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Original Research |
1 Department of Radiology, MRI Unit, University Hospital of Heraklion,
University of Crete Medical School, Crete, Greece.
3 First Department of Pediatrics, "Aghia Sophia" Children's
Hospital, Thalassemia Unit, University of Athens, Athens, Greece.
4 Thalassemia Unit, "Aghios Georgios" Hospital, Chania,
Greece.
Received May 19, 2004;
accepted after revision October 4, 2004.
Address correspondence to O. Papakonstantinou
(olypapak{at}hotmail.com).
Abstract
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MATERIALS AND METHODS. Abdominal MRI studies of 60 consecutive patients with ß-thalassemia major, performed for quantification of liver iron overload at a single institution, were retrospectively studied for the presence of lymph nodes and their distribution, size, and number. The signal intensity ratios of liver, spleen, and the largest lymph node to the right paraspinous muscle (L/M, S/M, and LN/M, respectively) were calculated on T1-weighted gradient-echo images. MRI findings for the lymph nodes were compared with the histologically assigned activity level of chronic hepatitis C that was available in 17 patients who had undergone liver biopsy within 1 month of the MRI examination.
RESULTS. Hypointense abdominal lymph nodes larger than 7 mm were seen in 19 (32%) of 60 thalassemic patients in perihepatic and paraortic distributions. Lymphadenopathy was related to both the severity of hepatic siderosis, as expressed by the L/M values, and the presence of chronic hepatitis C, given that 18 (95%) of the 19 thalassemic patients with lymphadenopathy had chronic hepatitis C. Moreover, thalassemic patients with a moderate or severe level of hepatic inflammation presented with abdominal lymphadenopathy more frequently than those with mild hepatic inflammation.
CONCLUSION. The development of hypointense abdominal lymphadenopathy in patients with ß-thalassemia major who have received multiple transfusions depends both on the severity of liver iron overload and on the presence and the activity level of coexistent chronic hepatitis C.
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During the last years, MRI has been used with increasing frequency for the noninvasive quantification of hepatic and cardiac iron overload in thalassemic patients [9-18], although a consensus in regard to the most effective MRI technique has not yet been reached. At our institution, indirect quantification of hemosiderosis of the liver and myocardium with MRI has been added in the diagnostic follow-up of thalassemic patients and has eliminated the need for liver biopsies.
We have noticed markedly hypointense perihepatic and retroperitoneal lymph nodes in several abdominal MRI studies of patients with ß-thalassemia major who were referred for evaluation of iron overload. Abdominal lymphadenopathy has been sporadically reported in patients with ß-thalassemia major, seen on abdominal radiography [19], lymphography [20], and abdominal CT [21] and more recently on sonography of the abdomen [22]. To our knowledge, the MRI findings of abdominal lymphadenopathy in ß-thalassemia major have not been described.
The goals of our study were, first, to identify the frequency of and describe the MRI findings of abdominal lymphadenopathy in a large series of patients with ß-thalassemia major who received multiple transfusions and, second, to investigate the relation between abdominal lymphadenopathy, the severity of iron overload, and the presence of posttransfusion hepatitis C in thalassemic patients.
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Forty-one patients had chronic hepatitis C, two of whom were also positive for HBsAg hepatitis. All patients were negative for HIV. No patient had a clinically or radiologically detectable neoplasm at the time of MRI or during the 1- or 2-year follow-up. The diagnosis of chronic hepatitis C was based on the presence of anti-hepatitis C virus antibodies and hepatitis C virus RNA in the serum and on histologic findings compatible with chronic hepatitis. All patients with chronic hepatitis C had increased serum alanine aminotransferase levels (> 80 U/L) for at least 1 year, whereas patients without hepatitis had alanine aminotransferase levels within the normal limits (25-73 U/L) or slightly above the normal range.
The pathology reports of 17 patients with hepatitis C who had undergone liver biopsy within 1 month before or after MRI were reviewed. On histology, the activity of hepatic inflammation was assessed by means of the histologic activity index, according to the criteria described by Knodell et al. [23]. The histologic activity index consists of four components: periportal necrosis with and without bridging necrosis, intralobular degeneration, portal inflammation, and fibrosis [23]. The extent of fibrosis and the development of cirrhosis were, in addition, evaluated according to Desmet et al. [24]. Subsequently, the thalassemic patients with available liver histology were categorized into two groups with regard to the activity level of chronic hepatitis: mild (n = 13 patients), moderate or severe (n = 4 patients [moderate, n =2; severe, n = 2]). The two patients with severe hepatic inflammation also had architectural changes of cirrhosis.
MRI
Technique—All examinations were performed on a 1.5-T MRI
system (Vision Plus, Siemens Medical Solutions). Breath-hold gradient-echo
sequences were performed using a body coil to avoid signal drop-off
[18] and to ensure the highest
uniformity in the signal-to-noise ratio throughout the whole scanned volume
compared with the phasedarray coil. In addition, the following sequences were
performed: a T1-weighted gradient-echo sequence (TR/TE, 182/4.6; flip angle,
90°) with 21 slices acquired, intermediate-weighted in-phase and
out-of-phase gradient-echo sequences (120/4; flip angle, 20°; and 120/2.7;
flip angle, 20°, respectively) with 15 slices acquired, and T2-weighted
gradient-echo (120/15; flip angle, 20°) and T1-weighted spin-echo (600/6)
sequences with 11 slices acquired. All images were obtained in the axial plane
with a slice thickness of 8-10 mm, an image matrix of 256 x 192, and a
field of view of 400-500 mm.
This MRI protocol is routinely used in patients with iron overload and is based on literature data [11, 12], trials with phantoms, equation fits between liver-to-muscle signal intensity ratios, and direct determination of liver iron concentration in liver biopsy specimens, so a wide spectrum of hepatic hemosiderosis can be evaluated (Papakonstantinou O and Maris TG, unpublished data).
Image interpretation—All MRI studies were retrospectively reviewed for the presence of abdominal lymphadenopathy by an experienced abdominal radiologist who was unaware of the clinical and laboratory data. All lymph nodes with a long-axis diameter equal to or greater than 8 mm were recorded and were defined as nontubular soft-tissue structures that were clearly distinguishable from adjacent anatomic structures [25]. A conservative approach was taken in the declaration of the presence of visible lymph nodes; ambiguous findings were excluded.
Lymph nodes were categorized into two major groups with regard to location: perihepatic (including periportal, peripancreatic, portacaval, celiac, and gastrohepatic) and paraortic lymph nodes in the retroperitoneum [26]. For each nodal group, the number of lymph nodes was estimated, the long and the short axes of the largest node in each group were recorded, and their size was estimated by multiplying the short axis and long axis of the node [27]. For identification of lymph nodes, images obtained with all MRI sequences were reviewed, whereas estimations of nodal number, size, and signal intensity were performed on the T1-weighted gradient-echo images, which had the best spatial resolution and depicted most conspicuously the lymph nodes over a wide spectrum of nodal signal intensities. Subsequently, the signal intensity ratios of the liver, spleen, and the largest lymph node of each nodal group to the right paraspinous muscle (L/M, S/M, and LN/M, respectively) were calculated on the same images. The signal intensity of the hepatic parenchyma was considered as the average of three signal intensity measurements obtained at circular regions of interest that measured 1-2 cm2 and were located in the right liver lobe, away from vascular structures and breathing artifacts. The signal intensity of the spleen was the average of measurements in two similar regions of interest at the periphery of the posterior segment of splenic parenchyma, whereas the signal intensity of the largest lymph node was measured in a single region of interest that was located in the central part of the node and measured 0.5-1 cm2.
Statistics
Linear regression analysis was used to correlate L/M, S/M, and LN/M ratios.
To determine the impact of hepatic siderosis (i.e., L/M values), chronic
hepatitis, and splenectomy on the presence of abdominal lymphadenopathy, we
performed multivariable logistic analysis. The chi-square test was used for
pair-wise comparisons of patients with mild hepatitis and patients with
moderate or severe hepatitis in regard to the presence of abdominal
lymphadenopathy, whereas the t test was used to compare nodal size
and number between the two groups. All analyses were performed using
statistical software (TableCurve 2D, Systat [version 7.3], MedCalc
Software).
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Of the 60 thalassemic patients in our study group, 41 were positive for the hepatitis C virus; in 17 of these 41 patients with hepatitis C, liver histology results obtained within 1 month from the time of MRI were available. According to the histologic report, 13 of the 17 patients had mild level of activity of hepatic inflammation and the remaining four patients had moderate or severe level of activity. For this group of 17 thalassemic patients with hepatitis C and available liver histology, we considered the relation between the activity level of chronic hepatitis and the development of abdominal lymphadenopathy.
We found that the presence of lymphadenopathy was related to the activity level of chronic hepatitis C (p < 0.05) for the 17 thalassemic patients with available evaluation of the level of hepatic inflammation on histology. As shown in Table 2, of the 13 patients with histologically confirmed mild activity of hepatic inflammation, only four developed abdominal lymphadenopathy. Nodes were seen in all four patients with moderate or severe level of activity of hepatic inflammation. In addition, patients with moderate or severe level of activity of hepatic inflammation had larger mean size and higher mean number of affected lymph nodes than patients with mild activity of hepatitis, but pair-wise comparison was significant only for nodal size. Table 2 summarizes the results regarding the presence of lymphadenopathy and the number and size of lymph nodes with respect to the activity level of chronic hepatitis.
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Parsons [20] referred to lymphographic patterns of enlarged paraortic and iliac lymph nodes that ranged from coarsely granular nodes to large filling defects. In a more recent study, Chu et al. [22] reported enlargement of lymph nodes at the hepatoduodenal ligament on sonography in 12 (32.4%) of 37 consecutive thalassemic patients. The latter authors did not specify whether they searched for retroperitoneal lymphadenopathy [22]; detection of lymph nodes in the ventral portion of the hepatoduodenal ligament and retroperitoneum may be difficult on sonography [27, 28] because of the surrounding fat and connective tissue.
We found a similar frequency of abdominal lymphadenopathy (32%) in a larger series of 60 consecutive patients with ß-thalassemia, with perihepatic distribution in all patients and paraortic in 74% of them. Abdominal lymphadenopathy in patients with ß-thalassemia who have received multiple transfusions is a rather common imaging finding on sonography, CT, or MRI studies of the upper abdomen. Because this finding is underscored in the literature, it may cause confusion and anxiety in clinicians and patients that then lead to unnecessary investigations. In this study, we present a systematic description of the MRI features of abdominal lymphadenopathy in ß-thalassemia; furthermore, we attempt to explore the relation of lymphadenopathy with posttransfusion chronic hepatitis C and the severity of iron overload.
Abdominal lymphadenopathy has been associated with a variety of pathologic conditions, including lymphoma and metastatic disease, which are the most common, but it has also been associated with benign causes, such as tuberculosis, histiocytosis, sarcoidosis, lymphoproliferative disorders, Whipple's disease, and Crohn's disease [29-31]. Patients with chronic hepatitis C and other chronic liver diseases such as primary biliary sclerosis or sclerosing cholangitis often present with perihepatic lymphadenopathy on cross-sectional imaging studies, whereas enlargement of the retroperitoneal lymph nodes is less common [25, 32-34].
The pathologic conditions, however, are not known to exhibit hypointense lymph nodes on T1- and T2-weighted spin-echo or gradient-echo sequences. Hypointensity of lymph nodes in thalassemic patients who have received multiple transfusions is presumably because of iron deposition in the reticuloendothelial cells of the nodes. To our knowledge, abdominal lymphadenopathy has not been reported in patients with primary hemochromatosis.
The signal intensities of lymph nodes in the thalassemic patients of our study were similar to that of the liver for each individual patient, as shown by the strong correlation between the L/M and LN/M values; this correlation implies that the mechanisms of iron delivery and storage are similar in the liver and lymph nodes. Iron deposition in the spleen did not follow hepatic and lymph node iron overload, as suggested by the lack of correlation between the S/M values and the L/M or LN/M values. The capability of MRI to depict iron deposition in solid viscera may be of value in elucidating the mechanisms of iron distribution in various tissues.
Both posttransfusion chronic hepatitis and the severity of iron overload, as expressed by L/M ratios, seem to contribute to the development of lymphadenopathy. Most of our patients with abdominal lymphadenopathy also had chronic hepatitis C (95%), in contrast to Chu et al. [22] who found that only 32.4% of the thalassemic patients with lymphadenopathy in their study were positive for chronic hepatitis C [22]. Zhang et al. [27] reported that the size, number, and signal intensities of perihepatic enlarged lymph nodes correlated with the severity of hepatic inflammation in patients with chronic hepatitis C and advocated their use as criteria for the activity of hepatic inflammation [27], whereas others have proposed estimation of nodal size with sonography [28]. For the limited number of thalassemic patients with coexistent chronic hepatitis C and available liver biopsy, we found that the size of the abdominal lymph nodes related to the activity level of chronic hepatitis.
A drawback of our study is the lack of histologic findings for the abnormal lymph nodes. Another disadvantage is that thin sections with a smaller field of view were not obtained because MRI examinations aimed to quantify liver iron and to achieve the highest possible signal-to-noise ratios, which scarifies spatial resolution; therefore, estimation of nodal size and signal may not be accurate enough because of partial volume effects, although we have considered the largest node for each patient.
In conclusion, enlarged hypointense lymph nodes in perihepatic and paraortic distributions is a common MRI finding in patients with ß-thalassemia who have received multiple transfusions and have posttransfusion chronic hepatitis C. Although abdominal lymphadenopathy is frequently seen in patients with hepatitis C, hypointense lymph nodes seem to occur only in association with ß-thalassemia. Further studies should verify whether MRI, along with its emerging application as a noninvasive alternative to liver biopsy for the evaluation of liver iron overload, might provide indications with regard to the activity of posttransfusion chronic hepatitis C, which is common in patients with ß-thalassemia who have received multiple transfusions.
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