Systematic review

Meta-analysis of the risk of small bowel obstruction following

open or laparoscopic colorectal surgery
T. Yamada1 , K. Okabayashi1 , H. Hasegawa1 , M. Tsuruta1 , J.-H. Yoo2 , R. Seishima1 and Y. Kitagawa1
1 Department of Surgery, Keio University School of Medicine, Tokyo, and 2 Department of Surgery, National Hospital Organization Saitama National
Hospital, 2–1 Suwa Wako, Saitama, Japan
Correspondence to: Dr K. Okabayashi, Department of Surgery, Keio University School of Medicine, 35 Shinano-machi Shinjuku-ku, 1608582 Tokyo, Japan
(e-mail: okabayashikoji@gmail.com)

Background: One of the potential advantages of laparoscopic compared with open colorectal surgery is a
reduction in postoperative bowel obstruction events. Early reports support this proposal, but accumulated
evidence is lacking.
Methods: A systematic review and meta-analysis was performed of randomized clinical trials and
observational studies by searching the PubMed and Cochrane Library databases from 1990 to August
2015. The primary outcomes were early and late postoperative bowel obstruction following laparoscopic
and open colorectal surgery. Both ileus and bowel obstruction were defined as a postoperative bowel
obstruction. Subgroup and sensitivity analyses were performed, and a random-effects model was used to
account for the heterogeneity among the studies.
Results: Twenty-four randomized clinical trials and 88 observational studies were included in the
meta-analysis; 106 studies reported early outcome and 12 late outcome. Collectively, these studies
reported on the outcomes of 148 392 patients, of whom 58 133 had laparoscopic surgery and 90 259 open
surgery. Compared with open surgery, laparoscopic surgery was associated with reduced rates of early
(odds ratio 0⋅62, 95 per cent c.i. 0⋅54 to 0⋅72; P < 0⋅001) and late (odds ratio 0⋅61, 0⋅41 to 0⋅92; P = 0⋅019)
postoperative bowel obstruction. Weighted mean values for early postoperative bowel obstruction were
8 (95 per cent c.i. 6 to 10) and 5 (3 to 7) per cent for open and laparoscopic surgery respectively, and for
late bowel obstruction were 4 (2 to 6) and 3 (1 to 5) per cent respectively.
Conclusion: The reduction in postoperative bowel obstruction demonstrates an advantage of laparo-
scopic surgery in patients with colorectal disease.
Presented to the Annual Meeting of the American Society of Colon and Rectal Surgeons, Phoenix, Arizona, USA, April
2013

Paper accepted 14 December 2015

Published online 22 February 2016 in Wiley Online Library (www.bjs.co.uk). DOI: 10.1002/bjs.10105

Introduction with surgical manoeuvres and the inflammation induced

Adhesions and subsequent bowel obstruction repre-
sent a lifelong risk for patients who have undergone
colectomy1 – 4 , with one-third needing surgery5 . The cost
of each admission is estimated at €5000 for those managed
surgically and €2000 for conservative therapy5 . Laparo-
scopic surgery for colorectal disease reportedly achieves
superior short-term outcomes, including better cosmesis
and quality of life with lower morbidity6 – 9 . However, it is
unclear whether the risks of small bowel obstruction are
reduced.
Adhesion formation is closely related to wound heal-
ing pathways, and these processes are closely associated
by exposure of tissues to intestinal contents, the irritation
caused by exposure to foreign materials, abrasion, desicca-
tion, and many other causes10,11 . Laparoscopic surgery may
reduce adhesion formation because it involves shorter inci-
sions and less tissue trauma, causes less bleeding, reduces
the potential for desiccation, and lowers the potential for
contamination by foreign bodies11 . A nationwide study12
following minimal-access colorectal surgery in England
revealed a lower adhesion-related readmission rate for
laparoscopic than open surgery.
Randomized clinical trials (RCTs) have generated
conflicting results. The Australasian Laparoscopic Colon
Cancer Study13 demonstrated that laparoscopic surgery

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Published by John Wiley & Sons Ltd
494 T. Yamada, K. Okabayashi, H. Hasegawa, M. Tsuruta, J.-H. Yoo, R. Seishima and Y. Kitagawa
was superior to open surgery in terms of risk of early
postoperative bowel obstruction (3⋅1 versus 7⋅7 per cent
respectively). However, the COlon cancer Laparoscopic
or Open Resection (COLOR)I6 (early bowel obstruction:
3 per cent for open versus 2 per cent for laparoscopic
surgery) and COLOR II14 trials (ileus: 3 versus 5 per cent
respectively) did not show significant differences.
The aim of the present study was to quantify the impact of
laparoscopic surgery for colorectal disease on the incidence
of early and late postoperative bowel obstruction using the
accumulated evidence.
Methods
This manuscript was written in accordance with the
Preferred Reporting Items for Systematic Reviews and
Meta-analyses statement15 .
Search strategy
A systematic search was undertaken of PubMed (MED-
LINE) and Cochrane Library databases from 1990 to
August 2015 for publications written in English that
described early and late postoperative bowel obstruction
following open and laparoscopic surgery for colorectal
disease. Search terms were ‘colorectal’ (colo* or rect* or
colorect*) and ‘operation’ (laparoscop* or laparotomy or
open).
Inclusion and exclusion criteria
The primary endpoints for this study were defined as the
early and late bowel obstruction following open or laparo-
scopic colorectal surgery. As definitions of ileus/prolonged
ileus and bowel obstruction differed among the studies,
both ileus and bowel obstruction were defined in this study
as a postoperative bowel obstruction because of no vali-
dated definition of these words. The study designs included
were RCT, cohort studies and case–control studies that
compared open colorectal surgery with laparoscopic
surgery. The study included colorectal surgical procedures
for colorectal cancer, diverticular disease, ulcerative colitis,
familial adenomatous polyposis (FAP) and rectal prolapses.
As it was difficult to distinguish between complications
associated with bowel obstruction and disease recurrence
in patients with Crohn’s disease, all studies involving such
patients were excluded. Experimental and unpublished
studies were also excluded. Two investigators indepen-
dently assessed the eligibility of studies for inclusion in the
meta-analysis.
© 2016 BJS Society Ltd
Published by John Wiley & Sons Ltd
Potentially relevant studies identified
and screened for retrieval n = 6154
PubMed n = 5513
Cochrane Library n = 641
Records after duplicates removed
n = 5884
Records excluded n = 5533
Full-text articles assessed for eligibility
n = 351
Articles excluded from review n = 239
Multiple publications of same cohort n = 59
Irrelevant study n = 171
Language limitation (not in English) n = 9
Studies included in meta-analysis
n = 112
Fig. 1 PRISMA diagram for the systematic review
Assessment of methodological quality and data
extraction
The total numbers of patients participating in the stud-
ies and events occurring during follow-up were extracted
from studies included in the meta-analysis. In addition, data
relating to study design, participant demographic details,
co-variables, and incidence rates of ileus and/or bowel
obstruction were extracted. The same two investigators
independently assessed the quality of the observational
studies and the risk of bias within all studies using the
Newcastle–Ottawa Scale (NOS) and the Cochrane Col-
laboration’s tool for assessing the risk of bias respectively16 .
Studies with NOS scores of 7 or above were categorized as
being of higher quality, and those with NOS scores below
7 were categorized as being of lower quality.
Statistical analysis
Weighted mean averages were calculated by means of
the random-effects model using generic inverse effect.
The DerSimonian–Laird procedure was used to fit the
random-effects model and to compute the odds ratios
(ORs) as surrogates for measures of effect size. The 95
per cent confidence intervals were calculated, and het-
erogeneity among the studies was quantified using the I 2
index, which was interpreted as follows: I 2 values of 0–30
per cent represented low levels of heterogeneity; I2 values
of more than 30 to 50 per cent represented moderate
levels of heterogeneity; I2 values of more than 50 to 90
per cent represented substantial levels of heterogeneity;
www.bjs.co.uk BJS 2016; 103: 493–503
Small bowel obstruction after colorectal surgery
and I2 values above 90 per cent represented considerable
heterogeneity. Studies were assessed for publication bias by
testing for funnel plot asymmetry using Begg’s test. Sub-
group analysis was performed, based on the type of disease
being treated (cancer, diverticular disease, ulcerative colitis
or FAP), whether the study was an RCT or observational
study, and whether the patients were of Western or Asian
ethnicity. A random-effects metaregression was conducted
to evaluate the influence of several co-variables (year in
which the study was published, type of disease, type of
study and patients’ ethnicity) on the heterogeneity of
the ORs generated. Stata® version 12.1 (StataCorp LP,
College Station, Texas, USA) was used for all analyses. For
all comparisons, except those relating to heterogeneity,
statistical significance was defined as P < 0⋅050, and all
tests were two-sided.
Results
Search process
Fig. 1 provides an overview of the search process. Searches
of electronic and other sources identified 6154 publica-
tions. Some 5533 studies were excluded after removing
duplicates from the title and abstract searches. Of the 351
full-text papers reviewed, 112 (106 for early outcome, 12
for late outcome) met the search criteria and were included
in the meta-analysis6,13,14,17 – 125 . Collectively, the studies
reported on the outcomes of 148 392 patients (58 133
laparoscopic surgery, 90 259 open surgery). Of the 106
studies reviewed that reported on early postoperative bowel
obstruction, 43 defined 30 days as early and two defined
28 days as early; the other studies did not clearly define
early postoperative bowel obstruction. Table S1 (support-
ing information) lists the studies included in the review,
which comprised 24 RCTs and 88 observational studies.
The NOS determined that 26 observational studies were
of higher quality and 62 were of lower quality. Figs S1 and
S2 (supporting information) present the evaluation of bias
for all studies.
Morbidity associated with bowel obstruction
A total of 106 studies reported on early postoperative bowel
obstruction. These studies included 146 494 patients, of
whom 89 370 underwent open surgery and 57 124 had
laparoscopic surgery. Of these participants, 14 708 devel-
oped a small bowel obstruction following open surgery
and 6752 developed one following laparoscopic surgery.
Weighted mean values for complications associated with
early postoperative bowel obstruction were 8 (95 per cent
© 2016 BJS Society Ltd
Published by John Wiley & Sons Ltd
495
0·25
Event rate for laparoscopic surgery
0 0·25
Event rate for open surgery
Fig. 2 L’Abbé plot of bowel obstruction morbidity outcomes for
all trials to investigate potential sources of heterogeneity.
Dimensions of the circles are proportional to the numbers of
patients enrolled in individual studies. The solid line depicts the
overall odds ratio (OR), which represents the OR estimation
attained by pooling the results of all studies
Table 1 Univariable meta-regression analysis of factors related to
short-term morbidity associated with postoperative bowel
obstruction
Coefficient P
Cancer −0⋅044 (−0⋅157, 0⋅689) 0⋅445
Western ethnicity 0⋅281 (0⋅093, 0⋅468) 0⋅003
RCT 0⋅039 (−0⋅205, 0⋅284) 0⋅754
Year of publication 0⋅015 (−0⋅008, 0⋅039) 0⋅200
Values in parentheses are 95 per cent confidence intervals. RCT,
randomized clinical trial.
c.i. 6 to 10) and 5 (3 to 7) per cent for open and laparo-
scopic surgery respectively. Fig. 2 presents a l’Abbé plot of
bowel obstruction outcomes that shows variations in the
observed results across all of the studies included. Com-
parisons demonstrated that laparoscopic surgery was asso-
ciated with less early obstruction (OR 0⋅62, 95 per cent c.i.
0⋅54 to 0⋅72; P < 0⋅001), with a moderate level of hetero-
geneity (I 2 = 37⋅7 per cent) (Fig. 3). Testing for funnel plot
asymmetry using Begg’s test did not identify any significant
publication bias (P = 0⋅349) (Fig. 4).
Twelve studies reported on late postoperative bowel
obstruction. Of the 3406 study participants, 1759 under-
went open surgery and 1647 underwent laparoscopic
surgery. Sixty-nine patients (3⋅9 per cent) developed a small
bowel obstruction following open surgery and 39 (2⋅4 per
cent) after laparoscopic surgery. Weighted mean values for
late postoperative bowel obstruction were 4 (95 per cent
c.i. 2 to 6) per cent for open surgery and 3 (1 to 5) per cent
for laparoscopic surgery. The incidence of postoperative
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496 T. Yamada, K. Okabayashi, H. Hasegawa, M. Tsuruta, J.-H. Yoo, R. Seishima and Y. Kitagawa

Events
Laparoscopic Open Odds ratio P I2 Odds ratio
Overall 6752 of 57 124 14 708 of 89 370 0·62 (0·54, 0·72) < 0·001 37·7
Type of disease
Cancer 582 of 12 460 1254 of 15 867 0·62 (0·51, 0·73) < 0·001 40·4
Diverticular disease 24 of 719 90 of 1032 0·39 (0·24, 0·63) < 0·001 0
FAP or UC 25 of 247 34 of 457 1·08 (0·58, 2·01) 0·803 0
Type of study
RCT 140 of 3759 168 of 3362 0·74 (0·58, 0·94) 0·015 0
Observational study 6612 of 53 365 14 540 of 86 008 0·59 (0·50, 0·70) < 0·001 44·6
Ethnicity
Western 6567 of 50 731 14 257 of 81 715 0·69 (0·57, 0·83) < 0·001 48·8
Asia 185 of 6393 451 of 7655 0·54 (0·43, 0·66) < 0·001 9·6

0·25 0·5 1·0 1·5 2·0 2·5

Forest plot of odds ratios for short-term morbidity associated with postoperative bowel obstruction for the subgroups.
Fig. 3
A random-effects model was used for meta-analysis. Values in parentheses are 95 per cent confidence intervals. FAP, familial
adenomatous polyposis; UC, ulcerative colitis; RCT, randomized clinical trial

4 Type of disease
Early postoperative bowel obstruction events were less
frequent when laparoscopic surgery was undertaken in
2
patients with cancer (OR 0⋅62, 95 per cent c.i. 0⋅51 to 0⋅73;
P < 0⋅001) and in those with diverticular disease (OR 0⋅39,
Log[OR]

0 0⋅24 to 0⋅63; P < 0⋅001), compared with open surgery. No

–2
–4
0 0·5 1·0 1·5
s.e. of log[OR]
Fig. 4Funnel plot for visual assessment of the presence of
publication bias associated with all studies included in the
meta-analysis. The symbols indicate individual studies. The
central line represents the pooled odds ratios (ORs), and the
dotted lines depict pseudo 95 per cent confidence intervals.
Begg’s test did not identify any significant publication bias
(Kendall’s τ coefficient −0⋅94, P = 0⋅349)
bowel obstruction was significantly reduced following
laparoscopic surgery (OR 0⋅61, 0⋅41 to 0⋅92; P = 0⋅019,
I2 = 0) (Fig. 5).
Subgroup analysis
Subgroup analyses were performed to explore the sources
of moderate heterogeneity across the studies included in
the meta-analysis and to conduct sensitivity analyses to
validate the benefit of laparoscopic surgery.
significant difference was seen in relation to the early post-
operative bowel obstruction when laparoscopic surgery was
performed in patients with ulcerative colitis or FAP (OR
1⋅08, 0⋅58 to 2⋅01; P = 0⋅803). Similarly, late small bowel
obstruction was less frequent after laparoscopic surgery
2·0
for cancer (OR 0⋅63, 0⋅40 to 0⋅98; P = 0⋅039), but not for
diverticular disease (OR 0⋅31, 0⋅01 to 7⋅76; P = 0⋅475). The
number of events (12 open, 1 laparoscopic) and patients
(290 and 100 respectively) were small, limiting the analysis
for ulcerative colitis and FAP.
Type of study
Twenty-two RCTs and 84 observational studies reported
on early postoperative bowel obstruction. Laparoscopic
surgery was associated with a lower risk of early postop-
erative bowel obstruction in the RCTs (OR 0⋅74, 95 per
cent c.i. 0⋅58 to 0⋅94; P = 0⋅015) and in observational stud-
ies (OR 0⋅59, 0⋅50 to 0⋅70; P < 0⋅001). Three RCTs and
nine observational studies reported on late postoperative
bowel obstruction, with no significant difference identi-
fied in either observational studies (OR 0⋅64, 0⋅41 to 1⋅02;
P = 0⋅058) or RCTs (OR 0⋅50, 0⋅20 to 1⋅25; P = 0⋅14).
Early postoperative bowel obstruction was less frequent
following laparoscopic than open surgery both in patients
of Western (OR 0⋅69, 95 per cent c.i. 0⋅57 to 0⋅83;
P < 0⋅001) and those of Asian (OR 0⋅54, 0⋅43 to 0⋅66;

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Published by John Wiley & Sons Ltd
Small bowel obstruction after colorectal surgery 497

Events
Reference Laparoscopic Open Weight (%) Odds ratio Odds ratio
Franklin et al.95 2 of 191 6 of 224 6·5 0·38 (0·08, 1·93)
Champault et al.62 0 of 74 3 of 83 1·9 0·15 (0·01, 3·04)
Kairaluoma et al.90 0 of 53 1 of 53 1·6 0·33 (0·01, 8·21)
Patankar et al.94 3 of 172 2 of 172 5·2 1·51 (0·25, 9·14)
Thaler et al.82 1 of 49 5 of 50 3·5 0·19 (0·02, 1·67)
Braga et al.74 3 of 190 6 of 201 8·6 0·52 (0·13, 2·12)
Haughn et al.28 0 of 61 1 of 61 1·6 0·33 (0·01, 8·21)
Taylor et al.24 7 of 280 4 of 131 10·9 0·81 (0·23, 2·83)
Dolejs et al.110 2 of 100 9 of 290 7·0 0·64 (0·14, 3·00)
Gervaz et al.61 0 of 54 1 of 51 1·6 0·31 (0·01, 7·76)
Schölin et al.25 17 of 383 24 of 403 41·6 0·73 (0·39, 1·39)
Ng et al.78 4 of 40 7 of 40 9·8 0·52 (0·14, 1·95)

Combined 39 of 1647 69 of 1759 100·0 0·61 (0·41, 0·92)

0·1 1 10
Heterogeneity: = 0·00; = 4·34, 11 d.f., P = 0·96;
τ2 χ2 I2 = 0%
Test for overall effect: Z = 2·35, P = 0·019 Favours laparoscopic Favours open

Forest plot of the odds ratio for long-term morbidity associated with postoperative bowel obstruction. A random-effects model
Fig. 5
was used for meta-analysis. Values in parentheses are 95 per cent confidence intervals

P < 0⋅001) ethnicity. Late obstruction following laparo-
scopic surgery was less common in Western patients (OR
0⋅61, 0⋅40 to 0⋅96; P = 0⋅031); however, no significant dif-
ference was seen in Asian patients (OR 0⋅52, 0⋅14 to 1⋅95;
P = 0⋅336)
Meta-regression analyses
In an exploration of the co-variables affecting the hetero-
geneity of the ORs among the included studies, univariable
meta-regression analysis of early postoperative bowel
obstruction identified that studies carried out in Western
countries were a significant source of heterogeneity (co-
efficient 0⋅281, 95 per cent c.i. 0⋅093 to 0⋅468; P = 0⋅003)
(Table 1). Univariable meta-regression did not identify
any significant co-variables for late postoperative bowel
obstruction.
Discussion
Laparoscopic surgery for colorectal disease reduces over-
all early postoperative bowel obstruction, including ileus,
as well as early bowel obstruction in subgroups of patients
having surgery for cancer and diverticular disease, but
not for ulcerative colitis or FAP. Laparoscopic surgery for
ulcerative colitis and FAP included non-restorative opera-
tions, for which a stoma is commonly used. Comparisons
with colectomy for cancer may be limited (mostly restora-
tive without a stoma).
This study also showed that laparoscopic surgery was
associated with lower overall rates of late postoperative
bowel obstruction, but only for cancer operations in sub-
group analysis. Just 12 studies compared laparoscopic with
open surgery with respect to late postoperative bowel
obstruction, but they did not represent primary study end-
points. Only the COLOR trial25 and the Conventional
versus Laparoscopic-Assisted Surgery In Colorectal Can-
cer (CLASICC) trial24 have described the incidence of
late postoperative bowel obstruction over time. The 3-year
cumulative incidence rate was 3⋅1 and 2⋅5 per cent for
open and laparoscopic surgery respectively in the CLA-
SICC trial, and the 5-year rate was 6⋅5 and 5⋅1 per cent
in the COLOR trial. Adhesion prevention barriers can
reduce surface adhesion formation by between 23 and 48
per cent126,127 , but reduce bowel obstruction by only 2⋅9
per cent128 .
Although most of the studies included in the present
meta-analysis did not specify the patient ethnicities, people
of Western ethnicity have a slightly higher risk of bowel
obstruction. Similarly, Causey and colleagues129 reported
that, among patients undergoing emergency abdominal
surgery, the overall complication rate was higher among
blacks than Asians or Hispanics. In addition to the genetic
variations, surgical style differences between East and West
may be factors.
There were some limitations to this meta-analysis. First,
the definition of early postoperative bowel obstruction dif-
fered among the individual studies. Second, several con-
cerns existed with respect to the terminology used to

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498 T. Yamada, K. Okabayashi, H. Hasegawa, M. Tsuruta, J.-H. Yoo, R. Seishima and Y. Kitagawa
describe small bowel obstruction as a mechanical entity
versus ileus. Although the term ileus generally means a post-
operative paralytic intestinal state, several studies included
this as bowel obstruction. Rigorously applied definitions
might be useful to help understand bowel obstruction
more precisely. Third, there were few high-quality RCTs
describing late postoperative bowel obstruction, although
these may follow in time. Perhaps the best evidence
comes from population-based data, where a lower risk of
late obstruction has been observed following laparoscopic
surgery12 .
Disclosure
The authors declare no conflict of interest.
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Supporting information

Additional supporting information may be found in the online version of this article:
Table S1 Overview of studies included in the meta-analysis (Word document)
Fig. S1 Quality assessment of each study included in the meta-analysis that used the Cochrane Collaboration tool to
assess the risk of bias (Word document)
Fig. S2 Risk-of-bias graph (Word document)

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