Abstract
Introduction:
Surgical site infection (SSI) is a substantial cause of peri-operative morbidity among patients undergoing radical cystectomy (RC). The purpose of this study was to identify the risk factors of SSI after RC and to classify and characterize treatment of SSIs.
Methods:
We retrospectively analyzed peri-operative characteristics and SSI, for patients undergoing RC from 2007 to 2022. Patients were stratified by SSI versus no SSI and differences were assessed. Uni-variable/multi-variable logistic regression analyses were performed to identify factors associated with SSI. SSIs were categorized by the Centers for Disease Control and Prevention (CDC) type: Superficial incisional, deep incisional, and organ/space confined.
Results:
Three hundred and ninety-eight patients had RC, 279 open, and 119 robotic; 78 (19.6%) developed SSI. Cohorts were similar demographically. Length of stay (LOS) was longer in the SSI cohort (8.8 d versus 12.4 d, p < 0.001), and body mass index (BMI) was greater in patients with SSI (24.34 vs. 25.39, p = 0.0003). On uni-variable analysis, age, gender, Charlson Comorbidity Index, diabetes mellitus, diversion, odds ratio (OR) time, blood loss, and open versus robotic technique were not substantial SSI predictors. BMI was an independent risk factor for SSI on both uni-variable (OR: 1.07, 95% confidence interval [CI]: 1.018–1.115, p = 0.0061) and multi-variable analysis (OR: 1.06, 95% CI: 1.009–1.109, p = 0.02) for 10 (12.8%) and 24 (30.8%) superficial and deep-incisional SSIs, respectively. Superficial wound SSI was treated conservatively with 60% receiving antibiotic agents and no procedural intervention. Deep SSIs received antibiotic agents and 50% required surgical intervention. There were 44 (56.4%) organ/space SSIs, and the most common treatment was antibiotic agents (100%) and IR drain placement (30, 68.2%).
Conclusion:
In patients undergoing RC, BMI was an independent risk factor for SSI. Type of the surgical procedure, robotic versus open, was not predictive of SSI. LOS was longer for patients with SSI. SSI was managed differently depending on CDC classification.
Keywords: bladder cancer, open cystectomy, robotic cystectomy, surgical site infection
Bladder cancer is the 10th most common cancer diagnosed globally. An estimated 83,000 patients will be diagnosed with bladder cancer in the United States alone, with an estimated 16,000 bladder cancer-related deaths in 2023.1 Radical cystectomy (RC) is commonly used to treat recurrent non-muscle invasive bladder cancer and muscle invasive bladder cancer. However, RC is associated with a high peri-operative complication rate, with almost one-third of patients experiencing a post-operative complication.2 One such complication, surgical site infection (SSI), is a substantial cause of morbidity, increased healthcare cost, and extended hospital stay.3 SSIs vary in characteristics and associated treatments, ranging from observation to surgical or interventional procedures.4 However, there is a paucity in literature discussing the risk factors and management of SSI after RC.
The purpose of this study was to identify the risk factors of SSI after RC and to classify and characterize treatment of SSIs. We used a comprehensive retrospective institutional database that covers RCs over a 16-year period.
Patients and Methods
Patient selection
Institutional review board approval was obtained. A retrospective chart review of the electronic medical record and paper charts was performed to identify patients with Current Procedural Terminology (CPT) coding for RC with urinary diversion and pelvic lymph node dissection between 2007 and 2022. Surgical procedures were performed by seven attending urologists across two institutions. The decision on open versus robot-assisted surgical approach and continent versus incontinent urinary diversion was based on surgeon discretion and patient preference. All patients were given peri-operative IV antibiotic agents. All patients were cleared for operation from an anesthesia and medicine perspective, with blood glucose and routine labs checked before the surgical procedure. All living patients were followed for at least 90 days.
Variables
Data regarding patient characteristics were obtained in the form of age, gender, Charlson comorbidity status, body mass index (BMI), and history of diabetes mellitus. Peri-operative data were obtained in the form of surgical approach, surgeon, date of operation, operative time, estimated blood loss, type of urinary diversion, number of blood units transfused, and length of stay (LOS). Enhanced recovery after surgery (ERAS) pathway was implemented for patients’ post-operative care starting in 2015.
SSIs were classified based on the Centers for Disease Control and Prevention (CDC) classification system (Fig. 1). The first classification is superficial incisional, which follows the general criteria of involving the skin or subcutaneous tissue only and has at least one of the following: Purulent drainage or organisms identified from a culture or dehiscence plus at least one sign of symptom such as swelling, pain, erythema, or heat. The second classification or deep incisional SSI involves the deep soft tissues (fascial and muscle layers). Patients must have at least one of the following: Purulent drainage, culture documented organisms, or abscess or other evidence of infection involving the deep incision or dehiscence plus localized symptoms and/or fever. The final category is organ/space SSI, which involves any part of the body deeper than the fascial/muscle layer that is opened or manipulated during the operative procedure. Patients must have one of the following: purulent drainage from a drain placed into the space, organisms identified from culture or abscess, or other infection from the organ space on examination or imaging. They must also be from a specific site, which includes urinary system/intra-abdominal infections.5
FIG. 1.
CDC wound classification. CDC = Centers for Disease Control and Prevention.
Outcome measures
The primary outcome was post-operative SSI based on demographic and operation risk factors. Secondary outcomes were differences in management of SSIs by classification.
Statistical analysis
Patients were stratified into two cohorts based on presence or absence of SSI. Differences between the two cohorts were assessed using Student’s t-test for continuous variables and Pearson’s Chi-square analysis for categorical variables. For non-parametric variables, a Mann–Whitney U test was performed. Uni-variable and multi-variable logistic regression was performed to identify predictors of SSI. P-values were two sided and considered statistically significant if <0.05. Statistical analysis was performed using StataMP 17 (StataCorp, College Station, TX) and Excel (Redmond, WA).
Results
A total of 398 patients were identified, who underwent an RC with urinary diversion between 2007 and 2022. One hundred and nineteen (29.9%) patients had a robotic approach, and 279 (70.1%) patients had an open approach. Two hundred and eighty-seven (72.1%) patients had an incontinent diversion (conduit). Urinary diversions were performed through an open extra-corporeal approach. There was no substantial increase in the percentage of cases performed robotically overtime. The surgical procedures were performed by multiple urologists at two teaching hospitals within the same health institution. A total of 15 patients died within the first 90 days (3.8%).
When stratified, a total of 78 (19.6%) patients had an SSI (Table 1). There was no substantial trend in SSI rates overtime (p > 0.05). Table 1 describes the baseline characteristics of the patients included. Specifically, the two cohorts were similar in terms of patients’ characteristics such as age (p = 0.90), gender (p = 0.93), history of diabetes mellitus (p = 0.74), and Charlson Comorbidity Index (CCI) (p = 1). Between the two cohorts, the patients had a similar distribution of continence versus incontinent urinary diversions (p = 0.964), similar operative times (p = 0.43), estimated blood loss (p = 0.56), need for blood transfusions (p = 0.31), blood transfusion units (p = 0.22), and robotic technique (p = 0.88). On uni-variable analysis, age, gender, CCI, diabetes mellitus, type of diversion, odds ratio (OR) time, blood loss, and open versus robotic technique were not substantial predictors of SSI.
Table 1.
Baseline Characteristics of Patients Who Developed SSI Compared with Those Who Did Not
| Demographics | ||||
|---|---|---|---|---|
| All patients | No SSI | SSI | p | |
| Number | 398 | 320 (80.4%) | 78 (19.6%) | — |
| Age (years) | 69.0 ± 9.96 70(63–77) | 69.1 ± 9.9 | 68.3 ± 10.4 | 0.901 |
| Male gender (%) | 318 (79.9%) | 256 (80.0%) | 62 (79.5%) | 0.930 |
| History of diabetes mellitus (%) | 76 (19.1%) | 60 (18.8%) | 16 (20.5%) | 0.742 |
| BMI (kg/m2) | 24.52 ± 3.1725 (22.4–26.5) | 24.34 ± 3.1125 (22.4–26.4) | 25.39 ± 3.3525.7 (23.1–27.1) | 0.0003 |
| BMI ≥ 30 | 118 (26.6%) | 84 (26.3%) | 34 (43.6%) | 0.0026 |
| Urinary diversion | 0.964 | |||
| Incontinent | 287 (72.1%) | 229 (71.6%) | 50 (74.4%) | |
| Continent | 111 (27.9%) | 91 (28.4%) | 20 (25.6%) | |
| Charlson Comorbidity Index | 4.5 ± 2.44 (2–6) | 4.5 ± 2.44 (2–6) | 4.5 ± 2.44 (2–6) | 1 |
| Operative time (mins) | 408.5 ± 146.8 409 (289–509) | 404.9 ± 146.7407 (287.5–495) | 423 ± 147.9415 (302–535) | 0.430 |
| Estimated blood loss (mL) | 710.8 ± 516.8600 (400–800) | 703.2 ± 531600 (400–800) | 741.7 ± 455.7575 (500–1,000) | 0.555 |
| Length of stay (days) | 9.5 ± 6.58 (6–10) | 8.8 ± 4.78 (6–9) | 12.4 ± 10.78 (7–14) | <0.001 |
| Blood transfusion required | 106 (26.6%) | 82 (25.6%) | 24 (30.8%) | 0.312 |
| Blood transfusion units | 0.62 ± 1.320 (0–1) | 0.60 ± 0.070 (0–1) | 0.69 ± 1.30 (0–1) | 0.224 |
| Robotic approach | 119 (29.9%) | 95 (29.7%) | 24 (30.8%) | 0.881 |
Mean ± SD, median (IQR: 25%−75%).
SSI = surgical site infection; BMI = body mass index; SD = standard deviation; IQR, interquartile range.
LOS was longer in the SSI cohort (8.8 d versus 12.4 d, p < 0.001). Pre-operative BMI was different between patients with SSI and patients with no SSI with larger average BMI in patients with SSI (24.34 vs. 25.39, p = 0.0003). Obesity, as defined by BMI ≥ 30, was more common among patients with SSI (26.3% vs. 43.6%, p = 0.0026). BMI was an independent risk factor for SSI on uni-variable analysis (OR: 1.07, 95% confidence interval [CI]: 1.018–1.115, p = 0.0061). A model for multi-variable logistic regression was created, which included age, gender, BMI, history of diabetes mellitus, CCI, operative duration, LOS, type of urinary diversion, blood loss, transfusion, and type of surgical approach. On multi-variable analysis, BMI remained a predictive risk factor for SSI (OR: 1.06, 95% CI: 1.009–1.109, p = 0.02).
Per the CDC classification, there were 10 (12.8%) superficial incisional, 24 (30.8%) deep incisional, and 44 (56.4%) organ or space confined SSIs (Table 2). There was no substantial difference in SSI between robotic and open approach when stratified by infection classification. The majority of patients presented with SSI after initial discharge (80.8%). For superficial infections, the median time to identification was 15 days and three (30%) patients required readmission. Around 40% were managed with conservative therapy only, whereas six (60%) required antibiotic agents. Dehiscence was observed in five (50%) patients. For deep incisional infection, the median time to identification was 13 days. All patients (24, 100%) either had identification of infection during primary admission or required readmission. All were treated with antibiotic agents (24, 100%) and 12 (50%) required surgical exploration. None was treated with interventional radiology placed drain. Nineteen (79%) had a wound dehiscence. Eight (33.3%) required a wound vac for healing. Organ or space SSI had a median identification time of 22.5 days. All (44, 100%) were either identified during primary surgical admission or required readmission and all required antibiotic agents. Treatment was primarily with drain placement (30, 68.2%). Three (6.8%) required surgical exploration, and only two (4.5%) had a wound dehiscence. Wound cultures varied by infection with no discernible predominant organism.
Table 2.
SSI Based on CDC Wound Classification
| SSI type | Superficial wound n = 10 (12.8%) |
Deep wound n = 24 (30.8%) |
Organ or space SSI n = 44 (56.4%) |
|---|---|---|---|
| Timing after (median) | 15 d | 13 d | 22.5 d |
| Readmission | 3 (30%) | 19 (79%) | 37 (84.1%) |
| During operation admission | 3 (30%) | 5 (21%) | 7 (15.9%) |
| Antibiotic agents | 6 (60%) | 24 (100%) | 44 (100%) |
| Drain | 0 | 0 | 30 (68.2%) |
| Surgery | 0 | 12 (50%) | 3 (6.8%) |
| Wound vac | 0 | 8 (33.3%) | 1 (2.3%) |
| Dehiscence | 5 (50%) | 19 (79%) | 2 (4.5%) |
| Wound culture |
Candida: 2 Viridans streptococci: 1 Other/mixed: 8 |
Pseudomonas: 3 Enterococcus: 2 Escherichia coli: 2 Bacteroides: 2 MRSA: 2 Viridans streptococci: 1 Other/mixed: 14 |
E. coli: 5 Candida: 4 Bacteroides: 3 MRSA: 2 Pseudomonas: 1 Klebsiella: 1 Other/mixed: 28 |
CDC = Centers for Disease Control and Prevention.
Discussion
In a retrospective analysis at a large academic hospital system, patients who experienced an SSI post-operatively had greater BMIs and longer hospital stays. BMI was a predictive risk factor in a multi-variable analysis. Type of surgical intervention, whether robotic or open, was not related to the development of SSI. LOS was longer in patients with SSI; however, it is unclear whether the presence of SSI increased LOS or if LOS was a cause of SSI. Other demographic factors, including age, gender, diabetes mellitus, CCI, blood loss, transfusions, operative duration, and type of urinary diversion, were not predictive of SSI.
SSIs were managed differently based on classification. Classification of surgical incisions may aid in timely and appropriate treatment. Superficial incisional wounds were primarily treated conservatively with or without antibiotic agents. Superficial SSIs were the least commonly identified infection classification, which may be artificially low because of under-diagnosis/under-identification if patients did not have symptoms or dehiscence of wound.
Deep incisional wounds predominately required surgical exploration for incision and drainage and antibiotic agents. The majority of identified SSIs were open or space-confined infections, and the majority required drain placement and antibiotic agents. Timely consultation of interventional radiology for drain placement should be considered on presentation. Given no clear majority organism identified in surgical incisions, patients should be first treated with broad-spectrum microbials and should then be transitioned to culture-based antibiotic agent therapy.
Our overall SSI rate of 19.6% is comparable with the available literature with the rate of SSI at 20%–25%.6 Goldberg et al. investigated predictors of SSI in 405 patients treated exclusively by Open cystectomy. The rate of SSI was 23.7% with BMI, pre-operative ceftriaxone, and intensive care unit hospitalization increasing the risk of SSI.6 In an observational study, Takeyama et al. investigated SSI after Open cystectomy in 104 patients. The overall incidence of SSI was 33%, with MRSA (Methicillin-resistant Staphylococcus aureus) being the most isolated organism. Operative time was shown to be a substantial risk factor for SSI.7 The Robot-assisted radical cystectomy versus open radical cystectomy in patients with bladder cancer (RAZOR) trial was a randomized, open-label, non-inferiority phase 3 clinical trial comparing Robotic cystectomy with Open cystectomy. The study was powered to determine progression-free survival. Safety was assessed in the same population. Although not powered to determine significance, superficial and deep SSIs were more common in the Open cystectomy group compared with the Robotic cystectomy group (superficial SSI, 12% versus 7%, respectively, and deep SSI, 7% and 2%, respectively).8 Unlike our study, Kamei et al. determined that lower bleeding volume contributed to decreased SSI after RC. In a cohort of 231 patients, the incidence of SSI was substantially associated with greater blood loss with a cutoff of Estimated blood loss (EBL) for predicting SSI of 1630 cc. Within our cohort, the SSI rate of those with EBL >1,600 was lower than the overall (18.5% and 19.6%, respectively).
Obesity has been associated with SSI. The effect of elevated BMI and obesity on increased risk of SSI is multi-factorial. Patients with obesity have been shown to have poorer subcutaneous tissue oxygenation than normal weight patients, leading to wound hypoxia.9,10 Wound hypoxia impairs healing surgical incisions, which require a high metabolic demand and oxygenation. Furthermore, patients with elevated BMI have thicker layers of subcutaneous fat with greater risk of dead space formation upon wound closure.11 In a cohort of 387,919 patients undergoing surgical procedures in The Netherlands, there was a trend of increasing risk of SSI when BMI increased. The largest increase was observed in patients who were morbidly obese (BMI > 40).12 Winfield et al. analyzed the American College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP) database for patients who had abdominal operation and similarly found obesity to be an independent risk factor of SSI development (obesity OR = 1.757, p < 0.001).13 Specifically, to RC, Lenardis et al. analyzed the ACS-NSQIP database for 3,930 patients who underwent RC. Patients with BMI > 30 were more likely to have infectious complications when compared with patients with BMI 18.5–25 (OR: 1.59, 95% CI: 1.17–2.16).14
SSIs cause morbidity for patients, with risk for reoperation, longer hospital stays, longer recovery times, and more cosmetic outcomes. Furthermore, SSIs are a major financial loss to healthcare systems, with an estimated $3.3 billion burden in the United States.15 Therefore, the prevention of SSI is imperative. Siedelman et al. highlighted six general tactics for preventing SSI, including using clippers over razors for hair removal, decolonization with intranasal and skin antiseptic anti-staphylococcal agents, using chlorhexidine and alcohol-based skin preparation, maintaining normothermia with active warming during procedures, peri-operative glycemic control, and use of negative pressure wound therapy as needed.16 In addition, the CDC recommends the use of prophylactic antimicrobial agents when appropriate and administering increased fraction of inspired oxygen during operation and after extubation. Furthermore, transfusion of blood products should not be withheld to prevent SSI.17 In our institution, these preventative principles are followed. Recently, novel prevention tactics have been proposed for curtailing SSI. Zmora et al. investigated, in a phase 2 randomized clinical trial, the use of D-PLEX, an antibiotic agent-eluting polymer-lipid matrix to supply high local concentrations of doxycycline to prevent SSI in a cohort of 179 patients undergoing elective colorectal operation. There was a 64% relative risk reduction in the SSI rate in patients treated with D-PLEX compared with the standard of care alone (8% vs. 22%, respectively, p = 0.0115).18 In mouse models, targeting the gut microbiota with an orally delivered phosphate-rich polymer before operation has shown promising reductions in SSI.19 The Alexis wound retractor has also been proposed to curtail SSI after RC. In a retrospective analysis, Sidhu et al. compared rates of infection between RC using the Alexis and RC using a Bookwalter in a cohort of 237 patients. The SSI rate for the Alexis group was 3% compared with 11% in the Bookwalter cohort; however, the difference was not statistically significant.20 Prehabilitation before RC has been investigated for its efficacy on reducing infection rates and typically includes the utilization of pre-operative nutrition optimization and physical therapy/exercise for patients.21 Specialized immunonutrition shakes have been investigated for their efficacy in reducing SSI after RC. In a pilot RCT, Hamilton-Reeves et al. investigated the effects of immunonutrition on SSI after RC. In a cohort of 29 patients, those who received immunonutrition compared with normal nutritional supplements had a 39% reduction in SSI (p = 0.027).22 Given the substantial risk of elevated BMI and SSI in our cohort, our institution is currently providing immunonutrition to patients before RC in a pilot trial setting.
Our study classifies SSIs in patients who had RC and delineates characteristics and management based on infection classification. Strengths include the multi-variable analysis, control of confounders, and the moderate cohort size. Limitations of our study include the potential for additional confounders affecting SSI rate, cancer-specific factors, underdiagnosis of infections, and the retrospective nature of the study. In addition, the SSIs were classified at time of analysis to the CDC classifications based on chart review, imaging, and prior physical examination description. Randomized control trials are needed to validate the findings of our study.
Conclusion
In a retrospective study, bladder cancer patients with increased BMI had a greater risk of SSI after RC. There was no substantial difference in other factors, including blood loss, transfusion rate, operative time, or LOS. Patients with different classifications of SSI, including superficial and deep incisional and organ/space confined infections, presented and were managed differently. Further randomized control trials are needed to validate these results.
Acknowledgments
None.
Authors’ Contributions
Study concepts: S.D.L., A.U.C., K.L.I., J.F.J.-D., M.S.L., T.V.M., and D.G.H. Study design: S.D.L., A.U.C., J.F.J.-D., M.S.L., T.V.M., and D.G.H. Data acquisition: S.D.L., A.U.C., K.L.I., S.S., and D.G.H. Quality control of data and algorithms: S.D.L., A.U.C., K.L.I., J.F.J.-D., M.S.L., T.V.M., and D.G.H. Data analysis and interpretation: S.D.L., A.U.C., K.L.I., S.S., J.F.J.-D., M.S.L., T.V.M., and D.G.H. Statistical analysis: S.D.L., A.U.C., and S.N.R.
Funding Information
No funding or financial support was received for the research, authorship, and/or publication of this article.
Author Disclosure Statement
The authors declare no conflicts of interest.
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