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Outcomes Associated With a Five-Point Surgical Site Infection Prevention Bundle in Women Undergoing Surgery for Ovarian Cancer

Lippitt, Melissa, H., MD; Fairbairn, Melissa, Gerardi, PA-C; Matsuno, Rayna, PhD; Stone, Rebecca, L., MD; Tanner, Edward, J., III, MD; Wick, Elizabeth, C., MD; Angarita, Ana, C., MD; Roche, Kara, Long, MD, MSc; Levinson, Kimberly, L., MD, MPH; Bergstrom, Jennifer, E., MD; Sinno, Abdulrahman, K., MD; Curless, Melanie, S., RN, MPH; Wethington, Stephanie, MD; Temkin, Sarah, M., MD; Efron, Jonathan, MD; Hobson, Deborah, RN; Fader, Amanda, N., MD

doi: 10.1097/AOG.0000000000002213
Contents: Original Research

OBJECTIVE: To identify risk factors for surgical site infection and to define rates associated with cytoreductive surgery before and after implementation of an infection prevention bundle.

METHODS: We conducted a prospective quality improvement study. Patients who underwent ovarian, fallopian tube, or peritoneal cancer cytoreductive surgery at an academic tertiary care center from April 2014 to April 2016 were prospectively enrolled. Patient demographics, surgical variables, and surgical site infection rates were compared with a historical cohort after introduction of a 5-point infection prevention bundle, including: 1) preoperative and intraoperative skin preparation with 4% chlorhexidine and intraoperative vaginal preparation with 4% chlorhexidine; 2) preoperative use of oral antibiotics and mechanical bowel preparation; 3) appropriate timing of intraoperative antibiotics; 4) adoption of enhanced sterile surgical techniques for colon procedures and incisional closure; and 5) perioperative incision management.

RESULTS: During the study period, 219 women underwent surgery: 91 prebundle and 128 treated in the postbundle period. Stage, body mass index, proportion of patients undergoing colon or upper abdominal surgery, and estimated blood loss were not different between the cohorts. Overall, the surgical site infection rate prebundle was 18 (20%); this was reduced to four (3%) postbundle (odds ratio [OR] 0.13, 95% CI 0.037–0.53; P<.001). Patients who underwent a colon resection prebundle had an infection rate of 14 (33%) compared with three (7%) in the postbundle group (OR 0.14, 95% CI 0.037–0.53; P<.001). Additionally, rates of surgical site infection–related hospital readmission were also lower in the postbundle (4/128 [3%]) compared with the prebundle group (12/91 [13%]; P=.005).

CONCLUSION: Infection is common after ovarian cancer cytoreductive surgery. Implementation of a 5-point surgical site infection prevention bundle in women undergoing ovarian cancer operations was associated with dramatically decreased infection rates and lower hospital readmission rates.

Implementation of an infection prevention bundle in women undergoing ovarian cancer surgery is associated with decreased infection rates.

Kelly Gynecologic Oncology Service, Department of Gynecology and Obstetrics, Johns Hopkins Medicine, Baltimore, Maryland; the Department of Surgery, Johns Hopkins University, Baltimore, Maryland; Moores Cancer Center, University of California, San Diego, La Jolla, California; the Department of Gynecologic Surgery, Memorial Sloan Kettering Cancer Center, New York, New York; and Hospital Epidemiology and Infection Control, Johns Hopkins Hospital, Baltimore, Maryland.

Corresponding author: Amanda N. Fader, MD, Johns Hopkins University School of Medicine, 600 N Wolfe Street, Phipps 287, Baltimore, MD 21287; email:

Financial Disclosure The authors did not report any potential conflicts of interest.

Presented at the Western Association of Gynecologic Oncology Annual Meeting, June 8–11, 2016, Sedona, Arizona.

Each author has indicated that he or she has met the journal's requirements for authorship.

Complications related to surgery represent a significant burden of harm in the United States with an estimated yearly cost of $25 billion.1–5 Nearly 25% of the estimated two million nosocomial infections occurring in U.S. hospitals are surgical site infections that result in substantial patient-related morbidity, reduction in quality of life, a higher likelihood of readmission, reintervention, and an increase in health care-related costs.

Preventing adverse perioperative events, including surgical site infection, has become the focus of U.S. quality improvement efforts.6 The Centers for Disease Control and Prevention National Health Service Network is the nation's most widely utilized health care-associated infection tracking system.7 The National Health Service Network establishes surgical site infection benchmarks and reports infection rates within hospitals stratified by surgery type.7 The agency's overarching goal is to eliminate health care-associated infections. Surgical site infection rates are currently utilized as a quality indicator for the Centers for Medicare & Medicaid Services with financial penalties exacted to hospital systems when benchmarks are not met.8 Although not all factors associated with infection are modifiable, the majority of infections may be preventable9 and evidence-based strategies have been implemented in many hospitals as nationally recognized by the Surgical Care Improvement Project and National Surgical Quality Improvement Program.10

Surgical site infection is commonly observed in women after ovarian cancer cytoreductive surgery. Published surgical site infection rates for major gynecologic cancer procedures range from 3% to 36%.9,11–14 Optimal treatment of advanced ovarian cancer often requires radical pelvic and upper abdominal procedures with multiorgan resection.15 Given the nature of cytoreductive surgery for ovarian cancer, these procedures are inherently associated with high perioperative morbidity.11,16 Additionally, most women diagnosed with advanced ovarian cancer have ascites, are elderly, and may possess comorbidities associated with advancing age such as obesity, hypertension, and diabetes that further increase their risk of perioperative morbidity.11–14,16

In 2013, the faculty of the Kelly Gynecologic Oncology Service at Johns Hopkins Hospital joined an existing multidisciplinary, surgery-based Comprehensive Unit-based Safety Program aimed at reduction of the high, hospital-wide surgical site infection rates after colon (27.3% for all services combined) and other surgeries. The Comprehensive Unit-based Safety Program team specifically initiated efforts to decrease surgical site infection rates for patients undergoing a colon resection by the colorectal surgery, surgical oncology, trauma surgery, and gynecologic oncology services. Using several evidence-based measures, a 5-point surgical site infection prevention bundle was developed that included administration of preoperative chlorhexidine showers, standardization of intraoperative skin preparation, selective utilization of antibiotic mechanical bowel preparation, addressing lapses in prophylactic antibiotic administration, adoption of enhanced sterile techniques for bowel and skin portions of the case, and rigorous postoperative wound care.13 Initially, our goal on each surgical service was to lower the surgical site infection rates by half in the first year and then below 3–7% in the second year per the National Health Service Network-defined national benchmarks for colon and hysterectomy procedures.14 Our current study objective was to examine the reduction in surgical site infections after implementation of this standardized infection prevention bundle in the surgical care of women with advanced ovarian cancer and especially in those undergoing colon procedures. In an effort to define other opportunities to reduce infection rates, a secondary objective was to identify modifiable risk factors for surgical site infection.

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This prospective quality improvement study was approved by the institutional review board, Johns Hopkins Hospital, Baltimore, Maryland (“Quality Assessment of Surgical Outcomes in Gynecologic Oncology”). All women who underwent surgical cytoreduction for presumed advanced (stage II–IV) or recurrent ovarian, fallopian tube, or primary peritoneal cancer from April 1, 2014, to April 1, 2016, on the Kelly Gynecologic Oncology Service, Johns Hopkins Hospital, were included. Cytoreductive procedure types included primary, interval, and secondary or tertiary surgeries. Six, high-volume gynecologic oncologists performed all surgeries and 30-day perioperative aftercare. A gynecologic oncology fellow or upper-level gynecology resident was involved in all cases. A high-volume surgeon was previously defined as one who performs 10 or greater ovarian cancer cytoreductive surgeries annually17 as well as 10 or greater colectomies per year.18 All patients underwent at least two perioperative visits at Johns Hopkins Hospital within the first 30 days after surgery, specifically at 2 and 4 weeks after their surgeries.

A 5-point, evidence-based surgical site infection reduction bundle of care based on the previously established Johns Hopkins colorectal surgery bundle was implemented on the Kelly Gynecologic Oncology Service during the study period. The bundled elements are detailed in Box 1. Of note, the intraoperative, prophylactic antibiotic regimen for ovarian cancer surgery was standardized on the Kelly Gynecologic Oncology Service in January 2014 and included a first-generation cephalosporin (ie, cefazolin) and metronidazole when colon surgery was anticipated. This was based on published data from the Veterans Affairs Surgical Quality Improvement Program demonstrating that regimens combining a first-generation cephalosporin and metronidazole reduced surgical site infection rates in patients undergoing colon surgery compared with other penicillin or cephalosporin-containing regimens.18 The bundle was formally implemented and audited by the study principal investigator (gynecologic oncologist A.N.F.) by the Comprehensive Unit-based Safety Program leadership (consisting of a colorectal surgeon, E.C.W., and nurse, D.H.) and by the institutional Hospital Epidemiology and Infection Control Department (infection prevention specialist, M.S.C.). Measures were developed to optimize implementation and patient compliance with the bundle of care. Specifically, all preoperative bundle elements were added to surgical posting forms, and literature with instructions on chlorhexidine bathing and mechanical bowel preparation were developed, approved by the Comprehensive Unit-based Safety Program team, and provided to patients at their preoperative visit. Additionally, the Kelly Gynecologic Oncology Service faculty (n=6) and surgical schedulers (n=2) were trained regarding the surgical site infection reduction bundle and collectively educated all surgical patients on the bundle rationale and instructions. As part of this education, the patients were instructed that the mechanical bowel preparation and oral antibiotics might induce nausea. Therefore, patients were prescribed an antiemetic before starting the bowel preparation and received a call from the schedulers the day before surgery to provide further instructions on skin and bowel preparation.

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Box 1.

Johns Hopkins 5-Point Surgical Site Infection Prevention Bundle Elements Cited Here...



Bundled elements ordered by the treating surgeon were recorded in the electronic medical record by the surgical schedulers. Nursing staff in the preoperative area recorded patient-reported compliance with the skin preparation and mechanical bowel preparation in the electronic medical record. Patients who reported noncompliance with the skin preparation were provided with 4% chlorhexidine wipes in the preoperative area and instructed on their use before transfer to the operating room. If the patient claimed an allergy to chlorhexidine, then no preoperative skin preparation was administered and an iodine-based skin preparation was used in the operating room. If a patient did not subjectively consume at least 50% of her bowel preparation volume, this preoperative measure was recorded as “no” for that patient. Data on 30-day postoperative surgical site infections were prospectively and independently monitored by the Johns Hopkins Hospital Epidemiology and Infection Control Department and reported quarterly to the Comprehensive Unit-based Safety Program team and hospital administrative leadership.

Surgical site infection was defined as superficial, deep, or organ space by the National Health Service Network definitions for the year in which the procedure was performed (ie, 2016 definition).19

The bundle of care was instituted on January 1, 2014, and a 2-month grace period was established to allow the multidisciplinary Comprehensive Unit-based Safety Program team and the Kelly Gynecologic Oncology Service an opportunity to further educate team members and assess protocol violations. Full bundle implementation occurred on March 1, 2014. We conducted a prospective review of the patients with ovarian cancer who participated in the 5-point surgical site infection prevention bundle of care during the 2-year study period (April 1, 2014, to April 1, 2016) and compared their outcomes with those of patients with ovarian cancer treated within the 2 years before bundle implementation (January 1, 2012, to January 1, 2014). Historical case information from those treated prebundle was obtained from a prospectively maintained divisional ovarian cancer database and crossreferenced with a prospectively maintained institutional epidemiology and infection control procedural database. Notable differences in institutional infection prevention practices during the historical prebundle care period (compared with the prospective bundle care period) were: 1) preoperative chlorhexidine was not utilized; 2) iodine was used for both intraoperative skin and vaginal preparations; 3) an intravenous first- or second-generation cephalosporin was used; 4) enhanced sterile techniques and instrumentation were not utilized; and 5) antibiotic bowel preparations were utilized inconsistently based only on physician preference.

Operative records were reviewed for surgical data including surgical approach, type of cytoreduction, performance of upper abdominal procedures (defined as supracolic omentectomy for omental cake, splenectomy with or without distal pancreatectomy, stripping or full-thickness diaphragm resection with or without diaphragm repair, partial gastrectomy, cholecystectomy, or liver resection), bowel resection (defined as removal of ascending, transverse, or proximal descending colon; small bowel or stomach resection; and anastomosis), anterior abdominal wall resection, residual disease status, intraoperative estimated blood loss, intravenous fluid administration, and intra- and postoperative packed red blood cell transfusion. Thirty-day perioperative surgical site infection and readmission rates related to infection were analyzed and reported by the Hospital Epidemiology and Infection Control Department. Readmissions occurring at hospitals other than Johns Hopkins were noted in the medical record. Infection and readmission rates were determined from review of the electronic medical record of every patient who had undergone ovarian cancer surgery during the study period. The 30-day surveillance period and other surgical site infection inclusion factors were per the Centers for Disease Control and Prevention surgical site infection definitions.19

Patient comorbidities were recorded and are detailed in Table 1. Eastern Cooperative Oncology Group definitions were used for performance status.20,21 Anesthesia Society Association severity scores were also calculated.22 Pathology reports were verified to confirm International Federation of Gynecology and Obstetrics stage and ovarian cancer histology and grade.

Table 1

Table 1

Infection rates in surgical patients before implementation of the 5-point surgical site infection reduction bundle (prebundle cohort) were compared with those treated after implementation of the bundle of care (postbundle cohort). Before bundle implementation, the baseline surgical site infection rate in the overall ovarian cancer cytoreductive surgery cohort was 20%, whereas it was 33% in those whose procedures included colon surgery. Within the Comprehensive Unit-based Safety Program, we set an interim goal of reducing the overall infection rate for ovarian cancer cytoreductive surgeries by approximately half within Year 1 of bundle implementation (goal rate approximately 10%) and to reduce this to below 7% for hysterectomy with colon procedures in the second year. Readmission rates pre- and postbundle implementation were also analyzed. Demographic, surgical, and infection-related variables were compared between the pre- and postbundle cohorts using χ2, Fisher exact, and Brown-Mood tests for categorical variables and Student t test and Mann–Whitney test for continuous variables. Unadjusted odds ratios (ORs) using surgical group as the exposure and infection as the outcome were reported for the pre- and postbundle cohorts. All statistical analyses were performed using STATA 13. A P value <.05 was considered statistically significant.

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Two hundred twenty-four patients underwent ovarian cancer cytoreductive surgery during the study period. Five were excluded as a result of missing data elements, leaving 219 patients; 91 patients were treated in the historical prebundle cohort and 128 treated in the postbundle implementation group. Patient demographic and clinical characteristics pre- and postbundle are listed in Table 1. The mean patient age 62.4 years (SD 12.3) compared with 55.7 years (SD 13.3) P<.01); comorbidity profile (greater than two comorbidities—19% in prebundle and 8% in postbundle; P=.02) and American Society of Anesthesiologists score (0 or 1–91% prebundle compared with 97% postbundle; P=.03) were higher in the prebundle cohort. Patient body mass index, estimated blood loss, length of hospital stay, cytoreductive surgery type, International Federation of Gynecology and Obstetrics stage, rates of radical upper abdominal procedures or colon surgery, and residual disease status were not significantly different between the groups.

The overall surgical site infection rate (Table 2) in the prebundle cohort was 20% (18/91). After implementation of the 5-point surgical site infection prevention bundle, the infection rate decreased significantly to 3% (4/128; OR 0.13, 95% CI 0.037–0.53; P<.001). Similarly, among patients who had colon surgery, the surgical site infection rate fell from 33% (14/42) to 7% (3/46; OR 0.14, 95% CI 0.037–0.53; P<.001) after implementation of the infection reduction bundle. This infection reduction was achieved within the first year of care bundle implementation and then maintained within the second year. Distribution of surgical site infection type (based on the National Health Service Network definition in the year the patient underwent surgery)19 included 13 superficial infections, eight deep infections, and one organ space infection (Table 3); types of infection were not different in the pre- and postbundle cohorts. Additionally, rates of surgical site infection-related hospital readmission were also lower in the postbundle (4/128 [3%]) compared with the prebundle group (12/91 [13%]; P=.005). There were no differences in surgical site infection rates when analyzed by individual surgeon.

Table 2

Table 2

Table 3

Table 3

Ninety-seven percent of patients reported compliance with preoperative chlorhexidine skin preparation. Additionally, 91% of patients reported self-administration of 50% or more oral antibiotics and mechanical bowel preparations. Among those who did not complete this regimen, three patients were diagnosed with preoperative small bowel or colon obstructions.

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In this prospective, single-institution quality improvement trial conducted within a high-volume gynecologic oncology service, utilization of a 5-point surgical site infection prevention bundle was associated with a dramatic reduction in the infection rates in our ovarian cancer patient population undergoing cytoreductive surgery—especially in those requiring colectomy procedures. Additionally, the implementation of the prevention bundle was associated with reductions in costly hospital readmissions related to surgical site infection during the study period. Given that women undergoing cytoreductive surgery for advanced ovarian cancer are often elderly, obese, malnourished, and possess comorbidities that put them at risk for development of perioperative complications, this is a population that will particularly benefit from efforts to reduce infection. Our study findings support the use of a 5-point bundle as an effective tool for improving patient safety and quality of care in the setting of ovarian cancer surgery.

Individual elements in our study bundle were derived from evidence-based practice and included skin and vaginal preparation with 4% chlorhexidine23,24 and proper timing and dosing of prophylactic antibiotics (Box 1), which are important infection prevention measures across multiple surgical disciplines.25,26 However, combining these and other individual elements into an infection reduction bundle of care may be the most effective method of decreasing infection rates in vascular, colorectal, and gynecologic surgery.26–31

In 2016, investigators from the Mayo Clinic demonstrated that utilizing a bundled intervention in major gynecologic cancer surgeries (open abdominal endometrial and ovarian cancer cases) reduced surgical site infections.31 An important difference between the current Johns Hopkins study and the Mayo Clinic report was the use of oral antibiotics and mechanical bowel preparation in the Johns Hopkins bundle of care compared with no oral antibiotics or bowel preparation included in the Mayo care bundle. A recent Cochrane database review and other reports indicate that combined preoperative mechanical bowel preparation with oral antibiotics significantly reduces surgical site infections after colectomy surgery.32–41 Scarborough et al40 demonstrated a significant reduction in 30-day surgical site infections rates from 9.0% to 3.2% (P<.001) when 4,999 patients undergoing colectomy from the 2012 National Surgical Quality Improvement Program database received a preoperative mechanical bowel preparation and oral antibiotics compared with patients who did not receive this regimen. A subsequent National Surgical Quality Improvement Program study of bowel and per oral antibiotic prepped elderly patients undergoing colectomy demonstrated significant reductions in anastomotic leak, ileus, superficial and organ space surgical site infection, and respiratory compromise compared with similar patient cohorts who received no bowel preparation, bowel preparation only, or an oral antibiotic preparation only.41 Our prospective data add to a robust body of work24,25,38–40,42 suggesting that use of a combination bowel preparation and oral antibiotic protocol is associated with significant improvement in surgical site infection rates in patients undergoing colectomy surgery.

Surgical site infection surveillance is vital to hospital infection control and quality improvement programs. However, hospitals with surgeons who treat complex patients with nonmodifiable risk factors may have higher infection rates.41–46 Therefore, risk adjustment that controls for differences in patient case mix is essential to allow for meaningful comparisons between hospitals. Historically, the National Health Service Network, a web-based system used by the Centers for Disease Control and Prevention for surveillance of hospital-acquired infections, has calculated risk-stratified surgical site infection rates using an index of three weighted factors: the American Society of Anesthesiologists score, wound classification, and procedure duration.46 Recently, multivariate risk models (ie, standardized infection ratio) that incorporate additional weighted patient factors may calculate more credible and standardized risk-adjusted infection metrics than stratified surgical site infection rates that are limited to the traditional National Health Service Network risk index.46 The establishment of realistic, risk-adjusted infection benchmarks in the setting of gynecologic cancer surgery is warranted.

A critical aspect of our bundle of care intervention was its implementation within a surgery-based, multidisciplinary Comprehensive Unit-based Safety Program. Comprehensive Unit-based Safety Programs were developed by Johns Hopkins safety and quality researchers to reduce the incidence of preventable patient harm by executing specialty-specific, hospital-wide quality improvement initiatives.43 This model allows for physicians, nurses, infection prevention specialists, and other clinical team members to work collaboratively and prospectively to apply best practices and safety science to reduce adverse hospital-related events. Our study methodology and findings suggest that a clinical community such as a Comprehensive Unit-based Safety Program is an effective strategy to conduct quality improvement interventions.43

Strengths of this study include the prospective study design, inclusion of a high-volume patient population undergoing ovarian cancer cytoreductive surgery at a comprehensive cancer center, utilization of an evidence-based protocol that was audited regularly, and independent data collection by a trained infection prevention specialist. We recognize there are also study limitations. There may be confounding factors that contributed to a change in infection rates in the postbundle intervention cohort. However, on multivariate analysis, the implementation of our 5-point infection reduction bundle of care was independently associated with reduced infection rates. The sample size and low overall number of adverse outcomes place limits on the statistical power of the study and the baseline characteristics of the study population may have contributed, in part, to the outcomes. Additionally, because the infection rate in the postbundle cohort was so low, the ratio of adverse events to confounding variables did not allow precise multivariate adjustment. Furthermore, our prospective, observational quality improvement study was not randomized or simultaneous in design. Lastly, given the use of multiple simultaneous interventions, we do not know if one, some, or all of the interventions account for the change in the observed surgical site infection rates.

Surgical site infection continues to be a major factor contributing to perioperative morbidity and mortality and high costs of care in surgical patients. Before our Comprehensive Unit-based Safety Program-led initiative, approximately one in five women undergoing ovarian cancer cytoreductive surgery developed an infection after surgery at our institution; this was significantly reduced to 1 in 21 women with successful implementation of our infection prevention bundle of care. Additionally, by preventing surgical site infections in this setting, costly hospital readmissions and delays in chemotherapy administration may also be thwarted. More studies are needed to determine the generalizability of our bundle of care and Comprehensive Unit-based Safety Program approach to assess the effect of individual bundle elements on infection rates and to ascertain whether the addition of new elements will further decrease these rates.

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