- Email: [email protected]
Modern Elective Laparoscopic Cholecystectomy Carries Extremely Low Postoperative Infection Risk
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Modern Elective Laparoscopic Cholecystectomy Carries Extremely Low Postoperative Infection Risk Sora Ely, MD,a,b,* Kara A. Rothenberg, MD,a,b Genna Beattie, MD,a,b Rebecca C. Gologorsky, MD,a,b Michelle R. Huyser, MD,a,b and Ching-Kuo Chang, MDb a b
UCSF East Bay Surgery, Oakland, California Department of Surgery, Kaiser Permanente e Oakland Medical Center, Oakland, California
article info
abstract
Article history:
Background: The studies that established historical rates of surgical infection after chole-
Received 1 May 2019
cystectomy predate the modern era of laparoscopy and routine prophylactic antibiotics.
Received in revised form
Newer studies have reported a much lower incidence of infections in “low-risk” elective,
31 August 2019
outpatient, laparoscopic cholecystectomies. We investigated the current rate of post-
Accepted 18 September 2019
operative infections in these cases within a large, U.S. database.
Available online xxx
Methods: We retrospectively reviewed elective laparoscopic cholecystectomies from the 2016-2017 American College of Surgeons National Surgical Quality Improvement Program
Keywords:
database. Our primary outcome was postoperative surgical site infection; secondary was
Elective laparoscopic
Clostridium difficile infection. Logistic models evaluated the associations of patient and
cholecystectomy
operation characteristics with these outcomes.
Surgical site infection
Results: Surgical infection occurred in 1.0% of cases (293/30,579). C difficile infection occurred
Postoperative infection
in 0.1% (31 cases). In our adjusted multivariable models, other/unknown race/ethnicity,
Clostridium difficile colitis
diabetes, hypertension, smoking, American Society of Anesthesiologists >2, operative minutes, and wound class 4 were associated with a significantly higher odds of surgical infection; no covariates were significantly associated with C difficile infection. Conclusions: In the setting of modern U.S. surgical practice, the incidence of infection after elective laparoscopic cholecystectomy is very low, on par with clean cases. Our study identified several patient characteristics that were strongly associated with surgical infection. Many of these are not included as risk factors in current guidelines for antibiotic prophylaxis and may help to identify those at higher risk for this rare complication. ª 2019 Elsevier Inc. All rights reserved.
Introduction The Surgical Care Improvement Project (SCIP) introduced prophylactic, preincision antibiotic administration as a measure to reduce surgical site infection in 2005 and subsequently
modified this to a selective recommendation based on the procedure and wound classification.1 Given that the biliary tract is technically entered during transection of the cystic duct, cholecystectomy is classically considered to have a minimum wound classification of “clean-contaminated”
* Corresponding author. Department of Surgery, 1411 E 31st Street, QIC#22134, Oakland, CA 94602. Tel.: þ1 480 420 7672; fax: þ1 480 264 0266. E-mail address: [email protected] (S. Ely). 0022-4804/$ e see front matter ª 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jss.2019.09.038
2
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
(class 2),2 making this SCIP quality measure applicable to the procedure. In open cholecystectomies, the practice of antibiotic prophylaxis has been supported by studies showing decreases in infection rates since its adoption.3 However, since the advent and proliferation of laparoscopy, newer studies have shown that laparoscopic cholecystectomies are associated with a lower incidence of wound infection than are open. Reported wound infection rates among open cholecystectomy cases range from 1.8% to 7.9%,4,5 on par with the expected rate of 3%-11% for clean-contaminated cases6; by contrast, wound infection rates among laparoscopic cholecystectomy cases in comparative studies are consistently half or less of those for open cases and have been reported as low as 0.5%.7-9 These rates of 0.5% to 1.5%7,10,11 are comparable to the expected 1%-5% infection rate for “clean” (class 1) cases.6 These provocative data, combined with increasing general concern about antibiotic stewardship and antibioticassociated infections such as Clostridium difficile colitis, led surgeons to question the necessity of antibiotic prophylaxis for laparoscopic cholecystectomy cases. A number of studies have investigated the rates of infection and utility of routine prophylactic antibiotics in laparoscopic cholecystectomies over the last 2 decades. Though their conclusions have been heterogeneous, these studies have consistently identified “low-risk” cholecystectomy cases as those that are performed laparoscopically on an elective, outpatient basis. Although contemporary reports have suggested a much lower incidence of surgical infection in these low-risk (outpatient, elective) laparoscopic cholecystectomy cases, none of these studies have evaluated U.S. populations. We used a large, national database to investigate the incidence of surgical or C difficile infection after elective laparoscopic cholecystectomy in the modern American surgery setting, and the factors associated with either occurrence.
Methods We retrospectively reviewed adult elective, outpatient laparoscopic cholecystectomy cases from the 2016-2017 American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) Participant Use Files. Laparoscopic cholecystectomies were identified by Current Procedural Terminology code 47,562 “laparoscopy, surgical; cholecystectomy.” Related Current Procedural Terminology codes 47,563 and 47,564, which add “with cholangiography” and “with exploration of common duct,” respectively, were not included. These additional procedures were felt not to be representative of routine elective cases, and the more extensive manipulation of the biliary system could have a potential confounding effect. Only elective (INOUT ¼ “Outpatient”), outpatient (ELECTSURG ¼ “Yes”) procedures were included. To obtain a realistic representation of risk among cases planned as elective and outpatient, we did not use postoperatively defined variables such as length of stay or wound class in our study criteria. Only cases with an American Society of Anesthesiologists (ASA) class of 5 (“moribund”) were excluded because this classification seemed incompatible with elective, outpatient status. We did not further restrict the study population, recognizing that this could result in the inclusion of some higher-risk cases, in favor
of producing a more conservative estimate of risk and maximizing the generalizability of our findings. Our primary outcome was occurrence of postoperative surgical site infection, defined as any superficial wound, deep wound, or organ space infection; our secondary outcome was occurrence of C difficile infection. Chi-squared test, Fisher’s exact test, and Student’s t test were used to evaluate the associations between patient and operative characteristics and postoperative infections. Multiple logistic regression (with surgical infection and C difficile infection modeled separately) was then used to further characterize the associations between the covariates and our outcomes of interest. A threshold of P < 0.05 was set for statistical significance. All statistical tests were performed using Stata statistical software, version 15 (StataCorp LP, College Station, TX). Because this study used publicly available, deidentified data and did not impact patient care, it was not required to undergo IRB review.
Results A total of 30,579 elective laparoscopic cholecystectomy cases met study criteria. Our study population demographics (Table 1) were as expected for routine cholecystectomies, with a mean age of 48.6 y, a 3:1 female predominance, and a majority being obese (52.6%). Mean operative time was just under an hour (56.9 min), though with considerable variability (standard deviation 32.1 min). Wound class was most frequently identified as 2 (clean-contaminated), but it is interesting to note the small proportion of cases that were classified erroneously as 1 (clean). Postoperative surgical site infection occurred in 293 cases, or 1%; C difficile infection occurred in 31 cases, or 0.1% (Table 2). Wound infections were predominantly superficial (46.2%). C difficile infections occurred in the absence of a surgical infection in most cases (90.0%). Only 3 patients had occurrences of both infections, representing 0.01% of the total study population, 1% of the patients with surgical infection, or 9.7% of the patients with C difficile infection. The proportional occurrence of surgical infections among cases with wound classes 1-3 was low and markedly higher with wound class 4. Within each wound class (1-4), the percentages of patients with surgical infections were, respectively, 1.0%, 0.9%, 1.4%, and 4.3%. Most of the demographic characteristics, comorbidities, and operative factors investigated as covariates were found to be significantly associated with surgical infection, and a few with C difficile infection (Table 3). Of the many characteristics associated with surgical infection, age and operative minutes (P < 0.00001), followed by race/ethnicity, diabetes, hypertension, ASA class, and wound class (P < 0.0001), were highly statistically significant. Only age, chronic obstructive pulmonary disease, and steroids were significantly associated with C difficile infection. In our multivariable models, several factors were independently associated with higher odds of surgical infection (Table 4), all with clinically relevant OR of 1.5 except operative time, which was calculated per 1 min. The greatest increases in surgical infection odds were seen with ASA of 3 (2.34, 95% CI: 1.22, 4.52), ASA of 4 (4.48, 95% CI: 1.92, 10.5), and
3
ely et al low infection risk in elective lap chole
Table 1 e Patient and case characteristics of 2016-2017 NSQIP elective laparoscopic cholecystectomies. Characteristic, n (%) Age, m(s)
Study population (n ¼ 30,579) 48.6 (16.5)
Sex Female Male
21.0
8051 (26.3)
Organ space
98
33.1
C. difficile infection
31
0.1
19,624 (64.2)
Hispanic
3473 (11.4)
Other/unknown
3805 (12.4) 31.6 (7.5)
BMI* 223 (0.7)
Normal
5254 (17.3)
Overweight
8932 (29.4) 15,959 (52.6)
Comorbidities
COPD Hypertension CHF
3617 (11.8) 698 (2.3) 9975 (32.6) 71 (0.2)
Renal failure
83 (0.3)
Ascites
10 (0.03)
Smoking
4931 (16.1)
Steroids
659 (2.2)
ASA class 1
3294 (10.8)
2
18,350 (60.0)
3
8541 (28.0)
4 Operative time, min m(s)
Superficial wound
46.2
981 (3.2)
Diabetes
1.0
61
2696 (8.8)
Obese
293 137
Black
Underweight
Surgical infection
Deep wound
Asian
BMI, m(s)
(N ¼ 30,579) n, %
Characteristic
22,528 (73.7)
Race White
Table 2 e Infection occurrences by type among NSQIP database elective laparoscopic cholecystectomy cases.
362 (1.2) 56.9 (32.1)
Wound class 1
1369 (4.5)
2
24,975 (81.7)
3
4026 (13.2)
4
209 (0.7)
BMI, body mass index; COPD, chronic obstructive pulmonary disease; CHF, congestive heart failure. * BMI classes reported in addition to the continuous variable’s mean and standard deviation to better illustrate the distribution in the study cohort; only the continuous variable was used in statistical analyses.
wound class of 4 (2.59, 95% CI: 1.06, 6.35). Meanwhile, none of the covariates were independently associated with higher odds of C difficile colitis in our multiple regression analysis.
Discussion Postoperative occurrences of surgical or C difficile infections were overall very rare among elective laparoscopic
cholecystectomy cases. Our 1% rate of surgical site infection confirms the trend suggested in prior literature that currentpractice laparoscopic cholecystectomy has a much lower incidence of postoperative infection than historically associated with either open or laparoscopic cholecystectomy,4,5,7-9 on par with modern rates of most wound class 1 (“clean”) cases.6 Our study also demonstrates an exceedingly low 0.1% rate of C difficile infection. This rate is comparable to the rate of 0.41% after cholecystectomy from an analysis of 1999-2003 National Inpatient Sample data.11 This suggests that, at least in this population, the risk of C difficile infection has not increased meaningfully as a result of practice changes over the last 15-20 y. Nonetheless, its 0.1% incidence represents a rate of 10% of the frequency of surgical infection, and C difficile infection may carry a greater morbidity and mortality. Most C difficile infections occurred in the absence of a surgical site infection and thus likely in patients prescribed only prophylactic antibiotics. Our study is the first to show that the risk of infection after elective, outpatient cholecystectomy in the setting of contemporary American surgical practice is now extremely low. Although we cannot draw any conclusions about the causes for this decreased infection rate, there are a number of possible factors. Of note, SCIP was instituted in 2005 and antibiotic prophylaxis was already becoming widespread at this time. Both the antibiosis and other SCIP quality measures may have contributed to reductions in overall surgical infections since the original studies of infection rates in these operations. In addition, laparoscopy has become standard practice among general surgeons. The prevalence of laparoscopy and the increased expertise in its use are almost certainly contributing to these findings, though this effect is difficult to quantify. This study identifies several factors associated with higher odds of surgical infection that could be accurately and reliably determined preoperatively (Table 4), and with an OR 1.50 (“other/unknown” race/ethnicity, diabetes, hypertension, smoking, and ASA>2). Among intraoperative factors assessed by NSQIP criteria, operative minutes and wound class of 4 were highly significantly associated with increased odds of infection. Of the covariates strongly associated with surgical infection in our multiple regression model, diabetes, ASA>2, operative time, and wound class are included as risk factors in U.S. guidelines but hypertension and smoking are not. Since 2013, the American Society of Health System Pharmacists’/ Infectious Diseases Society of America/Surgical Infection Society/Society for Healthcare Epidemiology of America (ASHP/
4
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
Table 3 e Characteristics of elective laparoscopic cholecystectomy NSQIP patients (N [ 30,579) with surgical or C. difficile infection. Characteristic, n (%)
Age, m(s)
Infection Surgical (n ¼ 293)
P value
C. difficile (n ¼ 31)
P value*
54.5 (17.2)
<0.00001z
55.8 (18.5)
0.02z
Sex
*
0.001
Female
191 (73.7)
Male
102 (26.3)
0.25 20 (64.5) 11 (35.5) 0.05y
<0.0001
Race/ethnicity White
181 (64.2)
Asian
9 (3.2)
1 (3.2)
Black
21 (8.8)
2 (6.5)
Hispanic
22 (11.4)
Other/unknown
60 (12.4)
BMI, m(s)
32.7 (8.6)
27 (87.1)
0 (0.0) 1 (3.2) 0.02z
30.3 (7.9)
0.33z
Comorbidities Diabetes
79 (26.9)
<0.0001
5 (16.1)
0.46
COPD
15 (5.1)
0.001
4 (12.9)
0.005y
15 (48.4)
159 (54.3)
<0.0001
CHF
3 (1.0)
0.03
Renal failure
4 (1.4)
0.008y
Ascites
1 (0.3)
0.09y
0 (0.0)
d
Smoking
64 (21.8)
0.007
7 (22.6)
0.33
Steroids
10 (3.4)
0.14
3 (9.7)
0.03y
Hypertension
0 (0.0) 1 (3.2)
1
13 (4.4)
1 (3.2)
2
127 (43.3)
13 (41.9)
3
137 (46.8)
15 (48.4)
4 Operative time, min m (s)
16 (5.5) 70.3 (36.1)
2 (6.5) <0.00001z
62.1 (43.2)
0.37z 0.57y
<0.0001
Wound class
d 0.08y
0.005y
<0.0001
ASA class
0.06
1
14 (4.8)
1 (3.2)
2
213 (72.7)
24 (77.4)
3
57 (19.5)
6 (19.4)
4
9 (3.1)
0 (0.0)
BMI ¼ body mass index; COPD ¼ chronic obstructive pulmonary disease; CHF ¼ congestive heart failure. * Chi-squared test. y Fisher’s exact test. z t test.
IDSA/SIS/SHEA) joint guidelines have not recommended the use of routine antibiotic prophylaxis in low-risk, elective, laparoscopic cholecystectomy patients.11 The guidelines exclude from the “low-risk” category patients with any of these risk factors: age >70y, diabetes, immunosuppression, ASA>2, anticipated operative time >120 min, risk of gallbladder rupture, risk of conversion to open, biliary colic <30 d prior, anticipated bile spillage, pregnancy, and nonfunctioning gallbladder (emergency, acute cholecystitis, open cholecystectomy, reoperation for complication <1 mo from initial biliary operation, and jaundice were also included, but these were excluded by our study criteria).11 The ASHP/IDSA/ SIS/SHEA guidelines are the only major U.S. clinical practice guidelines to specifically address antibiotic prophylaxis in this
subgroup. The Centers for Disease Control and ACS/SIS do not yet address or acknowledge this question in their 2017 and 2016 guidelines, respectively.12,13 Interestingly, most of the “high-risk” features delineated by the national guidelines are based on risk of bile spillage and bacterial colonization, which have not been convincingly demonstrated to affect the occurrence of surgical infections and can be difficult to estimate preoperatively. We identified only a few covariates significantly associated with C difficile infection in our univariate analysis, and none in our multiple regression model. This may be indicative of an inadequate sample size; the study sample of 31 cases is an order of magnitude smaller than that for surgical site infection. The relevant univariate factors associated with C difficile
5
ely et al low infection risk in elective lap chole
Table 4 e Adjusted multivariable model of patient and operative characteristics associated with surgical or C. difficile infection after elective laparoscopic cholecystectomy. Characteristic
Infection Surgical, OR (95% CI)
*
P value
C. difficile, OR (95% CI)
P value*
Age (per 1 y)
1.01 (0.99, 1.02)
0.22
1.00 (0.98, 1.03)
0.74
Male
1.02 (0.79, 1.32)
0.86
1.10 (0.51, 2.36)
0.82
Asian
0.96 (0.48, 1.91)
0.91
0.71 (0.09, 5.48)
0.74
Black
0.72 (0.45, 1.14)
0.16
0.57 (0.13, 2.45)
0.45
Hispanic
0.83 (0.53, 1.30)
0.42
d
d
Other/unknown
2.01 (1.49, 2.72)
<0.0001
0.21 (0.03, 1.58)
0.13
1.00 (0.99, 1.02)
0.58
0.97 (0.92, 1.02)
0.24
Diabetes
1.67 (1.25, 2.24)
0.001
0.92 (0.33, 2.58)
0.87
COPD
1.13 (0.65, 1.98)
0.66
2.65 (0.83, 8.50)
0.10
Hypertension
1.52 (1.14, 2.04)
0.005
1.05 (0.45, 2.47)
0.91
CHF
1.75 (0.53, 5.85)
0.36
d
d
Renal failure
2.47 (0.86, 7.05)
0.09
6.09 (0.73, 50.6)
0.09
Ascites
3.99 (0.46, 35.0)
0.21
d
d
Smoking
1.50 (1.11, 2.01)
0.007
1.21 (0.49, 2.96)
0.68
Steroids
1.20 (0.63, 2.30)
0.58
2.62 (0.76, 9.01)
0.13
2
1.52 (0.82, 2.80)
0.18
1.77 (0.22, 14.1)
0.59
3
2.34 (1.22, 4.52)
0.01
3.23 (0.36, 28.8)
0.29
4
4.48 (1.92, 10.5)
0.001
5.65 (0.39, 82.9)
0.21
1.006 (1.004, 1.008)
<0.0001
1.003 (0.99, 1.01)
0.54
2
0.82 (0.47, 1.43)
0.48
1.21 (0.16, 9.00)
0.85
3
1.16 (0.64, 2.11)
0.63
1.77 (0.21, 14.9)
0.60
4
2.59 (1.06, 6.35)
0.04
d
d
Race/ethnicity (Ref. white)
BMI Comorbidities
ASA class (Ref. 1)
Operative time (per 1 min) Wound class (Ref. 1)
BMI, body mass index; COPD, chronic obstructive pulmonary disease; CHF, congestive heart failure. * Multiple logistic regression.
colitis (age, chronic obstructive pulmonary disease, steroids, and ASA) may be representative of overall immunocompromised states, which is a known risk factor for C difficile colitis in general. This study has several strengths. It is one of the largest database studies of this issue to date, and it is the first study on this topic to evaluate a U.S. patient population. Because the NSQIP database provided adequate case numbers while drawing only from recent (2016-2017) data, this study also represents an updated assessment of postoperative infection risk after elective laparoscopic cholecystectomy, compared to older studies, many of which predated the implementation of SCIP quality measures. Furthermore, the NSQIP database samples predominantly from large academic hospitals,14 which account for most acute care facilities in the United States,15 and so, our study may be considered reasonably representative of American general surgical practice. The most significant limitation of our study is that the NSQIP database does not record antibiotic timing or administration, and so we cannot draw any direct conclusions about the impact of routine preoperative antibiotic use on these findings. However, prescribing practices here and abroad
overwhelmingly favor routine administration. Even in the U.K., where the National Health Service’s guidelines recommend no antibiotic prophylaxis in elective laparoscopic cholecystectomy, a majority of patients still receive it16,17din a 2017 British study, only 5.6% of surgeons consistently did not administer antibiotics for low-risk, elective cases.18 Furthermore, in the United States, the practice has been reinforced by adherence to the SCIP quality measures. We can likely conclude that the vast majority of NSQIP patients would have received antibiotics. There are some other minor limitations related to the structure of the NSQIP database. We could not directly evaluate many of the intraoperative, predominantly biliary-based variables designated as “high-risk” by national guidelines. The granularity of data was not sufficient to evaluate details of the surgical infections such as their specific locations (beyond depth), the causative organisms, and so on. Finally, with all retrospective observational studies, we cannot ascertain causality in our results. This study highlights three key areas for further work on this topic. First, data on the current antibiotic prescribing practices of surgeons are extremely limited. There are only a handful of publications describing antibiotic administration in
6
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
varied surgical settings, some of which are sourced from survey-report rather than medication administration records, and almost none of which examine data from the United States. A published investigation of antibiotic prophylaxis practices, now a long-standing quality measure, is sorely needed. Second, we propose that the NSQIP database should be expanded to include SCIP measure variables to better assess the role of these interventions in key preventable complications, such as preoperative antibiotic administration for surgical site infection and chemoprophylaxis administration for deep venous thrombosis. Finally, in this descriptive study, we speculated that most of the patients in our study received prophylactic antibiotics, and we cannot determine what, if any, role this played in our findings. A comparative study will be needed to evaluate the effect of preoperative antibiotics on infection rates and to elucidate the role of routine antibiotic prophylaxis in the overall decline in the postoperative infection rates after laparoscopic cholecystectomy. A large, multicenter, randomized, controlled trial of elective, outpatient laparoscopic cholecystectomy patients receiving prophylactic antibiotics or placebo will be crucial to better define the relationship of antibiotic prophylaxis with key surgical outcomes such as wound infection and C difficile colitis.
Conclusions The incidence of surgical infection after elective laparoscopic cholecystectomy is very low, on par with clean (wound class 1) cases. The incidence of C difficile infection is also extremely low. Guidelines, where available, delineate several factors for consideration of cases as higher than “low-risk” for infection. Our study identified the following mostly patient-related risk factors that are not included in current guidelines: diabetes, hypertension, smoking, ASA class >2, operative time (per minute), and wound class 4. This study represents an updated assessment of the surgical site infection rate after elective laparoscopic cholecystectomy in current U.S. surgical practice. Further study is needed to evaluate the role of current antibiotic prophylaxis in achieving these infection rates much lower than historically reported.
Acknowledgment This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Authors’ contributions: S.E. and C.K.C. conceived the study and were subsequently involved with all phases of the project. K.A.R., G.B., R.C.G., and M.R.H. additionally assisted with study design and editing. K.A.R. and C.K.C. performed the statistical analyses. All authors were involved in the writing and editing process.
Disclosure The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
references
1. Medicare quality improvement community: surgical care improvement project. Available at: http://www.medqic.org/ dcs/ContentServer?cid¼1137346750659&pagename¼Medqic% 2FContent%2FParentShellTemplate&parentName¼Topic Cat&c¼MQParents. Accessed April 29, 2019. 2. Sanabria A, Dominguez LC, Valdivieso E, Gomez G. Antibiotic prophylaxis for patients undergoing elective laparoscopic cholecystectomy. Cochrane Database Syst Rev. 2010:CD005265. 3. Yanni F, Mekhail P, Morris-Stiff G. A selective antibiotic prophylaxis policy for laparoscopic cholecystectomy is effective in minimising infective complications. Ann R Coll Surg Engl. 2013;95:345e348. 4. Romy S, Eisenring M-C, Bettschart V, Petignat C, Francioli P, Troillet N. Laparoscope use and surgical site infections in digestive surgery. Ann Surg. 2008;247:627e632. 5. Varela JE, Wilson SE, Nguyen NT. Laparoscopic surgery significantly reduces surgical-site infections compared with open surgery. Surg Endosc. 2009;24:270e276. 6. Mioton LM, Jordan SW, Hanwright PJ, Bilimoria KY, Kim JY. The relationship between preoperative wound classification and postoperative infection: a multi-institutional analysis of 15,289 patients. Arch Plast Surg. 2013;40:522. 7. Sarkut P, Kilicturgay S, Aktas H, Ozen Y, Kaya E. Routine use of prophylactic antibiotics during laparoscopic cholecystectomy does not reduce the risk of surgical site infections. Surg Infect. 2017;18:603e609. 8. Catarci M, Mancini S, Gentileschi P, Camplone C, Sileri P, Grassi GB. Antibiotic prophylaxis in elective laparoscopic cholecystectomy: lack of need or lack of evidence? Surg Endosc. 2004;18:638e641. 9. Biscione FM, Couto RC, Pedrosa TM, Neto MC. Comparison of the risk of surgical site infection after laparoscopic cholecystectomy and open cholecystectomy. Infect Control Hosp Epidemiol. 2007;28:1103e1106. 10. Zerey M, Paton L, Lincourt AE, Gersin KS, Kercher KW, Heniford BT. The Burden of Clostridium difficile in surgical patients in the United States. Surg Infect. 2007;8:557e566. 11. Bratzler DW, Patchen D, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Surg Infect. 2013;14:73e156. 12. Berrios-Torres SI, Umscheld CA, Bratzler DW, et al. Centers for disease control and prevention guideline for the prevention of surgical site infection. JAMA Surg. 2017;152:784e791. 13. Ban KA, Minei JP, Laronga C, et al. American College of surgeons and surgical infection society: surgical site infection guidelines, 2016 update. J Am Coll Surg. 2017;224:59e74. 14. Alluri RK, Leland H, Heckmann N. Surgical research using national databases. Ann Transl Med. 2016;4:393. 15. Steiner CA, Karaca Z, Moore BJ, Imshaug MC, Pickens G. Surgeries in Hospital-based Ambulatory surgery and hospital Inpatient settings, 2014. HCUP statistical Brief #223; 2017. Rockville, MD: Agency for Healthcare Research and Quality; 2017. Available at: www. hcup-us.ahrq.gov/reports/statbriefs/sb223-AmbulatoryInpatient-Surgeries-2014.pdf. Accessed April 30, 2019. 16. Graham HE, Vasireddy A, Nehra D. A national audit of antibiotic prophylaxis in elective laparoscopic cholecystectomy. Ann R Coll Surg Engl. 2014;96:377e380. 17. Vohra RS, Hodson J, Pasquali S, Griffiths EA. Effectiveness of antibiotic prophylaxis in non-emergency cholecystectomy using data from a population-based cohort study. World J Surg. 2017;41:2231e2239. 18. Macano CAW, Griffiths EA, Vohra RS. Current practice of antibiotic prophylaxis during elective laparoscopic cholecystectomy. Ann R Coll Engl. 2017;99:216e217.
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Modern Elective Laparoscopic Cholecystectomy Carries Extremely Low Postoperative Infection Risk Sora Ely, MD,a,b,* Kara A. Rothenberg, MD,a,b Genna Beattie, MD,a,b Rebecca C. Gologorsky, MD,a,b Michelle R. Huyser, MD,a,b and Ching-Kuo Chang, MDb a b
UCSF East Bay Surgery, Oakland, California Department of Surgery, Kaiser Permanente e Oakland Medical Center, Oakland, California
article info
abstract
Article history:
Background: The studies that established historical rates of surgical infection after chole-
Received 1 May 2019
cystectomy predate the modern era of laparoscopy and routine prophylactic antibiotics.
Received in revised form
Newer studies have reported a much lower incidence of infections in “low-risk” elective,
31 August 2019
outpatient, laparoscopic cholecystectomies. We investigated the current rate of post-
Accepted 18 September 2019
operative infections in these cases within a large, U.S. database.
Available online xxx
Methods: We retrospectively reviewed elective laparoscopic cholecystectomies from the 2016-2017 American College of Surgeons National Surgical Quality Improvement Program
Keywords:
database. Our primary outcome was postoperative surgical site infection; secondary was
Elective laparoscopic
Clostridium difficile infection. Logistic models evaluated the associations of patient and
cholecystectomy
operation characteristics with these outcomes.
Surgical site infection
Results: Surgical infection occurred in 1.0% of cases (293/30,579). C difficile infection occurred
Postoperative infection
in 0.1% (31 cases). In our adjusted multivariable models, other/unknown race/ethnicity,
Clostridium difficile colitis
diabetes, hypertension, smoking, American Society of Anesthesiologists >2, operative minutes, and wound class 4 were associated with a significantly higher odds of surgical infection; no covariates were significantly associated with C difficile infection. Conclusions: In the setting of modern U.S. surgical practice, the incidence of infection after elective laparoscopic cholecystectomy is very low, on par with clean cases. Our study identified several patient characteristics that were strongly associated with surgical infection. Many of these are not included as risk factors in current guidelines for antibiotic prophylaxis and may help to identify those at higher risk for this rare complication. ª 2019 Elsevier Inc. All rights reserved.
Introduction The Surgical Care Improvement Project (SCIP) introduced prophylactic, preincision antibiotic administration as a measure to reduce surgical site infection in 2005 and subsequently
modified this to a selective recommendation based on the procedure and wound classification.1 Given that the biliary tract is technically entered during transection of the cystic duct, cholecystectomy is classically considered to have a minimum wound classification of “clean-contaminated”
* Corresponding author. Department of Surgery, 1411 E 31st Street, QIC#22134, Oakland, CA 94602. Tel.: þ1 480 420 7672; fax: þ1 480 264 0266. E-mail address: [email protected] (S. Ely). 0022-4804/$ e see front matter ª 2019 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jss.2019.09.038
2
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
(class 2),2 making this SCIP quality measure applicable to the procedure. In open cholecystectomies, the practice of antibiotic prophylaxis has been supported by studies showing decreases in infection rates since its adoption.3 However, since the advent and proliferation of laparoscopy, newer studies have shown that laparoscopic cholecystectomies are associated with a lower incidence of wound infection than are open. Reported wound infection rates among open cholecystectomy cases range from 1.8% to 7.9%,4,5 on par with the expected rate of 3%-11% for clean-contaminated cases6; by contrast, wound infection rates among laparoscopic cholecystectomy cases in comparative studies are consistently half or less of those for open cases and have been reported as low as 0.5%.7-9 These rates of 0.5% to 1.5%7,10,11 are comparable to the expected 1%-5% infection rate for “clean” (class 1) cases.6 These provocative data, combined with increasing general concern about antibiotic stewardship and antibioticassociated infections such as Clostridium difficile colitis, led surgeons to question the necessity of antibiotic prophylaxis for laparoscopic cholecystectomy cases. A number of studies have investigated the rates of infection and utility of routine prophylactic antibiotics in laparoscopic cholecystectomies over the last 2 decades. Though their conclusions have been heterogeneous, these studies have consistently identified “low-risk” cholecystectomy cases as those that are performed laparoscopically on an elective, outpatient basis. Although contemporary reports have suggested a much lower incidence of surgical infection in these low-risk (outpatient, elective) laparoscopic cholecystectomy cases, none of these studies have evaluated U.S. populations. We used a large, national database to investigate the incidence of surgical or C difficile infection after elective laparoscopic cholecystectomy in the modern American surgery setting, and the factors associated with either occurrence.
Methods We retrospectively reviewed adult elective, outpatient laparoscopic cholecystectomy cases from the 2016-2017 American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) Participant Use Files. Laparoscopic cholecystectomies were identified by Current Procedural Terminology code 47,562 “laparoscopy, surgical; cholecystectomy.” Related Current Procedural Terminology codes 47,563 and 47,564, which add “with cholangiography” and “with exploration of common duct,” respectively, were not included. These additional procedures were felt not to be representative of routine elective cases, and the more extensive manipulation of the biliary system could have a potential confounding effect. Only elective (INOUT ¼ “Outpatient”), outpatient (ELECTSURG ¼ “Yes”) procedures were included. To obtain a realistic representation of risk among cases planned as elective and outpatient, we did not use postoperatively defined variables such as length of stay or wound class in our study criteria. Only cases with an American Society of Anesthesiologists (ASA) class of 5 (“moribund”) were excluded because this classification seemed incompatible with elective, outpatient status. We did not further restrict the study population, recognizing that this could result in the inclusion of some higher-risk cases, in favor
of producing a more conservative estimate of risk and maximizing the generalizability of our findings. Our primary outcome was occurrence of postoperative surgical site infection, defined as any superficial wound, deep wound, or organ space infection; our secondary outcome was occurrence of C difficile infection. Chi-squared test, Fisher’s exact test, and Student’s t test were used to evaluate the associations between patient and operative characteristics and postoperative infections. Multiple logistic regression (with surgical infection and C difficile infection modeled separately) was then used to further characterize the associations between the covariates and our outcomes of interest. A threshold of P < 0.05 was set for statistical significance. All statistical tests were performed using Stata statistical software, version 15 (StataCorp LP, College Station, TX). Because this study used publicly available, deidentified data and did not impact patient care, it was not required to undergo IRB review.
Results A total of 30,579 elective laparoscopic cholecystectomy cases met study criteria. Our study population demographics (Table 1) were as expected for routine cholecystectomies, with a mean age of 48.6 y, a 3:1 female predominance, and a majority being obese (52.6%). Mean operative time was just under an hour (56.9 min), though with considerable variability (standard deviation 32.1 min). Wound class was most frequently identified as 2 (clean-contaminated), but it is interesting to note the small proportion of cases that were classified erroneously as 1 (clean). Postoperative surgical site infection occurred in 293 cases, or 1%; C difficile infection occurred in 31 cases, or 0.1% (Table 2). Wound infections were predominantly superficial (46.2%). C difficile infections occurred in the absence of a surgical infection in most cases (90.0%). Only 3 patients had occurrences of both infections, representing 0.01% of the total study population, 1% of the patients with surgical infection, or 9.7% of the patients with C difficile infection. The proportional occurrence of surgical infections among cases with wound classes 1-3 was low and markedly higher with wound class 4. Within each wound class (1-4), the percentages of patients with surgical infections were, respectively, 1.0%, 0.9%, 1.4%, and 4.3%. Most of the demographic characteristics, comorbidities, and operative factors investigated as covariates were found to be significantly associated with surgical infection, and a few with C difficile infection (Table 3). Of the many characteristics associated with surgical infection, age and operative minutes (P < 0.00001), followed by race/ethnicity, diabetes, hypertension, ASA class, and wound class (P < 0.0001), were highly statistically significant. Only age, chronic obstructive pulmonary disease, and steroids were significantly associated with C difficile infection. In our multivariable models, several factors were independently associated with higher odds of surgical infection (Table 4), all with clinically relevant OR of 1.5 except operative time, which was calculated per 1 min. The greatest increases in surgical infection odds were seen with ASA of 3 (2.34, 95% CI: 1.22, 4.52), ASA of 4 (4.48, 95% CI: 1.92, 10.5), and
3
ely et al low infection risk in elective lap chole
Table 1 e Patient and case characteristics of 2016-2017 NSQIP elective laparoscopic cholecystectomies. Characteristic, n (%) Age, m(s)
Study population (n ¼ 30,579) 48.6 (16.5)
Sex Female Male
21.0
8051 (26.3)
Organ space
98
33.1
C. difficile infection
31
0.1
19,624 (64.2)
Hispanic
3473 (11.4)
Other/unknown
3805 (12.4) 31.6 (7.5)
BMI* 223 (0.7)
Normal
5254 (17.3)
Overweight
8932 (29.4) 15,959 (52.6)
Comorbidities
COPD Hypertension CHF
3617 (11.8) 698 (2.3) 9975 (32.6) 71 (0.2)
Renal failure
83 (0.3)
Ascites
10 (0.03)
Smoking
4931 (16.1)
Steroids
659 (2.2)
ASA class 1
3294 (10.8)
2
18,350 (60.0)
3
8541 (28.0)
4 Operative time, min m(s)
Superficial wound
46.2
981 (3.2)
Diabetes
1.0
61
2696 (8.8)
Obese
293 137
Black
Underweight
Surgical infection
Deep wound
Asian
BMI, m(s)
(N ¼ 30,579) n, %
Characteristic
22,528 (73.7)
Race White
Table 2 e Infection occurrences by type among NSQIP database elective laparoscopic cholecystectomy cases.
362 (1.2) 56.9 (32.1)
Wound class 1
1369 (4.5)
2
24,975 (81.7)
3
4026 (13.2)
4
209 (0.7)
BMI, body mass index; COPD, chronic obstructive pulmonary disease; CHF, congestive heart failure. * BMI classes reported in addition to the continuous variable’s mean and standard deviation to better illustrate the distribution in the study cohort; only the continuous variable was used in statistical analyses.
wound class of 4 (2.59, 95% CI: 1.06, 6.35). Meanwhile, none of the covariates were independently associated with higher odds of C difficile colitis in our multiple regression analysis.
Discussion Postoperative occurrences of surgical or C difficile infections were overall very rare among elective laparoscopic
cholecystectomy cases. Our 1% rate of surgical site infection confirms the trend suggested in prior literature that currentpractice laparoscopic cholecystectomy has a much lower incidence of postoperative infection than historically associated with either open or laparoscopic cholecystectomy,4,5,7-9 on par with modern rates of most wound class 1 (“clean”) cases.6 Our study also demonstrates an exceedingly low 0.1% rate of C difficile infection. This rate is comparable to the rate of 0.41% after cholecystectomy from an analysis of 1999-2003 National Inpatient Sample data.11 This suggests that, at least in this population, the risk of C difficile infection has not increased meaningfully as a result of practice changes over the last 15-20 y. Nonetheless, its 0.1% incidence represents a rate of 10% of the frequency of surgical infection, and C difficile infection may carry a greater morbidity and mortality. Most C difficile infections occurred in the absence of a surgical site infection and thus likely in patients prescribed only prophylactic antibiotics. Our study is the first to show that the risk of infection after elective, outpatient cholecystectomy in the setting of contemporary American surgical practice is now extremely low. Although we cannot draw any conclusions about the causes for this decreased infection rate, there are a number of possible factors. Of note, SCIP was instituted in 2005 and antibiotic prophylaxis was already becoming widespread at this time. Both the antibiosis and other SCIP quality measures may have contributed to reductions in overall surgical infections since the original studies of infection rates in these operations. In addition, laparoscopy has become standard practice among general surgeons. The prevalence of laparoscopy and the increased expertise in its use are almost certainly contributing to these findings, though this effect is difficult to quantify. This study identifies several factors associated with higher odds of surgical infection that could be accurately and reliably determined preoperatively (Table 4), and with an OR 1.50 (“other/unknown” race/ethnicity, diabetes, hypertension, smoking, and ASA>2). Among intraoperative factors assessed by NSQIP criteria, operative minutes and wound class of 4 were highly significantly associated with increased odds of infection. Of the covariates strongly associated with surgical infection in our multiple regression model, diabetes, ASA>2, operative time, and wound class are included as risk factors in U.S. guidelines but hypertension and smoking are not. Since 2013, the American Society of Health System Pharmacists’/ Infectious Diseases Society of America/Surgical Infection Society/Society for Healthcare Epidemiology of America (ASHP/
4
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
Table 3 e Characteristics of elective laparoscopic cholecystectomy NSQIP patients (N [ 30,579) with surgical or C. difficile infection. Characteristic, n (%)
Age, m(s)
Infection Surgical (n ¼ 293)
P value
C. difficile (n ¼ 31)
P value*
54.5 (17.2)
<0.00001z
55.8 (18.5)
0.02z
Sex
*
0.001
Female
191 (73.7)
Male
102 (26.3)
0.25 20 (64.5) 11 (35.5) 0.05y
<0.0001
Race/ethnicity White
181 (64.2)
Asian
9 (3.2)
1 (3.2)
Black
21 (8.8)
2 (6.5)
Hispanic
22 (11.4)
Other/unknown
60 (12.4)
BMI, m(s)
32.7 (8.6)
27 (87.1)
0 (0.0) 1 (3.2) 0.02z
30.3 (7.9)
0.33z
Comorbidities Diabetes
79 (26.9)
<0.0001
5 (16.1)
0.46
COPD
15 (5.1)
0.001
4 (12.9)
0.005y
15 (48.4)
159 (54.3)
<0.0001
CHF
3 (1.0)
0.03
Renal failure
4 (1.4)
0.008y
Ascites
1 (0.3)
0.09y
0 (0.0)
d
Smoking
64 (21.8)
0.007
7 (22.6)
0.33
Steroids
10 (3.4)
0.14
3 (9.7)
0.03y
Hypertension
0 (0.0) 1 (3.2)
1
13 (4.4)
1 (3.2)
2
127 (43.3)
13 (41.9)
3
137 (46.8)
15 (48.4)
4 Operative time, min m (s)
16 (5.5) 70.3 (36.1)
2 (6.5) <0.00001z
62.1 (43.2)
0.37z 0.57y
<0.0001
Wound class
d 0.08y
0.005y
<0.0001
ASA class
0.06
1
14 (4.8)
1 (3.2)
2
213 (72.7)
24 (77.4)
3
57 (19.5)
6 (19.4)
4
9 (3.1)
0 (0.0)
BMI ¼ body mass index; COPD ¼ chronic obstructive pulmonary disease; CHF ¼ congestive heart failure. * Chi-squared test. y Fisher’s exact test. z t test.
IDSA/SIS/SHEA) joint guidelines have not recommended the use of routine antibiotic prophylaxis in low-risk, elective, laparoscopic cholecystectomy patients.11 The guidelines exclude from the “low-risk” category patients with any of these risk factors: age >70y, diabetes, immunosuppression, ASA>2, anticipated operative time >120 min, risk of gallbladder rupture, risk of conversion to open, biliary colic <30 d prior, anticipated bile spillage, pregnancy, and nonfunctioning gallbladder (emergency, acute cholecystitis, open cholecystectomy, reoperation for complication <1 mo from initial biliary operation, and jaundice were also included, but these were excluded by our study criteria).11 The ASHP/IDSA/ SIS/SHEA guidelines are the only major U.S. clinical practice guidelines to specifically address antibiotic prophylaxis in this
subgroup. The Centers for Disease Control and ACS/SIS do not yet address or acknowledge this question in their 2017 and 2016 guidelines, respectively.12,13 Interestingly, most of the “high-risk” features delineated by the national guidelines are based on risk of bile spillage and bacterial colonization, which have not been convincingly demonstrated to affect the occurrence of surgical infections and can be difficult to estimate preoperatively. We identified only a few covariates significantly associated with C difficile infection in our univariate analysis, and none in our multiple regression model. This may be indicative of an inadequate sample size; the study sample of 31 cases is an order of magnitude smaller than that for surgical site infection. The relevant univariate factors associated with C difficile
5
ely et al low infection risk in elective lap chole
Table 4 e Adjusted multivariable model of patient and operative characteristics associated with surgical or C. difficile infection after elective laparoscopic cholecystectomy. Characteristic
Infection Surgical, OR (95% CI)
*
P value
C. difficile, OR (95% CI)
P value*
Age (per 1 y)
1.01 (0.99, 1.02)
0.22
1.00 (0.98, 1.03)
0.74
Male
1.02 (0.79, 1.32)
0.86
1.10 (0.51, 2.36)
0.82
Asian
0.96 (0.48, 1.91)
0.91
0.71 (0.09, 5.48)
0.74
Black
0.72 (0.45, 1.14)
0.16
0.57 (0.13, 2.45)
0.45
Hispanic
0.83 (0.53, 1.30)
0.42
d
d
Other/unknown
2.01 (1.49, 2.72)
<0.0001
0.21 (0.03, 1.58)
0.13
1.00 (0.99, 1.02)
0.58
0.97 (0.92, 1.02)
0.24
Diabetes
1.67 (1.25, 2.24)
0.001
0.92 (0.33, 2.58)
0.87
COPD
1.13 (0.65, 1.98)
0.66
2.65 (0.83, 8.50)
0.10
Hypertension
1.52 (1.14, 2.04)
0.005
1.05 (0.45, 2.47)
0.91
CHF
1.75 (0.53, 5.85)
0.36
d
d
Renal failure
2.47 (0.86, 7.05)
0.09
6.09 (0.73, 50.6)
0.09
Ascites
3.99 (0.46, 35.0)
0.21
d
d
Smoking
1.50 (1.11, 2.01)
0.007
1.21 (0.49, 2.96)
0.68
Steroids
1.20 (0.63, 2.30)
0.58
2.62 (0.76, 9.01)
0.13
2
1.52 (0.82, 2.80)
0.18
1.77 (0.22, 14.1)
0.59
3
2.34 (1.22, 4.52)
0.01
3.23 (0.36, 28.8)
0.29
4
4.48 (1.92, 10.5)
0.001
5.65 (0.39, 82.9)
0.21
1.006 (1.004, 1.008)
<0.0001
1.003 (0.99, 1.01)
0.54
2
0.82 (0.47, 1.43)
0.48
1.21 (0.16, 9.00)
0.85
3
1.16 (0.64, 2.11)
0.63
1.77 (0.21, 14.9)
0.60
4
2.59 (1.06, 6.35)
0.04
d
d
Race/ethnicity (Ref. white)
BMI Comorbidities
ASA class (Ref. 1)
Operative time (per 1 min) Wound class (Ref. 1)
BMI, body mass index; COPD, chronic obstructive pulmonary disease; CHF, congestive heart failure. * Multiple logistic regression.
colitis (age, chronic obstructive pulmonary disease, steroids, and ASA) may be representative of overall immunocompromised states, which is a known risk factor for C difficile colitis in general. This study has several strengths. It is one of the largest database studies of this issue to date, and it is the first study on this topic to evaluate a U.S. patient population. Because the NSQIP database provided adequate case numbers while drawing only from recent (2016-2017) data, this study also represents an updated assessment of postoperative infection risk after elective laparoscopic cholecystectomy, compared to older studies, many of which predated the implementation of SCIP quality measures. Furthermore, the NSQIP database samples predominantly from large academic hospitals,14 which account for most acute care facilities in the United States,15 and so, our study may be considered reasonably representative of American general surgical practice. The most significant limitation of our study is that the NSQIP database does not record antibiotic timing or administration, and so we cannot draw any direct conclusions about the impact of routine preoperative antibiotic use on these findings. However, prescribing practices here and abroad
overwhelmingly favor routine administration. Even in the U.K., where the National Health Service’s guidelines recommend no antibiotic prophylaxis in elective laparoscopic cholecystectomy, a majority of patients still receive it16,17din a 2017 British study, only 5.6% of surgeons consistently did not administer antibiotics for low-risk, elective cases.18 Furthermore, in the United States, the practice has been reinforced by adherence to the SCIP quality measures. We can likely conclude that the vast majority of NSQIP patients would have received antibiotics. There are some other minor limitations related to the structure of the NSQIP database. We could not directly evaluate many of the intraoperative, predominantly biliary-based variables designated as “high-risk” by national guidelines. The granularity of data was not sufficient to evaluate details of the surgical infections such as their specific locations (beyond depth), the causative organisms, and so on. Finally, with all retrospective observational studies, we cannot ascertain causality in our results. This study highlights three key areas for further work on this topic. First, data on the current antibiotic prescribing practices of surgeons are extremely limited. There are only a handful of publications describing antibiotic administration in
6
j o u r n a l o f s u r g i c a l r e s e a r c h - 2 0 1 9 ( - ) 1 e6
varied surgical settings, some of which are sourced from survey-report rather than medication administration records, and almost none of which examine data from the United States. A published investigation of antibiotic prophylaxis practices, now a long-standing quality measure, is sorely needed. Second, we propose that the NSQIP database should be expanded to include SCIP measure variables to better assess the role of these interventions in key preventable complications, such as preoperative antibiotic administration for surgical site infection and chemoprophylaxis administration for deep venous thrombosis. Finally, in this descriptive study, we speculated that most of the patients in our study received prophylactic antibiotics, and we cannot determine what, if any, role this played in our findings. A comparative study will be needed to evaluate the effect of preoperative antibiotics on infection rates and to elucidate the role of routine antibiotic prophylaxis in the overall decline in the postoperative infection rates after laparoscopic cholecystectomy. A large, multicenter, randomized, controlled trial of elective, outpatient laparoscopic cholecystectomy patients receiving prophylactic antibiotics or placebo will be crucial to better define the relationship of antibiotic prophylaxis with key surgical outcomes such as wound infection and C difficile colitis.
Conclusions The incidence of surgical infection after elective laparoscopic cholecystectomy is very low, on par with clean (wound class 1) cases. The incidence of C difficile infection is also extremely low. Guidelines, where available, delineate several factors for consideration of cases as higher than “low-risk” for infection. Our study identified the following mostly patient-related risk factors that are not included in current guidelines: diabetes, hypertension, smoking, ASA class >2, operative time (per minute), and wound class 4. This study represents an updated assessment of the surgical site infection rate after elective laparoscopic cholecystectomy in current U.S. surgical practice. Further study is needed to evaluate the role of current antibiotic prophylaxis in achieving these infection rates much lower than historically reported.
Acknowledgment This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Authors’ contributions: S.E. and C.K.C. conceived the study and were subsequently involved with all phases of the project. K.A.R., G.B., R.C.G., and M.R.H. additionally assisted with study design and editing. K.A.R. and C.K.C. performed the statistical analyses. All authors were involved in the writing and editing process.
Disclosure The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
references
1. Medicare quality improvement community: surgical care improvement project. Available at: http://www.medqic.org/ dcs/ContentServer?cid¼1137346750659&pagename¼Medqic% 2FContent%2FParentShellTemplate&parentName¼Topic Cat&c¼MQParents. Accessed April 29, 2019. 2. Sanabria A, Dominguez LC, Valdivieso E, Gomez G. Antibiotic prophylaxis for patients undergoing elective laparoscopic cholecystectomy. Cochrane Database Syst Rev. 2010:CD005265. 3. Yanni F, Mekhail P, Morris-Stiff G. A selective antibiotic prophylaxis policy for laparoscopic cholecystectomy is effective in minimising infective complications. Ann R Coll Surg Engl. 2013;95:345e348. 4. Romy S, Eisenring M-C, Bettschart V, Petignat C, Francioli P, Troillet N. Laparoscope use and surgical site infections in digestive surgery. Ann Surg. 2008;247:627e632. 5. Varela JE, Wilson SE, Nguyen NT. Laparoscopic surgery significantly reduces surgical-site infections compared with open surgery. Surg Endosc. 2009;24:270e276. 6. Mioton LM, Jordan SW, Hanwright PJ, Bilimoria KY, Kim JY. The relationship between preoperative wound classification and postoperative infection: a multi-institutional analysis of 15,289 patients. Arch Plast Surg. 2013;40:522. 7. Sarkut P, Kilicturgay S, Aktas H, Ozen Y, Kaya E. Routine use of prophylactic antibiotics during laparoscopic cholecystectomy does not reduce the risk of surgical site infections. Surg Infect. 2017;18:603e609. 8. Catarci M, Mancini S, Gentileschi P, Camplone C, Sileri P, Grassi GB. Antibiotic prophylaxis in elective laparoscopic cholecystectomy: lack of need or lack of evidence? Surg Endosc. 2004;18:638e641. 9. Biscione FM, Couto RC, Pedrosa TM, Neto MC. Comparison of the risk of surgical site infection after laparoscopic cholecystectomy and open cholecystectomy. Infect Control Hosp Epidemiol. 2007;28:1103e1106. 10. Zerey M, Paton L, Lincourt AE, Gersin KS, Kercher KW, Heniford BT. The Burden of Clostridium difficile in surgical patients in the United States. Surg Infect. 2007;8:557e566. 11. Bratzler DW, Patchen D, Olsen KM, et al. Clinical practice guidelines for antimicrobial prophylaxis in surgery. Surg Infect. 2013;14:73e156. 12. Berrios-Torres SI, Umscheld CA, Bratzler DW, et al. Centers for disease control and prevention guideline for the prevention of surgical site infection. JAMA Surg. 2017;152:784e791. 13. Ban KA, Minei JP, Laronga C, et al. American College of surgeons and surgical infection society: surgical site infection guidelines, 2016 update. J Am Coll Surg. 2017;224:59e74. 14. Alluri RK, Leland H, Heckmann N. Surgical research using national databases. Ann Transl Med. 2016;4:393. 15. Steiner CA, Karaca Z, Moore BJ, Imshaug MC, Pickens G. Surgeries in Hospital-based Ambulatory surgery and hospital Inpatient settings, 2014. HCUP statistical Brief #223; 2017. Rockville, MD: Agency for Healthcare Research and Quality; 2017. Available at: www. hcup-us.ahrq.gov/reports/statbriefs/sb223-AmbulatoryInpatient-Surgeries-2014.pdf. Accessed April 30, 2019. 16. Graham HE, Vasireddy A, Nehra D. A national audit of antibiotic prophylaxis in elective laparoscopic cholecystectomy. Ann R Coll Surg Engl. 2014;96:377e380. 17. Vohra RS, Hodson J, Pasquali S, Griffiths EA. Effectiveness of antibiotic prophylaxis in non-emergency cholecystectomy using data from a population-based cohort study. World J Surg. 2017;41:2231e2239. 18. Macano CAW, Griffiths EA, Vohra RS. Current practice of antibiotic prophylaxis during elective laparoscopic cholecystectomy. Ann R Coll Engl. 2017;99:216e217.