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Acute cholecystitis: risk factors for conversion to an open procedure
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 x x x ( 2 0 1 5 ) 1 e5
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Acute cholecystitis: risk factors for conversion to an open procedure Megan Sippey, MD, Marysia Grzybowski, PhD, MPH, BSN, Mark L. Manwaring, MD, Kevin R. Kasten, MD, William H. Chapman, MD, Walter E. Pofahl, MD, Walter J. Pories, MD, and Konstantinos Spaniolas, MD* Department of Surgery, Brody School of Medicine at East Carolina University, Greenville, North Carolina
article info
abstract
Article history:
Background: Laparoscopic cholecystectomy is one of the most common general surgical
Received 27 February 2015
procedures performed. Conversion to an open procedure (CTO) is associated with
Received in revised form
increased morbidity and length of stay. Patients presenting with acute cholecystitis are at
21 April 2015
higher risk for CTO. Studies have attempted to examine risk factors for CTO in patients
Accepted 21 May 2015
who undergo laparoscopic cholecystectomy for acute cholecystitis but are limited by small
Available online xxx
sample size. The aim of this study was to identify preoperative variables that predict higher risk for CTO in patients presenting with acute cholecystitis.
Keywords:
Materials and methods: Patients undergoing laparoscopic cholecystectomy for acute chole-
Acute Cholecystitis
cystitis from 2005e2011 were identified from the American College of Surgeons’ National
Laparoscopic Cholecystectomy
Surgical Quality Improvement Program Participant Use File. Patients who underwent
Conversion
successful laparoscopic surgery were compared with those who required CTO.
ACS-NSQIP
Demographics, comorbidities, and 30-d outcomes were analyzed. Multivariable logistic regression was used for variables with P value <0.1, with CTO used as the dependent variable. Results: A total of 7242 patients underwent laparoscopic cholecystectomy for acute cholecystitis. CTO was reported in 436 patients (6.0%). Those who required conversion were older (60.7 16.2 versus 51.6 18.0, P ¼ 0.0001) and mean body mass index was greater (30.8 7.6 versus 30.0 7.3, P ¼ 0.033) compared with those whose procedure was completed laparoscopically. Vascular, cardiac, renal, pulmonary, neurologic, hepatic disease, diabetes, and bleeding disorders were more prevalent in CTO patients. Mortality (2.3% versus 0.7%, P < 0.0001), overall morbidity (21.8% versus 6.0%, P < 0.0001), serious morbidity (14.9% versus 3.8%, P < 0.0001), reoperation (3.4% versus 1.4%, P ¼ 0.001), and surgical site infection (9.2% versus 1.8%, P < 0.0001) rates, as well as length of stay (8.6 13.0 versus 3.4 6.7, P < 0.0001) were greater in those requiring CTO. The following factors were independently associated with CTO: age (odds ratio [OR], 1.01, P ¼ 0.015), male gender (OR, 1.77, P ¼ 0.005), body mass index (OR, 1.04, P < 0.0001), preoperative alkaline phosphatase (OR, 1.01, P ¼ 0.0005), white blood cell count (OR, 1.06, P ¼ 0.0001), and albumin (OR, 0.52, P ¼ 0.0001).
This study was presented in part at the 10th Annual Academic Surgical Congress on February 3, 2015. * Corresponding author. Department of Surgery, Brody School of Medicine at East Carolina University, 600 Moye Boulevard, Greenville, NC 27834. Tel.: þ1 252 744 0292; fax: þ1 252 744 5775. E-mail address: [email protected] (K. Spaniolas). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2015.05.040
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 x x x ( 2 0 1 5 ) 1 e5
Conclusions: CTO for acute cholecystitis remains low but not clinically negligible. The identified risk factors can potentially guide management and patient selection for delayed intervention for acute cholecystitis. ª 2015 Elsevier Inc. All rights reserved.
1.
Introduction
The laparoscopic approach to cholecystectomy was introduced in the late 1980s, originally in the elective setting, but promptly became the gold standard of treatment for patients presenting with acute cholecystitis in the United States [1]. Laparoscopic cholecystectomy is associated with decreased costs, length of stay (LOS), postoperative pain, and risk for wound complications compared with an open procedure [2,3]. Furthermore, patients have a much shorter convalescence time after laparoscopic cholecystectomy compared with open surgery [2]. However, conversion to an open procedure (CTO) is still reported in 1.9%e11.9% of cases [3e10]. Given these disadvantages of open surgery, it may be beneficial to preoperatively identify patients with acute cholecystitis that are at an increased risk of CTO and potentially modify their risk factors before surgical intervention. Current literature indicates that numerous factors may place a patient at risk for CTO including male gender, increased age, hypertension, and systemic inflammatory response syndrome and/or sepsis at diagnosis, preoperative albumin, low hematocrit, leukocytosis, hyponatremia, elevated international normalized ratio (INR), thickened wall and pericholecystic fluid on ultrasound, dilated common bile duct, previous abdominal surgery, and emergent status of the surgery [3,4,6,7,11e16]. However, these studies are limited by either small sample size or broad inclusion criteria in their study populations. The aim of this study was to assess risk factors for CTO for patients undergoing a laparoscopic cholecystectomy for acute cholecystitis.
2.
Materials and methods
The American College of Surgeons’ National Surgical Quality Improvement Program (ACS-NSQIP) Participant Use File was used for this study. This is a national database with data entered by trained clinical reviewers. It includes preoperative risk factors, laboratory values, intraoperative variables, and 30-d postoperative morbidity and mortality data. The ACSNSQIP administration periodically audits the data to ensure high reliability. International Classification of Diseases, Ninth Revision current procedural terminology (CPT) codes were used to identify patients that underwent laparoscopic cholecystectomy (47562, 47563, and 47564) for acute cholecystitis (575.0, 575.12, 575.2, 575.3, and 575.4) between 2005 and 2011. Patients who were converted were identified as those with primary CPT code as a laparoscopic procedure with a secondary code for an open cholecystectomy (47600, 47605, 47610, 47612, or 47620). Patients were also included and considered converted if their primary CPT code was diagnostic laparoscopy (49320) with a secondary code for open cholecystectomy or if the primary code was exploratory laparotomy (49000) with a secondary code for laparoscopic cholecystectomy.
Baseline demographics included age, gender, body mass index (BMI), preoperative laboratory values, and presence of comorbid disease. Comorbidities were grouped based on organ system as previously published [17,18]. Diabetes, bleeding disorders, a history of active smoking, and weight loss >10% within 6 mo were analyzed individually. The primary outcome assessed was CTO. Approval for this study was obtained by the East Carolina University Institutional Review Board. Data analysis was performed using SPSS for Macintosh version 21 (IBM, Somers, NY). Univariate analysis was performed to assess the effect of demographics, comorbidities, and preoperative laboratory values on conversion using chi-square for nominal and ordinal variables with frequencies reported. BMI was used both as a categorical variable as well as a continuous variable. Two-tailed independent samples t-test was used for continuous variables with mean and standard deviation reported. Multivariable logistic regression was then performed with all variables with an a priori P value <0.1 on univariate analysis entered into the model with CTO as the dependent variable with BMI as a continuous variable. Odds ratios (OR) with 95% confidence intervals were reported. A P value of <0.05 was considered statistically significant.
3.
Results
We identified 7242 patients who underwent laparoscopic cholecystectomy for acute cholecystitis between 2005 and 2011: 2989 (41.4%) were male, mean age was 52.1 y (18.0), and mean BMI was 30.1 (7.3). CTO was reported in 436 patients (6.0%). Baseline patient characteristics are shown in Table 1. Those who required conversion were older (60.7 16.2 versus 51.6 18.0, P ¼ 0.0001) and mean BMI was greater (30.8 7.6 versus 30.0 7.3, P ¼ 0.033) compared with those whose procedure was completed laparoscopically. There were significant differences in those requiring conversion compared with those completed laparoscopically in the incidence of all comorbidities. Table 2 shows the unadjusted associations between selected independent variables and CTO. Mortality (2.3% versus 0.7%, P < 0.0001), overall morbidity (21.8% versus 6.0%, P < 0.0001), serious morbidity (14.9% versus 3.8%, P < 0.0001), reoperation (3.4% versus 1.4%, P ¼ 0.001), and surgical site infection (SSI) (9.2% versus 1.8%, P < 0.0001) rates, as well as LOS (8.6 13.0 versus 3.4 6.7, P < 0.0001) were greater in those requiring CTO (Table 3). Logistic regression revealed that the following factors were independently associated with CTO: age (OR, 1.01, P ¼ 0.015), male gender (OR, 1.77, P ¼ 0.005), BMI (OR, 1.04, P < 0.0001), preoperative alkaline phosphatase (OR, 1.01, P ¼ 0.0005), white blood cell (WBC) count (OR, 1.06, P ¼ 0.0001), and albumin (OR, 0.52, P ¼ 0.0001). The overall model had a strong ability to
3
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 x x x ( 2 0 1 5 ) 1 e5
Table 1 e Preoperative characteristics of patients undergoing cholecystectomy for acute cholecystitis.
Table 3 e Unadjusted outcomes of patients undergoing cholecystectomy for acute cholecystitis.
Variable
Variable
Converted Laparoscopic P (n ¼ 436) (n ¼ 6806) value
Mean age 60.69 16.18 Mean BMI 30.80 7.55 Gender, % (n) 59.7 (258) ASA classification IV or V 11.9 (52) Diabetes, % (n) 21.3 (93) Vascular comorbidity, 61.7 (264) % (n) Cardiac comorbidity, % (n) 17.5 (71) Renal comorbidity, % (n) 2.5 (11) Pulmonary comorbidity, 9.1 (37) % (n) Neurologic comorbidity, 12.8 (52) % (n) Hepatic comorbidity, % (n) 3.2 (13) Smoking, % (n) 13.3 (58) Chronic steroid use, % (n) 2.8 (12) >10% weight loss, % (n) 1.8 (8) Bleeding disorder, % (n) 10.6 (46) Obesity, % (n) 48.4 (211) Days from admission 2.11 4.53 to operating room Emergent surgery, % (n) 34.2% (149) 30.9 (125) Attending operating alone, % (n)
51.55 17.97 30.00 7.31 40.2 (2731) 3.5 (235) 13.9 (947) 43.1 (2719)
<0.0001 0.033 <0.0001 <0.0001 <0.0001 <0.0001
10.8 (650) 1.3 (86) 4.4 (263)
<0.0001 0.027 <0.0001
5.9 (355)
<0.0001
1.1 (65) 19.3 (1315) 2.3 (159) 1.4 (98) 5.7 (390) 42.7 (2908) 1.35 5.43
<0.0001 0.002 0.579 0.506 <0.0001 0.021 0.001
27.0 (1839) 33.5 (2011)
0.001 0.284
Converted (n ¼ 436)
Median operation 122.09 50.96 time (min) Median hospital stay (d) 8.60 13.00 Surgical site infection, 9.2 (40) % (n) Mortality, % (n) 2.3 (10) Serious Morbidity, % (n) 14.9 (65) Overall Morbidity, % (n) 21.8 (95) Readmission, % (n) 10.7 (8) Reoperation, % (n) 3.4 (15)
Laparoscopic (n ¼ 6806)
P value
79.99 42.60
<0.0001
3.42 6.74 1.8 (123)
<0.0001 <0.0001
0.7 (47) 3.8 (258) 6.0 (411) 8.0 (112) 1.4 (96)
<0.0001 <0.0001 <0.0001 0.402 0.001
greater than 9.19 and alkaline phosphatase greater than 114, the risk for CTO is 21%. A patient with these characteristics may benefit from interval cholecystectomy to allow for laboratory normalization and possible preoperative weight loss. In contrast, a female patient with acute cholecystitis and none of the mentioned risk factors have a 1.5% risk of CTO and would likely benefit from immediate cholecystectomy.
4.
Discussion
ASA ¼ American Society of Anesthesiology.
discriminate between patients who did and did not require CTO (c ¼ 0.74). The overall likelihood ratio chi-square was 122.9 with 6 of freedom (P < 0.0001). The Hosmer and Lemeshow goodness-of-fit test was nonsignificant. The risks factors identified in this study can allow for preoperative risk stratification and possibly risk modification. Clinical patient scenarios with associated probability for CTO are shown in Table 4. For example, our model predicts that for an obese male patient with albumin less than 3.7, WBC count
Table 2 e Association between selected characteristics and CTO. Variable Male Obesity Bleeding disorder Diabetes Vascular comorbidity Cardiac comorbidity Renal comorbidity Pulmonary comorbidity Neurologic comorbidity Hepatic comorbidity Smoking Steroid use Weight loss Attending alone Emergent case CI ¼ confidence interval.
OR (95% CI)
P value
2.20 (1.81e2.69) 1.26 (1.04e1.53) 1.94 (1.41e2.68) 1.68 (1.32e2.13) 2.13 (1.74e2.60) 1.74 (1.33e2.28) 2.02 (1.07e3.82) 2.18 (1.52e3.12) 2.33 (1.71e3.18) 3.01 (1.65e5.51) 0.64 (0.48e0.85) 1.18 (0.65e2.14) 1.28 (0.62e2.65) 0.89 (0.71e1.10) 1.40 (1.14e1.72)
<0.0001 0.021 <0.0001 <0.0001 <0.0001 <0.0001 0.027 <0.0001 <0.0001 0.0002 0.0019 0.579 0.506 0.284 0.0012
The present study is the first to examine risk factors for conversion from a laparoscopic to open cholecystectomy specifically for acute cholecystitis on a large scale. In this patient population, 436 patients (6.0%) required CTO. This is consistent with previously reported rates of CTO for cholecystectomy of 1.9%e11.9% [3e10]. Select single institutional studies limited to acute cholecystitis have shown conversion rates as high as 28% [11e14]. However, these studies either include patients dating back to the infancy of laparoscopic surgery or include patient populations that differ from the present study (higher percentage male, older, and different practice environment). In our study, patients with CTO had increased overall morbidity, serious morbidity, SSI, reoperation rate, LOS, and mortality. Given these worse outcomes, despite being low, this rate of CTO is not clinically negligible.
Table 4 e Clinical patient scenarios with probability of CTO for acute cholecystitis. Case Gender BMI
A B C D E F G H I J
F F F F F M M M M M
28 28 28 28 30 28 28 28 28 30
Alkaline WBC Albumin Conversion phosphatase probability, % 90 90 90 116 116 90 90 90 116 116
8 8 12 12 12 8 8 12 12 12
4 3 3 3 3 4 3 3 3 3
1.5 2.2 6.3 10.1 15.3 4.3 5.5 10.9 15.4 20.9
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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 x x x ( 2 0 1 5 ) 1 e5
Although laparoscopic cholecystectomy is the gold standard of care for acute cholecystitis, alternative acceptable treatment includes intravenous antibiotics followed by an interval laparoscopic cholecystectomy. For complicated acute cholecystitis or persistent symptoms, a percutaneous cholecystostomy tube placed under radiographic guidance is another option in addition to the mentioned antibiotics and interval cholecystectomy [1,19]. Patient satisfaction is reduced with these delayed approaches (75.34 12.85 versus 92.66 6.8, P 0.0001), whereas number of readmissions and total mean hospital days (5.7 2.32 versus 2.4 1.1 d, P 0.0001) are increased compared with those with early operative intervention [20]. Cholecystostomy tubes are also prone to blockage, dislodgement, and can cause injury on placement with overall complication rates as high as 47.8% when placed in radiology and 33.3% when placed operatively [19]. However, these studies reports outcomes on all patients presenting with acute cholecystitis and the conclusion that early intervention is optimal may not translate to special high-risk subpopulations. For the subgroup of patients at high risk for CTO (with associated postoperative morbidity and mortality), the incidence of complications from early cholecystectomy, compared with the risks of delayed intervention, are unknown. However, up to now, studies had provided with limited ability to identify that high-risk group. The disadvantages of delayed operative intervention must be weighed against the increased morbidity and mortality risks associated with CTO cholecystectomy. This study provides a guidance tool for surgeons to identify patients at risk for CTO so that these delayed approaches to management of acute cholecystitis can be optimally used. Factors found to be independently associated with CTO included male gender. This is consistent with previous publications [3,4,6]. It is thought that males may delay seeking medical attention for their symptoms longer than females, which leads to a more hostile operative field and higher likelihood of conversion. Increased BMI was also independently associated with CTO. Although the current literature is divided as to whether BMI is predictive of conversion [4,6,8,9,15], possible explanations that support this finding include increased difficulty with liver retraction, increased pneumoperitoneum requirements, and difficult laparoscopic instrument placement and manipulation given the increased abdominal wall thickness. Increased preoperative alkaline phosphatase and WBC and decreased albumin were also predictive of CTO. These values are indicative of an advanced disease process potentially correlating with an increasingly difficult dissection and poor definition of anatomy leading to a higher CTO rate. Limitations of this study include those intrinsic to retrospective database reviews. A selection bias of sites that participate in ACS-NSQIP on a voluntary basis may exist. This may bias toward surgeons with increased laparoscopic training, experience, and comfort level. These factors were not included in our analysis but could play a role in CTO. Although the ACS-NSQIP Participant Use File captures postoperative diagnosis, it does not include pathologic documentation of cholecystitis. Therefore, coding bias may exist. However, the use of NSQIP data for research in acute cholecystitis has been well established despite this limitation
[21e24]. This data set also lacks information regarding the onset of symptoms and therefore timing of operation was not analyzed. The ACS-NSQIP Participant Use File only collects outcomes data for the first 30 postoperative days. Therefore, data regarding long-term complications, such as late readmission and incisional hernia formation, are lacking. Furthermore, data were unavailable to compare outcomes of those whose acute cholecystitis was managed with radiologyplaced cholecystostomy tubes and antibiotics followed by interval cholecystectomy to those who received an open cholecystectomy because the database only includes patients who received an operation. Although the strength of this study lies in the magnitude of the data set; unfortunately, this additional information is unavailable by nature of the retrospective database design. Given these limitations, future aims of the study include examining outcomes in those who require CTO compared with patients managed with delayed operative intervention for acute cholecystitis. While Hokkam’s [20] recent study compared outcomes and patient satisfaction between those with early cholecystectomy versus delayed cholecystectomy, there was no subgroup analysis comparing our patients of interest who required CTO or even a group at higher risk for CTO. The present study identifies this high-risk group and shows increased morbidity and mortality in those requiring conversion. This lays the groundwork to next compare treatment approaches in this high-risk group.
5.
Conclusions
This was the first study to assess risk factors for conversion from laparoscopic to open cholecystectomy on a large scale for patients with acute cholecystitis. Although the CTO rate remains low, it is not clinically negligible. The identified risk factors including male gender, obesity, and increased age in combination with preoperative laboratory values can guide management and patient selection for delayed intervention for acute cholecystitis.
Acknowledgment This study received no external funding. Authors’ contributions: M.S. and K.S. were responsible for the conception and design of this work. M.S., K.S., M.G., M.L.M., K.R.K., W.H.C., W.E.P., and W.J.P. contributed to the acquisition, analysis, and interpretation of the work. M.S. was responsible for drafting the work. K.S., M.G., M.L.M., K.R.K., W.H.C., W.E.P., and W.J.P. contributed to revising the work critically for important intellectual content.
Disclosure The authors of this study have no conflicts of interest to report. The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
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 x x x ( 2 0 1 5 ) 1 e5
references
[1] Overby DW, Awad Z, Haggerty S, et al (2010) Society of American Gastrointestinal Endoscopic Surgeons (SAGES) guidelines for the clinical application of laparoscopic biliary tract surgery. Available from: http://www.sages.org/public ations/guidelines/guidelines-for-the-clinical-application-oflaparoscopic-biliary-tract-surgery/. Accessed Dec 31, 2014. [2] Begos DG, Modlin IM. Laparoscopic cholecystectomy; from gimmick to gold standard. J Clin Gastroenterol 1994;19:325. [3] Kaafarani HM, Smith TS, Neumayer L, Berger DH, Depalma RG, Itani KM. Trends, outcomes, and predictors of open and conversion to open cholecystectomy in Veterans Health Administration hospitals. Am J Surg 2010; 2010:32. [4] Papandria D, Lardaro R, Rhee D, et al. Risk factors for conversion from laparoscopic to open surgery: analysis of 2,138 converted operations in the American College of Surgeons National Surgical Quality Improvement Program. Am Surg 2013;79:914. [5] Lengyel BI, Azagury D, Varban O, et al. Laparoscopic cholecystectomy after a quarter century: why do we still convert? Surg Endosc 2012;26:508. [6] Hutchinson CH, Traverso LW, Lee FT. Laparoscopic cholecystectomy. Do preoperative factors predict the need to convert to open? Surg Endosc 1994;8:875. [7] Lee NW, Collins J, Britt R, Britt LD. Evaluation for preoperative risk factors for converting laparoscopic to open cholecystectomy. Am Surg 2012;78:831. [8] Simopoulos C, Polychronidis A, Botaitis S, Perente S, Pitiakoudis M. Laparoscopic cholecystectomy in obese patients. Obes Surg 2005;15:243. [9] Farkas DT, Moradi D, Moaddel D, Nagpal K, Cosgrove JM. The impact of body mass index on outcomes after laparoscopic cholecystectomy. Surg Endosc 2012;26:964. [10] Paajanen H, Kakela P, Suuronen S, Paajanen J, Juvonen P, Pihlajamaki J. Impact of obesity and associated diseases on outcome after laparoscopic cholecystectomy. Surg Laparosc Endosc Percutan Tech 2012;22:509. [11] Wevers KP, van Westreenen HL, Patijn GA. Laparoscopic cholecystectomy in acute cholecystitis: c-reactive protein level combined with age predicts conversion. Surg Laparosc Endosc Percutan Tech 2013;23:163. [12] Cwik G, Skoczylas T, Wyroslak-Najs J, Wallner G. The value of percutaneous ultrasound in predicting conversion from laparoscopic to open cholecystectomy due to acute cholecystitis. Surg Endosc 2013;27:2561.
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[13] Kim MS, Kwon HJ, Park HW, et al. Preoperative prediction model for conversion of laparoscopic to open cholecystectomy in patient with acute cholecystitis: based on clinical, laboratory, and CT parameters. J Comput Assist Tomogr 2014;38:727. [14] Oymaci E, Ucar AD, Aydogan S, Sari E, Erkan N, Yildirim M. Evaluation of affecting factors for conversion to open cholecystectomy in acute cholecystitis. Prz Gastroenterol 2014;9:336. [15] Rosen M, Brody F, Ponsky J. Predictive factors for conversion of laparoscopic cholecystectomy. Am J Surg 2002;184:254. [16] Sikora SS, Kumar A, Saxena R, Kapoor VK, Kaushik SP. Laparoscopic cholecystectomydcan conversion be predicted? World J Surg 1995;19:858. [17] Spaniolas K, Laycock WS, Adrales GL, Trus TL. Laparoscopic paraesophageal hernia repair: advanced age is associated with minor but not major morbidity or mortality. J Am Coll Surg 2014;218:1187. [18] Spaniolas K, Trus TL, Adrales GL, Quigley MT, Pories WJ, Laycock WS. Early morbidity and mortality of laparoscopic sleeve gastrectomy and gastric bypass in the elderly: a NSQIP analysis. Surg Obes Relat Dis 2014;10:584. [19] Sneider EB, Lewis J, Friedrich A, et al. Timing and choice of intervention influences outcome in acute cholecystitis: a prospective study. Surg Laparosc Endosc Percutan Tech 2014; 24:414. [20] Saber A, Hokkam EN. Operative outcome and patient satisfaction in early and delayed laparoscopic cholecystectomy for acute cholecystitis. Minim Invasive Surg 2014;2014:162643. http://dx.doi.org/10.1155/2014/162643. [21] Brooks KR, Scarborough JE, Vaslef SN, Shapiro ML. No need to wait: an analysis of the timing of cholecystectomy during admission for acute cholecystitis using the American College of Surgeons National Surgical Quality Improvement Program database. J Trauma Acute Care Surg 2013;74:167. [22] Karamanos E, Sivrikoz E, Beale E, Chan L, Demetriades D. Effect of diabetes on outcomes in patients undergoing emergent cholecystectomy for acute cholecystitis. World J Surg 2013;37:2257. [23] Gelbard R, Karamanos E, Teixeira PG, et al. Effect of delaying same-admission cholecystectomy on outcomes in patients with diabetes. Br J Surg 2014;101:74. [24] Ingraham AM, Cohen ME, Ko CY, Hall BL. A current profile and assessment of North American cholecystectomy: results from the American College of Surgeons National Surgical Quality Improvement Program. J Am Coll Surg 2010;211:176.
Available online at www.sciencedirect.com
ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Acute cholecystitis: risk factors for conversion to an open procedure Megan Sippey, MD, Marysia Grzybowski, PhD, MPH, BSN, Mark L. Manwaring, MD, Kevin R. Kasten, MD, William H. Chapman, MD, Walter E. Pofahl, MD, Walter J. Pories, MD, and Konstantinos Spaniolas, MD* Department of Surgery, Brody School of Medicine at East Carolina University, Greenville, North Carolina
article info
abstract
Article history:
Background: Laparoscopic cholecystectomy is one of the most common general surgical
Received 27 February 2015
procedures performed. Conversion to an open procedure (CTO) is associated with
Received in revised form
increased morbidity and length of stay. Patients presenting with acute cholecystitis are at
21 April 2015
higher risk for CTO. Studies have attempted to examine risk factors for CTO in patients
Accepted 21 May 2015
who undergo laparoscopic cholecystectomy for acute cholecystitis but are limited by small
Available online xxx
sample size. The aim of this study was to identify preoperative variables that predict higher risk for CTO in patients presenting with acute cholecystitis.
Keywords:
Materials and methods: Patients undergoing laparoscopic cholecystectomy for acute chole-
Acute Cholecystitis
cystitis from 2005e2011 were identified from the American College of Surgeons’ National
Laparoscopic Cholecystectomy
Surgical Quality Improvement Program Participant Use File. Patients who underwent
Conversion
successful laparoscopic surgery were compared with those who required CTO.
ACS-NSQIP
Demographics, comorbidities, and 30-d outcomes were analyzed. Multivariable logistic regression was used for variables with P value <0.1, with CTO used as the dependent variable. Results: A total of 7242 patients underwent laparoscopic cholecystectomy for acute cholecystitis. CTO was reported in 436 patients (6.0%). Those who required conversion were older (60.7 16.2 versus 51.6 18.0, P ¼ 0.0001) and mean body mass index was greater (30.8 7.6 versus 30.0 7.3, P ¼ 0.033) compared with those whose procedure was completed laparoscopically. Vascular, cardiac, renal, pulmonary, neurologic, hepatic disease, diabetes, and bleeding disorders were more prevalent in CTO patients. Mortality (2.3% versus 0.7%, P < 0.0001), overall morbidity (21.8% versus 6.0%, P < 0.0001), serious morbidity (14.9% versus 3.8%, P < 0.0001), reoperation (3.4% versus 1.4%, P ¼ 0.001), and surgical site infection (9.2% versus 1.8%, P < 0.0001) rates, as well as length of stay (8.6 13.0 versus 3.4 6.7, P < 0.0001) were greater in those requiring CTO. The following factors were independently associated with CTO: age (odds ratio [OR], 1.01, P ¼ 0.015), male gender (OR, 1.77, P ¼ 0.005), body mass index (OR, 1.04, P < 0.0001), preoperative alkaline phosphatase (OR, 1.01, P ¼ 0.0005), white blood cell count (OR, 1.06, P ¼ 0.0001), and albumin (OR, 0.52, P ¼ 0.0001).
This study was presented in part at the 10th Annual Academic Surgical Congress on February 3, 2015. * Corresponding author. Department of Surgery, Brody School of Medicine at East Carolina University, 600 Moye Boulevard, Greenville, NC 27834. Tel.: þ1 252 744 0292; fax: þ1 252 744 5775. E-mail address: [email protected] (K. Spaniolas). 0022-4804/$ e see front matter ª 2015 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.jss.2015.05.040
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 x x x ( 2 0 1 5 ) 1 e5
Conclusions: CTO for acute cholecystitis remains low but not clinically negligible. The identified risk factors can potentially guide management and patient selection for delayed intervention for acute cholecystitis. ª 2015 Elsevier Inc. All rights reserved.
1.
Introduction
The laparoscopic approach to cholecystectomy was introduced in the late 1980s, originally in the elective setting, but promptly became the gold standard of treatment for patients presenting with acute cholecystitis in the United States [1]. Laparoscopic cholecystectomy is associated with decreased costs, length of stay (LOS), postoperative pain, and risk for wound complications compared with an open procedure [2,3]. Furthermore, patients have a much shorter convalescence time after laparoscopic cholecystectomy compared with open surgery [2]. However, conversion to an open procedure (CTO) is still reported in 1.9%e11.9% of cases [3e10]. Given these disadvantages of open surgery, it may be beneficial to preoperatively identify patients with acute cholecystitis that are at an increased risk of CTO and potentially modify their risk factors before surgical intervention. Current literature indicates that numerous factors may place a patient at risk for CTO including male gender, increased age, hypertension, and systemic inflammatory response syndrome and/or sepsis at diagnosis, preoperative albumin, low hematocrit, leukocytosis, hyponatremia, elevated international normalized ratio (INR), thickened wall and pericholecystic fluid on ultrasound, dilated common bile duct, previous abdominal surgery, and emergent status of the surgery [3,4,6,7,11e16]. However, these studies are limited by either small sample size or broad inclusion criteria in their study populations. The aim of this study was to assess risk factors for CTO for patients undergoing a laparoscopic cholecystectomy for acute cholecystitis.
2.
Materials and methods
The American College of Surgeons’ National Surgical Quality Improvement Program (ACS-NSQIP) Participant Use File was used for this study. This is a national database with data entered by trained clinical reviewers. It includes preoperative risk factors, laboratory values, intraoperative variables, and 30-d postoperative morbidity and mortality data. The ACSNSQIP administration periodically audits the data to ensure high reliability. International Classification of Diseases, Ninth Revision current procedural terminology (CPT) codes were used to identify patients that underwent laparoscopic cholecystectomy (47562, 47563, and 47564) for acute cholecystitis (575.0, 575.12, 575.2, 575.3, and 575.4) between 2005 and 2011. Patients who were converted were identified as those with primary CPT code as a laparoscopic procedure with a secondary code for an open cholecystectomy (47600, 47605, 47610, 47612, or 47620). Patients were also included and considered converted if their primary CPT code was diagnostic laparoscopy (49320) with a secondary code for open cholecystectomy or if the primary code was exploratory laparotomy (49000) with a secondary code for laparoscopic cholecystectomy.
Baseline demographics included age, gender, body mass index (BMI), preoperative laboratory values, and presence of comorbid disease. Comorbidities were grouped based on organ system as previously published [17,18]. Diabetes, bleeding disorders, a history of active smoking, and weight loss >10% within 6 mo were analyzed individually. The primary outcome assessed was CTO. Approval for this study was obtained by the East Carolina University Institutional Review Board. Data analysis was performed using SPSS for Macintosh version 21 (IBM, Somers, NY). Univariate analysis was performed to assess the effect of demographics, comorbidities, and preoperative laboratory values on conversion using chi-square for nominal and ordinal variables with frequencies reported. BMI was used both as a categorical variable as well as a continuous variable. Two-tailed independent samples t-test was used for continuous variables with mean and standard deviation reported. Multivariable logistic regression was then performed with all variables with an a priori P value <0.1 on univariate analysis entered into the model with CTO as the dependent variable with BMI as a continuous variable. Odds ratios (OR) with 95% confidence intervals were reported. A P value of <0.05 was considered statistically significant.
3.
Results
We identified 7242 patients who underwent laparoscopic cholecystectomy for acute cholecystitis between 2005 and 2011: 2989 (41.4%) were male, mean age was 52.1 y (18.0), and mean BMI was 30.1 (7.3). CTO was reported in 436 patients (6.0%). Baseline patient characteristics are shown in Table 1. Those who required conversion were older (60.7 16.2 versus 51.6 18.0, P ¼ 0.0001) and mean BMI was greater (30.8 7.6 versus 30.0 7.3, P ¼ 0.033) compared with those whose procedure was completed laparoscopically. There were significant differences in those requiring conversion compared with those completed laparoscopically in the incidence of all comorbidities. Table 2 shows the unadjusted associations between selected independent variables and CTO. Mortality (2.3% versus 0.7%, P < 0.0001), overall morbidity (21.8% versus 6.0%, P < 0.0001), serious morbidity (14.9% versus 3.8%, P < 0.0001), reoperation (3.4% versus 1.4%, P ¼ 0.001), and surgical site infection (SSI) (9.2% versus 1.8%, P < 0.0001) rates, as well as LOS (8.6 13.0 versus 3.4 6.7, P < 0.0001) were greater in those requiring CTO (Table 3). Logistic regression revealed that the following factors were independently associated with CTO: age (OR, 1.01, P ¼ 0.015), male gender (OR, 1.77, P ¼ 0.005), BMI (OR, 1.04, P < 0.0001), preoperative alkaline phosphatase (OR, 1.01, P ¼ 0.0005), white blood cell (WBC) count (OR, 1.06, P ¼ 0.0001), and albumin (OR, 0.52, P ¼ 0.0001). The overall model had a strong ability to
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Table 1 e Preoperative characteristics of patients undergoing cholecystectomy for acute cholecystitis.
Table 3 e Unadjusted outcomes of patients undergoing cholecystectomy for acute cholecystitis.
Variable
Variable
Converted Laparoscopic P (n ¼ 436) (n ¼ 6806) value
Mean age 60.69 16.18 Mean BMI 30.80 7.55 Gender, % (n) 59.7 (258) ASA classification IV or V 11.9 (52) Diabetes, % (n) 21.3 (93) Vascular comorbidity, 61.7 (264) % (n) Cardiac comorbidity, % (n) 17.5 (71) Renal comorbidity, % (n) 2.5 (11) Pulmonary comorbidity, 9.1 (37) % (n) Neurologic comorbidity, 12.8 (52) % (n) Hepatic comorbidity, % (n) 3.2 (13) Smoking, % (n) 13.3 (58) Chronic steroid use, % (n) 2.8 (12) >10% weight loss, % (n) 1.8 (8) Bleeding disorder, % (n) 10.6 (46) Obesity, % (n) 48.4 (211) Days from admission 2.11 4.53 to operating room Emergent surgery, % (n) 34.2% (149) 30.9 (125) Attending operating alone, % (n)
51.55 17.97 30.00 7.31 40.2 (2731) 3.5 (235) 13.9 (947) 43.1 (2719)
<0.0001 0.033 <0.0001 <0.0001 <0.0001 <0.0001
10.8 (650) 1.3 (86) 4.4 (263)
<0.0001 0.027 <0.0001
5.9 (355)
<0.0001
1.1 (65) 19.3 (1315) 2.3 (159) 1.4 (98) 5.7 (390) 42.7 (2908) 1.35 5.43
<0.0001 0.002 0.579 0.506 <0.0001 0.021 0.001
27.0 (1839) 33.5 (2011)
0.001 0.284
Converted (n ¼ 436)
Median operation 122.09 50.96 time (min) Median hospital stay (d) 8.60 13.00 Surgical site infection, 9.2 (40) % (n) Mortality, % (n) 2.3 (10) Serious Morbidity, % (n) 14.9 (65) Overall Morbidity, % (n) 21.8 (95) Readmission, % (n) 10.7 (8) Reoperation, % (n) 3.4 (15)
Laparoscopic (n ¼ 6806)
P value
79.99 42.60
<0.0001
3.42 6.74 1.8 (123)
<0.0001 <0.0001
0.7 (47) 3.8 (258) 6.0 (411) 8.0 (112) 1.4 (96)
<0.0001 <0.0001 <0.0001 0.402 0.001
greater than 9.19 and alkaline phosphatase greater than 114, the risk for CTO is 21%. A patient with these characteristics may benefit from interval cholecystectomy to allow for laboratory normalization and possible preoperative weight loss. In contrast, a female patient with acute cholecystitis and none of the mentioned risk factors have a 1.5% risk of CTO and would likely benefit from immediate cholecystectomy.
4.
Discussion
ASA ¼ American Society of Anesthesiology.
discriminate between patients who did and did not require CTO (c ¼ 0.74). The overall likelihood ratio chi-square was 122.9 with 6 of freedom (P < 0.0001). The Hosmer and Lemeshow goodness-of-fit test was nonsignificant. The risks factors identified in this study can allow for preoperative risk stratification and possibly risk modification. Clinical patient scenarios with associated probability for CTO are shown in Table 4. For example, our model predicts that for an obese male patient with albumin less than 3.7, WBC count
Table 2 e Association between selected characteristics and CTO. Variable Male Obesity Bleeding disorder Diabetes Vascular comorbidity Cardiac comorbidity Renal comorbidity Pulmonary comorbidity Neurologic comorbidity Hepatic comorbidity Smoking Steroid use Weight loss Attending alone Emergent case CI ¼ confidence interval.
OR (95% CI)
P value
2.20 (1.81e2.69) 1.26 (1.04e1.53) 1.94 (1.41e2.68) 1.68 (1.32e2.13) 2.13 (1.74e2.60) 1.74 (1.33e2.28) 2.02 (1.07e3.82) 2.18 (1.52e3.12) 2.33 (1.71e3.18) 3.01 (1.65e5.51) 0.64 (0.48e0.85) 1.18 (0.65e2.14) 1.28 (0.62e2.65) 0.89 (0.71e1.10) 1.40 (1.14e1.72)
<0.0001 0.021 <0.0001 <0.0001 <0.0001 <0.0001 0.027 <0.0001 <0.0001 0.0002 0.0019 0.579 0.506 0.284 0.0012
The present study is the first to examine risk factors for conversion from a laparoscopic to open cholecystectomy specifically for acute cholecystitis on a large scale. In this patient population, 436 patients (6.0%) required CTO. This is consistent with previously reported rates of CTO for cholecystectomy of 1.9%e11.9% [3e10]. Select single institutional studies limited to acute cholecystitis have shown conversion rates as high as 28% [11e14]. However, these studies either include patients dating back to the infancy of laparoscopic surgery or include patient populations that differ from the present study (higher percentage male, older, and different practice environment). In our study, patients with CTO had increased overall morbidity, serious morbidity, SSI, reoperation rate, LOS, and mortality. Given these worse outcomes, despite being low, this rate of CTO is not clinically negligible.
Table 4 e Clinical patient scenarios with probability of CTO for acute cholecystitis. Case Gender BMI
A B C D E F G H I J
F F F F F M M M M M
28 28 28 28 30 28 28 28 28 30
Alkaline WBC Albumin Conversion phosphatase probability, % 90 90 90 116 116 90 90 90 116 116
8 8 12 12 12 8 8 12 12 12
4 3 3 3 3 4 3 3 3 3
1.5 2.2 6.3 10.1 15.3 4.3 5.5 10.9 15.4 20.9
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Although laparoscopic cholecystectomy is the gold standard of care for acute cholecystitis, alternative acceptable treatment includes intravenous antibiotics followed by an interval laparoscopic cholecystectomy. For complicated acute cholecystitis or persistent symptoms, a percutaneous cholecystostomy tube placed under radiographic guidance is another option in addition to the mentioned antibiotics and interval cholecystectomy [1,19]. Patient satisfaction is reduced with these delayed approaches (75.34 12.85 versus 92.66 6.8, P 0.0001), whereas number of readmissions and total mean hospital days (5.7 2.32 versus 2.4 1.1 d, P 0.0001) are increased compared with those with early operative intervention [20]. Cholecystostomy tubes are also prone to blockage, dislodgement, and can cause injury on placement with overall complication rates as high as 47.8% when placed in radiology and 33.3% when placed operatively [19]. However, these studies reports outcomes on all patients presenting with acute cholecystitis and the conclusion that early intervention is optimal may not translate to special high-risk subpopulations. For the subgroup of patients at high risk for CTO (with associated postoperative morbidity and mortality), the incidence of complications from early cholecystectomy, compared with the risks of delayed intervention, are unknown. However, up to now, studies had provided with limited ability to identify that high-risk group. The disadvantages of delayed operative intervention must be weighed against the increased morbidity and mortality risks associated with CTO cholecystectomy. This study provides a guidance tool for surgeons to identify patients at risk for CTO so that these delayed approaches to management of acute cholecystitis can be optimally used. Factors found to be independently associated with CTO included male gender. This is consistent with previous publications [3,4,6]. It is thought that males may delay seeking medical attention for their symptoms longer than females, which leads to a more hostile operative field and higher likelihood of conversion. Increased BMI was also independently associated with CTO. Although the current literature is divided as to whether BMI is predictive of conversion [4,6,8,9,15], possible explanations that support this finding include increased difficulty with liver retraction, increased pneumoperitoneum requirements, and difficult laparoscopic instrument placement and manipulation given the increased abdominal wall thickness. Increased preoperative alkaline phosphatase and WBC and decreased albumin were also predictive of CTO. These values are indicative of an advanced disease process potentially correlating with an increasingly difficult dissection and poor definition of anatomy leading to a higher CTO rate. Limitations of this study include those intrinsic to retrospective database reviews. A selection bias of sites that participate in ACS-NSQIP on a voluntary basis may exist. This may bias toward surgeons with increased laparoscopic training, experience, and comfort level. These factors were not included in our analysis but could play a role in CTO. Although the ACS-NSQIP Participant Use File captures postoperative diagnosis, it does not include pathologic documentation of cholecystitis. Therefore, coding bias may exist. However, the use of NSQIP data for research in acute cholecystitis has been well established despite this limitation
[21e24]. This data set also lacks information regarding the onset of symptoms and therefore timing of operation was not analyzed. The ACS-NSQIP Participant Use File only collects outcomes data for the first 30 postoperative days. Therefore, data regarding long-term complications, such as late readmission and incisional hernia formation, are lacking. Furthermore, data were unavailable to compare outcomes of those whose acute cholecystitis was managed with radiologyplaced cholecystostomy tubes and antibiotics followed by interval cholecystectomy to those who received an open cholecystectomy because the database only includes patients who received an operation. Although the strength of this study lies in the magnitude of the data set; unfortunately, this additional information is unavailable by nature of the retrospective database design. Given these limitations, future aims of the study include examining outcomes in those who require CTO compared with patients managed with delayed operative intervention for acute cholecystitis. While Hokkam’s [20] recent study compared outcomes and patient satisfaction between those with early cholecystectomy versus delayed cholecystectomy, there was no subgroup analysis comparing our patients of interest who required CTO or even a group at higher risk for CTO. The present study identifies this high-risk group and shows increased morbidity and mortality in those requiring conversion. This lays the groundwork to next compare treatment approaches in this high-risk group.
5.
Conclusions
This was the first study to assess risk factors for conversion from laparoscopic to open cholecystectomy on a large scale for patients with acute cholecystitis. Although the CTO rate remains low, it is not clinically negligible. The identified risk factors including male gender, obesity, and increased age in combination with preoperative laboratory values can guide management and patient selection for delayed intervention for acute cholecystitis.
Acknowledgment This study received no external funding. Authors’ contributions: M.S. and K.S. were responsible for the conception and design of this work. M.S., K.S., M.G., M.L.M., K.R.K., W.H.C., W.E.P., and W.J.P. contributed to the acquisition, analysis, and interpretation of the work. M.S. was responsible for drafting the work. K.S., M.G., M.L.M., K.R.K., W.H.C., W.E.P., and W.J.P. contributed to revising the work critically for important intellectual content.
Disclosure The authors of this study have no conflicts of interest to report. The authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article.
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references
[1] Overby DW, Awad Z, Haggerty S, et al (2010) Society of American Gastrointestinal Endoscopic Surgeons (SAGES) guidelines for the clinical application of laparoscopic biliary tract surgery. Available from: http://www.sages.org/public ations/guidelines/guidelines-for-the-clinical-application-oflaparoscopic-biliary-tract-surgery/. Accessed Dec 31, 2014. [2] Begos DG, Modlin IM. Laparoscopic cholecystectomy; from gimmick to gold standard. J Clin Gastroenterol 1994;19:325. [3] Kaafarani HM, Smith TS, Neumayer L, Berger DH, Depalma RG, Itani KM. Trends, outcomes, and predictors of open and conversion to open cholecystectomy in Veterans Health Administration hospitals. Am J Surg 2010; 2010:32. [4] Papandria D, Lardaro R, Rhee D, et al. Risk factors for conversion from laparoscopic to open surgery: analysis of 2,138 converted operations in the American College of Surgeons National Surgical Quality Improvement Program. Am Surg 2013;79:914. [5] Lengyel BI, Azagury D, Varban O, et al. Laparoscopic cholecystectomy after a quarter century: why do we still convert? Surg Endosc 2012;26:508. [6] Hutchinson CH, Traverso LW, Lee FT. Laparoscopic cholecystectomy. Do preoperative factors predict the need to convert to open? Surg Endosc 1994;8:875. [7] Lee NW, Collins J, Britt R, Britt LD. Evaluation for preoperative risk factors for converting laparoscopic to open cholecystectomy. Am Surg 2012;78:831. [8] Simopoulos C, Polychronidis A, Botaitis S, Perente S, Pitiakoudis M. Laparoscopic cholecystectomy in obese patients. Obes Surg 2005;15:243. [9] Farkas DT, Moradi D, Moaddel D, Nagpal K, Cosgrove JM. The impact of body mass index on outcomes after laparoscopic cholecystectomy. Surg Endosc 2012;26:964. [10] Paajanen H, Kakela P, Suuronen S, Paajanen J, Juvonen P, Pihlajamaki J. Impact of obesity and associated diseases on outcome after laparoscopic cholecystectomy. Surg Laparosc Endosc Percutan Tech 2012;22:509. [11] Wevers KP, van Westreenen HL, Patijn GA. Laparoscopic cholecystectomy in acute cholecystitis: c-reactive protein level combined with age predicts conversion. Surg Laparosc Endosc Percutan Tech 2013;23:163. [12] Cwik G, Skoczylas T, Wyroslak-Najs J, Wallner G. The value of percutaneous ultrasound in predicting conversion from laparoscopic to open cholecystectomy due to acute cholecystitis. Surg Endosc 2013;27:2561.
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[13] Kim MS, Kwon HJ, Park HW, et al. Preoperative prediction model for conversion of laparoscopic to open cholecystectomy in patient with acute cholecystitis: based on clinical, laboratory, and CT parameters. J Comput Assist Tomogr 2014;38:727. [14] Oymaci E, Ucar AD, Aydogan S, Sari E, Erkan N, Yildirim M. Evaluation of affecting factors for conversion to open cholecystectomy in acute cholecystitis. Prz Gastroenterol 2014;9:336. [15] Rosen M, Brody F, Ponsky J. Predictive factors for conversion of laparoscopic cholecystectomy. Am J Surg 2002;184:254. [16] Sikora SS, Kumar A, Saxena R, Kapoor VK, Kaushik SP. Laparoscopic cholecystectomydcan conversion be predicted? World J Surg 1995;19:858. [17] Spaniolas K, Laycock WS, Adrales GL, Trus TL. Laparoscopic paraesophageal hernia repair: advanced age is associated with minor but not major morbidity or mortality. J Am Coll Surg 2014;218:1187. [18] Spaniolas K, Trus TL, Adrales GL, Quigley MT, Pories WJ, Laycock WS. Early morbidity and mortality of laparoscopic sleeve gastrectomy and gastric bypass in the elderly: a NSQIP analysis. Surg Obes Relat Dis 2014;10:584. [19] Sneider EB, Lewis J, Friedrich A, et al. Timing and choice of intervention influences outcome in acute cholecystitis: a prospective study. Surg Laparosc Endosc Percutan Tech 2014; 24:414. [20] Saber A, Hokkam EN. Operative outcome and patient satisfaction in early and delayed laparoscopic cholecystectomy for acute cholecystitis. Minim Invasive Surg 2014;2014:162643. http://dx.doi.org/10.1155/2014/162643. [21] Brooks KR, Scarborough JE, Vaslef SN, Shapiro ML. No need to wait: an analysis of the timing of cholecystectomy during admission for acute cholecystitis using the American College of Surgeons National Surgical Quality Improvement Program database. J Trauma Acute Care Surg 2013;74:167. [22] Karamanos E, Sivrikoz E, Beale E, Chan L, Demetriades D. Effect of diabetes on outcomes in patients undergoing emergent cholecystectomy for acute cholecystitis. World J Surg 2013;37:2257. [23] Gelbard R, Karamanos E, Teixeira PG, et al. Effect of delaying same-admission cholecystectomy on outcomes in patients with diabetes. Br J Surg 2014;101:74. [24] Ingraham AM, Cohen ME, Ko CY, Hall BL. A current profile and assessment of North American cholecystectomy: results from the American College of Surgeons National Surgical Quality Improvement Program. J Am Coll Surg 2010;211:176.