DOI:10.2214/AJR.07.3197
AJR 2008; 191:228-232
© American Roentgen Ray Society
Hepatobiliary and Pancreatic MRI and MRCP Findings in Patients with HIV Infection
Mehmet Bilgin1,2,
N. Cem Balci3,
Ali Erdogan4,
Amir Javad Momtahen3,
Samer Alkaade5 and
Wigbert S. Rau1
1 Department of Radiology, University Hospital Giessen and Marburg, Giessen,
Germany.
2 Turkish–German Health Foundation, Giessen, Germany.
3 Department of Radiology, St. Louis University and St. Louis University
Hospital, 3635 Vista Ave., St. Louis, MO 63110.
4 Department of Cardiology, University Hospital Giessen and Marburg, Giessen,
Germany.
5 Department of Gastroenterology, St. Louis University, St. Louis, MO.
Received September 21, 2007;
accepted after revision January 6, 2008.
Address correspondence to N. C. Balci
(ncbalci{at}gmail.com).
CME
This article is available for CME credit.
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Abstract
OBJECTIVE. The purpose of this article is to describe the spectrum
of MRI and MR cholangiopancreatography (MRCP) findings of hepatic, pancreatic,
and biliary manifestations in patients with HIV infection.
CONCLUSION. The spectrum of MRI and MRCP findings in HIV-infected
patients includes acute or chronic hepatitis (or both), pancreatitis,
cholangitis, acalculous cholecystitis, and biliary strictures that may
resemble primary sclerosing cholangitis. The presence of segmental
extrahepatic biliary strictures is characteristic of AIDS cholangiopathy.
Keywords: biliary tract • HIV • liver • MRI • pancreas
Introduction
Involvement of the liver, biliary tree, and pancreas is not rare during the
course of HIV infection. Opportunistic infections are the major causes of
AIDS-related hepatobiliary and pancreatic disease. Clinical symptoms and
supporting laboratory findings, including blood cultures and serology tests,
raise the suspicion for hepatobiliary or pancreatic involvement
[1–3].
ERCP reveals unique findings of biliary involvement; the first descriptions of
AIDS cholangiopathy were based on ERCP findings
[4,
5]. Pancreatic and hepatic
parenchymal imaging findings in patients with HIV infection include papillary
stenosis, biliary strictures involving long extrahepatic segments that are
shown on ERCP, hepatomegaly, periportal adenopathy, acalculous cholecystitis,
and acute or chronic pancreatitis, all of which are visualized on CT and
sonography [4]. ERCP is a
costly and invasive imaging technique for the screening of these patients, and
liver and pancreatic parenchymal infection cannot be diagnosed on ERCP. CT and
sonography may be diagnostic for the liver and pancreatic parenchymal
involvement; however, they fail to show the characteristic imaging features of
biliary abnormalities [1,
2,
5]. The combined use of
contrast-enhanced MRI and MR cholangiopancreatography (MRCP) can help in
evaluating both biliary disorders and parenchymal diseases of the liver and
the pancreas [6,
7]. Thus, HIV-related
hepatobiliary disease may be evaluated in one single session using combined
MRI and MRCP. To our knowledge, the spectrum of MRI and MRCP findings of
HIV-related hepatobiliary and pancreatic disease has not been reported.
The purpose of this retrospective study was to review the spectrum of
hepatobiliary and pancreatic MRI and MRCP findings in patients with HIV
infection.
Materials and Methods
We conducted a retrospective review of the charts of all patients who were
referred to our clinics for pancreaticobiliary disease who had HIV infection
and underwent MRI and MRCP between January 2003 and November 2006. Patients
with a preexisting hepatobiliary disease before HIV diagnosis were not
included in this study. This study was HIPAA-compliant; the institutional
review board approved the study and waived the requirement for informed
consent for our review of patient data.
Thirty-one patients (19 men, 12 women; age range, 34–64 years; mean,
48.3 years) were identified who underwent MRCP and MRI of the upper abdomen at
the same session. All patients met the criteria for the diagnosis of AIDS as
defined by the Centers for Disease Control
[8]; and the onset of
hepatobiliary symptoms was 2–3 years (mean, 2.64 years) after the
initial AIDS diagnosis. The indications for the MRI and MRCP referrals were as
follows: isolated or combined presence of elevated liver enzymes (n =
8), elevated cholestasis markers (n = 12), low fecal elastase I
(n = 8), right upper quadrant pain (n = 14), or high fever
(n = 5). Twenty patients underwent MRI and MRCP as the initial
examination. In 11 patients, MRI and MRCP were performed as complementary
imaging to sonography or CT of the abdomen. Two patients had histopathologic
proof of granulomatous hepatitis (n = 1) and chronic active hepatitis
(n = 1). Blood cultures revealed Mycobacterium tuberculosis
(n = 1) and Cryptococcus organisms (n = 1); and in
two patients serology tests revealed hepatitis C infection. In two patients,
Cryptosporidium parvum was isolated on cytologic analysis of the
ERCP-guided bile duct brushings. Other final diagnoses relied on ERCP alone
(n = 4), low fecal elastase I (n = 8), and histopathology of
the gallbladder wall (n = 1) in patients with abnormal imaging
findings. Five patients had established MRI and MRCP findings and associated
clinical and laboratory findings.
All patients underwent combined MRI of the upper abdomen and MRCP. MRI was
performed on a 1.5-T MR scanner (Intera, Philips Medical Systems) using a
four-element quadrature phased-array surface coil. The standard upper abdomen
MRI protocol consisted of the following imaging sequences and parameters:
T1-weighted spoiled gradient-echo dual-phase (TR range/TE range,
140–170/4.4–2.2; flip angle, 70°) and single-shot fast
spin-echo (TR/TE, infinite/80) sequences with and without fat saturation. All
images were obtained in the axial plane with 6-mm section thickness and
160–190 x 256 matrix with the sensitivity-encoding (SENSE) factor
of 2. MRCP images were obtained using 2D breath-hold thick-slab T2-weighted
fat-saturated single-shot fast spin-echo images (infinite/1,200) with a slab
thickness of 30–50 mm in 12 paracoronal planes constituting an angle of
360°. For the acquisition of each plane, patients held their breath for 5
seconds. Gadopentetate dimeglumine (Magnevist, Bayer HealthCare) was injected
in a dose of 0.1 mmol/kg of body weight as a bolus injection at 2 mL/s using a
power injector (Spectris MR Injector, Medrad). Images were acquired at 18
(arterial dominant phase), 45 (portal venous phase), and 90 (late venous
phase) seconds after contrast admini stration. For serial contrast-enhanced
images, a T1-weighted 2D spoiled gradient-echo sequence (TR range/TE,
140–170/4.4; flip angle, 70°) was used with (n = 19) or
without (n = 12) fat saturation. All late venous images were obtained
with fat saturation.
All images were loaded to a workstation (Easy Vision, Philips Medical
Systems) and reviewed by two fellowship-trained radiologists in consensus.
Both radiologists had more than 5 years of experience in interpreting
abdominal MRI and MRCP. During evaluation of the images, both radiologists
were blinded to clinical information. On MRI, the liver and pancreas sizes and
parenchymal findings were assessed on T1- and T2-weighted images; contrast
enhancement of the liver, pancreas, gallbladder, and bile duct walls was
evaluated on serial contrast-enhanced images. On MRI, liver was evaluated for
the homogeneous or heterogeneous enhancement on arterial phase images, size,
signal change on in-phase and out-of-phase images as a marker for steatosis,
and the presence of nodules. Hepatomegaly was considered when the liver
dimensions exceeded 22 cm across its widest point, 17 cm at its greatest
vertical height (slice thickness x number of slices), and 12 cm in
anteroposterior distance. The pancreas was evaluated for its enhancement in
the arterial and portal venous phases; delayed increased enhance ment was
considered to represent chronic pan creatitis
[7]. The biliary tree was
evaluated for enhancement and thickening of the bile ducts and gallbladder
wall. Gallbladder wall thickness and dimensions were measured on
contrast-enhanced late venous phase images from the sections showing the
thickest part of the wall and the largest transverse gallbladder dimension.
Increased gallbladder wall thickening was deter mined to exist when the
gallbladder wall thick ness exceeded 3 mm. Increased bile duct enhancement was
considered when bile ducts revealed more enhancement than the background liver
or pancreas on late venous phase images. Cholangitis was considered when
patchy in creased arterial enhancement of the periductal intrahepatic segments
of the biliary tree and intense late enhancement of the intra- and
extrahepatic bile ducts were present. On MRCP, the caliber of the common bile
duct (CBD), the intrahepatic bile ducts, and the main pancreatic duct,
including its side branches; the presence and length of strictures; and the
presence of a stone in the CBD, main pancreatic duct, and gallbladder lumen
were evaluated.
Results
Eight patients revealed normal MRI and MRCP findings. In 23 patients, MRI
and MRCP findings were present. The CD4 T lymphocyte count was
200–500/mm3 (mean, 343.5/mm3) in 12 patients,
100–200/mm3 (mean, 183.5/mm3) in five patients,
and less than 100/mm3 (mean, 88/mm3) in six patients.
Findings were present in the liver (n = 6), pancreas (n =
14), and biliary sys tem (n = 14). Combined biliary and pancreatic
findings were present in nine patients, and combined biliary and hepatic
findings were present in two patients.
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Fig. 1A —48-year-old man with AIDS and Mycobacterium
tuberculosis infection. On T1-weighted spoiled gradient-echo images
(TR/TE, 140/4.4; flip angle, 70°) of liver, arterial phase (A)
reveals nodular enhancement that fades on late phase (B).
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Fig. 1B —48-year-old man with AIDS and Mycobacterium
tuberculosis infection. On T1-weighted spoiled gradient-echo images
(TR/TE, 140/4.4; flip angle, 70°) of liver, arterial phase (A)
reveals nodular enhancement that fades on late phase (B).
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Liver findings included heterogeneous patchy arterial phase enhancement
(n = 2) in patients with chronic active hepatitis, and nodular liver
parenchyma (n = 2) with increased enhancement of nodules during the
arterial phase that became indistinguishable from the background liver
enhancement in the late venous phase images in patients with diagnosed or
suspected granulomatous hepatitis (Fig.
1A,
1B). Other liver parenchymal
findings included hepatomegaly (n = 6) and hepatosteatosis
(n = 3). In two patients, periportal lymph nodes (n = 5)
were present; their sizes ranged from 2 to 5 cm (mean, 3.2 cm).
Enhancement of the pancreatic parenchyma increased gradually in venous
phase images compared with arterial phase images in nine patients. MRCP
revealed side branch ectasia in 12 patients and main pancreatic duct
dilatation in four patients (Fig.
2A,
2B,
2C). In one patient, a
pseudocyst was present. In five patients, the gallbladder lumen contained
multiple small stones (Fig. 3A,
3B,
3C). None of the patients
underwent cholecystectomy before MRI and MRCP. In one patient, gallbladder
wall thickening with increased contrast enhancement and pericholecystic fluid
were present without the presence of intraluminal stones, which was consistent
with acalculous cholecystitis (Fig.
4) and was confirmed during cholecystectomy.
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Fig. 2A —43-year-old woman with HIV infection. MR
cholangiopancreatography image reveals terminal segmental stricture of dilated
common bile duct (CBD) (long arrow) as well as dilatation and side
branch ectasia of main pancreatic duct (short arrows).
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Fig. 2B —43-year-old woman with HIV infection. On corresponding
arterial phase T1-weighted fat-saturated spoiled gradient-echo MR images
(TR/TE, 140/4.4; flip angle, 70°), pancreatic gland (arrow)
enhances less on arterial phase (B) than on early venous phase
(C).
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Fig. 2C —43-year-old woman with HIV infection. On corresponding
arterial phase T1-weighted fat-saturated spoiled gradient-echo MR images
(TR/TE, 140/4.4; flip angle, 70°), pancreatic gland (arrow)
enhances less on arterial phase (B) than on early venous phase
(C).
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Fig. 3B —52-year-old man with HIV infection. Segmental stricture is
present in terminal common bile duct that is better seen on a different MRCP
projection (arrow, B) and on corresponding ERCP image
(arrow, C).
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Fig. 3C —52-year-old man with HIV infection. Segmental stricture is
present in terminal common bile duct that is better seen on a different MRCP
projection (arrow, B) and on corresponding ERCP image
(arrow, C).
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Fig. 4 —48-year-old man with HIV infection and acalculous
cholecystitis. Contrast-enhanced T1-weighted spoiled gradient-echo image
(TR/TE, 140/4.4; flip angle, 70°) shows gallbladder wall thickening and
increased wall enhancement as well as pericholecystic fluid
(arrow).
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In 11 patients, CBD dilatation with distal tapering was present; the mean
diameter was 8.9 mm (range, 8.4–11.2 mm). Intrahepatic biliary
dilatation was a coexistent finding with all CBD dilatations. Extrahepatic
segmental terminal CBD stricture with a measured length of 1–3 cm (mean,
1.5 cm) was observed in four patients (Figs.
3A,
3B,
3C and
5A,
5B). In seven patients, focal
strictures were present in the intrahepatic bile ducts, causing saccular
dilatations of the intrahepatic bile ducts resembling primary sclerosing
cholangitis (Fig. 5A,
5B). Intra- and extrahepatic
strictures were confirmed in four patients on ERCP.
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Fig. 5A —54-year-old woman with HIV infection and right upper quadrant
pain. MR cholangiopancreatography image shows multiple strictures (short
thin arrows) that cause saccular dilatation of bile ducts and diffuse
biliary dilatation of left liver lobe (short thick arrow). Segmental
terminal common bile duct (CBD) stricture is also noted (long
arrow).
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Fig. 5B —54-year-old woman with HIV infection and right upper quadrant
pain. Corresponding contrast-enhanced late venous phase T1-weighted
fat-saturated spoiled gradient-echo image shows intense enhancement of distal
CBD wall (white arrow) and intrahepatic bile duct wall (black
arrow).
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In two patients with a dilated CBD, papillary stenosis was diagnosed on
ERCP using the criteria of CBD diameter greater than 8 mm and associated 2- to
4-mm distal tapering and contrast retention in the CBD
[5]. On contrast-enhanced MRI,
two patients with findings resembling those of primary sclerosing cholangitis
revealed subtle patchy increased arterial enhancement of the liver parenchyma;
and in seven patients, increased enhancement of the CBD and an intrahepatic
bile duct wall were seen on the late venous images. Frequency of findings and
the associated CD4 T lymphocyte counts are listed in
Table 1.
Discussion
The spectrum of hepatobiliary and pancreatic imaging findings on MRI and
MRCP was not different from previous reports of clinicopathologic and
radiologic assessment of HIV patients with associated clinical symptoms
[1–5].
In HIV-infected patients, parenchymal liver disease occurs in the setting of
fungal, protozoan, or bacterial opportunistic infections or exacerbation of
preexisting viral hepatitis by superimposed HIV infection
[3]. Granuloma formation is
observed in fungal and mycobacterial manifestations of the liver. In two
patients, we observed findings similar to previously described MRI findings of
granulomatous hepatitis with nodular liver parenchyma and indistinguishable
enhancement of the nodules from background liver parenchyma
[9]. Patchy arterial phase
parenchymal enhancement has been described as a characteristic imaging feature
in patients with chronic active hepatitis and was also observed in two of our
cases with positive serology for hepatitis C
[10]. Other rare causes of
AIDS-related hepatic parenchymal involvement include vascular lesions such as
Kaposi's sarcoma, peliosis hepatis, and drug-induced hepatosteatosis
[3].
Pancreatitis occurs during the course of HIV infection and is attributed to
HIV-related medications or, to a lesser degree, to opportunistic infections.
The acute form of pancreatitis is observed more frequently in patients with
HIV infection [2,
5]. In our patient population,
we observed MRI and MRCP findings of chronic pancreatitis, including
pancreatic duct changes according to the Cambridge classification
[11] and associated decreased
contrast enhancement of the gland in the arterial phase images compared with
early venous phase images. This gradually increasing enhancement has been
observed in patients with chronic pancreatitis
[7].
Biliary tract disorders in HIV-infected patients are grouped as AIDS
cholangiopathy. The spectrum of disorders involved in AIDS cholangiopathy
includes acalculous cholecystitis, sclerosing cholangitis, papillary stenosis,
lymphoma, Kaposi's sarcoma, and gallstones
[4]. Patients are usually
affected when the CD4 T lymphocyte count is less than 100/mm3;
however, 20% of cases may have findings in which the CD4 T lymphocyte count is
greater than 100/mm3. Several pathogens are responsible for the
opportunistic infections, Cryptosporidium parvum and cytomegalovirus
being the most frequently involved
[2,
4]. In two of our patients,
Cryptosporidium organisms were identified in bile aspirates.
Previously described imaging features of AIDS cholangiopathy rely on
cholangiographic patterns that include findings resembling those of primary
sclerosing cholangitis and the presence of papillary stenosis, papillary
stenosis alone, the isolated presence of findings resembling those of primary
sclerosing cholangitis, and segmental extrahepatic bile duct strictures.
Biliary strictures are most likely caused by chronic inflammation by one or
more opportunistic pathogens
[2]. The diagnosis of papillary
stenosis is made when a dilated CBD reveals tapering at its terminal portion
and when marked and delayed contrast retention occurs during ERCP
[4]. On MRCP, we observed
dilatation of CBD with distal tapering that was associated with papillary
stenosis on ERCP. However, there are no established criteria on MRCP for the
diagnosis of papillary stenosis, which is believed to be caused by recurrent
inflammation at the papilla by the previous ly mentioned pathogens.
Extrahepatic segmental biliary strictures and primary sclerosing
cholangitis-type strictures also develop during the inflammatory process
[2,
4]. In our patient population,
we observed the entire previously mentioned spectrum of imaging findings on
MRCP.
On MRI, we saw thickening and enhancement of the CBD wall as well as
enhancement along the intrahepatic bile ducts that is associated with
cholangitis [6].
Contrast-enhanced T1-weighted fat-saturated images show the enhancement and
thickening of the bile duct walls, which were also seen in our patients.
Previously described MRI and MRCP findings of primary sclerosing cholangitis
include increased segmental arterial enhancement in the liver parenchyma,
predominantly in the periphery
[12]; we observed this finding
in two patients. Unlike the MRCP findings of primary sclerosing cholangitis,
we also observed longer extrahepatic bile duct strictures that have been
described as one of the cholangiographic patterns of AIDS cholangiopathy
[2,
4]. Biliary strictures in AIDS
cholangiopathy are indistinguishable from primary sclerosing cholangitis in
the absence of segmental extrahepatic biliary strictures; clinical history may
help to distinguish one from the other.
Acalculous cholecystitis has been reported to occur during HIV infection.
We observed one case of acute acalculous cholecystitis that was best shown
with increased enhancement and thickening of the gallbladder wall seen on
contrast-enhanced T1-weighted fat-saturated images, as described in a recent
article [13].
With the combined use of MRI and MRCP, we were able to show imaging
findings of hepatobiliary involvement during HIV infection in a single imaging
session. Hepatic and pancreatic infections did not reveal unique imaging
findings associated with HIV infection; however, on MRCP segmental
extrahepatic biliary strictures were characteristic of HIV-related
cholangitis.
This study has some limitations. First, with the limited number of patients
we could not evaluate the broader spectrum of MRI and MRCP findings, including
Kaposi's sarcoma and peliosis hepatis in the liver. Second, we had a limited
number of patients who had a histopathologic or ERCP final diagnosis of
hepatobiliary involvement. Therefore, the sensitivity of MRI and MRCP was not
determined in this study, especially in patients with normal imaging findings
in the absence of a final diagnosis.
In conclusion, we describe the spectrum of hepatobiliary and pancreatic MRI
and MRCP findings in HIV-infected patients. Contrast-enhanced MRI showed
inflammatory parenchymal changes and increased patchy arterial enhancement of
the liver and decreased arterial enhancement in patients with chronic
pancreatitis. MRCP findings of AIDS cholangiopathy were similar to those of
primary sclerosing cholangitis with associated segmental extrahepatic biliary
strictures in AIDS cholangiopathy; MRI findings included biliary tract and
gallbladder wall contrast enhancement. Although the presented findings were
not specific for HIV, the combination of our described findings and the
presence of segmental extrahepatic biliary strictures may be considered novel
MRI features of HIV-related hepatobiliary and pancreatic disease.
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Abstract
Introduction
