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SYSTEMATIC REVIEW AND META ANALYSIS

Laparoscopic Surgery Compared With Open Surgery Decreases


Surgical Site Infection in Obese Patients
A Systematic Review and Meta-Analysis
Daniel M. Shabanzadeh, MD and Lars T. Sørensen, MD

surgery has proven to have fewer postoperative complications and


Objective: To compare surgical site infections rate in obese patients after
a shorter length of in-hospital stay and postoperative convalescence
laparoscopic surgery with open general abdominal surgery.
compared with open procedures.15–22
Background: In mixed surgical populations, surgical site infections are fewer
Although laparoscopic surgery does not seem to change the
in laparoscopic surgery than in open surgery. It is not clear if this is also the
fact that the incidence of surgical site infection in obese patients re-
case for obese patients, who have a higher risk of surgical site infections than
mains higher than in nonobese patients,23,24 several authors have sug-
nonobese patients.
gested that obese patients may benefit from laparoscopic surgery in a
Methods: MEDLINE, Embase, and The Cochrane library (CENTRAL) were
similar way as nonobese patients.18,25–29 The objective of this system-
searched systematically for studies on laparoscopic surgery compared with
atic review is to assess the impact of laparoscopic versus open general
open abdominal surgery. Randomized controlled trials (RCTs) and observa-
surgical procedures on surgical site infections in obese patients.
tional studies reporting surgical site infection in groups of obese patients
(body mass index ≥ 30) were included. Separate meta-analyses with a fixed
effects model for RCTs and a random effects model for observational studies METHODS
were performed. Methodological quality of the included studies was assessed The process of the systematic review and meta-analysis
according to the Cochrane method and the Newcastle-Ottawa Scale. was performed according to the Cochrane Collaboration
Results: Eight RCTs and 36 observational studies on bariatric and non- recommendations.30 A detailed protocol was produced in advance of
bariatric surgery were identified. Meta-analyses of RCTs and observational data collection describing the process of the systematic review. This
studies showed a significantly lower surgical site infection rate after laparo- embraced a number of prespecified criteria for inclusion of studies
scopic surgery (OR = 0.19; 95% CI [0.08-0.45]; P = 0.0002 and OR = 0.33; and reporting of results according to the MOOSE (Meta-analysis
95% CI [0.26-0.42]; P = 0.00001). Sensitivity analyses to assess the impact Of Observational Studies in Epidemiology) and PRISMA (Pre-
of selection and detection bias confirmed the significant estimates with ac- ferred Reporting Items for Systematic Reviews and Meta-Analyses)
ceptable heterogeneity. No publication bias was present for the observational recommendations.31,32
studies.
Conclusions: Laparoscopic surgery in obese patients reduces surgical site Search Strategy
infection rate by 70%–80% compared with open surgery across general ab- We systematically searched MEDLINE, Embase, and The
dominal surgical procedures. Future efforts should be focused on further Cochrane Library (including CENTRAL). The search strategy was
development of laparoscopic surgery for the growing obese population. produced by the authors under the supervision of a specialized trial
Keywords: BMI, laparoscopic surgery, obesity, surgical site infection,
search coordinator from the Cochrane Colorectal Cancer Group.
systematic review
The following index terms were included: laparoscopy, laparotomy,
body mass index (BMI), obesity, morbid obesity, bariatric, postoper-
(Ann Surg 2012;256: 934–945) ative complications, wound/surgical/postoperative infection, surgical
wound infection, wound complication, fistula, and abscess. All index
terms were exploded. Free text words were searched using index terms

I n general surgery, most studies have found obesity to be an indepen-


dent risk factor for surgical site infection.1–5 Surgical site infection
is the third most prevalent hospital acquired infection accounting for
and additional relevant words in combination with asterisks: open,
conventional, complications, SSI, postoperative/wound morbidity,
wound sepsis, and superficial/deep/organ/space/visceral/skin/soft tis-
approximately 30%.6 Considering that obesity is a growing world- sue/subcutis/site/tissue/mesh infection. No limitations or restrictions
wide epidemic with a prevalence over 30% in populations in Europe such as publication year or filters for study design were used in the
and the United States,7,8 the relative significance of surgical site infec- search strategy. The date of the most recent search was May 4, 2011.
tion for postoperative mortality and morbidity seems only to increase Ovid was used for searches, and the computer program ProCite5 was
in the future.9–14 used for managing references. Additional searches were performed
Today, laparoscopic surgery has become the primary choice of by hand-searching reference lists of included studies. The full search
most general surgical procedures. In nonobese patients, laparoscopic strategies are outlined in the Supplemental Digital Content Figure 1
(available at http://links.lww.com/SLA/A281).

From the Department of Surgery K, Bispebjerg Hospital, Copenhagen, Denmark. Study Selection and Data Extraction
Disclosure: No funding contributed to the production of this review.
Supplemental digital content is available for this article. Direct URL citations
For the selection of studies, first titles and abstracts were eval-
appear in the printed text and are provided in the HTML and PDF versions of uated. Subsequently, full-text articles were obtained to assess study
this article on the journal’s Web site (www.annalsofsurgery.com). eligibility. Conference proceedings and abstracts were included if rel-
Reprints: Daniel M. Shabanzadeh, MD, Department of Surgery K, Bispebjerg evant data could be retrieved. Both authors conducted the searches
Bakke 23, 2400 Copenhagen, Denmark. E-mail: dmshaban@gmail.com.
Copyright C 2012 by Lippincott Williams & Wilkins
and identification of studies independently. Inconsistencies were re-
ISSN: 0003-4932/12/25606-0934 solved by discussion. Articles written in English, German, Dutch,
DOI: 10.1097/SLA.0b013e318269a46b and Scandinavian languages were retrieved.

934 | www.annalsofsurgery.com Annals of Surgery r Volume 256, Number 6, December 2012

Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Annals of Surgery r Volume 256, Number 6, December 2012 Laparoscopic Versus Open Surgery in Obese Patients

FIGURE 1. Study flow diagram.

Data were extracted from each study to preformatted tables by 2. A specified general surgical laparoscopic operation and an open
the primary author of this systematic review. Inadequate data were comparator operation.
resolved by contacting the authors of studies. According to the pro- 3. Surgical site infection or wound infection defined as the presence
tocol, the extracted data were the following: first author, year of pub- of pus11 or as a superficial, deep, or organ/space infection during
lication, study design [randomized controlled trial (RCT), retrospec- the first 30 postoperative days according to the criteria of the Center
tive/prospective data collection], BMI in each group/ICD (Interna- for Disease Control (CDC),34 reported in such a way that data on
tional Classification of Disease) diagnosis of obesity/other measures obese patients in each treatment group could be extracted.
of obesity, definition of surgical site infection, number of patients in
each group, number of patients with surgical site infection in each Quality Scoring and Risk of Bias Assessment
group, and postoperative follow-up for surgical site infection or post- Risk of bias assessment in RCTs was performed according
operative complications. to Cochrane methodology under consideration of random sequence
generation, allocation concealment, blinding of participants and per-
Inclusion Criteria sonnel, blinding of outcome assessment, incomplete outcome data,
and selective reporting.35 Each category was scored as low, unclear
Observational studies and RCTs complying with all the fol-
or high risk of bias and expressed in a summary table with a plus,
lowing criteria were included:
question mark and minus, respectively.
1. Inclusion of obese patients defined as having a BMI ≥ 30 or an The Newcastle-Ottawa Quality Assessment Scale (NOS) for
ICD diagnosis of obesity or morbid obesity.33 Other measures of cohort studies36 was used for quality assessment of observational
obesity were accepted if a body weight was included. studies. This score assesses studies according to selection of patients


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Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Shabanzadeh and Sørensen

TABLE 1. Characteristics of RCTs


Study (Author Obesity Patients Lap./ Surgical Criteria Follow-Up

936 | www.annalsofsurgery.com
and Year) Category n Open n Procedure Outcome for SSI for SSI Attrition ITT/AT Conversion Results
Bariatric surgery
Azagra et al, 1999 BMI = 43 (37–66) 68 30/38 VBG WI N.R. Once a month 0% AT 4 L 1/30; O 4/38;
(Belgium)40 P = 0.04
De Wit et al, 1999 BMI = 51.3 50 25/25 AGB Wound abscess N.R. N.R. 0% ITT 2 L 0/25, O 1/25
(The (10.4)/49.7 (5.6);
Netherlands)41 NS
Luján et al, 2004 BMI = 48.5 104 53/51 RYGBP WI, subphrenic N.R. 15 days and after 0% N.R. 4 WI: L 0/53,
(Spain)42 (36–78)/52.2 abscess 3 months O 4/51; SA:
(37–80); NS L 0/53, O 4/51
Nguyen et al, 2001 BMI = 47.6 155 79/76 RYGBP WI Erythema/purulent 1 month 0% ITT 2 L 1/79, O 8/76
(US)4 (4.7)/48.4 (5.4); NS discharge
Sundbom and BMI = 44 (36–54)/45 50 25/25 RYGBP WI Purulent discharge 1 month 0% AT 0 HALS 1/25,
Gustavsson, 2004 (34–54) O 1/25
(Sweden)44
van Dielen et al, BMI = 46.7 100 50/50 LAGB vs. open WI N.R. No postdischarge 0% ITT 3 LAGB 0/50, VBG
2005 (The (6.1)/46.6 (6.4); NS VBG follow-up 1/50
Netherlands)45 before 3 months
Westling and BMI = 41 (4)/44 (4); 51 30/21 RYGBP Minor WI N.R. After 4–6 weeks ITT 7 L 0/30, O 3/21
Gustavsson, 2001 P < 0.05
(Sweden)46
Appendectomy
Clarke et al, 2011 BMI > 30 37 23/14 Appendectomy WI, wound Redness and drainage After 2 weeks N.R. ITT N.R. WI: L 2/23, O
(US)47 drainage from the wound 1/14; Drainage:
requiring opening L 0/23, O 1/14
of the skin incision


AGB indicates adjustable gastric banding; AT, as treated analysis; HALS, hand-assisted laparoscopic surgery; ITT, intention to treat; LAGB, laparoscopic adjustable gastric banding; Lap. or L., laparoscopic; N.R., not reported;
NS, not significant; O, open; RYGBP, Roux-en-Y gastric bypass; SSI, surgical site infections; VBG, vertical banded gastroplasty; WI, wound infection.

Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
C 2012 Lippincott Williams & Wilkins
Annals of Surgery r Volume 256, Number 6, December 2012

TABLE 2. Characteristics of Observational Studies
Study (Author Lap./Open Surgical Criteria Follow-Up
and Year) Design NOS Obesity Category Patients n n Procedure Outcome for SSI for SSI Attrition ITT/AT Conversion Results

Bariatric surgery
Agaba et al, 2008 Retrospective ∗∗∗∗∗∗ BMI = 46.2 1367 806/561 RYGBP WI N.R. 1 week 0% N.R. 18 L 2/806; O 5/561
(US)48 (4.7)/47.6
(5.7)
Campos et al, 2007 Prospective ∗∗∗∗∗∗ BMI = 46.4 404 332/72 RYGBP WI N.R. 2 weeks N.R. AT 11 L 1/332; O 3/72
(US)49 (42.4–
52.4)/57.4
(49.6–67);
P < 0.001
Coskun et al, 2003 Retrospective ∗∗∗ BMI = 45.2 70 35/35 AGB WI N.R. N.R. N.R. N.R. N.R. L 0/35; O 10/35

C 2012 Lippincott Williams & Wilkins


(Turkey)50
Courcoulas et al, Retrospective ∗∗∗∗ BMI = 35–67 160 80/80 RYGBP Wound/port N.R. N.R. N.R. AT 0 L 3/80; O 9/80
2003 (US)51 infection
Dolan et al, 2004 Retrospective ∗∗∗∗∗ BMI = 56.9 23 35/11 Biliopancreatic WI N.R. N.R. N.R. AT 0 L 2/35; O 3/11
(Australia)52 case- (50.8–83.7)/ diversion and
matched 55.9 LAGB
(50.7–90.6);
P = 0.89
Ezri et al, 2004 Retrospective ∗∗∗∗∗ BMI = 42.3 234 167/67 Restrictive WI N.R. 30 days N.R. ITT 3 L 0/167; O 3/167
(Israel)53 (5.3)/42.2 bariatric
(5.7); surgery (no
Annals of Surgery r Volume 256, Number 6, December 2012

P = 0.86 gastric
bypass)
Gartner et al, 2008 Retrospective ∗∗∗∗ BMI = 47.8 662 231/431 VBG, RYGBP, WI N.R. N.R. N.R. N.R. N.R. L 9/231; O 42/431
(Germany)54 (7.9)/46.5 gastric
(7.6); P < banding
0.005
Gonzalez et al, Prospective ∗∗∗∗∗ BMI = 38– 300 164/136 RYGBP WI N.R. N.R. N.R. N.R. 3 L 5/164; O 17/136
2006 (US)55 database 64/39–94
Gorman et al, 2006 Prospective ∗∗∗∗∗ BMI > 35 22 3/19 RYGBP WI N.R. N.R. N.R. AT N.R. L 0/3; O 2/19
(US)56
Hutter et al, 2006 Prospective ∗∗∗∗∗∗∗ BMI = 47.5 1356 401/955 RYGBP Deep WI NSQIP 30 days 0% N.R. N.R. L 1/401; O 8/955
(US)57 database (43–51)/ (CDC)
(NSQIP) 50.5
(44–55);
P < 0.0001
Lancaster and Prospective ∗∗∗∗∗∗∗ BMI = 47.9 5777 4631 + RYGBP, VGB, Sup. WI, deep NSQIP 30 days 0% N.R. N.R. Sup.: L 2.3%; O
Hutter, 2008 database (8.3)/50.5 3580/ and other Lap. WI, organ (CDC) 5.2%; Deep: L
(US)58 (NSQIP) (10.1); P < 1146 WI 0.2%; O: 1.1%;
0.001 Org.: L 0.6%; O
1.6%; Numbers
for 2006
LRYGB: Sup.:
2.3% of 3580;
Deep: 0.2%;
Org.: 0.5%;

Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
LAGB: Sup.:
1.4%; Deep:
0.1%; Org.:
0.1%
(Continued)

www.annalsofsurgery.com | 937
Laparoscopic Versus Open Surgery in Obese Patients
TABLE 2. (Continued)
Study (Author Lap./Open Surgical Criteria Follow-Up
and Year) Design NOS Obesity Category Patients n n Procedure Outcome for SSI for SSI Attrition ITT/AT Conversion Results

Lindsey et al, 2009 Prospective ∗∗∗∗∗ BMI > 35 5921 6404/ RYGBP, LAGB Abscess N.R. N.R. N.R. N.R. N.R. L 6/3912, O
(US,)59 database 2009 5/2009; LAGB:
3/2492
Livingston Prospective ∗∗∗∗∗∗∗ BMI = 47.4 575 73/502 Bariatric Sup. WI, deep NSQIP 30 days 0% N.R. N.R. Sup.: L 0/73, O
et al, 2006 (US)60 database (7)/49.9 procedures WI (CDC) 11/502; Deep:
Shabanzadeh and Sørensen

(NSQIP) (8.4); L 0/73, O 1/502


P = 0.013
Marema et al, 2005 Retrospective ∗∗∗∗∗ BMI = 47.9 2275 1077/ RYGBP WI N.R. 1 year N.R. N.R. 28 L 6.1%; O 12.2%
(US)61 (0.53)/52 1198

938 | www.annalsofsurgery.com
(0.40);
P < 0.01
Miller et al, 2002 Prospective ∗∗∗∗∗ BMI = 46.9 1011 448/563 Lap. AGB and WI N.R. N.R. N.R. N.R. 3 L 0/448; O 19/563
(Germany)62 (7.8)/46.9 open VBG
(9.9); P =
0.57
Nguyen et al, 2000 Retrospective ∗∗∗∗∗ BMI = 51 70 35/35 RYGBP WI (severe and N.R. No N.R. AT 0 Sev. WI: L 0/35, O
(US)63 case- (40–60)/48 minor) follow– 2/35; Min. WI:
matched (41–60); NS up L 1/35, O 1/35
Nguyen, 2007 Prospective ∗∗∗∗∗ ICD-9 codes 22,422 16,357/ RYGBP WI N.R. No N.R. N.R. N.R. L 0.5%; O 2.3%
(US)64 database for obe- 6065 follow-
sity/morbid up
obesity
O’Brien et al, 1999 Prospective ∗∗∗∗∗∗∗ BMI = 44.5 302 277/25 AGB Infected N.R. 4 weeks 0% AT 5 L 1/277; O 4/25
(Australia)65 database (6) reservoir site
See et al, 2002 Prospective ∗∗∗∗∗ BMI = 41.8 72 20/52 RYGBP Intraabdominal N.R. N.R. N.R. N.R. N.R. L 4/20; O 0/52
(US)66 (35–49)/ abscess
46.7
(37–66);
P < 0.001
Sekhar et al, 2007 Prospective ∗∗∗∗∗ BMI = 58.9 967 568/399 RYGBP WI N.R. N.R. N.R. N.R. 10 L 1.7%; O 9.2%
(US)67 database (10.6)/49.1
(7.6); P =
0.001
Smith et al, 2004 Retrospective ∗∗∗∗∗∗ BMI = 46.7 656 328/328 RYGBP WI, subphrenic N.R. 2nd + 0% N.R. N.R. WI: L 4/328, O
(US)68 (35–62)/ abscess 6th 28/328; SA: L
49.5 week 1/328, O 1/328


(35–83)
Suter et al, 1999 Retrospective ∗∗∗∗∗ BMI = 273 76/197 Lap. AGB and WI N.R. 30 days N.R. N.R. 8 L 0/76; O 15/197
(Switzerland)69 45.5/42.7 open VBG
(37–64); P
< 0.01
Tevis et al, 2011 Prospective ∗∗∗∗∗∗ BMI = 25 4/21 RYGBP WI, intraab- N.R. N.R. N.R. AT 0 WI: L 0/4, O 4/21;
(US)70 database 43.9/42.9; P dominal IA: L 0/4, O
= 0.6 abscess, 1/21; FD: L 0/4,
fascia O 1/21

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dehiscence
van Doesburg et al, Retrospective ∗∗∗∗∗∗ BMI = 49.5 290 57/233 RYGBP WI, intraab- N.R. 30 days 0% N.R. N.R. WI and IA: L
2010 (The (33.2–84.9) dominal 0/57; O 16/233
Netherlands)71 abscess
(Continued)

C 2012 Lippincott Williams & Wilkins


Annals of Surgery r Volume 256, Number 6, December 2012

TABLE 2. (Continued)
Study (Author Lap./Open Surgical Criteria Follow-Up
and Year) Design NOS Obesity Category Patients n n Procedure Outcome for SSI for SSI Attrition ITT/AT Conversion Results

Weingarten et al, 2011 Retrospective ∗∗∗∗ BMI = 49.5 797 355/442 Bariatric WI N.R. N.R. N.R. N.R. N.R. L 14/355; O
(US)72 (9.4) procedures 52/442
Westling et al, 1998 Retrospective ∗∗∗∗∗∗ BMI = 43 90 47/43 AGB WI N.R. 4 weeks 0% AT 16 L 0/47; O 4/43
(Sweden)73 (34–57)
Hernia
Ballem et al, 2008 Retrospective ∗∗∗∗∗∗ BMI = 31.9 331 199/192 Ventral hernia WI Based on Initial N.R. ITT 20 L 7.5%; O 9%
(US)74 (1.2); NS repair CDC follow-
up by

C 2012 Lippincott Williams & Wilkins


surgeon
Cholecystectomy
Koperna et al, 1999 Retrospective ∗∗∗∗ BMI > 30 30 15/15 Cholecystec WI N.R. N.R. N.R. AT N.R. L 0/15; O 5/15
(Austria)75 case- (subgroup) tomy
matched
Miles et al, 1992 Retrospective ∗∗∗∗∗ Morbidly 32 21/11 Cholecystec WI N.R. N.R. N.R. AT 0 L 0/21; O 1/11
(US)76 case- obese = tomy
matched 100 pounds
over ideal
body weight
Nicholson Prospective ∗∗∗∗∗∗∗ BMI > 30 63 33/30 Cholecystec WI N.R. N.R. N.R. AT 8 L 1/33; O 2/30
et al, 1995 (UK)77 (subgroup) tomy
Annals of Surgery r Volume 256, Number 6, December 2012

Paajanen et al, 2011 Retrospective ∗∗∗∗ BMI > 30 82 42/40 Cholecystec SSI N.R. N.R. N.R. ITT 16 L 2/42; O 3/40
(Finland)38 diabetic tomy
patients
Appendectomy
Corneille Retrospective ∗∗∗∗ BMI > 30 116 73/43 Appendectomy WI (require in- N.R. N.R. N.R. AT 12 WI: L 0/73, O
et al, 2007 (US)78 tervention), 3/43; IA: L
intraabdom- 5/73, O 5/43
inal
abscess
Varela et al, 2008 Prospective ∗∗∗∗∗ ICD-9 code 1943 906/1037 Appendectomy WI N.R. No follow- N.R. N.R. N.R. L 1/906; O 3/1037
(US)79 database for morbid for acute/ up
obesity perforated
appendicitis
Colorectal resection
Delaney et al, 2005 Prospective ∗∗∗∗∗∗ BMI = 33.3 188 94/94 Colorectal WI, Intraab- N.R. N.R. N.R. ITT 28 WI: L 8/94, O
(US)80 database, (3.7)/33.8 resections dominal 8/94; IA: L
case- (4.5); P = abscess 2/94, O 2/94
matched 0.38
Wick et al, 2011 Retrospective ∗∗∗∗ BMI > 35 or 1243 204/1039 Colorectal ICD-9 codes Based on N.R. N.R. N.R. N.R. L 15/204;
(US)39 ICD-9 code resections for SSI CDC O 116/1039
obesity (sup., deep,
organ)
General surgery
Dindo et al, 2003 Prospective ∗∗∗∗∗ BMI = 34.9 808 377/431 Elective general SSI N.R. N.R. N.R. N.R. N.R. L 8/377; O 17/431

Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
(Switzerland)81 (6) surgery
AGB indicates adjustable gastric banding; AT, as treated analysis; ITT, intention to treat; LAGB, laparoscopic adjustable gastric banding; Lap. or L., laparoscopic; N.R., not reported; NS, not significant; NSQIP, National
Surgical Quality Improvement Program; O, open; RYGBP, Roux-en-Y gastric bypass; SSI, surgical site infections; Sup., superficial; VBG, vertical banded gastroplasty; WI, wound infection.

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Laparoscopic Versus Open Surgery in Obese Patients
Shabanzadeh and Sørensen Annals of Surgery r Volume 256, Number 6, December 2012

in the exposed and in the nonexposed group, comparability of the Quality Assessment
2 groups, and outcome of the single studies. A study can obtain 0– The most apparent methodological flaw in the RCTs was the
9 stars based on these criteria. A threshold of 6 stars or above has missing description of blinded outcome assessment and criteria for
been considered as indicative for high quality in other meta-analyses diagnosis of surgical site infection. Accordingly, all RCTs had an
and was chosen as well for this review.35 Inspection of funnel plots unclear risk of detection bias. Six RCTs had no adequate descrip-
based on meta-analyses, including more than 10 studies, was used for tion of allocation concealment and 4 RCTs had comparable BMIs in
assessment of publication bias.30 the intervention and control groups, introducing an unclear risk of
selection bias. Risk of attrition bias was not present across studies.
Statistical Analysis The overall risk of all types of bias in the RCTs was generally low to
Meta-analyses of RCTs and observational studies were per- unclear (Fig. 2).
formed separately in all analyses by the use of Review Manager In the observational studies, the clinical heterogeneity was
5.1. Separate meta-analysis was performed for bariatric surgery and considerable. The most typical methodological flaw was a risk of se-
nonbariatric surgery and across both subgroups. In all analyses, the lection bias. None of the studies had confounder control for surgical
outcomes of surgical site infection were calculated as odds ratios site infection outcome and many studies (30/36) had significant dif-
(ORs) with 95% confidence intervals (CIs). For pooled estimates, the ferences in BMI between groups. Attrition bias was present because
Mantel-Haenszel χ 2 method was used. Statistical heterogeneity for of inadequate reporting on postdischarge follow-up (29/36). Detec-
the pooled OR was calculated as I2 with a Z-statistic test for overall tion bias was present because of inadequate reporting on surgical site
effect. The fixed effects model was applied for the meta-analyses of infection definition (33/36) and inadequate reporting on time point
the RCTs in the case of I2 < 40%. The random effects model was for postdischarge follow-up (24/36). About half of the studies had ret-
used for the meta-analyses of observational studies irrespective of rospective data collection (19/36). Reporting bias was considerable
I2 value because of a considerable clinical heterogeneity in different and was aimed to be eliminated through sensitivity analyses. Risk
surgical procedures and study designs.37 of language bias was present as 10 bariatric observational studies
Sensitivity analysis was performed to test the validity of the were excluded because of language restriction. The latter, however,
meta-analyses under consideration of the identified bias. In addition, 2 is unlikely to have changed the pooled estimates of the observational
sensitivity analyses were performed for the observational studies. The studies because the findings were reproducible across bariatric and
first one only included studies with a NOS score of 6 stars or above, nonbariatric surgery for both RCTs and observational studies. Thir-
whereas the second one assumed converted laparoscopy operations teen observational studies across surgical procedures had a NOS score
as open operations in the analysis. In all analyses, a threshold of P < of 6 stars or above (Table 2).
0.05 for overall effect was considered statistically significant. There were not adequate numbers of RCTs to assess publi-
cation bias. A funnel plot of observational studies was symmetrical
RESULTS and thereby no publication bias was present (Supplemental Digital
The electronic searches yielded 2974 records. Additional 6 Content Figure 2, available at http://links.lww.com/SLA/A281).
records were found through hand-search (Fig. 1). The authors of
1 article and 1 conference abstract provided unpublished data that Surgical Site Infection in Obese Patients
were included in the analysis.38,39 Two observational studies had zero Across surgical procedures, the meta-analysis of RCTs dis-
events of surgical site infection and were, therefore, excluded during closed significantly fewer surgical site infections after laparoscopic
analysis.30

Characteristics of RCTs
Eight RCTs published between 1999 and 2011 were included.
They originate from the United States, Sweden, The Netherlands,
Belgium, and Spain.40–47 A total of 615 obese patients with BMI
≥ 30 randomized to laparoscopic and open surgery were included.
Seven of the RCTs studied bariatric surgery,40–46 and 1 RCT com-
prised a subgroup analysis of the obese patients included in a RCT of
appendectomy.47 Four of the RCTs reported a nonsignificant dif-
ference in BMI between the intervention and the control group
(Table 1).

Characteristics of Observational Studies


Thirty-six prospective and retrospective observational stud-
ies were included in the meta-analysis. The studies were published
between 1992 and 2011 and originated from the United States, Aus-
tria, England, Finland, Germany, The Netherlands, Sweden, Switzer-
land, Turkey, Australia, and Israel. The total number of obese pa-
tients with BMI ≥ 30 included was 58,755. The studies included
patients who had undergone bariatric surgery,48–73 hernia surgery,74
cholecystectomy,38,75–77 appendectomy,78,79 colorectal resection,39,80
and pooled general surgery.81 Studies on colorectal and general
surgery included patients with cancer, adenomas, inflammatory bowel
disease, and diverticulitis. Seven observational studies reported a non-
significant difference in BMI between the intervention and the control
group (Table 2). FIGURE 2. Risk of bias in RCTs.

940 | www.annalsofsurgery.com 
C 2012 Lippincott Williams & Wilkins

Copyright © 2012 Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Annals of Surgery r Volume 256, Number 6, December 2012 Laparoscopic Versus Open Surgery in Obese Patients

FIGURE 3. Meta-analysis of RCTs.

TABLE 3. Laparoscopy Versus Open Surgery: Development of Surgical Site Infection in RCTs
Number of Number of
Analysis Studies OR Fixed Effect 95% CI P Patients Heterogeneity I2
All procedures (Fig. 3) 8 0.19 0.08–0.45 0.0002 615 0%
Sensitivity analysis: RCTs with 3 0.28 0.08–0.93 0.04 242 0%
surgical site infection criteria and
postdischarge follow-up
(Supplemental Digital Content
Figure 3, available at http://links.
lww.com/SLA/A281)
Sensitivity analysis: RCTs with 4 0.11 0.03–0.43 0.001 409 0%
comparable BMI between groups
(Supplemental Digital Content
Figure 4, available at http://links.
lww.com/SLA/A281)

surgery than after open procedures (OR = 0.19; 95% CI [0.08–0.45]; numbers of studies when compared with the total pool of included
P = 0.0002; Fig. 3 and Table 3). In the meta-analysis of the observa- observational studies included in the meta-analysis. However, they
tional studies, the similar estimated result was an OR = 0.33 (95% disclosed similar estimates with similar and acceptable heterogene-
CI [0.26–0.42]; P < 0.00001), thus favoring laparoscopic procedures ity as in the meta-analysis and the sensitivity analyses of the RCTs
compared with open procedures (Fig. 4 and Table 4). (Table 4). For forest plots of the sensitivity analyses of observational
studies, see Supplemental Digital Content Figures 5–8 (available at
Sensitivity Analysis http://links.lww.com/SLA/A281).
The RCTs showed an acceptable statistical heterogeneity (I2 =
0%). Both analyses showed significantly fewer surgical site infections DISCUSSION
in laparoscopic surgery compared with open surgery (OR = 0.28; This systematic review and meta-analysis shows that in the
95% CI [0.08–0.93]; P = 0.04 and OR = 0.11; 95% CI [0.03–0.43]; obese surgical patients, the incidence of surgical site infection is
P = 0.001; Table 3). When combined, a 70%–80% risk reduction was significantly less after laparoscopic surgery than after open surgery.
found. Across general abdominal surgical procedures, the obese patients
A considerable statistical heterogeneity was present in the have a 70%–80% lower risk of surgical site infection after laparo-
meta-analysis of observational studies (I2 = 48%; Fig. 4 and Table 4). scopic surgery than after open surgery.
When only studies with a NOS score of 6 stars were included in Obesity is associated with deficient collagen formation82 and
sensitivity analysis, similar estimates as in the meta-analysis and a impaired immunity in responsiveness of lymphocytes,83 in addition
reduced heterogeneity were found. In the “as treated” analysis, sim- to avascularity of subcutaneous layer of fat tissue.84 Previous clini-
ilar estimates were found, but the heterogeneity was minimal (I2 = cal and experimental studies have shown that laparoscopic surgery
0%). Sensitivity analyses to assess the impact of detection and selec- induces a less pronounced proinflammatory response than open
tion bias on bariatric and nonbariatric surgery were based on small surgery and a better preservation of the systemic immune function


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FIGURE 4. Meta-analysis of observational studies.

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Annals of Surgery r Volume 256, Number 6, December 2012 Laparoscopic Versus Open Surgery in Obese Patients

TABLE 4. Laparoscopy Versus Open Surgery: Development of Surgical Site Infection in Observational Studies (For Forest Plots
See Supplemental Digital Content Figures 5–8, available at http://links.lww.com/SLA/A281)
Number of Number of
Analysis Studies OR Random Effect 95% CI P Patients Heterogeneity I2
All procedures (Fig. 4) 37 0.33 0.26–0.42 <0.00001 58,328 48%
Studies with NOS score of 6 stars or 13 0.30 0.18–0.52 <0.0001 16,180 42%
above
Sensitivity analysis: Studies with 4 0.50 0.40–0.63 <0.00001 12,795 0%
surgical site infection criteria and
postdischarge follow-up
Sensitivity analysis: Studies with 7 0.36 0.14–0.90 0.03 409 32%
comparable BMI between groups
Sensitivity analysis: Studies with 12 0.20 0.11–0.37 <0.00001 1360 0%
converted surgery in the open
group in analysis (“as treated”
analysis)

postoperatively.85,86 The lesser surgical trauma and the fact that la- continue the development and implementation of the laparoscopic
paroscopy produces smaller incisions than conventional open surgery and other minimally invasive operative procedures to reduce adverse
may explain the reduced incidence of surgical site infection. Conver- surgical outcome in the rising population of obese patients.
sion from laparoscopic to open surgery has been reported to worsen
postoperative outcome.87,88 In our sensitivity analysis, including “as ACKNOWLEDGMENTS
treated” operations, similar estimates were found compared with the
The authors are indebted to Peer Wille-Jørgensen for devel-
meta-analysis.
oping the idea to this review and for contributing to the editing of
Some studies have reported obesity to be better defined by dis-
the protocol. We thank Marija Barbateskovic, trial search coordina-
tribution of fat tissue instead of the BMI. Accordingly, the thickness
tor at the Cochrane Colorectal Cancer Group, for her assistance in
of subcutaneous fat89 and waist circumference90 have proven to be
conducting the electronic searches. Finally, we want to thank Karin
predictive factors for surgical site infection. In this systematic review,
Mønsted Shabanzadeh for the linguistic corrections and Bispebjerg
we defined obesity as a BMI ≥ 3033 or as defined by other quantitative
Hospital for providing office facilities.
measures involving body weight being the most accepted measures
for obesity in surgical trials. Some authors have suggested that fewer
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