Cholecystitis - Complications of Cholecystitis A Comprehensive Contemporary Imaging Review
Cholecystitis - Complications of Cholecystitis A Comprehensive Contemporary Imaging Review
Cholecystitis - Complications of Cholecystitis A Comprehensive Contemporary Imaging Review
https://doi.org/10.1007/s10140-021-01944-z
REVIEW ARTICLE
Abstract
Acute cholecystitis is a common cause of right upper quadrant pain in patients presenting to the emergency department.
Ultrasound, computed tomography, HIDA scans, and magnetic resonance imaging are increasingly utilized to evaluate
suspected cases. The prognosis of acute cholecystitis is usually excellent with timely diagnosis and management. However,
complications associated with cholecystitis pose a considerable challenge to the clinician and radiologist. Complications of
acute cholecystitis may result from secondary bacterial infection or mural ischemia secondary to increased intramural pres-
sure. The recognized subtypes of complicated cholecystitis are hemorrhagic, gangrenous, and emphysematous cholecystitis,
as well as gallbladder perforation. Acute acalculous cholecystitis is a form of cholecystitis that occurs as a complication of
severe illness in the absence of gallstones or without gallstone-related inflammation. Complicated cholecystitis may cause
significant morbidity and mortality, and early diagnosis and recognition play a pivotal role in the management and early
surgical planning. As appropriate utilization of imaging resources plays an essential role in diagnosis and management,
the emergency radiologist should be aware of the spectrum of complications related to cholecystitis and the characteristic
imaging features. This article aims to offer a comprehensive contemporary review of clinical and cross-sectional imaging
findings of complications associated with cholecystitis. In conclusion, cross-sectional imaging is pivotal in identifying the
complications related to cholecystitis. Preoperative detection of this complicated cholecystitis can help the care providers
and operating surgeon to be prepared for a potentially more complicated procedure and course of recovery.
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Emergency Radiology
population is often critically ill before developing cholecys- Allowing for limitations, the diagnosis of acute chol-
titis. It is hypomotility-related gallbladder stasis, rather than ecystitis by US and CT is usually straightforward. The
an obstructing calculus, that results in increased intraluminal imaging findings suggesting cholecystitis on US and CT
pressure. Acalculous cholecystitis can be complicated by include gallstones, thickened and striated gallbladder wall,
mural inflammation, ischemia, and potential necrosis and distended gallbladder, pericholecystic fluid, fluid collections,
also result in perforation. Barie P.S et al. reported gallblad- and inflammatory fat changes. However, the detection of
der perforation in about 10% of acalculous cholecystitis cholecystitis complications on imaging is more challenging.
cases [5]. Wu et al. and Shapira-Rootman et al. concluded that the US
Overall, complicated cholecystitis is associated with could diagnose only a minimal portion (9% and 10%) of
higher morbidity and mortality [6]. Clinical presentation cases of cholecystitis complications [10, 11], but the sup-
may vary and is often masked by concomitant multiple plementary role of CT in the evaluation of complicated chol-
medical comorbidities, specifically in critically ill patients. ecystitis is well established, with sensitivity rates of 88–92%
Complicated cholecystitis necessitates timely management [8, 12]. Given some of the detection challenges, diagnosis of
to avoid catastrophic systemic complications, and radiologi- complicated cholecystitis should be considered a diagnosis
cal evaluation plays a critical role in proper management on a continuum from uncomplicated cholecystitis rather than
and patient prioritization in the ED setting. Clinically, it a discrete one.
is often very challenging to accurately diagnose patients MRI is not part of routine imaging for acute cholecystitis
with complicated cholecystitis because there is consider- in ED. However, MRI with MRCP is a useful complemen-
able overlap in the clinical presentation with other acute tary technique in cholecystitis evaluation, particularly in
abdominal disorders such as perforated duodenal ulcer, patients with inconclusive clinical findings and equivocal
liver abscess, pancreatitis, and other causes of septicemia imaging results on US and CT [13]. MRI has high sensitivity
[7]. Kim et al. designed a predictive model to complement for gallstone detection and assess for stones in the common
CT findings in diagnosing complicated cholecystitis [6]. The bile duct [2, 14]. MRI offers high sensitivity and specificity
potential risk of complicated cholecystitis increases with the in cholecystitis diagnosis and assists in preoperative assess-
following clinical variable as age > /65 years, male gender, ment of complications associated with cholecystitis [15].
BMI > /25, serum leukocyte count > /10,000/mm3, serum Algin et al. illustrated the utility of hepatocyte-specific MRI
neutrophil fraction > /80%, serum platelet count < 20,000/ contrast agent Gd-BOPTA in delineating GB wall perfora-
mm3, serum ALT level > /40 IU/L, and admission via the tion [16].
emergency department [6]. Together, clinical and imaging Hepatobiliary scintigraphy is an instrumental diagnos-
findings of complicated cholecystitis help prioritize patient tic tool in the ED setting when US and CT findings are
management. equivocal for acute cholecystitis. HIDA scanning, hepato-
biliary scintigraphy with technetium 99 m-labeled imino-
diacetic acid analog, has higher sensitivity and specificity
for the detection of acute cholecystitis than US [17]. How-
Overview of Imaging and key concepts ever, to our knowledge, there is no literature on the utili-
zation of HIDA scanning in the evaluation of cholecystitis
In patients presenting with right upper quadrant pain, US is complications.
the preferred imaging modality for initial evaluation. Nev- This review article will familiarize the radiologist with
ertheless, CT is used as an initial examination when patients the spectrum of imaging findings in severe or complicated
present with diffuse abdominal pain in a significant propor- cholecystitis (Table 1) and understand the challenges in early
tion of cases. Our experience shows that the utilization of detection of cholecystitis complications in the ED setting.
both CT and US is not uncommon. The significance of reviewing medical history extensively
Ultrasound is inexpensive, portable, and readily avail- as a criterion before interpreting complicated cholecystitis
able, and does not utilize ionizing radiation, making it most imaging findings is also emphasized in our discussion. The
convenient to begin the imaging evaluation of the patient. diagnosis of complicated cholecystitis is not straightfor-
Imaging with the US is ideally performed after at least 6 h ward; however, in the appropriate clinical context, critical
of fasting to achieve gallbladder distention, but this is omit- attention to specific imaging findings may indicate severe or
ted in the ED setting due to time constraints. US is more complicated cholecystitis and necessitate a more aggressive
sensitive than CT in detecting gallstones and substantially treatment approach or need for additional imaging workup,
more sensitive for the detection of acute biliary disease [8]. closer patient observation, monitoring, and even early sur-
Additionally, sonographers can assess for the presence of a gical intervention. The prognosis for most patients with
sonographic Murphy’s sign. However, US and CT’s specific- complicated cholecystitis is guarded, even after successful
ity are relatively similar at 95% and 93%, respectively [2, 9]. management [6].
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Table 1 Spectrum of imaging findings in severe or complicated cholecystitis
AC acute cholecystitis; RA Rokitansky-Aschoff; GB gallbladder; DM diabetes mellitus; BMT bone marrow transplant; ESRD end-stage renal disease; XG xanthogranulomas; IP-OP in-phase and
opposed phase; TPN total parental nutrition
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Fig. 1 Hemorrhagic cholecysti-
tis: 81-year-old female, known
hypertension with severe RUQ
pain. (A) US image shows
echogenic debris suggesting
tumefactive sludge or hemor-
rhage in distended gallbladder
(arrow) and gallstones in the
fundus casting acoustic shadow-
ing (arrowhead). (B) Doppler
interrogation reveals normal
flow in the gallbladder wall
(arrow) mitigating against wall
necrosis, and no color uptake
within the luminal contents
represents sludge or blood clot
rather than a mass lesion. (C)
Axial non-contrast CT image
of abdomen demonstrates
hyperdense layering fluid in the
gallbladder (arrow) suggest-
ing hemorrhage. (D) Coronal
CECT image shows heteroge-
neously dense fluid collection
in the gallbladder (arrow) and
gallstone in the fundus region
(arrowhead). Patient was treated
with CT-guided cholecystos-
tomy, and thick sanguinous fluid
was drained. Eventually patient
underwent cholecystectomy
cholecystitis [8]. Similar to uncomplicated cholecystitis, mucosa or strands of fibrinous exudate, is more charac-
intraluminal sludge and gallstones can be seen in gangre- teristic of gangrenous cholecystitis[8].
nous cholecystitis. However, the presence of intraluminal Hyperdense gallbladder wall (34 to 50 HU) on unen-
membranes (Fig. 3A), which represent either sloughed hanced CT can help diagnose gangrenous cholecystitis but
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Fig. 2 Hemorrhagic cholecys-
titis secondary to adenocarci-
noma of GB. Non-contrast axial
CT image (A) shows fluid–fluid
level (arrow) with intrinsic
attenuation of dependent
fluid around 40 HU, indicat-
ing hemorrhage within the
gallbladder lumen. CTA arterial
phase image (B) shows contrast
extravasation (arrow) from an
enhancing mass lesion (arrow-
head) in the non-dependent
portion of the gallbladder
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Emergency Radiology
Fig. 4 Gangrenous cholecys-
titis (MRI). 59-year-old male
with right upper quadrant pain
and fever. (A) Axial CT image
shows gallstones and gallblad-
der wall thickening (arrow),
and no acute abnormality was
diagnosed. MRI was performed
in regard to severe symptoms.
(B) Axial fat-suppressed
T2-weighted image shows irreg-
ular gallbladder wall thickening
with increased signal intensity
(arrow). (C) Precontrast axial
fat-suppressed T1-weighted
image delineates irregular
wall thickening and mucosal
irregularity (arrow). (D) Post-
contrast axial fat-suppressed
T1-weighted image clearly
demonstrates the disruption of
mucosal layer (arrow head) and
additionally illustrates a tiny
fluid pocket in the gallbladder
wall representing abscess
enhancement and better delineation of mucosal disruption [41]. EC results from infection of the gallbladder wall by
(Fig. 4D) [40]. anaerobes like Clostridium sp., or other microorganisms
Although open cholecystectomy is more commonly used like Escherichia coli, Klebsiella sp., Proteus culgaris, and
to treat gangrenous cholecystitis than patients with acute Salmonella derby [42].
cholecystitis, laparoscopic cholecystectomy remains the The pathophysiology of EC is different from acute or
mainstay of treatment. The utilization of open cholecys- chronic cholecystitis. Acute or chronic cholecystitis is
tectomy was reported to be between 15 and 21% in one induced by obstruction of gallbladder neck or cystic duct
study [34], but it is unclear if the preoperative diagnosis of due to gallstones. In contrast, emphysematous cholecystitis
gangrenous cholecystitis influences the surgical approach. usually results from thrombosis or occlusion of the cystic
Severe pericholecystic inflammation, perforation, or con- artery leading to ischemic necrosis of the gallbladder wall
cerning preoperative physical examination findings can and subsequent gallbladder necrosis and secondary infec-
prompt open cholecystectomy. When adjusted for patient tion by gas-forming organisms. Compared to acute chol-
and operative characteristics, the differences in risk of mor- ecystitis, EC carries a higher risk of perforation, and the
tality between open and laparoscopic cholecystectomy was mortality rate is also considerably higher at 15% vs. 4%
not significant [34]. [42].
EC usually presents as right upper quadrant abdominal
Emphysematous cholecystitis pain, significantly accompanying clinical symptoms include
fever, nausea, and vomiting. EC poses a diagnostic dilemma
Emphysematous cholecystitis (EC) is an unusual and clinically when presenting symptoms are vague and indis-
life-threatening type of complicated cholecystitis with tinguishable from uncomplicated acute cholecystitis. Addi-
an incidence of 1 to 3% of acute cholecystitis cases. EC tionally, the symptoms may be very subtle in patients with
predominantly involves male patients aged 50 to 70 years diabetes mellitus and end-stage renal disease [43].
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Identifying gas in the gallbladder lumen or wall and/or yield false-negative results, and a calcified wall or multiple
in the biliary tract is the key imaging feature in diagnosing stones may mimic gas shadows and result in false-positive
emphysematous cholecystitis. It is imperative to ensure the results [45]. CT is a more sensitive and specific imaging
patient did not undergo any recent diagnostic or therapeutic study to recognize gas within the gallbladder lumen or
biliary tract intervention as a cause of luminal or mural gas. wall (Fig. 5B)[45]. Ancillary CT findings suggestive of EC
Some authors classify EC into three different stages based include pneumobilia, irregularity or discontinuity of gall-
on the location of gas on conventional radiographs: stage 1, bladder wall, pericholecystic fluid, and abscess formation
intraluminal gas; stage 2, intramural gas; and stage 3, gas in the liver [28]. MR imaging plays only a supplementary
within the pericholecystic tissues [44]. Plain radiograph role in the evaluation of EC with gas in the gallbladder
workup is unusual in the evaluation of RUQ pain; how- wall or lumen appearing as signal voids [31]. Gallstones
ever, intraluminal or intramural gas (Fig. 5A and B) can are usually differentiated from intraluminal gas by loca-
be identified on CT topogram images. Ultrasound is often tion: gas is identified as numerous floating signal void in
the initial mode of evaluation, though diagnosing EC can the non-dependent portion of the gallbladder lumen and/
be challenging on ultrasound. The imaging findings differ or within the bile ducts, whereas gallstones are seen in the
depending on the amount of gas in the gallbladder wall or dependent portion. Susceptibility artifact at air-tissue inter-
lumen: a fair amount of intramural or intraluminal gas will face is better appreciated on fat-suppressed T1-weighted,
produce highly echogenic reflectors with low level poste- T2-weighted, and black blood T2-weighted spin-echo pla-
rior shadowing and reverberation artifact known as dirty nar images than heavily T2-weighted images [31].
shadowing (ring down artifact) (Fig. 5C) [45]. Intraluminal Treatment requires aggressive care in the ICU with anti-
gas can form multiple small non-shadowing echogenic foci biotics, and fluid resuscitation until cholecystectomy can
that are mobile with a changes in the patient’s position, also be performed. Percutaneous drainage (Fig. 5D) has also
known as effervescent gallbladder [46]. On US, pockets of been used in the acute setting as a bridge to cholecystec-
gas in the pericholecystic region may obscure detail and tomy with favorable outcomes [47].
Fig. 5 Emphysematous
cholecystitis. A 68-year-old
male presents to ED. CT scout
image (A) shows air in the
lumen(arrowhead) and wall
of the enlarged gallbladder
(arrows). Axial CECT of the
abdomen (B) shows gas in the
wall of the gallbladder(arrows)
and an air-fluid level in the
lumen (arrowhead). Ultrasound
image (C) of the same patient
shows echogenic reflectors in
the gallbladder wall (arrow)
with dirty acoustic shadowing
and ring down artifact (arrow-
head). The patient was treated
with CT-guided cholecysto-
stomy, and axial CECT (D)
shows percutaneous transhe-
patic cholecystostomy tube
(arrow) within the gallbladder
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Acalculous cholecystitis
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Gallbladder perforation
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Emergency Radiology
gallstones, the gallbladder lumen distends leading to an in which a cholecystobiliary fistula forms between the gall-
ischemic change in the gallbladder wall, necrosis, and result- bladder and common bile duct or proximal bile ducts [66].
ant perforation. The fundus is the most frequent site of per- The most common clinical presentation is pain abdomen,
foration due to relatively lower vascular supply [3, 62, 64]. fever, and vomiting, and some patients may present with
Niemeier described three main types of gallbladder per- signs of peritonitis. The perforated gallbladder may also pre-
forations in 1934, including acute perforations into the peri- sent atypically, like abdominal wall abscess or liver abscess,
toneal cavity (type I), subacute perforations with walled-off perplexing the clinical presentation [67].
peri-cholecystic abscess (type II), and chronic perforations Discontinuity of the gallbladder wall and recognition of
with cholecystoenteric fistula formation (type III) [65]. The extraluminal gallstones are more reliable imaging findings to
majority of cases in the reported series is subacute/type II diagnose gallbladder perforation [68]. While US is often per-
[64, 65]. A rare fourth type has been described by Andersen formed as the initial imaging test, CT is more sensitive for
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Emergency Radiology
complications, including perforation [64]. Sonographic find- Emergency laparotomy is indicated in acute perforation
ing specific for perforation is “sonographic hole sign,” first of the gallbladder, particularly those with findings of large
described by Chau et al., which can be seen along with per- hemoperitoneum. However, laparoscopic cholecystectomy
icholecystic fluid or collection [69, 70]. While some authors has become an acceptable choice even in most severe com-
reported sonographic identification of the wall defect in 70% of plications of cholecystitis, despite free intraperitoneal bleed-
patients, other studies failed to identify a defect in any confirmed ing [72].
cases [3, 70, 71]. Boruah et al. demonstrated that US was able
to identify all cases when the defect in the gallbladder wall was
greater than 10 mm but could not make the diagnosis in type II Mimics of complicated cholecystitis
cases and type III cases with defects less than 10 mm [64]. with chronic etiology
CT findings specific for perforation include a defect in the
gallbladder wall (Fig. 8A and B) and extraluminal position Xanthogranulomatous cholecystitis
of gallstones (Fig. 8B) [28]. Initially described sonographi-
cally as a “hole sign,” defects in the gallbladder wall are Xanthogranulomatous cholecystitis (XGC) is an uncom-
more commonly seen at CT imaging (Fig. 8B) [71]. The mon sequela of cholecystitis and is typically seen in
other described findings are pericholecystic fluid, associ- women in their sixth or seventh decade [2]. Gallstones
ated abscess (or fluid collection), gallbladder wall thicken- are seen in 80% of cases of XGC [73]. XGC is a chronic
ing, layering gallbladder wall, gallbladder wall bulging or inflammatory disease of the gallbladder, and both focal
defect, and omental/mesenteric stranding, and peritoneal and diffuse forms of gallbladder involvement are reported.
air (Fig. 9A and B) [3, 71]. CT is valuable in recognizing Lipid-laden macrophages accumulate in the gallbladder
the type of perforation, extent of intraperitoneal free fluid, wall and form grayish-yellow nodules or streaks [74]. It is
and identifying complications like free intraperitoneal air believed that when the intraluminal pressure increases due
(Fig. 10A, B and C), bile leak, abscess formation, and small to obstruction of gallbladder outflow, superficial mucosal
bowel obstruction [28]. ulceration of the wall, or rupture of Rokitansky-Aschoff
Fig. 10 Gallbladder perforation,
type I acute free perforation as a
complication of gangrenous and
hemorrhagic gallbladder. Axial
CT images (A) and (B) depict
non-enhancing gallbladder wall
(arrow heads) and hyperdense
intraluminal contents (*) repre-
senting blood products within
a grossly distended gallblad-
der. Also note heterogeneous
intraperitoneal free fluid and
pockets of air (arrow). Coronal
CT image (C) shows heteroge-
neously dense intraperitoneal
free fluid (arrow) in commu-
nication with gallbladder and
surrounding omental/mesenteric
stranding
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Emergency Radiology
sinuses can lead to intramural extravasation of bile, occasionally the inflammatory process can extend to the
which results in an inflammatory response as histiocytes liver, colon, or surrounding soft tissues[74].
ingest chemically irritating cholesterol crystals [75, 76]. Pathophysiology of XGC helps in understanding the
Although XGC is a chronic form of cholecystitis, 22% of imaging findings. As mentioned earlier, the extravasa-
cases can present as acute cholecystitis[77]. Complica- tion of bile into the gallbladder wall and subsequent mural
tions are reported in 32% of cases and include perfora- inflammation causes diffuse GB wall thickening. On imag-
tion, abscess formation, and enterocutaneous fistulas, and ing, XGC may present as diffuse or focal gallbladder wall
Fig. 11 57-year-old-female (A).
US image shows diffuse hyper-
echoic gallbladder wall thicken-
ing (arrow). Note is made of
mucosal defect and perichole-
cystic fluid in the fundus of gall-
bladder (arrowhead). (B) Axial
CECT image shows thickened
gallbladder wall, intramural tiny
hypodense nodules, and severe
inflammatory striations in the
pericholecystic region (arrow).
(C) Coronal CT clearly depicts
the hypodense nodules in the
wall (arrow heads). (D) Coronal
CECT image more anteriorly
demonstrates enhancing fluid
filled collection adjacent to gall-
bladder wall suggesting abscess
formation (arrow) and spread of
inflammation to adjacent bowel
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Emergency Radiology
thickening, ranging from 3 to 25 mm, with or without dis- different treatment protocols that demonstrate significant
tinct wall margins [78]. On ultrasound, gallbladder wall levels of morbidity and mortality. Emergency radiolo-
thickening is hyperechoic (Fig. 11A) in comparison to gists should be aware of these imaging findings to provide
the liver, and Parra et al. noticed this finding in 100% of timely diagnosis, proper management, and expedite treat-
patients in their study [78]. On US, the other hallmark is the ment. Preoperative detection of this complicated cholecys-
identification of intramural hypoechoic nodules that repre- titis can help the care providers and operating surgeon to
sent foci of xanthogranulomatous inflammation or small be prepared for a potentially more complicated procedure
abscesses [79]. Additional recognized sonographic findings and course of recovery.
are disruption of the mucosal lining, pericholecystic fluid,
GB stones and sludge, and hypoechoic echogenicity of the
adjacent liver parenchyma [79, 80]. CT findings include Compliance with ethical standard
hypodense intramural nodules (5 to 20 mm), heterogeneous
enhancement of the wall, and infiltration into the perichole- Conflict of interest The authors declare that they have no conflict in-
terest.
cystic fat and adjacent liver parenchyma (Fig. 11B) [2, 81].
Goshima et al. describe five imaging findings to differenti- Disclosures Unrelated grant funding from NHTSA/CIREN.
ate XGC from gallbladder wall carcinoma: (1) continuous
linear enhancement of the mucosa, (2) intramural hypo-
attenuated nodules (Fig. 11C), (3) diffuse thickening of
the gallbladder wall (seen in 91% of XGC), (4) the absence
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