Author Affiliations: Department of General Surgery (Karakayali FY, Akdur A, Kirnap M, Ekici Y and Moray G), and Department of Radiology (Harman A), Baskent University School of Medicine, Ankara, Turkey

Corresponding Author: Feza Y Karakayali, MD, Department of General Surgery, Baskent University School of Medicine, Ankara, Turkey (Tel: 90-532-6455407; Fax: 90-532-6455312; Email: fezaykar@yahoo.com)

 

© 2014, Hepatobiliary Pancreat Dis Int. All rights reserved.

doi: 10.1016/S1499-3872(14)60045-X

Published online March 27, 2014.

 

Contributors: KFY proposed the study. AA and KM collected and analyzed the data. KFY wrote the first draft. KFY, EY and MG performed the operations. HA performed the percutaneous cholecystostomy procedures. All authors contributed to the study design, interpretation of study and writing the manuscript. KFY is the guarantor.

Funding: None.

Ethical approval: The study protocol was approved by the Institutional Review Board of Baskent University.

Competing interest: No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article.

BACKGROUND: In low-risk patients with acute cholecystitis who did not respond to nonoperative treatment, we prospectively compared treatment with emergency laparoscopic cholecystectomy or percutaneous transhepatic cholecystostomy followed by delayed cholecystectomy.

 

METHODS: In 91 patients (American Society of Anesthesiologists class I or II) who had symptoms of acute cholecystitis ≥72 hours at hospital admission and who did not respond to nonoperative treatment (48 hours), 48 patients were treated with emergency laparoscopic cholecystectomy and 43 patients were treated with delayed cholecystectomy at ≥4 weeks after insertion of a percutaneous transhepatic cholecystostomy catheter. After initial treatment, the patients were followed up for 23 months on average (range 7-29).

 

RESULT: Compared with the patients who had emergency laparoscopic cholecystectomy, the patients who were treated with percutaneous transhepatic cholecystostomy and delayed cholecystectomy had a lower frequency of conversion to open surgery [19 (40%) vs 8 (19%); P=0.029], a frequency of intraoperative bleeding ≥100 mL [16 (33%) vs 4 (9%); P=0.006], a mean postoperative hospital stay (5.3±3.3 vs 3.0±2.4 days; P=0.001), and a frequency of complications [17 (35%) vs 4 (9%); P=0.003].

 

CONCLUSION: In patients with acute cholecystitis who presented to the hospital ≥72 hours after symptom onset and did not respond to nonoperative treatment for 48 hours, percutaneous transhepatic cholecystostomy with delayed laparoscopic cholecystectomy produced better outcomes and fewer complications than emergency laparoscopic cholecystectomy.

 

(Hepatobiliary Pancreat Dis Int 2014;13:316-322)

 

KEY WORDS: acute abdomen; acute cholecystitis; complications; laparoscopy; surgery; biliary tract

Acute cholecystitis is commonly treated with laparoscopic cholecystectomy, which has a surgical mortality of less than 0.8%.^[1] Acute cholecystitis was considered a contraindication for laparoscopic cholecystectomy because of frequent complications, but results may have improved because of increased laparoscopic experience and improvements in laparoscopic instruments.^{[2, 3]} A meta-analysis of 10 prospective, randomized trials concluded that patients who had emergency laparoscopic cholecystectomy (24 to 96 hours after onset of symptoms) had a shorter hospital stay and a similar frequency of complications compared with those who had open cholecystectomy.^[4]

 

The Tokyo guidelines of the Japanese Society of Hepato-Biliary-Pancreatic Surgery include diagnostic criteria, therapeutic strategies, and clinical flowcharts for acute cholangitis and cholecystitis.^[5] The severity of acute cholecystitis is graded as mild (grade I), moderate (grade II), or severe (grade III), and surgical treatment options vary with grade. Emergency cholecystectomy is indicated for patients with symptoms >72 hours (grade II), and patients with grade II concomitant local severe inflammation may be treated with emergency or urgent gallbladder drainage, medical treatment, and delayed cholecystectomy.^[5]

 

Laparoscopic cholecystectomy may be recommended at 6 to 12 weeks after the onset of symptoms.^[6-10] In patients with acute cholecystitis, laparoscopic cholecystectomy is technically feasible and safe within 72 to 96 hours after the onset of symptoms.^[10-14] Within 72 hours after the onset of symptoms and before the development of fibrosis, laparoscopic cholecystectomy may be a safe procedure because the anatomy usually is clear and dissection may be guided by edema.^{[15, 16]} For patients who are admitted more than 72 hours after the onset of symptoms, however, treatment is controversial and results are unclear. Laparoscopic cholecystectomy 72 hours after the onset of symptoms may be difficult and the risk of complications may increase.^[17] However, some studies^[18-21] showed no difference in frequency of conversion to open surgery, morbidity, or length of postoperative hospital stay between patients with symptoms more or less than 72 hours.

 

Many patients with acute cholecystitis may not respond to nonoperative treatment but require urgent surgery to avoid gallbladder gangrene or perforation. In this situation, laparoscopic surgery may have limited safety and a high-risk of complications, and such patients may need conversion to open cholecystectomy.^[22-24] Most patients with acute cholecystitis more than 72 hours may have severe inflammation and dense adhesions that increase the risk of complications of laparoscopic cholecystectomy and conversion to open surgery. Therefore, these patients are frequently treated nonoperatively, discharged from the hospital when the acute attack has subsided, and treated with cholecystectomy 4 to 8 weeks later.^[25-27] Conversion from laparoscopic to open surgery is associated with more surgical complications than laparoscopic surgery alone.^[28]

 

Percutaneous transhepatic cholecystostomy is a treatment option for patients with acute cholecystitis.^[29] This minimally invasive procedure guided by imaging methods is an alternative treatment for patients with acute or complicated cholecystitis, who require urgent treatment.^[30] This procedure could help critically ill and complex patients to recover from the acute episode before delayed elective laparoscopic cholecystectomy is performed. Despite the use of percutaneous cholecystostomy in high-risk patients with acute cholecystitis, other indications for this procedure are not clear. Although emergency laparoscopic cholecystectomy is suitable for surgery low-risk patients without response to nonoperative treatment, percutaneous transhepatic cholecystostomy is preferred in some centers.

 

Literature search showed no prospective studies evaluating preferred treatment for low-risk patients with acute cholecystitis who had no response to nonoperative treatment. The present study was undertaken to compare emergency laparoscopic cholecystectomy and percutaneous transhepatic cholecystostomy followed by delayed laparoscopic cholecystectomy in patients with low-risk acute cholecystitis who had no response to nonoperative treatment.

 

 

From May 2007 to September 2012, a total of 1814 patients were admitted to our surgery department because of their clinical, radiographic, and laboratory findings of calculous cholecystitis. Acute cholecystitis was diagnosed by the clinical criteria including local (Murphy sign or right upper quadrant mass, pain, or tenderness) and systemic (fever, elevated C-reactive protein, or elevated white blood cell count) signs of inflammation in addition to imaging findings. Emergency laparoscopic cholecystectomy was recommended for patients with symptoms at 0 to 72 hours before admission and was not included in this study.

 

In 369 patients (20%) with symptoms which appeared more than 72 hours before admission, recommended nonoperative treatment included fasting, use of ceftriaxone, a third generation broad spectrum antibiotic, intravenous anti-inflammatory drugs, and intravenous fluids. After 48 hours of nonoperative treatment, symptoms persisted or worsened in 122 patients (33%), and radiographic evaluation was repeated (ultrasonography in all patients; computed tomography in 12 patients who had inconclusive ultrasonographic studies). Thirty-one patients were excluded because of high surgical risk [American Society of Anesthesiologists (ASA) class III to V] or severe comorbidity (chronic obstructive pulmonary disease, ischemic heart disease, cerebrovascular disease, cancer, age >80 years, previous abdominal surgery, choledocholithiasis, acute cholangitis, pancreatitis, free biliary perforation, or intra-abdominal abscess). The remaining 91 patients were included in the study (Fig. 1). The study protocol was approved by the Institutional Review Board of Baskent University, and informed consent was obtained from all patients.

 

The 91 patients were consecutively allocated to two treatment groups: one for emergency laparoscopic cholecystectomy (48 patients) and the other for percutaneous transhepatic cholecystostomy with delayed laparoscopic cholecystectomy from 4 to 8 weeks after cholecystostomy (43 patients) (Fig. 1). The patients were allowed to change assigned treatment based on their preference. Patients in both groups were followed up after treatment for an average of 23 months (range 7-29).

 

Laparoscopic cholecystectomy was performed by two qualified surgeons using a 4-port method. The decisions to convert to open cholecystectomy or use abdominal drains were made according to the clinical factors including the difficulty of dissection, poor control of intraoperative hemorrhage, and adhesions of the Calot triangle and the liver bed. The difficulty in dissecting the Calot triangle was assessed according to an adhesion scoring system previously described (presence of adhesions, 1; absence of adhesions, 0).^[31]

 

A percutaneous transhepatic cholecystostomy was performed by a specialized interventional radiology team under the ultrasonographic guidance, with or without fluoroscopy, in the interventional radiology unit. The gallbladder fundus was visualized with ultrasonography and accessed from a transhepatic approach with an 18-gauge needle. The needle was advanced to avoid puncturing the anterior wall of the gallbladder. Bile samples were taken from all patients for anaerobic and aerobic cultures. After placing a guidewire (Amplatz Super Stiff Guide Wire, Boston Scientific Corp, Natick, MA, USA) and sequentially dilating the track, an 8- to 10-French lockable, all purpose, pigtail catheter was introduced into the gallbladder. A small volume of contrast agent was injected and fluoroscopy was used to confirm the position of the catheter and determine the patency of the biliary ductal system. The catheter was secured to the abdominal wall with 2-0 silk sutures at the puncture site and allowed to drain with gravity. At 24 hours after placement, the position of the catheter was checked with ultrasonography or fluoroscopy with water-soluble contrast solution injection.

 

Clinical improvement after percutaneous transhepatic cholecystostomy was defined as (1) resolution of pain or tenderness of the right upper quadrant, (2) body temperature ≤37.5 �� during a 24-hour period, and (3) resolution of leukocytosis. After the patient was discharged from the hospital, the catheter was monitored twice weekly at the outpatient surgery clinic. Transcatheter cholangiography was performed 2 weeks after the percutaneous transhepatic cholecystostomy. In patients with obstruction of the cystic duct, a percutaneous transhepatic cholecystostomy catheter was left open until delayed cholecystectomy was performed; in patients with a patent cystic duct, the catheter was left in place, closed, and secured under wound dressings. All patients had laparoscopic cholecystectomy at less than 4 weeks after discharge from the hospital.

 

Data analysis was performed with statistical software (SPSS 15.0, SPSS Inc., Chicago, IL, USA). Quantitative data were analyzed with the Mann-Whitney U test. Proportions were compared using the Chi-square test. A P<0.05 was considered statistically significant.

 

 

The mean age of the patients was lower in the emergency laparoscopic cholecystectomy group than in the percutaneous transhepatic cholecystostomy and delayed cholecystectomy group (Table 1). The two groups were similar in gender, ASA class, time from the onset of symptoms to admission, temperature, white blood cell count, C-reactive protein level, and radiographic findings (Table 1).

 

Percutaneous transhepatic cholecystostomy was technically successful in all 43 patients without any early complications. In two patients with abscess of the gallbladder bed, drainage of the abscess was observed on imaging studies when the gallbladder was aspirated with the percutaneous transhepatic cholecystostomy catheter; in another patient who did not have communication between the abscess and gallbladder, an additional percutaneous transhepatic aspiration was performed. After percutaneous transhepatic cholecystostomy placement, 40 patients (93%) had early resolution of cholecystitis symptoms (within 24 hours), and the 3 patients with pericholecystic abscess had improvement within 48 hours. All of the 43 patients were discharged after complete resolution of symptoms, and the mean time from percutaneous transhepatic cholecystostomy to discharge was 4.7±2.0 days (range 3-11).

 

During follow-up, bile leak around the cholecystostomy catheter was observed in two patients and was treated with repeat catheterization with a larger catheter. Two weeks after the placement of the percutaneous transhepatic cholecystostomy catheter, all patients underwent cholangiography; in 9 patients (21%) the cystic duct was obstructed, and the cholecystostomy catheter was left open until surgery (Fig. 2). Although there were no clinical symptoms, common bile duct stones were observed by cholangiography in 3 patients; these stones were successfully removed by endoscopic retrograde cholangiopancreatography and sphincterotomy before the operation. In all patients, laparoscopic cholecystectomy was performed at an average of 5 weeks (range 4-7) after percutaneous transhepatic cholecystostomy.

 

Conversion from laparoscopic to open surgery (most commonly because of difficulty with dissection at the gallbladder and Calot triangle) was significantly more frequent in patients who were treated with emergency laparoscopic cholecystectomy than cholecystostomy and delayed cholecystectomy (40% vs 19%; P=0.029). In 19 of the 48 emergency laparoscopic cholecystectomy patients, conversion to open surgery decision was realized because of difficulty with dissection(15 patients) and uncontrolled bleeding (4) (Table 2). Intraoperative bleeding ≥100 mL was also more frequent in patients undergoing emergency laparoscopic cholecystectomy than in those having cholecystostomy and delayed cholecystectomy (33% vs 9%; P=0.006); bleeding was stopped in most patients undergoing hemostatic laparoscopic procedures without open surgery (Table 2). Intraoperative cholangiography was required in several patients because of difficulty in evaluating the anatomy of Calot triangle after conversion to open surgery (Table 2). Abdominal drains were used in each complicated operation that had intraoperative bleeding, difficulty with dissection, or bile leakage from the gallbladder bed. Patients who had had emergency laparoscopic cholecystectomy had more frequent use of abdominal drains and longer postoperative hospital stay than those who had had initial treatment with percutaneous transhepatic cholecystostomy (Table 2).

 

There were no patients with bile duct injury or deaths. Overall postoperative complications were more frequent in patients undergoing emergency laparoscopic cholecystectomy, and the most frequent complications were bile leakage and subhepatic fluid collection (Table 2). In 6 patients with bile leakage (5 in the emergency laparoscopic cholecystectomy group and 1 in the percutaneous transhepatic cholecystostomy and delayed laparoscopic cholecystectomy group), the diagnosis was made by CT or the drainage results from the drain placed at surgery. Endoscopic retrograde cholangiopancreatography was performed in all 6 patients. Cystic duct stump leakage was found in 5 of them (the emergency laparoscopic cholecystectomy group) and was treated with sphincterotomy and either stenting (3 patients) or stone extraction (2). Bile leakage caused by an open duct of Luschka was observed in one patient who underwent percutaneous transhepatic cholecystostomy and delayed cholecystectomy, and treatment included sphincterotomy and percutaneous drainage of biloma. In 6 patients with postoperative abdominal subhepatic fluid collection (Table 2), 5 recovered spontaneously and one had percutaneous drainage of the biloma. On the long-term follow-up, choledocholithiasis was diagnosed with magnetic resonance cholangiopancreatography in one patient at 9 months after emergency laparoscopic cholecystectomy. Treatment of this patient included hospital admission, endoscopic retrograde cholangiopancreatography, and stone extraction.

 

 

In the present study, patients with persistent symptoms and signs of acute cholecystitis after nonoperative treatment (48 hours) had better clinical outcomes in the percutaneous transhepatic cholecystostomy and delayed cholecystectomy group than in the emergency laparoscopic cholecystectomy group.

 

Initial nonoperative treatment was unsuccessful in 122 (33%) of 369 patients, which was similar to previous studies (32%).^[24] Treatment for these patients is commonly based on the general condition of the patients (ASA class), and includes emergency surgery for low-risk patients and percutaneous transhepatic cholecystostomy for high-risk patients. Urgent or early drainage may be recommended for patients with acute cholecystitis defined by leukocytosis (white blood cell count >18×10⁹/L); painful and palpable mass at the right upper quadrant; and symptoms >72 hours or marked local inflammation (8 mm gallbladder wall thickness).^[5] We defined 72 hours as the minimum duration of symptoms for inclusion in the study and prospectively evaluated the results of treatment in low-risk patients with acute cholecystitis.

 

In patients with acute cholecystitis who did not respond to nonoperative treatment, the results of treatment with emergency laparoscopic cholecystectomy or percutaneous transhepatic cholecystostomy followed by delayed laparoscopic cholecystectomy are similar for low-risk (ASA I) patients, but the conversion rate to open surgery is significantly higher for high-risk (ASA II or III) patients who are treated with emergency laparoscopic cholecystectomy.^[22] However, controversial findings have also been reported that percutaneous transhepatic cholecystostomy had a higher frequency of conversion to open surgery and the shorter operative time or shorter postoperative hospital stay than emergency cholecystectomy did.^[32]

 

We observed a shorter mean postoperative hospital stay, a lower frequency of complications, and a lower frequency of conversion to open surgery in patients treated initially with percutaneous transhepatic cholecystostomy than in those treated with emergency laparoscopic cholecystectomy. Therefore, elective delayed surgery after percutaneous transhepatic cholecystostomy may produce better outcomes. Although the present study was performed at a tertiary care university hospital and the operations were performed by experienced hepatobiliary and liver transplant surgeons, the frequency of conversion to open surgery after emergency laparoscopic cholecystectomy (40%) was higher than that reported (11%-28%).^{[10, 23, 33]} This may be due to the differences in timing of emergency laparoscopic cholecystectomy and disease severity between studies. In the patients who were treated with emergency laparoscopic cholecystectomy, the mean time between the onset of symptoms and admission to the hospital was 5 days and the duration of failed nonoperative treatment was 2 days. Our results were in consistent with those of another study showing a similar high frequency of conversion to open surgery (31%) in patients operated upon 7 days after the onset of symptoms.^[14]

 

We did not find major perioperative complications or bile duct injuries, but the overall frequency of complications was significantly higher in patients undergoing emergency laparoscopic cholecystectomy. The most common complication, bile leakage from the cystic duct stump, was likely caused by slipped surgical clips because of retained common bile duct stones, or resolution of inflammation. In 3 patients who underwent emergency laparoscopic cholecystectomy, common bile duct stones were noted early (2 patients) or late (1) after surgery. Early diagnosed retained common bile duct stones were a major cause of bile leakage. However, in patients treated with percutaneous transhepatic cholecystostomy, choledocholithiasis was noted in 3 patients on cholangiography before delayed laparoscopic cholecystectomy; in these patients, the percutaneous transhepatic cholecystostomy enabled elective extraction of common bile duct stones before surgery and avoided perioperative cholangiography and common bile duct exploration. In a study,^[25] percutaneous transhepatic cholecystostomy was used for cholangiography in 12 of 54 patients with persistently elevated levels of liver enzyme, and common bile duct stones were observed in 5 patients.

 

The timing of delayed laparoscopic cholecystectomy after percutaneous transhepatic cholecystostomy is controversial. Patients treated with laparoscopic cholecystectomy within 72 hours after percutaneous transhepatic cholecystostomy may have a shorter mean hospital stay and lower hospital costs than those who underwent laparoscopic cholecystectomy more than 72 hours after percutaneous transhepatic cholecystostomy, but the latter subjects may have a lower frequency of complications and a shorter operative time.^[33] We scheduled laparoscopic cholecystectomy over 4 weeks after percutaneous transhepatic cholecystostomy to avoid marked inflammation that appeared commonly before 4 weeks. Another controversial issue is whether the cholecystostomy catheter should be removed during or before delayed laparoscopic cholecystectomy. In the present study, we did not remove the catheter until delayed laparoscopic cholecystectomy was done to decrease the risk of recurrent acute cholecystitis after catheter removal because of cystic duct obstruction. Besides, patients with complete relief of symptoms may postpone the scheduled operation after catheter removal, and the risk of subsequent admission because of gallstones is 50% after one year.^[34] Furthermore, tract formation may require 2-3 weeks before the catheter is removed safely. The decision about the timing of cholecystectomy after percutaneous transhepatic cholecystostomy and catheter removal may be affected by institutional policy, surgical judgment, and experience.

 

Limitations of the present study included the absence of random allocation of patients to the two study groups. After providing patients with detailed information about the treatment options and possible complications, some patients insisted on emergency laparoscopic cholecystectomy being performed and others preferred to have delayed surgery. In these situations, the patient preference was followed; otherwise, the patients were allocated consecutively to the two treatment groups.

 

In summary, there is controversy about the treatment of acute cholecystitis in patients who are admitted to the hospital over 72 hours after the onset of symptoms. In this study, nonoperative treatment was given for 48 hours, and the patients who did not respond were referred for emergency laparoscopic cholecystectomy or percutaneous transhepatic cholecystostomy and delayed laparoscopic cholecystectomy. The frequency of conversion to open surgery, intraoperative bleeding, drain use, mean postoperative hospital stay, and postoperative complications was greater in patients who underwent emergency laparoscopic cholecystectomy than in those who had percutaneous transhepatic cholecystostomy. In addition, percutaneous transhepatic cholecystostomy could make biliary system imaging before delayed cholecystectomy possible and decrease the risk of retained common bile duct stones or the need for peroperative cholangiography and common bile duct exploration. Therefore, in patients who presented to the hospital ≥72 hours after the onset of symptoms and did not respond to nonoperative therapy for 48 hours, percutaneous transhepatic cholecystostomy combined with delayed cholecystectomy could produce better outcomes and fewer complications than emergency laparoscopic cholecystectomy.

 

 

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