- Email: [email protected]
Surgical-site infection in gynecologic surgery: pathophysiology and prevention
Accepted Manuscript Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention Holly L. Steiner, MD, Eric A. Strand, MD PII:
S0002-9378(17)30254-5
DOI:
10.1016/j.ajog.2017.02.014
Reference:
YMOB 11534
To appear in:
American Journal of Obstetrics and Gynecology
Received Date: 22 November 2016 Revised Date:
25 January 2017
Accepted Date: 7 February 2017
Please cite this article as: Steiner HL, Strand EA, Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention, American Journal of Obstetrics and Gynecology (2017), doi: 10.1016/ j.ajog.2017.02.014. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention Holly L. STEINER, MD1
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Eric A. STRAND, MD1
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The authors report no conflict of interest.
Please address reprint requests to:
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Holly L. Steiner, MD Department of Obstetrics and Gynecology
Washington University School of Medicine 4911 Barnes Jewish Plaza Campus Box 8064
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St. Louis, MO 63110 314-362-4211
Correspondence:
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[email protected]
Holly L. Steiner, MD
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Department of Obstetrics and Gynecology Washington University School of Medicine 4911 Barnes Jewish Plaza Campus Box 8064
St. Louis, MO 63110 314-362-4211 (office) 314-222-6245 (fax) 314-282-0170 (home)
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[email protected] Abstract: 147 words
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Main Text: 3482 words 1
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Department of Obstetrics and Gynecology, Division of General Obstetrics and Gynecology, Washington University, St. Louis, MO
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Condensation: Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention
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We discuss the epidemiology and pathophysiology of surgical site infections (SSIs) in
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gynecology, with a review of the available literature regarding SSI prevention.
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Abstract:
Surgical site infections (SSIs) represent a well-known cause of patient morbidity as well
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as added healthcare costs. In gynecologic surgery, particularly hysterectomy, SSIs are often the result of a number of risk factors that may or may not be modifiable. As both the Centers for Medicaid and Medicare Services and the Joint Commission on the Accreditation of Healthcare
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Organizations have identified SSIs as a patient safety priority, gynecologic surgeons continue to seek out the most effective interventions for SSI prevention. This review studies the
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epidemiology and pathophysiology of SSIs in gynecologic surgery and evaluates the current literature regarding possible interventions for SSI prevention, both as individual measures and as bundles. Data from the obstetrical and general surgery literature will be reviewed when gynecological data is either unclear or unavailable. Practitioners and hospitals may use this
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information as they develop strategies for SSI prevention in their own practice.
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hyperglycemia
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Key words: Surgical site infection, hysterectomy, prophylactic antibiotics, skin antisepsis,
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Introduction Surgical site infection (SSI) represents a significant source of surgical morbidity and mortality. SSIs complicate roughly 2-5% of all surgeries, including approximately 2% of
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hysterectomies.1,2 These estimates are most likely low, as many infections occur after hospital discharge, and patients may present to other healthcare facilities for care.1 These infections result in significant social and economic costs for the patient and the healthcare system; for
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example, each SSI related to hysterectomy is estimated to add $5,000 in patient costs.3,4
Recent initiatives by the Centers for Medicaid and Medicare Services and the Joint
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Commission on the Accreditation of Healthcare Organizations (JCAHO) have identified SSI as a patient safety priority. In an effort to limit SSIs, the JCAHO developed several accountability measures, including timing and selection of prophylactic antibiotics, pre-operative glucose control, and appropriate hair removal.5 Despite these and other initiatives, SSIs are still a
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significant burden for our gynecologic patients. The purpose of this review is to outline the pathophysiology and risk factors involved in the development of SSIs, describe the various evidence-based interventions that may decrease SSI occurrence, and provide suggestions
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Definition
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regarding interventions for clinical practice.
The Centers for Disease Control define an SSI as “an infection related to an operative
procedure that occurs at or near the surgical incision within 30 days.”6 This time frame is extended to 12 months if a surgical implant is used. Infections can be further categorized as (Figure 1)7: •
Superficial incisional: involving the skin and subcutaneous tissues
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•
Deep incisional: involving the deeper soft tissues of the incision, such as muscle or fascia
•
Organ/Space: involving any part of the anatomy other than the incised body layers (skin,
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fascia, and muscle layers)
In gynecologic surgery, SSIs generally fit into these categories, including superficial incisional cellulitis, deep incisional abscesses, and pelvic or vaginal cuff abscess formation.
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Approximately two-thirds of gynecologic SSIs are superficial incisional infections.8
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Pathophysiology
Many gynecologic surgeries, including hysterectomies, are classified as “clean contaminated” procedures, implying that the genital tract is entered in a controlled fashion and without unusual contamination.9 During a hysterectomy, the surgical site is exposed to a unique
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variety of endogenous flora, including common bacteria of the skin, gastrointestinal tract, and vaginal tract. Selection of prophylactic antibiotics must consider the need to cover a variety of gram positive, gram negative, and anaerobic organisms (Figure 2).10
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SSIs arise from a complex interaction of several factors, including the type and number of contaminating bacteria, the virulence of those bacteria, and the resistance of the patient
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involved.11 Bacteria involved may originate from the host patient or arise from other sources, such as the surgical personnel, equipment, and the operating room environment. The presence of a foreign body, such as an implant or mesh, is also relevant, as studies have shown the “dose” of contaminating bacteria required to cause an infection is lower in the presence of foreign material.12
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Patient characteristics that impact the risk of SSI are numerous. Increasing rates of obesity pose a significant problem as obesity contributes to infection in many ways—poor nutritional status, limited surgical visualization, longer operating times, decreased oxygenation
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of tissues, and decreased antibiotic penetration—and has consistently been associated with
increased rates of SSI.13,14 Tobacco use is a known cause of tissue ischemia and delayed wound healing, leading to increased rates of SSI.15 Increased operative time has been consistently
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shown to increase SSI rates in a variety of settings, possibly due to temperature regulation,
inflammation, and anesthesia management.16,17 Hyperglycemia in diabetics is a well-known risk
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factor for several surgical complications, including SSIs.17,18
Additional risk factors are shown in Figure 3.19 Many of these factors are amenable to risk-reduction interventions by the surgical team—examples include administration of prophylactic antibiotics, abdominal skin and vaginal preparation, meticulous surgical technique,
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and maintenance of glycemic control. However, other risk factors, such as obesity, a history of multiple prior surgeries, or encouraging smoking cessation are much harder to modify. Given that only some factors are amenable to intervention, gynecologic surgeons should be well-
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educated regarding the evidence for interventions that reduce SSIs in their patients. The
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remainder of this review will focus on providing evidence-based strategies for SSI reduction. Preoperative factors
The idea of washing or bathing with an antimicrobial wash before surgery has long been
suggested as a means to decrease overall bacterial counts on the skin and thus decrease SSI risk. A Cochrane meta-analysis20 reviewed seven trials comparing different antiseptic washes (4% chlorhexidine scrub, povodine iodine, or regular bar soap) to no wash or placebo. Although SSI incidences did not significantly differ between those using chlorhexidine vs. other wash solutions
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before surgery, use of chlorhexidine was associated with a lower incidence of SSI when compared to no wash in one large study (RR 0.36, 95% CI 0.17 to 0.79).21 The findings of the Cochrane meta-analysis may be explained by either poor washing technique or the lack of a
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specific washing protocol. Indeed, a study performed by Edmiston et al.22 showed significantly higher (P <0.001) chlorhexidine concentrations on the skin after two sequential showers with at least a one-minute pause before rinsing. These levels were above the 90% minimum inhibitory
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concentrations for most gram negative and positive surgical wound pathogens. Using this standardized approach would likely correct deficiencies in current non-standardized
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preadmission shower protocols for patients undergoing elective surgery and thus help decrease overall SSI rates.
Traditionally, hair has been removed before surgery in an attempt to reduce SSI risk. However, a 2011 Cochrane review of six trials involving 972 patients comparing hair removal
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versus no hair removal found no statistically significant difference in SSI rates between the two groups, suggesting that hair removal has no impact on decreasing SSI rates.23 However, this review did find a higher risk of SSI with hair shaving than with clipping (RR 2.09, 95% CI 1.15
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to 3.80). There were no data to support different time frames for hair removal (i.e., day before or
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day of surgery). Therefore, when removal of hair is desired to facilitate the creation of the incision, improve visualization, or enhance the use of a post-operative dressing, clipping should be the preferred approach.
Bacterial vaginosis (BV) is a known risk factor for vaginal cuff infection after
hysterectomy.24 While BV should be treated when identified preoperatively, there are no studies to suggest that routine preoperative screening is warranted. In addition, many of the studies linking BV to vaginal cuff infections occurred before universally timed antibiotic prophylaxis
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was the standard of care.25,26 However, a decision analysis performed by McElligott et al27 investigating three different strategies (screen all patients and treat if positive, treat all patients, or neither screen nor treat) found the strategy of treating all patients prophylactically for BV to
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be most cost effective based on documented rates of vaginal cuff cellulitis. Clinical trials should confirm these findings before universal treatment for BV is adopted for infection prevention. Methicillin resistant staphylococcus aureus (MRSA) is becoming an increasingly
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common pathogen in surgical site infections. Patients can often be colonized from prior
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hospitalizations.28 The literature regarding MRSA decontamination in the gynecologic population is somewhat limited; overall, it does not seem to reduce SSI with any statistical significance.29,30 The impact appears limited to clean surgical procedures, whereas gynecologic procedures are largely clean contaminated. Thus, we do not recommend universal screening for
Intraoperative factors
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MRSA carriage in the gynecologic population.
While certain clinical scenarios dictate a particular surgical approach, evidence
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consistently supports that minimally invasive surgical techniques can decrease the rates of SSI. Several studies have shown that patients undergoing laparoscopic hysterectomies (using either a
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traditional laparoscopic approach or robotic technology) experience about a 50% reduction in SSI incidence compared to those undergoing open abdominal hysterectomies.13,31,32 For this and other reasons, ACOG recommends a minimally invasive approach (vaginal or laparoscopic) when feasible.33
Preoperative antibiotic prophylaxis is now the standard of care for all hysterectomies.34 The preferred option is a single dose of a β-lactam antibiotic, most commonly cefazolin 1-2 g
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intravenous (IV). Based upon pharmacokinetic data in obese patients,35-37 several authors have recommended an increased dose of 3 g for obese patients.38,39 Secondary options for patients with severe penicillin allergies include clindamycin 600 mg IV plus gentamicin 1.5 mg/kg IV or
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metronidazole 500 mg IV plus gentamicin 1.5 mg/kg IV.24 Antibiotics should be administered 30-60 minutes prior to skin incision to provide optimal infection prevention.40 Adjustments and re-dosing of the drugs may be made for morbidly obese patients or for intraoperative factors such
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as an operative length >3 hours or excessive blood loss. A recent study by Uppal et al.41 found that SSI rates were higher in hysterectomy patients who received β-lactam alternatives (such as
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clindamycin/gentamicin or metronidazole/gentamicin) or non-standardized antibiotics (such as clindamycin or gentamicin alone) than in those who received traditional β-lactam antibiotic prophylaxis. Given that β-lactams seem to be the most effective agents for preventing SSI, this study highlights the importance of investigating a patient’s reported β-lactam allergy.
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For skin antisepsis, a large randomized controlled trial involving patients undergoing clean-contaminated surgeries found that chlorhexidine-alcohol was significantly more effective than a povidone-iodine scrub in preventing superficial (4.2% vs. 8.6%, P=0.008) and deep (1%
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vs 3%, P=0.05) incisional infections.42 Several other smaller studies have reported similar findings.43,44 Within the Cochrane meta-analysis, a mixed treatment comparison analysis
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concluded that alcohol-based preparations have the highest probability of effectiveness.45 Thus, although none of these studies specifically addressed gynecologic surgeries, selecting a chlorhexidine-alcohol-based skin preparation seems to be justified. Decreasing overall bacterial counts in the vagina has been proven to reduce the risk of SSI in gynecologic surgeries.46 Traditionally, povodine-iodine preparations were used in the vagina, but trends are shifting towards chlorhexidine-based preparations. Chlorhexidine more
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effectively reduces vaginal bacterial counts47 and remains effective even in the presence of blood, unlike povodine-iodine.48 Surgeons have often been reluctant to use chlorhexidine in the vagina because of the potential for irritation, allergic reactions, and the risk of electrosurgical
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burns due to the alcohol content. However, in concentrations of 4% or less, the solution seems to be well tolerated and its use is supported by the American College of Obstetricians and Gynecologists.48
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The peritoneal cavity is often irrigated during surgery. The traditional teaching promoted
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the idea that irrigation, by reducing operative debris and contaminants, may reduce the risk of infection.49 Overall, the studies regarding intra-abdominal irrigation either report no apparent impact in reducing SSI risk 50-53 or show a possible effect but have a considerable risk of bias.54 The available evidence indicates that irrigation is unlikely to play a role in SSI prevention.
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The data for drain placement is somewhat mixed but appears to argue against the use of routine, prophylactic drain placement. The majority of information, however, comes from the obstetric, rather than the gynecologic, literature.55-58 Outside of this literature, Kosins et al.59
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performed a large systematic review and meta-analysis in 2013 to determine the value of prophylactic subcutaneous drain placement in various surgical wounds. When specifically
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assessing abdominal surgical procedures, their group found no benefit to prophylactic drain placement for the prevention of hematoma, seroma, or infection, even in obese patients. In gynecologic patients with 3 cm or more subcutaneous fat and a vertical midline incision, Cardosi et al.60 found no differences in wound infections or overall complication rates between skin closure techniques with or without closed suction drainage. The data for subcutaneous tissue reapproximation is not straightforward in benign gynecology. In obstetrics, the literature has shown that for patients with >2 cm of subcutaneous
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tissue, closure of the dead space reduces wound separation and seroma formation.61,62 However, in a 2014 Cochrane review of six studies including 815 patients with “non-cesarean” surgeries, rates of SSI or superficial dehiscence were not improved by closure of the subcutaneous tissue.63
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Only two of the six trials were in gynecologic patients, both involving patients with vertical midline incisions and a subcutaneous tissue depth of >2 cm. Given the paucity of data, future studies are needed to examine this area, especially given that the depth of the subcutaneous tissue
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is considered an independent risk factor for wound complications.64
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When planning for skin closure, limited data for gynecologic patients lead us to rely on the obstetrical literature for guidance. Multiple studies65-68 have shown subcuticular suturing to be superior to staples in decreasing the incidence of wound complications and SSI during cesarean delivery. In contrast, a randomized controlled trial performed in general surgery patients found no differences in SSI rates (P=0.882) between laparotomy closure with
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subcuticular sutures or staples 69 Although these data are conflicting, it is important to note that most of the general surgery patients underwent gastrointestinal, pancreatic, or hepatobiliary surgeries, and a large portion received intra-abdominal drains. In addition, the bacterial flora
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encountered at the time of hysterectomy more closely resemble that encountered at cesarean
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delivery, making reliance on available obstetrical data a reasonable approach. A 2014 Cochrane review studying skin closure found that sutures were significantly
better than tissue adhesives for reducing the risk of wound dehiscence.70 No other differences were noted between suture and tissue adhesives in regard to infection rates, and no evidence suggested that the use of both adhesives and suture would provide a superior result. Of note, one study 66 also investigated various suture types (braided vs. mono-filament) and found no difference in the distribution of wound complications. Given the available data, using suture to
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approximate the skin seems to be indicated. The type of suture may be left to the surgeon’s discretion.
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Thermoregulation has been suggested as an important intraoperative adjunct to prevent SSI. Decreased temperature leads to vasoconstriction, lowering oxygen tension in tissues and impairing oxidative killing of bacteria by neutrophils. A randomized controlled study from the mid 1990’s showed that colorectal patients who maintained normothermia during surgery had
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lower rates of wound complications than those who became hypothermic during surgery.71
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However, this study may have been biased as patients in the hypothermia group were more likely to receive a blood transfusion, a known risk factor for SSI. Numerous contemporary studies in the colorectal literature have failed to document decreased SSI rates with various intraoperative protocols for maintaining normothermia.72-74 Despite the mixed data, hypothermia causes other harms, including impaired drug metabolism, cardiac dysfunction, and coagulopathy. Thus, we
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strongly recommend maintenance of normothermia even though its impact on SSI risk is likely negligible.
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Supplemental intraoperative oxygen has several proposed benefits that may lead to reduced incidence of SSI. These include increased oxygen exposure to the tissue bed leading to
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increased collagen deposition and improved immune function. Additionally, the activity of antibiotics may be amplified at higher levels of oxygen.75 Although there is some suggestion that hyperoxia may help prevent SSIs in colorectal surgery, the available data have generally not supported this conclusion in gynecologic surgery.51, 76 Postoperative factors
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Hyperglycemia in diabetics is a well-known risk factor for several surgical complications, including SSIs.17,18 Although optimizing postoperative blood sugar levels is an important method to decrease SSI rates, the impact of “aggressive” glucose control seems less clear. A
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Cochrane review from 200977 comparing strict glycemic control versus conventional
management (maintenance of glucose <200 mg/dL) for the prevention of SSI concluded the evidence was insufficient to support strict glycemic control. The authors did note significant
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heterogeneity between the studies, which limited their ability to perform the meta-analysis. However, a more recent study by Al-Niaimi et al. suggests that aggressive management
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significantly reduces SSI rates in postsurgical diabetic patients.78 In this retrospective study, gynecologic surgery patients with a glucose above 150 mg/dL were managed with either intermittent subcutaneous insulin injections or an insulin infusion. Once started, the insulin infusion was continued for 24 hours. The authors showed that patients whose hyperglycemia was
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managed via insulin infusion had significantly lower SSI rates than those who received subcutaneous insulin (19% vs 29%, P=0.001). Even more compelling, the authors found that the SSI rate for patients on the insulin infusion was comparable to that for patients who did not have
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diabetes.
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Emerging evidence indicates that post-operative glycemic control may be important even in the non-diabetic population. Stress hyperglycemia, a natural phenomenon that results after illness or injury, can have multiple consequences, including impaired immune function, stimulation of inflammatory markers, increased thrombotic activity, and endothelial cell dysfunction.79 In a review of the Surgical Care and Outcomes Assessment Program in Washington, Kwon et al.80 evaluated the effects of perioperative hyperglycemia (glucose >180 mg/dL) and insulin administration on various outcomes for >11,000 patients undergoing bariatric
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and colorectal surgeries. The authors found an increased risk of SSI for all patients experiencing hyperglycemia, regardless of whether or not they carried a pre-operative diagnosis of diabetes. In this study, 13.5% of the non-diabetic patients experienced hyperglycemia, and the greatest risk
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of infection existed in the patients with no history of diabetes experiencing hyperglycemia. Regardless of diabetic status, insulin administration mitigated the SSI risk for both groups. Often, the argument against strict glucose control is to avoid the side effects of
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hypoglycemia that can occur with over-aggressive insulin administration, including seizures or
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even death. However, as demonstrated in the Al-Niaimi et al. study,78 the incidence of hypoglycemic events may be decreased by following a clear protocol of insulin infusion instead of subcutaneous insulin injection (0.7 vs. 5.4%, P <0.05). Although further studies are needed in benign gynecologic populations, tight glycemic control may prove beneficial in reducing SSI
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rates in both diabetic and non-diabetic patients.
The surgical dressing was once thought to prevent SSIs by protecting the surgical wound from outside bacterial contamination until initial epithelization can occur. However, recent data
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in the general surgery literature indicate that this may not be the case. A large systematic review in 2012 concluded that SSI rates did not differ between those who did and did not receive
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surgical dressings.81 A 2014 Cochrane review failed to find evidence suggesting that surgical dressings reduce the SSI risk or that any one type of dressing is preferred over another.82 Similarly, a 2015 Cochrane review found that removal of surgical dressings within the first 48 hours did not increase SSI rates.83 In the obstetrical literature, a study by Peleg et al.84 compared dressing removal at 6 versus 24 hours after cesarean section. They found no differences in wound dehiscence or SSI rates between the groups. In general, a post-operative dressing should
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be chosen on the basis of cost and symptom management properties, as it is unlikely to affect SSI rates.
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Perioperative blood transfusions are an independent risk factor for SSIs.3,17,85,86 Given this association, we recommend limiting their use based on clinical indications and not on predefined hemoglobin values.
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Use of SSI Prevention Bundles
Many groups have investigated the potential benefit of creating, and following, SSI
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prevention bundles. One nice example involved a review from the Michigan Surgical Quality Collaborative performed by Waits et al.87 In evaluating >4000 patients undergoing colectomies, the authors assessed compliance with a group of six perioperative measures that were independently associated with SSI risk:
Appropriate selection of prophylactic antibiotics
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Post-operative normothermia (T>98.6oF)
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Oral antibiotics with mechanical bowel prep
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Post-operative day #1 glucose ≤ 140 mg/dL
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Minimally invasive approach
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•
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•
Short operative time <100 minutes
The authors found a strong, stepwise, inverse association between SSI rates and the number of measures followed (Figure 4). Although not all of the measures (i.e., surgical time or minimally invasive approach) are always under the surgeon’s control, the finding that these measures prevented SSI in a stepwise fashion shows the potential for SSI bundles to be more beneficial than implementing any single step for prevention.
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The effectiveness of SSI prevention bundles has also been shown in a colorectal surgery meta-analysis,88 in cesarean delivery,89 and in the gynecologic oncology population.90 A thorough SSI prevention bundle for benign gynecology has recently been published by the
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Council on Patient Safety in Women’s Health Care.91 Although the specific measures vary
between studies, most have focused on antibiotic administration, appropriate hair removal (when indicated), normothermia, and glycemic control.
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Conclusion
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SSI represents a significant source of post-operative morbidity for gynecologic surgery patients. Gynecologic surgeries, particularly hysterectomies, expose the surgical site to a variety of endogenous bacteria unique to our specialty. Although several preoperative risk factors (e.g., obesity, prior surgery, ability to pursue a minimally invasive approach) may not be within the
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surgeon’s control, several evidence-based interventions can limit the incidence of SSIs. Research on SSI bundles also indicates that implementation of several evidence-based strategies is likely to have a larger impact than pursuing any single intervention. Interventions clearly
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supported by the literature include the timely administration of appropriately selected prophylactic antibiotics, use of a chlorhexidine-alcohol based prep, use of suture for skin closure,
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and maintenance of glycemic control in the postoperative period. The impact of preserving normothermia on SSIs is less clear but should be standard practice given the potential harms associated with hypothermia. Several interventions, including the use of specified pre-operative chlorhexidine shower protocols, universal pre-operative screening for bacterial vaginosis, reapproximation of the subcutaneous tissue, and the use of peri-operative or post-operative hyperoxia, should be further investigated in the continued effort to decrease the occurrence of SSI in our patients.
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18. Martin ET, Kaye KS, Knott C, et al. Diabetes and Risk of Surgical Site Infection: A Systematic Review and Meta-analysis. Infect Control Hosp Epidemiol 2016; 37(1): 88-99. 19. Anderson DJ, Podgorny K, Berrios-Torres SI, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 update. Infection control and hospital epidemiology 2014; 35(6): 605-27. 20. Webster J, Osborne S. Preoperative bathing or showering with skin antiseptics to prevent surgical site infection. Cochrane Database Syst Rev 2015; (2): CD004985. 21. Wihlborg O. The effect of washing with chlorhexidine soap on wound infection rate in general surgery. A controlled clinical study. Ann Chir Gynaecol 1987; 76(5): 263-5. 22. Edmiston CE, Jr., Lee CJ, Krepel CJ, et al. Evidence for a Standardized Preadmission Showering Regimen to Achieve Maximal Antiseptic Skin Surface Concentrations of Chlorhexidine Gluconate, 4%, in Surgical Patients. JAMA Surg 2015; 150(11): 1027-33. 23. Tanner J, Norrie P, Melen K. Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev 2011; (11): CD004122. 24. Bulletins--Gynecology ACoP. ACOG practice bulletin No. 104: antibiotic prophylaxis for gynecologic procedures. Obstet Gynecol 2009; 113(5): 1180-9. 25. Larsson PG, Carlsson B. Does pre- and postoperative metronidazole treatment lower vaginal cuff infection rate after abdominal hysterectomy among women with bacterial vaginosis? Infectious diseases in obstetrics and gynecology 2002; 10(3): 133-40. 26. Persson E, Bergstrom M, Larsson PG, et al. Infections after hysterectomy. A prospective nation-wide Swedish study. The Study Group on Infectious Diseases in Obstetrics and Gynecology within the Swedish Society of Obstetrics and Gynecology. Acta obstetricia et gynecologica Scandinavica 1996; 75(8): 757-61. 27. McElligott KA, Havrilesky LJ, Myers ER. Preoperative screening strategies for bacterial vaginosis prior to elective hysterectomy: a cost comparison study. Am J Obstet Gynecol 2011; 205(5): 500 e1-7. 28. Edmiston CE, Jr., Ledeboer NA, Buchan BW, Spencer M, Seabrook GR, Leaper D. Is Staphylococcal Screening and Suppression an Effective Interventional Strategy for Reduction of Surgical Site Infection? Surg Infect (Larchmt) 2016; 17(2): 158-66. 29. Pofahl WE, Goettler CE, Ramsey KM, Cochran MK, Nobles DL, Rotondo MF. Active surveillance screening of MRSA and eradication of the carrier state decreases surgical-site infections caused by MRSA. J Am Coll Surg 2009; 208(5): 981-6; discussion 6-8. 30. Perl TM, Cullen JJ, Wenzel RP, et al. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 2002; 346(24): 1871-7. 31. Gandaglia G, Ghani KR, Sood A, et al. Effect of minimally invasive surgery on the risk for surgical site infections: results from the National Surgical Quality Improvement Program (NSQIP) Database. JAMA surgery 2014; 149(10): 1039-44. 32. Roy S, Patkar A, Daskiran M, Levine R, Hinoul P, Nigam S. Clinical and economic burden of surgical site infection in hysterectomy. Surgical infections 2014; 15(3): 266-73. 33. ACOG Committee Opinion No. 444: choosing the route of hysterectomy for benign disease. Obstetrics and gynecology 2009; 114(5): 1156-8. 34. Bratzler DW, Houck PM, Surgical Infection Prevention Guideline Writers W. Antimicrobial prophylaxis for surgery: an advisory statement from the National Surgical Infection Prevention Project. Am J Surg 2005; 189(4): 395-404. 35. Edmiston CE, Krepel C, Kelly H, et al. Perioperative antibiotic prophylaxis in the gastric bypass patient: do we achieve therapeutic levels? Surgery 2004; 136(4): 738-47.
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36. Swank ML, Wing DA, Nicolau DP, McNulty JA. Increased 3-gram cefazolin dosing for cesarean delivery prophylaxis in obese women. American journal of obstetrics and gynecology 2015; 213(3): 415.e1-8. 37. Pevzner L, Swank M, Krepel C, Wing DA, Chan K, Edmiston CE, Jr. Effects of maternal obesity on tissue concentrations of prophylactic cefazolin during cesarean delivery. Obstetrics and gynecology 2011; 117(4): 877-82. 38. Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. American journal of health-system pharmacy : AJHP : official journal of the American Society of Health-System Pharmacists 2013; 70(3): 195-283. 39. Lachiewicz MP, Moulton LJ, Jaiyeoba O. Pelvic surgical site infections in gynecologic surgery. Infectious diseases in obstetrics and gynecology 2015; 2015: 614950. 40. Classen DC, Evans RS, Pestotnik SL, Horn SD, Menlove RL, Burke JP. The timing of prophylactic administration of antibiotics and the risk of surgical-wound infection. The New England journal of medicine 1992; 326(5): 281-6. 41. Uppal S, Harris J, Al-Niaimi A, et al. Prophylactic Antibiotic Choice and Risk of Surgical Site Infection After Hysterectomy. Obstetrics and gynecology 2016; 127(2): 321-9. 42. Darouiche RO, Wall MJ, Jr., Itani KM, et al. Chlorhexidine-Alcohol versus PovidoneIodine for Surgical-Site Antisepsis. N Engl J Med 2010; 362(1): 18-26. 43. Paocharoen V, Mingmalairak C, Apisarnthanarak A. Comparison of surgical wound infection after preoperative skin preparation with 4% chlorhexidine [correction of chlohexidine] and povidone iodine: a prospective randomized trial. J Med Assoc Thai 2009; 92(7): 898-902. 44. Rodrigues AL, Simoes Mde L. Incidence of surgical site infection with pre-operative skin preparation using 10% polyvidone-iodine and 0.5% chlorhexidine-alcohol. Rev Col Bras Cir 2013; 40(6): 443-8. 45. Dumville JC, McFarlane E, Edwards P, Lipp A, Holmes A. Preoperative skin antiseptics for preventing surgical wound infections after clean surgery. Cochrane Database Syst Rev 2013; (3): CD003949. 46. Eason E, Wells G, Garber G, et al. Antisepsis for abdominal hysterectomy: a randomised controlled trial of povidone-iodine gel. BJOG 2004; 111(7): 695-9. 47. Culligan PJ, Kubik K, Murphy M, Blackwell L, Snyder J. A randomized trial that compared povidone iodine and chlorhexidine as antiseptics for vaginal hysterectomy. Am J Obstet Gynecol 2005; 192(2): 422-5. 48. American College of O, Gynecologists Women's Health Care P, Committee on Gynecologic P. Committee Opinion No. 571: Solutions for surgical preparation of the vagina. Obstet Gynecol 2013; 122(3): 718-20. 49. Edmiston CE, Jr., Leaper DJ. Intra-Operative Surgical Irrigation of the Surgical Incision: What Does the Future Hold-Saline, Antibiotic Agents, or Antiseptic Agents? Surg Infect (Larchmt) 2016. 50. Temizkan O, Asicioglu O, Gungorduk K, Asicioglu B, Yalcin P, Ayhan I. The effect of peritoneal cavity saline irrigation at cesarean delivery on maternal morbidity and gastrointestinal system outcomes. J Matern Fetal Neonatal Med 2016; 29(4): 651-5. 51. Eke AC, Shukr GH, Chaalan TT, Nashif SK, Eleje GU. Intra-abdominal saline irrigation at cesarean section: a systematic review and meta-analysis. J Matern Fetal Neonatal Med 2016; 29(10): 1588-94. 52. Al-Ramahi M, Bata M, Sumreen I, Amr M. Saline irrigation and wound infection in abdominal gynecologic surgery. Int J Gynaecol Obstet 2006; 94(1): 33-6.
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53. Schein M, Gecelter G, Freinkel W, Gerding H, Becker PJ. Peritoneal lavage in abdominal sepsis. A controlled clinical study. Arch Surg 1990; 125(9): 1132-5. 54. Mueller TC, Loos M, Haller B, et al. Intra-operative wound irrigation to reduce surgical site infections after abdominal surgery: a systematic review and meta-analysis. Langenbecks Arch Surg 2015; 400(2): 167-81. 55. Al-Inany H, Youssef G, Abd ElMaguid A, Abdel Hamid M, Naguib A. Value of subcutaneous drainage system in obese females undergoing cesarean section using pfannenstiel incision. Gynecol Obstet Invest 2002; 53(2): 75-8. 56. Ramsey PS, White AM, Guinn DA, et al. Subcutaneous tissue reapproximation, alone or in combination with drain, in obese women undergoing cesarean delivery. Obstet Gynecol 2005; 105(5 Pt 1): 967-73. 57. Magann EF, Chauhan SP, Rodts-Palenik S, Bufkin L, Martin JN, Jr., Morrison JC. Subcutaneous stitch closure versus subcutaneous drain to prevent wound disruption after cesarean delivery: a randomized clinical trial. Am J Obstet Gynecol 2002; 186(6): 1119-23. 58. Gates S, Anderson ER. Wound drainage for caesarean section. Cochrane Database Syst Rev 2013; (12): CD004549. 59. Kosins AM, Scholz T, Cetinkaya M, Evans GR. Evidence-based value of subcutaneous surgical wound drainage: the largest systematic review and meta-analysis. Plast Reconstr Surg 2013; 132(2): 443-50. 60. Cardosi RJ, Drake J, Holmes S, et al. Subcutaneous management of vertical incisions with 3 or more centimeters of subcutaneous fat. American journal of obstetrics and gynecology 2006; 195(2): 607-14; discussion 14-6. 61. Chelmow D, Huang E, Strohbehn K. Closure of the subcutaneous dead space and wound disruption after Cesarean delivery. J Matern Fetal Neonatal Med 2002; 11(6): 403-8. 62. Naumann RW, Hauth JC, Owen J, Hodgkins PM, Lincoln T. Subcutaneous tissue approximation in relation to wound disruption after cesarean delivery in obese women. Obstet Gynecol 1995; 85(3): 412-6. 63. Gurusamy KS, Toon CD, Davidson BR. Subcutaneous closure versus no subcutaneous closure after non-caesarean surgical procedures. Cochrane Database Syst Rev 2014; (1): CD010425. 64. Soper DE, Bump RC, Hurt WG. Wound infection after abdominal hysterectomy: effect of the depth of subcutaneous tissue. Am J Obstet Gynecol 1995; 173(2): 465-9; discussion 9-71. 65. Figueroa D, Jauk VC, Szychowski JM, et al. Surgical staples compared with subcuticular suture for skin closure after cesarean delivery: a randomized controlled trial. Obstet Gynecol 2013; 121(1): 33-8. 66. Mackeen AD, Khalifeh A, Fleisher J, et al. Suture compared with staple skin closure after cesarean delivery: a randomized controlled trial. Obstet Gynecol 2014; 123(6): 1169-75. 67. Tuuli MG, Rampersad RM, Carbone JF, Stamilio D, Macones GA, Odibo AO. Staples compared with subcuticular suture for skin closure after cesarean delivery: a systematic review and meta-analysis. Obstet Gynecol 2011; 117(3): 682-90. 68. Zaki MN, Truong M, Pyra M, Kominiarek MA, Irwin T. Wound complications in obese women after cesarean: a comparison of staples versus subcuticular suture. J Perinatol 2016; 36(10): 819-22. 69. Imamura K, Adachi K, Sasaki R, et al. Randomized Comparison of Subcuticular Sutures Versus Staples for Skin Closure After Open Abdominal Surgery: a Multicenter Open-Label Randomized Controlled Trial. J Gastrointest Surg 2016.
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70. Dumville JC, Coulthard P, Worthington HV, et al. Tissue adhesives for closure of surgical incisions. Cochrane Database Syst Rev 2014; (11): CD004287. 71. Kurz A, Sessler DI, Lenhardt R. Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N Engl J Med 1996; 334(19): 1209-15. 72. Baucom RB, Phillips SE, Ehrenfeld JM, et al. Association of Perioperative Hypothermia During Colectomy With Surgical Site Infection. JAMA Surg 2015; 150(6): 570-5. 73. Geiger TM, Horst S, Muldoon R, et al. Perioperative core body temperatures effect on outcome after colorectal resections. Am Surg 2012; 78(5): 607-12. 74. Melton GB, Vogel JD, Swenson BR, Remzi FH, Rothenberger DA, Wick EC. Continuous intraoperative temperature measurement and surgical site infection risk: analysis of anesthesia information system data in 1008 colorectal procedures. Ann Surg 2013; 258(4): 60612; discussion 12-3. 75. Munoz-Price LS, Sands L, Lubarsky DA. Effect of high perioperative oxygen supplementation on surgical site infections. Clin Infect Dis 2013; 57(10): 1465-72. 76. Wetterslev J, Meyhoff CS, Jorgensen LN, Gluud C, Lindschou J, Rasmussen LS. The effects of high perioperative inspiratory oxygen fraction for adult surgical patients. Cochrane Database Syst Rev 2015; (6): CD008884. 77. Kao LS, Meeks D, Moyer VA, Lally KP. Peri-operative glycaemic control regimens for preventing surgical site infections in adults. Cochrane Database Syst Rev 2009; (3): CD006806. 78. Al-Niaimi AN, Ahmed M, Burish N, et al. Intensive postoperative glucose control reduces the surgical site infection rates in gynecologic oncology patients. Gynecol Oncol 2015; 136(1): 71-6. 79. Kao LS, Phatak UR. Glycemic control and prevention of surgical site infection. Surg Infect (Larchmt) 2013; 14(5): 437-44. 80. Kwon S, Thompson R, Dellinger P, Yanez D, Farrohki E, Flum D. Importance of perioperative glycemic control in general surgery: a report from the Surgical Care and Outcomes Assessment Program. Annals of surgery 2013; 257(1): 8-14. 81. Walter CJ, Dumville JC, Sharp CA, Page T. Systematic review and meta-analysis of wound dressings in the prevention of surgical-site infections in surgical wounds healing by primary intention. Br J Surg 2012; 99(9): 1185-94. 82. Dumville JC, Gray TA, Walter CJ, Sharp CA, Page T. Dressings for the prevention of surgical site infection. Cochrane Database Syst Rev 2014; (9): CD003091. 83. Toon CD, Lusuku C, Ramamoorthy R, Davidson BR, Gurusamy KS. Early versus delayed dressing removal after primary closure of clean and clean-contaminated surgical wounds. Cochrane Database Syst Rev 2015; (9): CD010259. 84. Peleg D, Eberstark E, Warsof SL, Cohen N, Ben Shachar I. Early wound dressing removal after scheduled cesarean delivery: a randomized controlled trial. Am J Obstet Gynecol 2016; 215(3): 388 e1-5. 85. Young H, Berumen C, Knepper B, et al. Statewide collaboration to evaluate the effects of blood loss and transfusion on surgical site infection after hysterectomy. Infect Control Hosp Epidemiol 2012; 33(1): 90-3. 86. Mahdi H, Gojayev A, Buechel M, et al. Surgical site infection in women undergoing surgery for gynecologic cancer. Int J Gynecol Cancer 2014; 24(4): 779-86. 87. Waits SA, Fritze D, Banerjee M, et al. Developing an argument for bundled interventions to reduce surgical site infection in colorectal surgery. Surgery 2014; 155(4): 602-6.
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88. Tanner J, Padley W, Assadian O, Leaper D, Kiernan M, Edmiston C. Do surgical care bundles reduce the risk of surgical site infections in patients undergoing colorectal surgery? A systematic review and cohort meta-analysis of 8,515 patients. Surgery 2015; 158(1): 66-77. 89. Hsu CD, Cohn I, Caban R. Reduction and sustainability of cesarean section surgical site infection: An evidence-based, innovative, and multidisciplinary quality improvement intervention bundle program. American journal of infection control 2016; 44(11): 1315-20. 90. Johnson MP, Kim SJ, Langstraat CL, et al. Using Bundled Interventions to Reduce Surgical Site Infection After Major Gynecologic Cancer Surgery. Obstetrics and gynecology 2016; 127(6): 1135-44. 91. Pellegrini JE, Toledo P, Soper DE, et al. Consensus Bundle on Prevention of Surgical Site Infections After Major Gynecologic Surgery. Obstetrics and gynecology 2017; 129(1): 5061.
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Figures: Figure 1: Types of Surgical Site Infections. A cross-section of the abdominal wall illustrating
Figure 2: Potential Bacteria Implicated in Gynecologic SSIs.10
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the CDC classifications for surgical site infections.7
Figure 3: SSI Development. A number of factors, both modifiable and not modifiable,
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contribute to the ultimate development of a surgical site infection.
Figure 4: Use of an SSI Bundle. Risk-stratified SSI rates as a measure of SSI prevention
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measures followed.87
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S0002-9378(17)30254-5
DOI:
10.1016/j.ajog.2017.02.014
Reference:
YMOB 11534
To appear in:
American Journal of Obstetrics and Gynecology
Received Date: 22 November 2016 Revised Date:
25 January 2017
Accepted Date: 7 February 2017
Please cite this article as: Steiner HL, Strand EA, Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention, American Journal of Obstetrics and Gynecology (2017), doi: 10.1016/ j.ajog.2017.02.014. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention Holly L. STEINER, MD1
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Eric A. STRAND, MD1
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The authors report no conflict of interest.
Please address reprint requests to:
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Holly L. Steiner, MD Department of Obstetrics and Gynecology
Washington University School of Medicine 4911 Barnes Jewish Plaza Campus Box 8064
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St. Louis, MO 63110 314-362-4211
Correspondence:
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[email protected]
Holly L. Steiner, MD
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Department of Obstetrics and Gynecology Washington University School of Medicine 4911 Barnes Jewish Plaza Campus Box 8064
St. Louis, MO 63110 314-362-4211 (office) 314-222-6245 (fax) 314-282-0170 (home)
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[email protected] Abstract: 147 words
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Main Text: 3482 words 1
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Department of Obstetrics and Gynecology, Division of General Obstetrics and Gynecology, Washington University, St. Louis, MO
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Condensation: Surgical Site Infection in Gynecologic Surgery: Pathophysiology and Prevention
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We discuss the epidemiology and pathophysiology of surgical site infections (SSIs) in
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gynecology, with a review of the available literature regarding SSI prevention.
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Abstract:
Surgical site infections (SSIs) represent a well-known cause of patient morbidity as well
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as added healthcare costs. In gynecologic surgery, particularly hysterectomy, SSIs are often the result of a number of risk factors that may or may not be modifiable. As both the Centers for Medicaid and Medicare Services and the Joint Commission on the Accreditation of Healthcare
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Organizations have identified SSIs as a patient safety priority, gynecologic surgeons continue to seek out the most effective interventions for SSI prevention. This review studies the
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epidemiology and pathophysiology of SSIs in gynecologic surgery and evaluates the current literature regarding possible interventions for SSI prevention, both as individual measures and as bundles. Data from the obstetrical and general surgery literature will be reviewed when gynecological data is either unclear or unavailable. Practitioners and hospitals may use this
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information as they develop strategies for SSI prevention in their own practice.
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hyperglycemia
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Key words: Surgical site infection, hysterectomy, prophylactic antibiotics, skin antisepsis,
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Introduction Surgical site infection (SSI) represents a significant source of surgical morbidity and mortality. SSIs complicate roughly 2-5% of all surgeries, including approximately 2% of
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hysterectomies.1,2 These estimates are most likely low, as many infections occur after hospital discharge, and patients may present to other healthcare facilities for care.1 These infections result in significant social and economic costs for the patient and the healthcare system; for
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example, each SSI related to hysterectomy is estimated to add $5,000 in patient costs.3,4
Recent initiatives by the Centers for Medicaid and Medicare Services and the Joint
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Commission on the Accreditation of Healthcare Organizations (JCAHO) have identified SSI as a patient safety priority. In an effort to limit SSIs, the JCAHO developed several accountability measures, including timing and selection of prophylactic antibiotics, pre-operative glucose control, and appropriate hair removal.5 Despite these and other initiatives, SSIs are still a
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significant burden for our gynecologic patients. The purpose of this review is to outline the pathophysiology and risk factors involved in the development of SSIs, describe the various evidence-based interventions that may decrease SSI occurrence, and provide suggestions
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Definition
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regarding interventions for clinical practice.
The Centers for Disease Control define an SSI as “an infection related to an operative
procedure that occurs at or near the surgical incision within 30 days.”6 This time frame is extended to 12 months if a surgical implant is used. Infections can be further categorized as (Figure 1)7: •
Superficial incisional: involving the skin and subcutaneous tissues
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•
Deep incisional: involving the deeper soft tissues of the incision, such as muscle or fascia
•
Organ/Space: involving any part of the anatomy other than the incised body layers (skin,
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fascia, and muscle layers)
In gynecologic surgery, SSIs generally fit into these categories, including superficial incisional cellulitis, deep incisional abscesses, and pelvic or vaginal cuff abscess formation.
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Approximately two-thirds of gynecologic SSIs are superficial incisional infections.8
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Pathophysiology
Many gynecologic surgeries, including hysterectomies, are classified as “clean contaminated” procedures, implying that the genital tract is entered in a controlled fashion and without unusual contamination.9 During a hysterectomy, the surgical site is exposed to a unique
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variety of endogenous flora, including common bacteria of the skin, gastrointestinal tract, and vaginal tract. Selection of prophylactic antibiotics must consider the need to cover a variety of gram positive, gram negative, and anaerobic organisms (Figure 2).10
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SSIs arise from a complex interaction of several factors, including the type and number of contaminating bacteria, the virulence of those bacteria, and the resistance of the patient
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involved.11 Bacteria involved may originate from the host patient or arise from other sources, such as the surgical personnel, equipment, and the operating room environment. The presence of a foreign body, such as an implant or mesh, is also relevant, as studies have shown the “dose” of contaminating bacteria required to cause an infection is lower in the presence of foreign material.12
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Patient characteristics that impact the risk of SSI are numerous. Increasing rates of obesity pose a significant problem as obesity contributes to infection in many ways—poor nutritional status, limited surgical visualization, longer operating times, decreased oxygenation
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of tissues, and decreased antibiotic penetration—and has consistently been associated with
increased rates of SSI.13,14 Tobacco use is a known cause of tissue ischemia and delayed wound healing, leading to increased rates of SSI.15 Increased operative time has been consistently
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shown to increase SSI rates in a variety of settings, possibly due to temperature regulation,
inflammation, and anesthesia management.16,17 Hyperglycemia in diabetics is a well-known risk
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factor for several surgical complications, including SSIs.17,18
Additional risk factors are shown in Figure 3.19 Many of these factors are amenable to risk-reduction interventions by the surgical team—examples include administration of prophylactic antibiotics, abdominal skin and vaginal preparation, meticulous surgical technique,
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and maintenance of glycemic control. However, other risk factors, such as obesity, a history of multiple prior surgeries, or encouraging smoking cessation are much harder to modify. Given that only some factors are amenable to intervention, gynecologic surgeons should be well-
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educated regarding the evidence for interventions that reduce SSIs in their patients. The
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remainder of this review will focus on providing evidence-based strategies for SSI reduction. Preoperative factors
The idea of washing or bathing with an antimicrobial wash before surgery has long been
suggested as a means to decrease overall bacterial counts on the skin and thus decrease SSI risk. A Cochrane meta-analysis20 reviewed seven trials comparing different antiseptic washes (4% chlorhexidine scrub, povodine iodine, or regular bar soap) to no wash or placebo. Although SSI incidences did not significantly differ between those using chlorhexidine vs. other wash solutions
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before surgery, use of chlorhexidine was associated with a lower incidence of SSI when compared to no wash in one large study (RR 0.36, 95% CI 0.17 to 0.79).21 The findings of the Cochrane meta-analysis may be explained by either poor washing technique or the lack of a
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specific washing protocol. Indeed, a study performed by Edmiston et al.22 showed significantly higher (P <0.001) chlorhexidine concentrations on the skin after two sequential showers with at least a one-minute pause before rinsing. These levels were above the 90% minimum inhibitory
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concentrations for most gram negative and positive surgical wound pathogens. Using this standardized approach would likely correct deficiencies in current non-standardized
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preadmission shower protocols for patients undergoing elective surgery and thus help decrease overall SSI rates.
Traditionally, hair has been removed before surgery in an attempt to reduce SSI risk. However, a 2011 Cochrane review of six trials involving 972 patients comparing hair removal
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versus no hair removal found no statistically significant difference in SSI rates between the two groups, suggesting that hair removal has no impact on decreasing SSI rates.23 However, this review did find a higher risk of SSI with hair shaving than with clipping (RR 2.09, 95% CI 1.15
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to 3.80). There were no data to support different time frames for hair removal (i.e., day before or
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day of surgery). Therefore, when removal of hair is desired to facilitate the creation of the incision, improve visualization, or enhance the use of a post-operative dressing, clipping should be the preferred approach.
Bacterial vaginosis (BV) is a known risk factor for vaginal cuff infection after
hysterectomy.24 While BV should be treated when identified preoperatively, there are no studies to suggest that routine preoperative screening is warranted. In addition, many of the studies linking BV to vaginal cuff infections occurred before universally timed antibiotic prophylaxis
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was the standard of care.25,26 However, a decision analysis performed by McElligott et al27 investigating three different strategies (screen all patients and treat if positive, treat all patients, or neither screen nor treat) found the strategy of treating all patients prophylactically for BV to
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be most cost effective based on documented rates of vaginal cuff cellulitis. Clinical trials should confirm these findings before universal treatment for BV is adopted for infection prevention. Methicillin resistant staphylococcus aureus (MRSA) is becoming an increasingly
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common pathogen in surgical site infections. Patients can often be colonized from prior
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hospitalizations.28 The literature regarding MRSA decontamination in the gynecologic population is somewhat limited; overall, it does not seem to reduce SSI with any statistical significance.29,30 The impact appears limited to clean surgical procedures, whereas gynecologic procedures are largely clean contaminated. Thus, we do not recommend universal screening for
Intraoperative factors
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MRSA carriage in the gynecologic population.
While certain clinical scenarios dictate a particular surgical approach, evidence
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consistently supports that minimally invasive surgical techniques can decrease the rates of SSI. Several studies have shown that patients undergoing laparoscopic hysterectomies (using either a
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traditional laparoscopic approach or robotic technology) experience about a 50% reduction in SSI incidence compared to those undergoing open abdominal hysterectomies.13,31,32 For this and other reasons, ACOG recommends a minimally invasive approach (vaginal or laparoscopic) when feasible.33
Preoperative antibiotic prophylaxis is now the standard of care for all hysterectomies.34 The preferred option is a single dose of a β-lactam antibiotic, most commonly cefazolin 1-2 g
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intravenous (IV). Based upon pharmacokinetic data in obese patients,35-37 several authors have recommended an increased dose of 3 g for obese patients.38,39 Secondary options for patients with severe penicillin allergies include clindamycin 600 mg IV plus gentamicin 1.5 mg/kg IV or
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metronidazole 500 mg IV plus gentamicin 1.5 mg/kg IV.24 Antibiotics should be administered 30-60 minutes prior to skin incision to provide optimal infection prevention.40 Adjustments and re-dosing of the drugs may be made for morbidly obese patients or for intraoperative factors such
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as an operative length >3 hours or excessive blood loss. A recent study by Uppal et al.41 found that SSI rates were higher in hysterectomy patients who received β-lactam alternatives (such as
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clindamycin/gentamicin or metronidazole/gentamicin) or non-standardized antibiotics (such as clindamycin or gentamicin alone) than in those who received traditional β-lactam antibiotic prophylaxis. Given that β-lactams seem to be the most effective agents for preventing SSI, this study highlights the importance of investigating a patient’s reported β-lactam allergy.
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For skin antisepsis, a large randomized controlled trial involving patients undergoing clean-contaminated surgeries found that chlorhexidine-alcohol was significantly more effective than a povidone-iodine scrub in preventing superficial (4.2% vs. 8.6%, P=0.008) and deep (1%
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vs 3%, P=0.05) incisional infections.42 Several other smaller studies have reported similar findings.43,44 Within the Cochrane meta-analysis, a mixed treatment comparison analysis
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concluded that alcohol-based preparations have the highest probability of effectiveness.45 Thus, although none of these studies specifically addressed gynecologic surgeries, selecting a chlorhexidine-alcohol-based skin preparation seems to be justified. Decreasing overall bacterial counts in the vagina has been proven to reduce the risk of SSI in gynecologic surgeries.46 Traditionally, povodine-iodine preparations were used in the vagina, but trends are shifting towards chlorhexidine-based preparations. Chlorhexidine more
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effectively reduces vaginal bacterial counts47 and remains effective even in the presence of blood, unlike povodine-iodine.48 Surgeons have often been reluctant to use chlorhexidine in the vagina because of the potential for irritation, allergic reactions, and the risk of electrosurgical
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burns due to the alcohol content. However, in concentrations of 4% or less, the solution seems to be well tolerated and its use is supported by the American College of Obstetricians and Gynecologists.48
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The peritoneal cavity is often irrigated during surgery. The traditional teaching promoted
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the idea that irrigation, by reducing operative debris and contaminants, may reduce the risk of infection.49 Overall, the studies regarding intra-abdominal irrigation either report no apparent impact in reducing SSI risk 50-53 or show a possible effect but have a considerable risk of bias.54 The available evidence indicates that irrigation is unlikely to play a role in SSI prevention.
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The data for drain placement is somewhat mixed but appears to argue against the use of routine, prophylactic drain placement. The majority of information, however, comes from the obstetric, rather than the gynecologic, literature.55-58 Outside of this literature, Kosins et al.59
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performed a large systematic review and meta-analysis in 2013 to determine the value of prophylactic subcutaneous drain placement in various surgical wounds. When specifically
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assessing abdominal surgical procedures, their group found no benefit to prophylactic drain placement for the prevention of hematoma, seroma, or infection, even in obese patients. In gynecologic patients with 3 cm or more subcutaneous fat and a vertical midline incision, Cardosi et al.60 found no differences in wound infections or overall complication rates between skin closure techniques with or without closed suction drainage. The data for subcutaneous tissue reapproximation is not straightforward in benign gynecology. In obstetrics, the literature has shown that for patients with >2 cm of subcutaneous
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tissue, closure of the dead space reduces wound separation and seroma formation.61,62 However, in a 2014 Cochrane review of six studies including 815 patients with “non-cesarean” surgeries, rates of SSI or superficial dehiscence were not improved by closure of the subcutaneous tissue.63
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Only two of the six trials were in gynecologic patients, both involving patients with vertical midline incisions and a subcutaneous tissue depth of >2 cm. Given the paucity of data, future studies are needed to examine this area, especially given that the depth of the subcutaneous tissue
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is considered an independent risk factor for wound complications.64
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When planning for skin closure, limited data for gynecologic patients lead us to rely on the obstetrical literature for guidance. Multiple studies65-68 have shown subcuticular suturing to be superior to staples in decreasing the incidence of wound complications and SSI during cesarean delivery. In contrast, a randomized controlled trial performed in general surgery patients found no differences in SSI rates (P=0.882) between laparotomy closure with
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subcuticular sutures or staples 69 Although these data are conflicting, it is important to note that most of the general surgery patients underwent gastrointestinal, pancreatic, or hepatobiliary surgeries, and a large portion received intra-abdominal drains. In addition, the bacterial flora
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encountered at the time of hysterectomy more closely resemble that encountered at cesarean
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delivery, making reliance on available obstetrical data a reasonable approach. A 2014 Cochrane review studying skin closure found that sutures were significantly
better than tissue adhesives for reducing the risk of wound dehiscence.70 No other differences were noted between suture and tissue adhesives in regard to infection rates, and no evidence suggested that the use of both adhesives and suture would provide a superior result. Of note, one study 66 also investigated various suture types (braided vs. mono-filament) and found no difference in the distribution of wound complications. Given the available data, using suture to
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approximate the skin seems to be indicated. The type of suture may be left to the surgeon’s discretion.
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Thermoregulation has been suggested as an important intraoperative adjunct to prevent SSI. Decreased temperature leads to vasoconstriction, lowering oxygen tension in tissues and impairing oxidative killing of bacteria by neutrophils. A randomized controlled study from the mid 1990’s showed that colorectal patients who maintained normothermia during surgery had
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lower rates of wound complications than those who became hypothermic during surgery.71
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However, this study may have been biased as patients in the hypothermia group were more likely to receive a blood transfusion, a known risk factor for SSI. Numerous contemporary studies in the colorectal literature have failed to document decreased SSI rates with various intraoperative protocols for maintaining normothermia.72-74 Despite the mixed data, hypothermia causes other harms, including impaired drug metabolism, cardiac dysfunction, and coagulopathy. Thus, we
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strongly recommend maintenance of normothermia even though its impact on SSI risk is likely negligible.
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Supplemental intraoperative oxygen has several proposed benefits that may lead to reduced incidence of SSI. These include increased oxygen exposure to the tissue bed leading to
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increased collagen deposition and improved immune function. Additionally, the activity of antibiotics may be amplified at higher levels of oxygen.75 Although there is some suggestion that hyperoxia may help prevent SSIs in colorectal surgery, the available data have generally not supported this conclusion in gynecologic surgery.51, 76 Postoperative factors
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Hyperglycemia in diabetics is a well-known risk factor for several surgical complications, including SSIs.17,18 Although optimizing postoperative blood sugar levels is an important method to decrease SSI rates, the impact of “aggressive” glucose control seems less clear. A
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Cochrane review from 200977 comparing strict glycemic control versus conventional
management (maintenance of glucose <200 mg/dL) for the prevention of SSI concluded the evidence was insufficient to support strict glycemic control. The authors did note significant
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heterogeneity between the studies, which limited their ability to perform the meta-analysis. However, a more recent study by Al-Niaimi et al. suggests that aggressive management
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significantly reduces SSI rates in postsurgical diabetic patients.78 In this retrospective study, gynecologic surgery patients with a glucose above 150 mg/dL were managed with either intermittent subcutaneous insulin injections or an insulin infusion. Once started, the insulin infusion was continued for 24 hours. The authors showed that patients whose hyperglycemia was
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managed via insulin infusion had significantly lower SSI rates than those who received subcutaneous insulin (19% vs 29%, P=0.001). Even more compelling, the authors found that the SSI rate for patients on the insulin infusion was comparable to that for patients who did not have
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diabetes.
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Emerging evidence indicates that post-operative glycemic control may be important even in the non-diabetic population. Stress hyperglycemia, a natural phenomenon that results after illness or injury, can have multiple consequences, including impaired immune function, stimulation of inflammatory markers, increased thrombotic activity, and endothelial cell dysfunction.79 In a review of the Surgical Care and Outcomes Assessment Program in Washington, Kwon et al.80 evaluated the effects of perioperative hyperglycemia (glucose >180 mg/dL) and insulin administration on various outcomes for >11,000 patients undergoing bariatric
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and colorectal surgeries. The authors found an increased risk of SSI for all patients experiencing hyperglycemia, regardless of whether or not they carried a pre-operative diagnosis of diabetes. In this study, 13.5% of the non-diabetic patients experienced hyperglycemia, and the greatest risk
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of infection existed in the patients with no history of diabetes experiencing hyperglycemia. Regardless of diabetic status, insulin administration mitigated the SSI risk for both groups. Often, the argument against strict glucose control is to avoid the side effects of
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hypoglycemia that can occur with over-aggressive insulin administration, including seizures or
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even death. However, as demonstrated in the Al-Niaimi et al. study,78 the incidence of hypoglycemic events may be decreased by following a clear protocol of insulin infusion instead of subcutaneous insulin injection (0.7 vs. 5.4%, P <0.05). Although further studies are needed in benign gynecologic populations, tight glycemic control may prove beneficial in reducing SSI
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rates in both diabetic and non-diabetic patients.
The surgical dressing was once thought to prevent SSIs by protecting the surgical wound from outside bacterial contamination until initial epithelization can occur. However, recent data
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in the general surgery literature indicate that this may not be the case. A large systematic review in 2012 concluded that SSI rates did not differ between those who did and did not receive
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surgical dressings.81 A 2014 Cochrane review failed to find evidence suggesting that surgical dressings reduce the SSI risk or that any one type of dressing is preferred over another.82 Similarly, a 2015 Cochrane review found that removal of surgical dressings within the first 48 hours did not increase SSI rates.83 In the obstetrical literature, a study by Peleg et al.84 compared dressing removal at 6 versus 24 hours after cesarean section. They found no differences in wound dehiscence or SSI rates between the groups. In general, a post-operative dressing should
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be chosen on the basis of cost and symptom management properties, as it is unlikely to affect SSI rates.
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Perioperative blood transfusions are an independent risk factor for SSIs.3,17,85,86 Given this association, we recommend limiting their use based on clinical indications and not on predefined hemoglobin values.
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Use of SSI Prevention Bundles
Many groups have investigated the potential benefit of creating, and following, SSI
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prevention bundles. One nice example involved a review from the Michigan Surgical Quality Collaborative performed by Waits et al.87 In evaluating >4000 patients undergoing colectomies, the authors assessed compliance with a group of six perioperative measures that were independently associated with SSI risk:
Appropriate selection of prophylactic antibiotics
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Post-operative normothermia (T>98.6oF)
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Oral antibiotics with mechanical bowel prep
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Post-operative day #1 glucose ≤ 140 mg/dL
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Minimally invasive approach
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•
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•
Short operative time <100 minutes
The authors found a strong, stepwise, inverse association between SSI rates and the number of measures followed (Figure 4). Although not all of the measures (i.e., surgical time or minimally invasive approach) are always under the surgeon’s control, the finding that these measures prevented SSI in a stepwise fashion shows the potential for SSI bundles to be more beneficial than implementing any single step for prevention.
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The effectiveness of SSI prevention bundles has also been shown in a colorectal surgery meta-analysis,88 in cesarean delivery,89 and in the gynecologic oncology population.90 A thorough SSI prevention bundle for benign gynecology has recently been published by the
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Council on Patient Safety in Women’s Health Care.91 Although the specific measures vary
between studies, most have focused on antibiotic administration, appropriate hair removal (when indicated), normothermia, and glycemic control.
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Conclusion
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SSI represents a significant source of post-operative morbidity for gynecologic surgery patients. Gynecologic surgeries, particularly hysterectomies, expose the surgical site to a variety of endogenous bacteria unique to our specialty. Although several preoperative risk factors (e.g., obesity, prior surgery, ability to pursue a minimally invasive approach) may not be within the
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surgeon’s control, several evidence-based interventions can limit the incidence of SSIs. Research on SSI bundles also indicates that implementation of several evidence-based strategies is likely to have a larger impact than pursuing any single intervention. Interventions clearly
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supported by the literature include the timely administration of appropriately selected prophylactic antibiotics, use of a chlorhexidine-alcohol based prep, use of suture for skin closure,
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and maintenance of glycemic control in the postoperative period. The impact of preserving normothermia on SSIs is less clear but should be standard practice given the potential harms associated with hypothermia. Several interventions, including the use of specified pre-operative chlorhexidine shower protocols, universal pre-operative screening for bacterial vaginosis, reapproximation of the subcutaneous tissue, and the use of peri-operative or post-operative hyperoxia, should be further investigated in the continued effort to decrease the occurrence of SSI in our patients.
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18. Martin ET, Kaye KS, Knott C, et al. Diabetes and Risk of Surgical Site Infection: A Systematic Review and Meta-analysis. Infect Control Hosp Epidemiol 2016; 37(1): 88-99. 19. Anderson DJ, Podgorny K, Berrios-Torres SI, et al. Strategies to prevent surgical site infections in acute care hospitals: 2014 update. Infection control and hospital epidemiology 2014; 35(6): 605-27. 20. Webster J, Osborne S. Preoperative bathing or showering with skin antiseptics to prevent surgical site infection. Cochrane Database Syst Rev 2015; (2): CD004985. 21. Wihlborg O. The effect of washing with chlorhexidine soap on wound infection rate in general surgery. A controlled clinical study. Ann Chir Gynaecol 1987; 76(5): 263-5. 22. Edmiston CE, Jr., Lee CJ, Krepel CJ, et al. Evidence for a Standardized Preadmission Showering Regimen to Achieve Maximal Antiseptic Skin Surface Concentrations of Chlorhexidine Gluconate, 4%, in Surgical Patients. JAMA Surg 2015; 150(11): 1027-33. 23. Tanner J, Norrie P, Melen K. Preoperative hair removal to reduce surgical site infection. Cochrane Database Syst Rev 2011; (11): CD004122. 24. Bulletins--Gynecology ACoP. ACOG practice bulletin No. 104: antibiotic prophylaxis for gynecologic procedures. Obstet Gynecol 2009; 113(5): 1180-9. 25. Larsson PG, Carlsson B. Does pre- and postoperative metronidazole treatment lower vaginal cuff infection rate after abdominal hysterectomy among women with bacterial vaginosis? Infectious diseases in obstetrics and gynecology 2002; 10(3): 133-40. 26. Persson E, Bergstrom M, Larsson PG, et al. Infections after hysterectomy. A prospective nation-wide Swedish study. The Study Group on Infectious Diseases in Obstetrics and Gynecology within the Swedish Society of Obstetrics and Gynecology. Acta obstetricia et gynecologica Scandinavica 1996; 75(8): 757-61. 27. McElligott KA, Havrilesky LJ, Myers ER. Preoperative screening strategies for bacterial vaginosis prior to elective hysterectomy: a cost comparison study. Am J Obstet Gynecol 2011; 205(5): 500 e1-7. 28. Edmiston CE, Jr., Ledeboer NA, Buchan BW, Spencer M, Seabrook GR, Leaper D. Is Staphylococcal Screening and Suppression an Effective Interventional Strategy for Reduction of Surgical Site Infection? Surg Infect (Larchmt) 2016; 17(2): 158-66. 29. Pofahl WE, Goettler CE, Ramsey KM, Cochran MK, Nobles DL, Rotondo MF. Active surveillance screening of MRSA and eradication of the carrier state decreases surgical-site infections caused by MRSA. J Am Coll Surg 2009; 208(5): 981-6; discussion 6-8. 30. Perl TM, Cullen JJ, Wenzel RP, et al. Intranasal mupirocin to prevent postoperative Staphylococcus aureus infections. N Engl J Med 2002; 346(24): 1871-7. 31. Gandaglia G, Ghani KR, Sood A, et al. Effect of minimally invasive surgery on the risk for surgical site infections: results from the National Surgical Quality Improvement Program (NSQIP) Database. JAMA surgery 2014; 149(10): 1039-44. 32. Roy S, Patkar A, Daskiran M, Levine R, Hinoul P, Nigam S. Clinical and economic burden of surgical site infection in hysterectomy. Surgical infections 2014; 15(3): 266-73. 33. ACOG Committee Opinion No. 444: choosing the route of hysterectomy for benign disease. Obstetrics and gynecology 2009; 114(5): 1156-8. 34. Bratzler DW, Houck PM, Surgical Infection Prevention Guideline Writers W. Antimicrobial prophylaxis for surgery: an advisory statement from the National Surgical Infection Prevention Project. Am J Surg 2005; 189(4): 395-404. 35. Edmiston CE, Krepel C, Kelly H, et al. Perioperative antibiotic prophylaxis in the gastric bypass patient: do we achieve therapeutic levels? Surgery 2004; 136(4): 738-47.
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36. Swank ML, Wing DA, Nicolau DP, McNulty JA. Increased 3-gram cefazolin dosing for cesarean delivery prophylaxis in obese women. American journal of obstetrics and gynecology 2015; 213(3): 415.e1-8. 37. Pevzner L, Swank M, Krepel C, Wing DA, Chan K, Edmiston CE, Jr. Effects of maternal obesity on tissue concentrations of prophylactic cefazolin during cesarean delivery. Obstetrics and gynecology 2011; 117(4): 877-82. 38. Bratzler DW, Dellinger EP, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. American journal of health-system pharmacy : AJHP : official journal of the American Society of Health-System Pharmacists 2013; 70(3): 195-283. 39. Lachiewicz MP, Moulton LJ, Jaiyeoba O. Pelvic surgical site infections in gynecologic surgery. Infectious diseases in obstetrics and gynecology 2015; 2015: 614950. 40. Classen DC, Evans RS, Pestotnik SL, Horn SD, Menlove RL, Burke JP. The timing of prophylactic administration of antibiotics and the risk of surgical-wound infection. The New England journal of medicine 1992; 326(5): 281-6. 41. Uppal S, Harris J, Al-Niaimi A, et al. Prophylactic Antibiotic Choice and Risk of Surgical Site Infection After Hysterectomy. Obstetrics and gynecology 2016; 127(2): 321-9. 42. Darouiche RO, Wall MJ, Jr., Itani KM, et al. Chlorhexidine-Alcohol versus PovidoneIodine for Surgical-Site Antisepsis. N Engl J Med 2010; 362(1): 18-26. 43. Paocharoen V, Mingmalairak C, Apisarnthanarak A. Comparison of surgical wound infection after preoperative skin preparation with 4% chlorhexidine [correction of chlohexidine] and povidone iodine: a prospective randomized trial. J Med Assoc Thai 2009; 92(7): 898-902. 44. Rodrigues AL, Simoes Mde L. Incidence of surgical site infection with pre-operative skin preparation using 10% polyvidone-iodine and 0.5% chlorhexidine-alcohol. Rev Col Bras Cir 2013; 40(6): 443-8. 45. Dumville JC, McFarlane E, Edwards P, Lipp A, Holmes A. Preoperative skin antiseptics for preventing surgical wound infections after clean surgery. Cochrane Database Syst Rev 2013; (3): CD003949. 46. Eason E, Wells G, Garber G, et al. Antisepsis for abdominal hysterectomy: a randomised controlled trial of povidone-iodine gel. BJOG 2004; 111(7): 695-9. 47. Culligan PJ, Kubik K, Murphy M, Blackwell L, Snyder J. A randomized trial that compared povidone iodine and chlorhexidine as antiseptics for vaginal hysterectomy. Am J Obstet Gynecol 2005; 192(2): 422-5. 48. American College of O, Gynecologists Women's Health Care P, Committee on Gynecologic P. Committee Opinion No. 571: Solutions for surgical preparation of the vagina. Obstet Gynecol 2013; 122(3): 718-20. 49. Edmiston CE, Jr., Leaper DJ. Intra-Operative Surgical Irrigation of the Surgical Incision: What Does the Future Hold-Saline, Antibiotic Agents, or Antiseptic Agents? Surg Infect (Larchmt) 2016. 50. Temizkan O, Asicioglu O, Gungorduk K, Asicioglu B, Yalcin P, Ayhan I. The effect of peritoneal cavity saline irrigation at cesarean delivery on maternal morbidity and gastrointestinal system outcomes. J Matern Fetal Neonatal Med 2016; 29(4): 651-5. 51. Eke AC, Shukr GH, Chaalan TT, Nashif SK, Eleje GU. Intra-abdominal saline irrigation at cesarean section: a systematic review and meta-analysis. J Matern Fetal Neonatal Med 2016; 29(10): 1588-94. 52. Al-Ramahi M, Bata M, Sumreen I, Amr M. Saline irrigation and wound infection in abdominal gynecologic surgery. Int J Gynaecol Obstet 2006; 94(1): 33-6.
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53. Schein M, Gecelter G, Freinkel W, Gerding H, Becker PJ. Peritoneal lavage in abdominal sepsis. A controlled clinical study. Arch Surg 1990; 125(9): 1132-5. 54. Mueller TC, Loos M, Haller B, et al. Intra-operative wound irrigation to reduce surgical site infections after abdominal surgery: a systematic review and meta-analysis. Langenbecks Arch Surg 2015; 400(2): 167-81. 55. Al-Inany H, Youssef G, Abd ElMaguid A, Abdel Hamid M, Naguib A. Value of subcutaneous drainage system in obese females undergoing cesarean section using pfannenstiel incision. Gynecol Obstet Invest 2002; 53(2): 75-8. 56. Ramsey PS, White AM, Guinn DA, et al. Subcutaneous tissue reapproximation, alone or in combination with drain, in obese women undergoing cesarean delivery. Obstet Gynecol 2005; 105(5 Pt 1): 967-73. 57. Magann EF, Chauhan SP, Rodts-Palenik S, Bufkin L, Martin JN, Jr., Morrison JC. Subcutaneous stitch closure versus subcutaneous drain to prevent wound disruption after cesarean delivery: a randomized clinical trial. Am J Obstet Gynecol 2002; 186(6): 1119-23. 58. Gates S, Anderson ER. Wound drainage for caesarean section. Cochrane Database Syst Rev 2013; (12): CD004549. 59. Kosins AM, Scholz T, Cetinkaya M, Evans GR. Evidence-based value of subcutaneous surgical wound drainage: the largest systematic review and meta-analysis. Plast Reconstr Surg 2013; 132(2): 443-50. 60. Cardosi RJ, Drake J, Holmes S, et al. Subcutaneous management of vertical incisions with 3 or more centimeters of subcutaneous fat. American journal of obstetrics and gynecology 2006; 195(2): 607-14; discussion 14-6. 61. Chelmow D, Huang E, Strohbehn K. Closure of the subcutaneous dead space and wound disruption after Cesarean delivery. J Matern Fetal Neonatal Med 2002; 11(6): 403-8. 62. Naumann RW, Hauth JC, Owen J, Hodgkins PM, Lincoln T. Subcutaneous tissue approximation in relation to wound disruption after cesarean delivery in obese women. Obstet Gynecol 1995; 85(3): 412-6. 63. Gurusamy KS, Toon CD, Davidson BR. Subcutaneous closure versus no subcutaneous closure after non-caesarean surgical procedures. Cochrane Database Syst Rev 2014; (1): CD010425. 64. Soper DE, Bump RC, Hurt WG. Wound infection after abdominal hysterectomy: effect of the depth of subcutaneous tissue. Am J Obstet Gynecol 1995; 173(2): 465-9; discussion 9-71. 65. Figueroa D, Jauk VC, Szychowski JM, et al. Surgical staples compared with subcuticular suture for skin closure after cesarean delivery: a randomized controlled trial. Obstet Gynecol 2013; 121(1): 33-8. 66. Mackeen AD, Khalifeh A, Fleisher J, et al. Suture compared with staple skin closure after cesarean delivery: a randomized controlled trial. Obstet Gynecol 2014; 123(6): 1169-75. 67. Tuuli MG, Rampersad RM, Carbone JF, Stamilio D, Macones GA, Odibo AO. Staples compared with subcuticular suture for skin closure after cesarean delivery: a systematic review and meta-analysis. Obstet Gynecol 2011; 117(3): 682-90. 68. Zaki MN, Truong M, Pyra M, Kominiarek MA, Irwin T. Wound complications in obese women after cesarean: a comparison of staples versus subcuticular suture. J Perinatol 2016; 36(10): 819-22. 69. Imamura K, Adachi K, Sasaki R, et al. Randomized Comparison of Subcuticular Sutures Versus Staples for Skin Closure After Open Abdominal Surgery: a Multicenter Open-Label Randomized Controlled Trial. J Gastrointest Surg 2016.
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70. Dumville JC, Coulthard P, Worthington HV, et al. Tissue adhesives for closure of surgical incisions. Cochrane Database Syst Rev 2014; (11): CD004287. 71. Kurz A, Sessler DI, Lenhardt R. Perioperative normothermia to reduce the incidence of surgical-wound infection and shorten hospitalization. Study of Wound Infection and Temperature Group. N Engl J Med 1996; 334(19): 1209-15. 72. Baucom RB, Phillips SE, Ehrenfeld JM, et al. Association of Perioperative Hypothermia During Colectomy With Surgical Site Infection. JAMA Surg 2015; 150(6): 570-5. 73. Geiger TM, Horst S, Muldoon R, et al. Perioperative core body temperatures effect on outcome after colorectal resections. Am Surg 2012; 78(5): 607-12. 74. Melton GB, Vogel JD, Swenson BR, Remzi FH, Rothenberger DA, Wick EC. Continuous intraoperative temperature measurement and surgical site infection risk: analysis of anesthesia information system data in 1008 colorectal procedures. Ann Surg 2013; 258(4): 60612; discussion 12-3. 75. Munoz-Price LS, Sands L, Lubarsky DA. Effect of high perioperative oxygen supplementation on surgical site infections. Clin Infect Dis 2013; 57(10): 1465-72. 76. Wetterslev J, Meyhoff CS, Jorgensen LN, Gluud C, Lindschou J, Rasmussen LS. The effects of high perioperative inspiratory oxygen fraction for adult surgical patients. Cochrane Database Syst Rev 2015; (6): CD008884. 77. Kao LS, Meeks D, Moyer VA, Lally KP. Peri-operative glycaemic control regimens for preventing surgical site infections in adults. Cochrane Database Syst Rev 2009; (3): CD006806. 78. Al-Niaimi AN, Ahmed M, Burish N, et al. Intensive postoperative glucose control reduces the surgical site infection rates in gynecologic oncology patients. Gynecol Oncol 2015; 136(1): 71-6. 79. Kao LS, Phatak UR. Glycemic control and prevention of surgical site infection. Surg Infect (Larchmt) 2013; 14(5): 437-44. 80. Kwon S, Thompson R, Dellinger P, Yanez D, Farrohki E, Flum D. Importance of perioperative glycemic control in general surgery: a report from the Surgical Care and Outcomes Assessment Program. Annals of surgery 2013; 257(1): 8-14. 81. Walter CJ, Dumville JC, Sharp CA, Page T. Systematic review and meta-analysis of wound dressings in the prevention of surgical-site infections in surgical wounds healing by primary intention. Br J Surg 2012; 99(9): 1185-94. 82. Dumville JC, Gray TA, Walter CJ, Sharp CA, Page T. Dressings for the prevention of surgical site infection. Cochrane Database Syst Rev 2014; (9): CD003091. 83. Toon CD, Lusuku C, Ramamoorthy R, Davidson BR, Gurusamy KS. Early versus delayed dressing removal after primary closure of clean and clean-contaminated surgical wounds. Cochrane Database Syst Rev 2015; (9): CD010259. 84. Peleg D, Eberstark E, Warsof SL, Cohen N, Ben Shachar I. Early wound dressing removal after scheduled cesarean delivery: a randomized controlled trial. Am J Obstet Gynecol 2016; 215(3): 388 e1-5. 85. Young H, Berumen C, Knepper B, et al. Statewide collaboration to evaluate the effects of blood loss and transfusion on surgical site infection after hysterectomy. Infect Control Hosp Epidemiol 2012; 33(1): 90-3. 86. Mahdi H, Gojayev A, Buechel M, et al. Surgical site infection in women undergoing surgery for gynecologic cancer. Int J Gynecol Cancer 2014; 24(4): 779-86. 87. Waits SA, Fritze D, Banerjee M, et al. Developing an argument for bundled interventions to reduce surgical site infection in colorectal surgery. Surgery 2014; 155(4): 602-6.
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88. Tanner J, Padley W, Assadian O, Leaper D, Kiernan M, Edmiston C. Do surgical care bundles reduce the risk of surgical site infections in patients undergoing colorectal surgery? A systematic review and cohort meta-analysis of 8,515 patients. Surgery 2015; 158(1): 66-77. 89. Hsu CD, Cohn I, Caban R. Reduction and sustainability of cesarean section surgical site infection: An evidence-based, innovative, and multidisciplinary quality improvement intervention bundle program. American journal of infection control 2016; 44(11): 1315-20. 90. Johnson MP, Kim SJ, Langstraat CL, et al. Using Bundled Interventions to Reduce Surgical Site Infection After Major Gynecologic Cancer Surgery. Obstetrics and gynecology 2016; 127(6): 1135-44. 91. Pellegrini JE, Toledo P, Soper DE, et al. Consensus Bundle on Prevention of Surgical Site Infections After Major Gynecologic Surgery. Obstetrics and gynecology 2017; 129(1): 5061.
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Figures: Figure 1: Types of Surgical Site Infections. A cross-section of the abdominal wall illustrating
Figure 2: Potential Bacteria Implicated in Gynecologic SSIs.10
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the CDC classifications for surgical site infections.7
Figure 3: SSI Development. A number of factors, both modifiable and not modifiable,
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Figure 4: Use of an SSI Bundle. Risk-stratified SSI rates as a measure of SSI prevention
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measures followed.87
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AC C
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TE D
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AC C
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