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1
Department of Radiology, Massachusetts General Hospital, Harvard Medical
School, 55 Fruit St., Boston, MA 02114.
2
Present address: Department of Radiology, Beaumont Hospital, Beaumont Rd.,
Dublin 9, Ireland.
Received December 14, 1998;
accepted after revision August 25, 1999.
Address correspondence to G. W. L. Boland.
Abstract
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SUBJECTS AND METHODS. Fifty-five consecutive patients (age range, 18-94 years old; mean age, 56 years; 33 men, 22 women), who were admitted to the ICU with a variety of diagnoses, underwent sonography of the gallbladder twice a week. Patients with gallbladder calculi were excluded from the study. The gallbladder was examined for the recognized sonographic features of acalculous cholecystitis: gallbladder wall thickening, gallbladder distention, intramural gallbladder lucencies (striated gallbladder wall), pericholecystic fluid, gallbladder sludge, and Murphy's sign. These findings were correlated with clinical and laboratory parameters that are associated with acalculous cholecystitis: fever, WBC, liver function tests, levels of serum bilirubin, mechanical ventilation status, and administration of parenteral nutrition, narcotic analgesics, antibiotics, and pressor agents.
RESULTS. Eleven of the 55 patients were found to have gallbladder calculi and were excluded from the study. Thirty-seven (84%) of the remaining 44 patients had at least one sonographic abnormality while in the ICU. Twenty-five (57%) of the 44 patients had as many as three abnormalities found on sonography, and six (14%) of 44 patients had four or five sonographic findings of gallbladder abnormalities while in the ICU. No statistically significant correlation was found among any of these sonographic abnormalities and the clinical and laboratory parameters.
CONCLUSION. Gallbladder abnormalities are frequently seen on sonography in ICU patients, even if these patients are not suspected of having acalculous cholecystitis; therefore, sonography appears to be of limited value in diagnosing acalculous cholecystitis in ICU patients.
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In an attempt to clarify the prevalence and significance of gallbladder findings seen on sonography in ICU patients, we prospectively embarked on a study to evaluate the range of gallbladder abnormalities in ICU patients without gallstones and to correlate these radiologic findings with clinical and biochemical parameters.
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Right upper quadrant sonograms were obtained in all patients within 24 hr of admission, and follow-up examinations were performed twice a week until the patients either were discharged from the ICU or died. Eleven patients were found to have gallbladder calculi and were excluded from further analysis because the study was designed to examine patients with the potential of developing acalculous cholecystitis, leaving 44 patients available for analysis. A total of 136 sonograms were obtained (range, 1-11 sonograms per patient). Gallbladder sonography was performed by one of four experienced operators, all gastrointestinal radiologists, using an Aloka 650 sonography unit (Gorometrics Medical Systems, Wallingford, CT) and a 3.5- or 5-MHz sector scanner transducer (Gorometrics Medical Systems), depending on the size of the patient.
In all patients, images of diagnostic quality were obtained, and the gallbladder was visualized. Multiple static images were obtained in the sagittal and transverse planes of the gallbladder, and wall thickness was measured from transverse images relative to the long axis of the gallbladder. The images were examined together by two radiologists for sonographic features consistent with acalculous cholecystitis features that have been described: gallbladder wall thickening, gallbladder distention, intramural gallbladder wall lucencies (striated gallbladder wall), pericholecystic fluid, gallbladder sludge, and the presence of a sonographic Murphy's sign [1,2,3,4,5,6,7,8,9]. Gallbladder wall thickening was defined as a transverse wall measurement adjacent to the liver and perpendicular to the sonography beam of greater than 3 mm. Gallbladder distention was defined as a shortaxis diameter of the gallbladder of 40 mm or greater [1]. Gallbladder wall lucencies (Fig. 1) were defined as irregular discontinuous lucent and echogenic bands in the gallbladder wall. Patients with abnormal gallbladder sonographic findings (except for the presence of gallbladder sludge) when transferred from the ICU underwent follow-up sonography twice a week until the appearance of the gallbladder returned to normal. Fifteen follow-up sonograms were obtained in seven patients.
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The referring physicians were not aware of the results of each sonogram so that the natural course of any underlying disease process was unbiased by the study. Sonographic examinations of the right upper quadrant that were requested on clinical grounds were performed separately and not included in the study.
Clinical and laboratory parameters that have been described as indications of acalculous cholecystitis [4] were recorded at the time of each sonogram: temperature, WBC, liver function tests, serum bilirubin, mechanical ventilation status, administration of parenteral nutrition, narcotic analgesics, antibiotics, and administration of pressor agents. Using the chi-square test, these clinical parameters were correlated with the sonographic findings to determine the statistical significance of association.
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Of the 44 patients included in the study, 37 (84%) had at least one sonographic abnormality in the ICU. Twenty-five (57%) of the 44 patients had up to three sonographic abnormalities, and six (14%) had four or five positive sonographic findings in the ICU. These findings were not present on the initial study.
Of the 136 sonograms obtained, sludge was present in the gallbladder lumen in 80 (59%) of 136 sonograms in 24 (55%) patients and was the most frequent positive finding. Gallbladder sludge was graded as mild (<25% of gallbladder volume) in 30 of 80 scans, moderate (25-50%) in 18 of 80 scans, and severe (>50%) in 32 of 80 scans. Gallbladder distention, as defined by a short-axis diameter of the gallbladder of 40 mm or greater [1], was present in 45 (33%) of 136 sonograms in 26 (59%) patients (Fig. 2). Mean short-axis diameter of the gallbladder in these 26 patients was 44 mm (range, 40-58 mm). In the 18 patients with nondistended gallbladders, mean short-axis diameter of the gallbladder was 29 mm (range, 12-39 mm).
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Lucencies of the gallbladder wall were present in 18 (13%) of 136 sonograms in seven of 44 (16%) patients. Gallbladder wall thickening of 4 mm or greater was present in 26 (19%) of 136 sonograms (range, 4-12 mm) in 11 (25%) of 44 patients. Localized pericholecystic fluid (fluid around the gallbladder wall) was present in 16 (12%) of 136 scans or in eight (18%) of 44 patients. In eight of these 16 scans, ascites was not present. Right upper quadrant ascites was also present in eight of these 16 sonograms. In four patients, ascites was seen in the abdomen, but not adjacent to the gallbladder bed.
Clinical parameters that are recognized risk factors for developing acalculous cholecystitis are included in Table 1 [1,2,3,4,5]. Of the 44 patients, 39 of 44 were ventilated at some time during their ICU stay, 25 of 44 received IV pressor agents for intermittent hypotension, 27 of 44 had WBCs greater than 11 x 103 µl, 34 of 44 had temperature elevations greater than 38.1°C (100.5°F) at some time during their ICU stays, 12 of 44 had total bilirubin levels greater than 1 mg/dl, 19 of 44 had alkaline phosphatase levels greater than 115 U/l, and 16 of 44 had aspartate aminotransferase levels greater than 40 U/l. No statistically significant correlation was found between any of these parameters and sonographic findings suggestive of cholecystitis (Table 2).
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Outcome
The sonographic findings of all 44 patients were not available to the
referring physicians so that the clinical outcome in these patients would not
be influenced. However, referring physicians specifically requested sonography
of the gallbladder in eight patients during the study. In these eight
patients, acalculous cholecystitis was suspected on clinical and biochemical
grounds by the referring physicians. These additional sonograms requested by
the referring physicians did not affect the frequency of sonography performed
for the study and were not evaluated as part of the study. In two of these
eight patients, after a surgical consultation, acalculous cholecystitis was
considered to have developed during their ICU stays. Sonographic and
laboratory findings in these two patients revealed no specific features of
acalculous cholecystitis. The sonographic findings in one of these patients
indicated gallbladder sludge, distention, and pericholecystic fluid, but no
wall thickening. The sonographic findings in the other patient only indicated
gallbladder distention. The clinical and biochemical parameters were
nonspecific, with one patient having an elevated WBC and the other having a
normal WBC. Both patients had fevers exceeding 38.3°C (101°F). One had
rapid defervescence after surgical cholecystostomy, the other had percutaneous
cholecystostomy. The clinical and sonographic findings in these two patients
were not statistically different from those in the 42 patients who did not
develop clinical acalculous cholecystitis.
Thirty-five of the 44 patients were discharged from the ICU. Nine of the 44 patients died in the ICU. None was thought to have acalculous cholecystitis on clinical or laboratory grounds. Autopsies were performed on five of these patients and none showed evidence of acalculous cholecystitis. The other six patients died of causes related to their admission to the ICU (trauma, three patients; medically related disease, three patients).
Sonographic findings became normal during the ICU stay in 30 of the 37 patients who had at least one sonographic gallbladder abnormality during the early period of their ICU stay. Of the 35 patients who were discharged from the ICU, seven of 35 patients underwent sonographic follow-up because of persistent sonographic abnormalities. A total of 15 sonograms were obtained in these seven patients. Sonographic abnormalities returned to normal after 3 days in two patients, 6 days in three patients and 9 days in two patients.
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Because of the difficulty in clinically diagnosing acalculous cholecystitis, radiologists are frequently requested to sonographically evaluate the gallbladder in the ICU. The reported sonographic findings for acalculous cholecystitis include a distended gallbladder, gallbladder sludge, a thickened gallbladder wall (>3 mm), intramural gallbladder lucencies or striations, pericholecystic fluid, and a sonographic Murphy's sign [1,2,3,4]. Many of these findings can be seen as a result of a variety of other causes frequently encountered in ICU patients. For example, a distended gallbladder may reflect diminished gallbladder emptying as a result of parenteral nutrition and the administration of multiple cholestatic drugs, particularly narcotics [1]. Gallbladder sludge or echogenic bile may be a result of bile stasis from fasting, parenteral nutrition, or functional obstruction of the Oddi's sphincter after narcotic analgesic administration [4]. Furthermore, normal sonographic appearances do not necessarily rule out early acalculous cholecystitis [10]. Another report has also suggested that color Doppler sonography of the gallbladder may be helpful in distinguishing acute cholecystitis from a normal gallbladder [11]. This report suggests that the cystic artery lengthens in acute cholecystitis, although the presence or absence of flow does not help in the diagnosis of acute cholecystitis. However, color Doppler sonography has not generally proved helpful in clinical practice and is rarely performed today.
Our prospective study was performed to evaluate the presence and range of these sonographic findings in ICU patients who were not clinically suspected to have acalculous cholecystitis. Indeed, this study confirms that the majority of patients (85%) admitted to the ICU have sonographic gallbladder abnormalities. Furthermore, 25 (57%) of 44 patients had up to three sonographic abnormalities suggesting possible acalculous cholecystitis. Only one of these 25 patients developed acalculous cholecystitis. One other patient, in whom only a single abnormality (distention) could be found on sonography, developed acalculous cholecystitis. In the other surviving patients, the abnormalities shown on sonography returned to normal either during the ICU stay or shortly after discharge.
The most frequently described abnormality in acalculous cholecystitis is a distended gallbladder [1,2,3,4,5,6]; however, gallbladder distention occurs in any condition predisposing to gallbladder stasis. Because ICU patients often receive multiple cholestatic drugs and parenteral nutrition, it is perhaps not surprising that gallbladder distention was found in 22 (50%) of the 44 patients in this study. Gallbladder sludge can develop similarly under conditions of cholestasis and was found in 24 (55%) of 44 patients. Diffuse gallbladder wall thickening is also a nonspecific finding for acalculous cholecystitis. Wall thickening was seen in 27% of patients and was not a finding in either of the patients who developed acalculous cholecystitis. Similarly, intramural wall lucencies, defined as irregular discontinuous lucent and echogenic bands in the gallbladder wall [1], were not seen in either of the two patients who developed acalculous cholecystitis, but were seen in 15% of patients who did not develop acalculous cholecystitis. Localized pericholecystic fluid (defined as fluid around the gallbladder alone, not associated with ascites) has been reported to show some specificity for acute cholecystitis [3, 8]; however, in our study, this fluid was found in 19% of patients, none of whom developed acalculous cholecystitis.
These findings, which, to our knowledge, have not been reported in the radiology literature, have been discussed in a smaller subset of ICU patients [12], but have not been widely recognized. A study by Raunest et al. [12] of patients with severe trauma admitted to the ICU reported similar gallbladder sonographic changes in trauma patients who were not clinically suspected to have acalculous cholecystitis. In the study by Raunest et al. with serial gallbladder sonography, eight of 41 patients were considered to have developed acalculous cholecystitis. Cholecystectomy was performed in two of these patients, but, in the other six, the gallbladder findings returned to normal on serial sonography despite conservative treatment.
However, Raunest et al. [12] did not discuss the significance of the sonographic Murphy's sign, which is perhaps the most specific sign for acalculous cholecystitis in the ICU [1, 2]. In one study of ICU patients, Murphy's sign was present in 35% of patients with acalculous cholecystitis [2]. In this same study, 89% of patients with a sonographic Murphy's sign had documented acalculous cholecystitis. No patient included in our study had a positive sonographic Murphy's sign; however, the significance of this finding is uncertain because of the proportion of patients in whom it is difficult to evaluate a sonographic Murphy's sign. Other reports have indicated that pain may be difficult to elicit because of the altered mental status common to ICU patients, who are frequently prescribed regular narcotic analgesics and muscular relaxants for endotracheal intubation [1,2,3].
In an attempt to corroborate clinical and laboratory parameters with the sonographic findings, each patient in our study was also assessed for the presence of mechanical ventilation, administration of total parenteral nutrition, IV narcotics, and IV pressor agents. Furthermore, individual assessments were also made for temperature, WBC, total bilirubin level, alkaline phosphatase level, and aspartate aminotransferase levels. No individual clinical and biochemical parameters correlated with any specific sonographic findings. Sonographic findings of gallbladder distention and sludge were found more frequently, but these were not statistically more likely to occur in patients who had a particular abnormal clinical or biochemical parameter.
These clinical parameters were also obtained to address one of the limitations of the study: pathologic proof of the presence or absence of acalculous cholecystitis could not be obtained for obvious reasons. Without the ability to obtain tissue for pathologic confirmation of acalculous cholecystitis, we attempted to document, for each patient, the previously recognized predisposing clinical and biochemical factors that render patients susceptible to acalculous cholecystitis [1,2,3,4].
A combination of these abnormal clinical and biochemical parameters were likely the cause of the frequent abnormal sonographic findings [4, 10]. This is in keeping with the earlier reports in the literature that suggested that the sensitivity and specificity of sonographic findings in acalculous cholecystitis in critically ill patients is low [1, 2]. Interestingly, the sonographically abnormal gallbladder returned to normal during the latter stages of the ICU stay in most patients, presumably reflecting the gradual improvement in clinical and biochemical parameters that is likely to occur as the patient approaches discharge from the ICU.
The significance of these findings only confuses the issue of diagnosing acalculous cholecystitis in the ICU patient, which is already difficult to diagnose. These findings suggest that it can be extremely difficult to differentiate gallbladders with acalculous cholecystitis from those that have abnormal appearances because of the combination of adverse clinical and biochemical parameters. Gallbladder abnormalities shown on sonography may mean very little, with the possible exception of a positive sonographic Murphy's sign.
We conclude that this study corroborates previous reports that sonography appears to be of limited value in diagnosing acalculous cholecystitis in ICU patients. Certainly, the presence of a sonographically normal gallbladder is very unlikely to represent acalculous cholecystitis, but a gallbladder with multiple sonographic abnormalities may not represent acalculous cholecystitis. Considering the continuing difficulty of diagnosing acalculous cholecystitis in the ICU patient, a prophylactic percutaneous cholecystostomy may be required to rule out the gallbladder as a source of sepsis in those patients who have at least one sonographic abnormality [1, 2]. In patients in whom acalculous cholecystitis is not suspected, findings on sonographic follow-up of the gallbladder should return to normal as the patient approaches discharge from the ICU or rapidly return to normal once the patient is discharged from the ICU.
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