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The Role of Bowel Preparation in Colorectal Surgery

Results of the 2012–2015 ACS-NSQIP Data

Klinger, Aaron L., MD*; Green, Heather, MS*; Monlezun, Dominique J., MD, PhD, MPH; Beck, David, MD*; Kann, Brian, MD*; Vargas, Herschel D., MD*; Whitlow, Charles, MD*; Margolin, David, MD*

doi: 10.1097/SLA.0000000000002568
ORIGINAL ARTICLES
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Objective: To analyze potential benefits with regards to infectious complications with combined use of mechanical bowel preparation (MBP) and ABP in elective colorectal resections.

Background: Despite recent literature suggesting that MBP does not reduce infection rate, it still is commonly used. The use of oral antibiotic bowel preparation (ABP) has been practiced for decades but its use is also controversial.

Methods: Patients undergoing elective colorectal resection in the 2012 to 2015 American College of Surgeons National Surgical Quality Improvement Program cohorts were selected. Doubly robust propensity score–adjusted multivariable regression was conducted for infectious and other postoperative complications.

Results: A total of 27,804 subjects were analyzed; 5471 (23.46%) received no preparation, 7617 (32.67%) received MBP only, 1374 (5.89%) received ABP only, and 8855 (37.98%) received both preparations. Compared to patients receiving no preparation, those receiving dual preparation had less surgical site infection (SSI) [odds ratio (OR) = 0.39, P < 0.001], organ space infection (OR = 0.56, P ≤ 0.001), wound dehiscence (OR = 0.43, P = 0.001), and anastomotic leak (OR = 0.53, P < 0.001). ABP alone compared to no prep resulted in significantly lower rates of surgical site infection (OR = 0.63, P = 0.001), organ space infection (OR = 0.59, P = 0.005), anastomotic leak (OR = 0.53, P = 0.002). MBP showed no significant benefit to infectious complications when used as monotherapy.

Conclusions: Combined MBP/ABP results in significantly lower rates of SSI, organ space infection, wound dehiscence, and anastomotic leak than no preparation and a lower rate of SSI than ABP alone. Combined bowel preparation significantly reduces the rates of infectious complications in colon and rectal procedures without increased risk of Clostridium difficile infection. For patients undergoing elective colon or rectal resection we recommend bowel preparation with both mechanical agents and oral antibiotics whenever feasible.

*Department of Colon and Rectal Surgery, Ochsner Medical Center, New Orleans, LA and Ochsner Clinic School, University of Queensland School of Medicine, Brisbane, Queensland, Australia

Department of Medicine, University of Texas Health Sciences Center, Houston, TX.

Reprints: David Margolin, MD, FACS, FASCRS, Department of Colon and Rectal Surgery, Ochsner Medical Center and Ochsner Clinic School, University of Queensland School of Medicine, 1514 Jefferson Highway, New Orleans, LA 70121. E-mail: damargolin@ochsner.org.

The American College of Surgeons National Surgical Quality Improvement Program and the hospitals participating in the ACS NSQIP are the source of the data used herein; they have not verified and are not responsible for the statistical validity of the data analysis or the conclusions derived by the authors.

The authors disclose no conflicts of interest.

Cleansing the bowel to limit the infectious complications of colorectal surgery is hardly a new concept. In fact, in 1887 Halsted noted that “the chief danger of infection of the peritoneal cavity is manifestly from the contents of the intestine.”1 Shortly after the discovery of penicillin, surgeons began using oral antibiotics in attempts to reduce intraluminal bacterial counts. This was usually used in conjunction with purgatives or bowel irrigation to reduce stool burden and further reduce the bacterial counts. At the time these methods were being developed mortality rates for colorectal surgery was as high as 10% to 12% with as many as 90% of survivors developing surgical site infections (SSIs).2 By the 1950s patients began to receive perioperative antibiotics and would often demand them regardless of their surgeon's recommendations.3 In 1972 Nichols et al4 introduced their protocol, still commonly used today, consisting of mechanical bowel preparation (MBP) and doses of neomycin and erythromycin which they found to reduce rates of SSI from 43% to 9%.

In recent years, the benefit of MBP has been called into question in various clinical trials.5–8 In a 2011 Cochrane review Güenaga et al9 analyzed more than 5800 colorectal surgery patients from 20 trials. They compared patients receiving MBP to patients receiving no preparation and found no significant difference between these groups in rates of anastomotic leakage or wound infection in colon or rectal resection. In 2015 Atkinson et al10 found ABP alone to result in fewer SSIs than no preparation and questioned whether combined bowel preparation is necessary. Others have questioned if antibiotic bowel preparation offers any benefit when systemic intravenous antibiotics have been provided.11,12 Furthermore, Wren et al13 found oral antibiotics to result in increased rates of Clostridium difficile infection.

The high rate of infections and other postoperative complications in colorectal surgery and the desire to reduce hospital costs has led many surgeons to follow “fast-track” or “enhanced recovery pathways” (ERPs). These pathways vary but typically consist of limited perioperative fasting with early postoperative feeding, careful intravenous fluid management, attempts to limit postoperative nausea, vomiting, and ileus, and early discharge planning. Although some authors suggest using MBP as part of an ERP,14–16 others insist a key component of enhanced recovery is avoidance of MBP. 17–20 In fact, recently published guidelines from the American Society of Colon and Rectal Surgeons and the Society of American Gastrointestinal and Endoscopic Surgeons recommend the use of combined MBP and ABP.21

Despite multisociety guidelines calling for the use of MBP and ABP in addition to IV antibiotic prophylaxis, the use of preparation remains controversial.22 The Society of American Gastrointestinal and Endoscopic Surgeons recognizes this controversy and suggest that for colonic resection, if MBP is to be used, ABP must also be used. They note a lack of data for elective rectal surgery and do not make any specific recommendations.23

Surveys of the American Society of Colon and Rectal Surgeons have shown a trend in recent years toward abandoning preoperative bowel preparation. A 1990 survey by Beck and Fazio24 found all respondents to use MBP and 87% to use oral antibiotics. Nichols created a similar survey in 1997 and again found 100% to use MBP and 88.5% using ABP plus IV antibiotics.25 A 2003 survey by Zmora et al26 found 99% of American Society of Colon and Rectal Surgeons (ASCRS) members to routinely use MBP and 75% to routinely use ABP, although only half thought ABP was essential. An ASCRS member survey by Markell et al27 in 2010 found that 76% of respondents used MBP routinely before elective colectomy but only 36% used ABP routinely. Most recently in a 2016 ASCRS survey Beck and McCoy (Current perioperative management of the colorectal surgery patient: an ASCRS survey. unpublished observation. 2017) found only 59% to always use MBP and 48% to always use ABP.

We hypothesize that there is a significant benefit with regards to infectious complications with combined use of mechanical and antibiotic preparation in elective colorectal resections without an increased incidence of C. difficile infection.

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METHODS

This study is a retrospective case-control study of the prospectively collected American College of Surgeons National Surgical Quality Improvement Program (ACS-NSQIP) Colectomy Targeted database from 2012 to 2015. Inclusion criteria were patients undergoing elective colorectal resection without concomitant stoma creation from 2012 to 2015 (CPT codes 44140, 44145, 44160, 44204, 44205, and 44207). Exclusion criteria included patients with known infection or sepsis at the time of operation, American Society of Anesthesiologist (ASA) Class V patients, emergency operations, and obstructive cancers. Further exclusions were made for those without antibiotic or MBP data and those with no recorded values for postoperative incisional SSI. NSQIP differentiates between superficial and deep SSI; for the purpose of this study SSI refers to any superficial or deep SSI.

The primary endpoints were a −3% independent likelihood postoperative outcomes. Sample size calculations indicated that 1873 subjects were required to assess these endpoints with 80% power and 5% error (using postestimation predictive margins for 2 sample proportions test after fully adjusted regression models). Descriptive statistics were performed for the entire sample. Bivariable analysis based on overall SSI (deep and superficial) was conducted with independent sample t test comparing means and Wilcoxon rank sum tests comparing medians for continuous variables as appropriate, and Pearson chi square test or Fisher exact test comparing proportions for categorical variables as appropriate. To provide causal inference and so approximate results from a randomized clinical trial of similar endpoint and patient sample, doubly robust propensity score adjusted multivariable logistic regression was then conducted for the study endpoints with adjustments for patient demographic, disease, and risk stratification variables significant in bivariable analysis or previously documented in the literature for being clinically and/or statistically meaningful. This propensity score-adjusted regression was augmented with a modified forward and backward stepwise regression that assessed model inclusion of every variable in the bivariable analysis.

Following the final model recommended by both stepwise algorithms, variables were added or deleted based upon prior published research, clinical intuition, and statistical model fit. The propensity score was constructed based on the likelihood of receiving both mechanical and antibiotic bowel prep using statistically and/or clinically important variables from the bivariable analysis, and balance was verified based on the final number of blocks identified (7 total). A modified doubly robust propensity score method was used at this stage with variables for consideration in the propensity score from the bivariable analysis being also used in the final regression model for the study endpoints. Stratified analysis was then conducted for colon and rectal surgery patients separately. Predictive margins were calculated for the fully adjusted final regression model to investigate significant predictors. The final regression models were reviewed by an academic physician and academic biostatistician/data scientist to ensure support by substantive clinical and statistical theory and evidence. Correlation matrix and variance inflation factor were used to ensure no multicollinearity in the final models. Hosmer-Lemeshow goodness-of-fit test was also conducted to determine whether the final models fit the data well. All regression estimates with 95% confidence intervals are reported as fully adjusted results. Statistical significance was set at 2-tailed P value <0.05. All analyses were conducted using STATA 14.2 (STATACorp, College Station, TX).

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RESULTS

There were 64,357 patients with bowel preparation data and 27,804 subjects met the study criteria. Of these 5471 (23.46%) received no preparation, 7617 (32.67%) received MBP only, 1374 (5.89%) received ABP only, and 8855 (37.98%) received dual (MBP + ABP) preparation. The demographics and patient comorbidities are shown in Table 1. On average, those patients who had a SSI were younger, had a higher BMI, were more likely active smokers, and had a higher ASA class. In addition, patients with SSI were more likely to have diabetes, ascites, hypertension, disseminated cancer, and to be on chronic steroid treatment.

TABLE 1

TABLE 1

In modified forward and backward stepwise regression augmenting a doubly robust propensity score-adjusted multivariable regression using patients receiving no bowel preparation as the reference, those receiving dual preparation were less likely to develop a SSI [odds ratio (OR) = 0.39, P < 0.001], organ space infection (OR = 0.56, P < 0.001), anastomotic leak (OR = 0.53, P < 0.001), or wound dehiscence (OR = 0.43, P = 0.001). Compared to unprepped patients, those treated with dual preparation were also less likely to develop C. difficile infection (OR = 0.53, P = 0.035). Combined preparation patients were also less likely to have an unplanned return to the operating room (OR = 0.70, P < 0.001) and had a shorter length of stay in days (β = −0.66, P < 0.001) (Table 2).

TABLE 2

TABLE 2

Oral antibiotic preparation alone was also compared to no preparation. Patients receiving ABP had lower odds of SSI (OR = 0.63, P = 0.001), organ space infection (OR = 0.59, P = 0.005), and anastomotic leak compared to those receiving no preparation. ABP patients also had a shorter length of stay in days than unprepped patients (β = −0.43, P = 0.004). ABP had no statistically significant differences compared to no preparation in frequency of C. difficile, wound dehiscence, or unplanned reoperation. Mechanical preparation did not show any significant difference in primary outcomes compared to no preparation (Table 2). Individual ABP and MBP were then compared to combined preparation. Antibiotic preparation and MBP alone resulted in more SSI (OR = 1.61, P = 0.002) than combined MBP/ABP and there was a higher leak rate when comparing MBP to dual prep (OR = 1.60, P < 0.001) (Table 3).

TABLE 3

TABLE 3

Stratified analysis for colon surgery alone was then performed. Compared to no preparation, MBP/ABP patients again had less SSI (OR = 0.35, P < 0.001), organ space infection (OR = 0.56, P < 0.001), anastomotic leak (OR = 0.33, P = 0.004), wound dehiscence (OR = 0.54, P = 0.026), C. difficile (OR = 0.60, P < 0.001), and unplanned reoperation (OR = 0.70, P < 0.001). Likewise ABP alone patients had fewer SSIs (OR = 0.35, P < 0.001), organ space infections (OR = 0.59, P = 0.020), and C. difficile infections (OR = 0.62, P = 0.047) but did not show a difference in anastomotic leak rates, wound dehiscence, or unplanned reoperation (Table 4). Compared to no preparation, dual prep (β = −0.85, P < 0.001), ABP (β = −0.46, P = 0.011), and MBP (β = −0.26, P = 0.013) all were associated with reduced hospital length of stay.

TABLE 4

TABLE 4

When rectal resections were evaluated independently, MBP/ABP compared to no preparation once again showed lower odds of SSI (OR = 0.49, P < 0.001), organ space infection (OR = 0.53, P < 0.001), wound dehiscence (OR = 0.24, P = 0.005), C. difficile (OR = 0.39, P < 0.001), and unexpected reoperation (OR = 0.68, P = 0.028). There were no significant differences in rates of anastomotic leak however. Outcomes for antibiotic preparation alone in rectal resection was no better than no preparation except for in rates of C. difficile (OR = 0.34, P = 0.007) (Table 5). Dual preparation resulted in lower odds of reoperation (OR = 0.68, P = 0.028), but there were no significant differences in length of stay.

TABLE 5

TABLE 5

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DISCUSSION

Our data show that compared to no preparation combined mechanical and oral antibiotic bowel preparation before colon or rectal surgery is associated with reduced odds of SSI, organ space infection, anastomotic leak, wound dehiscence, and C. difficile colitis and reduced length of stay. Likewise, when compared to either mechanical bowel prep or antibiotic bowel prep alone combined prep is associated with reduced odds of SSI.

Here we provide strong evidence that combined bowel preparation works to decrease infectious complications. Although we use powerful statistical methods in this study, a randomized controlled study would offer stronger evidence and is lacking. This study has several key strengths. It is the largest known multiyear and multisite analysis of postoperative infection and complications. It compares not only dual preparation to no preparation but also dual preparation to MBP and ABP alone. We also provide stratified analysis for colon and rectal patients, and use propensity score analysis and forward and backward regression to produce optimal final regression models. Although causative relationships between bowel preparation techniques and study endpoints are optimally tested using a randomized trial design, this study's use of such a large dataset with such advanced statistical techniques provides the closest approximation to randomized results given the latest statistical best practices. Furthermore ACS-NSQIP data are collected by trained specialists from patients treated by surgeons from multiple institutions and practice types resulting in results that are germane to all practices. To provide true causal evidence however, a randomized controlled trial would have to be performed.

The limitations of this study are important and should not be ignored. ACS-NSQIP follows patients for 30 days and any complication beyond this period will not be captured. Furthermore, although ACS-NSQIP measures many important variables, these data can be lacking for some patients and it does not record all measures. Importantly, the database does not record usage of preoperative intravenous antibiotic prophylaxis. Analysis of the Surgical Care Improvement Project suggest compliance with appropriate preoperative antibiotics is >90%.28,29 Although this treatment has become standard of care, one cannot assume that all patients received systemic prophylaxis, that they received appropriate antibiotics, that antibiotics were given at the appropriate time, or that repeat antibiotic doses were given when indicated. Likewise many patients were excluded from analysis because of missing data. We cannot assume that these patients were otherwise the same as those patients included in the study. There is also not a standardized bowel preparation protocol for this database and there is room for variation in what preparation was provided. We do know that incomplete preparation and enemas or suppositories were counted as “no mechanical preparation.” As a retrospective study, room exists for selection bias between prepped and unprepped patients. Although propensity matching theoretically controls for this potential bias, it is always possible that unmeasured factors contributed to the observed outcomes. Lastly, although we included a variety of commonly performed colorectal procedures (by CPT code), we cannot extend our findings to patients that received a diverting stoma or to other procedures not included in our analysis.

MBP before colorectal surgery, practiced for decades, was previously thought of as surgical dogma. The benefits provided by MBP were first challenged by Hughes in 1972. He reviewed his own results and compared 46 patients who received some form of mechanical preparation (no standardization) to 51 who received no preparation. He found a 15% infection rate in the prepared group and a 19% infection rate in the unprepared group. He noted that despite mechanical preparation bowel was often found to be loaded with stool intraoperatively. Based on this review he concluded that “vigorous mechanical preparation is not necessary.”30

The value of MBP came under further scrutiny in the late 1980s and 1990s when various studies failed to find any benefit to the use of MBP alone.31–34 The first randomized controlled study of MBP was performed by Brownson et al35 in 1992. They compared 86 patients receiving MBP to 93 receiving no preparation. They found no improvement in rates of wound infection, intra-abdominal infection, or anastomotic leak with MBP use. A 2003 Cochrane review by Güenaga et al,9,36–38 updated in 2005, 2009, and again in 2011 analyzed 20 studies on MBP in colorectal surgery. This review found no significant difference between surgical outcomes on prepped versus unprepped bowel and even suggested that MBP may be dangerous. A 2010 study by Eskicioglu et al39 reviewed 14 randomized controlled trials and 8 meta-analyses. She concluded, based on these studies, that MBP should be omitted prior to elective open colectomy, a statement officially endorsed by the Canadian Society of Colon and Rectal Surgeons. More recently, Atkinson et al10 found oral antibiotics without mechanical preparation to result in decreased rates of SSI compared to no preparation suggesting that it may be possible to omit MBP.

Others have challenged the benefit offered by oral antibiotic preparation, especially with preoperative systemic antibiotic administration becoming standard of care.11,12 The use of preoperative oral antibiotics has also been linked to increased rates of C. difficile colitis.13

Englesbe et al's40 analysis of the effects of bowel preparation on 370 paired colorectal cases in Michigan found dual preparation to reduce SSI and organ space infection compared to mechanical preparation alone with no significant differences in C. difficile infection. A follow-up study of the Michigan cohort by Kim et al evaluated dual preparation to no preparation for 957 paired cases. This too showed dual preparation to have reduced incidences of infectious complications as well as a decrease in C. difficile.41 Importantly, neither study evaluated rectal resection or the effects of ABP given without MBP.

Scarborough42 and Kiran43 in 2 separate studies evaluated the effects of bowel preparation using the 2012 ACS-NSQIP colon targeted database. Kiran et al found dual preparation to result in lower rates of SSIs and anastomotic leak and postoperative ileus. This study included patients with diverting stomas which have the potential to account for reduction in infectious complications and anastomotic leak rates. Furthermore, ABP alone was not evaluated.

Scarborough compared ABP, MBP, dual preparation, and no preparation. He found dual preparation to result in fewer SSIs, leaks, and readmissions than no preparation but found no significant benefit to MBP or ABP alone. Neither study evaluated Clostridium rates as this outcome was not included in the 2012 ACS-NSQIP database.

Multiple studies during the past 70 years have shown benefit to operating on mechanically cleared and antibiotic treated bowel. These benefits have been questioned more recently, however, and multiple studies dispute previously shown advantages. This camp points toward large cohort studies that find no advantage to MBP alone and question the role of oral antibiotics in an era where the vast majority of patients receive systemic intravenous antibiotics preoperatively. Furthermore, potential complications of bowel preparation including Clostridium infection have been noted. Despite this, preoperative bowel preparation remains popular but not universal in elective colorectal resection.

We show that while MBP alone does not offer significant advantages over no bowel preparation, ABP needs MBP to function properly. Furthermore, not only do bowel preparations not increase the rate of postoperative C. difficile colitis, combined ABP/MBP actually results in fewer C. difficile infections. Given the strength of our data and statistical methods, we are confident in recommending combined bowel preparation, when possible, for every colorectal resection.

It is clear that combined MBP/ABP results in lower rates of infectious complications in elective colon and rectal surgery. It is still unknown what the ideal mechanical and oral antibiotic agents are. The most commonly used mechanical preparations consist of polyethylene glycol or sodium phosphate, both osmotic cathartics although other drugs exist and are used. The best studied antibiotic protocol is the Nichols/Condon neomycin and erythromycin preparation, as described in 1972 or modified to substitute metronidazole for erythromycin but a variety of other oral antibiotic preparations have been studied over the past 70 years.2,44

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CONCLUSIONS

Combined MBP and oral antibiotic bowel preparation significantly reduces infectious complications, including C. difficile colitis, after elective colon and rectum resections. MBP alone does not reduce infectious outcomes and oral antibiotics are not fully effective without a purged bowel. Combined preparation should be used before every elective colorectal resection unless otherwise contraindicated.

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Keywords:

bowel preparation; antibiotic preparation; colorectal surgery; National Surgical Quality Improvement Program; surgical site infection

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