Can acute cholecystitis with gallbladder perforation be detected preoperatively by computed tomography in ED?
Brief Report
Can acute cholecystitis with gallbladder perforation be detected preoperatively by computed tomography in ED?
Correlation with clinical data and computed tomography features
Ming-Jen Tsai MDa, Jen-Dar Chen MDb,c,?, Chui-Mei Tiu MDb,c, Yi-Hong Chou MDb,c,
Sheng-Chuan Hu MDa, Cheng-Yen Chang MDb,c
aDepartment of Emergency Medicine, Buddhist Tzu-Chi General Hospital, Hualien 970, Taiwan
bDepartment of Radiology, Taipei Veterans General Hospital, Taipei 112, Taiwan
cNational Yang-Ming University School of Medicine, Taipei 112, Taiwan
Received 11 September 2007; revised 23 April 2008; accepted 24 April 2008
Abstract
Purpose: The purpose of this study is to determine which computed tomography findings and clinical data can help to diagnose gallbladder perforation in acute cholecystitis.
Materials and Methods: The medical records and CT findings of patients with surgically proven acute cholecystitis within the last recent 5 years were retrospectively reviewed and compared between 2 groups with and without gallbladder perforation.
Results: A total of 75 patients with acute cholecystitis were included in the study, and 16 patients were proven to have gallbladder perforation. Higher mortality rate was found in the perforation group (18.8% vs 1.7%; P = .029). Older age (N70 years; P = .004) and higher percentage of segmented neutrophil (N80%; P = .027) were significant clinical factors for predicting gallbladder perforation in acute cholecystitis. The significant CT signs related to gallbladder perforation included visualized gallbladder wall defect (P = .000), Intramural gas (P = .043), intraluminal gas (P = .000), intraluminal membrane (P = .043), pericholecystic abscess or biloma formation (P = .009), intraperitoneal Free air (P = .001), and presence of ascites in the absence of hypoalbuminemia or other intraabdominal malignancy (P =
.017). In multivariate analysis, visualized gallbladder wall defect was the most significant predicting CT feature for diagnosing gallbladder perforation in acute cholecystitis.
Conclusion: Elderly patients with higher segmented neutrophil and CT signs of gallbladder wall defect associated with acute cholecystitis may have high possibility of gallbladder rupture.
(C) 2009
* Corresponding author. Department of Radiology, Taipei Veterans General Hospital, Taipei 112, Taiwan. Tel.: +886 928832812; fax: +886 2 2871 0848.
E-mail address: [email protected] (J.-D. Chen).
0735-6757/$ - see front matter (C) 2009 doi:10.1016/j.ajem.2008.04.024
Introduction
Gallbladder perforation is one of the most severe complications of acute cholecystitis. High morbidity and mortality associated with gallbladder perforation have been reported. Early diagnosis and early cholecystectomy are the standard for management of gallbladder perforation [1-4]. In addition to higher morbidity and mortality, late operative intervention in patients with gallbladder perforation is also associated with increased number of intensive care unit admissions and long postoperative hospital stays [3]. There- fore, early and preoperative diagnosis of gallbladder perforation in patients with acute cholecystitis is very important. The criteria of diagnosis of acute cholecystitis have been well investigated, including imaging studies and clinical pictures [1,5-13]. However, preoperative diagnosis of gallbladder perforation is still difficult, and most cases can be diagnosed only during surgery [14]. Although the ultrasound findings in the diagnosis of gallbladder perfora- tion have been described before, computed tomography (CT) has a higher accuracy rate than does ultrasonography in the diagnosis of gallbladder perforation [10-13,15]. Neverthe- less, the useful CT findings to detect gallbladder perforation in acute cholecystitis are not emphasized. Therefore, this study aimed to determine which CT findings and clinical data can help to diagnose the complication of gallbladder perforation in acute cholecystitis.
Materials and methods
Patient population and eligibility
Our hospital is a tertiary care center with 3000 beds in northern Taiwan. The emergency department (ED) staff provide care for approximately more than 80000 patient visits per year. We retrospectively searched for the patients who underwent cholecystectomy with pathologic diagnosis of acute cholecystitis between March 2002 and March 2007 from the computerized database in our hospital. Among them, those patients who received Preoperative CT scans at the ED were included in this study.
We evaluated the CT images and reviewed the medical charts from the computerized database for the patient’s age, sex, duration of symptoms before CT examination, survived or not, clinical laboratory data in the ED, operative findings, and Pathologic findings. The duration of symptoms before CT examination was defined as the days from the onset of symptoms until receiving CT examination. Laboratory data were reviewed for white blood cell counts, percentage of segmented neutrophil, alkaline phosphatase (ALP) level, aspartate aminotransferase level, alanine aminotransferase (ALT) level, total and direct bilirubin, and C-reactive protein level. We used the earliest laboratory reports examined in the ED as our study data.
Not all the patients received every laboratory test described as above. If that test was not done, it was recorded as a missing value in our database.
The diagnosis of gallbladder perforation was based on the operative findings. We divided those patients into 2 groups, acute cholecystitis with and without gallbladder perforation. Both clinical data and CT findings were compared between the 2 groups. Moreover, we also defined acalculous cholecystitis when there was no stone found in surgery. When either operative or pathologic findings revealed gangrenous or emphysematous change of gallbladder, we defined it as gangrenous or emphysematous cholecystitis.
Computed tomographic protocol
All CT scans were performed both before and after intravenous (IV) injection of contrast media, except for 4 patients (5.3%) who did not receive postcontrast CT scan because of poor renal function and histories of drug allergy and 7 patients (9.3%) who did not receive precontrast CTscan of upper abdomen. No patient received oral contrast. All examinations were performed with a helical CT scanner (HiSpeed Advantage; GE Medical Systems, Milwaukee, WI). Each scan was obtained with a 5-mm collimation and a pitch of 1.0 from the dome of the diaphragm to above the Iliac crest before IV contrast administration and a 5-mm collimation and a pitch of 1.0 to 1.5 from the dome of the diaphragm to the symphysis pubis after IV contrast administration.
Computed tomographic interpretation
All abdominal CT studies were retrospectively reviewed on the Picture Archiving and Communication System. The CT findings of acute cholecystitis were recorded by the consensus of the first 2 authors, 1 radiologist, and 1 emergency physician. Both authors knew that these patients have acute cholecystitis, but before reviewing these CT scans, they did not know which patients have gallbladder perforation. According to the CT findings of acute cholecystitis reported in the past literatures, we divided these findings into 3 categories-primary gallbladder changes, pericholecystic changes, and findings of extra- gallbladder organs (Table 1) [10-13,16-27].
Primary gallbladder changes included gallbladder wall thickening pattern (regular, irregular, or no thickening), wall enhancement and enhancing pattern (homogeneous pattern, heterogeneous pattern, target pattern, or no enhancement), wall defect, intramural abscess, intramural gas, mural hemorrhage, presence of gall stones, common bile duct stones or cystic duct stones, intraluminal membrane, and intraluminal gas. Mural hemorrhage was defined as the attenuation of focal gallbladder wall more than 50 Houns- field units in precontrast CT scan. Moreover, the largest gallbladder wall thickness, largest gallbladder diameter of short axis, and bile attenuation were also measured.
|
Primary gallbladder changes Wall thickening pattern No thickening 17 (22.7) Regular thickening 54 (72) Irregular thickening 4 (5.3) Wall enhancement (n = 71) a No enhancement 7 (9.3) Enhancement 64 (85.3) Wall enhancing pattern (n = 71) a No enhancement 7 (9.3) Homogeneous enhancement 25 (33.3) Heterogeneous enhancement 16 (21.3) Target pattern 23 (30.7) Wall defects 10 (13.3) Intramural abscess 0 (0) Intramural gas 2 (2.7) Mural hemorrhage (n = 68) b 3 (4) Gall stones 46 (61.3) CBD stones 11 (14.7) Cystic duct stones 15 (20) Intraluminal membrane 2 (2.7) Intraluminal gas 4 (5.3) Gallbladder diameter (mm) 46.05 +- 10.26 Gallbladder wall thickness (mm) 4.882 +- 3.71 Bile attenuation (HU) 13.89 +- 12.29 Pericholecystic changes Pericholecystic fat stranding 71 (94.7) pericholecystic fluid collection 52 (69.3) Pericholecystic abscess or biloma 8 (10.7) Extraluminal stones 0 (0) Findings of extra-gallbladder organs Pericholecystic liver enhancement (n = 71) a 31 (41.3) Liver abscess formation 1 (1.3) portal vein thrombosis (n = 71) a 0 (0) Mural thickening of adjacent organ No mural thickening 34 (45.3) Duodenum 16 (21.3) Both 13 (17.3) Intraperitoneal free air 4 (5.3) Ascites 32 (42.7) lymph nodes 57 (76) Mirrizzi syndrome 1 (1.3) Adynamic ileus No ileus 13 (17.3) Local 31 (41.3) General 31 (41.3) |
Values are shown as n (%) or mean +- SD, as appropriate. HU indicates Hounsfield units. a Four patients did not receive postcontrast CT scan. b Seven patients did not receive precontrast CT scan. |
Pericholecystic changes included pericholecystic fat stranding, pericholecystic fluid collection, pericholecystic abscess or biloma formation, and presence of extra- luminal stones.
Table 1 CT findings in 75 patients with acute cholecystitis
Findings of extra-gallbladder organs included perichole- cystic liver enhancement, liver abscess, portal vein thrombosis, reactive mural thickening of adjacent hollow organ (hepatic flexure of colon and duodenum), presence of lymph nodes, intraperitoneal free air, ascites, the bowel ileus pattern (localized, generalized, or no adynamic ileus), and Mirizzi syndrome, which was first described in 1948 as obstructive jaundice due to a gallstone impacted in the cystic duct or Hartmann pouch compressing the common hepatic duct [27,28].
Statistical analysis
To identify the significant CT findings or clinical laboratory data associated with gallbladder perforation, we used Student t test for continuous variables and ?2 test (corrected with fisher’s exact test as appropriate) for categorical variables to perform univariate analysis. For multivariate analysis, logistic regression was conducted by forward stepwise Wald test for the significant variables derived from the univariate analysis (SPSS 14.0; SPSS Institute Inc, Chicago, IL). A P value less than .05 was considered statistically significant.
Results
A total of 142 patients who underwent cholecystectomy with pathologic diagnosis of acute cholecystitis between March 2002 and March 2007 were recorded. There were 75 patients who received preoperative CT scans at the ED whose data were available for review. The operative findings of these 75 patients disclosed that there were 16 patients (21.3%) with gallbladder perforation and 59 patients (78.7%) without gallbladder perforation.
Demographic and clinical laboratory data
In the univariate analysis, 3 variables listed in Table 2 showed statistically significant difference between the 2 groups of acute cholecystitis with and without gallbladder perforation, including age, mortality, and percentage of segmented neutrophil.
In the group with acute cholecystitis with gallbladder perforation, 15 (93.8%) of 16 patients were older than 70 years. In the group with acute cholecystitis without gallbladder perforation, only 32 (54.2%) of 59 patients were older than 70 years (P = .004). The mean age (77.44 +- 5.96 years) of patients with gallbladder perforation (n = 16) was obviously higher than the mean age (65.78 +- 15.942 years) of patients without gallbladder perforation (n = 59; P =
.000). Higher mortality rate in the group with gallbladder perforation was also found (18.8% vs 1.7%, respectively; P =
.029). Segmented neutrophil predominance (percentage
N80%) was found in 14 patients (87.5%) with gallbladder
|
45 (76.3) |
15 (93.8) |
NS |
Age (y) |
65.78 +- 15.94 |
77.44 +- 5.97 |
.000 |
Mortality |
1 (1.7) |
3 (18.8) |
.029 |
Duration of symptoms (d) |
2.86 +- 3.11 (n = 56) |
3.67 +- 4.34 (n = 15) |
NS |
WBC/uL |
12490.2 +- 5892.04 (n = 51) |
14756.25 +- 4654.60 (n = 16) |
NS |
Segmented neutrophil N80% |
34 (57.6) (n = 51) |
14 (87.5) (n = 15) |
|
CRP (mg/dL) |
12.68 +- 9.62 (n = 24) |
18.92 +- 9.20 (n = 10) |
NS |
ALP (IU/L) |
125.02 +- 89.6 (n = 46) |
136.23 +- 105.78 (n = 13) |
NS |
AST (IU/L) |
68.90 +- 126.38 (n = 41) |
268.50 +- 602.27 (n = 10) |
NS |
ALT (IU/L) |
59.89 +- 77.55 (n = 47) |
85 +- 168.28 (n = 11) |
NS |
Total bilirubin (mg/dL) |
2.19 +- 2.15 (n = 47) |
2.62 +- 1.64 (n = 13) |
NS |
Direct bilirubin (mg/dL) |
1.28 +- 1.93 (n = 34) |
2.10 +- 1.46 (n = 8) |
NS |
Values are shown as n (%) or mean +- SD, as appropriate. |
perforation and in only 34 patients (57.6%) without gallbladder perforation (P = .027). The mean +- SD percentage of segmented neutrophil was 85.49% +- 10.96% in the gallbladder perforation group and 79.11% +- 10.11% in the nonperforation group (P = .039). However, sex; WBC counts; CRP, ALP, AST, and ALT level; and total and direct bilirubin did not show significant differences.
Table 2 Demographic and clinical laboratory data in patients with acute cholecystitis with and without gallbladder perforation (GBP) Variables Acute cholecystitis
Without GBP (n = 59) With GBP (n = 16) P
Computed tomographic findings
The 3 most common CT findings of acute cholecystitis in our study (Table 1) were pericholecystic fat stranding in 71 (94.7%) of 75 cases, gallbladder wall enhancement in 64 (85.3%) of 71 cases, and pericholecystic fluid collection in 52 (69.3%) of 75 cases (Fig. 1).
In the univariate analysis of the CT findings between the 2 groups, 7 CT findings showed statistically significant higher
Fig. 1 Computed tomographic scan of a 72-year-old woman with acute cholecystitis without gallbladder rupture shows enhancement of thickened gallbladder wall (arrowhead), pericho- lecystic fat stranding (white arrow), and pericholecystic fluid collection (black arrow).
incidences in the perforation group than in the nonperforation group, including gallbladder wall defect (50% vs 3.4%) (Fig. 2), intramural gas (12.5% vs 0%) (Fig. 3), intraluminal gas (25% vs 0%) (Fig. 3), intraluminal membrane (12.5% vs 0%) (Fig. 4), pericholecystic abscess or biloma formation (31.3% vs 5.1%) (Fig. 5), intraperitoneal free air (25% vs 0%) (Fig. 6), and presence of ascites (68.8% vs 35.6%) (Table 3). Among the perforation group, there were 13 patients (81.3%) who had at least 1 of these 7 CT findings. Nonetheless, there were 3 patients (18.7%) without any visible significant CT finding of gallbladder perforation, who all survived.
However, other CT findings including gallbladder wall thickening and enhancing pattern, presence of gall stones, CBD stones or cystic duct stones, intramural abscess, mural hemorrhage, pericholecystic fat stranding, fluid collection and liver abscess formation, mural thickening of adjacent
Fig. 2 Computed tomographic scan of an 87-year-old man with acute ruptured cholecystitis shows marked wall thickening with target pattern of Contrast enhancement. Note a focal wall defect (long arrow) at the gallbladder body, communicating with pericholecystic fluid (short arrows).
Fig. 3 The lung window of the CT scan of an 81-year-old man with acute ruptured cholecystitis shows intraluminal gas (arrowheads) and intramural gas (large arrow) at the fundus wall of the marked distended gallbladder. There is also extraluminal gas (small arrow) beside the gallbladder, indicating gallbladder perforation.
organ, presence of lymph nodes, and association with Mirizzi syndrome did not show statistical difference between these 2 groups.
In considering the number of cases with gallbladder perforation, we performed the multivariate analysis by logistic regression for the 2 CT findings with the highest statistical significance derived from the above univariate analysis (wall defect sign and intraluminal gas). Wall defect
Fig. 4 Computed tomographic scan of a 74-year-old man with acute ruptured cholecystitis shows intraluminal membrane (short arrow) and focal wall defect (long arrow) of gallbladder, with surrounding pericholecystic fluid collection (arrowhead). C indi- cates hepatic cyst.
Fig. 5 Computed tomographic scan of an 84-year-old woman with acute ruptured cholecystitis shows marked distension of gallbladder containing a large gall stone (long arrow) and intraluminal gas (arrowhead). There is a pericholecystic gas- containing abscess (short arrow).
sign was the most significant CT finding associated with gallbladder perforation in the patients with acute cholecys- titis (odds ratio = 14.250; 95% confidence interval, 2.237-
90.779; P = .005).
Other operative and pathologic findings
Fourteen patients (18.7%) were diagnosed with acalculous acute cholecystitis by the operative and CT findings in our study. Among them, 6 patients (42.9%) had the diagnosis of gallbladder perforation. Among the other 61 patients with stone-related acute cholecystitis, 10 patients (16.4%) had
Fig. 6 Computed tomographic scan of a 79-year-old man with acute ruptured cholecystitis shows intraperitoneal free air (short arrows). Intramural gas (arrowhead) at the wall of gallbladder body and intraluminal gas (long arrow) are also demonstrated.
gallbladder perforation. However, there was no statistical difference in the incidence of gallbladder perforation between the groups of acalculous and stone-related cholecystitis (P =
.063). There were 15 patients (20%) with gangrenous or emphysematous cholecystitis proved by operative or patholo- gic findings in our study. Acalculous cholecystitis was found in 6 of these patients (40%) and in only 8 of those 60 patients without gangrenous or emphysematous cholecystitis
(13.3%). Gangrenous or emphysematous cholecystitis was obviously associated with acalculous cholecystitis (P = .028).
Discussion
In this study, men (93.8%) account for most of the patients with gallbladder perforation. This finding is consistent with
previous studies [1-3,29,30]. However, no statistical significance for sexual predilection was noted between acute cholecystitis with and without gallbladder perforation in our study. Older patients are more likely to have gallbladder perforation [1-3,14]. In our study, the mean age (77.44 years) of patients with gallbladder perforation was higher than the mean age (65.78 years) of patients without gallbladder perforation (P = .000). Higher mortality rate was also found in the gallbladder perforation group (P =
.029). The same finding has been reported in previous studies [1-4]. Stefanidis et al [3] also reported that early surgical intervention may improve outcome and decrease the days of postoperative hospital stays in patients with gallbladder perforation.
In clinical laboratory data, only segmented neutrophil predominance (percentage N80%) is significantly associated with gallbladder perforation (P = .027). The other common and useful adjuvant tests for acute cholecystitis, including WBC counts; CRP, ALP, AST, and ALT level; and total and direct bilirubin, did not show, in any way, the benefit in diagnosis of gallbladder perforation, and the result was similar to that of the study of Wang et al [1].
The CT findings of acute cholecystitis can be divided into primary gallbladder changes, pericholecystic changes, and findings of extra-gallbladder organs. Significant primary gallbladder changes associated with gallbladder perforation in this study are wall defect and presence of intramural gas, intraluminal membrane, and intraluminal gas. Gallbladder wall defect is a direct sign of gallbladder rupture, which was also demonstrated by the ultrasono- graphy in the literature [8,9,11]. However, CT scan is superior to ultrasonography in depicting the wall defect sign [11]. In our study, the presence of wall defect sign is significantly associated with gallbladder perforation in either univariate or multivariate analysis.
The CT findings of intramural gas, intraluminal mem- brane, and intraluminal gas were mainly described in emphysematous or gangrenous cholecystitis in the past studies [18,19]. All the patients with the above 3 findings in our study had gallbladder perforation diagnosed by surgery. Emphysematous or gangrenous cholecystitis might be caused by ischemic change of gallbladder wall due to vascular insufficiency [31,32]. Further Ischemic necrosis of gallbladder wall predisposes to wall perforation more easily. In pericholecystic changes of acute cholecystitis, only pericholecystic abscess or biloma formation is significantly related to gallbladder perforation. Organisms or infective bile pass through the gallbladder perforation site, and then local pericholecystic inflammatory change develops, result- ing in the formation of pericholecystic abscess or biloma. Niemeier (1934) classified this type of gallbladder perfora- tion as subacute or type II gallbladder perforation. Free gallbladder perforation with generalized Biliary peritonitis was classified as acute or type I gallbladder perforation, and cholecystoenteric fistula, as chronic or type III gallbladder
perforation [33].
In CT findings of extra-gallbladder organs, the presence of intraperitoneal free air and ascites is significantly correlated with gallbladder perforation. Four patients with intraperitoneal free air were found in the present study, and all of them were diagnosed with gallbladder perforation by operation. Intraluminal gas was simultaneously found in all these patients, and intramural gas, in 2 patients. The intraperitoneal free air was caused by air leakage of ruptured emphysematous cholecystitis. The relationship between ascites and gallbladder perforation has not been described. Our study showed the significant association of ascites with gallbladder perforation in the presence of acute cholecystitis. There was no underlying condition of significant hypoalbu- minemia or intraabdominal malignancy for these patients in our study. This association can be explained by the fact that bile leakage due to gallbladder perforation causes peritoneal irritation and results in ascites.
One interesting finding in our study is that gangrenous or emphysematous cholecystitis is more commonly correlated with acalculous cholecystitis (P = .028). This can be explained as that the cause of gangrenous or emphysematous cholecys- titis is mainly related to vascular insufficiency and the resultant ischemia and necrosis of gallbladder, not directly related to the stone-induced biliary tract obstruction [29,30]. There were some limitations to this study. First, this study was a retrospective study; the authors had known that all the patients had acute cholecystitis before reviewing their CT scans, although they did not know which ones have gallbladder perforation. This situation may facilitate the image reading focused on gallbladder condition and may differ from the daily practice without reading focus. Second, the number of cases in our study was small. Only 75 of 142 patients with proven acute cholecystitis received CT scan because of prior equivocal ultrasound results, physician’s preference for imaging modalities, or clinical suspicion of other intra-abdominal infectious sources. Third, we did not describe the clinical features and operative and pathologic findings of the other 67 patients with acute cholecystitis who did not receive preoperative CT scans but received sonogram. In the evaluation of which clinical data were associated with gallbladder perforation, it would be better if
we can survey all the 142 patients’ clinical features.
Conclusion
Early diagnosis and early surgical intervention are the key to decrease mortality and morbidity in the management of acute cholecystitis with gallbladder perforation. A high index of suspicion for gallbladder perforation should be posed for acute cholecystitis, especially when risk factors such as older age (N70 years) and higher percentage of segmented neutrophil (N80%) are identified. Although gallbladder perforation in acute cholecystitis may not always be shown on CT, visualized gallbladder wall defect is the most significant predicting CT
feature for gallbladder perforation. Elderly patients with higher segmented neutrophil and CT signs of gallbladder wall defect associated with acute cholecystitis may have a high possibility of gallbladder rupture.
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