Significance of ultrasonography in selecting methods for the treatment of acute cholecystitis

Abstract

Surgical removal of the gallbladder is indicated in nearly all cases of complicated acute cholecystitis. In the 1990s, laparoscopic cholecystectomy became the method of choice in the treatment of cholecystolithiasis. Due to a large inflammatory reaction in the course of acute inflammation, a laparoscopic procedure is conducted in technically difficult conditions and entails the risk of complications.

The aim of this paper

The aim of this paper was: 1) to analyze ultrasound images in acute cholecystitis; 2) to specify the most common causes of conversion from the laparoscopic method to open laparotomy; 3) to determine the degree to which the necessity for such a conversion may be predicted with the help of ultrasound examinations.

Material and methods

In 1993–2011, in the Second Department and Clinic of General, Gastroenterological and Oncological Surgery of the Medical University in Lublin, 5,596 cholecystectomies were performed including 4,105 laparoscopic procedures that constituted 73.4% of all cholecystectomies. Five hundred and forty-two patients (13.2%) were qualified for laparoscopic procedure despite manifesting typical symptoms of acute cholecystitis in ultrasound examination, which comprise: thickening of the gallbladder wall of > 3 mm, inflammatory infiltration in the Calot's triangle region, gallbladder filled with stagnated or purulent contents and mural or intramural effusion.

Results

In the group of operated patients, the conversion was necessary in 130 patients, i.e. in 24% of cases in comparison with 3.8% of patients with uncomplicated cholecystolithiasis (without the signs of inflammation). The conversion most frequently occurred when the assessment of the anatomical structures of the Calot's triangle was rendered more difficult due to local inflammatory process, mural effusion and thickening of the gallbladder wall of >5 mm. The remaining changes occurred more rarely.

Conclusions

Based on imaging scans, the most common causes of conversion included inflammatory infiltration in the Calot's triangle region, mural effusion and wall thickening to > 5 mm. The classical cholecystectomy in acute cholecystitis should be performed in patients with three major local complications detected on ultrasound examination and in those, who manifest acute clinical symptoms.

Laparoscopic cholecystectomy (LCh) is currently a safe procedure and, as most of the surgeons say, a golden standard in the management of symptomatic cholecystolithiasis^(1–3). The laparoscopic method ensures a much shorter hospitalization period and quicker recovery. The patients experience limited pain following the procedure and the cosmetic effect is incomparable to the classical cholecystectomy^(2–7). However, the role of laparoscopy in complicated cholelithiasis, particularly in the course of acute cholecystitis (ACh) still remains controversial and brings about numerous discussions^{(3, 8–10)}. A large inflammatory reaction causes difficult technical conditions for a laparoscopic procedure: gallbladder wall perforation or extensive damage of the wall may occur more frequently. The inflammatory infiltration in the region of the Calot's triangle may inhibit the accurate assessment of anatomic relationships, which, in turn, may lead to the damage of the bile duct and to severe postoperative complications^{(1, 11, 12)}. Therefore, prior to the laparoscopic procedure, patients are informed about the possibility of conversion.

On the other hand, the aforementioned complications occur more and more seldom. Recently, with growing experience of laparoscopic surgeons, acute inflammation ceased to be the unconditional limitation for LCh^{(4, 10, 13, 14)}.

In current medical publications, laparoscopic cholecystectomy is defined as a technically adequate and safe method in ACh management. The only constraints constitute the technical skills of surgeons performing the procedure and the advancement of inflammatory reaction in the wall and adjacent regions, particularly in severe and complicated cases^{(2, 3, 8, 13, 15)}. The advancement of inflammatory changes may be determined by analysing the patient's condition and laboratory parameters. However, the most important are the findings of imaging examinations, the basis of which is a preoperative transabdominal ultrasound^{(1–3, 6, 16)}. Despite currently noted positive effects of surgeries, prior to the procedure, patients with ACh are usually informed about the possibility of conversion if difficulties to assess the main anatomical structures should arise^{(6, 17, 18)}. In such a situation, conversion prevents a serious complication, i.e. iatrogenic bile duct injury.

The aim of the paper was:

1. to analyze US images in acute cholecystitis including the main measurable features;

2. to specify the most common causes of conversion from the laparoscopic method to open laparotomy with respect to the changes visualized in imaging examinations and clinical evaluation;

3. to determine in what situation and to what degree the necessity for such a conversion may be predicted with the help of US examinations.

Material and methods

In 1993–2011 in the Second Department and Clinic of General, Gastroenterological and Oncological Surgery of the Medical University in Lublin, 5,596 cholecystectomies were performed including 4,105 laparoscopic procedures that constituted 73.4% of all cholecystectomies. The major criteria for qualification to the classical or laparoscopic procedures were US findings obtained in the authors’ own laboratory directly before a planned surgery as well as a clinical picture and laboratory tests. In the aforementioned period of time, US examinations were performed with the use of the following equipment: Hitachi 410 EUB with convex probe of 3.5 MHz, Kretz 6000 and BK Medical Pro-Focus with convex probes specific for abdominal examinations of various frequencies (over the last 5 years). In US examinations, gallbladder wall was assessed including its thickness, separation by inflammatory reaction and mural echoes. Furthermore, the gallbladder contents (bile, concrements) were evaluated as well as the degree of its tension and enlargement. What is more, the tissues adjacent to the gallbladder were evaluated as well in search for free fluid or fluid cisterns. Subsequently, the neck of the gallbladder, common bile duct and arterial vessel were found and the intensity of the inflammatory infiltration within the region of the Calot's triangle was assessed (Calot's triangle – anatomical space bordered by the common hepatic duct, cystic duct and cystic artery)⁽¹⁹⁾. Additionally, the pancreas as well as the width and contents of the common bile duct were also subject to examination.

Among 4,105 patients qualified for cholecystectomy, the preoperative US examination revealed characteristic features of ACh in 542 persons (13.2%), such as wall thickening > 3 mm, gallbladder filled with stagnated or purulent contents and intramural or mural effusion. These patients were qualified for LCh. Two hundred and eighty-seven patients with ACh were qualified for classical cholecystectomy. The most common causes for abandoning the LCh method were: symptoms of peritonitis, suspicion of diffuse gangrenous cholecystitis or wall perforation and pericholecystic abscess, rapid bilirubin increase, large intensity of inflammatory changes which inhibited the interpretation of anatomical details in ultrasound examination as well as emergency procedure or lack of consent to LCh method.

In the group of 542 patients qualified to LCh with the symptoms of ACh, 187 patients (34.5%) manifested elevated bilirubin in initial tests. In the majority of cases, it was caused by the inflammatory reaction in the region of the neck of the gallbladder and Calot's triangle and was reduced upon the administration of antibiotics. Moreover, in this group, choledocholithiasis or dilatation of the CBD of > 10 mm was observed in 61 patients (11.3%). In all patients, endoscopic papillotomy was performed before the procedure. Positive results were confirmed in 50 patients who usually had LCh performed on the second day following the papillotomy. The remaining patients with cholecystolithiasis and dilated common bile duct were at that time qualified for classical cholecystectomy with bile duct exploration due to papillotomy failure, contraindications to perform it or lack of the patient's consent.

Another US examination was performed when after LCh, pain and increased temperature persisted and when irregularities were found in laboratory tests – this usually took place on the second or third day following the procedure.

All patients had a control US examination scheduled 30 days after the surgery. Four hundred and twelve patients (76%) reported for this examination. The following were assessed: the condition of the cholecystectomy site, the width and course of the CBD as well as the appearance and dimensions of the pancreas.

The changes in the US image of the gallbladder and its surroundings in the cases of ACh were assessed prior to the surgery taking into account the possibility of the occurrence of difficulties during the procedure itself. The examination results in specific groups were analyzed statistically by means of χ² test.

Results

Both before and after the procedure (LCh) a thorough assessment of the patients was made. The patients who underwent laparoscopic cholecystectomy because of acute cholecystitis (542 persons) constituted a non-uniform group particularly due to the intensity of the symptoms. Nonetheless, all of them presented increased typically localized pain, temporarily or permanently raised temperature, elevated leukocytosis (> 10 × 10⁹/l), high ESR, and at least one of the US features of ACh described above. In this group, the conversion was necessary in 130 patients, i.e. in 24.0% of cases in comparison with 3.8% of patients with uncomplicated cholecystolithiasis (without the signs of inflammation). In all cases, the presence of acute cholecystitis was verified by a postoperative histopathological examination of the wall of the removed specimen, which confirmed the presence of lesions.

The detailed ultrasound analysis also concerned the images of the gallbladder and its surroundings both when conversion was and was not necessary. The type of changes in the wall and their intensity were determined and a part of the gallbladder or its surroundings was specified in which the greatest intensity of such changes occurred (tab. 1).

Tab. 1.

Changes in US image in patients suffering from ACh, who underwent and did not undergo conversion

ACh feature in US image	ACh – 412 patients without conversion	ACh – 130 patients with conversion	Statistical significance level p (χ2 test)
Wall thickening 3–5 mm	258 (62,6%)	18 (13,8%)	< 0,000001
Wall thickening > 5 mm	36 (8,8%)	41 (31,5%)	< 0,000001
Intramural effusion	67 (16,3%)	24 (18,5%)	0,56
Mural effusion	76 (18,4%)	44 (33,8%)	0,002
Suspicion of gangrenous cholecyst	42 (10,2%)	21 (16,1%)	0,06
Pericholecystic abscess	27 (6,6%)	23 (17,7%)	0,0001
Large wall deformity	38 (9,2%)	28 (21,5%)	0,0002
Inhibited anatomic evaluation	96 (23,3%)	52 (40,0%)	0,003
Cholecystocele	112 (27,2%)	31 (23,8%)	0,45

The analysis of the changes visible during US examination, conducted each time prior to the procedure, revealed that the most common irregularities coexistent with the necessity of conversion were: inhibited assessment of anatomical structures (particularly in the region of the Calot's triangle) connected with local inflammation (40.0%), mural effusion (33.8%), wall thickening of > 5 mm (31.5%), tense, enlarged gallbladder (23.8%) and considerable deformity of the wall that inhibited adequate structure assessment (21.5%). The remaining changes occurred more rarely. The group of patients, in whom conversion was not necessary, manifested less intense changes. The most common irregularities in US image in the case of cholecystitis were: wall thickening of 3–5 mm (in 258 patients – 62.6%), tense and enlarged gallbladder (in 112 patients – 27.2%), mural effusion (in 76 patients – 18.4%) and intramural effusion (in 67 patients – 16.3%).

On the basis of the homogeneity test χ², statistically significant differences were obtained between conversion and non-conversion groups (p < 0.05). Thus, in the conversion group, the following symptoms occurred significantly more frequently: wall thickening (31.5% vs. 8.8%), mural effusion (33.8% vs. 18.4%), pericholecystic abscess (17.7% vs. 6.6%) as well as considerable wall deformity (21.5% vs. 9.2%) and inhibited anatomic assessment (40.0% vs. 23.3%). In the non-conversion group, however, wall thickening of 3–5 mm occurred significantly more frequently (62.6% vs. 13.8%)

In the cases of conversion, the changes in the US image practically did not exist in a solitary form. A few simultaneous changes were observed, which comprised the complete clinical picture of local inflammation. The groups of observed changes are presented in tab. 2.

Tab. 2.

Number of simultaneously coexistent US features

Number of US features occurring simultaneously	Number of patients (N = 130)
3 simultaneous features	57 patients (43.9%)
2 simultaneous features	38 patients (29.2%)
1 US feature	35 patients (26.9%)

The frequency of conversion was affected in a significant way by the number of ACh features visible in US images, particularly in those patients who manifested three features at the same time. This group included the greatest number of conversions. The conversion of laparoscopic procedure to classical open abdominal surgery was necessary in more than a half cases because of the inhibited assessment of anatomical structures of the Calot's triangle region, gallbladder wall thickening of > 5 mm and pericholecystic effusion. This entailed the lack of progress of the surgery and too difficult technical conditions, even for an experienced laparoscopist. In all patients, the features of acute cholecystitis in US image correlated with clinical indices (laboratory tests, physical examination) and the presentation of changes in the histopathological analysis.

Discussion

Laparoscopic cholecystectomy is a commonly recommended method both in uncomplicated and complicated forms of cholecystolithiasis^{(4, 9, 13, 15)}. The number of conversions in uncomplicated cholecystolithiasis is usually slight – in the author's own material, it equaled 3.2%. Information quoted in the references indicate similar values, usually in the range of 1–6%^{(6, 12–14, 16)}. Conversions are rarely performed in slim patients without clinical symptoms of inflammation. In this group, the US image of the gallbladder wall and surrounding tissues is correct^{(6, 12)}.

The situation of the patients who manifest symptoms of ACh is completely different. In such cases, the percentage of conversions increases and in the authors’ own material, it equaled 24.0%. This value is also comparable to the ones obtained in other centers where they constituted 12–25.5%^{(3, 8, 12, 20, 21)} and even as much as 35%^{(5, 10, 13, 18, 22)}. There are many reasons of such a state for instance: duration of acute symptoms, large damage to the gallbladder wall, inflammatory infiltration of the Calot's triangle, adhesions in the upper level of the abdominal cavity and intraoperative complications. The degree of damage to the gallbladder wall should be emphasized as an important factor contributing to the raise of the number of conversions^{(3, 13, 23)}. The gangrenous cholecyst constitutes a frequent example due to the damaged continuity of the wall, flaccidity and susceptibility to tearing during retraction and removal (fig. 1). Some authors claim that the suspicion of the gangrenous gallbladder in a preoperative US examination (massive gallbladder distension with wall atrophy, presence of gas in the wall) constitutes an indication for laparotomy due to large number of conversions and complications^{(8, 13, 14)}.

Fig. 1.

Gangrenous cholecystitis. Flaccid, thin-walled gallbladder filled with contents of increased echogenicity (probably indicating infected bile)

Considerable wall thickening related to acute inflammation as well as infiltration of the gallbladder wall and elements of the Calot's triangle constitute further causes for conversion^{(1, 4–6, 11, 24)}. Wall thickening of > 4–5 mm, intensified intramural effusion and mural abscess are the main indications for open cholecystectomy. Such decisions usually result from the difficulties to assess anatomical structures and the possibility of making errors such as damaging important anatomical structures, mainly the common bile duct and hepatic artery. This is of considerable significance since inflammatory wall thickening constitutes the cause of numerous conversions, even up to 33–35%^{(1, 5, 13, 24, 25)}.

Choledocholithiasis, which is diagnosed in 10–12% of cases, is not a contraindication for LCh if the concrements are removed prior to the procedure by means of endoscopic papillotomy (ES)^{(10, 23, 26, 27)}. Defining the indications for ES is of key importance. Ultrasound constitutes a fundamental examination but its sensitivity in bile duct assessment ranges merely from 68–94%⁽²⁸⁾. Additionally, the levels of bilirubin phosphatase, lipase and transaminase need to be tested and the course of disease should be traced^{(14, 23, 25, 28)}. In the majority of cases, elevated bilirubin in ACh depends on the inflammation process in the Calot's triangle, similarly to the dilatation of the lumen. This level decreases upon the administration of antibiotics^{(5, 17, 29)}. One should remember, however, that such a symptom may also occur in Mirizzi's syndrome (chronic cholelithiasis that leads to the obstruction of the common hepatic duct) which also increases the number of recorded conversions⁽²⁵⁾. A method of high sensitivity and, especially, specificity in assessing choledocholithiasis is magnetic resonance cholangiopancreatography (MRCP). This examination is recommended in all cases in which the diagnosis is not unambiguous⁽³⁰⁾.

The thickening and deformation of the gallbladder wall and symptoms similar to inflammation in patients older than 60 may suggest gallbladder neoplasm – such situation occurs in 3–10% of patients^{(20, 22)}. Gallbladder neoplasm constitutes a contraindication to LCh. Such a method usually causes peritoneal carcinomatosis and dissemination in the trocar channels⁽²⁰⁾. If the neoplasm is detected during LCh, each time the conversion and performance of radical procedure including the removal of trocar channels are indicated⁽²²⁾. The differential diagnosis of cholecystitis and neoplasm requires detailed analysis. Often, more precise imaging examinations are indicated such as multi-slice computed tomography or magnetic resonance imaging. As long as the images of advanced gallbladder neoplasm are characteristic, early forms are difficult to distinguish from inflammatory changes, where the gallbladder wall is considerably, irregularly thickened (fig. 2). Both thickening and deformation of the gallbladder wall may also result from other pathological conditions such as hypoalbuminemia, adenomyomatosis, AIDS and portal hypertension^{(25, 26)}.

Fig. 2.

Deformity and irregular thickening of the gallbladder wall, which requires the differentiation from gallbladder neoplasm

The surgical management of acute cholecystitis is a rather common procedure, both when performed as an emergency and as a planned operation after adequate preparation of patients. Currently, it is believed that ACh does not constitute a contraindication to LCh. This method, however, has certain limitations, particularly in patients with highly advanced inflammatory changes^{(11, 13, 17)}. Can contraindications to laparoscopy be defined? This is a difficult question and to answer it, one should analyze the reasons for conversion. The conducted statistical analyses determine these causes in a way that is not unambiguous enough. The most commonly listed causes of conversion were: considerably thickened inflamed wall, inhibited orientation in the case of calculous and cirrhotic lesions, cholelithiasis in male patients above 65 years of age and palpable mass of the gallbladder during physical examination^{(2, 16, 21)}. Other authors listed abdominal adhesions and the lack of appropriate anatomical orientation as the most important causes of conversion. Additionally, obesity, older age, male patients, thickening of the gallbladder on US scan and persistent elevated body temperature are listed^{(6, 12, 16–18, 25, 29)}. The number of conversions is also influenced by elevated alkaline phosphatase (over 200), WBC of > 14.0, score > 10 in a prognostic APACHE II scale as well as elevated levels of LDH and BMI of > 25–30 kg/m^{2(2, 12, 16, 25, 29)}.

Imaging examinations are the basis for the qualification for a given manner of treatment. A detained US assessment of the upper quadrant of the abdominal cavity provides significant information on the present complications of cholecystolithiasis. The most commonly mentioned features are gallbladder wall thickening, suspicion of calculous and cirrhotic lesions and, additionally, pericholecystic fluid, US Murphy's sign as well as obstructed and distended gallbladder^{(1, 6, 7, 16, 18, 21, 24, 27)} (figs. 3, 4). Other parameters of US image, which may indicate certain difficulties in laparoscopic procedures include: increased volume of the gallbladder, blocked concrements in the region of the neck, choledocholithiasis, large dimensions of concrements, increased perfusion in the gallbladder wall and adjacent liver visualized in color and power Doppler examinations as well as specific changes visible in the structure of the thickened, inflamed wall^{(7, 18, 25–27)}. US examination plays a vital role in determining a therapeutic procedure. When the intensified inflammatory process has been confirmed by ultrasound, necessary conversion during laparoscopic cholecystectomy might be anticipated to take place 7–8 times more frequently^{(4, 16, 25, 29)}.

Fig. 3.

ACh. Considerable wall thickening (8–9 mm). A large concrement obstructs the area of the gallbladder neck

Fig. 4.

ACh. Gallbladder blocked by a large concrement. Features of inflamed wall and pericholecystic effusion

Based on the material gathered over eighteen years in our Clinic, we attempted to determine the causes of conversion during cholecystectomy. These reasons mainly encompassed difficulties in anatomical orientation in the region of the Calot's triangle, flaccid, gangrenous gallbladder and massive adhesions. Additionally, it was stated that in all cases of ACh where conversion occurred, a preoperative US examination revealed advanced inflammatory lesions. The most frequent features include: inhibited assessment of anatomical structures, particularly in the region of the Calot's triangle, related to local inflammation (40.0%), mural effusion (33.8%), wall thickening > 5 mm (31.5%), tense, enlarged gallbladder (23.8%) and considerable deformity of the wall that inhibited adequate structure assessment (21.5%) (figs. 5, 6). The remaining changes occurred more rarely (figs. 7, 8). The statistical analysis (χ² test) of patients with and without conversion revealed significant differences concerning the frequency of occurrence of the following symptoms: wall thickening (31.5% vs. 8.8%), mural effusion (33.8% vs. 18.4%), pericholecystic abscess (17.7% vs. 6.6%) as well as considerable wall deformity (21.5% vs. 9.2%). The greatest number of conversions was observed in patients whose US scans revealed three described changes at the same time. Based on this information, it might be stated that when three aforementioned signs of acute cholecystitis are observed on a US scan, a classical cholecystectomy should be chosen, particularly when such findings correspond to the current clinical condition of the patient. The final decision concerning the type of surgery, however, is made by the surgeon on the basis of the entire clinical picture, current patient condition and own experience, which, beside imaging examinations, remains the most important decisive factor.

Fig. 5.

Considerably thickened wall, enlarged gallbladder obstructed by a concrement. The misshaped region of the Calot's triangle inhibits accurate assessment of anatomical structures

Fig. 6.

ACh. Massive damage to the continuity of the wall that causes complete blurring of the gallbladder and liver borders. Large inflammatory reaction and infiltration in the region of the Calot's triangle

Fig. 7.

ACh. Considerable gallbladder wall thickening with visible intramural effusion

Fig. 8.

ACh. Gallbladder wall that is changed by inflammatory process and thickened. At the side of the liver bed, a fluid cistern is visible – pericholecystic abscess

Conclusions

1. In a preoperative US assessment of the gallbladder in patients with ACh, the character of lesions in the gallbladder and adjacent structures should be precisely determined, as should be their intensity and total number in a given patient.

2. Based on imaging scans, the most common causes of conversion included: inflammatory infiltration in the Calot's triangle region, mural effusion and wall thickening of > 5 mm.

3. The classical cholecystectomy in ACh should encompass patients who manifest three major local complications as revealed on US examination and who manifest acute clinical symptoms.

Conflict of interest

Authors do not report any financial or personal links with other persons or organizations, which might affect negatively the content of this publication and/or claim authorship rights to this publication.