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Research Article

An Assessment of Risk Factors for Surgical Site Infection and Superficial Wound Separation in Gynecologic Oncology Patients

Sarah E. Taylor, Gabriella G. Gosman, Joseph L. Kelley, Paniti Sukumvanich, Madeleine Courtney-brooks, Jessica Berger, John Comerci, Sushil Beriwal and Alexander B. Olawaiye

Correspondence Address :

Alexander B. Olawaiye, MD
Magee-Womens Hospital of University of Pittsburgh Medical Center
Division of Gynecologic Oncology
300 Halket Street, Pittsburgh, PA 15213
Tel: (412)641-5468
Fax: (412)641-5417
Email: olawaiyea@mail.magee.edu

Received on: Octaber 15, 2016, Accepted on: January 26, 2017, Published on: February 03, 2017

Citation: Sarah E. Taylor, Gabriella G. Gosman, Joseph L. Kelley, et al. (2017). An Assessment of Risk Factors for Surgical Site Infection and Superficial Wound Separation in Gynecologic Oncology Patients

Copyright: 2017 Alexander B. Olawaiye, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Abstract
Objective: Approximately 500,000 surgical site infections (SSI) are diagnosed every year. Risk factors are reported mostly from cardiac and orthopedic literature. The purpose of this study was to evaluate risk factors for SSI and superficial wound separation (SWS) in gynecologic oncology patients undergoing primary surgery with a vertical midline incision.
Materials and Methods: A retrospective chart review was performed on patients who underwent surgery between January and December 2008 and were diagnosed with a superficial SSI or SWS within 30 days of surgery. Cases were matched with controls, in a ratio of 1:2, during this period with the same type of surgery but did not develop a SSI or a SWS. Charts were reviewed for patient characteristics and surgical data. Univariate and multivariate analysis were performed to assess for factors associated with SSI and SWS.
Results: Fifty cases were matched with 100 controls, resulting in 150 subjects. Cases and controls had similar demographic characteristics. Nine co-morbid conditions were identified. Median BMI was lower for controls, 27.2 vs. 36.8 kg/m2 (p<0.001). Obesity, transfusion rate, hypothermia prevention, type of skin closure, operating time, and length of stay (LOS) were statistically significant with univariate analysis. With multivariate analysis, obesity and rate of transfusion were the only factors that remained statistically significant.
Conclusions: Several variables may contribute to SSI and SWS. Obesity and higher rate of blood transfusion were the significant risk factors in this study. Prospective studies are needed to evaluate these factors, particularly alternatives to transfusion, like intraoperative autologous blood recovery.
Keywords: Surgical site infection, Wound infection, Superficial wound separation, Gynecologic surgery, Gynecologic cancer

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Introduction
The Center for Disease Control's (CDC) National Nosocomial Infections Surveillance (NNIS) system reports on all hospital acquired infections, including surgical site infections (SSI). In a report from 2008, it was noted that there are approximately 500,000 surgical site infections reported every year and accounts for up to 5% of all inpatient surgeries. It has also been observed that these patients require an average of seven to ten additional postoperative hospital days and incur up to $10 billion in health care expenditures on an annual basis. These estimates are based upon inpatient costs that accrue at the time of the initial operation and do not account for the expenses of outpatient follow-up care and re-hospitalization [1]. Superficial infections are common and contribute to overall patient morbidity as well as a substantial portion of health care dollars spent.
There is an abundance of literature examining the risk factors for development of surgical site infections. However, the majority of patients studied are males and have undergone either cardiac or orthopaedic surgery [2]. Some literature exists within the field of obstetrics and gynecology, but is concentrated in obstetrics, looking at cesarean section as the primary operation [3-17]. Hence, gynecologic practices often rely on the outcomes from the general surgery literature. This data is contingent on the fact that the majority of the patients are male and although the skin incision is often the same or similar, the internal procedures are quite different. 
Patients with gynecologic malignancies pose another level of complexity because cancer has been identified as risk factor for the development of surgical site infections. The purpose of this study was to evaluate risk factors for SSI and superficial wound separation (SWS) in gynecologic oncology patients undergoing primary surgery with a vertical midline incision.
Materials and Methods
A retrospective chart review was completed on patients who underwent a primary surgery with a vertical midline incision for a gynecologic malignancy between January and December 2008 at Magee Women's Hospital of the University of Pittsburgh Medical Center and were subsequently diagnosed with either a superficial SSI or SWS within 30 days of the initial surgery. The CDC has published standardized definitions for surgical site infections through the NNIS network. For superficial surgical site infections this includes an infection that occurs within 30 days after the operation and involves only skin or subcutaneous tissue of the incision and at least one of the following: 1. Purulent drainage, with or without laboratory confirmation, from the superficial incision. 2. Organisms isolated from an aseptically obtained culture of fluid or tissue from the superficial incision. 3. At least one of the following signs or symptoms of infection: pain or tenderness, localized swelling, redness, or heat and superficial incision is deliberately opened by surgeon, unless incision is culture-negative. 4. Diagnosis of superficial incisional SSI by the surgeon or attending physician [2]. This can be delineated from deep and organ space surgical site infection because these infections do not involve the underlying muscle, fascia or internal organs. These CDC guidelines were used to define the cases of surgical site infection in this study. Superficial wound separation was defined as any wound that needed to be opened because of non-purulent drainage or opened on its own without evidence of infection, as previously define. Regardless of the etiology responsible for the superficial wound opening (infection or uninfected seroma collection), the end result and management is similar therefore our analysis combined both SSI and SWS and treated the combination as a single entity.
Cases were matched with controls, in a ratio of two controls for every case, during the study period that had the same type of surgery, but did not develop a SSI or a SWS. Controls were matched for age, cancer diagnosis, incision type and medical co-morbidities. Inpatient and outpatient charts were reviewed for demographic information, comorbidities, surgical and postoperative data. Univariate and multivariate analysis were performed using SPSS v16.0 assessing for factors associated with SSI and SWS. Factors that were significant in univariate analysis were incorporated into the multivariate model. All statistical tests were two-tailed with the significance level set at α = 0.05.
Results
Fifty cases were matched with 100 controls, resulting in 150 subjects. Cases and controls had similar demographic characteristics (Table 1). 
Nine co-morbid conditions were identified, including, obesity, defined as a BMI greater than 30 kg/m2, hypertension, diabetes, hypothyroidism, vascular disease, including coronary and peripheral, other cancer, pulmonary disease, including COPD and asthma, tobacco use and chronic renal disease. The only co-morbid condition that showed a statistical difference between the controls and the cases was obesity (p<0.0001) (Table 2).
A univariate analysis was performed reviewing commonly identified risk factors for surgical site infections. As an additional assessment of obesity, the BMI, was analyzed for each of the groups. Average BMI was lower for controls, 27.2 vs. 36.8 kg/m2 (p<0.001). Hypothermia prevention, defined by use of a warming device, type of skin closure, staple vs. suture, and operating time were found to be statistically significant with univariate analysis. Similarly, post-operative data revealed a difference in length of stay (LOS) in the univariate analysis as well. Transfusion rate was lower among controls compared to cases, 10 (10%) vs. 19 (38%) transfusions (p<0.001) (Table 3).
These same data points were then assessed with multivariate analysis. The only statistically significant difference between cases and controls were obesity, represented by BMI >30 kg/m2, and rate of transfusion (Table 4).
Discussion
Surgical site infections are frequent, representing 38% of all postoperative complications [2]. SSI enhances morbidity to patients, increase hospital stays and accrues billions of dollars within the health care system [1]. In order to decrease the incidence of surgical site infections, underlying risk factors need to be identified so that preventative measures can be implemented. Previous works have identified suspected risk factors, but most of these are reported in the cardiac and orthopedic literature [2]. These studies are a helpful starting point, but do not directly address the patients or the surgeries done in gynecologic oncology. In this study, we identified a number of factors in the univariate analysis that were associated with both superficial surgical site infection as well as superficial wound separation. Upon further examination with the multivariate analysis, we isolated 2 independent risk factors for the development of SSI and SWS: obesity, identified as elevated BMI and rate of transfusion.
Obesity is one of the most commonly identified risk factors for endometrial cancer, with up to 40% of cases attributed to underlying obesity [18], and continues to be an increasingly widespread problem in the United States. In fact, the National Health and Nutrition Examination Survey (NHANES) for 2007-2008 showed that 68% of U.S. adults age 20 years and older are overweight or obese [19]. Additionally, adipose tissue has relatively poor vascularization, which leads to poor oxygenation and impaired healing, so it is not surprising that obesity has been shown to be a risk factor for surgical site infections [20]. Furthermore, leptin, which regulates T cell response and is acutely increased during infection and inflammation, is decreased in obesity. Its deficiency increases susceptibility to infectious and inflammatory stimuli and is associated with dysregulation of cytokine production [21]. The challenge is finding a modifiable way to decrease the risk of infection for the obese patients who require surgery. 
Unfortunately, surgery for a gynecologic malignancy cannot be postponed until the patients lose weight, so looking for other measures to decrease risk need to be employed. Forse, et al. looked at increasing the dose of prophylactic antimicrobial agent for morbidly obese patients and found a significant drop in the wound infection rate after the implementation of this process [22]. 
Pevzner, et al. tested the idea that higher doses of antibiotics might be required, by stratifying prophylactic antibiotic amounts by BMI then analyzing antibiotic concentrations in tissue samples. They found that cefazolin concentrations within adipose tissue at skin incision were inversely proportional to maternal BMI. All specimens demonstrated therapeutic levels for gram-positive cocci. However, 20% of obese and 33% of extremely obese patients did not achieve therapeutic levels for gram-negative rods [23]. This report does not look directly at SSI, but certainly raises a concern. Even with the increased doses of antibiotic, we may not be reaching levels that are appropriate for prophylaxis. This may mean that greater doses of antibiotics may need to be administered for increasing BMI.
In this study, need for transfusion was a statistically significant risk factor for development of superficial surgical site infection or wound separation. There have been randomized control trials done in the general surgery and cardiac literature looking at transfusion as a risk factor for SSI that have shown a positive correlation [24-28]. However, these studies are mostly observational in nature, because they did not provide an intention-to-treat analysis and thus were not protected from confounding. Because of this and other studies that have not demonstrated a positive correlation, it has been speculated that need for transfusion may not be a true risk factor and instead may be a surrogate for other processes like underlying anemia or immune modulation from transfusion.
Interestingly, elevated blood loss was not a statistically significant risk factor for SSI or SWS in our analysis. This further suggests that transfusion may be separate process from blood loss or anemia. Other studies have shown increased blood loss to be a risk factor for SSI [6,7]. However, neither of these studies included a multivariate analysis, so there is no control for confounding. This may be a surrogate for anemia and its effect on the body's ability to deliver oxygen needed for wound healing. Moreover, data indicate that a second dose of the prophylactic antibiotic may be appropriate in surgical cases with an increased blood loss, greater than 1,500 mL [29]. Looking at this in a prospective fashion would allow this data to be recorded since it is not otherwise recorded in our medical charts as a dose given for increased blood loss. This could add information to whether increased blood loss and transfusion are separate risk factors.
Ideally, we would avoid the need for transfusion given the associated morbidities beyond the correlation with increased risk for SSI and SWS. This can be a difficult task in gynecologic oncology, given the neovascularization that accompanies cancer and the often complex nature of the surgery which can lead to bleeding inta-operatively and need to maintain hemodynamic stability. However, no one has looked at alternatives to transfusion, like intraoperative autologous blood recovery as possibility for decreasing the risk of subsequent infection. Prospective trials in this area would be helpful to elucidate the role of transfusion as a risk factor. It is important to note that concern has been raised previously about the use of autologous blood in the setting of cancer surgery and subsequent metastases and increased risk of recurrence. In a recent meta-analysis, Waters, et al. show that the data from current studies do not show an increased risk of metastases or recurrence [30].
Limitations
Limitations of this study include the observational retrospective nature and the relatively small sample size. The retrospective nature of the study may have introduced a recall bias in that we did not necessarily captured every single case of SWS or SSI in this time period even though we tried very hard to achieve. In addition, we controlled for the type of abdominal preparation used but it was not possible to control for the actual technique utilized by individual surgeons which is another potential source of bias. Surgical site infections are common, many groups have examined possible modifiable risk factors. However, this has not been done in this population of patients. In a recent paper by Anaya, et al. they examined patients for cancer-specific predictors of postoperative surgical site infections. They developed a stratification tool to help identify cancer patients at increased risk for surgical site infection [31]. At this time, the tool has only been validated internally and its generalizability to other cancer types, like those seen in gynecologic oncology, is still yet to be determined. Consequently, there is still no other literature examining the risk factors for gynecologic oncology patients. Further trials examining the identified risk factors from this study need to be done to validate our findings in a prospective fashion with larger numbers to see if any additional differences are born out. 
Conclusion
Superficial surgical site infection and superficial wound separation is a common complication in gynecologic oncology patients and is associated with obesity and transfusion. This paper highlights a very common problem with multiple associated morbidities that need to be further examined in a prospective, detailed fashion.
Acknowledgment
The authors wish to thank Jeff Lin for his help with statistical analysis.
Conflict of Interest
The authors declare that there are no conflicts of interest and have no funding disclosures.

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Tables & Figures
Table 1: Demographic Data

Table 2: Comorbid Conditions

BMI= Body Mass Index, EBL= estimated blood loss, OR= Operating Room 
Table 3: Univariate Analysis

BMI=Body Mass Index, EBL=estimated blood loss, OR= Operating Room
Table 4:  Multivariable Analysis


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