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AJR Integrative Imaging LIFELONG LEARNING FOR RADIOLOGY |
1 Department of Diagnostic Radiology, Mayo Clinic, 13400 E Shea Blvd.,
Scottsdale, AZ 85259.
2 Department of Laboratory Medicine and Pathology, Mayo Clinic, Scottsdale,
AZ.
Received August 31, 2006; accepted after revision November 21, 2006.
Address correspondence to A. C. Silva
(silva.alvin{at}mayo.edu).
Keywords: abdominal imaging • cancer • liver disease • MR contrast agents • oncologic imaging
Clinical History
An otherwise asymptomatic 62-year-old man with end-stage liver disease secondary to hepatitis C presents for routine follow-up and screening to exclude hepatocellular carcinoma (HCC).
Radiologic Description
Contrast-enhanced CT of the abdomen (Figs. 1A and 1B) reveals two hepatic masses with subtle peripheral hypervascularity and central hypovascularity on arterial and portal venous phases, neither of which shows portal venous shunting on the delayed images. In addition, several low-attenuation foci are present in the spleen, the largest measuring up to 1.3 cm. Contrast-enhanced MRI of the abdomen using gadobenate dimeglumine (MultiHance, Bracco) (Figs. 1C and 1D) shows the same arterial and portal venous phases findings as on CT; however, the hepatic lesions show a target-like appearance with delayed central enhancement and a hypointense rim on 1-hour delayed phase imaging. The hepatic and splenic lesions are isointense to normal splenic tissue on the T1- and T2-weighted series. Sonographically guided core biopsy of the posterior right hepatic lobe mass, seen as a well-defined hypoechoic lesion (Fig. 1G), yielded the pathologic diagnosis of large B-cell lymphoma (Fig. 1J). The indeterminate splenic lesions improved after therapy, consistent with lymphomatous deposits.
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The differential diagnosis in this patient includes infection (pyogenic and fungal), atypical or previously treated HCC, metastases, and lymphoma.
Diagnosis
With the given clinical history and imaging findings, lymphoma is the most likely diagnosis.
Commentary
Although the association of chronic hepatitis C infection with cirrhosis and HCC is well-known, the association of hepatitis C with hepatic B-cell lymphoma is not as well recognized [1–4]. Because hepatitis C is the major cause of chronic hepatitis and cirrhosis in the United States, an understanding of this potential complication of the disease is important, particularly in light of the growing use of cross-sectional imaging for HCC surveillance.
Primary non-Hodgkin's lymphoma of the liver is rare, although the number of reported cases in hepatitis C virus (HCV)–infected individuals is increasing [5], with large B-cell lymphoma the usual histologic type. A recent meta-analysis revealed that HCV prevalence in patients with non-Hodgkin's lymphoma was 15%, as opposed to 1.5% in the general population and 2.9% in patients with other hematologic malignancies, implying a causative role of HCV in non-Hodgkin's lymphoma [6]. Although the exact mechanism of pathogenesis of HCV-associated lymphoma is unknown, evidence indicates that HCV can induce clonal proliferation of B cells in chronic HCV carriers, which may play a role in the development of malignant lymphocytes [7].
In general, lymphomatous hepatic masses can be either primary (rare) or secondary. Primary lymphoma more commonly presents as a solitary solid hepatic lesion, whereas secondary lymphoma tends to present as multiple or diffusely infiltrative lesions, with more variability in the imaging appearances [8]. At MRI, focal lymphomatous lesions usually show low T1 signal intensity and variable signal intensity on T2-weighted imaging (Figs. 1C and 1D). The lesions are typically hypovascular, minimally enhancing just after gadolinium administration, and show a faint peripheral rim on subsequent contrast-enhanced phases [9]. Secondary lymphomatous involvement of the liver can occur in up to 50% of patients with non-Hodgkin's lymphoma and 20% of patients with Hodgkin's lymphoma [10, 11].
Gadobenate dimeglumine is a gadolinium-based paramagnetic contrast agent that has the properties of both a conventional extracellular fluid contrast agent and a liver-specific contrast agent (3–5% of the injected dose is taken up by functioning hepatocytes and excreted in bile) [12]. The combination of uptake by the functioning hepatocytes coupled with an inherently twofold higher T1-relaxivity allows prolonged hepatic parenchymal enhancement. Consequently, that enhancing property may provide increased detectability and further characterization of focal hepatic lesions. The gadobenate dimeglumine–enhanced delayed phase imaging provides distinctive enhancement characteristics of these focal liver lesions, adding some valuable information for their characterization (Figs. 1E and 1F).
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With regard to the differential considerations, the hepatic lesions in this patient do not display the characteristic enhancement pattern of HCC—that is, heterogeneous arterial hypervascularity with portal venous phase contrast washout and an enhancing capsule in the delayed phase. Rather, these masses exhibit peripheral ring enhancement initially, which has a fairly broad differential diagnosis: metastases (particularly hypovascular metastases such as colon, lung, prostate, gastric, and transitional cell); infection, including pyogenic abscesses and fungal abscesses; lymphoma; and atypical or previously treated HCC (rim enhancement related to a pseudocapsule or previous ablation). Nevertheless, the masses show a 1-hour delayed target appearance composed of a central round enhancing portion and a peripheral hypointense rim. This is identical to the delayed appearance of most metastases (up to 85%) and cholangiocarcinoma, but uniquely different from other tumors such as HCC, which are often heterogeneously enhancing on the 1-hour delayed images [12]. Thus, this target appearance of enhancement is a unique feature of non-hepatocyte-containing malignancy and allows a more focused differential diagnosis. Similarly, the "peripheral washout sign" previously described on conventional contrast-enhanced MRI specifically indicates malignancy and has been described in some cases of hepatic metastases, including carcinoid, breast, colon, and gastric cancers [13]. This sign is best seen 10 minutes after IV contrast administration and consists of a peripheral rim that is hypointense relative to the center of the lesion.
Although metastases cannot be reliably differentiated from primary hepatic lymphoma on the basis of imaging findings, in general metastases are less commonly seen in the setting of end-stage liver disease [14]. In addition, the patient did not have a history of another primary malignancy. Pyogenic hepatic abscesses, on the other hand, can be excluded on the basis of the lack of symptoms in this patient. Abscesses typically will present with abdominal pain and associated fever or leukocytosis in an immunocompetent host. On MRI, these lesions can have a variable appearance on T1- and T2-weighted imaging, but perilesional edema on T2-weighted sequences and the presence of clustered smaller perilesional abscesses are helpful clues to the appropriate diagnosis [15]. After contrast administration, ring enhancement with variable wall thickening as well as perilesional hyperemia can be seen.
As primary hepatic B-cell non-Hodgkin's lymphoma is an uncommon, but potential, complication of chronic hepatitis C infection, the following points should be kept in mind:
First, as a general rule, focal hepatic B-cell non-Hodgkin's lymphoma typically is hypovascular after contrast administration, with a peripheral enhancing rim on late arterial and early portal venous phase sequences.
Second, primary hepatic B-cell non-Hodgkin's lymphoma can have an appearance identical to that of hepatic metastases on gadobenate dimeglumine–enhanced delayed phase imaging, characterized by a target appearance. Correlation with clinical history and tissue sampling may be required for accurate differentiation.
Third, primary hepatic lymphoma typically presents as a solitary solid mass, whereas secondary hepatic lymphoma will more often present as multiple or diffusely infiltrative lesions.
Objective
The educational objective of this article is to describe the typical imaging findings of hepatic lymphoma, as well as to highlight the association of B-cell non-Hodgkin's lymphoma with hepatitis C.
Conclusion
This article describes primary hepatic B-cell non-Hodgkin's lymphoma in a patient with HCV-related cirrhosis and illustrates an important, but underrecognized, association between B-cell non-Hodgkin's lymphoma and HCV. Furthermore, gadobenate dimeglumine–enhanced MRI can be helpful in focusing the differential diagnosis of focal hepatic lesions because it provides distinguishable features on delayed phase imaging.
References
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  C.-H. Liu, D. C. Rivard, A. C. Silva, K. J. Burkholz, and S. D. Beaty Imaging of Focal Hepatic Lesions: Self-Assessment Module Am. J. Roentgenol., June 1, 2008; 190(6_Supplement): S65 - S68. [Abstract] [Full Text] [PDF]
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