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AJR 2000; 174:1433-1439
© American Roentgen Ray Society


Sonography for Selecting Candidates for Laparoscopic Cholecystectomy

A Prospective Study

Hans-Peter Dinkel1,2, Simon Kraus1, Johannes Heimbucher3, Roland Moll1, Joachim Knüpffer1, Heinz-Jochen Gassel3, Stefan M. Freys3, Karl-Hermann Fuchs3 and Gerhard Schindler1

1 Department of Diagnostic Radiology. University of Würzburg, Luitpoldkrankenhaus, Josef-Schneiderstr. 2, D-97080 Würzburg, Germany
2 Present address: Institut für Diagnostische Radiologie, Inselspital, Universität Bern, Freiburgstr. 20, CH-3010 Bern, Switzerland.
3 Department of Surgery, University of Würzburg, D-97080 Würzburg, Germany.

Received February 8, 1999; accepted after revision November 1, 1999.

 
Presented in part at the annual meeting of the American Roentgen Ray Society, San Francisco, May 1998.

Address correspondence to H.-P. Dinkel.


Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
OBJECTIVE. We assessed the value of sonography in predicting intraoperative difficulties for patients undergoing laparoscopic cholecystectomy and in identifying indicators for conversion to conventional cholecystectomy.

SUBJECTS AND METHODS. Upper abdominal sonography was performed (according to a checklist) in 75 consecutive patients before laparoscopic cholecystectomy. Sonographic findings were verified by the surgeon in the operating room.

RESULTS. Conversion from laparoscopic surgery to laparotomy was performed in five patients (6.7%). Of 75 patients, 19 had sonograms revealing gallbladder wall thickening (>4 mm); surgical preparation difficulties in 16 of these patients led to laparotomy in four patients. Sensitivity, specificity, positive predictive value, and accuracy of wall thickening as an indicator of technical difficulties were 66.7%, 94.1%, 84.2%, and 85.3%, respectively. Sensitivity, specificity, positive predictive value, and accuracy of wall thickening as an indicator of surgical conversion were 80.0%, 78.6%, 21.1%, and 78.7%, respectively. Technical difficulties at laparoscopy occurred in all five patients with pericholecystic fluid on sonography (sensitivity, 20.8%; specificity, 100%; positive predictive value, 100%; accuracy, 74.7%) and led to laparotomy in three patients (sensitivity 60.0%, specificity 97.1%, positive predictive value 60%, accuracy 94.7%). The accuracy of sonography for cholecystolithiasis was 100%.

CONCLUSION. On sonography, gallbladder wall thickening is the most sensitive indicator and pericholecystic fluid is the most specific indicator of technical difficulties during laparoscopic cholecystectomy. Such difficulties may require conversion to laparotomy.


Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
In the western hemisphere, the prevalence of gallbladder stone disease is high: approximately every third woman and every fifth man are affected [1]. Although cholecystolithiasis only becomes symptomatic in about 50% of stone carriers, cholecystectomy is a common surgical procedure. Laparoscopic cholecystectomy first became popular during the late 1980s and now the procedure is considered standard [2, 3]. Conventional open cholecystectomy is still performed in patients who are not amenable to minimally invasive surgery [2, 4, 5]. Certain conditions preclude laparoscopic cholecystectomy and may lead surgeons to perform conventional open cholecystectomy, including pericholecystic adhesions and adhesions between the common bile duct, the cystic duct, and the cystic artery (Calot's triangle), which are exposed during surgery. These conditions may significantly prolong laparoscopic preparation time and may cause bleeding or gallbladder rupture. Frequently, conversion to laparotomy occurs after a patient has complications during laparoscopic cholecystectomy [2], such as rupture of the gall-bladder, significant bleeding from the gallbladder bed, or inadvertent injury to a bile duct, which may occur after the incomplete surgical exposure of Calot's traingle [4]. Surgical time and cost increases considerably in patients who must undergo conventional cholecystectomy. Therefore, candidates for laparoscopic cholecystectomy should be identified before they go to the operating room. Gallbladder wall thickening and pericholecystic fluid are indicators of cholecystitis in patients presenting with symptoms of gallstone disease. Gai and Thiele [6] reported technical difficulties in patients with gallbladder wall thicknesses more than 4 mm.

We assessed the value of sonography in predicting intraoperative difficulties for patients undergoing laparoscopic cholecystectomy and in identifying indicators for conversion to conventional cholecystectomy.


Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Seventy-five consecutive patients who underwent laparoscopic cholecystectomy during a 1-year period were included in our prospective study. All patients had a history of symptomatic cholecystolithiasis and many of them were specifically referred to our institution because it is a well-known center for laparoscopic interventions. Patients were consecutive with the exception that patients admitted and operated on during off-hours were included only when one of the radiologists involved in the study was on duty. Therefore, 11 emergency patients who underwent surgery during off-hours were not included in the study.

Patients were interviewed according to a standardized questionnaire; patients were asked about their symptoms and all other relevant medical history. Sonography was performed by four radiologists on a SI-450 scanner (Siemens, Erlangen, Germany), using 3.5-MHz and 5-MHz curved array probes. After fasting, patients were examined in the supine and the left decubitus positions. Some patients were also examined in the right decubitus, upright, or knee-elbow positions. We examined 75 patients (57 women, 18 men; age range, 19-78 years; mean age, 50.1 years).

According to a checklist, we recorded specific data about the morphology of the gallbladder; gallbladder wall; configuration of the liver bed; diameter of the intrahepatic and extrahepatic bile ducts; and presence, number, and location of stones in the gallbladder, cystic duct, intrahepatic bile ducts, and common bile duct. The diagnosis of a gallbladder stone was made when one of the following criteria was noted: circumscribed intraluminal echoic lesions with sonic shadows, circumscribed intraluminal hyperechoic lesions without sonic shadows but with gravity-induced change of position depending on posture changes, or total eclipse of the gallbladder with typical wedge-shaped shadows corresponding to a completely stone-filled contracted gallbladder (the wall-echo-shadow sign) [7]. Findings were required to be found in multiple planes. The gallbladder was considered stone-free if it could be scanned from the fundus to the proximal cystic duct, or at least to the tip of the infundibulum, without finding evidence of the aforementioned criteria. Diagnosis of a contracted gallbladder (shrunken gallbladder) was made when the organ measured less than 2 cm in diameter on repeated examinations (under fasting conditions) or when the aforementioned wall-echo-shadow sign was found. The diameter of the common bile duct was measured by positioning calipers between the (inner) common bile duct walls at the point of maximum duct thickness. Thickness of the gallbladder wall was measured orthogonally to the liver surface at the anterior wall adjacent to the liver. A transcostal approach in the anterior axillary line was selected using the liver as a sonic window if applicable. Measurements were obtained in axial and longitudinal sections relative to the gallbladder and perpendicular to the liver surface. We did not measure the free surface of the gallbladder to avoid inadvertently including the adjacent colonic wall in the measurement of gallbladder wall thickness. Multiple measurements were obtained; the minimum and maximum thicknesses were noted. Calipers were placed between the inner fluid-wall interface of the gallbladder and the gallbladder-liver interface (Fig. 1A,1B).



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Fig. 1A. —53-year-old woman with history of chronic cholecystolithiasis and acute upper abdominal pain. Transverse sonogram of gallbladder region reveals thickened (4.8 mm) gallbladder wall (arrow).

 


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Fig. 1B. —53-year-old woman with history of chronic cholecystolithiasis and acute upper abdominal pain. Longitudinal section reveals hydropic gallbladder (length, 9.4 cm; diameter, 5.1 cm). Thickening is most pronounced and focal at fundus (arrow), consistent with advanced inflammatory change. Preparation of gallbladder bed was difficult during laparoscopy because of pericholecystic adhesions of severe acute cholecystitis.

 

A gallbladder was considered hydropic when the area of its short and long axes (in centimeters) was greater than 50 cm2 (corresponding to a surface area of 50 cm2 x [{pi}/4]) in any plane of view [8]. We meticulously checked for the presence of pericholecystic fluid—small fluid collections or thin layers of fluid in or around the gallbladder wall or in the liver bed (Figs. 2A,2B,3A,3B,4A,4B). Pericholecystic fluid on sonography is suggestive of inflammatory gallbladder change in patients with acute cholecystitis. The term "pericholecystic fluid" is different than ascites or diffuse peritoneal fluid, both of which were not encountered in our patients.



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Fig. 2A. —77-year-old woman with acute right upper abdominal pain and history of cholelithiasis. Transverse sonogram of gallbladder reveals severe wall thickening (11 mm) and cholecystolithiasis.

 


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Fig. 2B. —77-year-old woman with acute right upper abdominal pain and history of cholelithiasis. Longitudinal section reveals two gallstones (diameter, 2 cm) in lumen of acutely inflamed gallbladder with wall thickening and pericholecystic fluid (arrows) in gallbladder bed. Laparoscopy was difficult because of rigid gallbladder wall.

 


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Fig. 3A. —38-year-old woman with acute right upper abdominal pain. Transverse sonogram reveals pericholecystic fluid in liver bed and Morrison's pouch (arrow) and gallbladder wall thickening (10 mm) in acute cholecystitis. Pericholecystic fluid is strong indicator of conversion to laparotomy.

 


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Fig. 3B. —38-year-old woman with acute right upper abdominal pain. Longitudinal section shows striated gallbladder wall with pericholecystic fluid (arrows).

 


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Fig. 4A. —50-year-old woman with gallbladder empyema. Intraluminal echoes with sonic shadow (calipers) in gallbladder fundus and infundibulum represent gallbladder stones. Transverse sonogram reveals gallbladder wall that cannot be completely delineated from liver boundary. Poorly delineated wall is characteristic of severe inflammation. Note pericholecystic fluid and edema in triangular zone dorsal to gallbladder (arrow).

 


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Fig. 4B. —50-year-old woman with gallbladder empyema. Intraluminal echoes with sonic shadow (calipers) in gallbladder fundus and infundibulum represent gallbladder stones. Longitudinal right upper abdomen section reveals thickened gallbladder wall with regions of increased thickness or nodularity (curved arrow) towards fundus. Note thin fluid film (short arrow) between liver surface and wall. Also note zone of increased echogenicity (long arrow) in dependent part of gallbladder with fluid level representing pus in empyema. Fluid is inhomogeneous, unlike sludge; however, no evidence of gas inclusions exists.

 

All patients underwent surgery between 2 hr and 3 days after sonography (mean, 18.5 hr). An evaluation sheet on which we recorded sonographic data, lab results, history data, and a summarizing radiologic interpretation was sent to the operating room with each patient. The operating surgeon correlated the data on the checklist with intraoperative findings immediately after surgery. Intraoperative technical difficulties were defined by a preparation time (the time after insertion of the ports needed to identify all structures in Calot's triangle and to ligate the cystic duct and the cystic artery) of more than 30 min. The decision to convert to open surgery was made by the surgeon on a patient-by-patient basis. Our policy is to change to open laparotomy when laparoscopy would expose the patient to unreasonably high surgical risks.


Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Sonographic Findings
Seventy-four of 75 patients had surgically proven gallbladder stones. The remaining patient underwent surgery because of a gallbladder polyp, which was prospectively diagnosed on sonography. In all patients, the prospective diagnosis of cholecystolithiasis was correctly made on sonography. Thus sensitivity, specificity, and accuracy of sonography with regard to cholecystolithiasis were 100%. Direct visualization of choledocholithiasis was made in one of three patients with common bile duct stones, and one of six patients with cystic duct stones. However, there was a significant correlation between gallbladder size and the presence of occlusive cystic duct stones: of five patients with gallbladder hydrops, four had a cystic duct stone. In the other two patients with cystic duct stones, gallbladder size was normal in one patient (area, 17 cm2) and borderline normal in the other (area, 45 cm2).

Initially, all patients underwent laparoscopy. In five (6.7%) patients, the procedure was converted to open cholecystectomy because of difficulty in the initial phases of laparoscopy. To minimize the risk of complications, early conversion was performed deliberately, rather than under emergency conditions. Consequently, no surgical complications occurred.

Twenty patients had ancillary sonographic findings indicating cholecystitis beyond the presence of cholecystolithiasis (Table 1), including gallbladder wall thickening (n = 19), pericholecystic fluid (n = 5), shrunken gallbladder (n = 3), possible perforation (n = 2), or empyema (n = 1). Fifteen patients had one, two patients had two, and three patients had three or more of these findings. Thirteen patients' sonograms revealed Murphy's sign.


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TABLE 1 Sonographic Predictors of Intraoperative Difficulties for Patients Undergoing Laparoscopic Cholecystectomy

 

Outcome
Of 55 patients with cholecystolithiasis or gallbladder polyps on sonography without ancillary findings, we encountered difficulties at laparoscopic preparation in eight (14.5%). Surgical preparation was time-consuming or difficult because of adhesions in four patients, rigid gallbladder in two, and intraabdominal obesity in one. In one patient (1.8%), laparoscopic cholecystectomy was switched to laparotomy because of tense pericholecystic adhesions that could not be effectively removed. This was the only patient in whom sonography failed to reveal potential indicators of conversion: empyema was not detected on sonography because wall thickening was borderline, and intraluminal hyperdensities had been prospectively interpreted as sludge. A Murphy's sign was not present.

We identified 20 patients with ancillary sonographic findings in addition to cholecystolithiasis. In 16 patients (80%), laparoscopic preparation was difficult but feasible after additional effort. However, in four patients (20%), laparoscopy was deliberately switched to open laparotomy to avoid increased surgical risks. In four (20%) of 20 patients with ancillary findings on sonography, the laparoscopic procedure went as originally planned without complications.

Gallbladder wall thickness was an important predictor of difficulties during surgical preparation and difficulty in detaching the gallbladder from its bed in the liver: in 16 (84%) of 19 patients with a gallbladder wall thickness greater than 4 mm (or in which the wall could not be discriminated clearly by sonography), we encountered surgical preparation difficulties because of the limits of laparoscopic instruments or the visualization that led to conversion in four patients. These four patients underwent open laparotomy because of the rigidity of the thickened gallbladder wall, resulting from severe acute gangrenous cholecystitis (associated with empyema in one patient and perforations in two) or chronic inflammation (in a shrunken gallbladder). A thickened gallbladder wall made it impossible for surgeons to detach the gallbladder from its bed. One patient with empyema and one patient with perforation had wall thickening, causing the confines of the gallbladder wall to be partially obscured (Fig. 4A,4B). Focal thickening or nodularity of the gallbladder wall (mostly in proximity to the fundus) was identified in 10 patients, nine of whom were difficult to operate on, including five patients with gangrenous cholecystitis, three of which underwent open laparotomy. When gallbladder wall thickness was less than or equal to 4 mm, surgical preparation was difficult in eight (14%) of 56 patients, compared with 16 (84%) of 19 patients with a wall thickness greater than 4 mm (p < 0.01). Sensitivity of wall thickening as an indicator for difficulty in surgical preparation was 66.7%, specificity 94.1%, positive predictive value 84.2%, negative predictive value 85.7%, and accuracy 85.3%. Analogously, sensitivity of wall thickening as an indicator for surgical conversion was 80.0%, specificity 78.6%, positive predictive value 21.1%, negative predictive value 98.2%, and accuracy 78.7%. Three of 75 patients had a shrunken gallbladder that led to preparatory difficulties in three and to conversion to open laparotomy in one.

We encountered more difficulties during laparoscopic preparation and converted to open surgery more often in patients with pericholecystic fluid (n = 5) than in patients without pericholecystic fluid (p < 0.01). In all five patients with fluid around the gallbladder, preparation was difficult: sensitivity of pericholecystic fluid for technical difficulties at laparoscopy was 20.8%, specificity 100.0%, positive predictive value 100.0%, negative predictive value 72.9%, and accuracy 74.7%.

In three of five patients with fluid in the gallbladder bed, open laparotomy was required. Therefore, sensitivity and positive predictive value of fluid around the gallbladder with regard to conversion were 60%, and specificity and negative predictive value were each 97.1%.

Sonography identified gallbladder perforation prospectively in both patients with surgically proven perforation. Empyema was detected in one patient and overlooked in another. In both patients, the surgical procedure was converted to laparotomy (Tables 1 and 2). In summary, in four of five patients (80%) that underwent laparotomy, sonography predicted surgical difficulties by showing gallbladder wall thickening or pericholecystic fluid. All patients (with the exception of one patient with a gallbladder polyp) had a clinical history of recent upper right abdominal pain consistent with gallstone disease. Twenty-three patients had upper right abdominal pain at presentation, two of whom had pancreatitis. Seventeen patients had acute cholecystitis, and six had severe or gangrenous cholecystitis.


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TABLE 2 Value of Findings for Patients Undergoing Laparoscopic Cholecystectomy

 

In 15 patients, we identified a painful one-finger palpation of the gallbladder during inspiration corresponding to a sonographic Murphy's sign. In 12 (80%) of these patients, laparoscopy was difficult, including two (13.3%) patients that converted to open laparotomy. Three (20%) patients had no complications.


Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 
Preoperative diagnostic procedures should support the decision process for the adequate treatment of patients with gallstone disease. We assessed the value of sonography before laparoscopic cholecystectomy. The following information is required by surgeons to plan procedures: presence, number, and size of gallbladder stones; presence of calculi in the bile duct; and signs of inflammation. Sonography is a valuable tool to help surgeons detect gallbladder stones, estimate patients' surgical risks, and suggest whether further work-up of the bile duct is required. This study corroborates the well-established high accuracy of sonography for cholecystolithiasis[9, 10].

Cystic duct stones are difficult to directly visualize [11]. In most patients, the presence of cystic duct stones can be derived only from indirect signs, such as when gallbladder hydrops occlude the cystic duct. An important question is whether it is possible to assess local operability prospectively. In our study, the conversion rate to open surgery (6.7%) was similar to other studies (0.9-14%) [2, 4, 12,13,14,15,16,17]. A study by Fuchs et al. [18] found that laparoscopy may even be advantageous for patients who are difficult to operate on. Although conversion to laparotomy alone does not worsen patients' outcome, several reasons support the preoperative assessment of the feasibility of laparoscopy. It is important to have some idea about the individual patient's risk when obtaining informed consent. Also cost-efficiency aspects should be considered because the equipment for an unsuccessful laparoscopy is expensive. Identifying potential difficulties is especially important in a teaching hospital where an open cholecystectomy has become a rare procedure [19] and requires an experienced surgeon.

Our findings suggest that patients with excessive gallbladder wall thickening and symptoms of cholelithiasis tend to have technical difficulties during laparoscopic cholecystectomy. However, gallbladder wall thickening may also result from other causes such as hypoalbuminemia [20], hepatitis [21], sclerosing cholangitis or AIDS cholangitis [22, 23], adenomyomatosis [24], congestive heart failure, portal hypertension [20, 25], or tumors. In gallstone disease, the histopathologic substrate for sonographic thickening of the gallbladder most frequently is acute or chronic pericholecystic inflammatory change. Jantsch et al. [26] reported that a thickened gallbladder wall of more than 4 mm frequently indicates acute cholecystitis. In 84% of the patients with a gallbladder wall thickening (> 4 mm) in that study, surgeons encountered surgical difficulties. Similar findings have been reported by Gai and Thiele [6]. Gallbladder wall thickness can be assessed with a margin of error ranging from 1 to 1.5 mm. In healthy patients, 97% of individuals have a gallbladder wall thickness less than 2 mm [27, 28]. In our study, a gallbladder wall thickness of more than 4 mm was significantly associated with difficult surgical preparation and with the histopathologic report of chronic or acute inflammation (Figs. 1A,1B,2A,2B,3A,3B). The inflamed gallbladder wall becomes friable and the enlarged vessels are more likely to break. Inflammation may also lead to bleeding that compromises orientation and the visual exposure at surgery, forcing surgeons to change the operative access. In patients with chronic inflammation, pericholecystic adhesions frequently impede the detachment of the gallbladder from its bed. In gallstone disease, the most frequent histopathologic substrate for sonographic thickening of the gallbladder is pericholecystic inflammatory change [4].

Pericholecystic fluid is another predictor of technical difficulties and conventional cholecystectomy. In five patients with pericholecystic fluid on sonography (Figs. 2A,2B,3A,3B,4A,4B), laparoscopic cholecystectomy preparation was difficult, leading to conventional cholecystectomy in three patients (60%). Two of these patients had gallbladder perforation and the other patient had empyema. The finding of fluid in the gallbladder bed was significantly correlated to the necessity of conventional cholecystectomy (p < 0.05). In comparison, gallbladder wall thickening was more sensitive and pericholecystic fluid more specific a parameter of technical difficulties and conversion.

The importance of common bile duct stones as a reason for conversion is diminishing because experience shows that complications increase if open bile duct revision is performed. Therefore, we recommend endoscopic bile duct clearance before and sometimes after surgery [29]. In this study, no conversion was performed because of choledocholithiasis.

The severity of acute inflammatory change influences the degree of surgical difficulty. Four of the patients that underwent open surgery had severe acute gangrenous cholecystitis. Gangrenous cholecystitis may appear with intraluminal membranes [30], irregular or nodular wall thickening [31], or layered (striated) wall thickening [32]. We did not encounter intraluminal desquamative mucosa. However, focal thickening was found in five of six patients with gangrenous cholecystitis, four with intraluminal debris, and four with a positive Murphy's sign. Focal thickening was absent in two patients with gangrenous cholecystitis, including one with perforation. Painful palpation of the gallbladder is suggestive of acute cholecystitis [33]; however, this symptom may be absent in gangrenous or perforated cholecystitis [34], as encountered in our study.

In our study, conventional cholecystectomy was performed in patients with gallbladder perforation and in patients with empyema. However, perforation and empyema are not the only absolute contraindications for laparoscopic cholecystectomy. Gai and Thiele [6] report seven patients with empyema that successfully underwent laparoscopic cholecystectomy in a series of 340 patients. However, in patients with empyema, a surgeon with extensive experience and special expertise in laparoscopic procedures is recommended.

In conclusion, meticulous preoperative diagnostic technique is mandatory for planned laparoscopic gallbladder surgery to provide information for a rational selection of the most effective treatment and to avoid intraoperative difficulty and surprise. Therefore, sonography should play a central role in surgical planning. In our study, a checklist helped us to systematically record all relevant sonographic information and to convey it to the surgeon. Gallbladder wall thickening and pericholecystic fluid on sonography are the best predictors for converting a patient from laparoscopic cholecystectomy to open cholecystectomy.


References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
 

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