ORIGINAL ARTICLE
Effect of Laparoscopy on the Risk
of Small-Bowel Obstruction
A Population-Based Register Study
Eva Angenete, MD, PhD; Anders Jacobsson, MSc; Martin Gellerstedt, PhD; Eva Haglind, MD, PhD
Objective: To investigate the incidence and risk factors for small-bowel obstruction (SBO) after certain surgical procedures.
Design: A population-based retrospective register study.
Setting: Small-bowel obstruction causes considerable
patient suffering. Risk factors for SBO have been identified, but the effect of surgical technique (open vs laparoscopic) on the incidence of SBO has not been fully elucidated.
on demographic characteristics, comorbidity, previous
abdominal surgery, and death were collected.
Main Outcome Measures: Episodes of hospital stay
and surgery for SBO within 5 years after the index surgery.
Results: A total of 108 141 patients were included. The
incidence of SBO ranged from 0.4% to 13.9%. Multivariate analysis revealed age, previous surgery, comorbidity, and surgical technique to be risk factors for SBO. Laparoscopy exceeded other risk factors in reduction of the
risk of SBO for most of the surgical procedures.
Patients: The Inpatient Register held by the Swedish
National Board of Health and Welfare was used. The hospital discharge diagnoses and registered performed surgical procedures identified data for cholecystectomy, hysterectomy, salpingo-oophorectomy, bowel resection,
anterior resection, abdominoperineal resection, rectopexy, appendectomy, and bariatric surgery performed
from January 1, 2002, through December 31, 2004. Data
Conclusions: Open surgery seems to increase the risk
of SBO at least 4 times compared with laparoscopy for
most of the abdominal surgical procedures studied. Other
factors such as age, previous abdominal surgery, and comorbidity are also of importance.
Arch Surg. 2012;147(4):359-365
S
MALL - BOWEL OBSTRUCTION
(SBO) is a mechanical bowel
obstruction and a common
reason for emergency admission.1 The dominating etiology is intraperitoneal adhesions2,3 that develop as a response to peritoneal trauma,
such as abdominal surgery, and form
within days after a surgical procedure.4,5
Author Affiliations:
Scandinavian Surgical
Outcomes Research Group,
Gothenburg (Drs Angenete,
Gellerstedt, and Haglind);
Department of Surgery,
Sahlgrenska University
¨ stra, University of
Hospital/O
Gothenburg, Gothenburg
(Drs Angenete and Haglind);
and Swedish National Board of
Health and Welfare, Stockholm
(Mr Jacobsson), Sweden.
See Invited Critique
at end of article
In the immediate postoperative period it
may be clinically difficult to discriminate
adhesion-related mechanical bowel obstruction from postoperative ileus (nonmechanical bowel obstruction),6 but adhesion-related morbidity, such as SBO,
increases over time, and many patients
have several episodes of adhesion-related
readmissions after a surgical procedure
at different time intervals.7 AdhesionARCH SURG/ VOL 147 (NO. 4), APR 2012
359
related morbidity is related to substantial
health care costs8 and, as a complication
of surgery, it is becoming a medicolegal
issue.9
Reduction of adhesion-related morbidity, such as SBO, is thus of importance for
patients as well as for society. Risk factors for SBO after surgery include age, site
and type of surgery within the abdomen,
previous surgery for SBO, emergency surgery, and inflammatory conditions.10-12 Because adhesions can be reduced by improvement of surgical technique and
different types of mechanical barriers and
adhesion-reducing solutions,12 it is probable that these measures would reduce the
risk of SBO; however, the clinical impact
has not been fully elucidated. Laparoscopic surgery is considered to be associated with less surgical trauma,13 implying a reduction of adhesions. The reports
in the literature regarding the clinical effect of laparoscopy on adhesion-related
morbidity have not been convinc-
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ing,11,14-17 but a recent review found indications of a positive effect.12
Laparoscopic surgery is evolving and is now part of
the routine practice in most hospitals. Some clinical advantages of laparoscopic surgery compared with open surgery have been shown, such as shorter hospital stay, less
postoperative pain, and a faster recovery.18,19 Open surgery has advantages with better overview and tactile feedback, and laparoscopy has a longer learning curve, but
reports have proven the 2 techniques similar in outcome, for example, in colorectal malignancy.20 Despite
prolonged operating time and initial higher costs compared with open surgery, laparoscopic surgery has been
reported to reduce costs in a longer perspective.21
The aim of this study was to explore the incidence of
SBO after abdominal and pelvic surgery for several common surgical and gynecological conditions and to identify possible risk factors for SBO.
METHODS
STUDY DESIGN
Study Population
This study was undertaken using the Inpatient Register held
by the Swedish National Board of Health and Welfare, which
contains information on hospital discharge diagnoses (coded
according to the International Classification of Diseases, Tenth
Revision [ICD-10]) and on performed surgical procedures (coded
according to the Swedish version of the Nordic MedicoStatistical Committee Classification of Surgical Procedures, version 1.9) in all Swedish hospitals. It is required by legislation
that all health care providers keep records of and report all treated
patients, including those in day care. More than 98% of all episodes of hospitalization in Sweden are reported to the registry.22 The validity is considered high for surgical procedures.23
Inclusion Criteria
The study was undertaken in several steps. The use of laparoscopy was not sufficiently frequent before 2002 to allow for separate analyses of surgical technique, so no procedures before 2002
were included. Because previous studies have demonstrated that
the site and type of surgery affect adhesion formation,10 we chose
the most common abdominal procedures performed by an open
or a laparoscopic approach in 2002. All patients with surgical
codes identifying any of these procedures from January 1, 2002,
through December 31, 2004, were included: cholecystectomy; hysterectomy; salpingo-oophorectomy; bowel resection, including small-bowel resection and all types of colonic
resections but not rectal resections; anterior resection of the
rectum; abdominoperineal resection of the rectum; rectopexy;
appendectomy; and bariatric surgery, including gastric bypass
(representing most cases of bariatric surgery), vertical banded
gastroplasty, gastric banding, and other procedures to diminish gastric volume.
To address possible bias of confounding by indication and
with inflammation as a risk factor for adhesion formation,10,12
we separated the cholecystectomy performed because of ordinary gallstones (ICD-10 code K80.2) from the cholecystectomy performed because of cholecystitis and complicated gallstone disease. We also identified flegmonous appendicitis
(ICD-10 code K35.8) and separated this from all other types of
appendicitis.
Exclusion Criteria
All patients with hospitalization or surgery for SBO before the
index operation were excluded.24
Variables Studied
Age, sex, comorbidity (defined as at least 1 extra diagnosis apart
from the main diagnosis), surgical technique (open or laparoscopic), and abdominal surgery before the index operation were
studied.
Follow-up Time
Follow-up lasted until death or up to 5 years after the initial
surgical procedure. No patient was followed up more than 5
years.
Outcome Measures
We extracted data for each individual on hospital stay due to
SBO defined by the following ICD-10 diagnoses: K56.5 (“small
bowel obstruction due to adhesions”), K56.6 (“other and not
specified obstruction of the bowel”), and K56.7 (“small bowel
obstruction without further specification”). Early postoperative SBO (defined as hospitalization or surgery within 7 days
of the index procedure), which mainly represents postoperative ileus6 and not mechanical obstruction, was not included.
All surgical procedures during this period indicating surgery for bowel obstruction were identified by the Swedish surgical codes alone or in combination with the ICD-10 code for
bowel obstruction just mentioned. The surgical codes for colonic resection were not included to reduce the risk of including patients with bowel obstruction due to causes other than
adhesions. Each patient was counted for only the first admission or the first surgical procedure for SBO, even if there were
more episodes during the 5-year follow-up period.
ETHICAL ASPECTS
The data retrieval from the register did not include patient or
hospital identification. No individual patient medical records
have been studied, and results are presented only for groups.
No individual patient can be identified; thus, no approval from
the ethics committee was required or obtained.
STATISTICAL ANALYSIS
The age of an individual was replaced by the average age in the
corresponding age class (each age class ranged 5 years). For
comparing age between groups, either the independent t test
or, in the case of a significant Levene test indicating heteroscedasticity, the Welsh version of the test was used. For comparison of categorical variables between groups, the ␹2 test was used.
When comparing the risk of hospitalization for SBO, surgery
for SBO, and mortality between surgical techniques (open vs
laparoscopic), the odds ratio was calculated. In an adjusted analysis, the risk of hospitalization for SBO was studied by using logistic regression with surgical technique (open vs laparoscopic), age (dichotomized: older vs younger than the median
age per surgical procedure), previous abdominal surgery (yes
vs no), comorbidity (yes vs no), and when applicable, also sex
(male vs female) as explaining factors. When analyzing abdominoperineal resection, surgical technique was excluded as
an explaining factor because of the few cases of laparoscopic
surgery.
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112 190 Patients extracted
from register
108 141 Included
34 659 Had cholecystectomy
9319 Had salpingo-oophrectomy
Lap, 30%
SBO, 2.8%
14 392 Had hysterectomy
Lap, 1%
SBO, 3.3%
18 395 Had cholecystectomy
due to uncomplicated
disease
Lap, 89%
SBO, 0.4%
4049 Excluded for previous SBO
3523 Had anterior resection
Lap, 2%
SBO, 10.2%
14 486 Had bowel resection
Lap, 2%
SBO, 2.8%
275 Had rectopexia
Lap, 24%
SBO, 5.8%
1183 Had abdominoperineal
resection
Lap, 1%
SBO, 13.9%
16 264 Had cholecystectomy
due to uncomplicated
disease
Lap, 62%
SBO, 0.8%
1896 Had bariatic surgery
Lap, 35%
SBO, 3.2%
28 408 Had appendectomy
18 803 Had appendectomy
due to flegmonous
appendicitis
Lap, 17%
SBO, 0.4%
9605 Had appendectomy
including peritonitis
Lap, 12%
SBO, 1.8%
Figure. Incidence of small-bowel obstruction (SBO) in the study population. Lap indicates laparoscopic technique.
Table 1. Effect of Age, Sex, Previous Abdominal Surgery, and Comorbidity on the Rate of SBO
Age,
Mean (SD), y
Procedure
Cholecystectomy
Cholecystectomy due to
complicated disease
Hysterectomy
Salpingo-oophorectomy
Bowel resection
Anterior resection
Abdominoperineal
resection
Rectopexy
Appendectomy due to
flegmonous appendicitis
Appendectomy
Bariatric surgery
Female Sex, %
History of
Surgery, %
Presence of
Comorbidity, %
Died During
Follow-Up, %
No.
% SBO
SBO
No SBO
SBO
No SBO
SBO
No SBO
SBO
No SBO
SBO
No SBO
18 395
16 264
0.4
0.8
56 (17) a
64 (14) a
48 (15)
54 (17)
71
42 a
76
60
28 a
32 a
14
16
38 a
57 a
21
35
22 a
40 a
2
10
14 392
9319
14 486
3523
1183
3.3
2.8
6.6
10.2
13.9
62 (13) a
61 (14) a
64 (16) a
65 (14) a
66 (13) b
55 (13)
54 (15)
68 (16)
69 (12)
68 (12)
100
100
54
40c
39
100
100
53
46
44
11
19 c
25 a
24
39 c
10
14
19
20
31
49
42
58 b
45
50
51
41
54
50
51
48 a
55 a
43
41
42
10
10
40
38
43
275
18 803
5.8
0.4
74 (14)
43 (21) a
64 (19)
29 (17)
100
37
90
43
25
13 a
28
4
62
19 c
45
10
44
12 a
26
1
9605
1896
1.8
3.2
47 (24) a
42 (12)
35 (22)
41 (10)
52
74
50
77
12 c
16
8
20
46 a
36
24
36
23 a
0
6
3
Abbreviation: SBO, small-bowel obstruction.
a P ⬍ .001.
b P ⬍ .01.
c P ⬍ .05.
Sex was excluded as an explaining factor when analyzing rectopexy because there were few cases in the male population.
RESULTS
Data on 112 190 patients were extracted from the register; however, 4049 of those patients had a previous hospitalization for SBO and were thus excluded from further analysis. The remaining 108 141 patients were
included in the study (Figure). The incidence of SBO
ranged from 0.4% to 13.9% depending on the type of operation. The effect of age, sex, previous abdominal surgery, and comorbidity on the rate of SBO is displayed in
Table 1 (bivariate analysis). For most surgical procedures, patients with SBO were older, and SBO was more
common in patients with previous abdominal surgery.
In patients who underwent cholecystectomy, bowel resection, or appendectomy, a higher comorbidity was associated with a higher incidence of SBO. In the group of
complicated cholecystectomy as well as the group of anterior resection, SBO was more common among men.
Within 5 years, SBO was associated with an increased risk
of mortality (Table 1).
The mean age, sex, history of previous abdominal surgery, and the comorbidity for each procedure subdivided into groups of open and laparoscopic surgery are
displayed in Table 2. The mean age was higher in the
open group for cholecystectomy, hysterectomy, salpingooophorectomy, bowel resection, complicated appendectomy, and bariatric surgery. In general, there were more
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Table 2. Mean Age, Sex, History of Abdominal Surgery, and Presence of Comorbidity
for Each Procedure Divided Into Groups of Open and Laparoscopic Surgery
Age, Mean (SD), y
Procedure
Cholecystectomy
Cholecystectomy due to complicated
disease
Hysterectomy
Salpingo-oophorectomy
Bowel resection
Anterior resection
Abdominoperineal resection
Rectopexy
Appendectomy due to flegmonous
appendicitis
Appendectomy
Bariatric surgery
History of
Surgery, %
Female Sex, %
History of
Comorbidity, %
No.
% Lap
Open
Lap
Open
Lap
Open
Lap
Open
Lap
18 395
16 264
89
62
55 (17) a
62 (16) a
47 (15)
50 (16)
66 a
50 a
77
65
22 a
21 a
13
14
35 a
44 a
20
30
14 392
9319
14 486
3523
1183
275
18 803
1
30
2
2
1
24
17
56 (13) a
55 (15) a
68 (16) a
69 (13)
68 (12)
65 (18)
29 (18)
46 (8)
51 (12)
63 (16)
67 (12)
62 (17)
65 (20)
29 (14)
100
100
53
46
43
90
39 a
100
100
52
56
60
92
63
10 a
14
19
21
32
29
4c
22
13
23
29
40
24
5
51 b
44 a
54 a
50
51
44
10 a
61
34
42
49
60
52
14
9605
1896
12
35
36 (23) a
41 (10) c
32 (17)
40 (10)
48 a
78
66
76
7
21
8
18
25
34
23
38
Abbreviation: Lap, laparoscopic.
aP ⬍ .001.
bP ⬍ .01.
cP ⬍ .05.
Table 3. Frequency of Hospitalization or Surgery for SBO After Surgical Procedure
Hospitalized for SBO, %
Procedure
No.
Cholecystectomy
Cholecystectomy due to complicated disease
Hysterectomy
Salpingo-oophorectomy
Bowel resection
Anterior resection
Abdominoperineal resection
Rectopexy
Appendectomy due to flegmonous appendicitis
Appendectomy
Bariatric surgery
18 395
16 264
14 392
9319
14 486
3523
1183
275
18 803
9605
1896
% Lap
89
62
1
30
2
2
1
24
17
12
35
Open
1.1 a
1.6 a
3.3 c
3.8 a
6.7 b
10.2
14.1
7.2
0.4 b
1.9 b
2.9
Lap
0.3
0.3
0.5
0.5
1.6
9.5
0.0
1.5
0.1
0.8
3.9
Underwent Operation for SBO, %
OR
Open
0.3 b
3.8
5.5
7.2
7.8
4.4
1.1
0.5 a
1.0
1.2 a
2.0
2.8
3.9
4.8
0.2 c
0.8 c
1.3
5.0
4.3
2.4
0.7
Lap
OR
0.1
0.1
0.5
0.1
0.4
1.6
0.0
1.5
0.0
0.2
2.4
3.5
5.7
2.1
11.5
5.2
1.8
3.3
4.5
0.5
Abbreviations: Lap, laparoscopic; OR, odds ratio; SBO, small-bowel obstruction.
aP ⬍ .001.
bP ⬍ .01.
cP ⬍ .05.
females in the laparoscopic groups, especially for cholecystectomy and appendectomy. Previous abdominal surgery was more common in the open group for cholecystectomy, but the opposite was true for hysterectomy. There
were more patients with comorbidity in the open groups
for cholecystectomy, salpingo-oophorectomy, and bowel
resection, but fewer in the open group for hysterectomy
and appendectomy.
Except for bariatric surgery, there were no procedure groups that had a higher frequency of hospitalization for SBO in the laparoscopic group than in the open
group (Table 3).
An adjusted comparison between the 2 surgical techniques was performed as a multivariate analysis displayed in Table 4. The risk, calculated as an odds ratio,
was generally higher for the open technique with the exception of bariatric surgery. This was true especially for
cholecystectomy (odds ratio, 2.9), cholecystectomy for
complicated cholecystitis (4.0), salpingo-oophorectomy (7.6), bowel resection (4.9), and appendectomy due
to flegmonous appendicitis (4.5), where the odds ratio
for the surgical technique exceeded the odds ratio for all
other factors. Age was an important risk factor for SBO,
as were previous abdominal surgery and to some extent
comorbidity.
COMMENT
The aim of this study was to identify the incidence and
risk factors for mechanical SBO after a number of common abdominal and pelvic procedures. Small-bowel obstruction is a substantial health care challenge,8,9,25 and
correctly identified risk factors can provide improved tools
to reduce the risk of SBO after an abdominal surgical procedure. Of the possible factors to examine in a population-
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Table 4. Multivariate Analysis for the Risk of SBO in Relation to Age, Sex, History of Abdominal Surgery,
Presence of Comorbidity, and Surgical Technique
OR (95% CI)
Procedure
Age, y
Cholecystectomy
Cholecystectomy due to complicated
disease
Hysterectomy
Salpingo-oophorectomy
Bowel resection
Anterior resection
Abdominoperineal resection
Rectopexy
Appendectomy due to flegmonous
appendicitis
Appendectomy
Bariatric surgery
(1.0-2.8) a
Sex
Previous Surgery
Comorbidity
1.1 (0.6-1.8)
1.6 (1.1-2.2) a
2.1
1.9 (1.3-2.8) b
1.7
1.7 (1.2-2.5) b
2.9 (1.7-4.9)c
4.0 (2.6-6.2) c
5.6 (4.4-7.1) c
3.5 (2.6-4.7) c
0.5 (0.5-0.6) c
0.5 (0.4-0.7) c
0.7 (0.5-1.0) a
2.0 (0.7-5.8)
4.2 (2.2-7.9) c
0.9 (0.8-1.0)
1.3 (1.1-1.6) a
1.2 (0.8-1.7)
1.0 (0.8-1.2)
1.0 (0.8-1.3)
1.3 (1.1-1.5) c
0.8 (0.7-1.0)
1.0 (0.7-1.4)
2.2 (0.8-6.3)
1.6 (0.9-3.0)
4.3 (0.6-31.1)
7.6 (4.4-13.1) c
4.9 (1.8-13.1)b
1.1 (0.5-2.6)
1.2 (0.8-2.1)
1.5 (1.1-2.0) b
1.9 (1.4-2.6) c
1.4 (1.2-1.6) c
1.1 (0.9-1.5)
1.4 (1.0-2.0) a
0.7 (0.2-2.5)
2.4 (1.2-4.9) a
5.6 (0.7-43.3)
4.5 (1.4-14.3) a
1.7 (1.2-2.3) b
1.2 (0.7-2.1)
0.9 (0.7-1.3)
1.1 (0.6-2.1)
1.3 (0.8-2.1)
0.8 (0.4-1.6)
2.4 (1.7-3.2) c
0.9 (0.5-1.6)
2.2 (1.1-4.4) a
0.7 (0.4-1.2)
1.7
1.4 (1.0-2.2) a
(1.0-2.7) a
Open/Lap
(1.2-3.6) b
Abbreviations: Lap, laparoscopic; OR, odds ratio; SBO, small-bowel obstruction.
aP ⬍ .05.
bP ⬍ .01.
cP ⬍ .001.
based registry, our study identified the surgical technique, open vs laparoscopic, to be one of the more
important for the risk of SBO. Also, in contrast to several other risk factors, it is possible to influence the choice
of surgical technique.
The Swedish Inpatient Register provides an excellent
opportunity to provide information on factors important to consider in adhesion-related prevention. Even if
this study does not replace a properly performed controlled randomized trial, it includes a large number of
patients and is population based.22 The external validity
is high regarding surgical procedures,23 and there is no
reason to expect a biased reporting to the register dependent on any of the factors of interest. There is a risk
of identifying patients with other types of bowel obstruction using the ICD-10 codes,25 and this remains a risk unless each patient’s medical record is reviewed. We consider this risk to be equally distributed in all groups and
thus this should not influence the outcome of the analysis. It is possible that some port-site hernias causing SBO26
have been missed because of our exclusion of all registrations of SBO the first week after the index surgery; however, we also reduce the risk of including patients with
postoperative ileus, probably more common in the open
group.27
We identified age as a risk factor, but the results are
not similar for all groups. Younger patients operated on
for colorectal conditions had a higher risk of SBO, which
confirms previous results,10 but, in contrast, older patients undergoing a cholecystectomy or an appendectomy had a higher odds ratio for SBO. These findings are
in part new, indicating that risk factors may vary with
the type of procedure. It is probable that age as a risk factor requires further study before any clinical recommendation based on age can be developed.
Abdominal surgery before the index operation has been
considered a risk for SBO,10,11 and our results confirm this.
In the clinical setting, previous abdominal surgery has
often been regarded as a contraindication for laparos-
copy, although there are studies indicating that it is possible to perform laparoscopy in spite of previous abdominal surgery.28 The fact that previous abdominal surgery
is a risk factor for adhesive disease should perhaps prompt
a more liberal approach to laparoscopy in these patients
to possibly reduce further adhesive disorder, but caution must be taken to avoid complications due to already existing adhesions.29
It is problematic to define comorbidity, and our use of
secondary diagnoses as a definition of comorbidity at the
time of discharge must be considered a simplification.
There is a risk that the number of secondary diagnoses
has been registered incorrectly, because this registration is the basis of reimbursement, and studies indicate
that certain hospitals have added more secondary diagnoses to achieve better settlements.23 However, this is
probably performed systematically, and there is no reason to believe that this is performed differently because
of choice of surgical technique. In bivariate analysis as
well as in multivariate analysis, comorbidity was related
to the incidence of SBO in cholecystectomy, bowel resection, and appendectomy, but comorbidity was also related to whether open or laparoscopic surgery was performed. This suggests a possible confounding by
indication, although this must be further studied before
any conclusions can be made.
Some groups did not seem to benefit from laparoscopic surgery in the reduction of SBO. A previous large
study did not find an effect of laparoscopy on adhesive
morbidity compared with open surgery for patients undergoing hysterectomy,11 and our findings support these
results. One hypothesis is that this result may be related
to a limited dissection in the pelvis, but it is possible that
the small number of laparoscopic hysterectomy procedures in our study has affected our results, and we refrain from further conclusions.
In patients undergoing bariatric surgery, we found no
clear risk factors for SBO. However, interpretations should
be made with caution. Studies have shown that most SBO-
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related readmissions in patients who have had bariatric
surgery are due to internal obstruction after gastric bypass30 and not classic mechanical obstruction possibly related to adhesive disease. It is unfortunate that there is
no proper ICD-10 classification for this type of obstruction; many are probably classified as K56.6 or K56.7, making it difficult to distinguish patients with internal obstruction from other types of mechanical obstruction.
This study shows that, beyond important factors such
as age, previous abdominal surgery, and comorbidity, the
surgical technique is the most important factor related
to SBO. Compared with laparoscopic surgery, open surgery seems to increase the risk of SBO at least 4 times.
Of course, confounding by indication must be considered, which could affect the results. We have attempted
to address this with our separation of different types of
appendicitis and different indications for cholecystectomy, and although it may not be totally sufficient, we
believe that the present results certainly point in a clear
direction.
The fact that this study is population based and that the
group size is sufficiently large indicate that our results represent an actual difference due to surgical technique. The
safety20 and the short-term benefits of laparoscopy18,19 are
already known, and it is possible that laparoscopy should
be regarded as the preferred technique in an attempt to further reduce the complications of surgery.
Accepted for Publication: December 9, 2011.
Correspondence: Eva Angenete, MD, PhD, Department
¨ stra, 416
of Surgery, Sahlgrenska University Hospital/O
85 Gothenburg, Sweden ([email protected]).
Author Contributions: Drs Angenete, Gellerstedt, and
Haglind had full access to all the data in the study and
take responsibility for the integrity of the data and the
accuracy of the data analysis. Study concept and design:
Angenete, Gellerstedt, and Haglind. Acquisition of data:
Angenete, Jacobsson, Gellerstedt, and Haglind. Analysis
and interpretation of data: Angenete, Gellerstedt, and Haglind. Drafting of the manuscript: Angenete and Gellerstedt. Critical revision of the manuscript for important intellectual content: Angenete, Jacobsson, Gellerstedt, and
Haglind. Statistical analysis: Angenete, Jacobsson, Gellerstedt, and Haglind. Obtained funding: Angenete and
Haglind. Administrative, technical, and material support:
Angenete and Haglind. Study supervision: Gellerstedt.
Financial Disclosure: None reported.
Funding/Support: This project was supported by grant
CAN 2010/593 from the Swedish Cancer Foundation, grant
SLS96721 from the Swedish Medical Association, grant
GLS-93651 from the Gothenburg Medical Association,
grants FB09-44 and FB10-20 from the Assar Gabrielsson
Foundation, grants from the Magn Berwall’s Foundation,
and grant ALFGBG-136151 from the Swedish Research
Council funding clinical research in medicine.
Role of the Sponsors: None of the funding sources had
any role in the design and conduct of the study; the collection, management, analysis, and interpretation of the data;
or the preparation, review, or approval of the manuscript.
Previous Presentation: Parts of the results were presented at a Swedish Surgical Meeting; August 22, 2010;
Gothenburg, Kirurgveckan.
REFERENCES
1. Foster NM, McGory ML, Zingmond DS, Ko CY. Small bowel obstruction: a population-based appraisal. J Am Coll Surg. 2006;203(2):170-176.
2. Miller G, Boman J, Shrier I, Gordon PH. Etiology of small bowel obstruction. Am
J Surg. 2000;180(1):33-36.
3. Ellis H, Moran BJ, Thompson JN, et al. Adhesion-related hospital readmissions
after abdominal and pelvic surgery: a retrospective cohort study. Lancet. 1999;
353(9163):1476-1480.
4. Holmdahl L. Making and covering of surgical footprints. Lancet. 1999;353(9163):
1456-1457.
5. Weibel MA, Majno G. Peritoneal adhesions and their relation to abdominal surgery. A postmortem study. Am J Surg. 1973;126(3):345-353.
6. Sajja SB, Schein M. Early postoperative small bowel obstruction. Br J Surg. 2004;
91(6):683-691.
7. Parker MC, Wilson MS, Menzies D, et al; Surgical and Clinical Adhesions Research (SCAR) Group. Colorectal surgery: the risk and burden of adhesionrelated complications. Colorectal Dis. 2004;6(6):506-511.
8. Ivarsson ML, Holmdahl L, Franze´n G, Risberg B. Cost of bowel obstruction resulting from adhesions. Eur J Surg. 1997;163(9):679-684.
9. Ellis H, Crowe A. Medico-legal consequences of post-operative intra-abdominal
adhesions. Int J Surg. 2009;7(3):187-191.
10. Parker MC, Wilson MS, Menzies D, et al; Surgical and Clinical Adhesions Research (SCAR) Group. The SCAR-3 study: 5-year adhesion-related readmission
risk following lower abdominal surgical procedures. Colorectal Dis. 2005;7
(6):551-558.
11. Lower AM, Hawthorn RJ, Clark D, et al; Surgical and Clinical Research (SCAR)
Group. Adhesion-related readmissions following gynaecological laparoscopy or
laparotomy in Scotland: an epidemiological study of 24 046 patients. Hum Reprod.
2004;19(8):1877-1885.
12. Schnu¨riger B, Barmparas G, Branco BC, Lustenberger T, Inaba K, Demetriades
D. Prevention of postoperative peritoneal adhesions: a review of the literature.
Am J Surg. 2011;201(1):111-121.
13. Gutt CN, Oniu T, Schemmer P, Mehrabi A, Bu¨chler MW. Fewer adhesions induced by laparoscopic surgery? Surg Endosc. 2004;18(6):898-906.
14. Dowson HM, Bong JJ, Lovell DP, Worthington TR, Karanjia ND, Rockall TA.
Reduced adhesion formation following laparoscopic versus open colorectal surgery.
Br J Surg. 2008;95(7):909-914.
15. Taylor GW, Jayne DG, Brown SR, et al. Adhesions and incisional hernias following laparoscopic versus open surgery for colorectal cancer in the CLASICC trial.
Br J Surg. 2010;97(1):70-78.
16. Duron JJ, Hay JM, Msika S, et al; French Association for Surgical Research.
Prevalence and mechanisms of small intestinal obstruction following laparoscopic abdominal surgery: a retrospective multicenter study. Arch Surg. 2000;
135(2):208-212.
17. Scho¨lin J, Buunen M, Hop W, et al. Bowel obstruction after laparoscopic and
open colon resection for cancer: results of 5 years of follow-up in a randomized
trial. Surg Endosc. 2011;25(12):3755-3760.
18. Kennedy GD, Heise C, Rajamanickam V, Harms B, Foley EF. Laparoscopy decreases postoperative complication rates after abdominal colectomy: results from
the national surgical quality improvement program. Ann Surg. 2009;249(4):
596-601.
19. Janson M, Lindholm E, Anderberg B, Haglind E. Randomized trial of healthrelated quality of life after open and laparoscopic surgery for colon cancer. Surg
Endosc. 2007;21(5):747-753.
20. Buunen M, Veldkamp R, Hop WC, et al; Colon Cancer Laparoscopic or Open Resection Study Group. Survival after laparoscopic surgery versus open surgery
for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol.
2009;10(1):44-52.
21. Janson M, Bjo¨rholt I, Carlsson P, et al. Randomized clinical trial of the costs of
open and laparoscopic surgery for colonic cancer. Br J Surg. 2004;91(4):409417.
22. The National Board of Health and Welfare, Sweden. Kodningskvalitet i patientregistret—Slutenva˚rd 2008 [Coding Quality in Patient Register—Inpatient 2008]
[in Swedish]. http://www.socialstyrelsen.se/publikationer2010/2010-6-27. Accessed January 23, 2012.
23. Ludvigsson JF, Andersson E, Ekbom A, et al. External review and validation of
the Swedish national inpatient register. BMC Public Health. 2011;11(1):450. doi:
10.1186/1471-2458-11-450.
24. Duron JJ, Silva NJ, du Montcel ST, et al. Adhesive postoperative small bowel
obstruction: incidence and risk factors of recurrence after surgical treatment: a
multicenter prospective study. Ann Surg. 2006;244(5):750-757.
25. Menzies D, Parker M, Hoare R, Knight A. Small bowel obstruction due to postoperative adhesions: treatment patterns and associated costs in 110 hospital
admissions. Ann R Coll Surg Engl. 2001;83(1):40-46.
ARCH SURG/ VOL 147 (NO. 4), APR 2012
364
WWW.ARCHSURG.COM
Downloaded from www.archsurg.com at EIRA, on April 17, 2012
©2012 American Medical Association. All rights reserved.
26. Owens M, Barry M, Janjua AZ, Winter DC. A systematic review of laparoscopic port site hernias in gastrointestinal surgery. Surgeon. 2011;9(4):218224.
27. Veldkamp R, Kuhry E, Hop WC, et al; COlon cancer Laparoscopic or Open Resection Study Group (COLOR). Laparoscopic surgery versus open surgery for
colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;
6(7):477-484.
28. Tang B, Cuschieri A. Conversions during laparoscopic cholecystectomy: risk fac-
tors and effects on patient outcome. J Gastrointest Surg. 2006;10(7):10811091.
29. Van Der Krabben AA, Dijkstra FR, Nieuwenhuijzen M, Reijnen MM, Schaapveld
M, Van Goor H. Morbidity and mortality of inadvertent enterotomy during
adhesiotomy. Br J Surg. 2000;87(4):467-471.
30. Tucker ON, Escalante-Tattersfield T, Szomstein S, Rosenthal RJ. The ABC System: a simplified classification system for small bowel obstruction after laparoscopic Roux-en-Y gastric bypass. Obes Surg. 2007;17(12):1549-1554.
INVITED CRITIQUE
Minimal Invasion and Maximal Benefit
T
he short-term benefits of laparoscopy have been
well documented over the past 20 years: less postoperative pain, quicker return to baseline function, and shorter hospital stays. This study by Angenete
and colleagues1 suggests that the benefits of laparoscopy may extend beyond the immediate postoperative
period. Using a robust national database of more than
100 000 patients who were followed up for up to 5 years
or until death, the authors found that laparoscopy correlated highly with a reduced incidence of postoperative small-bowel obstruction (SBO) compared with open
surgery. This relationship held true for numerous commonly performed procedures including cholecystectomy, hysterectomy, oophorectomy, bowel resection, rectopexy, and appendectomy. The reduction in SBO
incidence remained for each of these procedures even after accounting for patient factors such as age, comorbidity, and previous surgery.
This finding adds to the body of literature suggesting
that laparoscopy decreases the incidence of adhesionrelated readmissions2 and has important implications for
both the quality and cost of surgical care. For patients,
who typically face up to a 1-in-3 chance that they will
be readmitted for management of adhesive-related disease within 10 years of open abdominal surgery,3 it offers an opportunity for improved quality of life and decreased morbidity. For surgeons, it highlights another
potential benefit of minimally invasive surgery and challenges us to continue to offer less invasive procedures
whenever they are feasible. For payers and health care
policy leaders, it suggests that substantial cost savings
could be achieved if open surgery were replaced with laparoscopic surgery more often. Given that inpatient expenditures on adhesiolysis-related complications ex-
ceed $2 billion annually in the United States,4 these savings
could be substantial.
One issue that has yet to be addressed is the way that
newer payment models, such as bundled or episodebased payments, would account for the higher initial cost
of laparoscopy but lower long-term cost related to shorter
hospitalizations, lower wound complication rates, fewer
readmissions, and fewer reoperations. Despite this unknown, Angenete and colleagues1 have provided strong
evidence that minimal invasion often results in maximal benefit.
Luke M. Funk, MD, MPH
Stanley W. Ashley, MD
Author Affiliations: Department of General Surgery,
Brigham and Women’s Hospital, Harvard Medical School,
Boston, Massachusetts.
Correspondence: Dr Ashley, Department of General Surgery, ASBII-3, Brigham and Women’s Hospital, Harvard
Medical School, 75 Francis St, Boston, MA 02115 (sashley
@partners.org).
Financial Disclosure: None reported.
1. Angenete E, Jacobsson A, Gellerstedt M, Haglind E. Effect of laparoscopy on
the risk of small-bowel obstruction: a population-based register study. Arch
Surg. 2012;147(4):359-365.
2. Schnu¨riger B, Barmparas G, Branco BC, Lustenberger T, Inaba K, Demetriades D. Prevention of postoperative peritoneal adhesions: a review of the
literature. Am J Surg. 2011;201(1):111-121.
3. Ellis H, Moran BJ, Thompson JN, et al. Adhesion-related hospital readmissions after abdominal and pelvic surgery: a retrospective cohort study. Lancet.
1999;353(9163):1476-1480.
4. Sikirica V, Bapat B, Candrilli SD, Davis KL, Wilson M, Johns A. The inpatient
burden of abdominal and gynecological adhesiolysis in the US. BMC Surg. 2011;
11:13. doi:10.1186/1471-2482-11-13.
ARCH SURG/ VOL 147 (NO. 4), APR 2012
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WWW.ARCHSURG.COM
Downloaded from www.archsurg.com at EIRA, on April 17, 2012
©2012 American Medical Association. All rights reserved.