Published online before print May 15, 2003, 10.1148/radiol.2281020323
(Radiology 2003;228:172-177.)
© RSNA, 2003
Alveolar Echinococcosis: MR Findings in the Liver1
Yoshihisa Kodama, MD,
Nobuyuki Fujita, MD, PhD,
Tadashi Shimizu, MD,
Hideho Endo, MD,
Toshikazu Nambu, MD,
Naoki Sato, MD, PhD,
Satoru Todo, MD, PhD and
Kazuo Miyasaka, MD, PhD
1 From the Department of Radiology (Y.K., T.S., H.E., T.N., K.M) and First Department of Surgery (N.S., S.T.), Hokkaido University School of Medicine, N15, W7, Kitaku, Sapporo, 060-8638, Japan; and Department of Radiology, Hakodate Chuo Hospital, Japan (N.F.). From the 2001 RSNA scientific assembly. Received March 20, 2002; revision requested June 6; revision received September 19; accepted November 18. Address correspondence to Y.K. (e-mail: ykodama@radi.med.hokudai.ac.jp).
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ABSTRACT
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PURPOSE: To clarify the magnetic resonance (MR) imaging findings of alveolar echinococcosis in the liver.
MATERIALS AND METHODS: Thirty-five patients with 50 lesions histologically proven to be alveolar echinococcosis were evaluated with MR imaging. Lesions were assessed with regard to the distribution pattern of solid and cystic components and pattern of contrast material enhancement.
RESULTS: Cystic components exhibited two patterns at T2-weighted MR imaging: small round cysts and large and/or irregular cysts. Forty-eight lesions (96%) contained small round cysts. Twenty-six lesions (52%) had large and/or irregular cysts. Forty-five lesions (90%) were associated with a solid component. MR imaging characteristics were categorized into five types: multiple small round cysts without a solid component (two lesions [4%], type 1), multiple small round cysts with a solid component (20 lesions [40%], type 2), a solid component surrounding large and/or irregular cysts with multiple small rounds cysts (23 lesions [46%], type 3), a solid component without cysts (two lesions [4%], type 4), and a large cyst without a solid component (three lesions [6%], type 5). In most cases (97%), contrast enhancement was weak.
CONCLUSION: The MR findings of alveolar echinococcosis in the liver are multiple small round cysts with a weakly enhanced solid component. The cystic component can be a large and/or irregular lesion, and such lesions are depicted clearly at T2-weighted MR imaging.
© RSNA, 2003
Index terms: Echinococcosis, 761.2083 • Liver, cysts, 761.312 • Liver, echinococcosis, 761.2083 • Liver neoplasms, MR, 761.121411 • Parasites, 761.2083
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INTRODUCTION
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Alveolar echinococcosis is a rare parasitic disease that is caused by the larva of Echinococcus multilocularis (1–4). This parasite introduces various patterns of hepatic lesions, and it is somewhat different from echinococcosis caused by Echinococcus granulosus, the hydatid species that is common worldwide. The imaging characteristics of E granulosus have been established (5–7) and include sharply defined cystic lesions with a thick wall. They sometimes have septa, daughter cysts, and/or calcifications, and a solid component is rarely seen. These conclusions were clarified with the use of ultrasonography, and the lesions have been classified into five types (5). By contrast, alveolar echinococcosis usually has a solid component. Consequently, the imaging characteristics are different for the two conditions. To date, magnetic resonance (MR) imaging findings of alveolar echinococcosis in the liver have been sparsely reported, and the imaging findings of this disease have not been established (4,8–13). The purpose of this study was to clarify the MR imaging findings of alveolar echinococcosis in the liver.
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MATERIALS AND METHODS
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Patients
The Hokkaido University School of Medicine does not require its approval or informed consent for review of patient records and images. This retrospective study included all patients with surgically proven alveolar echinococcosis who underwent preoperative MR imaging from 1990 to 2001. Thirty-five patients fulfilled the criteria and were thus selected, including 13 men and 22 women with an age range of 10–74 years (mean age, 49 years). Twenty-four patients had one lesion, seven had two lesions, three had three lesions, and one had more than three lesions. In the latter patient, the largest three lesions were evaluated. Consequently, 50 lesions were included in this study.
MR Imaging
From 1990 to 1997, all patients underwent MR examination with a 1.5-T unit (Magnetom; Siemens, Erlangen, Germany). Transverse T1-weighted spin-echo (repetition time msec/echo time msec, 650/15) and T2-weighted spin-echo (2,300/90) MR images were acquired with an 8-mm section thickness. From 1997 to 2001, patients underwent 1.5-T MR examination (Magnetom Vision; Siemens, Erlangen, Germany) with the following sequences: Transverse T1-weighted (120/4; flip angle, 30°) MR images were acquired by using a fast low-angle shot breath-hold sequence with 8-mm section thickness, and transverse T2-weighted (4.4/90) MR images were acquired by using a half-Fourier rapid acquisition with relaxation enhancement, or RARE, sequence with 8-mm section thickness.
In 39 lesions in 27 patients, T1-weighted MR images were obtained before and after intravenous administration of 1.0 mmol per kilogram of body weight of gadopentetate dimeglumine (Magnevist; Schering, Berlin, Germany).
Image Evaluation
Three experienced radiologists (Y.K, T.S, H.E; 8–15 years of experience) reviewed all images independently, and interpretation discrepancies were resolved by means of consensus.
The following items were assessed: diameter and location of the lesion, lesion structure (solid, cystic, or a mixture of both), distribution pattern of the solid and cystic portions of the lesion, signal intensity of the solid components on T1- and T2-weighted MR images, and pattern of lesion enhancement after administration of contrast material.
Hyperintensity on T2-weighted MR images that correlated with signal intensity of the cerebrospinal fluid was defined as a cystic component. Other types of signal intensity on T2-weighted images were defined as solid components. The signal intensities of the solid components were classified as hyperintense, isointense, or hypointense compared with the surrounding liver parenchyma on both T1- and T2-weighted images. The pattern of enhancement after contrast material injection was categorized as unenhanced, slightly enhanced (enhanced by up to 20% more than surrounding tissue, including peritumoral enhancement), or markedly enhanced.
Imaging characteristics were categorized into the following five types, according to the presence of solid and cystic components, the pattern of the cystic component, and the distribution pattern of these components (Fig 1): multiple small round cysts without a solid component (type 1), multiple small round cysts with a solid component (type 2), a solid component surrounding large and/or irregular cysts with multiple small round cysts (type 3), a solid component without cysts (type 4), and a large cyst without a solid component (type 5).
The presence of solid and cystic components, the pattern of the cystic component, and the distribution pattern of the solid and cystic components in the lesion were compared on the basis of the five types described.
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RESULTS
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The lesions ranged from 2 to 18 cm in diameter (mean, 6.1 cm). Thirty lesions were located in the right lobe of the liver, 15 in the left lobe, three in both lobes, and two in the caudate lobe. Cystic components exhibited two patterns: small round cysts and large and/or irregular cysts. Forty-eight lesions (96%) contained small round cysts, while 26 lesions (52%) had large and/or irregular cysts. A solid component was observed in 45 lesions (90%). Two lesions (4%) were classified as type 1 (Fig 2), 20 (40%) as type 2 (Fig 3), 23 (46%) as type 3 (Fig 4), two (4%) as type 4 (Fig 5), and three (6%) as type 5 (Fig 6). The small cysts tended to be located at the periphery of the lesion.
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Figure 2a. Transverse MR images show type 1 lesions. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows clustered small cysts in segments 5 (arrow) and 4 (arrowhead). (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows low signal intensity of the lesions (arrow and arrowhead). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement in small round cysts (arrow and arrowhead) and slightly enhanced adjacent liver parenchyma.
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Figure 2b. Transverse MR images show type 1 lesions. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows clustered small cysts in segments 5 (arrow) and 4 (arrowhead). (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows low signal intensity of the lesions (arrow and arrowhead). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement in small round cysts (arrow and arrowhead) and slightly enhanced adjacent liver parenchyma.
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Figure 2c. Transverse MR images show type 1 lesions. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows clustered small cysts in segments 5 (arrow) and 4 (arrowhead). (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows low signal intensity of the lesions (arrow and arrowhead). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement in small round cysts (arrow and arrowhead) and slightly enhanced adjacent liver parenchyma.
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Figure 3a. Transverse MR images show a type 2 lesion. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows an isointense solid component with peripheral small cysts (arrowheads). (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence depicts low signal intensity of the lesion (arrow). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement in the lesion (arrow).
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Figure 3b. Transverse MR images show a type 2 lesion. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows an isointense solid component with peripheral small cysts (arrowheads). (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence depicts low signal intensity of the lesion (arrow). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement in the lesion (arrow).
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Figure 3c. Transverse MR images show a type 2 lesion. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows an isointense solid component with peripheral small cysts (arrowheads). (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence depicts low signal intensity of the lesion (arrow). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement in the lesion (arrow).
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Figure 4a. Transverse MR images show type 3 lesions. (a) T2-weighted spin-echo (2,300/90) image shows an isointense solid component (arrow) with multiple small cysts (small arrowheads) and large irregular cysts (large arrowheads). (b) T1-weighted spin-echo (650/15; flip angle, 30°) image shows a large area with low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted spin-echo (650/15; flip angle, 30°) image shows heterogeneous enhancement (arrowheads) at the peripheral area of the mass.
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Figure 4b. Transverse MR images show type 3 lesions. (a) T2-weighted spin-echo (2,300/90) image shows an isointense solid component (arrow) with multiple small cysts (small arrowheads) and large irregular cysts (large arrowheads). (b) T1-weighted spin-echo (650/15; flip angle, 30°) image shows a large area with low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted spin-echo (650/15; flip angle, 30°) image shows heterogeneous enhancement (arrowheads) at the peripheral area of the mass.
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Figure 4c. Transverse MR images show type 3 lesions. (a) T2-weighted spin-echo (2,300/90) image shows an isointense solid component (arrow) with multiple small cysts (small arrowheads) and large irregular cysts (large arrowheads). (b) T1-weighted spin-echo (650/15; flip angle, 30°) image shows a large area with low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted spin-echo (650/15; flip angle, 30°) image shows heterogeneous enhancement (arrowheads) at the peripheral area of the mass.
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Figure 5a. Transverse MR images show a type 4 lesion. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows a lesion with low signal intensity (arrowheads) without a cystic component in segment 5. (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows the lesion as an area of low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement of the lesion (arrowheads).
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Figure 5b. Transverse MR images show a type 4 lesion. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows a lesion with low signal intensity (arrowheads) without a cystic component in segment 5. (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows the lesion as an area of low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement of the lesion (arrowheads).
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Figure 5c. Transverse MR images show a type 4 lesion. (a) T2-weighted (4.4/90) image obtained with half-Fourier rapid acquisition with relaxation enhancement shows a lesion with low signal intensity (arrowheads) without a cystic component in segment 5. (b) T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows the lesion as an area of low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted (120/4; flip angle, 30°) image obtained with a fast low-angle shot sequence shows no enhancement of the lesion (arrowheads).
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Figure 6a. Transverse MR images show a type 5 lesion. (a) T2-weighted spin-echo (2,300/90) image shows a prominent lesion (arrowheads) with high signal intensity, which matches that of cerebrospinal fluid. This is an example of a cystic component without a solid component. (b) T1-weighted spin-echo (650/15) image shows a lesion with low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted spin-echo (650/15) image shows no enhancement of the lesion (arrowheads).
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Figure 6b. Transverse MR images show a type 5 lesion. (a) T2-weighted spin-echo (2,300/90) image shows a prominent lesion (arrowheads) with high signal intensity, which matches that of cerebrospinal fluid. This is an example of a cystic component without a solid component. (b) T1-weighted spin-echo (650/15) image shows a lesion with low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted spin-echo (650/15) image shows no enhancement of the lesion (arrowheads).
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Figure 6c. Transverse MR images show a type 5 lesion. (a) T2-weighted spin-echo (2,300/90) image shows a prominent lesion (arrowheads) with high signal intensity, which matches that of cerebrospinal fluid. This is an example of a cystic component without a solid component. (b) T1-weighted spin-echo (650/15) image shows a lesion with low signal intensity (arrowheads). (c) Contrast-enhanced T1-weighted spin-echo (650/15) image shows no enhancement of the lesion (arrowheads).
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All 45 solid lesions we identified were hypointense compared with the liver parenchyma on T1-weighted MR images. T2-weighted images showed hypointensity in 16 lesions (36%), isointensity in 12 (27%), and hyperintensity in 17 (38%). After intravenous contrast material administration, slight enhancement was seen in 24 lesions (62%), and marked enhancement was seen in one (3%). Fourteen lesions (36%) were not enhanced. The Table shows the relationship between the size of the lesions and the type of imaging characteristics. The type 1 lesions were the smallest and type 3 lesions the largest, with type 2 lesions in the middle.
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DISCUSSION
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The genus Echinococcus includes several parasitic species, including E granulosus, E multilocularis, Echinococcus oligoarthrus, and Echinococcus vogeli (1). E granulosus is the most common of these, while E multilocularis appears less frequently than the others (6,7).
The parasitic cycle of Echinococcus has been well documented. Foxes are the main host of adult parasites (forest cycle). Less commonly, dogs and cats can also serve as hosts (rural cycle). Foxes or other hosts disseminate parasitic eggs within their feces, which contaminate vegetation and water. Intermediate hosts, mainly wild rodents, are contaminated by the intake of wild berries. Eventually, a larval infestation develops. Foxes in turn become contaminated by the intake of infested rodents. There are two modes of human contamination: (a) indirect, by intake of contaminated wild berries, plants, or water; and (b) direct, by contact with foxes. The main endemic regions include Japan, central Europe, the upper midwest region of the United States, Alaska, Canada, and parts of Russia (3).
E multilocularis produces multilocular alveolar cysts (1–10 mm in diameter) that resemble alveoli and grow by means of exogenous proliferation with cysts that progressively invade the host tissue and by means of peripheral extension of the processes originating in the germinal layer. The larva causes invasive and destructive changes in the human host that involve several organs, including the liver, spleen, lung, brain, muscloskeletal system, and soft tissue (4). The liver is the predominant site.
Liver involvement of alveolar echinococcosis commonly appears as an ill-defined infiltration of liver parenchyma (3). A hepatic lesion caused by alveolar echinococcosis consists of several components, roughly divided into cystic components and solid components. The cystic components comprise metacestodal vesicles and liquefaction necrosis. The solid components include coagulation necrosis, granuloma, and calcifications. MR imaging, especially T2-weighted imaging, is useful for the detection of cystic lesions (11). Small round cysts on MR images correspond to metacestodal vesicles, while large and irregular cystic lesions are consistent with liquefaction necrosis. Small cysts were depicted in 48 lesions (96%) in the present study. Solid components on MR images reflect coagulation necrosis, granuloma, and/or calcification. In our study, solid components were hypointense in all lesions on T1-weighted MR images. On T2-weighted images, lesions were hypointense, hyperintense, or isointense. Those findings are in accordance with a previous report, wherein Claudon et al (11) described the hypointense tissue on T2-weighted images as having low proton density in the chronic fibroinflammatory reaction, whereas the hyperintense tissue was in the prenecrotic stage.
Imaging characteristics were classified into five categories according to the presence of solid and cystic components, the distribution of the solid and cystic components within the lesions, and the pattern of the cystic lesions. In most lesions, a solid component with small round cysts was observed; the categorizations were types 2 and 3 in 43 lesions (86%). This pattern is thought to be characteristic of and highly specific to alveolar echinococcosis of the liver, and it is clearly demonstrated on T2-weighted MR images. Another characteristic finding is the presence of a solid component that may be slightly enhanced after intravenous contrast material administration. Marked enhancement of the lesion was rare, occurring in only one lesion (3%) in our study.
With regard to the size and characteristics of the lesions classified as types 1, 2, and 3, the average size was relatively increased from type 1 to type 3. Type 3 includes the pattern of type 2, and type 2 includes the pattern of type 1. We suggested that type 1 may be the earliest stage of alveolar echinococcosis in the liver, type 2 may indicate a lesion in the second stage, and type 3 probably indicates a lesion in the advanced stage. Type 4 is similar to type 2 because the lesion is mainly solid. On the other hand, type 5 resembles type 3 because both types include lesions with a large cyst.
Differential diagnoses of alveolar echinococcosis include the possibility of several hepatic tumors. Type 2 and 3 lesions in the present study may mimic cystadenoma, cystadenocarcinoma, and peripheral cholangiocarcinoma or metastasis with peripheral bile duct dilatation. These tumors can be differentiated from alveolar echinococcosis, however, because they are usually enhanced and rarely calcified. It is difficult to identify calcifications with MR imaging. Because of the high detectability of calcifications with computed tomography (CT), MR imaging and CT are complementary imaging techniques that allow precise depiction of alveolar echinococcal lesions. The pattern of type 1 lesions is seen in a patient with cystadenoma or localized Caroli disease, while a type 5 lesion is similar to a simple cyst. With type 4 lesions, a possible diagnosis might be granuloma, inflammatory pseudotumor, early hepatocellular carcinoma, or other rare solid hepatic tumors. Although types 1, 4, and 5 represent features seen only rarely in alveolar echinococcosis, they are difficult to differentiate from the other diseases solely on the basis of imaging findings. In the case of types 1, 4, and 5, serologic examination is helpful for the diagnosis of alveolar echinococcosis.
In conclusion, alveolar echinococcosis in the liver characteristically appears as a solid and cystic lesion at MR imaging. The solid component is minimally enhanced after intravenous administration of contrast material. A cluster of small cysts is often associated with a large and irregular cyst.
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FOOTNOTES
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Author contributions: Guarantor of integrity of entire study, Y.K.; study concepts and design, Y.K.; literature research, Y.K.; clinical studies, Y.K.; data acquisition, Y.K.; data analysis/interpretation, Y.K., T.S., H,E.; manuscript preparation, definition of intellectual content, and editing, Y.K.; manuscript revision/review and final version approval, all authors.
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ABSTRACT
INTRODUCTION
