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1
Department of Diagnostic Imaging, Chaim Sheba Medical Center, Tel Hashomer,
Ramat Gan 52621, Israel.
2
Department of Diagnostic Imaging, Sapir Medical Center, Kfar Saba 44281,
Sackler School of Medicine, University of Tel Aviv, Tel Aviv 69978,
Israel.
3
Institute of Hematology, Chaim Sheba Medical Center, Tel Hashomer, 52621
Israel.
Received June 11, 2001;
accepted after revision September 25, 2001.
Address correspondence to S. Apter.
Abstract
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SUBJECTS AND METHODS. CT of the chest, abdomen, and pelvis of 956 newly diagnosed patients with lymphoma was evaluated prospectively for calcifications in enlarged lymph nodes and lymphoma masses. Findings were correlated with histologic type of disease, tissue parameters, and clinical course. Calcifications were further evaluated on follow-up CT.
RESULTS. Of 956 patients with lymphoma (704 with non-Hodgkin's lymphoma and 252 with Hodgkin's lymphoma), eight patients (0.84%) showed calcifications in involved sites, seven of whom had non-Hodgkin's lymphoma and one of whom had Hodgkin's lymphoma. Calcifications were present in lymph nodes and masses in the mediastinum in five patients, in the retroperitoneum in two patients, and in the adrenal in one patient. All eight patients had the aggressive type of lymphoma. Four patients later relapsed, one of whom died. A fifth patient died after only minimal response to treatment.
CONCLUSION. Calcification in patients with lymphoma occurring before therapy is rare as opposed to that in lymphoma after therapy. It occurred in our patients more often in the mediastinum, in patients with non-Hodgkin's lymphoma rather than in patients with Hodgkin's lymphoma, and only in patients with the aggressive type of disease.
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Calcification in patients with lymphoma before treatment is extremely rare. A few such cases have been described [9,10,11,12,13,14,15,16,17,18,19,20], but to our knowledge, this topic has not yet been systematically evaluated.
The purpose of our study was to assess the CT features, prevalence, and clinical significance of calcification detected in lymphoma before therapy.
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All patients underwent CT of the chest, abdomen, and pelvis as part of staging. All studies were performed with enteric contrast material. CT of the abdomen and pelvis was always performed with IV contrast material unless there was a contraindication. Approximately 60% of chest CT studies were also performed with IV contrast material. These examinations were prospectively studied by two senior radiologists for the presence, shape, and extent of calcification in involved sites.
Calcifications caused by granulomatous disease were also observed. Calcifications seen in mediastinal or hilar nodes in association with calcified nodules in the ipsilateral lung were regarded as granulomatous disease [21]. Unenhanced scans were preferable for evaluation. Patterns of calcification were categorized as clustered, punctate, amorphous, or linear [6]. CT findings were correlated with histologic type of disease and tissue parameters (sclerosis, fibrosis, collagen tissue, cellular infiltrates, necrosis, and hemorrhage) when available. Diagnosis was established by biopsy of nodal (n = 7) or extranodal (n = 1) masses. Five patients underwent surgery, including three lymph node resections (cervical, axillary, and inguinal), one laparotomy (adrenalectomy), and one thoracotomy. Three patients had percutaneous CT-guided biopsies, including fine-needle aspiration (n = 2) and core biopsy (n = 1). Biopsies were obtained from nodal masses with calcifications in four and from separate anatomic sites (cervical, axillary, retroperitoneal, and inguinal) in the other four. The appearance of calcification was further evaluated on CT after treatment. Two patients with non-Hodgkin's lymphoma and generalized lymph node enlargement had a solitary small calcification in an enlarged mediastinal node, associated with a calcified lung nodule. Thus, we could not exclude lymphoma engulfing pre-existing granulomatous calcification and did not include them in the series.
CT was performed on a 2400 Elite scanner (conventional axial mode) (Elscint, Haifa, Israel) or a helical Twin scanner (Elscint).
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Radiologic Findings
Of the eight patients, two had disease limited to one anatomic site, and
six had disease in two or more anatomic sites. Of the latter, one had
calcifications in different foci of disease.
Five patients had califications in mediastinal foci of disease, and three had calcifications in involved sites in the abdomen. One of the former, a 32-year-old man with non-Hodgkin's lymphoma, has been reported previously [18]. Of patients with masses in the mediastinum, four had large masses located anteriorly, thymic in location, and one had subcarinal lymphadenopathy. Calcifications in these masses were clustered, multiple, punctate, and located in the center of the mass in all five patients (Fig. 1A,1B). Two patients showed calcification in the periphery of a hypodense, probably necrotic, area in the mass. These calcifications were linear in one patient (Fig. 1B) and punctate in the other patient (Fig. 2A).
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In two of the five patients, calcifications could also be identified on chest radiography, although less clearly. In the other three, calcifications appeared as small foci on CT and were not visible on chest radiography (Figs. 2B and 2C). Vascular calcifications were present in one (Fig. 1A,1B); granulomatous calcifications were not present in any of these patients.
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In the abdomen, enlarged nodes were present in the retroperitoneum, mesentery, and pelvis in two patients, and a mass was present in the adrenal in the third. Calcifications in the enlarged nodes were small, punctate, or amorphous (Fig. 3A). One of these patients had, in addition, tiny foci appearing around an area of low density in the node. Linear calcifications were present in the adrenal mass (Fig. 4). The calcifications in the mesenteric nodes were similar in appearance to surrounding opacified small-bowel loops, and those in pelvic nodes were similar to calcifications in adjacent iliac arterial wall. These calcifications caused some difficulty in diagnosis. Calcification in the adrenal mass suggested, mistakenly, a primary adrenal tumor, and therefore, adrenalectomy was performed.
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Clinical Findings
Of eight patients with calcifications, seven had non-Hodgkin's lymphoma.
The total number of patients with non-Hodgkin's lymphoma was 704. Of these,
245 had disease that was classified as aggressive, and 459 had disease
classified as indolent lymphoma, according to the World Health Organization
classification system [22]. Of
252 patients with Hodgkin's lymphoma, one patient had calcification.
Four of the patients with non-Hodgkin's lymphoma had large B-cell lymphoma, two had T-cell lymphoblastic lymphoma, and one had mantle cell type B-cell lymphoma. These types are regarded as the more aggressive forms of non-Hodgkin's lymphoma. The patient with Hodgkin's lymphoma had the mixed cellularity variant, also regarded as a more aggressive type of Hodgkin's lymphoma [22].
There were no calcifications in patients with the less aggressive indolent lymphoma.
Tissue Parameters
Findings showed sclerosis on biopsy in one patient, fibrosis and collagen
tissue in one patient, necrosis and hemorrhage in one patient, and cellular
infiltrates in two patients. The patient with Hodgkin's lymphoma also had
cellular infiltrates. Two patients had undergone only fine-needle aspiration
of the nodes involved with disease, with (n = 1) or without
(n = 1) calcification; thus, tissue parameters were not available in
these patients.
Follow Up
On clinical follow-up that occurred 3-48 months after diagnosis, findings
on repeated CT in four patients showed relapse. Calcifications remained
unchanged in size in three of these patients, although the nodes had increased
in size. Findings in one patient showed an increased size of calcifications,
whereas the nodes became smaller (during the first remission)
(Fig. 3B). Two patients died:
one, after minimal response to chemotherapy. Two patients are free of disease
1.5-4 years after treatment. The last patient was only recently diagnosed, and
follow-up studies have not yet been performed.
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Lymphoma nodes treated with radiation or chemotherapy may calcify. This calcification occurs in approximately 2-8% of cases typically at least 8 months after treatment [2, 3, 6, 12, 33]. We found calcifications in 0.84% of patients with lymphoma before treatment, most commonly in the mediastinum, and in patients with non-Hodgkin's lymphoma. All patients with calcifications had the more aggressive types of the disease. This small group of patients included findings of three different entities of aggressive non-Hodgkin's lymphoma, namely diffuse large B-cell, mantle cell, and T-cell lymphoblastic lymphoma. Moreover, one patient had a mixed cellularity type of Hodgkin's lymphoma. Each of these entities has its own reported rate of response to treatment and disease-free survival rate. Thus, it is not possible to draw conclusions from such a small number of patients. However, whereas calcification occurring after therapy is reported to point to a relatively good prognosis [4, 5, 7, 8], our experience would suggest that this seems not to be the case in calcification occurring before therapy. To our knowledge, this type of calcification has rarely been described in the literature. Only a few cases have been published, five with Hodgkin's lymphoma [9, 11, 13, 33] and 11 with non-Hodgkin's lymphoma [10, 13,14,15,16,17,18,19]. Five of the latter were in children younger than 12 years old, including three patients with Burkitt's lymphoma [10, 16, 34]. Calcifications were seen in nodal disease and in extranodal sites such as liver, lung brain, and small bowel [9,10,11,12,13,14,15,16,17,18,19,20].
The calcifications described in the literature appeared as massive [13], faintly punctate [14], or high-density foci [20] in lymph nodes or masses. Our observations were similar. Calcifications were seen as small punctate foci in the nodes, tiny calcifications around necrotic areas, amorphous or linear in or in the periphery of the enlarged nodes or masses. Calcifications were similar in appearance above and below the diaphragm. In the mediastinal masses, calcifications were more easily detected on CT than on chest radiography. Calcifications located adjacent to the aortic wall were somewhat difficult to differentiate from vascular calcifications. It was difficult to differentiate a solitary calcification in an enlarged mediastinal lymph node from a preexisting granulomatous calcification engulfed by lymphoma. The presence of a calcified lung nodule led us to assume the latter possibility.
Calcifications in the abdomen were similar to and difficult to distinguish from adjacent opacified bowel. The differential diagnosis from calcifications in the arterial wall next to the nodes in the pelvis was also complex, especially after treatment when the nodes were smaller and less obvious.
The pathogenesis of calcification in lymphoma occurring before therapy is uncertain. Generally, tissue calcifications can be metastatic or dystrophic [35]. In the former, they are caused by excessive or unstable calcium ion concentration in the blood. Such hypercalcemia was noted, however, in only one patient with Hodgkin's lymphoma reported in the literature [34]. Some types of T-cell lymphoma have been associated with disordered calcium metabolism that may be related to an osteoclast-activity factor produced by the tumor [36]. All our patients and those reported in the literature had normal calcium levels in the blood, thus making this explanation less reasonable.
Dystrophic calcification frequently occurs in degenerated or necrotic tissue [20]. Most reported patients with calcification in Hodgkin's lymphoma had the nodular sclerosing type. Intensive collagen fibrosis and areas of cellular degeneration and necrosis present in this form of Hodgkin's lymphoma may be a predisposing substance for the formation of dystrophic calcifications [9, 12].
Patients with non-Hodgkin's lymphoma with calcified lesions showed cell degeneration and necrosis similar to those reported in the patients with Hodgkin's lymphoma [14, 15, 19]. Cell degeneration and necrosis are the result of infarction and are followed by calcification. Such infarction occurs typically in the aggressive histologic type of lymphoma [37]. Our patients had the aggressive type of the disease, such as large B-cell lymphoma and T-cell lymphoblastic lymphoma [22]. This finding was similar to that of patients reported in the literature who had mainly aggressive types of lymphoma [37]. These findings may suggest a dystrophic mechanism as the pathogenesis for calcification in lymphoma occurring before therapy.
The clinical significance of de novo calcifications in untreated lymphoma is uncertain. The literature suggests that patients with tumoral calcification after lymphoma treatment (especially for Hodgkin's lymphoma) have a better prognosis [3,4,5, 8]. However, the presence of calcification in lymphoma before therapy, as in our patient population, may have a less favorable prognosis. Conclusions from such a small series cannot be generalized, however, and further studies are necessary.
The number of patients with detectable calcification in lymphoma seems to be on the increase, probably because of the widespread use of CT. Primary untreated Hodgkin's lymphoma and non-Hodgkin's lymphoma rarely exhibit calcification. However, calcification of nodal or extranodal masses in the chest, abdomen, and pelvis in patients with other clinical and imaging features of lymphoma should alert the radiologist to the possible diagnosis of an aggressive lymphoma.
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