Surgical Site Infection In The Morbidly Obese Patient: A Review

by Anirban Gupta, MD; Michael A. Schweitzer, MD; Kimberley E. Steele, MD; Anne O. Lidor, MD; and Jerome Lyn-Sue, MD

Introduction
Surgical site infection (SSI) is a common and potentially devastating complication that has plagued surgical patients since time immemorial. The surgical literature is rife with well-documented studies and guidelines examining the pathogenesis, risk factors, prevention, and management of such. SSI accounts for 38 percent of all nosocomial infections seen in surgical patients.1 Nosocomial infections are common and have a major impact on mortality and health care costs in the US. SSI leads to other wound-related complications, such as dehiscence, hernia, a potential 2- to 3-fold higher risk of death, and up to 60-percent higher risk of requiring an ICU stay. Length of stay (LOS) is increased by 7 to 12 days, the patient is at least five times more likely to be readmitted, and direct healthcare costs are increased by at least $5,000 by a nosocomial infection.1 The most quoted and implemented guideline for prevention of SSI was originally published in 1992 by the Center for Disease Control (CDC) and was subsequently expanded in 1999.

Obesity is an increasingly common medical condition in the Western world. More than one-third of Americans are obese and at least eight million Americans are morbidly obese. This poses a significant burden on healthcare in the US. More than 300,000 deaths per year are attributed to obesity-related comorbidities, such as diabetes mellitus (DM), hypertension, and coronary artery disease. Approximately $100 million is spent each year on direct treatment of obesity and obesity-related complications.1 The burgeoning morbidly obese population is creating a rapidly growing subset of high-risk surgical patients. In 2003, approximately 120,000 bariatric procedures were performed compared to only 20,000 bariatric procedures in 1993.2 Despite the dramatic rise in the morbidly obese population and bariatric procedures, there is a relative paucity of clear, systematic, evidence-based guidelines to prevent and manage SSI in the morbidly obese. In fact, the CDC guidelines clearly stipulate that they do not specifically recommend SSI prevention methods unique to laparoscopic surgery. The purpose of our review is to examine the considerations that are unique to SSI in the morbidly obese patient. We briefly summarize specific recommendations from the 1999 CDC paper as they apply to all surgical patients. However, a thorough discussion of the 1999 CDC guidelines is beyond the scope of this review. We discuss the pathogenesis of SSI in the morbidly obese patient, review potentially modifiable risk factors and strategies unique to this group of patients, and compare outcomes with regard to SSI between morbidly obese patients undergoing laparoscopic versus open surgery.

Discussion
The identification of SSI involves the interpretation of clinical and laboratory findings and is highly contingent on a surveillance program using standardized and consistent definitions.3 In fact, the CDC’s National Nosocomial Infections Surveillance (NNIS) system that was established in 1970 has developed standardized surveillance criteria for defining SSI (Table 1).4

SSIs are classified as incisional or organ/space. Incisional SSIs are further subdivided into those involving only the skin and subcutaneous tissue (superficial incisional SSI) and those involving deeper soft tissues (deep incisional SSI).3 Organ/space SSIs involve any part of the anatomy other than incised body wall layers that was opened or manipulated during an operation (Figure 1). The CDC NNIS definitions of SSIs have been consistently applied in many settings and are currently a de facto national
standard.3,4

A number of different studies have been done comparing morbidity and mortality in obese patients undergoing elective surgery in different fields such as general surgery, obstetrics, urology, cardiac surgery, and transplant.1,8 Most of these studies have found that obese patients do not appear to have a higher risk of perioperative death than non-obese patients. One important study looked prospectively at morbidity and mortality in patients undergoing general elective surgery, specifically looking at the impact of obesity. 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% vs. 3%).1,9 Another interesting study by Birkmeyer and colleagues evaluated the impact of obesity prospectively on 11,101 patients undergoing coronary artery bypass graft (CABG) operations. Again, there was no difference in postoperative complications or mortality in the two groups, but the risk of SSI was higher in obese patients and increased as their body mass index (BMI) increased.1,10 A number of other studies have reproduced these results.1 A study by Choban, et al., demonstrated that obese patients had a significantly higher rate of nosocomial infections, including SSI, clostridium difficile diarrhea, pneumonia, and bacteremia.11 Obesity increases the risk of perioerative complications of the skin and underlying tissue, including wound infection, dehiscence, pressure ulcers, and deep tissue injury.18,19 SSI and its risk factors have been studied extensively in cardiac surgery. The cardiac literature has consistently demonstrated that obese patients are at a significantly higher risk of developing SSI. These findings hold true for non-cardiac surgical specialties as well.1

SSI is one of the most common complications of bariatric surgery. Large series of open gastric bypass operations have described SSI rates between 15 and 25 percent.1 Christou, et al., retrospectively reviewed their prospectively collected database, specifically addressing the incidence and risks for SSI in patients undergoing open bariatric surgery. They observed an SSI rate of 20 percent, despite an expected score of four percent based on the NNIS system.12

Laparoscopic procedures, particularly in high-volume centers, have reduced the high risk of SSI in patients undergoing bariatric operations.1,13 Schauer and colleagues, as well as DeMaria and colleagues, have reported much lower rates of SSI compared to the open literature (5% and 1.5%, respectively).14,15 Several other recent studies have demonstrated similar low rates of SSI in patients undergoing laparoscopic bariatric operations compared to open procedures.

As stated, an exhaustive discussion of SSI as outlined in the CDC guidelines is beyond the purview of this paper; however, several issues are worth discussing. First, the distribution of pathogens has not changed markedly over the last decade (Table 2).3,5,6 There is no difference in distribution between obese and non-obese patients. Staphylococcus aureus, coagulase-negative staphylococci, enterococcus, and Escherichia coli remain the most frequently isolated pathogens.3

So what causes SSI? Microbial contamination of the surgical site is a necessary precursor. The risk is conceptualized according to the following relationship:3
(Dose of bacterial contamination x virulence)/Resistance of the host patient=Risk of SSI.
In fact, if a surgical site is contaminated with greater than 105 microorganisms per gram of tissue, the risk of SSI is markedly increased.3 The dose of contaminating microorganisms needed to produce infection may be much lower when foreign material such as silk suture, for example, is present at the site.3

Microorganisms may contain or produce toxins that increase their ability to invade a host or survive in host tissue—endotoxin, which stimulates cytokine production, is one such example. Other bacteria inhibit phagocytosis by secretion of a polysaccharide capsule, which also contributes to SSI. Certain strains of clostridia and streptococci produce exotoxins, disrupting cell membranes and altering cellular metabolism. Regardless of the pathogenetic mechanism, for most SSIs, the source of pathogens is the endogenous flora of the patient’s skin, mucousmembranes, or hollow viscera.3

Exogenous sources can contribute to SSI as well. They include surgical personnel, the operating room environment (including air), tools, and instruments brought into the sterile field.

Several very good studies have demonstrated the role of certain risk factors in the pathophysiology of SSI. These risk factors have been identified by both univariate and multivariate analyses. In broad terms, these risk factors can be classified as “patient factors” and “operative factors.” Patient factors include age, nutritional status, diabetes, smoking, obesity, and several others. Operative factors include surgical scrub duration, skin antisepsis, preoperative shaving, skin prep, duration of the operation, antimicrobial prophylaxis, foreign material, drains, and surgical technique (Table 3).3

Despite various speculations explaining SSI in obese patients, there are few studies offering rigorous scientific explanations. Clearly, obesity is a surrogate for other known risk factors for SSI, namely diabetes mellitus (DM).1 One recent study demonstrated that gastric bypass patients with elevated fasting blood glucose concentrations have a higher risk of SSI, which highlights the importance of preoperative hyperglycemia as well as that of DM.1,16 Obesity is associated with insulin resistance and hyperglycemia. A number of studies in the cardiac literature have shown a higher rate of SSI in patients with perioperative hyperglycemia. Furthermore, obesity is associated with longer operations, which is one of the independent predictors of SSI that is commonly significant in multiple series as well as in the NNIS data.1

It is generally agreed that obese patients have tissue hypoperfusion, which may predispose to SSI through a greater risk of ischemia, necrosis, and suboptimal neutrophil oxidative killing.1 Possibilities include a high ratio of tissue mass: capillaries in adipose tissue, larger wound surface areas, and decreased oxygen tension in adipose tissues. All of these point toward poor balance between tissue oxygen demand and supply. Kabon, et al., demonstrated that the measured incision oxygen tension during and after operation in obese and non-obese patients undergoing major abdominal operations differs significantly. Specifically, they showed that obese patients had a suboptimal tissue oxygen tension at and near the incision intraoperatively and until postoperative Day 1. 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.17 There is a growing body of evidence that would suggest that suboptimal wound tissue oxygen tension may in part explain the higher risk of SSI in obese patients.

An important factor in surgical wound healing is the rate of collagen synthesis. Collagen provides tensile strength to the wound. Oxygenation of tissues is critical for the processes that constitute wound healing—angiogenesis, collagen synthesis, and epithelialization.18 Numerous studies have documented that postoperative pain, sedation, and atelectasis can exacerbate carbon dioxide retention and increase hypoxia in patients who are obese.

Another mechanism contributing to SSI may be the tissue concentration of prophylactic antibiotic achieved in obese patients. Many studies have demonstrated the importance of antibiotic concentrations in serum and tissue during an operation.1 One such study noted a high rate of SSI in patients undergoing gastric bypass and recorded low serum concentrations of antibiotic in these patients. Doubling the dose of prophylactic antibiotic resulted in a significant decrease in the rate of SSI—16.5 percent versus 5.6 percent for 1g and 2g of preoperative cefazolin, respectively.1 Another well-designed study noted that as BMI increased, there was a significant decrease in antibiotic concentration at closure in adipose tissue and at incision and closure in deep tissues (omentum). These studies would suggest that obese patients need substantially higher doses of prophylactic antibiotics to achieve therapeutic concentrations and adequate protection against SSI.

Four general strategies have been proposed by Anaya and colleagues to prevent or decrease the risk of SSI in the obese—tight perioperative glucose control, optimizing tissue oxygen tension, larger doses of prophylactic antibiotics, and finally, performing laparoscopic operations whenever feasible.

The stress response to surgery, which increases blood glucose levels, can cause hyperglycemia regardless of presence or absence of diabetes. Hyperglycemia impairs immunity, inhibits the inflammatory response, and interferes with collagen synthesis.18 Further, microvascular changes that result from sustained hyperglycemia may further impair tissue oxygenation. Some studies advocate the goal of achieving blood glucose levels below 200mg/dL. Insulin by infusion may be more effective postoperatively than the oral or injected route. Of course, such infusion would require close monitoring to prevent hypoglycemia, and that could present logistical difficulties.

Some have suggested that oxygen saturation should be monitored for at least 24 hours after surgery by the use of pulse oximetry, given the close association between obesity and obstructive sleep apnea and the risk of rapid desaturation. However, further studies need to be done to corroborate this. Other groups have suggested that an oxygen saturation below 94 percent is associated with an increased risk of wound infection, which would substantiate the need for postsurgical supplemental oxygen. However, further studies need to be done before making any definitive consensus statements.

From a pharmacologic standpoint, it makes intuitive sense that patients with a higher BMI would require a larger dose of antibiotics to achieve similar concentrations in serum and tissue. Many centers of excellence have adopted this regimen and have developed standard protocols with higher doses than what would be used in non-obese patients.

Finally, based on several good studies from several centers over the past few years, it is clear that laparoscopic bariatric surgery results in a lower incidence of SSI compared to open bariatric surgery. This may be due to a multitude of factors, including decreased physical trauma to the skin and subcutaneous tissue (absence of large retractors), absence of a large open incision that is exposed to the surrounding environment, as well as any visceral misadventure, decreased blood loss, and overall decreased surface area for possible contamination.

Absence of a large midline incision translates to negligible suture material. Suture material obviously can serve as a nidus for microorganisms and subsequent SSI. Heavy metal retractors exert pressure on the skin, wound edges, and subcutaneous tissue, thereby causing damage to the capillaries and vessels, further impeding oxygen delivery to the affected areas, resulting in decreased oxygen tension, and, again, contributing to a milieu that is ideal for developing SSI.

Large incisions are also more subject to technical error and variability. Concurrently, large incisions are prone to other physical factors, such as increased intra-abdominal pressures, greater lateral tension exerted by the sheer mass effect of the abdominal pannus, as well as exposure to often devitalized and poorly oxygenated tissue and space. In experienced hands in high volume centers, laparoscopic bariatric surgery can be accomplished in a more expedient fashion with less external trauma to the skin and subcutaneous tissue, as well as less handling of the visceral structures. Decreased operative time translates to decreased pressure necrosis. The minimally invasive approach also allows for improved postoperative oxygenation and ventilation due to better analgesia and improved mechanics of ventilation since the patient does not have to deal with a large mid-line incision—and it is clear that adequate tissue oxygen tension is important to minimize or decrease the risk of SSI. Even when a trocar site does get infected, it poses significantly less morbidity to the patient than that associated with a large midline wound. A trocar site infection may be managed with simple maneuvers, such as opening up the incision. Conversely, a large midline wound infection can result in dehiscence, evisceration, difficult closure, and possible fistula formation. SSI associated with a large midline incision may result in more days of work lost compared to that noted with a trocar site. Indeed, there is a difference in morbidity between SSI in a trocar site versus a midline incision.

Finally, even within patients undergoing laparoscopic bariatric surgery, there may be differences in outcomes depending on what type of specific technique is used. It is possible that a circular stapler technique, for example, may be associated with a higher SSI rate due to the fact that it requires passage of the stapler and anvil through the skin and enteric system, respectively, which can cause local contamination as well as transmigration of oral and enteric flora.

Summary
In summary, SSI is the result of a complex interplay of patient factors, local wound-related factors, surgeon or technical factors, and systemic factors. There are adequate guidelines on SSI for the non-obese population. Given the burgeoning obese population in this country, and the burden that it imposes on the healthcare system, it is imperative to develop more specific guidelines to prevent and minimize SSI in morbidly obese patients.

References
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