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OBESITY IS ONE OF THE MOST COMMON medicalconditions in the Western world. Morethan one-third of all Americans are obese, andat least eight million are morbidly obese. Theburden of obesity is currently one of the mainconcerns in health care in the U.S. and world-wide; more than 300,000 deaths per year in theU.S. are attributed to obesity-related co-mor-bidities, including diabetes mellitus, hyperten-

sion, and coronary artery disease. Approxi-mately $100 million is spent each year on directtreatment of obesity and obesity-related com-plications [1, 2].

Nosocomial infections are common and have

a substantial impact on mortality and health-care costs in the U.S. Surgical site infection (SSI)alone accounts for 38% of all nosocomial infec-tions of surgical patients. Such infection is as-sociated with other wound complications (e.g.,dehiscence, hernia), a two- to three-fold higherrisk of death, and a 60% higher risk of requir-ing an intensive care unit (ICU) stay. Length ofstay (LOS) is increased by 712 days, the pa-

tient is five times more likely to require read-mission, and direct healthcare costs are in-creased by at least $5,000 by a nosocomialinfection [3, 4].

The increase in the number of obese persons,

SURGICAL INFECTIONSVolume 7, Number 5, 2006 Mary Ann Liebert, Inc.

The Obese Surgical Patient:A Susceptible Host for Infection

DANIEL A. ANAYA and E. PATCHEN DELLINGER

ABSTRACT

Background: Obesity is common in the Western world, and obese persons constitute a grow-ing population of surgical patients for both bariatric and non-bariatric operations. It is thetraditional perception that obese patients have a higher risk of perioperative morbidity and

mortality, although different studies show contradictory results.Purpose: To better delineate the perioperative morbidity and mortality in obese patients.Methods: Review of the pertinent English-language literature.Results: Obesity is a risk factor for nosocomial infection, particularly surgical site infection

(SSI). The mechanisms by which obese patients may be at higher risk for SSI are reviewed,and specific recommendations are outlined that should be implemented when treating obesepatients to minimize potentially preventable SSIs.Conclusion: The growing prevalence of obesity and the increasing number of operations

performed on obese patients, whether to achieve weight loss or for other purposes, will havea substantial impact on health care resources. Vigilant identification of high-risk patients andprovision of all proved preventive measures must suffice until new methods of preventionare identified and validated.

Department of Surgery, University of Washington, Seattle, Washington.Presented at the 25th Annual Meeting of the Surgical Infection Society and 2 nd Joint Meeting with the Surgical

Infection SocietyEurope, Miami, FL, May 57, 2005.

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especially those with severe obesity, is creatinga rapidly growing subset of high-risk surgicalpatients. This can be explained not only byobese patients who require standard surgicaloperations, but also by the fact that bariatricsurgery has experienced a dramatic increaseover the last few years: 120,000 bariatric pro-

cedures were performed in 2003 comparedwith only 20,000 in 1993 [5, 6]. It is perceivedthat obesity constitutes a major risk factor foroverall morbidity and mortality in surgical pa-tients, specifically for postoperative infectiouscomplications, including SSI. Despite the enor-mous impact that this fact could have on pa-tients and health care, the data are controver-sial, and many perceptions are based only onthe traditional teaching that obesity is a pre-dictor of poor outcome in surgical patients.

This paper reviews the studies of the impactof obesity on surgical outcomes, in particularthose evaluating infectious complications.From these results, we hope to establish a bet-ter estimate of the role of obesity as a risk fac-tor and give clear recommendations for mea-sures that will help prevent postoperativeinfections.

OBESITY AND OUTCOMES IN SURGERY

It has been a traditional teaching that obesityis associated with higher rates of perioperativecomplications and death. Several recent reportshave been able to estimate the impact of obe-sity. Although most reports do find an associ-ation of obesity with a higher risk for SSI, def-initions of obesity differ markedly amongpapers, and the reader is advised to verify thedefinition used when referring to a specific pa-per.

A series of studies have been performed com-paring morbidity and mortality in obese patients

undergoing elective surgery in different fields(general surgery, obstetrics/gynecology, urol-ogy, cardiothoracic, transplant) [714]. Mosthave found that obese patients do not appearto have a higher risk of perioperative deaththan non-obese patients. Dindo et al. lookedprospectively at the morbidity and mortality of6,336 patients who underwent general electivesurgery, specifically evaluating the impact of

obesity on these outcomes. A total of 808 pa-tients (13%) were obese (body mass index[BMI] 30). Postoperative complications andmortality were the same for both groups of pa-tients except for SSI, which was significantlymore common in the obese population (4% inobese patients vs. 3% in non-obese patients;

p 0.03) [15]. Birkmeyer et al. evaluated theimpact of obesity prospectively on 11,101 pa-tients undergoing coronary artery bypass graft(CABG) operations. Those investigators like-wise showed no difference in postoperativecomplications or mortality in the two groupsof patients, but again, the risk of SSI was higherin obese patients and increased as their BMI in-creased (odds ratio [OR] for wound infection2.1 in obese patients and 2.74 in severely obesepatients; p 0.001) [16]. These results havebeen reproduced in a number of other studiesevaluating patients after cardiac operations.Some of these studies have shown less postop-erative bleeding in obese patients, an effect thathas not been explained and that might other-wise be expected to result in a lower risk of SSI[1719].

Throughout this review, the reader may ap-preciate that different series find differentrisks associated with obesity. Although itseems that obesity does not carry a higher riskof perioperative death in general, some pa-

pers report contradictory results, and differ-ent reports often address different potentialrisk factors.

OBESITY AND INFECTIONS

Nosocomial infections

The association between obesity and post-operative infections has been the focus of re-cent studies. Choban et al. did a retrospective

review of the effect of obesity on nosocomialinfections in 849 surgical patients. Age, Amer-ican Society of Anesthesiologists (ASA) score[20], and mortality were similar for the obeseand non-obese groups. Despite a relativelysmall number of patients with nosocomial in-fections, obese patients had a significantlyhigher rate of these complications, includingSSI, Clostridium difficile diarrhea, pneumonia,

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OBESITY AND INFECTION 475

and bacteremia (0.05% for normal-weight pa-tients vs. 2.8% and 4% for obese and severelyobese patients, respectively; p 0.01) [21].Previously, Garibaldi et al. [22] and, more re-cently, Canturk et al. [23] showed a trend to-ward a higher risk of pneumonia and nosoco-mial infections in the obese population. A

more recent larger study by Pessaux et al., inwhich they evaluated the risk factors for noso-comial infections in 4,718 patients undergoingnon-colorectal abdominal operations, foundthat obesity, among other variables (age, un-derweight, cirrhosis, vertical abdominal inci-sion, gastrointestinal anastomosis, and pro-longed operative time), was an independentpredictor of postoperative infection by multi-variate analysis. However, obesity did not pre-dict risk of SSI specifically (overall infectionrate in obese patients 17.8%; p 0.05) [24].

Surgical site infections

A large number of studies have evaluated therisk of SSI (or wound infection, as described),and multiple scoring systems have been pro-posed to predict the risk. The National Nosco-mial Infections Surveillance (NNIS) score, pub-lished in 1991 by Culver et al. [25], constitutesthe best current way to estimate the risk of SSI.The score is based on three main variables: ASA

score, wound type, and operative time. Obesityper se is not included, but in more recent stud-ies, obesity was identified repeatedly as an in-dependent predictor of SSI in different popu-lations of patients.

Surgical site infection and its risk factors havebeen studied extensively in cardiac surgery. Ina recently published study by Harrington et al.,in which data were gathered prospectively on4,474 patients undergoing CABG operations atfive institutions, three independent predictorsof SSI were identified: Age, obesity, and dia-

betes mellitus (OR for SSI in obese patients 2.12;p 0.008) [26]. Another study, performed inthe United Kingdom by Lu et al., showed sim-ilar results. Those investigators collected dataprospectively on 4,228 patients undergoingCABG operations at one institution over a four-year period. By multivariate analyses, theyfound that obese patients were twice as likelyto develop sternal infections, and that patients

with sternal infections had a 1.6-fold higher riskof death than those without [27]. A similarstudy by Russo et al. showed that obesity, aswell as vascular disease, diabetes mellitus, andoperative time, were independent predictors ofSSI in a group of 2,345 patients who underwentCABG operations (OR for SSI in obese patients

1.78; p 0.002) [28].These findings hold for non-cardiac surgi-

cal specialties as well. In a recent study bySmith et al., SSI rates and risk factors wereevaluated retrospectively for a group of pa-tients undergoing elective colorectal surgery[29]. Increasing body mass index (BMI) andintraoperative hypotension were indepen-dently associated with SSI (OR 3.0 for SSI inpatients with BMI 30; p 0.01) [29]. Morriset al. [30] evaluated 110 consecutive patientsundergoing lower extremity or pelvic onco-logic operations. Obesity and blood transfu-sion were both independent predictors of SSI[30]. Another study, by Myles et al., evaluated611 patients who underwent elective and non-elective C-section at one institution over a 1-year period. Obesity was a risk factor for SSIafter both elective and urgent procedures [31].

In 1972 Postlethwait et al. evaluated 2,819 pa-tients undergoing elective operations for duo-denal ulcer disease and compared the postop-erative complications in obese (35 lb over ideal

body weight) and non-obese patients. Surgicalsite infections were more common in the for-mer group (15.3% vs. 8.4%); the discrepancy inincidence was exacerbated when obesity wasassociated with diabetes mellitus [32]. In amore recent study, Engelman et al. evaluatedthe impact of BMI and serum albumin concen-tration on the morbidity and mortality of pa-tients undergoing cardiac operations. Among5,168 patients, BMI 30 was associated with ahigher risk of infections of both the vein har-vest site and the sternal incision [33]. In a study

by Benoist et al. of 584 patients who underwentcolorectal surgery, obese patients (BMI 27)were more likely to have intra-abdominal col-lections after left colectomies and anastomoticleakage after proctectomies [34]. Tsukada et al.evaluated the impact of fat distribution on thepostoperative complications of Japanese pa-tients undergoing elective gastric and colorec-tal cancer operations. Those researchers mea-

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476 ANAYA AND DELLINGER

sured the intra-abdominal and subcutaneousfat using preoperative umbilical CT scans in139 patients and found that increased fat dis-tribution in these areas, as well as obesity ingeneral (BMI 25), was associated with ahigher risk of medical and surgical complica-tions (primarily infections) [35]. Although the

metabolic syndrome [36] per se, described inobese patients, has not been studied as a riskfactor for SSI, the Japanese study highlights theimpact of central obesity (a common feature ofmetabolic syndrome) as a predictor of SSI. It re-mains to be seen if these metabolic abnormali-ties associated with morbid obesity convey anadded risk of SSI compared with the obese pa-tient population in general.

Despite these results, obesity has not alwaysproved to be a risk factor for SSI [25,37,38].However, this also is true for well-establishedSSI predictors. The reasons are multiple. Thestudies performed in this area have heteroge-neous patient populations and focus on a widerange of surgical procedures, which definitelyhas an impact on the results. Also, interest inobesity as a medical condition is relatively re-cent, coinciding with the greatly increased in-cidence of obesity in the developed world. Pre-viously, although obesity traditionally wasconsidered a prognostic factor in surgery, itwas uncommon to see obesity as a recorded pa-

rameter in prospective studies or databases ofSSI. In addition, the definitions of obesity dif-fer widely among reports. It is only in recentyears, with the dramatic increase of bariatricsurgery, that standardized definitions of obe-sity based on BMI have become accepted. Nev-ertheless, the BMI reported or associated withhigher risk differs from study to study.

Bariatric surgery and SSI

Surgical site infection is one of the most com-

mon complications of bariatric surgery. The rel-atively low rates of SSI published in large seriesof both open and laparoscopic gastric bypassprocedures underestimate the magnitude of theproblem. Large series of open gastric bypass op-erations have described SSI rates between 15%and 25% [3942], and a pooled analysis of out-comes in open and laparoscopic bypassesshowed a rate of SSI of only 6.6% in open pro-

cedures [43]. Christou et al. did a retrospectivereview of their prospectively collected databasespecifically addressing the incidence of and riskfactors for SSI in patients undergoing openbariatric surgery. They recorded a wide range ofpotential risk factors and also scored each of 269patients according to the NNIS system. On the

basis of the NNIS score, 10.9 SSIs (4%) were ex-pected, but in fact, 54 (20%) were observed. Thisis the only study that addresses this issue specif-ically and highlights the real frequency of SSI(20%) in patients undergoing open gastric by-pass. It also is the only study focused on identi-fying specific risk factors for SSI in the obese pop-ulation undergoing open gastric bypass. Theauthors correlated the administration of epiduralanalgesia and delay in appropriate timing of pro-phylactic antibiotics with a higher risk of SSI.Christou et al. also found a high correlation be-tween SSI and incisional hernia, another com-mon complication after surgery in obese pa-tients. Incisional hernia was described bySugerman et al. to be more common after gastricbypass in morbidly obese patients than in pa-tients receiving chronic corticosteroids and un-dergoing colectomy for inflammatory bowel dis-ease [44,45].

Laparoscopic procedures, particularly inhigh-volume centers, have reduced the highrisk of SSI in patients undergoing bariatric op-

erations [46]. Schauer et al. [47], as well as De-Maria et al. [48], have published the resultswith their first few hundred laparoscopicbariatric operations, and reported incidences ofSSI of 5% and 1.5%, respectively [47,48]. Otherseries have had incidences of SSI of 1% and9% [49,50], and the pooled analysis publishedby Podnos et al. showed an SSI rate of 2.98%,all considerably lower than those described foropen procedures [43]. These data emphasizethe merit of a laparoscopic over an open pro-cedure for obese patients whenever feasible.

MECHANISMS OF INCREASEDINFECTION IN OBESITY

Although one can speculate about the reasonfor a higher risk of SSI in obese patients, thereare few studies offering plausible explanations.Obesity is undoubtedly a surrogate for other

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OBESITY AND INFECTION 477

known risk factors for SSI, particularly diabetesmellitus [51]. Studies evaluating risk factorsand outcomes in surgical patients have shownthat obese patients have a higher rate of thesecomorbidities [15,16,18], and other researchershave found that diabetes mellitus is an inde-pendent predictor of SSI in different popula-

tions of patients [26,28,34,35,37]. A recent studydemonstrated that gastric bypass patients withelevated fasting blood glucose concentrationshave a higher risk of SSI, highlighting the im-portance not only of diabetes mellitus but alsoof perioperative hyperglycemia [52]. A numberof reports demonstrate a higher rate of SSI as-sociated with perioperative hyperglycemia af-ter both cardiac and non-cardiac surgery[53,54]. Obesity is associated with insulin re-sistance and hyperglycemia [11]; it is the au-thors experience that hyperglycemia necessi-tating large doses of intravenous insulin forcontrol is common postoperatively in morbidlyobese patients, with or without known diabetesmellitus. Obesity also has been associated withlonger operations, which is one of the few in-dependent predictors of SSI that is commonlysignificant in multiple series as well as in theNNIS data [16,25]. The magnitude of blood losshas frequently been reported as a risk factorfor SSI [30,37,55]. Whereas some reports citegreater blood loss in obese patients [56], others

report a lower incidence of reoperation forbleeding [16,18].Obesity as an intrinsic risk factor has also

been postulated. In general, it is agreed thatobese patients have tissue hypoperfusion (sub-cutaneous adipose tissue), which may predis-pose to SSI through a greater risk of ischemia/necrosis and suboptimal neutrophil oxidativekilling. Proposed pathogenetic mechanisms in-clude a high ratio of tissue mass:capillaries inadipose tissues, larger wound surface areas(hence a larger area to become infected, greater

oxygen demand, and a larger dead space witha closed incision and a larger wound fluid vol-ume), and decreased oxygen tension in adiposetissues. Many of these factors may be catego-rized together as a poor balance between tissueoxygen demand and oxygen supply.

A robust literature of human and animalstudies supports the importance of local tissueoxygen tension in the resistance to SSI [5759].

Kabon et al. recently reported the measuredincision oxygen tension during and after oper-ation in obese and non-obese patients under-going major abdominal procedures. Obese pa-tients had a suboptimal tissue oxygen tensionat and near the incision intraoperatively anduntil postoperative day one. Furthermore, even

with oxygen supplementation during and afterthe procedure, suboptimal tissue oxygen ten-sion persisted, and a higher FIO2 was requiredto achieve the same PaO2 in obese patients thanin non-obese patients [60]. The same investiga-tors previously published a randomized studydemonstrating that perioperative oxygen sup-plementation to achieve higher tissue oxygentension at the incision during the decisive pe-riod (intraoperatively and up to two hourspostoperatively) decreased the rate of SSI in pa-tients undergoing colorectal operations [57].This evidence of suboptimal wound tissue oxy-gen tension may well be a partial explanationfor the higher risk of SSI in obese patients.

Another mechanism may be the tissue con-centrations of prophylactic antibiotic achievedin obese patients. A number of papers havedemonstrated the importance of antibiotic con-centrations in serum and tissue during an op-erative procedure in prevention of SSI [6164].Forse et al. observed a high rate of SSI in pa-tients undergoing gastric bypass and recorded

low serum concentrations of antibiotic in thesepatients. When the dose of prophylactic an-tibiotic was doubled, the rate of SSI decreased(16.5% vs. 5.6% for 1 g and 2 g of preoperativecefazolin, respectively; p 0.03) [65]. More re-cently, Edmiston et al. measured serum and tis-sue concentrations of prophylactic antibioticsin obese patients at different intervals from in-cision time. They divided 38 patients into threegroups according to BMI: Between 40 and 50,between 50 and 60, and above 60 and found de-creasing serum concentrations of antibiotic

with higher BMIs. More importantly, as theBMI increased, there was a significant decreasein antibiotic concentration at closure in adiposetissue and at incision and closure in deep tis-sues (omentum). Therapeutic tissue concentra-tions were achieved in only 48%, 28%, and 10%of the samples, respectively, from the patientsin the three BMI categories. In addition, serumconcentrations before a repeat dose of antibi-

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otic during operation achieved therapeutic lev-els in only 42%, 18%, and 0, respectively [66].Thus, it may be that obese patients need sub-stantially higher doses of prophylactic antibi-otics to achieve therapeutic concentrations andadequate protection against SSI.

SUMMARY AND SPECIFICRECOMMENDATIONS

Obese patients do not appear to have agreater risk of perioperative death. However,their risk of postoperative infection clearly ishigher, in particular, their risk of SSI, as shownin multiple studies of diverse populations ofpatients. As obesity is more often considered aserious medical condition, studies with similarconclusions likely will proliferate. Stratificationof infection risk for obese surgical patients withdifferent and specific tools (e.g., scores forobese patients) may be necessary.

From the existing data, it is clear that thereare at least four strategies that should be con-sidered in order to decrease the risk of SSIwhen operating on obese patients. First, tightperioperative glucose control is key to mini-mizing episodes of hyperglycemia that areassociated with a higher rate of SSI. Second,optimizing tissue oxygen tension through in-

creased perioperative FI

O2 and appropriateresuscitation improves the perfusion of tissuesand oxygen radical-mediated defense mecha-nisms against infection. Third, larger doses ofprophylactic antibiotics maximize serum andtissue concentrations, providing a real (and ex-pected) decrease in SSI. Fourth, performing la-paroscopic operations whenever feasible cer-tainly decreases the area at risk and has ademonstrated ability to reduce SSI.

The incidence of obesity is rising rapidly, andsurgeons will be expected to perform a greater

number of operations (both bariatric and non-bariatric) in obese patients in the future. Thiswill have a significant impact on the incidenceof postoperative infections, their final outcome,and healthcare costs. In order to decrease therate of SSI and minimize the incidence of po-tentially preventable SSI, particular vigilance isrequired in identifying high-risk patients anddelivering all proved preventive measures

within very strict parameters. New methods todecrease SSI rates in obese patients will surelybecome available as new studies are per-formed.

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Address reprint requests to:Dr. E. Patchen Dellinger

Department of SurgeryUniversity of Washington Medical Center

Box 356410, Room BB 4281959 N.E. Pacific St.

Seattle, WA 98195-6410

E-mail: patch@u.washington.edu