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/m 2 (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.
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. 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, neither the occurrence nor the risk factors of posthysterectomy SSI have been reported by hysterectomy route. 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. 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. 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/m 2 ), obesity (BMI, ≥30 and <40 kg/m 2 ), and morbid obesity (BMI, ≥40 kg/m 2 ). 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 and Heisler et al. Renal compromise was defined as a creatinine level of >1.5 mg/dL based on the findings of Dowdy et al. 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, 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. These definitions were also based on criteria set by the Centers for Disease Control and Prevention (CDC). 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.
Descriptive statistics, Student t test, Pearson χ 2 , 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. 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 ).
| Variable | Cellulitis (n = 221) | No cellulitis (n = 13,601) | P value |
|---|---|---|---|
| Age, n (%) | 1.0 | ||
| <80 y | 218 (98.6) | 13,378 (98.4) | |
| ≥80 y | 3 (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/m 2 | 78 (35.3) | 7598 (55.9) | |
| ≥30 and <40 kg/m 2 | 74 (33.5) | 4564 (33.6) | |
| ≥40 kg/m 2 | 69 (31.2) | 1439 (10.6) | |
| Ascites, n (%) | 6 (2.7) | 104 (0.8) | < .01 |
| Unintentional weight loss, n (%) a | 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 b | 18.7 ± 5.1 | 17.3 ± 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-Clean | 0 | 33 (0.2) | |
| 2-Clean/contaminated | 215 (97.3) | 13,443 (98.8) | |
| 3-Contaminated | 5 (2.3) | 92 (0.7) | |
| 4-Dirty | 1 (0.5) | 33 (0.2) |
a Loss of ≥10% of body weight in the previous 6 months not because of exercise or dieting
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/m 2 ; AOR, 2.65; 95% CI, 1.85–3.80), and diabetes mellitus (AOR, 1.54; 95% CI, 1.06–2.24; Table 2 ).
| Variable | Adjusted odds ratio | 95% CI | P value |
|---|---|---|---|
| Route of hysterectomy | |||
| Total vaginal hysterectomy (referent) | 1 | — | — |
| Laparotomy a | 3.74 | 2.26–6.22 | < .001 |
| Laparoscopic incisions b | 1.45 | 0.83–2.56 | .20 |
| Operative time >75th percentile duration | 1.84 | 1.40–2.44 | < .001 |
| American Society of Anesthesiologists class ≥3 | 1.79 | 1.31–2.43 | < .001 |
| Body mass index, kg/m 2 | |||
| <30 (referent) | 1 | — | — |
| ≥30 and <40 | 1.31 | 0.94–1.81 | .11 |
| ≥40 | 2.65 | 1.85–3.80 | < .001 |
| Diabetes mellitus | 1.54 | 1.06–2.24 | .02 |
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 ).
| Variable | Surgical site infection | P value | |
|---|---|---|---|
| Deep/organ-space (n = 154) | No deep/organ-space (n = 13,668) | ||
| Age, n (%) | 1.0 | ||
| <80 y | 152 (98.7) | 13,444 (98.4) | |
| ≥80 y | 2 (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/m 2 | 68 (44.2) | 7608 (55.7) | |
| ≥30 and <40 kg/m 2 | 50 (32.5) | 4588 (33.6) | |
| ≥40 kg/m 2 | 36 (23.4) | 1472 (10.8) | |
| Ascites, n (%) | 4 (2.6) | 106 (0.8) | .04 |
| Unintentional weight loss, n (%) a | 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 b | 17.8 ± 4.6 | 17.3 ± 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-Clean | 0 | 33 (0.2) | |
| 2-Clean/contaminated | 150 (97.4) | 13,508 (98.8) | |
| 3-Contaminated | 3 (2.0) | 94 (0.7) | |
| 4-Dirty | 1 (0.7) | 33 (0.2) | |
a Loss of ≥10% of body weight in the previous 6 months not because of exercise or dieting
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.
| Variable | Adjusted odds ratio | 95% CI | P value |
|---|---|---|---|
| American Society of Anesthesiologists class ≥3 | 1.81 | 1.25–2.62 | < .01 |
| Current smoker | 1.99 | 1.40–2.83 | < .001 |
| History of cerebrovascular accident with neurologic deficit | 4.41 | 1.54–12.65 | < .01 |
| Preoperative anemia (hematocrit, <36%) | 1.72 | 1.21–2.43 | < .01 |
| Body mass index, kg/m 2 | |||
| <30 (referent) | 1 | — | — |
| ≥30 and <40 | 1.19 | 0.82–1.74 | .36 |
| ≥40 | 2.23 | 1.43–3.49 | < .001 |
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 ).
| Variable | Urinary tract infection (n = 402) | No urinary tract infection (n = 13,420) | P value |
|---|---|---|---|
| Age, n (%) | .16 | ||
| <80 y | 392 (97.5) | 13,204 (98.4%) | |
| ≥80 y | 10 (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/m 2 | 215 (53.5) | 7461 (55.6) | |
| ≥30 and <40 kg/m 2 | 147 (36.6) | 4491 (33.5) | |
| ≥40 kg/m 2 | 40 (10.0) | 1468 (10.9) | |
| Ascites, n (%) | 2 (0.5) | 108 (0.8) | .77 |
| Unintentional weight loss, n (%) a | 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 b | 17.1 ± 3.8 | 17.3 ± 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-Clean | 0 | 33 (0.3) | |
| 2-Clean/contaminated | 398 (99.0) | 13,260 (98.8) | |
| 3-Contaminated | 3 (0.8) | 94 (0.7) | |
| 4-Dirty | 1 (0.3) | 33 (0.3) |
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