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World J Surg Proced. Mar 28, 2014; 4(1): 13-20
Published online Mar 28, 2014. doi: 10.5412/wjsp.v4.i1.13
Diagnostic imaging and interventional procedures in a growing problem: Hepatic alveolar echinococcosis
Mecit Kantarci, Berhan Pirimoglu, Yesim Kizrak
Mecit Kantarci, Berhan Pirimoglu, Yesim Kizrak, Department of Radiology, School of Medicine, Ataturk University, 25090 Erzurum, Turkey
Author contributions: Kantarci M and Pirimoglu B designed the research; Kantarci M, Pirimoglu B and Kizrak Y performed the research; Kantarci M and Kızrak Y analyzed the data; Kantarci M and Pirimoglu B wrote the paper.
Correspondence to: Mecit Kantarci, MD, PhD, Department of Radiology, School of Medicine, Ataturk University, 200 Evler Mah. 14. Sok No 5 Dadaskent, 25090 Erzurum, Turkey. akkanrad@hotmail.com
Telephone: +90-442-2361212 Fax: +90-442-2361301
Received: October 28, 2013
Revised: December 19, 2013
Accepted: February 16, 2014
Published online: March 28, 2014

Abstract

Alveolar echinococcosis (AE) of the liver is caused by the metacestode of the fox tapeworm Echinococcus multilocularis (E. multilocularis), which is endemic in many parts of the world. AE is a very aggressive and potentially fatal infestation which always affects the liver primarily and metastasizes to any part of the body. Without timely diagnosis and therapy, the prognosis is dismal, with death the eventual outcome in most cases. Diagnosis is usually based on findings at radiological imaging and in serological analyses. The alveolar cysts grow by exogenous proliferation and behave like a malignant neoplasm. Since AE lesions can occur almost anywhere in the body, familiarity with the spectrum of cross-sectional imaging appearances is advantageous. Therefore, AE lesions can cause physicians to generate a long list of differential diagnoses, including malignant tumors. Disseminated parasitic lesions in unusual locations with atypical imaging appearances may make it difficult to narrow the differential diagnosis. For diagnosis, ultrasonography (US) remains the first line examination. For a more accurate disease evaluation, aiming to guide the surgical strategy, computed tomography (CT), magnetic resonance imaging (MRI), including magnetic resonance cholangiography (MRC) imaging, are of importance, providing useful complementary information. However, making the correct diagnosis is possible if imaging findings are correlated with appropriate clinical findings. We present an overview of the radiological patterns produced by E. multilocularis lesions as seen on US, CT and MRI and discuss the interventional procedures in hepatic AE lesions.

Key Words: Alveolar echinococcosis, Liver, Diagnosis, Intervention, Imaging, Review

Core tip: Diagnosis and treatment of alveolar echinococcosis remains a challenge for clinicians. Most patients suffering from a chronic carrier status need continuous medical treatment and follow-up examinations. Diagnosis of alveolar echinococcosis is supported by results from imaging studies, histopathology and/or serological analyses. The present review summarizes current understanding of imaging features and knowledge of interventional procedures.



INTRODUCTION

Alveolar echinococcosis (AE) is a rare parasitic disease due to the intra-hepatic development of the larva of the small metacestode Echinococcus multilocularis (E. multilocularis). Metacestode cells of E. multilocularis proliferate in the liver, inducing slowly progressive, life-threatening tumor like growths[1,2]. The prognosis is generally poor and liver transplantation may be required in patients with inoperable lesions, chronic liver failure[2,3]. Most patients suffering from a chronic carrier status need continuous medical treatment and follow-up examinations[1,4]. In addition to anti-infective therapy with benzimidazoles, early diagnosis by imaging techniques, radical surgery, transplantation, radiological interventional procedures and long term medical care of the patients have contributed to the success of treatment and increase in patient survival time[5].

This article provides an epidemiological, pathophysiological, diagnostic profile of the disease as background for a detailed review of the clinical, interventional approach, and radiological features of hepatic AE. The current roles of specific imaging modalities are described to aid radiologists in the timely detection and characterization of AE infestations.

EPIDEMIOLOGICAL AND PATHOPHYSIOLOGICAL CHARACTERISTICS

Most human cases of E. multilocularis infection have been reported in endemic areas of western and central Europe, including Turkey, the former Soviet Union, Iran, Iraq, western and central China, and northern Japan[6]. Definitive hosts are foxes and, less commonly, cats and dogs. Intermediate hosts are wild rodents. Humans are infested either by direct contact with definitive hosts or indirectly by intake of contaminated water or contaminated plants, such as wild berries[6,7]. Humans are accidental intermediate hosts, becoming infected after ingesting contaminated foods, including fruits and vegetables[8]. The walls of the parasite eggs are destroyed in the host digestive system, after which the embryos penetrate the intestinal wall and reach the liver, by way of the portal or lymphatic system, where the larvae develop. In the liver, E. multilocularis larvae grow as tumor-like buds that evolve into multiple vesicles containing a germinal layer surrounded by a laminar membrane[4]. The liver parenchyma near the mass is typically atrophic with capsular retraction due to biliary or vascular invasion. Necrosis is observed in the center of the lesions; moreover, these lesions may become superinfected with bacteria and fungi, possibly leading to complications such as liver abscesses and septicemia. The larva causes invasive and destructive changes in the human host that often lead to complications[7-9].

Hepatic AE is a chronic disease with a latent stage that may last for years before signs and symptoms develop. If left untreated, the disease is usually fatal. Death eventually results from hepatobiliary complications, such as biliary obstruction with bacterial or fungal superinfection or secondary biliary cirrhosis, bleeding from esophageal or duodenal varices due to portal hypertension, Budd-Chiari disease or obstruction of the vena cava[9,10].

CLINICAL FEATURES

The liver is the most common site of E. multilocularis infection, with more than 90% of patients having infected livers. The lesions may be single or multiple[4]. Alveolar echinococcosis of the liver behaves like a slow growing liver cancer. Symptoms of hepatic alveolar echinococcosis are principally cholestatic jaundice and epigastric pain[3,7]. Involvement of the bile ducts and blood vessels leads to severe complications, such as cholangitis, portal hypertension, liver abscesses, septic shock and Budd-Chiari syndrome[11].

DIAGNOSIS

Clinical diagnosis of hepatic AE is based on the patient’s medical history, clinical features, morphological characteristics of lesions, determined at radiological imaging, and results of serological and histopathological analyses[7,8,12]. A diagnosis of alveolar echinococcosis is based on the presence of at least two of the following findings[4,12]: (1) a lesion or lesions with the typical appearance, detected in the usual sites at cross-sectional imaging; (2) echinococcus species-specific serum antibodies detected in blood tests with high diagnostic sensitivity and confirmed in immunoassays with high specificity; and (3) histopathological features suggestive of E. multilocularis and nucleic acid of E. multilocularis detected in a clinical specimen.

The World Health Organization Informal Working Group on Echinococcosis classification system, based on imaging findings, has been established as the international benchmark for standardized evaluation of diagnostic and therapeutic measures[13]. This PNM-system denotes the extension of the primary mass in the liver (P), the involvement of neighboring organs including lymph nodes (N), and metastases (M)[14] (Table 1).

Table 1 PNM classification of alveolar echinococcosis.
PPrimary lesion localized to the liver
PXPrimary lesion cannot be assessed
P0No detectable hepatic lesion
P1Peripheral hepatic lesion with no proximal hepatic vascular or biliary involvement
P2Central hepatic lesion with proximal involvement of vessels or biliary ducts in one lobe1
P3Central hepatic lesion with involvement of hilar vessels or biliary ducts in both lobes or with involvement of two hepatic veins
P4Hepatic lesion with extension along the vessels2 and biliary tree
NExtrahepatic involvement of neighboring organs or tissues [diaphragm, lung, pleura, pericardium, heart, gastric or duodenal wall, adrenal gland, peritoneum, retroperitoneum, parietal wall (muscles, skin, bone), pancreas, regional lymph nodes, hepatic ligaments, kidney]
NXCannot be evaluated
N0No regional involvement
N1Regional involvement of contiguous organs or tissues
MAbsence or presence of distant metastasis (in lung, distant lymph nodes, spleen, central nervous system, orbits, bone, skin, muscle, kidney, distant peritoneum, and retroperitoneum)
MXNot completely evaluated
M0No metastasis3
M1Metastasis
IMAGING METHODS FOR DETECTING THE HEPATIC AE LESIONS

Abdominal ultrasonography (US) is the first line imaging examination for evaluation of patients in whom the presence of alveolar echinococcosis is suspected. Computed tomography (CT) and magnetic resonance (MR) imaging performed with cholangiopancreatography and diffusion-weighted techniques, as well as standard sequences, typically are required for preoperative evaluation[4,8,10]. Recently, we have performed CT perfusion imaging for demonstration of the perfusion characteristics of the hepatic AE lesions and to make a differential diagnosis between AE and other malignant liver lesions.

US

US is the initial investigative modality of choice for detection of hepatic AE lesions[4,12]. Typical findings at abdominal US (in approximately 70% of cases) include a large hepatic mass with juxtaposed areas of internal hyper- and hypo-echoic, irregular margins and scattered foci of calcification, and a pseudocyst with a large area of central necrosis surrounded by an irregular ring like region of hyperechoic representing fibrous tissue[15] (Figure 1A). Less typical appearances (in approximately 30% of cases) include multiple clustered hemangioma-like hyperechoic nodules (Figure 1B). These lesions usually show a “hailstorm pattern”. This pattern represents the histopathologically heterogeneous stroma containing microscopic metacestode vesicles, areas of non liquefactive necrosis, entrapped host tissue and microcalcifications, which account for the stroma’s relatively increased echogenicity[16]. Irregular borders and a lack of enhancement are suggestive of AE; the other liver lesions usually enhance and are rarely calcified. A pseudocyst appearance might also be seen in recurrent foci of AE after percutaneous drainage of primary lesions[11,16]. Doppler US images can show distortion and displacement of the hepatic veins, portal vein and biliary tree resulting from mass effect, invasion of the inferior vena cava, hepatic or portal vein walls, and intrahepatic bile duct dilatation[8].

Figure 1
Figure 1 Alveolar echinococcosis in a 41-year-old woman. Abdominal gray-scale ultrasonography (US) image shows a heterogeneous mass lesion in the right lobe of the liver. The mass is generally hypoechoic but contains hyperechoic foci of calcifications (A). Alveolar echinococcosis in a 38 year old woman. Abdominal gray-scale US image shows a heterogeneous, hyperechoic lesion without calcifications (B).
CT

CT reveals anatomical and morphological features of lesions and best detects the characteristic pattern of calcification. It also allows to help determine the number, size and location of lesions in the liver and allows a comprehensive preoperative evaluation of vascular, biliary and extrahepatic extension, which is an important consideration when assessing lesion resectability[4,16,17]. Non-contrast enhanced CT images show an infiltrating tumor like hepatic mass with irregular margins and heterogeneous contents with varied attenuation, including scattered hyperattenuating calcifications and hypoattenuation areas corresponding to necrosis and parasitic tissue (Figure 2A); these findings are characteristic findings of alveolar echinococcosis (18). Calcifications are found approximately in 90% of all infected patients. Apart from the typical peripheral irregular calcifications, large homogeneous, multiple punctiform or scattered calcifications might be seen[4,8,9,16].

Figure 2
Figure 2 Alveolar echinococcosis in a 34-year-old man. Axial unenhanced computed tomography (CT) image demonstrates an infiltrating tumor-like hepatic mass with irregular margins and heterogeneous contents, including scattered hyperattenuating foci of calcification and areas of hypoattenuation corresponding to necrosis and parasite tissue (A). Alveolar echinococcosis in a 29 year old man. Abdominal CT images obtained after the administration of intravenous contrast medium show a poor enhancement, hypoattenuating lesion in the portal venous phase (B).

Large areas of central necrosis can be difficult to differentiate from abscesses. However, there is poor or no enhancement after bolus administration of intravenous contrast agent, emphasizing poor vascularization of the parasitic lesion (Figure 2B). Usually, no lymphadenopathy occurs[18,19]. Secondary pyogenic infection may occur at any time during the course of disease, resulting in abscess formation. Hilar infiltration occurs in approximately 50% of all patients, resulting in dilatation of the intrahepatic bile ducts and invasion of the portal vein, the portal branches and the hepatic veins. These conditions lead to hypoperfusion and subsequent atrophy of the affected liver segments[4,8,19]. CT findings of the hepatic AE lesions may be indistinguishable from primary hepatic neoplasms, such as cholangiocarcinoma, biliary cystadenoma and biliary cystadenocarcinoma, as well as hepatic metastases[4,9,20]. However, hypoattenuation, calcification and absence of contrast enhancement in a hepatic lesion can help identify it as hepatic AE.

CT perfusion, a non-invasive method that has been increasingly used in recent years, allows for functional assessment of the perfusion of normal and pathological tissues by means of parameters such as the blood flow (BF), blood volume (BV), mean transit time (MTT), arterial liver perfusion (ALP), portal liver perfusion (PLP) and hepatic perfusion index (HPI). This technique allows for quantitative determination of lesion characteristics, enabling differentiation between malignant lesions and benign ones. Many studies have reported the use of this method to assess hepatocellular carcinoma, cirrhotic nodules and normal liver parenchyma[21]. Our experience suggests that CT perfusion is a feasible method to quantitatively assess angiogenesis of AE lesions of liver. We determined lower BF, BV, ALP and PVP values in AE lesions compared with normal liver parenchyma by using CT perfusion imaging (Figure 3). The above results demonstrated that CT perfusion can be used in hepatic AE lesions of liver that are confusable, especially with malignant lesions such as hepatocellular and cholangiocellular carcinoma.

Figure 3
Figure 3 Transverse computed tomography perfusion functional maps of the blood volume, blood flow, portal-venous perfusion, arterial liver perfusion and hepatic perfusion index in a 49-year-old woman show a large alveolar echinococcosis lesion in the right lobe of the liver that has a distinct range of colors compared with the background liver parenchyma. Perfusion values from an ROI drawn in the solid component without calcification of alveolar echinococcosis (ROI 1) and normal tissue (ROI 2) show lower blood flow, blood volume, arterial liver perfusion and portal-venous perfusion values compared with normal liver parenchyma.
MRI

MRI is a good modality for detection of the components of parasitic lesions and depicting vascular or biliary tree involvement and extrahepatic extension. Therefore, it should be added to preoperative evaluations, particularly evaluations of patients who are to undergo extensive hepatic resection or liver transplantation[8]. MRC has been used to detect the relationship between hepatic AE lesions and the biliary tree before surgical treatment or liver transplantation[4]. However, non-contrast enhanced CT imaging is superior to MRI in detecting calcifications. The MRI characteristics are a heterogeneous infiltrative mass with irregular margins and a necrotic center that exhibits low to intermediate signal intensity on T1-weighted images and heterogeneous signal intensity (areas of low and high signal intensity) on T2-weighted images. Areas of high T2 signal intensity correspond to small cystic or necrotic components, whereas areas of low T2 signal intensity correspond to fibrotic or collagenous components (Figure 4). T2-weighted images are useful for detecting small hepatic cysts and extrahepatic cysts[22,23].

Figure 4
Figure 4 Alveolar echinococcosis in a 39-year-old man. Axial unenhanced T1-weighted image show an infiltrating hypointense mass in the right lobe of the liver (A). Axial magnetic resonance imaging obtained after the administration of intravenous contrast medium show no contrast enhancement within the mass (B). Axial T2-weighted image show an infiltrating hypointense mass in the right lobe of the liver (C).

Hepatic AE lesions are categorized on the basis of their imaging manifestations into five types. Type 1 (4%) lesions consist of multiple small cysts without a solid tissue component; type 2 (40%) lesions include a solid tissue component associated with multiple small cysts; type 3 (46%) lesions consist of a solid tissue component associated with irregular large cysts; type 4 (4%) lesions consist of solid tissue without cystic components; and type 5 (6%) lesions consist of a single large cyst without solid tissue components[22]. For lesions with characteristics not often seen in AE (especially types 1, 4 and 5), serological analyses can be helpful[8]. In particular, MRC can detect biliary dilatation, a reduced number of bile ducts within the lesion, invasion of the biliary wall, distortion and compression of the biliary tree, and communication of intrahepatic bile ducts with necrotic cystic regions[8,23].

Signal intensity at diffusion-weighted imaging can be quantified by calculating the apparent diffusion coefficient (ADC), a valuable indicator for the diagnosis and characterization of focal hepatic lesions[24]. Our experience suggests that AE lesions can be reliably identified on diffusion-weighted images obtained with b values of 50400800 and 1000 sec/mm2 and qualitatively assessed on ADC maps. These lesions usually result in a subjectively higher ADC in the lesion than in liver parenchyma on diffusion-weighted images obtained with a b value of 800 sec/mm2 (Figure 5). Restricted diffusion due to a superinfection (especially an abscess) may be observed in the necrotic central part of particularly large AE lesions. The general lack of diffusion restriction in hepatic AE lesions is an important finding that helps differentiate them from malignancies that have similar clinical features and imaging findings, including invasion and metastases. Table 2 summarizes characteristic imaging features that are helpful for diagnosing hepatic AE lesions.

Table 2 Morphological characteristics of hepatic alveolar echinococcosis lesions.
ModalityHepatic AE lesions
USMass with irregular margins, scattered foci of calcification, central necrosis, and vascular and biliary involvement
CT
UnenhancedMass with irregular margins, hyperattenuating foci of calcification, and hypoattenuating regions of necrosis and parasitic tissue
Contrast- enhancedMass with no substantial enhancement and peripheral fibroinflammatory components with slight but long-lasting enhancement
CT perfusionLower BF, BV, ALP and PVP values in AE lesions compared with normal liver parenchyma
MRI
T1-weightedHeterogeneous mass with irregular margins and a necrotic center that exhibits low to intermediate signal intensity
T2-weightedHeterogeneous mass with irregular margins, a necrotic center that exhibits high signal intensity, and low-signal-intensity fibrotic and collagenous components
Contrast-enhancedMass with no substantial enhancement and peripheral fibroinflammatory components with slight but long-lasting enhancement
Diffusion-weightedMass with hypointense signal and high ADC on images obtained with high b values
Figure 5
Figure 5 Alveolar echinococcosis in a 44-year-old man. Diffusion-weighted magnetic resonance images obtained with b values of 400 sec/mm2 (A), 800 sec/mm2 (B), and 1000 sec/mm2 (C) and corresponding apparent diffusion coefficient map (D) show signal hyperintensity in a hepatic mass.
INTERVENTIONAL PROCEDURES

In hepatic AE, radical surgical excision is followed by short-term antihelmintic therapy for resectable lesions and long-term aggressive antihelmintic therapy for partially resectable or unresectable lesions. Patients with hepatic AE have a poor prognosis and high fatality rate; curative treatment of AE is possible only with early detection and complete surgical excision or liver transplantation[7,11]. Liver transplantation should only be considered in patients with very severe hilar extension, leading to uncontrolled biliary infections, symptomatic secondary biliary cirrhosis with ascites and/or severe variceal bleeding owing to portal hypertension[25].

Cases of late diagnosis require lifelong pharmacological treatment with benzimidazoles and thorough follow-up because benzimidazoles are assumed to exert only a parasitostatic effect on hepatic AE lesions. Albendazole is a broad spectrum anthelmintic agent. Perioperative treatment with albendazole can decrease the recurrence rate and increase the success rate of the operation[17,26]. Management of the septic complications of alveolar echinococcosis of the liver, such as cholangitis or liver abscesses, should prioritize interventional radiology[4,25]. The liver abscess is usually treated by percutaneous catheterization, which may lead to complete disappearance of the hepatic alveolar echinococcus lesion[11] (Figure 6). Additionally, treatment of portal hypertension in alveolar echinococcosis of the liver is also problematic. In patients without cirrhosis, percutaneous stent placement in the hepatic veins is a promising treatment alternative[27].

Figure 6
Figure 6 Non-contrast enhanced axial (A) and sagittal (B) computed tomography images show the percutaneous drainage of an infected parasitic cyst in a 43 year old woman with hepatic alveolar echinococcosis.
CONCLUSION

Hepatic AE lesions mimic slow-growing tumors of the liver parenchyma that tend to infiltrate adjacent structures, especially the portal hilum, hepatic veins, inferior vena cava and biliary system. For effective service to referring clinicians and their patients, radiologists should be familiar with the cross-sectional imaging findings of hepatic AE. Therefore, radiologists should depict in detail the relationships between the mass and the portal bifurcation, especially any evidence of invasion or extension into the main portal vein, hepatic veins, inferior vena cava and bile ducts. Additionally, if liver transplantation is contemplated, the remaining functional hepatic parenchymal mass and reserve should be calculated and septic complications should be treated by percutaneous drainage until performing the radical surgical excision or liver transplantation.

Footnotes

P- Reviewers: Frider B, Gow KW, Keese M S-Editor: Song XX L- Editor: Roemmele A E- Editor: Wu HL

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