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Clinical Radiology xxx (2017) 1e6

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Clinical Radiology
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Imaging appearances of hepatic tuberculosis:


experience with 12 patients
L.S. Ch’ng a, *, H. Amzar a, K.C. Ghazali b, F. Siam b
a
Department of Radiology, Sarawak General Hospital, Kuching, Malaysia
b
Department of Hepatobiliary Surgery, Sarawak General Hospital, Kuching, Malaysia

art icl e i nformat ion AIM: To review computed tomography (CT), ultrasound (US), magnetic resonance chol-
angiopancreatography (MRCP), endoscopic retrograde cholangiopancreatography (ERCP) and
Article history: percutaneous transhepatic cholangiogram (PTC) appearances and their diagnostic value in
Received 14 July 2017 hepatic tuberculosis.
Accepted 23 October 2017 MATERIALS AND METHODS: The imaging studies for 12 patients with biopsy-proven hepatic
tuberculosis from January 2012 till March 2014 were reviewed retrospectively. These cases
were confirmed via ultrasound-guided biopsy.
RESULTS: The patients were aged 24e72 years. Four patients had parenchymal tuberculosis
only and eight patients had mixed parenchymal and biliary duct involvement. The paren-
chymal tuberculosis patients showed poorly enhancing, hypodense nodules on CT with central
calcification and adjacent dilated intrahepatic ducts. Most patients had multiple lesions except
for two patients with a single lesion. The size of the lesions ranged from 0.5 to 6 cm. Seven
patients with biliary duct involvement showed a hilar strictures involving the intrahepatic
ducts and common bile duct. Nine of the patients showed hilar stricture with atrophy of the
ipsilateral lobe of the liver and compensatory hypertrophy of the contralateral lobe. Hep-
atolithiasis was seen in five patients. Tuberculous lung involvement was seen in seven patients.
CONCLUSION: The presence of calcified and hypodense nodules with biliary duct dilatation
associated with lobar atrophy were the most consistent features of hepatic tuberculosis,
especially in the presence of active lung disease.
Ó 2017 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction Hepatic TB is a rare but curable disease. The diagnosis of


hepatic TB is difficult due to non-specific symptoms and
Tuberculosis (TB) is a common disease in underdevel- signs, as well as variations of non-specific imaging findings.
oped and developing nations, especially in low socioeco- Initial clinical and radiological evaluations provide indirect
nomic groups. Once the diagnosis is confirmed, the disease evidence of the presence and locations of involvement. For
is usually associated with good prognosis provided anti-TB confirmation, tissue samples need to be obtained for his-
treatment is completed. tological and microbiological evaluation. Imaging, such as
ultrasonography (US) and computed tomography (CT),
complemented by endoscopic evaluations, such as endo-
* Guarantor and correspondent: C. L. Shyan, Department of Radiology, scopic retrograde cholangiography (ERCP) and endoscopic
Sarawak General Hospital, Jalan Hospital, 93586 Kuching, Sarawak, Malaysia. ultrasonography (EUS), are not only the mainstay of in-
Tel.: þ603 61454333; fax: þ603 61454111.
E-mail address: lishyanc@yahoo.com (L.S. Ch’ng).
vestigations, but also direct and assist in tissue sampling.

https://doi.org/10.1016/j.crad.2017.10.016
0009-9260/Ó 2017 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Please cite this article in press as: Ch’ng LS, et al., Imaging appearances of hepatic tuberculosis: experience with 12 patients, Clinical Radiology
(2017), https://doi.org/10.1016/j.crad.2017.10.016
2 L.S. Ch’ng et al. / Clinical Radiology xxx (2017) 1e6

Many different classifications for hepatic TB have been 107 sequences. Most patients had multiple lesions except two
proposed.1e3 patients who had single lesions. The size of the lesions
Although some classify hepatic TB into serohepatic type ranged from 0.5 to 6 cm. The lesions tend to enlarge and
and parenchymal type, with tuberculous cholangitis being a appear more well-defined over time if untreated (Fig 1).
separate pathological/radiological entity,1 others classify Single lesions tend to be larger (>5 cm) and occur in
tuberculous cholangitis as part of parenchymal type of he- older age groups (50 and 70 years old). The location of
patic TB.4 The parenchymal type, which is the most com- single lesions are subdiaphragmatic (S7 and S8) and exo-
mon among the three types, can be further be subdivided phytic. Singular lesions have poor rim enhancement and
into miliary, nodular, and mixed TB. may be septated (Fig 1). One lesion had coarse rim calcifi-
Although the imaging features (CT and magnetic reso- cation (Fig 2).
nance imaging [MRI]) of hepatic TB have been described, Multiple lesions were located in either/both lobes of the
the imaging appearance of these lesions is considered non- liver and in difference phases of disease. There were calci-
specific. Histopathological or bacteriological confirmation is fications/hepatolithiasis and atrophy/fibrosis in one lobe of
often required especially when malignancy needs to be the liver, whereas enhancing lesions were found in the
excluded.5,6 contralateral lobe (Fig 3).

Materials and methods Biliary (duct) TB

The imaging studies of 12 patients with biopsy-proven Eight patients with biliary duct involvement showed
hepatic TB from January 2012 till March 2014 were strictures involving the intrahepatic ducts and/or common
reviewed retrospectively. Ethics committee approval was bile duct (CBD). Intrahepatic strictures usually form later at
not required as the liver biopsies and imaging were done to areas of previous granulomas (Fig 4). Biliary stricture at the
aid in the diagnosis and management of patients. The pa- right or left hepatic duct results in atrophy of the ipsilateral
tients were aged between 24e72 years (mean age of 45 lobe of the liver with compensatory hypertrophy of the
years) and there were six male and six female patients. contralateral lobe noted (Fig 3). Out of nine patients with
These patients were initially referred to the hepatobiliary lobar atrophy, two patients had a bile lake (Fig 5). The bile
department for liver masses, so the series only contained lakes occurred in the atrophied right lobe of the liver
cases of macronodular parenchymal TB. (Table 1). Hepatolithiasis was also seen in five patients.
CT, US, MRI cholangiopancreatography (MRCP), endo- There were no patients with solely biliary disease.
scopic retrograde cholangiopancreatography (ERCP), and
Extra-hepatic TB manifestations
percutaneous transhepatic cholangiogram (PTC) images of
the 12 patients were reviewed retrospectively and the
TB frequently presents as a systemic disease. Therefore
diagnostic value of their radiological appearances was
extrahepatic TB needs to be investigated in these patients.
evaluated. No standard protocol was outlined for the scans
Lung involvement of TB was seen in six patients either on
as the radiological studies were analysed retrospectively
chest radiography or CT. One of the patients had humeral
from two community hospitals.
bone TB. A splenic focus of TB was seen in one patient.
Ultrasound-guided biopsy of the liver lesions was per-
Upper abdominal lymphadenopathy was seen in four pa-
formed for all 12 patients. Biopsies yielded acid-fast bacilli
tients. The nodes did not have the typical matted with
(AFB) or showed caseous necrosis with occasional Langhans
necrotic centre appearance. Two patients had ascites. There
giant cell on histology. Alternatively, diagnosis was also
were no cases with associated pancreatic, adrenal, or peri-
confirmed by polymerase chain reaction (PCR) of the biopsy
toneal involvement in the present series.
tissue.
Correlation with liver function tests
Results
Bilirubin levels in patients with intra- and extrahepatic
Four patients with parenchymal TB and eight patients strictures were higher than in patients with only intra-
with mixed parenchymal and biliary duct involvement were hepatic strictures (p¼0.05) using the Mann-Whitney. Mean
observed. The majority of patients were either farmers or total bilirubin in patients with intra- and extrahepatic
housewives with two thirds being referred from rural areas strictures was 274 mmol/l (SD 50). Patients with only
and district hospitals. Besides that, two thirds of patients intrahepatic biliary strictures had a mean total bilirubin of
were referred from rural areas and district hospitals. 46 mmol/l (SD 33).
Hepatic (parenchymal) TB
Discussion
Parenchymal tuberculous patients showed hypodense
nodules on CT with poor rim enhancement, central calcifi- Despite advances in TB control through improved
cation, and adjacent dilated intrahepatic ducts. The hypo- nutrition, reduced crowding, public health measures, and
dense nodules were noted to be hypoechoic on ultrasound, effective chemotherapy, TB is still common today and re-
hypointense on T1-weighted (W) and hyperintense on T2W sults in significant morbidity and mortality. It has been

Please cite this article in press as: Ch’ng LS, et al., Imaging appearances of hepatic tuberculosis: experience with 12 patients, Clinical Radiology
(2017), https://doi.org/10.1016/j.crad.2017.10.016
L.S. Ch’ng et al. / Clinical Radiology xxx (2017) 1e6 3

Figure 1 (a) Transverse US image of a 50-year-old woman showed a heterogeneous lesion (*) in segment V/VIII, which is larger and more well-
defined in subsequent US performed 2 months later (b). (c) The CT image shows a multiseptate exophytic lesion (*) in segment V/VIII.

Figure 2 (a) US image of a 70-year-old woman showing an isoechoic lesion (*) in segment VII with wall calcification (thin arrow). (b) A poorly
enhancing hypodense lesion (*) with wall calcification seen on CT. The lesion (*) is hyperintense on the T2W (c) and hypointense on the T1W
sequences (d). The small splenic lesion (thick arrow) was hypodense on CT and hyperintense on T2W imaging.

Figure 3 Longitudinal view of (a) US and (b) CT images of the abdomen of a 24-year-old man showing hypoechoic and hypodense nodules in the
right lobe (arrowhead). Hepatolithiasis (thin arrows) and left lobe atrophy noted. (c) ERCP demonstrating truncated left hepatic duct near
bifurcation (thick arrow) with right intrahepatic duct stricture (*).

Please cite this article in press as: Ch’ng LS, et al., Imaging appearances of hepatic tuberculosis: experience with 12 patients, Clinical Radiology
(2017), https://doi.org/10.1016/j.crad.2017.10.016
4 L.S. Ch’ng et al. / Clinical Radiology xxx (2017) 1e6

Figure 4 (a) US image of a 27-year-old man showing a heterogeneous hypoechoic nodule (thick arrow), which was smaller 3 months ago on CT
(b) and shows central calcification with hypodense rim. Dilated distal intrahepatic ducts noted (thin arrow). MRI images show the lesion with
concentric rings (target appearance), which was predominantly hypointense on T1W (c) and hyperintense on T2W (d). (e) MRCP demonstrates
biliary strictures at the right intrahepatic and left hepatic ducts (arrowhead).

estimated two billion people have latent TB, with approxi- accounts for 15.5% of the reported TB cases in Malaysia in
mately 7e8 million new cases are detected worldwide 2013. Abdominal involvement in TB is one of the most
annually; however, in underdeveloped nations in particular, prevalent forms of extrapulmonary manifestations, and
two million affected individuals succumb to this infection generally refers to gastrointestinal, splenic, pancreatic,
annually even though TB is treatable.7 The increased inci- hepatobiliary, and abdominal lymph node involvement.10
dence of TB has been attributed to several causes, including The small bowel was the most commonly affected site
the acquired immunodeficiency syndrome (AIDS) epidemic, (33.8%), followed by the peritoneum (30.7%), large bowel
intravenous drug abuse, and an increase in the number of (22.3%), liver (14.6%), and the upper gastrointestinal tract
immunocompromised patients.8,9 (8.5%).3 Primary hepatic TB is rare because low oxygen
In the present study, TB tended to occur in patients in tension in the liver is unfavourable for the growth of
the age range of 25e55 years, particularly in the 25e34- mycobacteria.11
years category, which comprises 19.5% of patients with Most of the cases were referred from rural areas with the
TB in Malaysia in the year 2013. Extrapulmonary TB majority of patients being farmers.

Figure 5 (a) US images of a 33-year-old man showing a cavity/bile lake (*) in the right lobe of liver with adjacent echogenic (partially calcified)
nodules (thick arrows). Dilated left intrahepatic ducts seen (arrowheads). (b) CT demonstrated a bile lake (*) with calcified and non-calcified
nodules (thick arrows). (c) Cholangiogram showing dilated left intrahepatic ducts (arrowhead) connected to the bile lake (*) via biliary stric-
ture at the hilum (thin arrow). CBD with stent in situ (þ) is in continuity with the bile lake. Multiple filling defects seen in the bile lake are due to
the nodules within.

Please cite this article in press as: Ch’ng LS, et al., Imaging appearances of hepatic tuberculosis: experience with 12 patients, Clinical Radiology
(2017), https://doi.org/10.1016/j.crad.2017.10.016
L.S. Ch’ng et al. / Clinical Radiology xxx (2017) 1e6 5

Table 1 tuberculous granuloma, liquefactive necrosis, fibrosis, and


Incidence and location of biliary stricture. calcification occurring synchronously.1 The parenchymal
Location of biliary stricture No. of patients lesions in the present series showed rim enhancement or
Intrahepatic ducts only 2 poor enhancement. These findings are in keeping with
Intrahepatic ducts and common bile duct 3 central caseous necrosis with surrounding granulation tis-
Truncated right or left hepatic duct 3 sue that enhances. Calcifications, which range from small
No biliary stricture 4
isolated specks to coarse calcifications was found in the
present series, with one case of rim calcification.
Although considered to be a rare clinical entity, hepatic Parenchymal tuberculous macronodules were generally
TB it is the most common manifestation of upper abdomen hypodense nodules with mild peripheral rim enhancement
parenchymal organ TB and its incidence has also been on CT16,17; however, their appearance varied and may
increasing. The liver is a common site for granuloma for- appear similar to tumour such as metastases, lymphoma, or
mation owing to its rich blood supply, located at the distal pyogenic abscesses due to its multiplicity.18 Other features
end of the portal circulation as well as due to large number such as adjacent dilated intrahepatic ducts and coarse he-
of reticuloendothelial cells. Although hepatic TB is reported patic or nodal calcifications may suggest the diagnosis of TB.
to occur in 50e80% of patients who were dying from pul- The hypodense nodules were hypoechoic on ultrasound,
monary TB,12 most of the cases were usually clinically silent. hypointense on T1W, and hyperintense on T2W sequences.
Patients usually become symptomatic when they present Most patients had multiple lesions except two patients who
with cholangitis due to biliary obstruction secondary to had single lesions. Single lesions were more likely to be
biliary stricture. Therefore, hepatic TB is possibly under- abscesses than granulomas. Caseous material was aspirated
diagnosed and under-reported in clinical practice. Patients from the singular lesions.
with hepatic TB in this study were relatively young with Hepatic TB nodules were noted to be hypointense with
mean age of 47 years. Overall, the prevalence of abdominal an isointense rim on T1W imaging and hypointense, iso-
TB has been shown to correlate with the severity of pul- intense, or hyperintense with a less intense rim on T2W
monary TB. Prompt diagnosis and early treatment is needed imaging. Peripheral enhancement or internal septal
to reduce morbidity and mortality in this productive age enhancement was noted on contrast-enhanced MRI.16,19
group. The rim is likely due to peripheral granulomatous tissue.
Unless there is a high index of suspicion, the diagnosis of Pure biliary involvement is said to be extremely rare and
hepatic TB is often overlooked.13 Granulomas were usually occurs mainly in children. Strictures can be simple or mul-
located near the portal tract and there was only mild tiple. Isolated or complex calcifications may be seen along
perturbation of hepatic function, so most patients were the course of the bile ducts.20 Management of biliary
minimally symptomatic or asymptomatic. Abdominal mass, strictures includes biliary drainage along with standard
hepatomegaly, and jaundice were the most frequent clinical anti-TB therapy and possibly surgery. Although isolated
symptoms and signs. Other clinical manifestation of hepatic strictures can be managed easily with sequential placement
TB include right upper abdominal pain, upper abdominal of multiple plastic stents, multiple or complex strictures are
tenderness, low-grade fever, night sweat, weight loss, and more challenging and require combination therapy via
fatigue.2,4 Anaemia, raised erythrocyte sedimentation rate endoscopy, a percutaneous approach, and surgery.
(ESR), abnormal hepatic function, and positive tuberculin The classical findings were irregular dilated intrahepatic
test were other possible manifestations. Similar clinical ducts or diffuse miliary nodules. Even though 70% of patients
presentation was seen in the present series. had biliary involvement in the present series, this was asso-
The clinical classification and nomenclature of hepatic TB ciated with macronodular parenchymal disease in all pa-
is still unclear.3,11,14,15 While Levine has classified the cases tients. It is postulated that biliary strictures form at the site of
into miliary TB, pulmonary TB with hepatic involvement, granulomas, suggesting stricture formation secondary to
primary liver TB, focal tuberculoma or abscess, and tuber- healing of the granulomas. In the present series, the majority
culous cholangitis [3], Reed divided it into only three forms: of strictures occurred in the intrahepatic ducts with
TB of the liver associated with generalised miliary TB, pri- involvement of the CBD and hilum being less frequent.
mary miliary TB of the liver, and primary tuberculoma or Radiologically, it was difficult to exclude cholangiocarcinoma
abscess of the liver [14]. In the present study, pathological in this group of patients.
classification was chosen, which is divided into serohepatic, Hilar stricture causes chronic biliary obstruction lead-
parenchymal, and cholangitis subgroups. Serohepatic refers ing to secondary biliary cirrhosis and eventually atrophy
to subcapsular miliary liver lesions, which is the least of the affected lobe.7 In addition, bile lakes were also seen
common presentation. Parenchymal lesions are further as a sequela to chronic biliary obstruction. Although it is
subdivided into micronodular/miliary (<2 cm), macro- reported that splenic involvement is common in patients
nodular (>2 cm), and mixed micronodularemacronodular with hepatobiliary TB, particularly in patients with human
lesions. immunodeficiency virus (HIV)/AIDS, the patient with
In the present series, the parenchymal form was found to splenic involvement in the present series did not have
be the dominant type. The main CT features of hepatic TB HIV/AIDS. Half of the patients have concomitant pulmo-
were the presence of multiple lesions of varying densities nary TB in keeping with the haematogenous spread of
indicating lesions at different pathologic stages, i.e., infection.

Please cite this article in press as: Ch’ng LS, et al., Imaging appearances of hepatic tuberculosis: experience with 12 patients, Clinical Radiology
(2017), https://doi.org/10.1016/j.crad.2017.10.016
6 L.S. Ch’ng et al. / Clinical Radiology xxx (2017) 1e6

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The authors thank Hospital Sibu, Sarawak, Malaysia, for 2013;6:845e50.
providing some of the images used in this review and the
Director General of Health Malaysia for his permission to
publish this article.

Please cite this article in press as: Ch’ng LS, et al., Imaging appearances of hepatic tuberculosis: experience with 12 patients, Clinical Radiology
(2017), https://doi.org/10.1016/j.crad.2017.10.016

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