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1171

The Diagnosis of Acute Acalculous Cholecystitis:


Comparison Scintigraphy, of Sonography, and CT

Stuart E. Mirvi& Julian R. Vainright1 Ava W. Nelson1 Gerald S. Johnston1 Robert Shorr2 Aurelio Rodriguez3 Nancy 0. Whitley1

The clinical and laboratory diagnosis of acute acalculous cholecystitis is difficult, and the reliability of various diagnostic imaging techniques has not been established. The results of several imaging procedures performed over a 6-year period on 56 patients with clinically suspected acute acalculous cholecystitis were evaluated retrospectively.

Sonography

and CT were

both

highly

sensitive

(92%

and

100%,

respectively)

and

specific (96% and 100%, respectively). Hepatobiliary scintigraphy was compromised by frequent false-positives; the result was a specificity of only 38%. Percutaneous bile aspiration was insufficiently sensitive (33%) for diagnosis. Sonography was as sensitive as hepatobiliary scintigraphy and was more specific in establishing the diagnosis. Because sonography is relatively inexpensive and can be performed at the bedside, it should be regarded as a satisfactory screening procedure. However, CT is a good alternative in an easily transported patient when other intraabdominal disease is suspected.

Acute acalculous cholecystitis is an uncommon but potentially fatal complication of prolonged critical illness [1 -4]. The condition most likely results from a gradual increase in bile viscosity, due to prolonged stasis, that leads to a functional obstruction of the cystic duct [1 , 4]. Compromised perfusion of the metabolically active gallbladder mucosa may also be contributory [3]. Other factors such as prolonged hyperalimentation, prolonged suctioning by nasogastric tube, positive pressure ventilatory support, numerous transfusions, use of vasoactive amines, and use of morphine analgesia also have been implicated [1 , 4]. Unfortunately, both clinical and laboratory tests lack sensitivity and specificity for arriving at a preoperative diagnosis [1 -5]. Because patients with acute acalculous cholecystitis are typically victims of multisystem trauma or other severe illness, they represent a population for whom exploratory laparotomy should be avoided,
if at all possible, as a means of diagnosing this condition. Although hepatobiliary

Received April 21 June 24, 1986.


1

1986;

accepted

after revision

scintigraphy and sonography have been valuable chronic calculous cholecystitis, their usefulness and as CT and percutaneous aspiration of bile have diagnosis of acute acalculous cholecystitis [6-17]. To assess the value of imaging methods in the
cholecystitis, we undertook a 6-year retrospective

in the diagnosis of acute and that of other techniques such not been established in the diagnosis
study

of acute

acalculous
with clinically

Department of Diagnostic Radiology, University of Maryland Medical System/Hospital, 22 5. Greene St.. Baltimore, MD 21 201 . Address reprint requests to S. E. Mirvis. 2 Department of Surgery. University of Southem Califomia,
3

of patients

suspected nography,

acute acalculous cholecystitis in whom CT, or bile aspirations were performed.

hepatobiliary

scintigraphy,

so-

Los Angeles.

CA 90032.

Maryland institute for Emergency Medical Services System (MIEMSS), University of Maryland Medical System/Hospital, 22 5. Greene St., Baltimore, MD 21201. AJR 147:1171-1175, December 1986 0361 -803X/86/1 476-1171 American Roentgen Ray Society

Methods

and

Materials

Since 1 980, 60 patients have been evaluated by diagnostic imaging methods for possible acute acalculous cholecystitis after trauma. Complete medical records and imaging study results were available in 56. All patients were admitted to the Shock Trauma Center of the University of Maryland Medical System/Hospital after major trauma. There were 37 men and

1172

MIRVIS

ET

AL.

AJR:147,

December

1986

19 women; Most were

the age range was 14 to 83 years, injured in motor vehicle accidents

with a mean of 39. (39); the remainder

CT As part of of CT scans as and gallbladder. from the lung


evaluation

were involved

in falls (four), crush injuries

(three), diving accidents

(two), ballistic injuries (two), or other accidents (10). Two patients were admitted for hyperbaric oxygen therapy for severe anaerobic soft-tissue infections. All studies were evaluated retrospectively without clinical knowledge outcome. of No results particular of other imaging diagnostic sequence procedures algorithm or was final fol-

owed
during

as patients
the period

were
of the

cared
study.

for by a variety

of different

clinicians

a general evaluation for possible sources of sepsis or right upper quadrant pain, 1 5 patients had abdominal part of their imaging workup, which included the liver Studies were performed at 1 -cm contiguous sections bases to the iliac crests or to the symphysis pubis if clinically warranted. When possible, both oral (2% diatrizoate sodium [Hypaque) and IV (50 ml bolus of diatrizoate meglumine/sodium
[Angiovist

282]) contrast

media were administered.

Studies

were

conducted either on a General Electric 8800 or 9800, 10,000, or a Pfizer 0450. CT scans were reviewed
radiologists diagnosis was performed MBq) on 45 patients of injected for signs of gallbladder disease. Major included of acute acalculous cholecystitis

a CGR CT/T by two staff


criteria wall for thickening the

Hepatobiliary
Hepatobiliary intravenously

Scintigraphy
scintigraphy with 5-10 mCi

(185-370

99m-technetium-

greater than 4 mm, pericholecystic fluid, or subserosal ascites, intramural gas, or sloughed mucosa. Minor
subjective distension or hyperdense bile. Other

edema without criteria included


findings

tagged paraisopropylacetanilidoiminodiacetic acid (PIPIDA, Diagnostic Isotopes, Bloomfield, NJ). Serial scintigrams were obtained at 5-mm intervals. Static images were recorded at 2 hr and again at 46 hr if there was no visualization of the gallbladder. Static views were obtained from the anterior and right lateral projections. Imaging was performed by using a 37-tube Anger gamma camera. Studies were

pathologic

such as abscess,

ascites, or pancreatic

or hepatic lesions were also

noted, as well as the status of the biliary system. No patient received cholecystokinin for the CT studies. A positive diagnosis was established major by the criteria. presence of two major criteria or two minor and one

reviewed
uptake ization

by two staff radiologists

and were analyzed

for hepatic
Percutaneous Aspiration of Bile

and excretion of tracer into the biliary system, time to visualof activity in the small bowel, and time of visualization of the gallbladder if this occured within 6 hr. Studies demonstrating activity in the small bowel without visualization of the gallbladder within 6 hr

were considered

positive.

Visualization

of the gallbladder

after 1 hr

was considered to represent chronic cholecystitis. Cholecystokinin was administered to only one patient when the gallbladder had not been visualized 3 hr after injection of tracer.

Six patients underwent percutaneous aspiration of bile from the gallbladder guided by real-time sonography [5] or CT. Sonographic studies were performed by means of an ATL 1 00 portable sonographic unit with a biopsy transducer guide. All aspirations were
performed by using a 20-gauge aspiration needle and an anterior

Sonography
Sonographic examination of the gallbladder and right upper quad-

transhepatic approach Informed consent was


bile was quite viscous,

as described by McGahan and Walter obtained beforehand. On two occasions


and a 1 9-gauge needle was required

[5]. the

to obtain

a sample.
and were

Bile samples
cultured

were examined

for bacteria

and leukocytes
No complications

rant was performed

in 40 patients by using real-time

and/or articulat-

anaerobically

and aerobically.

ing arm transducers. Imaging devices used included a Toshiba Sonolayer L (Model SAL-20A) (Toshiba America Inc., Tustin, CA), an ATL MK-100 Precision series (Advanced Technology Laboratories, Bellevue, WA), a Picker Echoview System 80-L (Picker International Inc., Northford, CT), and a Phillips Sono Diagnostic B (Phillips Ultrasound Inc., Santa Ana, CA). All images were obtained with either a 3- or 3.5-mHz transducer. When necessitated by the patients clinical
condition, portable although, studies when were performed by using real-time equipin the

were

encountered

during

or after these

procedures.

Four

other

patients cultured.
neously

had bile specimens obtained These results are included


aspirated specimens.

intraoperatively, with those from

which were the percuta-

Results Hepatobiliary Scintigraphy

ment
supine, right

only.

The studies

generally
possible,

were
patients

performed
also were

with

the patients

examined

decubitus

position.

Erect images were seldom obtained

due to

the general severity of the illnesses. Sonographic studies were reviewed by two staff radiologists, and findings were divided into
major thickness and minor of 4 mm criteria as follows: when Major criteria included was distended a wall to or greater the gallbladder

Hepatobiliary scintigraphy was performed on 46 patients with clinically suspected acute acalculous cholecystitis. In 19 (41 %) the gallbladder was visualized within 1 hr after the
injection and was considered normal. In all but one of these

at least 5 cm in the longitudinal dimension and there was no evidence of ascites or hypoalbuminemia (serum protein <3.2 mg/dl), the presence of pericholecystic fluid or subserosal edema, calculi, intramural gas, a sloughed mucosal membrane, or a complete lack of response
to cholecystokinin. bile (sludge), in longitudinal tion. A study in the transverse Minor distension criteria greater included than the presence of echogenic

patients patients
ings

the clinical symptoms.

course suggested other causes for the However, one patient had normal findscan but markedly abnormal findings on

on hepatobiliary

8 cm in the longitudinal

or 5 cm

dimension, and transverse


considered

or a partial dimensions)
positive

response (<5O% decrease after cholecystokinin injeceither a minimum

was

if it included NJ) was

of two major
cholecystokinin

criteria

or one major
Squibb,

and two minor criteria.


Princeton,

In five cases
at

(Kinevac,

administered

a dosage of 0.02 pg/kg, and the gallbladder was reexamined 15 mm after the injection to assess for degree of contraction. Other evidence
of disease detected in the right upper quadrant, such as an abscess, ascites, or biliary-tree dilatation, was also noted.

sonographic and CT studies. Persistent fever and right upper quadrant pain prompted cholecystectomy, which revealed acalculous cholecystitis. In three patients gallbladder visualization was delayed (2-6 hr). In all cases subsequent clinical and sonographic correlation suggested chronic calculous cholecystitis. These patients were all managed without surgical intervention while recuperating from their acute traumatic injuries and had benign clinical courses. Findings of hepatobiliary scintigrams were abnormal in 24 patients. In two the results were considered indeterminate for

AJR:147,

December

1986

DIAGNOSIS

OF

ACUTE

ACALCULOUS

CHOLECYSTITIS

1173

the

gallbladder

because

of poor

hepatic

function

and

failure

TABLE
for Acute

1 : Sonographic
Cholecystitis

and CT Findings

in Patients

Evaluated

to secrete sufficient tracer into the biliary system. Another patient had obstruction of the proximal hepatic duct and were thus indeterminate findings for the gallbladder but at surgery was shown to have both acute and chronic calculous cholecystitis. ologically Eight by patients with abnormal of acute findings had acalculous

F in d ings
Minor criteria
Distensiona

Sonography
(N
=

CT
(N
=

40)

15)

17

(six), or calculous
the

(two)
presence

acute

cholecystitis

established

pathbacterial

inflammation,

invasion, or necrosis of the gallbladder wall. One patient with acute acalculous cholecystitis received cholecystokinin, but visualization of the gallbladder still did not occur. However, there were 1 3 other patients with nonvisualization of the gallbladder in whom the clinical course (1 1), or surgical inspection alone ering all cases (two) indicated in which the a normal gallbladder gallbladder. Considcould be evaluated,

Sludge Partial response Major criteria


Calculi

to CCKb

16 1
7

6 0
0

No response

to CCK

Wall thickening Pericholecystic


Subserosal

4 mmc fluidd
(halo)

4 13

0 4

2
5

1
5

edema

Positive (2 major or 1 major and 2 minor criteria)


Negative

14
26

5
10

1 3 (54%) of 24 were false-positive, yielding a specificity of only 38% in the posttrauma population. Hepatobiliary scintigraphy was 95% sensitive in the diagnosis of posttraumatic acute cholecystitis.

True positive True negative


Sensitivity Specificity

13 24

5 10

(%)
(%)

92
value (%)
value
(%)

100
100 100
100

Positive
Negative
a

predictive
predictive

96 92
92

Sonography

Sonographic
the study was

studies
considered

were

available

from 40 patients.

In 26
criteria

Longitudinal diameter >8 cm or transverse diameter >5 cm. <5% decrease in transverse or longitudinal axis. CCK = cholecystokinin. 5m protein >3.2 mg/di. a In absence of ascites.
a
C

negative

by our established

(see Methods). Of this group two patients shown at surgery to have either chronic
titis or both acute and first patient sonography

subsequently were calculous cholecys-

chronic calculous cholecystitis. In the revealed only minimal wall thickening

Percutaneous

Aspiration

of Bile

and echogenic bile without second the gallbladder was


mal echogenic bile but

visualization of calculi. In the moderately distended with minicalculi. Both studies were

no definite

performed early in this series with equipment than is currently available. In 1 4 patients sonographic findings
criteria. Seven had pathologically

less were

precise abnormal
acute

real-time by our

Bile was aspirated percutaneously in six cases and obtamed at surgery in four others. In two cases bacteria were obtained (Citrobacter and Escherichia co/i), and both patients had pathologically verified acute acalculous cholecystitis. In four patients the aspirate was sterile and contained no leukocytes; these patients had normal clinical (three) or surgical

verified

acalculous

cholecystitis and five had acute and chronic calculous cholecystitis. One patient had an equivocal result: calculi and mild wall thickening (5 mm), but a partial response to cholecystokinin injection (longitudinal diameter decreased from 7.4 to 6.8 cm). This patients symptoms and elevated bilirubin level resolved with conservative treatment. Three other patients
injected with cholecystokinin pathologically. failed to show patient any with gallbladder

(one) results. However, four other patients had sterile bile cultures and no organisms on Gram stains, as well as specimens without leukocytes, but had acute acalculous cholecystitis pathologically. Thus, although bile aspiration, either percutaneously or at surgery, was 1 00% specific, the method was only 33% sensitive in diagnosing acute gallbladder inflammation.

contraction
titis diagnosed

in 1 5 mm and all had acute


A single

acalculous

cholecysabnormal

Discussion

sonographic findings improved clinically and thus was considered false-positive. Overall, sonography demonstrated a sensitivity of 92% for acute cholecystitis with or without calculi present and a specificity of 96% (Table 1).

CT

Results of CT were available study was positive by our criteria


cystitis, patients and were all five cases considered were

for 1 5 patients. In five the for acute acalculous cholepathologically confirmed. for acute Ten acalculous

to be negative

cholecystitis, and all 1 0 cases were confirmed by clinical course (eight) or surgical pathology (two). Thus, in this limited series CT was both 1 00% sensitive and 1 00% specific in the diagnosis of acute acalculous cholecystitis (Table 1).

The contribution of imaging studies to the diagnosis of acute cholecystitis in general is well established. Overall sensitivity and specificity for hepatobiliary scintigraphy in the diagnosis of acute cholecystitis are 95-1 00% and 81-100%, respectively, whereas the sensitivity and specificity of sonography is reported as 67-93% and 82-1 00%, respectively [8, 12-17]. These series in general represent a substantial majority of cases of acute calculous cholecystitis and reflect the preponderance of the calculous form in the general population [7]. However, the value of diagnostic imaging in establishing the diagnosis of acute acalculous cholecystitis is far less firmly established. In 1983 Weissman et al. [1 1 described their experience with hepatobiliary scintigraphy and sonography in 15 patients with acute acalculous cholecystitis. They reported a 93% specificity and 93% accuracy for hepatobiliary scintigraphy

1174

MIRVIS

ET

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AJR:147,

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1986

but found sonography to be far less reliable, with numerous false-positive and false-negative results. In 1 984 Shuman et al. [7] evaluated hepatobiliary scintigraphy and sonography in 33 surgically proven cases of acute or chronic acalculous cholecystitis. They reported a sensitivity of only 67% for sonography and 68% for cholescintigraphy in establishing the diagnosis. They concluded that the imaging diagnosis of acalculous cholecystitis remains elusive. Our results are at variance with these previous studies. Although we have found hepatobiliary scintigraphy to be highly sensitive (95%) with only a single false-negative result, many false-positive result led to low specificity (38%). The high frequency of false-positive results is not surprising because prolonged parenteral alimentation, prolonged fasting, severe nonbiliary intercurrent illness, and hepatocellular dysfunction are among the conditions known to produce falsepositive results and are also commonly found in victims of major trauma [17-21]. By producing spasm of the sphincter of Oddi, morphine can increase pressure in the biliary system and direct flow of bile into the cystic duct [1 0]. In an effort to decrease falsepositive cholescintigrams, Choy et al. [1 0] have suggested the use of IV morphine sulfate; however, they cautioned that morphine sulfate may produce false-negative results in cases of acalculous cholecystitis by overcoming a functional obstruction in the cystic duct. We did not assess the usefulness of morphine sulfate in this study. Previous studies have suggested that injection of cholecystokinin to promote emptying of viscous bile from the gallbladder might decrease false-positive findings on scintograms. Davis et al. [22] evaluated cholecystokinin in the diagnosis of chronic acalculous cholecystitis and found it of little value in distinguishing symptomatic patients from volunteers. Proudfoot et al. [23] and Pickleman et al. [24], however, found the response to cholecystokinin useful in predicting symptomatic improvement after cholecystectomy. Experience with the use of cholecystokinin in the diagnosis of acute acalculous cholecystitis has been limited. Weissman et al. [25] specifically recommended injection of cholecystokinin in cases of possible acute acalculous cholecystitis. Choy et al. [1 0] raised the
criticism that injection of cholecystokinin after nonvisualization

Sonography was useful in establishing the diagnosis of acute acalculous cholecystitis, with a sensitivity of 92% and a specificity of 96%. Although distension of the gallbladder and echogenic bile were frequent abnormalities shown in the posttrauma population, the detection of wall thickening, pericholecystic fluid, and subserosal edema were more indicative of acute cholecystitis. In 1 1 patients with acute cholecystitis examined by sonography, Marchal et al. [26] saw a sonolucent halo around the gallbladder, which was shown pathologically to represent subserosal edema and cellular infiltration. They believed that this sign was specific for acute cholecystitis. Five of our patients with this finding also had acute acalculous cholecystitis; the sign was never observed in any patient shown clinically or surgically to have a noninflamed gallbladder. Five of 1 2 patients with posttraumatic acute cholecystitis had calculi as shown by sonography and proven pathologically. This high percentage suggests that patients with calculi or chronic cholecystitis may be at increased risk for the development of acute inflammation after major trauma or similar prolonged critical illness. CT was used to evaluate 1 5 patients with suspected acute acalculous cholecystitis and was 1 00% sensitive and specific in this limited series. The CT features of acute cholecystitis

have been

Thickening or nodularity of the gallbladder wall, gallstones, poor definition of the gallbladder/liver interface, and pericholecystic fluid without ascites have been reported most frequently [27, 29, 31 , 33]. The CT equivalent of the sonographic halo sign was present in all five patients with acute acalculous cholecystitis studied by CT. The rim of subserosal edema may mimic pericholecystic fluid, as recently reported by Goldstein et al. [34]. Although
sonography acceptance and hepatobiliary as initial screening scintigraphy have studies for patients gained wide with symp-

described

previously

[27-33].

toms initial

of the gallbladder will necessitate reinjection of the radiopharmaceutical and unduly prolong the time of study. Although our experience with cholecystokinin is limited, the three patients with no sonographically demonstrable response were subsequently proven to have acute acalculous cholecystitis and the single patient with a partial response experienced clinical resolution. One patient in our study had acute acalculous cholecystitis and normal findings on hepatobiliary scintigraphy. Shuman et al. [7] reported frequent false-negative results in their series of 33 patients, producing a low sensitivity of 68-76%. They suggested, as did Weissman et aI. [25], that patency of the cystic duct can persist in acute acalculous cholecystitis despite inflammation of the gallbladder. The inclusion of nine cases of chronic acalculous cholecystitis in the Shuman study [7] may also have contributed to the frequency of falsenegative results.

suggestive of acute cholecystitis, the use of CT as an diagnostic procedure seems quite reasonable. In the typical case our posttrauma patients are referred for imaging evaluation if they have fever and sepsis of unknown source. They commonly also have associated liver enzyme abnormalities, often related to other aspects of their injury. The investigation of the abdomen by CT facilitates the search for occult abscesses and the evaluation of the biliary system. In many instances sonographic assessment of the abdomen is hindered by intestinal ileus or overlying bandages. Recently, McGahan and Walter [5] reported their experience with percutaneous aspiration of bile in patients with
suspected acute acalculous cholecystitis. They emphasized

its value in suspected cases because of the potential for falsepositive findings on cholescintigrams or false-negative findings on sonograms. They believe that aspiration of bile provides a method of excluding the gallbladder as a source of infection. However, four ofour patients in whom bile aspiration was performed had pathologically verified acute acalculous cholecystitis despite the absence of bacteria or leukocytes in the bile specimen. Overall the technique was only 33% sensitive in determining patients with acute gallbladder inflammation. In describing the pathology of acute cholecystitis, Glenn [4] noted no significant difference in calculous vs acalculous disease. The number of leukocytes found in the gall-

AJR:147, December 1986

DIAGNOSIS

OF

ACUTE

ACALCULOUS

CHOLECYSTITIS

1175

bladder wall was variable; occasionally none were found. the basis of this experience, we believe that the absence
leukocytes or bacteria in the bile should not exclude

On of
the

tobiliary

scan

in acute

cholecystitis.

Am J Surg

1984;1 48: 607-

diagnosis of acute calculous or acalculous cholecystitis. In summary, our experience with 56 patients with clinically suspected acute acalculous cholecystitis has shown that sonography has sensitivity equivalent to and specificity supenor to cholescintigraphy. CT was accurate in evaluating the gallbladder for suspected acute cholecystitis and should be regarded as a reasonable screening test, especially when other intraabdominal diseases are anticipated [4]. Finally, percutaneous aspiration of bile may be a valuable method for confirming the diagnosis of acute cholecystitis, but a sterile specimen without leukocytes cannot be used reliably to exdude the diagnosis.

608 15. Suarez CA, Block F, Bernstein D, Serafin A, Rodman G, Zeppa A. The role of HIDA/PIPIDA scanning in diagnosing cystic duct obstruction. Ann Surg 1980;191:392-396 16. Shuman WP, Mack LA, Rudd TG, Rogers JV, Gibbs P. Evaluation of acute upper quadrant pain: sonography and Tc-PIPlDA
cholescintigraphy. AIR 1982; 139:61-64 17. RaIls PW, Colletti PM, Halls JM, Siemsen JK. Prospective evaluation of 99m Tc-IDA cholescintigraphy and grey-scale ultrasonography in the diagnosis of acute cholecystitis. Radiology

1982;144:369-371 18. Womack NA, Bricker

EM. Pathogenesis

of cholecystitis.

Arch

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