Predictors of prolonged laparoscopic cholecystectomy in the treatment of low‐grade acute cholecystitis: a single‐center, retrospective, observational study

Abstract

Aim

Laparoscopic cholecystectomy is frequently used to treat low‐grade acute cholecystitis. Improvements in technical skills have reduced the rate of conversion from laparoscopic to open surgery. In this study, we sought to identify factors that might predict the surgical time of laparoscopic cholecystectomy as possible markers for surgical difficulty.

Methods

We carried out a single‐center retrospective analysis of a Japanese medical insurance database. Data were retrieved for 87 patients with acute cholecystitis. The analyzed factors included age, sex, body mass index, medical history, blood laboratory data, computed tomography findings, and time from disease onset to surgery. Multiple regression analysis was used to identify factors associated with surgical time.

Results

Edema of the gallbladder wall on computed tomography, neutrophil sequestration, body mass index, and history of acute cholangitis were significantly associated with surgical time (P = 0.014, 0.027, 0.043, and 0.047, respectively). The conversion rate from laparoscopic surgery to open surgery was 2%.

Conclusions

Our results suggest that edema of the gallbladder wall on computed tomography, neutrophil sequestration, body mass index, and history of acute cholangitis are associated with surgical time of laparoscopic cholecystectomy in the treatment of acute cholecystitis in our hospital.

Introduction

Early laparoscopic cholecystectomy is widely accepted as one of the main strategies for treating acute cholecystitis. Although there are some difficulties associated with early laparoscopic cholecystectomy, recent improvements in surgical techniques have decreased the rate of conversion to open surgery. Percutaneous cholecystostomy is another option for severe cases of acute cholecystitis, and provides a bridge to second‐line surgery.

In our hospital, laparoscopic cholecystectomy is indicated for grade 1–2 acute cholecystitis, as defined using the Tokyo guidelines.1 In recent years, a few cases required conversion from laparoscopic to open surgery without an increased incidence of postoperative complications, although the surgical time tended to be longer than that in cases without conversion. Considering the technical skills of the surgeons, the causes of complications and/or conversion to open surgery are unlikely to be the only predictors of the technical difficulty of performing laparoscopic cholecystectomy.

In the present study, we used surgical time as a marker for surgical difficulty, and we sought to identify preoperative factors that might predict laparoscopic cholecystectomy surgical time in the treatment of acute cholecystitis in our hospital. Our hospital uses established laparoscopic procedures and rarely experiences complications and/or conversion to open surgery. Multivariate analysis was used to identify which predictors were independently associated with surgical time of laparoscopic cholecystectomy as markers for the difficulty of carrying out this surgical procedure.

Methods

Study design

We carried out a retrospective, single‐center observational study of patients included in a Japanese public insurance diagnosis procedure combination (DPC) database. Patients with acute cholecystitis who underwent laparoscopic cholecystectomy at our hospital between April 2008 and March 2012 were identified using the DPC.

Patients and treatments

Using the database, we identified 114 patients with acute cholecystitis. Of these, 87 (76%) patients underwent emergency laparoscopic cholecystectomy and were included in this study. All of the patients had right upper abdominal pain together with fever or increased inflammatory markers (white blood cell [WBC] count or C‐reactive protein [CRP]), which were suggestive of acute cholecystitis after excluding other possible diagnoses.1 Laparoscopic cholecystectomy was carried out in patients with grade 1–2 acute cholecystitis. Percutaneous cholecystostomy or open cholecystectomy were carried out in patients with grade 3 acute cholecystitis based on the presence of multiple organ dysfunction, emphysematous cholecystitis, or torsion, for example.

Assessments

The following variables that were recorded on the day of emergency surgery were retrieved from the DPC and clinical records: age, sex, body mass index (BMI), medical history (acute cholangitis, diabetes mellitus, and liver cirrhosis), laboratory data (WBC count, neutrophil sequestration, CRP, total bilirubin, aspartate aminotransferase [AST], and alanine aminotransferase [ALT]), multislice computed tomography (CT) findings described in the radiologist's report (gallstones, tense gallbladder [short axis diameter >5 cm], edema of the gallbladder wall, and ascites), laparoscopic cholecystectomy (time from onset to operation, conversion to open surgery, and surgical time), and length of hospital stay.

Statistical analyses

Statistical analyses were carried out using spss software version 16.0 (SPSS, Chicago, IL, USA). In the present study, surgical time was treated as objective variable. Age, sex, BMI, medical history, laboratory data, and multislice CT findings were included as explanatory variables. Categorical variables (sex, medical histories, and CT findings) were coded binary (0, 1) to make dummy variables. Multiple regression analysis was treated as multivariate analysis to explore factors that were significantly and independently associated with surgical time. The multiple regression analysis was carried out in two ways, with or without stepwise method. The calculated regression coefficient and standard regression coefficient are shown in Table 1. In the present study, a stepwise method was used to include or exclude variables into the model at the cut‐off P‐value of 0.10. The threshold for statistical significance was set at P = 0.05.

Table 1.

Patient characteristics and results of multiple regression analysis for surgical time in patients with acute cholecystitis who underwent laparoscopic cholecystectomy (n = 87)

Variable	Value	P‐value	Regression coefficient (95% CI)	Standard regression coefficient
n	87
Age, years	69 (60–79)	0.458	−0.285 (−1.047–0.478)	−0.092
Sex, males	58 (67%)	0.712	4.469 (−19.596–28.533)	0.045
Height, cm	160 (153–166)
Weight, kg	57 (52–66)
BMI (kg/m2)	23 (21–25)	0.106	2.146 (−0.469–4.761)
Medical history, yes
Acute cholangitis	9 (10%)	0.103	29.237 (−6.031–64.505)	0.189
Diabetes mellitus	15 (17%)	0.557	9.789 (−23.329–42.908)	0.079
Liver cirrhosis	4 (5%)	0.182	−35.484 (−88.011–17.042)	−0.158
Laboratory data
WBC count, /mm3	11,300 (8,360–15,400)	0.422	−0.001 (−0.004–0.002)	−0.117
Neutrophil sequestration, %	82.3 (74.3–87.3)	0.123	0.740 (−0.207–1.687)	0.195
CRP, mg/dL	1.6 (0.3–13.3)	0.739	−0.188 (−1.311–0.935)	−0.044
Total bilirubin, mg/dL	1.1 (0.7–1.8)	0.171	8.202 (−3.617–20.020)	0.251
AST, IU/L	28 (21–57)	0.634	−0.054 (−0.278–0.171)	−0.106
ALT, IU/L	29 (16–49)	0.097	−0.160 (−0.350–0.030)	−0.358
Multislice CT findings
Gallstones	74 (85%)	0.772	−4.358 (−34.307–25.590)	−0.032
Distension of the gallbladder	69 (79%)	0.643	7.074 (−23.205–37.353)	0.061
Edema of the gallbladder wall	73 (84%)	0.060	28.171 (−1.258–57.601)	0.220
Ascites	8 (9%)	0.154	30.478 (−11.745–72.701)	0.187
Surgical outcomes
Time from onset to surgery, days	3 (2–6)	0.353	1.088 (−1.232–3.408)	0.140
Conversion from laparoscopic to open surgery	2 (2%)
Surgical time, min	118 (90–156)
Duration of hospital stay, days	13 (10–18)

Values are n (%) or median (interquartile range), all regression coefficients are for surgical time. ALT, alanine aminotransferase; AST, aspartate aminotransferase; BMI, body mass index; CI, confidential interval; CRP, C‐reactive protein; CT, computed tomography; WBC, white blood cells.

Results

The characteristics of the 87 patients are summarized in Table 1. The median age was 69 years, 67% of the patients were male, the median BMI was 23 kg/m², and 10% had a medical history of acute cholangitis. The median WBC count, neutrophil sequestration rate, CRP level, total bilirubin level, AST level, and ALT level were 11,300/mm³, 82.3%, 1.6 mg/dL, 1.1 mg/dL, 28 IU/L, and 29 IU/L, respectively. Multislice CT images revealed gallstones in 85% of the patients, distention of the gallbladder in 79%, edema of the gallbladder wall in 84%, and ascites in 9%. The median duration of hospital stay was 13 days. The time from onset to surgery was 3 days. Conversion from laparoscopic surgery to open surgery was necessary in 2% of patients. The median surgical time was 118 min. There were no episodes of postoperative bleeding or biliary leakage as complications, confirming that emergency surgery was carried out in patients with grade 1–2 acute cholecystitis. In addition, the results of multiple regression analysis for surgical time are shown in Table 1, which were calculated by all explanatory variables. There was no significant explanatory variable.

Table 2 shows the results of multiple regression analysis with stepwise method for surgical time as the dependent variable. Edema of the gallbladder wall on CT, neutrophil sequestration, BMI, and history of acute cholangitis were significantly associated with operation time (P = 0.014, 0.027, 0.043, and 0.047, respectively).

Table 2.

Results of multiple regression analysis with stepwise method for surgical time in patients with acute cholecystitis who underwent laparoscopic cholecystectomy (n = 87)

Variable	P‐value	Regression coefficient (95% CI)	Standard regression coefficient	t	VIF
Edema of GB wall on CT	0.014	32.278 (6.798–57.757)	0.252	2.521	1.024
Neutrophil sequestration	0.027	0.873 (0.104–1.642)	0.230	2.260	1.067
Body mass index	0.043	2.386 (0.079–4.694)	0.210	2.058	1.066
History of acute cholangitis	0.047	31.030 (0.414–61.647)	0.218	2.017	1.016
Alanine aminotransferase	0.064	−0.084 (−0.173–0.005)	−0.208	−1.879	1.025
R2 = 0.171, F = 4.516	0.001

The following explanatory variables were entered into the model using the stepwise method: age, sex, body mass index, medical history (acute cholangitis, diabetes mellitus, and liver cirrhosis), laboratory data (white blood cell count, neutrophil sequestration, C‐reactive protein level, total bilirubin level, aspartate aminotransferase level, and alanine aminotransferase level), computed tomography (CT) findings (gallstones, distension of the gallbladder [GB], edema of the GB wall, and ascites), and time from onset to surgery. CI, confidential interval; VIF, variance inflation factor.

Discussion

Laparoscopic cholecystectomy is a common strategy for treating acute cholecystitis without increasing the risk of complications as compared with open surgery. Recent improvements in laparoscopic surgical techniques have also helped to decrease the rate of conversion to open surgery. Therefore, the difficulty of laparoscopic cholecystectomy should not only be assessed in terms of the rate of conversion to open surgery. In fact, the conversion rate in the present study was just 2%, which is much lower than that in a recent report describing the surgical outcomes of all grade acute cholecystitis (11.4%) in Belgium.2 The low rate of conversion in our study might be due to the inclusion of patients with low‐grade acute cholecystitis. However, the mean surgical time in our study (126 min) was longer than that in the Belgian study (86 min).

In the present study, we focused on surgical time as a possible marker for the difficulty of laparoscopic cholecystectomy. We found that edema of the gallbladder wall on CT (P = 0.014), neutrophil sequestration (P = 0.027), BMI (P = 0.043), and history of acute cholangitis (P = 0.047) were significant predictors for prolonged laparoscopic cholecystectomy. Although edema of the gallbladder wall is a common CT finding of acute cholecystitis, it was reported that CT sometimes misses edema of the gallbladder wall,3 because evidence of wall edema is sometimes observed intraoperatively in the absence of relevant CT findings. Therefore, the presence of gallbladder wall edema on CT images may suggest the presence of severe inflammation, which may prolong surgical time. Neutrophil sequestration is also associated with severe inflammation, which could increase the difficulty of the operation. Body mass index is an established risk factor for adverse outcomes after open surgery and laparoscopic surgery.4 History of acute cholangitis was also identified as an independent risk factor, and may be related to procedures involving the cystic duct and arteries.

Earlier studies identified several risk factors associated with the difficulty of carrying out laparoscopic cholecystectomy for acute cholecystitis. Several studies have focused on the risk factors for conversion from laparoscopic to open surgery; these risk factors included male sex, age > 65 years, BMI > 25 kg/m², history of biliary disease, a non‐palpable gallbladder, WBC count > 13,000/mm³, gangrenous cholecystitis, and the absence of gallbladder wall enhancement on CT and/or the presence of gallstones in the gallbladder infundibulum on CT.5, 6, 7 Although we focused on prolonged surgical time in the present study, we identified similar risk factors for this outcome to those observed in prior studies. In other words, although the conversion rate was low (2%), risk factors that were previously reported to be associated with conversion to open surgery were also associated with prolonged surgical time.

Several studies have shown that an early indication for laparoscopic cholecystectomy to treat acute cholecystitis has some clinical benefits. In particular, laparoscopic cholecystectomy within 72 h after onset was associated with a lower rate of conversion to open surgery, shorter surgical time, reduced cost, and shorter convalescence time.8 Laparoscopic cholecystectomy within 48 h was associated with a lower conversion/repeat surgery rate, lower incidence of postoperative complications, and shorter postoperative hospital stay.9 However, there were no differences in the mortality rate, surgical time, duration of hospital stay, or incidence of complications, except for the rate of conversion from laparoscopic to open surgery.10, 11 In the present study, the median time from onset to surgery was 3 days, which is not compatible with early surgery. However, in our study, the time from disease onset to diagnosis was not a risk factor for prolonged surgical time, and the conversion rate was low (2%). In addition, emergency laparoscopic cholecystectomy was basically carried out within 24 h of hospital admission, therefore, all cases received only one or two antibiotic infusions before operation. Furthermore, no patient received percutaneous transhepatic gallbladder drainage (PTGBD).

Although our laparoscopic cholecystectomy data showed a low conversion rate (2%), the median surgical time was approximately 120 min; however, median time from onset to surgery was 3 days. Nevertheless, almost all cases underwent surgery on admission day. Therefore, our data reflected the outcome of laparoscopic cholecystectomy for acute cholecystitis (at least 3 days from onset) without conversion. If the priority of laparoscopic cholecystectomy was avoidance open surgery, the operation difficulty might be decided by the degree of inflammation (CT finding and blood marker), adhesion of cystic duct (past history of cholangitis), and BMI, from our data.

Several recent studies have described the benefits of preoperative PTGBD, including a lower rate of complications, shorter surgical time, and shorter hospital stay.12, 13 Several studies have also attempted to assess the outcomes of PTGBD for acute cholecystitis.14, 15 According to the outcome of these ongoing PTGBD studies in the future, if surgical difficulty was predicted, laparoscopic cholecystectomy for acute cholecystitis might have to be reconsidered, and PTGBD could be better choice in some cases. However, this discussion will be addressed in future studies.

Our study has some limitations. First, although the result of R² was significant (P = 0.001), the value of R² was not high (R² = 0.171). Second, the rate of conversion was low, which means that very few of the patients were contraindicated for prolonged laparoscopic surgery. Third, the total surgical time was long because most of the patients underwent complete laparoscopic surgery. Fourth, seven surgeons carried out the surgical procedures in the present study and their skills were not assessed, although none were surgical residents. Thus, our preference for complete laparoscopic surgery possibly introduced some bias into our results.

In the present study, we have identified several risk factors for surgical time of laparoscopic cholecystectomy for treating acute cholecystitis. We think that other treatment options, including conservative therapy or PTGBD, should be considered for patients deemed unsuitable for prolonged laparoscopic surgery and patients with any of the risk factors identified in this study. Although laparoscopic surgery is a less invasive treatment strategy, continued evaluation of the risk factors seems to be necessary to identify patients suitable for laparoscopic surgery.

Conclusion

In this single‐center, retrospective, observational study, we found that edema of the gallbladder wall on CT, neutrophil sequestration, BMI, and history of acute cholangitis were risk factors for longer operation time. Because the rate of conversion from laparoscopic surgery to open cholecystectomy has decreased substantially in recent years, these factors may help surgeons to predict possible surgical difficulties.

Conflict of Interest

None.