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Surgical site infection after hysterectomy

      Objective

      Our objective was to estimate the occurrence of surgical site infections (SSI) after hysterectomy and the associated risk factors.

      Study Design

      We conducted a cross-sectional analysis of the 2005-2009 American College of Surgeons National Surgical Quality Improvement Program participant use data files to analyze hysterectomies. Different routes of hysterectomy were compared. The primary outcome was to identify the occurrence of 30-day superficial SSI (cellulitis) after hysterectomy. Secondary outcomes were the occurrence of deep and organ-space SSI after hysterectomy. Logistic regression models were conducted to further explore the associations of risks factors with SSI after hysterectomy.

      Results

      A total of 13,822 women were included in our final analysis. The occurrence of postoperative cellulitis after hysterectomy was 1.6% (n = 221 women). Risk factors that were associated with cellulitis were route of hysterectomy with an adjusted odds ratio (AOR) of 3.74 (95% confidence interval [CI], 2.26–6.22) for laparotomy compared with the vaginal approach, operative time >75th percentile (AOR, 1.84; 95% CI, 1.40–2.44), American Society of Anesthesia class ≥ 3 (AOR, 1.79; 95% CI, 1.31–2.43), body mass index ≥40 kg/m2 (AOR, 2.65; 95% CI, 1.85–3.80), and diabetes mellitus (AOR, 1.54; 95% CI, 1.06–2.24) The occurrence of deep and organ-space SSI was 1.1% (n = 154 women) after hysterectomy.

      Conclusion

      Our finding of the decreased occurrence of superficial SSI after the vaginal approach for hysterectomy reaffirms the role for vaginal hysterectomy as the route of choice for hysterectomy.

      Key words

      Recently, United States healthcare initiatives sponsored by the Centers for Medicare and Medicaid Services (CMS) and the Joint Commission on the Accreditation of Healthcare Organizations have targeted preventable hospital-acquired infections, such as postoperative surgical site infections (SSI), as a priority in improving patient safety. Effective January 2012, CMS required all Medicare-certified hospitals to publically report clinical data and outcome measures in a “Systematic Clinical Database Registry for General Surgery” in the Hospital Inpatient Quality Reporting Program.

      Centers for Medicare and Medicaid Services (CMS), HHS. Final rule CMS- 1498-F. federal register volume 75, number 157 (Monday, august 16, 2010)] [rules and regulations] [pages 50041-50677] from the federal register online via the government printing office [www.gpo.gov][FR doc no: 2010-19092. Available at: http://www.gpo.gov/fdsys/pkg/FR-2011-08-18/html/2011-19719.htm. Accessed Dec. 19, 2012.

      The consequence for an institution or hospital not reporting will be a payment penalty as of October 2013. The 2 surgical procedures that were identified by CMS in this recent mandate for public reporting of postoperative SSI are colon surgery and hysterectomy.
      Over the last 2 decades, remarkable advancements have been made in the choice of hysterectomy routes. Although the occurrence and risk factors of SSI after total abdominal hysterectomy (TAH) has been reported,
      • Edwards J.R.
      • Peterson K.D.
      • Andrus M.L.
      • et al.
      National healthcare safety network (NHSN) report, data summary for 2006 through 2007.
      neither the occurrence nor the risk factors of posthysterectomy SSI have been reported by hysterectomy route.
      • Edwards J.R.
      • Peterson K.D.
      • Andrus M.L.
      • et al.
      National healthcare safety network (NHSN) report, data summary for 2006 through 2007.
      • Olsen M.A.
      • Higham-Kessler J.
      • Yokoe D.S.
      • et al.
      Developing a risk stratification model for surgical site infection after abdominal hysterectomy.
      • Young H.
      • Bliss R.
      • Carey J.C.
      • Price C.S.
      Beyond core measures: identifying modifiable risk factors for prevention of surgical site infection after elective total abdominal hysterectomy.
      Better understanding of risk factors for SSI after hysterectomy can help target efforts at the reduction of modifiable risks to prevent infections. Additionally, understanding risk factors for SSI after hysterectomy can lead to better risk stratification in the reporting of quality outcomes. Our objective was to estimate the occurrence of 30-day postoperative SSI after all routes of hysterectomy and to identify associated risk factors.

      Materials and Methods

      We conducted a secondary database analysis of the 2005-2009 American College of Surgeons National Surgical Quality Improvement Program (ACS NSQIP) participant-use data files to analyze the data of women who underwent hysterectomies performed by gynecologic services. The ACS NSQIP is a national program for surgical quality improvement that collects uniform data on patients who undergo surgical procedures. Hospital participation in the ACS NSQIP program is voluntary and confidential. This information is collected by a formal chart review process in addition to a 30-day postoperative follow-up evaluation of patients.
      • Henderson W.G.
      • Daley J.
      Design and statistical methodology of the national surgical quality improvement program: why is it what it is?.
      Variables that are collected include preoperative characteristics, surgical information, and 30-day postoperative complications. The ACS NSQIP database and its quality control measures are further described on their website (http://www.acsnsqip.org). Exemption status for this study was obtained in writing from the Yale Human Investigation Committee, which serves as the Internal Review Board for Yale University.
      Exclusion criteria included (1) male sex, (2) women with the diagnosis of current pregnancy, (3) surgical procedure within 30 days before hysterectomy, (4) Current Procedural Terminology Coding System, 4th edition (CPT-4), code inconsistent with hysterectomy, (5) CPT-4 code that indicates pelvic exenteration procedure at the time of hysterectomy, and (6) women with a diagnosis of preoperative infection that includes sepsis, systemic inflammatory response syndrome, and septic shock immediately before hysterectomy. After exclusion for these criteria, the remaining participants were women who underwent hysterectomy.
      Hysterectomy route was assigned based on CPT-4 coding of the primary procedure: TAH, abdominal supracervical hysterectomy (SCH), total vaginal hysterectomy (TVH), laparoscopic-assisted vaginal hysterectomy (LAVH), total laparoscopic hysterectomy (TLH), and laparoscopic SCH (LASCH). We further examined SSI based on abdominal incisions: (1) laparotomy (TAH or SCH), (2) laparoscopic incisions (LAVH, TLH, or LASCH), or (3) TVH. Finally, we examined SSI based on vaginal cuff incisions: (1) no vaginal cuff incisions (SCH or LASCH) vs (2) vaginal cuff incisions (TAH, TVH, LAVH, and TLH).
      Risk factors for SSI were explored and grouped into the following categories: demographic features, preoperative medical comorbidities, and intraoperative factors. Demographic features included age, race, and ethnicity. Women were dichotomized into the 2 age categories (<80 years old and ≥80 years old) because of a previously demonstrated nonlinear association between age and the log-odds of postoperative infection.
      • Erekson E.A.
      • Yip S.O.
      • Ciarleglio M.M.
      • Fried T.R.
      Postoperative complications after gynecologic surgery.
      Preoperative comorbidities included medical diagnoses, obesity, hysterectomy for gynecologic cancer, preoperative functional status, unintentional weight loss, preoperative laboratory data, and American Society of Anesthesia (ASA) classification. Medical diagnoses that were considered included diabetes mellitus, a history of cerebrovascular accidents (CVA) with neurologic deficit, ascites, preoperative corticosteroid use, and obesity. Obesity was classified based on body mass index (BMI). Women were categorized as having normal weight (BMI, <30 kg/m2), obesity (BMI, ≥30 and <40 kg/m2), and morbid obesity (BMI, ≥40 kg/m2).
      National Institutes of Health
      Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report.
      Women who had undergone hysterectomies for gynecologic cancer were identified by CPT-4 codes that were consistent with lymph node dissection or radical debulking, the diagnoses of preoperative ascites, preoperative disseminated cancer, preoperative chemotherapy, and preoperative radiation therapy. Functional status was defined as a woman's ability to perform activities of daily living, which included bathing, feeding, dressing, toileting, and mobility and was categorized as either independent or dependent. Unintentional weight loss was used as a marker of frailty and was defined as loss of >10% of bodyweight over the previous 6 months. Preoperative laboratory data were used to identify anemia and renal compromise. Anemia was defined as hematocrit of <36% based on the findings of Wu et al
      • Wu W.C.
      • Schifftner T.L.
      • Henderson W.G.
      • et al.
      Preoperative hematocrit levels and postoperative outcomes in older patients undergoing noncardiac surgery.
      and Heisler et al.
      • Heisler C.A.
      • Aletti G.D.
      • Weaver A.L.
      • Melton 3rd, L.J.
      • Cliby W.A.
      • Gebhart J.B.
      Improving quality of care: development of a risk-adjusted perioperative morbidity model for vaginal hysterectomy.
      Renal compromise was defined as a creatinine level of >1.5 mg/dL based on the findings of Dowdy et al.
      • Dowdy S.C.
      • Borah B.J.
      • Bakkum-Gamez J.N.
      • et al.
      Factors predictive of postoperative morbidity and cost in patients with endometrial cancer.
      Intraoperative factors that were explored included the type of anesthesia, wound classification, intraoperative blood transfusion, and procedural difficulty. Concomitant procedures and procedural difficulty were accounted for by an examination of the total work relative value units and total operative time. Procedures had between 1 and 8 CPT codes. To consider the complexity of all the different possible combinations of procedures, work relative value units for all concomitant procedures were totaled. Operative time was categorized as a dichotomous variable above and below the 75th percentile, based on previous work by Culver et al,
      • Culver D.H.
      • Horan T.C.
      • Gaynes R.P.
      • et al.
      Surgical wound infection rates by wound class, operative procedure, and patient risk index: National Nosocomial Infections Surveillance System.
      who demonstrated that operative time of >75th percentile is a risk factor for SSI. For hysterectomies in the ACS NSQIP dataset, the operative time of >75th percentile was 149 minutes.
      SSI categories were defined by the criteria found in the participant use data file of the ACS NSQIP.

      American College of Surgeons National Surgical Quality Improvement Program. Participant use data file. Available at: http://site.acsnsqip.org/participant-use-data-file/. Accessed Aug. 15, 2012.

      These definitions were also based on criteria set by the Centers for Disease Control and Prevention (CDC).
      • Horan T.C.
      • Andrus M.
      • Dudeck M.A.
      CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting.
      The primary outcome was the occurrence of 30-day superficial SSI (cellulitis) after hysterectomy. Cellulitis was defined as an infection that involved only skin or subcutaneous tissue of the surgical incision. Secondary outcomes were the occurrence of deep and organ-space SSI and urinary tract infection (UTI) after hysterectomy. Deep and organ-space SSI included infections that involved deep soft tissues (fascia and muscle) at and around the surgical incision and infections in any part of the body that was opened or manipulated during the operative procedure. This includes vaginal cuff cellulitis and vaginal cuff abscess, peritonitis, and pelvic abscess. Deep and organ-space SSI were considered as 1 category, because these 2 categories were difficult to distinguish when hysterectomy is considered to be the primary procedure. Finally, we examined postoperative UTI, which was defined by CDC criteria for symptomatic UTI and asymptomatic bacteriuria, which take into account the recent use of indwelling catheters and the age of the patient.
      • Horan T.C.
      • Andrus M.
      • Dudeck M.A.
      CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting.
      Descriptive statistics, Student t test, Pearson χ2, and Fisher exact test (2-sided) were performed for bivariate analysis. Three logistic regression models were conducted to further explore the associations of risks factors for cellulitis, deep and organ-space SSI, and postoperative UTI after hysterectomy.
      • Wu W.C.
      • Schifftner T.L.
      • Henderson W.G.
      • et al.
      Preoperative hematocrit levels and postoperative outcomes in older patients undergoing noncardiac surgery.
      • Heisler C.A.
      • Aletti G.D.
      • Weaver A.L.
      • Melton 3rd, L.J.
      • Cliby W.A.
      • Gebhart J.B.
      Improving quality of care: development of a risk-adjusted perioperative morbidity model for vaginal hysterectomy.
      Variables that were associated with SSI were identified for potential inclusion in the final model based on bivariate analysis (P < .1). Variables were added to the model in a stepwise fashion with the use of forward selection (P ≤ .05). Adjusted odds ratios (AORs) and 95% confidence intervals (CIs) were calculated. Statistical analysis was performed with STATA statistical software (version 11.0; Stata Corporation, College Station, TX) and SAS statistical software (version 9.2; SAS Institute Inc, Cary, NC).

      Results

      A total of 23,569 participants were classified as having undergone a gynecologic procedure in the 2005-2009 ACS NSQIP participant use dataset. The following exclusions were made from the final analysis: (1) male sex (n = 51), (2) women with the diagnosis of current pregnancy (n = 416), (3) surgical procedure within 30 days before hysterectomy (n = 185), (4) CPT-4 code inconsistent with hysterectomy (n = 8943), (5) CPT-4 code that indicated pelvic exenteration procedure at the time of hysterectomy (n = 10), and (6) women with diagnosis of preoperative infection that included sepsis, systemic inflammatory response syndrome, and septic shock immediately before hysterectomy (n = 142). A total of 13,822 women underwent hysterectomy and were included in our final analysis.

      Cellulitis

      The overall occurrence of cellulitis (superficial SSI) after hysterectomy was 1.6% (n/N = 221/13,822). Four women (0.03%) received a diagnosis of both postoperative cellulitis and deep or organ-space SSI. Twelve women (0.08%) received a diagnosis of both postoperative cellulitis and UTI. Variables that were associated with cellulitis on bivariate analysis included diabetes mellitus (P < .001), BMI category (P < .001), preoperative ascites (P < .01), unintentional weight loss (P = .02), hysterectomy for cancer (P < .001), ASA class ≥3 (P < .001), work relative value unit (P < .001), use of general anesthesia (P = .001), and an operative time >75th percentile (P < .001; Table 1).
      Table 1Demographic and clinical characteristics of 30-day postoperative superficial surgical site infection after hysterectomy (n = 13,822 women)
      VariableCellulitis (n = 221)No cellulitis (n = 13,601)P value
      Age, n (%)1.0
       <80 y218 (98.6)13,378 (98.4)
       ≥80 y3 (1.4)223 (1.6)
      Race: white, n (%)129 (58.4)8265 (60.8).49
      Ethnicity: Hispanic, n (%)27 (12.2)2180 (16.0).14
      Diabetes mellitus, n (%)41 (18.6)982 (7.2%)< .001
      History of cerebrovascular accident with neurologic deficit, n (%)1 (0.5)65 (0.5%)1.0
      Current smoker, n (%)51 (23.1)2671 (19.6%).20
      Body mass index, n (%)< .001
       <30 kg/m278 (35.3)7598 (55.9)
       ≥30 and <40 kg/m274 (33.5)4564 (33.6)
       ≥40 kg/m269 (31.2)1439 (10.6)
      Ascites, n (%)6 (2.7)104 (0.8)< .01
      Unintentional weight loss, n (%)
      Loss of ≥10% of body weight in the previous 6 months not because of exercise or dieting
      4 (1.8)62 (0.5).02
      Functional status: dependent for activities of daily living, n (%)2 (0.9)97 (0.7).67
      Hysterectomy for gynecologic cancer, n (%)32 (14.5)871 (6.4)< .001
      Preoperative anemia: hematocrit (<36%), n (%)48 (22.3)2976 (22.8).94
      Preoperative creatinine level >1.5 mg/dL, n (%)3 (1.8)75 (0.9).18
      American Society of Anesthesiologists class ≥3, n (%)93 (42.1)2521 (18.5)< .001
      Intraoperative blood transfusion, n (%)15 (6.8)329 (2.4)< .001
      Work relative value unit
      Data are given as mean ± SD.
      18.7 ± 5.117.3 ± 3.8< .001
      Operative time >75th percentile duration, n (%)93 (42.1)3378 (24.8)< .001
      Type of anesthesia: general, n (%)221 (100.0)13,111 (96.4).001
      Wound class, n (%).06
       1-Clean033 (0.2)
       2-Clean/contaminated215 (97.3)13,443 (98.8)
       3-Contaminated5 (2.3)92 (0.7)
       4-Dirty1 (0.5)33 (0.2)
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.
      a Loss of ≥10% of body weight in the previous 6 months not because of exercise or dieting
      b Data are given as mean ± SD.
      Variables that were associated with 30-day postoperative cellulitis on multivariate logistic regression were the route of hysterectomy with an AOR of 3.74 (95% CI, 2.26–6.22) for laparotomy incisions compared with vaginal approach, operative time >75th percentile (AOR, 1.84; 95% CI, 1.40–2.44), ASA class ≥3 (AOR, 1.79; 95% CI, 1.31–2.43), morbid obesity (BMI, ≥40 kg/m2; AOR, 2.65; 95% CI, 1.85–3.80), and diabetes mellitus (AOR, 1.54; 95% CI, 1.06–2.24; Table 2).
      Table 2Logistic regression model for association of cellulitis after hysterectomy
      VariableAdjusted odds ratio95% CIP value
      Route of hysterectomy
       Total vaginal hysterectomy (referent)1
       Laparotomy
      Laparotomy included total abdominal hysterectomy and supracervical hysterectomy
      3.742.26–6.22< .001
       Laparoscopic incisions
      Laparoscopic incisions included laparoscopic-assisted vaginal hysterectomy, total laparoscopic hysterectomy, and laparoscopic supracervical hysterectomy.
      1.450.83–2.56.20
      Operative time >75th percentile duration1.841.40–2.44< .001
      American Society of Anesthesiologists class ≥31.791.31–2.43< .001
      Body mass index, kg/m2
       <30 (referent)1
       ≥30 and <401.310.94–1.81.11
       ≥402.651.85–3.80< .001
      Diabetes mellitus1.541.06–2.24.02
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.
      a Laparotomy included total abdominal hysterectomy and supracervical hysterectomy
      b Laparoscopic incisions included laparoscopic-assisted vaginal hysterectomy, total laparoscopic hysterectomy, and laparoscopic supracervical hysterectomy.

      Deep and organ-space SSI

      The occurrence of deep and organ-space SSI was 1.1% (n/N = 154/13,822) after hysterectomy. No women were categorized as having both a deep space SSI and an organ-space SSI. Twenty-one women (0.1%) were diagnosed with both postoperative deep/organ-space SSI and UTI. Variables that were associated with deep and organ-space SSI on bivariate analysis included race (P = .001), diabetes mellitus (P < .01), history of CVA with neurologic deficit (P < .01), current smoking (P = .001), obesity category (P = .11), preoperative ascites (P = .04), preoperative anemia (P < .01), ASA class ≥3 (P < .001), and an operative time >75th percentile (P = .03; Table 3).
      Table 3Demographic and clinical characteristics of 30-day postoperative deep or organ-space surgical site infection after hysterectomy (n = 13,822)
      VariableSurgical site infectionP value
      Deep/organ-space (n = 154)No deep/organ-space (n = 13,668)
      Age, n (%)1.0
       <80 y152 (98.7)13,444 (98.4)
       ≥80 y2 (1.3)224 (1.6)
      Race: white, n (%)73 (47.4)8321 (60.9).001
      Ethnicity: Hispanic, n (%)32 (20.8)2175 (15.9).12
      Diabetes mellitus, n (%)23 (14.9)1000 (7.3)< .01
      History of cerebrovascular accident with neurologic deficit, n (%)4 (2.6)62 (0.5)< .01
      Current smoker, n (%)47 (30.5)2675 (19.6).001
      Body mass index, n (%)< .001
       <30 kg/m268 (44.2)7608 (55.7)
       ≥30 and <40 kg/m250 (32.5)4588 (33.6)
       ≥40 kg/m236 (23.4)1472 (10.8)
      Ascites, n (%)4 (2.6)106 (0.8).04
      Unintentional weight loss, n (%)
      Loss of ≥10% of body weight in the previous 6 months not because of exercise or dieting
      2 (1.3)64 (0.5).17
      Functional status: dependent for activities of daily living, n (%)2 (1.3)97 (0.7).30
      Hysterectomy for gynecologic cancer, n (%)13 (8.4)890 (6.5).32
      Preoperative anemia: hematocrit (<36%), n (%)50 (33.8)2974 (22.7)< .01
      Preoperative creatinine >1.5 mg/dL, n (%)3 (2.8)75 (0.9).08
      American Society of Anesthesiologists class ≥3, n (%)54 (35.1)2560 (18.7)< .001
      Intraoperative blood transfusion, n (%)8 (5.2)336 (2.5).06
      Work relative value unit
      Data are given as mean ± SD.
      17.8 ± 4.617.3 ± 3.8.13
      Operative time: >75th percentile duration, n (%)51 (33.1)3420 (25.0).03
      Type of anesthesia: general, n (%)148 (96.1)13,184 (96.5).82
      Wound class, n (%).16
       1-Clean033 (0.2)
       2-Clean/contaminated150 (97.4)13,508 (98.8)
       3-Contaminated3 (2.0)94 (0.7)
       4-Dirty1 (0.7)33 (0.2)
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.
      a Loss of ≥10% of body weight in the previous 6 months not because of exercise or dieting
      b Data are given as mean ± SD.
      Variables that were associated with deep and organ-space SSI on multivariate logistic regression included ASA class ≥3 (AOR, 1.81; 95% CI, 1.25–2.62), current smoking (AOR, 1.99; 95% CI, 1.40–2.83), history of CVA with neurologic deficit (AOR, 4.41; 95% CI, 1.54–12.65), preoperative anemia (AOR, 1.72; 95% CI, 1.21–2.43), and morbid obesity (AOR, 2.23; 95% CI, 1.43–3.49; Table 4). When we examined hysterectomy route, both by abdominal incisions and by vaginal cuff incisions, with deep and organ-space SSI, we did not find any significant associations.
      Table 4Logistic regression model for association of deep or organ space surgical site infection after hysterectomy
      VariableAdjusted odds ratio95% CIP value
      American Society of Anesthesiologists class ≥31.811.25–2.62< .01
      Current smoker1.991.40–2.83< .001
      History of cerebrovascular accident with neurologic deficit4.411.54–12.65< .01
      Preoperative anemia (hematocrit, <36%)1.721.21–2.43< .01
      Body mass index, kg/m2
       <30 (referent)1
       ≥30 and <401.190.82–1.74.36
       ≥402.231.43–3.49< .001
      CI, confidence interval.
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.

      UTI

      Postoperative UTI occurred in 2.7% of women (n/N = 370/13,822) after hysterectomy. Variables that were associated with postoperative UTI on bivariate analysis included history of CVA with neurologic deficit (P = .01), ASA class ≥3 (P < .01), and an operative time >75th percentile (P < .001; Table 5). Variables that were associated with postoperative UTI on multivariate logistic regression were a history of CVA with neurologic deficit (AOR, 3.29; 95% CI, 1.41–7.70), current corticosteroid use (AOR, 2.37; 95% CI, 1.14–4.90), and operative time >75th percentile (AOR, 1.86; 95% CI, 1.52–2.29; Table 6).
      Table 5Demographic and clinical characteristics of 30-day postoperative urinary tract infection after hysterectomy (n = 13,822)
      VariableUrinary tract infection (n = 402)No urinary tract infection (n = 13,420)P value
      Age, n (%).16
       <80 y392 (97.5)13,204 (98.4%)
       ≥80 y10 (2.5)216 (1.6%)
      Race: white, n (%)259 (64.4)8135 (60.6%).13
      Ethnicity: Hispanic, n (%)57 (14.2)2150 (16.0%).37
      Diabetes mellitus, n (%)23 (5.7)1000 (7.5).21
      History of cerebrovascular accident with neurologic deficit, n (%)6 (1.5)60 (0.5).01
      Current smoker, n (%)90 (22.4)2632 (19.6).18
      Body mass index.42
       <30 kg/m2215 (53.5)7461 (55.6)
       ≥30 and <40 kg/m2147 (36.6)4491 (33.5)
       ≥40 kg/m240 (10.0)1468 (10.9)
      Ascites, n (%)2 (0.5)108 (0.8).77
      Unintentional weight loss, n (%)
      Loss of 10% or more of body weight in the previous 6 months not because of exercise or dieting
      4 (1.0)62 (0.5).13
      Functional status: dependent for activities of daily living, n (%)6 (1.5)93 (0.7).07
      Hysterectomy for gynecologic cancer, n (%)26 (6.5)877 (6.5)1.00
      Preoperative anemia: hematocrit (<36%), n (%)79 (20.6)2945 (22.9).32
      Preoperative creatinine >1.5 mg/dL, n (%)3 (1.2)75 (0.9).51
      American Society of Anesthesiologists class ≥3, n (%)99 (24.6)2515 (18.7)< .01
      Intraoperative blood transfusion, n (%)9 (2.2)335 (2.5).87
      Work relative value unit
      Data are given as mean ± SD.
      17.1 ± 3.817.3 ± 3.8.33
      Operative time: >75th percentile duration, n (%)153 (38.1)3318 (24.7)< .001
      Type of anesthesia: general, n (%)393 (97.8)12,939 (96.4).17
      Wound class, n (%).87
       1-Clean033 (0.3)
       2-Clean/contaminated398 (99.0)13,260 (98.8)
       3-Contaminated3 (0.8)94 (0.7)
       4-Dirty1 (0.3)33 (0.3)
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.
      a Loss of 10% or more of body weight in the previous 6 months not because of exercise or dieting
      b Data are given as mean ± SD.
      Table 6Logistic regression model for association of urinary tract infection after hysterectomy
      VariableAdjusted odds ratio95% CIP value
      History of cerebrovascular accident with neurologic deficit3.291.41–7.70< .01
      Current corticosteroid use2.371.14–4.90.02
      Operative time >75th percentile duration1.861.52–2.29< .001
      CI, confidence interval.
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.

      Occurrence of SSI by route of hysterectomy

      When we examined 6 different routes of hysterectomy (TAH, SCH, TLH, LASCH, LAVH, and TVH), we noticed similarities in the occurrence of SSI by abdominal incision type (Table 7). We examined routes of hysterectomy solely based on abdominal incisions (laparotomy, laparoscopic incisions, and no abdominal incisions) and noted that the route of hysterectomy was associated with superficial SSI, but not deep/organ-space SSI or postoperative UTI. Finally, we examined the association of posthysterectomy SSI by the presence or absence of vaginal cuff incisions (SCH vs vaginal colpotomy) and found no association with any postoperative SSI.
      Table 7All 30-day postoperative surgical site infections and urinary tract infections by hysterectomy route (n = 13,822)
      Type of surgical site infectionnTotal abdominal hysterectomy, n (%)Supracervical hysterectomy, n (%)Total vaginal hysterectomy, n (%)Laparoscopic-assisted vaginal hysterectomy, n (%)Total laparoscopic hysterectomy, n (%)Laparoscopic supracervical hysterectomy, n (%)
      None13,081 (94.6)5069 (93.8)688 (94.0)2921 (95.3)2094 (94.3)837 (95.2)1472 (96.7)
      Cellulitis217 (1.6)141 (2.6)17 (2.3)17 (0.6)17 (0.8)5 (0.6)20 (1.3)
      Deep/organ-space154 (1.1)67 (1.2)8 (1.1)32 (1.0)33 (1.5)4 (0.5)10 (0.7)
      Urinary tract infection370 (2.7)128 (2.4)19 (2.6)94 (3.1)76 (3.4)33 (3.8)20 (1.3)
      Lake. Surgical site infections after hysterectomy. Am J Obstet Gynecol 2013.

      Comment

      We found the overall occurrence of both 30-day cellulitis (superficial SSI) and deep and organ-space SSI after hysterectomy to be 2.7%. The occurrence of UTI after hysterectomy was 3.0%.
      The following risk factors were associated with the occurrence of postoperative cellulitis: hysterectomy route, operative time >75th percentile (149 minutes), ASA class ≥3, diabetes mellitus, and obesity category (BMI, ≥40 kg/m2). We did not find smoking status or hysterectomy for gynecologic cancer to be independent risk factors for postoperative cellulitis.
      Our finding of the decreased occurrence of superficial SSI after the vaginal approach for hysterectomy reaffirms the long-appreciated role for vaginal hysterectomy as the route of choice for hysterectomy.
      • Kovac S.R.
      Guidelines to determine the route of hysterectomy.
      • Falcone T.
      • Walters M.D.
      Hysterectomy for benign disease.
      American College of Obstetricians and Gynecologists
      ACOG committee opinion no. 444: choosing the route of hysterectomy for benign disease.
      Laparotomy independently increased the risk of superficial SSI after hysterectomy. A trend was seen for increased SSI with trocar incisions (minimally invasive hysterectomies), but this was not statistically significant.
      Our findings add to previous work with National Healthcare Safety Network (NHSN) data to examine SSI.
      • Edwards J.R.
      • Peterson K.D.
      • Andrus M.L.
      • et al.
      National healthcare safety network (NHSN) report, data summary for 2006 through 2007.
      • Mu Y.
      • Edwards J.R.
      • Horan T.C.
      • Berrios-Torres S.I.
      • Fridkin S.K.
      Improving risk-adjusted measures of surgical site infection for the national healthcare safety network.
      The NHSN is an internet-based surveillance system that is used by the CDC to monitor hospital-acquired infections that include SSI.

      Centers for Disease Control and Prevention. National Healthcare Safety Network (NHSN). Available at: http://www.cdc.gov/nhsn/. Accessed Aug. 15, 2012.

      Originally, the NHSN-based risk adjustment for all SSI was based on the predictive model of Culver et al
      • Culver D.H.
      • Horan T.C.
      • Gaynes R.P.
      • et al.
      Surgical wound infection rates by wound class, operative procedure, and patient risk index: National Nosocomial Infections Surveillance System.
      that incorporated wound classification, ASA classification, and operative time. Using these risk factors, Edwards et al
      • Edwards J.R.
      • Peterson K.D.
      • Andrus M.L.
      • et al.
      National healthcare safety network (NHSN) report, data summary for 2006 through 2007.
      analyzed nearly 7000 hysterectomies that were reported to the NHSN. The occurrence of all postoperative SSI (superficial, deep and organ-space) after TVH was 0.9% and after TAH was 1.7%. Unlike the reports by Culver et al and Edwards et al, our study sought to identify risk factors for SSI that are more specific to hysterectomy. By examining various possible risk factors, our study suggests additional risk factors, such as route of hysterectomy, preoperative anemia, smoking status, and history of CVA that should be considered in future studies that examine SSI after hysterectomy.
      Our findings are based on multiinstitutional data that were collected in a standardized fashion. Olsen et al
      • Olsen M.A.
      • Higham-Kessler J.
      • Yokoe D.S.
      • et al.
      Developing a risk stratification model for surgical site infection after abdominal hysterectomy.
      performed a multicenter retrospective case-controlled study with approximately 800 patients after TAH and TVH. The cases and control subjects were collected with the use of the International Classification of Diseases, Ninth Revision, Clinical Modification procedure codes for hysterectomy from 4 participating CDC Prevention Epicenter Program hospitals from 2003-2005. Both BMI >35 kg/m2 and intra-/postoperative blood transfusion were identified as independent risk factors for superficial SSI after hysterectomy with laparotomy. Similarly, a single institution chart review also found obesity (BMI, ≥30 kg/m2) and blood transfusion (pre-, intra-, and postoperative) to be associated with all SSI after abdominal hysterectomy.
      • Young H.
      • Bliss R.
      • Carey J.C.
      • Price C.S.
      Beyond core measures: identifying modifiable risk factors for prevention of surgical site infection after elective total abdominal hysterectomy.
      However, others have found obesity not to be a risk factor for postoperative complications after gynecologic surgery.
      • Chen C.C.
      • Collins S.A.
      • Rodgers A.K.
      • Paraiso M.F.
      • Walters M.D.
      • Barber M.D.
      Perioperative complications in obese women vs normal-weight women who undergo vaginal surgery.
      We found that, by considering BMI >30 kg/m2, BMI was identified as a risk-factor for superficial SSI (cellulitis).
      In our larger multicenter analysis, we did not find an association between preoperative transfusion and SSI. Although intraoperative transfusion was identified in our bivariate analysis to be associated with cellulitis and deep/organ-space SSI, we did not find a statistically significant association between intraoperative transfusion and SSI after adjusting for other variables. The differences in our findings and previous reports regarding transfusion (both pre- and intraoperative) as a risk factor for SSI after hysterectomy likely are related to the robust sample size of our study.
      We identified risk factors that were associated with deep and organ-space SSI after hysterectomy that included preoperative anemia and history of CVA, which may be reflective of chronic preoperative systemic disease. These risk factors are in addition to risk factors of ASA class ≥3, current smoking status, and morbid obesity (BMI, ≥40 kg/m2). We did not find a statistically significant difference in deep and organ-space SSI between different hysterectomy routes. We hypothesize that our findings of increased association of both preoperative anemia and history of CVA with deep and organ-space SSI may reflect a decrease of the body's ability to respond to stressors of surgery and to combat postoperative infection. We found an association between preoperative CVA with residual neurologic deficit and the risk of deep and organ-space SSI. CVA has been noted to be associated significantly with any adverse postoperative event.
      • Liu L.L.
      • Leung J.M.
      Predicting adverse postoperative outcomes in patients aged 80 years or older.
      We believe that we may have observed this relationship because CVA with residual neurologic deficit is a risk factor for functional dependence.
      • Fernandes T.G.
      • Goulart A.C.
      • Santos-Junior W.R.
      • Alencar A.P.
      • Bensenor I.M.
      • Lotufo P.A.
      Educational levels and the functional dependence of ischemic stroke survivors.
      Chen et al
      • Chen T.Y.
      • Anderson D.J.
      • Chopra T.
      • Choi Y.
      • Schmader K.E.
      • Kaye K.S.
      Poor functional status is an independent predictor of surgical site infections due to methicillin-resistant staphylococcus aureus in older adults.
      found functional dependence to be an independent risk factor for postoperative SSI, specifically methicillin-resistant Staphylococcus aureus SSI, in older adults.
      We did not find differences in risk factors for deep and organ-space SSI when we examined these infections separately. We ultimately chose to combine these 2 categories when examining SSI after hysterectomy. We believe that deep and organ-space SSI, although defined distinctly by the ACS NSQIP and CDC criteria, are functionally the same event after hysterectomy because of the incision at the vaginal cuff. After a hysterectomy, an example of a deep SSI would be considered a vaginal cuff abscess. We believe that a pelvic abscess that drains through the vaginal cuff, which would be considered as a deep space SSI draining through the surgical incision, is essentially similar to a pelvic abscess that requires drainage through interventional radiology, which alternatively would be categorized as an organ-space SSI. Because of the overlap between these terms, we elected to combine deep and organ-space SSI.
      The risk factors associated with postoperative UTI after hysterectomy were a history of CVA with neurologic deficit, chronic steroid use, and operative time >75th percentile. We found the occurrence of 30-day postoperative UTI was 3.0% (n = 402 women) after hysterectomy. Unfortunately, we did not have information on catheter use or duration because of limits of the dataset.
      One hundred forty-two women were identified as having preoperative systemic infection that included sepsis, septic shock, and systemic inflammatory response syndrome and were excluded because of the inherent difference in these cases from women who undergo scheduled elective surgery. Although these conditions may be associated with a greater risk of postoperative SSI, the small numbers and the various different causes of systemic infection made it difficult to draw conclusions in the current study.
      Our study has many limitations. The first is that our analysis was limited to the variables that existed in the database. For example, we were limited by the ACS NSQIP definition of deep and organ-space SSI; therefore, we were also unable to distinguish between pelvic abscesses, vaginal cuff cellulitis, or fasciitis.
      Second, specific variables were not collected in the general ACS-NSQIP dataset that would have enhanced our study findings. For example, the type and timing of preoperative prophylactic antibiotic administration, which is a factor linked to postoperative infection,
      • Rosenberger L.H.
      • Politano A.D.
      • Sawyer R.G.
      The surgical care improvement project and prevention of post-operative infection, including surgical site infection.
      American College of Obstetricians and Gynecologists Committee on Practice Bulletins: Gynecology
      ACOG practice bulletin, No. 104: antibiotic prophylaxis for gynecologic procedures.
      were not available in the database. Another limitation of this dataset was the lack of information about the indication for hysterectomy. Surgical procedures were categorized by CPT codes alone. The occurrence of postoperative UTI after prolapse or antiincontinence surgery has been reported to be higher than that found in our study.
      • Sutkin G.
      • Alperin M.
      • Meyn L.
      • Wiesenfeld H.C.
      • Ellison R.
      • Zyczynski H.M.
      Symptomatic urinary tract infections after surgery for prolapse and/or incontinence.
      Because the women were selected for inclusion in this study based on hysterectomy and not prolapse or incontinence procedures, we were not able to determine the occurrence of UTI after prolapse or incontinence procedures in our current analysis.
      We did not find an association with hysterectomies that were performed for gynecologic cancer and SSI based on CPT-4 codes. This finding may also be due to the lack of specific information in the dataset regarding cancer stage, grade, and pathologic condition in the ACS NSQIP dataset. We were limited to the identification of procedures for gynecologic cancer based on CPT-4 codes that indicated radical dissection and lymphadenectomies. Additionally, some hysterectomies for cancer that required bowel resection may have been coded primarily as colon surgery and therefore not included in our analysis. We did examine all cancer variables that were available in the ACS NSQIP dataset (including known disseminated tumor, chemotherapy, or radiation therapy within 30 days before procedure and known central nervous system tumor) both individually and as a composite group and did not find a statistically significant association with SSI. This, again, likely reflects the limitation of the dataset because it does not include cancer stage, grade, and disease.
      Last, hospital participation in the ACS NSQIP is voluntary and confidential, which may introduce selection bias; however, as of 2009, >320 hospitals were participating in the ACS NSQIP program, which included a wide-range of community hospitals and tertiary care centers. The ACS NSQIP participant-use data files do not allow for identification of participating hospitals within the dataset; therefore, we were not able to account for the effect of clustering of observations within centers. However, previous investigators have demonstrated that the clustering effect from the ASC NSQIP for other endpoints is minimal and did not change the overall adjusted outcomes.
      • Henderson W.G.
      • Daley J.
      Design and statistical methodology of the national surgical quality improvement program: why is it what it is?.
      • Cohen M.E.
      • Dimick J.B.
      • Bilimoria K.Y.
      • Ko C.Y.
      • Richards K.
      • Hall B.L.
      Risk adjustment in the American College of Surgeons National Surgical Quality Improvement Program: a comparison of logistic vs hierarchical modeling.
      Our study suggests that numerous factors, which include hysterectomy route, operative time, diabetes mellitus, ASA class ≥3, BMI, smoking status, preoperative anemia, CVA with neurologic deficit, and corticosteroid use are associated with SSI after hysterectomy. Development of a predictive model for SSI after all types of hysterectomy is needed. Unfortunately, we cannot develop a predictive model with this current work because of a lack of a validation cohort.
      Decreasing preventable hospital-acquired infections is important for the sake of quality patient care. In light of the recent national CMS mandate that requires all Medicare-certified hospitals to report data and outcome measures publicly, the prevention of SSI will soon become important for a hospital's financial stability as well.

      Centers for Medicare and Medicaid Services (CMS), HHS. Final rule CMS- 1498-F. federal register volume 75, number 157 (Monday, august 16, 2010)] [rules and regulations] [pages 50041-50677] from the federal register online via the government printing office [www.gpo.gov][FR doc no: 2010-19092. Available at: http://www.gpo.gov/fdsys/pkg/FR-2011-08-18/html/2011-19719.htm. Accessed Dec. 19, 2012.

      The ACS NSQIP program to improve quality and patient safety has succeeded by providing timely, consistent, confidential, risk-adjusted feedback to participating institutions on the institutional occurrence of a wide range of postoperative complications.
      • Henderson W.G.
      • Daley J.
      Design and statistical methodology of the national surgical quality improvement program: why is it what it is?.
      Institutions immediately can identify systems and strategies to improve patient outcomes in outlying areas.
      • Henderson W.G.
      • Daley J.
      Design and statistical methodology of the national surgical quality improvement program: why is it what it is?.
      This confidential risk-adjusted program has begun to improve surgical outcomes. Knowledge of the baseline occurrence of postoperative SSI after different routes of hysterectomy and associated risk factors is important to improve patient safety after hysterectomy by helping to identify modifiable factors to prevent SSI. Because CMS enforces mandatory public reporting of postoperative SSI after hysterectomy without risk adjustment specific to hysterectomy, careful monitoring must be used to identify unintended consequences.

      References

      1. Centers for Medicare and Medicaid Services (CMS), HHS. Final rule CMS- 1498-F. federal register volume 75, number 157 (Monday, august 16, 2010)] [rules and regulations] [pages 50041-50677] from the federal register online via the government printing office [www.gpo.gov][FR doc no: 2010-19092. Available at: http://www.gpo.gov/fdsys/pkg/FR-2011-08-18/html/2011-19719.htm. Accessed Dec. 19, 2012.

        • Edwards J.R.
        • Peterson K.D.
        • Andrus M.L.
        • et al.
        National healthcare safety network (NHSN) report, data summary for 2006 through 2007.
        Am J Infect Control. 2008; 36: 609-626
        • Olsen M.A.
        • Higham-Kessler J.
        • Yokoe D.S.
        • et al.
        Developing a risk stratification model for surgical site infection after abdominal hysterectomy.
        Infect Control Hosp Epidemiol. 2009; 30: 1077-1083
        • Young H.
        • Bliss R.
        • Carey J.C.
        • Price C.S.
        Beyond core measures: identifying modifiable risk factors for prevention of surgical site infection after elective total abdominal hysterectomy.
        Surg Infect (Larchmt). 2011; 12: 491-496
        • Henderson W.G.
        • Daley J.
        Design and statistical methodology of the national surgical quality improvement program: why is it what it is?.
        Am J Surg. 2009; 198: S19-S27
        • Erekson E.A.
        • Yip S.O.
        • Ciarleglio M.M.
        • Fried T.R.
        Postoperative complications after gynecologic surgery.
        Obstet Gynecol. 2011; 118: 785-793
        • National Institutes of Health
        Clinical guidelines on the identification, evaluation, and treatment of overweight and obesity in adults: the evidence report.
        Obes Res. 1998; 6: 51S-209S
        • Wu W.C.
        • Schifftner T.L.
        • Henderson W.G.
        • et al.
        Preoperative hematocrit levels and postoperative outcomes in older patients undergoing noncardiac surgery.
        JAMA. 2007; 297: 2481-2488
        • Heisler C.A.
        • Aletti G.D.
        • Weaver A.L.
        • Melton 3rd, L.J.
        • Cliby W.A.
        • Gebhart J.B.
        Improving quality of care: development of a risk-adjusted perioperative morbidity model for vaginal hysterectomy.
        Am J Obstet Gynecol. 2010; 202: 137.e1-137.e5
        • Dowdy S.C.
        • Borah B.J.
        • Bakkum-Gamez J.N.
        • et al.
        Factors predictive of postoperative morbidity and cost in patients with endometrial cancer.
        Obstet Gynecol. 2012; 120: 1419-1427
        • Culver D.H.
        • Horan T.C.
        • Gaynes R.P.
        • et al.
        Surgical wound infection rates by wound class, operative procedure, and patient risk index: National Nosocomial Infections Surveillance System.
        Am J Med. 1991; 91: 152S-157S
      2. American College of Surgeons National Surgical Quality Improvement Program. Participant use data file. Available at: http://site.acsnsqip.org/participant-use-data-file/. Accessed Aug. 15, 2012.

        • Horan T.C.
        • Andrus M.
        • Dudeck M.A.
        CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting.
        Am J Infect Control. 2008; 36: 309-332
        • Kovac S.R.
        Guidelines to determine the route of hysterectomy.
        Obstet Gynecol. 1995; 85: 18-23
        • Falcone T.
        • Walters M.D.
        Hysterectomy for benign disease.
        Obstet Gynecol. 2008; 111: 753-767
        • American College of Obstetricians and Gynecologists
        ACOG committee opinion no. 444: choosing the route of hysterectomy for benign disease.
        Obstet Gynecol. 2009; 114: 1156-1158
        • Mu Y.
        • Edwards J.R.
        • Horan T.C.
        • Berrios-Torres S.I.
        • Fridkin S.K.
        Improving risk-adjusted measures of surgical site infection for the national healthcare safety network.
        Infect Control Hosp Epidemiol. 2011; 32: 970-986
      3. Centers for Disease Control and Prevention. National Healthcare Safety Network (NHSN). Available at: http://www.cdc.gov/nhsn/. Accessed Aug. 15, 2012.

        • Chen C.C.
        • Collins S.A.
        • Rodgers A.K.
        • Paraiso M.F.
        • Walters M.D.
        • Barber M.D.
        Perioperative complications in obese women vs normal-weight women who undergo vaginal surgery.
        Am J Obstet Gynecol. 2007; 197: 98.e1-98.e8
        • Liu L.L.
        • Leung J.M.
        Predicting adverse postoperative outcomes in patients aged 80 years or older.
        J Am Geriatr Soc. 2000; 48: 405-412
        • Fernandes T.G.
        • Goulart A.C.
        • Santos-Junior W.R.
        • Alencar A.P.
        • Bensenor I.M.
        • Lotufo P.A.
        Educational levels and the functional dependence of ischemic stroke survivors.
        Cad Saude Publica. 2012; 28: 1581-1590
        • Chen T.Y.
        • Anderson D.J.
        • Chopra T.
        • Choi Y.
        • Schmader K.E.
        • Kaye K.S.
        Poor functional status is an independent predictor of surgical site infections due to methicillin-resistant staphylococcus aureus in older adults.
        J Am Geriatr Soc. 2010; 58: 527-532
        • Rosenberger L.H.
        • Politano A.D.
        • Sawyer R.G.
        The surgical care improvement project and prevention of post-operative infection, including surgical site infection.
        Surg Infect (Larchmt). 2011; 12: 163-168
        • American College of Obstetricians and Gynecologists Committee on Practice Bulletins: Gynecology
        ACOG practice bulletin, No. 104: antibiotic prophylaxis for gynecologic procedures.
        Obstet Gynecol. 2009; 113: 1180-1189
        • Sutkin G.
        • Alperin M.
        • Meyn L.
        • Wiesenfeld H.C.
        • Ellison R.
        • Zyczynski H.M.
        Symptomatic urinary tract infections after surgery for prolapse and/or incontinence.
        Int Urogynecol J. 2010; 21: 955-961
        • Cohen M.E.
        • Dimick J.B.
        • Bilimoria K.Y.
        • Ko C.Y.
        • Richards K.
        • Hall B.L.
        Risk adjustment in the American College of Surgeons National Surgical Quality Improvement Program: a comparison of logistic vs hierarchical modeling.
        J Am Coll Surg. 2009; 209: 687-693