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Differentiating Cirrhosis and Chronic Hepatosplenic Schistosomiasis Using MRI

¹ Department of Diagnostic Imaging, Federal University of São Paulo, Rua Napoleão de Barros 800, São Paulo, SP 04024-002, Brazil.
² The SARAH Network of Hospitals for Reabilitation, Brasília, Brazil.
³ Department of Medicine, Federal University of São Paulo, São Paulo, Brazil.
⁴ Department of Surgery, Federal University of São Paulo, São Paulo, Brazil.
⁵ Department of Radiology, Beth Israel Deaconess Medical Center, Boston, MA.

Received May 27, 2007; accepted after revision September 19, 2007.

 
Address corresopndence to A. S. A. Bezerra (alexbezerra{at}gmail.com).

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Abstract

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OBJECTIVE. The objective of our study was to identify which imaging features may be used to differentiate between cirrhosis and chronic hepatosplenic schistosomiasis and to assess image interpretation agreement for MRI findings.

MATERIALS AND METHODS. Retrospective review of 27 patients with alcoholic or virus-induced cirrhosis and 24 patients with chronic hepatosplenic schistosomiasis who underwent MRI (1.5 T) of the abdomen was performed. Images were interpreted independently by two radiologists evaluating the following MRI features: hepatic fissure widening, irregularity of hepatic contours, periportal fibrosis, hepatic parenchyma heterogeneity, and splenic siderotic nodules. Left, right, and caudate hepatic lobe measurements were obtained, and the splenic index was measured. The Fisher's exact test, chi-square test, and Student's t test were used to compare both groups, and regression analysis was performed. Observer agreement was measured using kappa and intraclass correlation tests.

RESULTS. Periportal fibrosis, heterogeneity of hepatic parenchyma, and splenic siderotic nodules were more frequent in the group with schistosomiasis (p < 0.05), with periportal fibrosis showing the largest difference in presence and distribution (peripheral greater than central). The transverse diameter of the right hepatic lobe, caudate lobe–right lobe ratio, and splenic index were larger in patients with chronic schistosomiasis (p < 0.001). At multiple regression analysis, splenic siderotic nodules, splenic index, and caudate lobe–right lobe ratio were predictive of schistosomiasis. Observer agreement was substantial or almost perfect for almost all variables analyzed ( or r = 0.81–1.00).

CONCLUSION. The presence of peripheral periportal fibrosis, heterogeneity of hepatic parenchyma, and splenic siderotic nodules, and the splenic index and caudate lobe–right lobe ratio are useful features for differentiating alcoholic or virus-induced cirrhosis from chronic schistosomiasis using MRI.

Keywords: cirrhosis • hepatosplenic schistosomiasis • liver disease • MRI • schistosomiasis

Introduction

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Chronic liver diseases, encompassing a wide range of pathologic entities, are a common cause of morbidity and mortality [1]. Of these, hepatic cirrhosis is one of the most common forms of chronic liver disease, related most commonly to alcohol-induced hepatic injury or underlying hepatitis B and C infection, and is among the 10 leading causes of death [1, 2]. In addition, chronic hepatosplenic schistosomiasis represents a second, commonly forgotten source of chronic liver disease that is especially prevalent in developing countries. More than 200 million people are at risk of developing the disease, with an increasing number of cases occurring in developed countries as well because of migration and globalization [3, 4].

Sonography is one of the main techniques used in the imaging evaluation of patients with chronic liver diseases, primarily because of equipment availability and cost-effectiveness [5]. However, in several studies, investigators have reported that results using this technique in hepatology are operator-dependent, with poor to moderate interobserver and intraobserver variability [6]. Recently, a few studies using MRI, an imaging technique being increasingly used to evaluate hepatic disease, have been reported in the assessment of patients with chronic hepatosplenic schistosomiasis [7, 8]. Previous studies have shown that certain morphologic changes, such as periportal fibrosis, hepatic fissure widening, heterogeneity of the hepatic parenchyma, and splenomegaly, may be suggestive of chronic schistosomiasis [7]. However, many of the findings in chronic hepatosplenic schistosomiasis can also be seen in cirrhosis, making differentiating these diseases difficult and important because patients with cirrhosis need to undergo biopsy in many cases, whereas schistosomiasis patients do not. Therefore, the purpose of this study was to compare MRI findings in patients with chronic hepatosplenic schistosomiasis with those in patients with cirrhosis to identify which imaging characteristics can be used to differentiate these two entities.

Materials and Methods

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Overall Experimental Design
MRI examinations performed in 27 patients with virus- or alcohol-induced cirrhosis and 24 patients with chronic hepatosplenic schistosomiasis were retrospectively reviewed. Initially, 27 patients with chronic hepatosplenic schistosomiasis were identified, but three were excluded because not all examinations could be retrieved on our institution's data storage system. In phase I of the study, inter- and intraobserver agreement in image interpretation was assessed for several commonly seen hepatic morphologic characteristics and several quantitative measurements of the liver and spleen. In phase II of the study, a comparison of the qualitative morphologic findings and quantitative measurements was performed between the cirrhosis patients and chronic schistosomiasis patients to identify differences in the presence of specific characteristics. Approval of our institutional review board was obtained before the initiation of this study.

Patients
Abdominal MR studies were performed in 51 patients with virus-induced or alcoholic cirrhosis (n = 27) or with chronic hepatosplenic schistosomiasis (n = 24). The cirrhotic group consisted of 18 men and nine women ranging in age from 33 to 73 years (mean ± SD, 54.6 ± 10.0 years). Cirrhosis was due to viral infection in 11 patients and alcohol abuse in 15 patients. One patient had both causes for cirrhosis. Viral infection was diagnosed by viral antigen test and antibody titration. The diagnosis of cirrhosis was established by percutaneous liver biopsy in 13 patients or by clinical evaluation including liver function tests in 14 patients as routinely used [9, 10]. Patients were not included in this group if they had hepatocellular carcinoma, which was diagnosed by the presence of hypervascular nodules and elevated -fetoprotein level, because the typical aspect of gross morphologic changes and the presence of ascites (which is rare in schistosomiasis) would lead to a specific diagnosis of cirrhosis by MRI.

View larger version (138K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1A —29-year-old man with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres, and splenic siderotic nodules (arrow). Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image (1,800/160) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (141K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1B —29-year-old man with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres, and splenic siderotic nodules (arrow). Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image (1,800/160) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (136K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 1C —29-year-old man with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres, and splenic siderotic nodules (arrow). Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image (1,800/160) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

MRI Technique
MR studies were performed on 1.5-T units (Gyroscan ACS/NT, Philips Medical Systems; or Excite HD, GE Healthcare) with the use of a whole-body coil or a synergy torso coil. All patients underwent axial T1-weighted and T2-weighted MRI. T1-weighted imaging included in-phase gradient-echo (TR range/TE range, 15–190/4.5–4.8; flip angle, 60–90°) and opposed-phase gradient-echo (15–190/2.1–2.4; flip angle, 60–90°) sequences. T2-weighted imaging included the sequences with (1,800–6,666/82.4–90; flip angle, 90°) and without (1,800–10,000/158–160; flip angle, 90°) fat suppression. Dynamic in-phase gradient-echo images (7–215/4.5–4.8; flip angle, 12–30°) were obtained before and after IV bolus injection of 0.1 mmol/kg of body weight of gadopentetate dimeglumine (Magnevist, Bayer HealthCare), at a rate of 3 mL/s and followed by a 20-mL saline flush. Images were acquired 30 seconds (arterial phase), 60 seconds (portal phase), and 5 minutes (delayed phase) after injection of contrast material. The imaging matrix was 256 x 256 with a field of view of 380–420 mm. The section thickness was 8 mm with an intersection gap of 0.8 mm or smaller.

Imaging Interpretation
Qualitative and quantitative interpretations of radiologic features of the liver and spleen at MRI were made independently by two abdominal radiologists with between 4 and 6 years of experience in abdominal radiology during two different reading sessions with an interval of at least 30 days between each evaluation. The readers had not previously seen the studies in clinical practice or preparation of the study. The observers were not aware of the clinical history of the patients at the time of interpretation, did not know that all patients who had undergone splenectomy had schistosomiasis, and agreed on common rules to perform the MRI evaluation before the start of the study.

Qualitative evaluation—Images were interpreted looking for the presence or absence of five subjective hepatic changes. The first change was fissure widening, which was characterized by the presence of fatty tissue in the enlarged space between liver surfaces that would normally be close to each other (Fig. 1A, 1B, 1C). The second change was periportal fibrosis, which was characterized by visual assessment of bands following portal vessels that were hypointense on T1-weighted images, that were hyperintense on T2-weighted images, and that showed enhancement after the injection of paramagnetic contrast material observed in the delayed venous phase [7] (Figs. 2A, 2B, 2C and 3A, 3B, 3C). Periportal fibrosis was considered to be central when these bands were present only along the main branches of the portal vein. Periportal fibrosis was considered to be peripheral when these bands were found away from the hilum of the liver, near the liver capsule or more outer portions of the organ. The third change was heterogeneity of hepatic parenchyma. The fourth change was irregularity of hepatic contours. The fifth change was the presence of siderotic nodules, which were characterized as round foci with absence of signal in all sequences and no enhancement after injection of contrast material [12, 13] (Fig. 1A, 1B, 1C).

View larger version (127K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2A —57-year-old woman with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres (arrow), and splenic siderotic nodules. Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image with fat suppression (1,800/90) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (116K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2B —57-year-old woman with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres (arrow), and splenic siderotic nodules. Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image with fat suppression (1,800/90) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (120K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 2C —57-year-old woman with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres (arrow), and splenic siderotic nodules. Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image with fat suppression (1,800/90) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3A —35-year-old man with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres, and splenic siderotic nodules (arrow). Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image (1,800/160) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (135K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3B —35-year-old man with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres, and splenic siderotic nodules (arrow). Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image (1,800/160) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

View larger version (126K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 3C —35-year-old man with schistosomiasis presenting with irregularity of hepatic contours, widening of ligamentum teres, and splenic siderotic nodules (arrow). Note absence of signal in nodules on T1-weighted turbo field-echo (TFE) in-phase image (TR/TE, 15/4.8) (A), T2-weighted turbo spin-echo image (1,800/160) (B), and contrast-enhanced T1-weighted TFE image (15/4.6) (C).

Quantitative evaluation—The following measurements were made using electronic calipers: first, transverse diameter of the caudate lobe [14]; second, transverse diameter of the right hepatic lobe [14]; third, caudate lobe–right lobe ratio, which was obtained from dividing the measurement of the caudate lobe by that of the right lobe (upper limit of normal = 0.65) [14]; fourth, anteroposterior diameter of the left lobe (upper limit of normal = 7 cm) [15]; and, fifth, splenic index, a measurement obtained from multiplying the longitudinal, transverse, and anteroposterior diameters of the spleen (upper limit of normal = 480 cm³) [16].

Statistical Analysis
The chi-square test or Fisher's exact test was used to evaluate the statistical difference of the qualitative variables between the group with cirrhosis and the group with chronic hepatosplenic schistosomiasis. The statistical difference of quantitative variables for both groups was analyzed using the Student's t test. A p value of < 0.05 was considered to indicate a statistically significant difference with both methods.

A logistic regression was performed to obtain an equation that could be used to differentiate between the two groups. Two models were obtained: One included all variables and the other did not include variables related to the spleen because some patients with schistosomiasis had previously undergone splenectomy. Statistical analysis was performed using statistics software (SPSS version 12.0, SPSS) for Windows (Microsoft).

Analysis of intraobserver and interobserver agreement of qualitative variables was assessed by the kappa agreement test [17]. For statistical purposes, the calculation of interobserver agreement used the first observations made by each examiner. The analysis of the intraobserver and interobserver agreement for quantitative variables (i.e., measurements) was assessed by the intraclass correlation coefficient. Kappa values and intraclass correlation coefficients were interpreted as poor ( or r = 0), slight (0.0–0.20), fair (0.21–0.40), moderate (0.41–0.60), substantial (0.61–0.80), or almost perfect (0.81–1.00) [17].

Results

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Phase I: Evaluating Intraobserver and Interobserver Agreement in Image Interpretation for All Patients
In the evaluation of qualitative morphologic findings, intraobserver agreement in image interpretation was almost perfect for nearly all findings except hepatic fissure widening for observer 2 ( = 0.59, moderate agreement) and heterogeneity of hepatic parenchyma for both observers ( = 0.77 and 0.76 for observers 1 and 2, respectively, substantial agreement) (Table 1). Similarly, interobserver agreement in image interpretation was almost perfect for nearly all qualitative findings except heterogeneity of hepatic parenchyma ( = 0.73, substantial agreement) and irregularity of hepatic contours ( = 0.65, substantial agreement) (Table 1).

In evaluation of quantitative measurements, intraobserver and interobserver agreement in image interpretation was almost perfect for all variables except transverse diameter of the spleen (0.77) (Table 1).

Phase II: Comparison of MRI Findings Between Patient Groups
Because interobserver and intraobserver agreement was high, only the results of observer 1 were used for comparison between the groups of patients with schistosomiasis and cirrhosis.

Evaluation of the qualitative morphologic findings showed that periportal fibrosis, heterogeneity of the hepatic parenchyma, and splenic siderotic nodules were more frequently seen in the schistosomiasis group than in the cirrhosis patients (Table 2). In addition, although periportal fibrosis was present more often in the patients with schistosomiasis than in those with cirrhosis, the morphologic distribution of this finding was also different, occurring peripherally in those with schistosomiasis compared with a central distribution in cirrhotic patients. No significant difference in the presence of irregularity of hepatic contours or fissure widening was seen between the two groups.

Evaluation of quantitative measurements of the liver and spleen showed significant differences between both groups for the transverse diameter of the right hepatic lobe, caudate lobe–right lobe ratio, and splenic index (p < 0.01 for all comparisons) (Table 3). The ratio of the caudate lobe to right hepatic lobe and the splenic index were larger in patients with schistosomiasis (p < 0.001).

We subsequently performed univariate logistic regression analysis for each variable studied. Two different models were obtained, the first including all variables and a second excluding the splenic index because seven of the patients with schistosomiasis had previously undergone splenectomy. The regression analysis including all variables showed that the presence of splenic siderotic nodules (PSN) and the splenic index (SI) were the variables that best fitted the model (probability of cirrhosis = 1/1 + e^[–6.0946 + 3.4243 (PSN) + 0.0034(SI)]). We performed a receiver operating characteristic curve analysis to determine a cutoff value that offered both sensitivity and specificity in differentiating both groups of patients (Fig. 4). A splenic index of 1,197 cm³ had a sensitivity of 94% and a specificity of 84% in determining the presence of schistosomiasis.

View larger version (8K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 4 —Receiver operating characteristic (ROC) curve derived shows sensitivity and false-positive rate (1–specificity) for diagnosis of schistosomiasis. Dotted line represents curve for test that is no better than chance. Continuous line represents data obtained from study data. Area under ROC curve was 0.921.

View larger version (8K): [in this window] [in a new window] [as a PowerPoint slide]   Fig. 5 —Graph shows percentage of cirrhotic patients according to caudate lobe–right lobe ratio.

Discussion

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Previous studies have shown that MRI findings in chronic hepatosplenic schistosomiasis include hepatic parenchymal heterogeneity, periportal thickening, hepatic fissure widening, and periportal venous collateralization [8, 18, 19]. These MRI findings are also observed in patients with cirrhosis, as confirmed by this study. Discrimination between cirrhosis and chronic hepatosplenic schistosomiasis is important because the treatment for and prognosis associated with the two diseases are quite different [20, 21].

To our knowledge, this study represents the first of its kind to compare MRI findings to differentiate alcoholic and virus-induced cirrhosis and chronic hepatosplenic schistosomiasis. Toward this end, our results showed that the presence of peripheral periportal fibrosis was more characteristic of chronic schistosomiasis than of cirrhosis, whereas central distribution of periportal fibrosis was present more often in patients with cirrhosis than in those with schistosomiasis. This difference in distribution of fibrosis may be explained by the mechanism of fibrosis formation: Periportal fibrosis occurs as a reaction to the deposition of the parasites' eggs and therefore is limited to the periportal space in schistosomiasis, whereas parenchymal injury and fibrosis are more diffuse with cirrhosis resulting from alcohol intake or viral infection and involve the whole parenchyma [2, 21–23]. Periportal fibrosis can be seen with sonography, making it useful for field studies in less developed countries, although studies have shown considerable interobserver variation in the assessment of schistosomiasis [24]. Other causes of periportal fibrosis besides schistosomiasis and cirrhosis exist but are less frequent [25].

Prior studies have suggested that a caudate lobe–right lobe ratio of > 0.65 is predictive of underlying cirrhosis [14]. In our study, chronic schistosomiasis resulted in a larger caudate lobe–right lobe ratio than cirrhosis, mostly because of a greater reduction in the right lobe, suggesting that this parameter is not specific for cirrhosis. Other studies have proposed modified ratios to attain greater sensitivity in the diagnosis of cirrhosis [26]; however, given that the caudate lobe–right lobe ratios were higher in patients with chronic schistosomiasis, modified values could still not be used to differentiate between these two entities. Although there was a statistical difference in caudate lobe–right lobe ratios between our groups, the practical use of this information is unclear given that there is overlapping of maximum and minimum values for each group and no threshold value for separating the group with cirrhosis from the group with chronic schistosomiasis [26].

Chronic schistosomiasis resulted in more marked splenic changes on imaging than cirrhosis, and these changes seen on imaging may be useful in differentiating these two entities. For example, the longitudinal diameter of the spleen and the splenic index were larger in patients with chronic schistosomiasis; indeed, regression analysis in patients who had not undergone splenectomy showed that splenic findings such as splenic index and the presence of siderotic nodules, are strong indicators of schistosomiasis. Using a splenic index cutoff value of > 1,197 cm³, we obtained a high sensitivity and specificity (94% and 84%, respectively) to discriminate the two groups of patients. In addition, although siderotic nodules in the spleen were present significantly more often in patients with schistosomiasis in our study than in patients with cirrhosis (64.7% vs 3.7%, respectively), data reported in the current literature document considerable variability in the presence of siderotic nodules in the spleen in patients with cirrhosis (ranging from 9% to 64%) [12, 13, 27]. Similarly, in the largest study published to date using sonography, Cerri et al. [18] found a lower prevalence of siderotic nodules in patients with schistosomiasis (7%) than we did, which may result from MRI's increased sensitivity in showing these nodules or from our patients having a more advanced stage of chronic schistosomiasis, thereby allowing more time for parenchymal hemorrhage and formation of the nodules [12, 13] than the patients in the study by Cerri et al.

Although several morphologic characteristics may be useful in diagnosing chronic hepatosplenic schistosomiasis on MRI, the role for MRI in evaluating patients with known chronic hepatosplenic schistosomiasis remains unclear. MRI is unlikely to replace sonography in the current diagnostic paradigm, and potential future roles for MRI evaluation require further investigation. Possibilities may include evaluating the subgroup of patients who have continued disease progression despite medical treatment for evaluating changes in disease burden given that sonography has shown greater variability in interobserver image interpretation [24]. In addition, some patients with more advanced chronic hepatosplenic schistosomiasis and speci fically with increased splenic size require surgical intervention, such as esophagogastric devascularization and splenectomy, and may benefit from more detailed cross-sectional imaging such as MRI [28, 29].

We included in this study patients with alcoholic and virus-induced cirrhosis. Despite the fact that a previous report showed distinct MRI features in these patients, we did not observe any significant difference among the variables analyzed in these two subgroups [10]. The small size of our population study could be responsible for these results.

Our results, confirming the results of a recent study by Bezerra et al. [7], show high intraobserver and interobserver agreement in image interpretation, which varied from moderate to almost perfect, with values being higher for the quantitative variables. These findings are consistent with the findings that have been previously reported for MRI and are superior to sonography for some variables such as periportal fibrosis [24, 30–32].

Our study has several limitations. As we have mentioned, the first limitation concerns the small size of our study population; a larger series might have revealed additional MRI features that could be used for differentiation between the two diseases. Second, our study was limited to patients with cirrhosis caused by viral hepatitis or alcohol abuse. We did not include patients with other causes of cirrhosis, such as patients with primary sclerosing cholangitis in which the caudate lobe tends to be more hypertrophied, similar to what we have seen in the group with schistosomiasis [33]. However, this sign was not the only one that could be used to differentiate between the two groups of patients. How the addition of patients with cirrhosis resulting from these other causes would have affected our results is unclear, and further studies may be necessary. Third, MR measurements and some findings in this study can also be assessed using helical CT, although MRI may offer a more extensive and comprehensive evaluation of chronic liver disease, including findings such as iron deposition, regenerative and dysplastic nodules, and splenic siderotic nodules [34]. Finally, we did not evaluate every single radiologic sign that has been described in cirrhosis, such as an expanded gallbladder fossa or the presence of a right posterior hepatic notch [35]. However, the right posterior hepatic notch is a consequence of hypertrophy of the caudate lobe and atrophy of the right hepatic lobe, both of which were measured in our study. We also analyzed findings such as fissure widening that are similar to the "expanded gallbladder fossa" sign. Further MRI findings can be described and could be used to discriminate cirrhosis and schistosomiasis.

In conclusion, several morphologic characteristics, such as enlargement of the caudate lobe, peripheral periportal fibrosis, and the presence of siderotic nodules in the spleen, on MRI are more frequent findings in patients with hepatosplenic schistosomiasis than in patients with virus-induced or alcoholic cirrhosis. In addition, the splenic index is significantly larger in patients with schistosomiasis. These MRI imaging features may be useful in differentiating cirrhosis and chronic hepatosplenic schistosomiasis.

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