SURGICAL INFECTIONS Volume 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 growing population of surgical patients for both bariatric and non-bariatric operations. It is the traditional 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 obese patients 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 have a substantial impact on health care resources. Vigilant identification of high-risk patients and provision of all proved preventive measures must suffice until new methods of prevention are identified and validated.

BESITY IS ONE OF THE MOST COMMON medical conditions in the Western world. More than one-third of all Americans are obese, and at least eight million are morbidly obese. The burden of obesity is currently one of the main concerns in health care in the U.S. and worldwide; more than 300,000 deaths per year in the U.S. are attributed to obesity-related co-morbidities, including diabetes mellitus, hypertension, and coronary artery disease. Approximately $100 million is spent each year on direct treatment of obesity and obesity-related complications [1, 2]. Nosocomial infections are common and have

a substantial impact on mortality and healthcare costs in the U.S. Surgical site infection (SSI) alone accounts for 38% of all nosocomial infections of surgical patients. Such infection is associated with other wound complications (e.g., dehiscence, hernia), a two- to three-fold higher risk of death, and a 60% higher risk of requiring an intensive care unit (ICU) stay. Length of stay (LOS) is increased by 712 days, the patient is five times more likely to require readmission, and direct healthcare costs are increased by at least $5,000 by a nosocomial infection [3, 4]. The increase in the number of obese persons,

Department of Surgery, University of Washington, Seattle, Washington. Presented at the 25th Annual Meeting of the Surgical Infection Society and 2nd Joint Meeting with the Surgical Infection SocietyEurope, Miami, FL, May 57, 2005.

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especially those with severe obesity, is creating a rapidly growing subset of high-risk surgical patients. This can be explained not only by obese patients who require standard surgical operations, but also by the fact that bariatric surgery has experienced a dramatic increase over the last few years: 120,000 bariatric procedures were performed in 2003 compared with only 20,000 in 1993 [5, 6]. It is perceived that obesity constitutes a major risk factor for overall morbidity and mortality in surgical patients, specifically for postoperative infectious complications, including SSI. Despite the enormous impact that this fact could have on patients and health care, the data are controversial, and many perceptions are based only on the traditional teaching that obesity is a predictor of poor outcome in surgical patients. This paper reviews the studies of the impact of obesity on surgical outcomes, in particular those evaluating infectious complications. From these results, we hope to establish a better estimate of the role of obesity as a risk factor and give clear recommendations for measures that will help prevent postoperative infections.

OBESITY AND OUTCOMES IN SURGERY It has been a traditional teaching that obesity is associated with higher rates of perioperative complications and death. Several recent reports have been able to estimate the impact of obesity. Although most reports do find an association of obesity with a higher risk for SSI, definitions of obesity differ markedly among papers, and the reader is advised to verify the definition used when referring to a specific paper. A series of studies have been performed comparing morbidity and mortality in obese patients undergoing elective surgery in different fields (general surgery, obstetrics/gynecology, urology, cardiothoracic, transplant) [714]. Most have found that obese patients do not appear to have a higher risk of perioperative death than non-obese patients. Dindo et al. looked prospectively at the morbidity and mortality of 6,336 patients who underwent general elective surgery, specifically evaluating the impact of

obesity on these outcomes. A total of 808 patients (13%) were obese (body mass index [BMI] 30). Postoperative complications and mortality were the same for both groups of patients except for SSI, which was significantly more common in the obese population (4% in obese patients vs. 3% in non-obese patients; p 0.03) [15]. Birkmeyer et al. evaluated the impact of obesity prospectively on 11,101 patients undergoing coronary artery bypass graft (CABG) operations. Those investigators likewise showed no difference in postoperative complications or mortality in the two groups of patients, but again, the risk of SSI was higher in obese patients and increased as their BMI increased (odds ratio [OR] for wound infection 2.1 in obese patients and 2.74 in severely obese patients; p 0.001) [16]. These results have been reproduced in a number of other studies evaluating patients after cardiac operations. Some of these studies have shown less postoperative bleeding in obese patients, an effect that has not been explained and that might otherwise be expected to result in a lower risk of SSI [1719]. Throughout this review, the reader may appreciate that different series find different risks associated with obesity. Although it seems that obesity does not carry a higher risk of perioperative death in general, some papers report contradictory results, and different reports often address different potential risk factors.

OBESITY AND INFECTIONS Nosocomial infections The association between obesity and postoperative infections has been the focus of recent studies. Choban et al. did a retrospective review of the effect of obesity on nosocomial infections in 849 surgical patients. Age, American Society of Anesthesiologists (ASA) score [20], and mortality were similar for the obese and non-obese groups. Despite a relatively small number of patients with nosocomial infections, obese patients had a significantly higher rate of these complications, including SSI, Clostridium difficile diarrhea, pneumonia,

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and bacteremia (0.05% for normal-weight patients vs. 2.8% and 4% for obese and severely obese patients, respectively; p 0.01) [21]. Previously, Garibaldi et al. [22] and, more recently, Canturk et al. [23] showed a trend toward a higher risk of pneumonia and nosocomial infections in the obese population. A more recent larger study by Pessaux et al., in which they evaluated the risk factors for nosocomial infections in 4,718 patients undergoing non-colorectal abdominal operations, found that obesity, among other variables (age, underweight, cirrhosis, vertical abdominal incision, gastrointestinal anastomosis, and prolonged operative time), was an independent predictor of postoperative infection by multivariate analysis. However, obesity did not predict risk of SSI specifically (overall infection rate in obese patients 17.8%; p 0.05) [24]. Surgical site infections A large number of studies have evaluated the risk of SSI (or wound infection, as described), and multiple scoring systems have been proposed to predict the risk. The National Noscomial Infections Surveillance (NNIS) score, published in 1991 by Culver et al. [25], constitutes the best current way to estimate the risk of SSI. The score is based on three main variables: ASA score, wound type, and operative time. Obesity per se is not included, but in more recent studies, obesity was identified repeatedly as an independent predictor of SSI in different populations of patients. Surgical site infection and its risk factors have been studied extensively in cardiac surgery. In a recently published study by Harrington et al., in which data were gathered prospectively on 4,474 patients undergoing CABG operations at five institutions, three independent predictors of SSI were identified: Age, obesity, and diabetes mellitus (OR for SSI in obese patients 2.12; p 0.008) [26]. Another study, performed in the United Kingdom by Lu et al., showed similar results. Those investigators collected data prospectively on 4,228 patients undergoing CABG operations at one institution over a fouryear period. By multivariate analyses, they found that obese patients were twice as likely to develop sternal infections, and that patients

with sternal infections had a 1.6-fold higher risk of death than those without [27]. A similar study by Russo et al. showed that obesity, as well as vascular disease, diabetes mellitus, and operative time, were independent predictors of SSI in a group of 2,345 patients who underwent CABG operations (OR for SSI in obese patients 1.78; p 0.002) [28]. These findings hold for non-cardiac surgical specialties as well. In a recent study by Smith et al., SSI rates and risk factors were evaluated retrospectively for a group of patients undergoing elective colorectal surgery [29]. Increasing body mass index (BMI) and intraoperative hypotension were independently associated with SSI (OR 3.0 for SSI in patients with BMI 30; p 0.01) [29]. Morris et al. [30] evaluated 110 consecutive patients undergoing lower extremity or pelvic oncologic operations. Obesity and blood transfusion were both independent predictors of SSI [30]. Another study, by Myles et al., evaluated 611 patients who underwent elective and nonelective C-section at one institution over a 1year period. Obesity was a risk factor for SSI after both elective and urgent procedures [31]. In 1972 Postlethwait et al. evaluated 2,819 patients undergoing elective operations for duodenal ulcer disease and compared the postoperative complications in obese (35 lb over ideal body weight) and non-obese patients. Surgical site infections were more common in the former group (15.3% vs. 8.4%); the discrepancy in incidence was exacerbated when obesity was associated with diabetes mellitus [32]. In a more recent study, Engelman et al. evaluated the impact of BMI and serum albumin concentration on the morbidity and mortality of patients undergoing cardiac operations. Among 5,168 patients, BMI 30 was associated with a higher risk of infections of both the vein harvest site and the sternal incision [33]. In a study by Benoist et al. of 584 patients who underwent colorectal surgery, obese patients (BMI 27) were more likely to have intra-abdominal collections after left colectomies and anastomotic leakage after proctectomies [34]. Tsukada et al. evaluated the impact of fat distribution on the postoperative complications of Japanese patients undergoing elective gastric and colorectal cancer operations. Those researchers mea-

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sured the intra-abdominal and subcutaneous fat using preoperative umbilical CT scans in 139 patients and found that increased fat distribution in these areas, as well as obesity in general (BMI 25), was associated with a higher risk of medical and surgical complications (primarily infections) [35]. Although the metabolic syndrome [36] per se, described in obese patients, has not been studied as a risk factor for SSI, the Japanese study highlights the impact of central obesity (a common feature of metabolic syndrome) as a predictor of SSI. It remains to be seen if these metabolic abnormalities associated with morbid obesity convey an added risk of SSI compared with the obese patient population in general. Despite these results, obesity has not always proved to be a risk factor for SSI [25,37,38]. However, this also is true for well-established SSI predictors. The reasons are multiple. The studies performed in this area have heterogeneous patient populations and focus on a wide range of surgical procedures, which definitely has an impact on the results. Also, interest in obesity as a medical condition is relatively recent, coinciding with the greatly increased incidence of obesity in the developed world. Previously, although obesity traditionally was considered a prognostic factor in surgery, it was uncommon to see obesity as a recorded parameter in prospective studies or databases of SSI. In addition, the definitions of obesity differ widely among reports. It is only in recent years, with the dramatic increase of bariatric surgery, that standardized definitions of obesity based on BMI have become accepted. Nevertheless, the BMI reported or associated with higher risk differs from study to study. Bariatric surgery and SSI Surgical site infection is one of the most common complications of bariatric surgery. The relatively low rates of SSI published in large series of both open and laparoscopic gastric bypass procedures underestimate the magnitude of the problem. Large series of open gastric bypass operations have described SSI rates between 15% and 25% [3942], and a pooled analysis of outcomes in open and laparoscopic bypasses showed a rate of SSI of only 6.6% in open pro-

cedures [43]. Christou et al. did a retrospective review of their prospectively collected database specifically addressing the incidence of and risk factors for SSI in patients undergoing open bariatric surgery. They recorded a wide range of potential risk factors and also scored each of 269 patients according to the NNIS system. On the basis of the NNIS score, 10.9 SSIs (4%) were expected, but in fact, 54 (20%) were observed. This is the only study that addresses this issue specifically and highlights the real frequency of SSI (20%) in patients undergoing open gastric bypass. It also is the only study focused on identifying specific risk factors for SSI in the obese population undergoing open gastric bypass. The authors correlated the administration of epidural analgesia and delay in appropriate timing of prophylactic antibiotics with a higher risk of SSI. Christou et al. also found a high correlation between SSI and incisional hernia, another common complication after surgery in obese patients. Incisional hernia was described by Sugerman et al. to be more common after gastric bypass in morbidly obese patients than in patients receiving chronic corticosteroids and undergoing colectomy for inflammatory bowel disease [44,45]. Laparoscopic procedures, particularly in high-volume centers, have reduced the high risk of SSI in patients undergoing bariatric operations [46]. Schauer et al. [47], as well as DeMaria et al. [48], have published the results with their first few hundred laparoscopic bariatric operations, and reported incidences of SSI of 5% and 1.5%, respectively [47,48]. Other series have had incidences of SSI of 1% and 9% [49,50], and the pooled analysis published by Podnos et al. showed an SSI rate of 2.98%, all considerably lower than those described for open procedures [43]. These data emphasize the merit of a laparoscopic over an open procedure for obese patients whenever feasible.

MECHANISMS OF INCREASED INFECTION IN OBESITY Although one can speculate about the reason for a higher risk of SSI in obese patients, there are few studies offering plausible explanations. Obesity is undoubtedly a surrogate for other

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known risk factors for SSI, particularly diabetes mellitus [51]. Studies evaluating risk factors and outcomes in surgical patients have shown that obese patients have a higher rate of these comorbidities [15,16,18], and other researchers have found that diabetes mellitus is an independent predictor of SSI in different populations of patients [26,28,34,35,37]. A recent study demonstrated that gastric bypass patients with elevated fasting blood glucose concentrations have a higher risk of SSI, highlighting the importance not only of diabetes mellitus but also of perioperative hyperglycemia [52]. A number of reports demonstrate a higher rate of SSI associated with perioperative hyperglycemia after both cardiac and non-cardiac surgery [53,54]. Obesity is associated with insulin resistance and hyperglycemia [11]; it is the authors experience that hyperglycemia necessitating large doses of intravenous insulin for control is common postoperatively in morbidly obese patients, with or without known diabetes mellitus. Obesity also has been associated with longer operations, which is one of the few independent predictors of SSI that is commonly significant in multiple series as well as in the NNIS data [16,25]. The magnitude of blood loss has frequently been reported as a risk factor for SSI [30,37,55]. Whereas some reports cite greater blood loss in obese patients [56], others report a lower incidence of reoperation for bleeding [16,18]. Obesity as an intrinsic risk factor has also been postulated. In general, it is agreed that obese patients have tissue hypoperfusion (subcutaneous adipose tissue), which may predispose to SSI through a greater risk of ischemia/ necrosis and suboptimal neutrophil oxidative killing. Proposed pathogenetic mechanisms include a high ratio of tissue mass:capillaries in adipose tissues, larger wound surface areas (hence a larger area to become infected, greater oxygen demand, and a larger dead space with a closed incision and a larger wound fluid volume), and decreased oxygen tension in adipose tissues. Many of these factors may be categorized together as a poor balance between tissue oxygen demand and oxygen supply. A robust literature of human and animal studies supports the importance of local tissue oxygen tension in the resistance to SSI [5759].

Kabon et al. recently reported the measured incision oxygen tension during and after operation in obese and non-obese patients undergoing major abdominal procedures. Obese patients had a suboptimal tissue oxygen tension at and near the incision intraoperatively and until postoperative day one. Furthermore, even with oxygen supplementation during and after the procedure, suboptimal tissue oxygen tension persisted, and a higher FIO2 was required to achieve the same PaO2 in obese patients than in non-obese patients [60]. The same investigators previously published a randomized study demonstrating that perioperative oxygen supplementation to achieve higher tissue oxygen tension at the incision during the decisive period (intraoperatively and up to two hours postoperatively) decreased the rate of SSI in patients undergoing colorectal operations [57]. This evidence of suboptimal wound tissue oxygen tension may well be a partial explanation for the higher risk of SSI in obese patients. Another mechanism may be the tissue concentrations of prophylactic antibiotic achieved in obese patients. A number of papers have demonstrated the importance of antibiotic concentrations in serum and tissue during an operative procedure in prevention of SSI [6164]. Forse et al. observed a high rate of SSI in patients undergoing gastric bypass and recorded low serum concentrations of antibiotic in these patients. When the dose of prophylactic antibiotic was doubled, the rate of SSI decreased (16.5% vs. 5.6% for 1 g and 2 g of preoperative cefazolin, respectively; p 0.03) [65]. More recently, Edmiston et al. measured serum and tissue concentrations of prophylactic antibiotics in obese patients at different intervals from incision time. They divided 38 patients into three groups according to BMI: Between 40 and 50, between 50 and 60, and above 60 and found decreasing serum concentrations of antibiotic with higher BMIs. More importantly, as the BMI increased, there was a significant decrease in antibiotic concentration at closure in adipose tissue and at incision and closure in deep tissues (omentum). Therapeutic tissue concentrations were achieved in only 48%, 28%, and 10% of the samples, respectively, from the patients in the three BMI categories. In addition, serum concentrations before a repeat dose of antibi-

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otic during operation achieved therapeutic levels in only 42%, 18%, and 0, respectively [66]. Thus, it may be that obese patients need substantially higher doses of prophylactic antibiotics to achieve therapeutic concentrations and adequate protection against SSI.

within very strict parameters. New methods to decrease SSI rates in obese patients will surely become available as new studies are performed. REFERENCES
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SUMMARY AND SPECIFIC RECOMMENDATIONS Obese patients do not appear to have a greater risk of perioperative death. However, their risk of postoperative infection clearly is higher, in particular, their risk of SSI, as shown in multiple studies of diverse populations of patients. As obesity is more often considered a serious medical condition, studies with similar conclusions likely will proliferate. Stratification of infection risk for obese surgical patients with different and specific tools (e.g., scores for obese patients) may be necessary. From the existing data, it is clear that there are at least four strategies that should be considered in order to decrease the risk of SSI when operating on obese patients. First, tight perioperative glucose control is key to minimizing episodes of hyperglycemia that are associated with a higher rate of SSI. Second, optimizing tissue oxygen tension through increased perioperative FIO2 and appropriate resuscitation improves the perfusion of tissues and oxygen radical-mediated defense mechanisms against infection. Third, larger doses of prophylactic antibiotics maximize serum and tissue concentrations, providing a real (and expected) decrease in SSI. Fourth, performing laparoscopic operations whenever feasible certainly decreases the area at risk and has a demonstrated ability to reduce SSI. The incidence of obesity is rising rapidly, and surgeons will be expected to perform a greater number of operations (both bariatric and nonbariatric) in obese patients in the future. This will have a significant impact on the incidence of postoperative infections, their final outcome, and healthcare costs. In order to decrease the rate of SSI and minimize the incidence of potentially preventable SSI, particular vigilance is required in identifying high-risk patients and delivering all proved preventive measures

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Address reprint requests to: Dr. E. Patchen Dellinger Department of Surgery University of Washington Medical Center Box 356410, Room BB 428 1959 N.E. Pacific St. Seattle, WA 98195-6410 E-mail: patch@u.washington.edu