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1 Department of Radiology, Samsung Medical Center, Sungkyunkwan University
School of Medicine, 50, Ilwon-Dong, Kangnam-Ku, Seoul 135-710, Korea.
2 Department of Internal Medicine, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Seoul 135-710, Korea.
3 Department of Diagnostic Pathology, Samsung Medical Center, Sungkyunkwan
University School of Medicine, Seoul 135-710, Korea.
Received July 10, 2001;
accepted after revision October 30, 2001.
Address correspondence to H. K. Lim.
Abstract
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MATERIALS AND METHODS. We retrospectively reviewed CT examinations of 58 patients with confirmed gastric MALT lymphomas. Using the histopathologic grade of the MALT lymphomas, we divided the patients into two groups: those with high-grade lymphoma (n = 21) and those with low-grade lymphoma (n = 37). Common CT findings for the two groups were reviewed and compared.
RESULTS. Forty (69%) of the 58 patients showed at least one abnormality of the stomach on CT. Abnormalities included diffuse or segmental gastric wall thickening (66%, 38/58), lymphadenopathy (40%, 23/58), ulcer (22%, 13/58), and gastric mass (3%, 2/58). Eighteen (31%) of 58 patients were found to have no abnormality. The high-grade group had a higher incidence of abnormalities seen on CT than the low-grade group (100% vs 51%, respectively). Gastric wall thickening in the high-grade group was more diffuse (48% vs 8%) and severe (71% vs 14%; severe or moderate) than that seen in the low-grade group. Lymphadenopathy was visualized in 67% of the high-grade group and in 24% of the low-grade group. Gastric ulcer was found in 57% of the high-grade group and in only 5% of the low-grade group. The gastric mass formation was seen in only two patients in the high-grade group.
CONCLUSION. The CT findings of gastric MALT lymphoma that the two groups had in common were gastric wall thickening and lymphadenopathy. Although our results pointed to no specific CT finding for differentiating high-grade from low-grade gastric MALT lymphomas, we found that the absence of abnormality on CT is highly predictive of low-grade MALT lymphoma.
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Despite its questionable value, CT has generally been used to stage primary gastric lymphoma [10]. There have been two reports [11, 12] regarding CT findings of gastric MALT lymphoma: Gollub et al. [11] found that 12 (71%) of 17 patients with gastric MALT lymphoma had focal gastric wall thickening or masses. Kessar et al. [12] found that minimal gastric wall thickening was the most common CT finding in seven patients with low-grade gastric MALT lymphoma. To the best of our knowledge, no report to date in the English-language radiology literature has described the helical CT findings of high- and low-grade gastric MALT lymphoma and the differences between the two entities.
The purpose of our study was to evaluate helical CT findings in 58 patients with pathologically proven high- or low-grade gastric MALT lymphoma and to determine CT findings helpful in distinguishing between the two.
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Using the histopathologic grade of MALT lymphomas, we divided these patients into two groups. The high-grade lymphoma group consisted of those patients with only high-grade MALT lymphomas (n = 17) and those with high-grade MALT lymphomas containing low-grade component (n = 4). The low-grade lymphoma group consisted of those patients with only low-grade MALT lymphomas (n = 32) and those with low-grade MALT lymphomas associated with small foci (not a cluster of large lymphoid cells but rather some areas of scattered large cells) of high-grade component (n = 5). We found that in some patients—particularly those in whom the diagnosis of low-grade gastric MALT lymphoma had been based on endoscopic biopsy findings alone—the grade of MALT lymphoma was established only after a 1-year follow-up period. The 21 patients in the high-grade lymphoma group (12 men and nine women) were between 26 and 71 years (mean age, 55 years). Nine of these patients underwent either total (n = 8) or subtotal (n = 1) gastrectomy. The 37 patients in the low-grade lymphoma group (18 men and 19 women) were between 24 and 78 years (mean age, 48 years). Thirteen of these patients underwent either total (n = 11) or subtotal (n = 2) gastrectomy. The presence of H. pylori infection was histopathologically confirmed in 13 patients (62%) in the high-grade group and 30 patients (81%) in the low-grade group by endoscopic biopsy, respectively.
All CT examinations were performed with a helical CT scanner (HiSpeed Advantage; General Electric Medical Systems, Milwaukee, WI) within 15 days (mean, 6 days) of initial endoscopy and surgery. All patients received 800-1200 mL of water as oral contrast material for the adequate distention of the stomach twice—30 min before and then immediately before the examination. The position of patients was prone if the lesion was known to be located in the antrum or lower gastric body. Non-ionic contrast medium (Iopamiro 300 [iopamidol, 300 mg I/mL]; Bracco, Milano, Italy) was used. A mechanical power injector administered 120 mL of Iopamiro at a rate of 3 mL/sec into the antecubital vein. Contrast-enhanced CT of the stomach was then performed in a craniocaudal direction from the dome of the right hemidiaphragm using 5-mm collimation, 5 mm/sec table speed, 120 kVp, and 200 mAs during one breath-hold 70 sec after IV injection of contrast medium. Helical scans were obtained through the upper abdomen, and the rest of the abdomen and pelvis were scanned in a clustered data acquisition mode (7-mm interval).
All images were archived on a commercially available PACS (picture archiving and communication system) workstation (PathSpeed; General Electric Medical Systems). Three abdominal radiologists independently reviewed CT images with window level and center settings controlled at a PACS work-station. They performed this retrospective review without knowledge of the endoscopic and pathologic findings, including the grade of MALT lymphoma, but with knowledge of the final diagnosis of gastric MALT lymphoma. Final interpretations were made by consensus. A standard questionnaire was completed for each patient. CT findings evaluated were the presence or absence of gastric wall thickening; mass formation; distribution of thickened gastric wall; extent of the lesions; maximal thickness of the lesions (including degree); degree of enhancement of the lesions; nature of the outer margin of the lesions; and presence or absence of normal overlying mucosa, perigastric or omental fat infiltration, calcification or low density within the gastric mass, ulcer, and lymphadenopathy.
The distribution of thickened gastric wall was categorized as being in the
antrum, body, or fundus. The extent of the lesions was judged and recorded as
focal (a mass in which the height of the lesion is longer than width), diffuse
(involving > 50% of the entire stomach), or segmental wall thickening
(involving 
50% of the entire stomach)
[13]. The maximal thickness of
the wall was measured using the PACS "measure distance" tool for
the enlarged images (full screen) on a 2000 x 2000 pixel monitor by one
radiologist. The degree of the wall thickness was rated as normal (<5 mm),
mild (5-10 mm), moderate (11-25 mm), or severe (>25 mm)
[14]. The degree of
enhancement of the lesions was recorded as either moderate (if the enhancement
of the lesion was stronger than that of back muscles) or minimal. The outer
margin of the lesions was recorded as lobulated or smooth. The presence or
absence of normal overlying mucosa, perigastric or omental fat infiltration,
calcification or low density within the gastric masses, and ulcers within the
lesions was recorded. The ulcer was rated as shallow (<5 mm in depth) or
deep (
5 mm). Lymphadenopathy was considered to be present if the
short-axis diameter of the largest lymph node measured 10 mm or more.
The data on the questionnaires filled out by the reviewers were collected, and statistical analyses were performed using a commercially available software (SPSS for Windows; SPSS, Chicago, IL). The Mann-Whitney test and the Student's two-tailed t test were used to test for significant differences, with a threshold p value of 0.05.
Twenty-two patients had undergone surgical resection: gross pathologic specimens were available for 14 of these patients (high-grade lymphoma group [n = 5] and low-grade lymphoma group [n = 9]). One experienced pathologist reviewed the pathologic specimens for the extent of the lesions. The depth of invasion and involvement of lymph nodes were also determined at histopathologic examination in all 22 patients who had undergone gastrectomy. Although detailed histopathologic mapping of the whole resected specimen was not performed, the pathologist tried to evaluate the pathologic features of all visible lesions. The pathologist reviewed the histologic diagnoses including immunohistochemical and molecular studies of materials in the study.
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We used records of clinical, surgical, and histopathologic examinations to apply the Ann Arbor staging scheme [9] in all 58 patients. Of the 21 patients with high-grade MALT lymphoma, eight patients had stage IE, nine had stage IIE, one had stage IIIE, and three had stage IV. Of the 37 patients with low-grade MALT lymphoma, 30 patients had stage IE, and seven had stage IIE.
Two of the 21 patients with high-grade MALT lymphoma were lost from follow-up after endoscopy. Eleven patients underwent chemotherapy with (n = 3) or without (n = 8) radiation therapy. Eight patients underwent curative surgical resection without preoperative chemotherapy. Six of these eight patients received adjunctive chemotherapy with (n = 2) or without (n = 4) radiation therapy.
Of 37 patients with low-grade MALT lymphoma, 23 received antibiotics for eradication of H. pylori. Complete remission was obtained in 21 patients and partial remission, in two. The two patients with partial remission underwent surgical resection. Eleven of 14 patients who did not receive antibiotic therapy underwent curative surgical resection. The remaining three patients received chemotherapy with (n = 1) or without (n = 2) radiation therapy.
CT Findings
All 21 patients with high-grade MALT lymphoma showed abnormality in the
gastric wall on CT. Of these patients, nine had lesions in both the antrum and
body of the gastric wall, seven had lesions only in the body, four had lesions
only in the antrum, and one had lesions in the body and fundus. Thus, 17
patients (81%) had involvement of the gastric body. Nineteen (51%) of the 37
patients with low-grade MALT lymphoma showed abnormal gastric wall thickening
on CT. Of these patients, nine had lesions in the body of the gastric wall,
seven had lesions in the antrum, and the remaining three had lesions in the
antrum and body. Thus, 12 patients (63%) had involvement of the gastric
body.
The findings observed on CT are summarized in Table 1. Abnormalities in 58 patients with gastric MALT lymphoma included diffuse or segmental gastric wall thickening (n = 38; 66%), lymphadenopathy (n = 23; 40%), ulcer (n = 13; 22%), and gastric mass (n = 2; 3%).
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In the high-grade MALT lymphoma group, diffuse gastric wall thickening (Fig. 1A,1B) was observed in 10 patients (48%) and segmental thickening (Fig. 2) in nine patients (43%). Mass formation (focal wall thickening) (Fig. 3) was found in the remaining two patients in the high-grade lymphoma group. All patients with high-grade MALT lymphoma had either gastric wall thickening or mass formation. In the low-grade MALT lymphoma group, segmental gastric wall thickening was observed in 16 patients (43%) and diffuse thickening in three patients (8%). In the remaining 18 patients (49%), the thickness of the gastric wall had a normal appearance (Fig. 4A,4B).
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Regarding the degree of lesion thickness in high-grade lymphoma group, we observed severe thickening in three patients (14%), moderate gastric wall thickening (Fig. 1A,1B) in 12 patients (57%), and mild thickening (Fig. 2) in six patients (29%). In the low-grade lymphoma group, we observed moderate thickening in five patients (14%) and mild gastric wall thickening in 14 patients (38%). Severe thickening was not found in any of the patients with low-grade histology. The thickness of gastric wall in patients with high-grade histology ranged from 7 to 40 mm (mean, 14.1 mm) and in patients with low-grade histology, from 2 to 18 mm (mean, 5.8 mm). Applying the statistical analysis, we found that the extent and thickness of the lesions in patients with high-grade histology were significantly wider and thicker than those in patients with low-grade histology (all patients, p < 0.001, Mann-Whitney test and Student's two-tailed t test).
The findings of moderate enhancement (Figs. 2 and 3), lobulated outer margin, and lack of normal mucosa overlying the lesions (Fig. 5) were more frequently observed in patients in the high-grade group than in patients in the low-grade group. However, these findings were not statistically significant (Table 1). The ulcers within the lesions were deep (n = 3) or shallow (n = 9) in the high-grade group (Fig. 5). An shallow ulcer within a lesion was revealed in one patient (5%) with low-grade histology (Fig. 6A,6B).
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Lymph nodes with a short-axis diameter of 1 mm or larger were observed at perigastric (n = 21 nodes), portocaval (n = 9), paraaortic (n = 6), and omental (n = 3) areas in 14 patients (67%) with high-grade histology (Fig. 7) and in nine patients (24%) with low-grade histology. Ulcer and lymphadenopathy in the high-grade group were more frequent than in the low-grade group (p < 0.001 and p = 0.002, respectively). The perigastric or omental fat infiltration was noted in two patients in the high-grade group, and low density within gastric mass was found in one patient in the same group. The calcification in the gastric mass was also found in one patient in the high-grade group. In two patients with high-grade histology, multiple small low-attenuated lesions were observed in the liver, which represented the involvement by lymphoma (Fig. 7).
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Pathologic Findings
In the pathologic specimens of 14 patients, 16 discrete abnormalities were
found. Three patients each had two discrete lesions. Ten patients each had
only one lesion. One patient had no definite focal abnormality on the gross
specimen. Nine lesions were found in the body of the gastric wall and seven,
in the antrum of the wall. These pathology results correlated well with CT
findings in 10 patients who had abnormal thickening of the gastric wall
depicted on CT. However, it was almost impossible to distinguish MALT lymphoma
from coexisting H. pylori gastritis in each of these lesions
visualized on CT. One of three ulcers in the surgical specimens from the
high-grade lymphoma group was not depicted on CT; the three small ulcers found
in surgical specimens from the low-grade lymphoma group were also not depicted
on CT.
At histopathologic examination of the nine lesions in the five specimens taken from the high-grade group, four lesions extended to subserosal adipose tissue, four lesions extended to proper muscle layer, and one lesion extended to submucosal layer. However, 10 (77%) of 13 lesions in the nine specimens from the low-grade group showed a proliferation of lymphoma cells within the submucosa. Regional lymph node dissection was performed in all patients who underwent surgical resection. Six (67%) of nine patients with high-grade histology had involvement of regional lymph nodes. In two of these six patients, lymphadenopathy was not depicted on CT. Four (31%) of 13 patients with low-grade histology had involvement of regional lymph nodes. In one of these four patients, lymphadenopathy was not visible on CT. In two patients with high-grade histology and one patient with low-grade histology, what was thought to be lymphadenopathy was seen on CT, but histologic examinations of the dissected lymph nodes revealed no evidence of involvement.
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Most patients with gastric MALT lymphomas have chronic H. pylori infection and develop MALT-linked H. pylori gastritis [5, 22]. Low-grade MALT lymphomas can regress after eradication of H. pylori [23, 24]. In our study, 81% (30/37) of patients with low-grade MALT lymphomas had histopathologic evidence of H. pylori infection. The finding is comparable to those of the previous studies [5, 22, 23].
Treatment of low-grade MALT lymphoma remains controversial. Some researchers [25, 26] have recommended radical gastrectomy, and other researchers [23, 27] have recommended medical treatments such as eradication of H. pylori or chemotherapy. However, as in the treatment of high-grade MALT lymphoma, radical gastrectomy and adjuvant chemotherapy with or without radiation therapy were generally recommended. Physicians in our institution consider both the Ann Arbor stage and pathologic degree of MALT lymphoma as important factors in determining the treatment and follow-up strategy. In our study, 23 patients with stage IE low-grade MALT lymphoma received antibiotics for the eradication of H. pylori. However, 11 patients with low-grade MALT lymphoma underwent gastrectomy without a trial of antibiotic therapy because such treatment for low-grade MALT lymphoma at an early stage had not been widely accepted.
In our study, patients with gastric MALT lymphoma showed nonspecific findings such as a thickened gastric wall with or without lymphadenopathy present, but we found statistically significant differences in the thickness and extent of involvement of the gastric wall, both of which were thicker and wider in patients with high-grade histology. The most useful and informative finding probably was that all patients without an abnormality visualized on CT had low-grade histology. We found that a clear distinction between high- and low-grade lymphomas was seen too infrequently to be generally applicable. For example, mass formation, severe wall thickening, or deep ulcer were reliable findings of high-grade lymphoma, but they were found in only 10-14% of our patients with high-grade lymphoma. CT findings of high-grade MALT lymphoma described in this study and those of non-Hodgkin's gastric lymphoma reported in some previous studies [13, 28, 29] are similar. Some CT appearances of low-grade MALT lymphoma can mimic those of H. pylori gastritis or the early stage of gastric cancer [5, 9, 12, 30].
On the basis of the results of our study, we believe that CT findings may suggest the histologic grade of gastric MALT lymphoma. Differentiation between high- and low-grade lymphomas from the time of the first diagnosis is fundamental to the correct treatment of the patients. According to the findings of a pathology study [31], 35% (13/37) of the patients with low-grade MALT lymphoma had from one to a few foci of high-grade B-cell lymphoma. In another report [24], four of five patients who had no change after the H. pylori infection had been cured and who then were treated surgically had high-grade B-cell lymphoma found at histologic examination of the resected stomach. Kessar et al. [12] suggested that the possibility of the lymphoma having been transformed into a high-grade form be considered if the lesion observed on follow-up CT appears to be more than mild gastric wall thickening.
According to a recent radiography study with pathologic correlation, the common findings of low-grade MALT lymphoma at upper gastrointestinal examination were mucosal nodularity, ulcer, and rugal thickening [32]. In a pathology study of [8] MALT lymphoma and early gastric lymphoma, a superficial, spreading lesion was a common finding. Considering the superficial, spreading nature of low-grade MALT lymphoma, the mild wall thickening frequently noted on CT in our study could represent infiltration of MALT lymphoma. When CT findings were correlated with features of pathologic examination, high-grade MALT lymphoma with deep invasion (to proper muscle or beyond) showed thicker involvement of the gastric wall. Hoshida et al. [25] suggested that the higher the grade of MALT lymphoma, the larger the tumor.
In conclusion, the common CT findings of gastric MALT lymphoma were gastric wall thickening and lymphadenopathy. Although CT findings of the two forms of the disease overlap, the visualization of diffuse gastric wall thickening of severe or moderate degree, mass formation, ulcer, and lymphadenopathy may help one to differentiate high-grade from low-grade gastric MALT lymphomas. The absence of abnormality on CT is highly predictive of low-grade MALT lymphoma.
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