79 20 73 5.5% 0.62 [0.29, 1.33]
Wang 2007$ 17 35 46 55 4.6% 0.18 [0.07, 0.49]
Xu 2006 59 120 36 68 6.4% 0.86 [0.47, 1.56]
Yang 2005 6 24 14 28 3.7% 0.33 [0.10, 1.09]
Yu 2005 6 31 19 39 4.1% 0.25 [0.08, 0.75]
Zheng 2007 10 36 13 104 4.7% 2.69 [1.06, 6.84]

Total (95% CI) 1555 1625 100.0% 0.57 [0.42, 0.77]


Total events 502 742
Heterogeneity: 2 = 0.29; 2 = 56.96, df = 20 (P < 0.0001); I2 = 65%
0.02 0.1 1 10 50
Test for overall effect: Z = 3.60 (P = 0.0003) Favours Starks Favours lower segment

D Grade 2 adhesion
Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2002 3 30 3 30 4.8% 1.00 [0.19, 5.40]
Chen 2007 30 75 5 87 7.0% 10.93 [3.97, 30.14]
Cheng 2005 1 34 10 42 3.7% 0.10 [0.01, 0.80]
Ding 2006 7 32 9 52 6.7% 1.34 [0.44, 4.03]
Huang 2007 203 482 203 482 9.4% 1.00 [0.77, 1.29]
Li 2005$ 16 46 2 36 5.2% 9.07 [1.92, 42.71]
Luo 2006 30 60 20 52 8.0% 1.60 [0.75, 3.40]
Niu 2006 6 20 4 20 5.5% 1.71 [0.40, 7.34]
Qu 2006 35 96 18 142 8.4% 3.95 [2.07, 7.54]
Ran 2004 0 29 6 40 2.4% 0.09 [0.00, 1.66]
Song 2008$ 11 79 2 40 5.2% 3.07 [0.65, 14.60]
Wang 2007$ 15 35 5 55 6.6% 7.50 [2.41, 23.39]
Xu 2006 20 120 12 68 7.9% 0.93 [0.42, 2.05]
Yang 2005 11 24 13 28 6.8% 0.98 [0.33, 2.91]
Yu 2005 10 31 2 39 5.0% 8.81 [1.76, 44.07]
Zheng 2007 7 36 36 104 7.4% 0.46 [0.18, 1.14]

Total (95% CI) 1229 1317 100.0% 1.78 [1.05, 3.00]


Total events 405 350
Heterogeneity: 2 = 0.74; 2 = 69.36, df = 15 (P < 0.00001); I2 = 78%
0.01 0.1 1 10 100
Test for overall effect: Z = 2.16 (P = 0.03) Favours Starks Favours lower segment

Figure 3. (Continued)

Controversies still exist about adhesion formation after ischaemia, tissue necrosis and inflammation.52 Hence, with-
previous caesarean section concerning closure of the perito- out closure of the peritoneum, there will be less adhesion
neum, both with reasonable theories. Some studies showed formation. However, it takes 6 weeks for the postpartum
that peritoneal healing occurs by simultaneous multi-site uterus to return to normal size and position completely,
repair as the result of migrating mesothelial cells with whereas peritoneal healing occurs within 35 days after
mesothelial matrix formation51 without the need for repo- caesarean section. Hence, the enlarged postpartum uterus
sitioning of the peritoneum, and peritoneal closure would may act as a mechanical disruptive barrier for the routine
lead to foreign body reactions to the suture material, mesothelial matrix formation of peritoneal healing,53

2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology 417
Shi et al.

E Grade 3 adhesion
Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight MH, Random, 95% CI MH, Random, 95% CI
Chen 2002 1 30 1 30 1.9% 1.00 [0.06, 16.76]
Chen 2007 17 75 4 87 7.4% 6.08 [1.95, 19.01]
Deng 2005 6 61 9 72 7.7% 0.76 [0.26, 2.28]
Ding 2006 8 32 2 52 4.7% 8.33 [1.64, 42.28]
Hong 2006 3 45 0 40 1.8% 6.67 [0.33, 133.22]
Huang 2007 145 482 25 482 13.8% 7.87 [5.03, 12.30]
Li 2005$ 8 46 3 36 5.8% 2.32 [0.57, 9.45]
Lin 2006 12 79 4 73 7.1% 3.09 [0.95, 10.06]
Liu 2007 7 62 0 50 1.9% 13.65 [0.76, 245.09]
Luo 2006 15 60 2 52 5.1% 8.33 [1.81, 38.46]
Niu 2006 5 20 1 20 2.9% 6.33 [0.67, 60.16]
Qu 2006 7 96 5 142 7.1% 2.16 [0.66, 7.00]
Ran 2004 0 29 1 40 1.5% 0.45 [0.02, 11.35]
Song 2008$ 5 79 0 40 1.8% 5.98 [0.32, 110.90]
Wang 2005 12 79 4 73 7.1% 3.09 [0.95, 10.06]
Wang 2007$ 3 35 2 55 3.9% 2.48 [0.39, 15.68]
Xu 2006 2 120 2 68 3.5% 0.56 [0.08, 4.06]
Yang 2005 7 24 1 28 3.0% 11.12 [1.26, 98.49]
Yu 2005 4 31 0 39 1.8% 12.93 [0.67, 249.97]
Zheng 2007 17 36 21 104 10.1% 3.54 [1.57, 7.96]

Total (95% CI) 1521 1583 100.0% 3.62 [2.38, 5.50]


Total events 284 87
Heterogeneity: 2 = 0.28; 2 = 30.75, df = 19 (P = 0.04); I2 = 38%
0.01 0.1 1 10 100
Test for overall effect: Z = 6.01 (P < 0.00001)
Favours Starks Favours lower segment

F Interval from skin incision to opening of peritoneum


Starks CS Lower segment CS Mean diffrence Mean diffrence
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% CI IV, Random, 95% CI

Huang 2007 14.1 2.9 482 9.2 3.4 482 29.5% 4.90 [4.50, 5.30]
Luo 2006 15.3 2.9 60 9.36 3.46 52 20.6% 5.94 [4.75, 7.13]
Song 2008$ 20 7 79 16 5 40 11.4% 4.00 [1.81, 6.19]
Wang 2007$ 9.46 2.52 35 6.25 1.89 55 23.2% 3.21 [2.24, 4.18]
Yang 2005 14.34 2.87 24 9.34 3.41 28 15.2% 5.00 [3.29, 6.71]

Total (95% CI) 680 657 100.0% 4.63 [3.70, 5.56]


Heterogeneity: 2 = 0.72; 2 = 14.52, df = 4 (P = 0.006); I2 = 72%
100 50 0 50 100
Test for overall effect: Z = 9.77 (P < 0.00001)
Favours Starks Favours lower segment

G Interval from skin incision to delivery of the newborn


Starks Lower segment Mean diffrence Mean diffrence
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% CI IV, Random, 95% CI

Chen 2002 9.67 7.18 30 10.83 8.14 30 29.7% 1.16 [5.04, 2.72]
Chen 2007 19.7 3.1 75 14.8 2.9 87 35.3% 4.90 [3.97, 5.83]
Xu 2006 7.8 4.2 120 9.4 3.5 68 35.1% 1.60 [2.72, 0.48]

Total (95% CI) 225 185 100.0% 0.82 [4.33, 5.97]


Heterogeneity: 2 = 19.37; 2 = 79.42, df = 2 (P = 0.00001); I2 = 97%
100 50 0 50 100
Test for overall effect: Z = 0.31 (P = 0.75)
Favours Starks Favours lower segment

H Blood loss from skin incision to opening of peritoneum


Starks Lower segment Mean diffrence Mean diffrence
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% CI IV, Random, 95% CI
Luo 2006 61.3 6.72 60 41.33 7.16 52 40.0% 19.97 [17.39, 22.55]
Wang 2007$ 50.26 6.44 35 31.45 5.28 55 41.1% 18.81 [16.26, 21.36]
Yang 2005 60.32 6.7 24 40.34 7.12 28 18.9% 19.98 [16.22, 23.74]

Total (95% CI) 119 135 100.0% 19.50 [17.86, 21.13]


Heterogeneity: 2 = 0.00; 2 = 0.47, df = 2 (P = 0.79); I2 = 0%
20 10 0 10 20
Test for overall effect: Z = 23.38 (P < 0.00001)
Favours Starks Favours lower segment

Figure 3. (Continued)

418 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology
Caesarean section techniques: under the cross-fire

A Total adhesion
Modified Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI

Chen 2007 13 57 33 87 50.1% 0.48 [0.23, 1.03]


Wang 2007 16 45 82 106 49.9% 0.16 [0.08, 0.35]

Total (95% CI) 102 193 100.0% 0.28 [0.10, 0.82]


Total events 29 115
Heterogeneity: 2 = 0.45; 2 = 4.02, df = 1 (P = 0.04); I2 = 75%
0.01 0.1 1 10 100
Test for overall effect: Z = 2.32 (P = 0.02)
Favours modified Starks Favours lower segment

B Grade 1 adhesion
Modified Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2007 8 57 24 87 42.8% 0.43 [0.18, 1.04]
Wang 2007 12 45 47 106 57.2% 0.46 [0.21, 0.98]

Total (95% CI) 102 193 100.0% 0.44 [0.25, 0.79]


Total events 20 71
Heterogeneity: 2 = 0.00; 2 = 0.01, df = 1 (P = 0.92); I2 = 0%
0.01 0.1 1 10 100
Test for overall effect: Z = 2.75 (P = 0.006) Favours modified Starks Favours lower segment

C Grade 2 adhesion
Modified Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2007 4 57 5 87 46.6% 1.24 [0.32, 4.82]
Wang 2007 4 45 28 106 53.4% 0.27 [0.09, 0.83]

Total (95% CI) 102 193 100.0% 0.55 [0.12, 2.45]


Total events 8 33
Heterogeneity: 2 = 0.76; 2 = 2.89, df = 1 (P = 0.09); I2 = 65%
0.01 0.1 1 10 100
Test for overall effect: Z = 0.78 (P = 0.43)
Favours modified Starks Favours lower segment

D Grade 3 adhesion
Modified Starks Lower segment Odds ratio Odds ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI M-H, Random, 95% CI
Chen 2007 1 57 4 87 62.9% 0.37 [0.04, 3.40]
Wang 2007 0 45 7 106 37.1% 0.15 [0.01, 2.61]

Total (95% CI) 102 193 100.0% 0.26 [0.05, 1.52]


Total events 1 11
Heterogeneity: 2 = 0.00; 2 = 0.26, df = 1 (P = 0.61); I2 = 0%
0.01 0.1 1 10 100
Test for overall effect: Z = 1.49 (P = 0.14)
Favours modified Starks Favours lower segment

E Interval from skin incision to delivery of the newborn


Modified Starks Lower segment Mean diffrence Mean diffrence
Study or Subgroup Mean SD Total Mean SD Total Weight IV, Random, 95% CI IV, Random, 95% CI
Chen 2007 10.5 2.4 57 14.8 2.9 87 100.0% 4.30 [5.17, 3.43]

Total (95% CI) 57 87 100.0% 4.30 [5.17, 3.43]


Heterogeneity: Not applicable
100 50 0 50 100
Test for overall effect: Z = 9.67 (P < 0.00001)
Favours modified Starks Favours lower segment

Figure 4. Modified Starks caesarean section versus classic lower-segment caesarean section: (A) total adhesions; (B) grade 1 adhesions; (C) grade 2
adhesions; (D) grade 3 adhesions; (E) interval from skin incision to delivery of the newborn.

particularly when the enlarged uterus is in direct contact isolation function of the peritoneum to avoid direct contact
with the anterior abdominal wall when the peritoneum is of the above-mentioned tissues and so reduce adhesion for-
left open. In addition, women after caesarean section are mation.
encouraged to move as soon as possible, so the left-open Recently, one meta-analysis compared adhesions after
visceral peritoneum can no longer isolate omentum and closure or non-closure of the peritoneum during the previ-
intestines from the healing uterus, neither will the non- ous caesarean section based on three qualified RCTs.54
closed parietal peritoneum separate omentum and intes- From the summary of 249 qualifying women, the authors
tines from the fascia and rectus abdominis. In this case, concluded that closure of the peritoneum had the advan-
closure of the peritoneum might maintain the original tage of reduced adhesion formation. However, although the

2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology 419
Shi et al.

authors mentioned that the RCTs included had adhesion diminished because this kind of adhesion is restricted to a
scoring scales, they did not report adhesions according to smaller region.
the degree of severity. Concerning multiple modifications In the comparison between modified caesarean section
of techniques in caesarean section procedures, it is also not and classic lower-segment caesarean section, data were less
sufficient to differentiate groups only by closure and non- persuasive because of the limited number of enrolled stud-
closure of the perineum, because other parameters like ies. Although there were many differences between these
longer abdominal operation time or pushing down of the two procedures, modified Starks caesarean section seems
bladder from its attachment position on the uterus may to incur fewer adhesions than classic lower-segment caesar-
also contribute to adhesion formation. Our results comple- ean section.
mented and did not overlap with those of the published Comparison subgroups for variables such as operation
meta-analysis. We addressed those problems by considering time and blood loss were also considered. Although these
various technique elements beyond closure versus non-clo- indices indirectly reflect the formation and severity of
sure of the peritoneum. adhesions, because of the limited number of studies avail-
able, the high heterogeneity in each subgroup, and the vari-
Interpretation of data ous skill levels of the operators, these results should be
In the comparison between Starks caesarean section and evaluated with caution.
modified Starks caesarean section, which differs only in
closure or non-closure of the two layers of peritoneum, Power of meta-analysis based on retrospective
there are significantly higher incidences of adhesion (both observational studies
in terms of total adhesions and individual grades of adhe- Generally, a RCT, which is the principal research design in
sion) when the peritoneum was left open. The value of I2 the evaluation of medical interventions, is a more qualified
in the grade 3 group was zero, indicating a more convinc- and persuasive study methodology compared with retro-
ing advantage of modified Starks caesarean section over spective observational study. However, meta-analysis based
Starks caesarean section in terms of severe adhesion for- on observational studies are not without merits.58 Such
mation, with little heterogeneity.55 importance becomes more prominent especially when it is
In comparisons of Starks caesarean section with lower- not possible or not convenient for RCTs to obtain data,
segment caesarean section and modified Starks caesarean such as for long-term prognosis through long periods of
section with lower-segment caesarean section, where the follow up accompanied by high drop-out rates, and limited
two corresponding groups differ in more aspects and there- size and number of available RCTs.59 Specifically, checking
fore lead to more variables, both the overall P values and the formation of adhesions after previous caesarean section
the I2 values were not supportive of significant and con- requires the opening of the abdominal or pelvic cavity,
vincing differences in adhesion formation (P > 0.05, and which can only be achieved during repeat operations.
I2 showing high heterogeneity). It was also shown that dif- No matter how well researchers design their prospective
ferent severities of adhesion formation existed between studies, it is difficult to collect adhesion data unless assigning
injury of visceral and injury of parietal peritoneum,56 so each participant an extra, and usually unnecessary, operation
studies comparing the closure of only the visceral perito- to confirm the formation of adhesions. Otherwise, the high
neum with closure of only the parietal peritoneum were rate of drop-out in this kind of RCT renders the study no
not included to avoid further complexity. The same condi- more persuasive than the retrospective observational studies
tion also applied to single-layer versus double-layer hyster- without randomisation or blinding. Furthermore, although
otomy closure at primary caesarean delivery and bladder scoring of adhesion might be influenced by individual
adhesions.57 Although the heterogeneity in each sub-com- perception, physicians who scored adhesions did not foresee
parison remained relatively high, there was an apparent the later retrospective study, and the formation of adhesions
trend suggesting that the less severe adhesions occurred was not influenced by expectations, stressors or actions of
more often in the classic lower-segment caesarean section, the participating women. Both these advantages, which serve
and the more severe adhesions occurred more often in the to decrease bias, may outweigh the disadvantages of nonran-
Starks caesarean section. This phenomenon has an ana- domisation and nonblinding.
tomical basis. In Starks caesarean section, because the ori-
ginal barrier of peritoneum is not restored, adhesions may Influencing factors of this meta-analysis
involve the attachment of omentum to the abdominal wall Because of the high heterogeneity, we employed the Man-
or uterus, intestines to uterus, or bladder to uterus, while telHaenszel random effect model for analysis.14 Most of
in classic lower-segment caesarean section, the peritoneum the included studies were carried out in China, probably
barrier is restored so the adhesion only involves attachment because small-scale retrospective observational studies are
of bladder to uterus. In the latter case, the severity is less popular for publication. We searched only for studies

420 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology
Caesarean section techniques: under the cross-fire

published in English or Chinese, which might also render a Table S1. Characteristics of adhesion.
selection bias. Both the adhesion scoring system and the Table S2. Intervals in repeat caesarean sections.
allocation of each woman into the corresponding group Table S3. Blood loss during Repeat caesarean sections
were based on personal skills and views, hence there might (from skin incision to delivery of newborn, in millilitres).
be possible bias based on personal judgment. As shown by Additional supporting information may be found in the
funnel plots, the estimated OR is probably biased in favour online version of this article.
of the Starks caesarean section or modified Starks caesar- Please note: Wiley-Blackwell are not responsible for the
ean section because of publication bias. More RCTs of content or functionality of any supporting information
higher quality and larger size are needed for further investi- supplied by the authors. Any queries (other than missing
gations and more robust results. material) should be directed to the corresponding
Generally speaking, our meta-analysis provides strong author. j
evidence that closure of both layers of peritoneum during
modified Starks caesarean section significantly reduces the
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422 2010 The Authors Journal compilation RCOG 2010 BJOG An International Journal of Obstetrics and Gynaecology