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Japanese Journal of Clinical Oncology Pages 101-106

Clinicopathological Studies on Coexisting Gastric Malignant Lymphoma and Gastric Adenocarcinoma: Report of Four Cases and Review of the Japanese Literature
Introduction
Case Reports
   Case 1
   Case 2
   Case 3
   Case 4
Review Of The Japanese Literature
Discussion
Acknowledgements
References

Clinicopathological Studies on Coexisting Gastric Malignant Lymphoma and Gastric Adenocarcinoma: Report of Four Cases and Review of the Japanese Literature

Clinicopathological Studies on Coexisting Gastric Malignant Lymphoma and Gastric Adenocarcinoma: Report of Four Cases and Review of the Japanese Literature Tetsuyoshi Ishihama1, Hitoshi Kondo1, Daizo Saito1, Hajime Yamaguchi1, Kuniaki Shirao1, Toshihiro Yokota1, Koichi Hosokawa1, Hiroyuki Ono1, Masahiro Iwabuchi1, Takushi Gotoda1, Yoshihiro Matsuno2, Narikazu Boku3, Atsushi Ohtsu3 and Shigeaki Yoshida3

1Department of Gastrointestinal Oncology, National Cancer Center Hospital, 2Pathology Division, National Cancer Center Research Institute, Tsukiji, Chuo-ku, Tokyo, and 3Department of Gastrointestinal Oncology, National Cancer Center Hospital East, Chiba, Japan

Among 121 cases of primary gastric malignant lymphoma from 1962 to 1994 at the National Cancer Center Hospital, Tokyo, we found four cases (three males and one female) of adenocarcinoma coexisting in the stomach. The incidence of gastric malignant lymphoma together with gastric adenocarcinoma was 3.3%, suggesting that patients with lymphoma may have an increased incidence of gastric adenocarcinoma. A review of the Japanese literature revealed an additional 62 patients who developed coexisting gastric malignant lymphoma and adenocarcinoma. In the total series of 66 patients whose age and sex were recorded, there were 48 males with a mean age of 63.8 years and 18 females with a mean age of 58.6 years. Most adenocarcinomas were macroscopically early (76%) and of histologically differentiated type (75%). Conversely, 71% of lymphomas were of the advanced type macroscopically. The correct preoperative diagnoses were made in only 27% (16/59) of cases, when both tumors were located independently.

Key words: gastric malignant lymphoma - gastric adenocarcinoma - coexistence

INTRODUCTION

Although many reports have been published on multiple carcinomas of the stomach, little is known about the coexistence of gastric malignant lymphoma and gastric carcinoma. We present here four cases of malignant lymphoma coexisting with gastric adenocarcinoma. We also review an additional 62 patients with a similar condition in the Japanese literature and analyze clinical and histological features of both neoplasms.

CASE REPORTS

Among 121 cases of primary gastric malignant lymphoma that were surgically resected from 1962 to 1994 at the National Cancer Center Hospital, Tokyo, four cases coexisted with gastric adenocarcinoma (Table 1). Three of these patients were male and one was female, with ages ranging from 61-77 years. Macroscopically, three of the malignant lymphomas and all of the adenocarcinomas were superficial according to the General Rules for the Gastric Cancer Study in Japan (1). Malingnant lymphoma was classified according to Working Formulation (WF) classification (2). The relationship between the site of the two neoplasms was classified as follows (3): (i) Collision tumors: two coexisting tumors that have developed at different sites and have invaded each other, especially in the border zones, during growth; (ii) Contiguous tumours: the two tumors have developed contiguously without any intermingling between the malignant components; (iii) Independent tumors: the tumors are separated macroscopically and microscopically by areas of tumor-free gastric mucosa.

Case 1

In February 1992, a 68-year-old male was referred to our hospital for evaluation of abnormal shadows revealed by upper gastrointestinal series of x-ray examinations takenat an annual health check. An endoscopic examination revealed an elevatedlesion located at the cardia and a discolored depressive lesion at the greater curvature of the lower body of the stomach (Fig. 1 (a) and (b)). The patient underwent total gastrectomy on March 2 1992, and the resected specimen revealed type I early carcinoma, 1.5 × 2.2 cm, and a superficial type malignant lymphoma 3 cm in diameter. Histopathological examination demonstrated that the former was a well differentiated adenocarcinoma with submucosal invasion (Fig. 2 (a) and (b)) and the latter was a malignant lymphoma, diffuse small cleaved cell type according to the WF classification (Fig. 3 (a) and (b)).


Figure 1. (a) An endoscopic view from above of type I early gastric carcinoma at the esophago-gastric junction. (b) A discoloured shallow depressed lesion with marked fold convergence at the greater curvature of the lower body, suggesting malignant lymphoma.


Figure 2. Histological findings of type I early gastric carcinoma in the resected specimens of Case 1. (a) Low-power view and (b) high-power view of well differentiated adenocarcinoma.


Figure 3. Histological findings of malignant lymphoma in Case 1. (a) Low- power view shows that the lymphoma cells infiltrate massively into the submucosal layer of the stomach. (b) High-power view reveals diffuse small cleaved cell type. Some lymphoma cells invade gastric glands to form the characteristic lymphoepithelial lesion.

Case 2

A 61-year-old male presented with a chief complaint of loss of appetite to our hospital on March 16th l992. Electronic endoscopy revealed a shallow reddish depressed lesion at the greater curvature of the antrum and two small ulcerative tumours with surrounding elevation in the lower body of the stomach (Fig. 4 (a) and (b)). Histologically, they were respectively a type IIc early gastic carcinoma, a poorly differentiated adenocarcinoma (Fig. 5 (a) and (b)) and a superficial malignant lymphoma, diffuse large cell type (Fig. 6 (a) and (b)). Total gastrectomy was done with D2 lymph node dissection, and none of the regional lymph nodes was swollen.


Figure 4.(a) A reddish depressed lesion at the greater curvature of the antrum. Endoscopic diagnosis was type IIc early gastric carcinoma. (b) Two small ulcerative lesions with surrounding elevation in the lower body of the stomach, which endoscopic examination suggested was malignant lymphoma.


Figure 5. Histologcal findings of the biopsy specimens from the type IIc early gastric carcinoma in Case2. (a) Low-power view of poorly differntiated adenocarcinoma. (b) Infiltration of Signet ring cells shown in high-power view.


Case 3

In January 1974, a 61-year-old female was admitted to our hospital for an operation for early gastric carcinoma. Endoscopic examination showed a shallow depressed lesion with marked converging folds at the posterior wall of the middle body and widespread discolored uneven mucosa withseveral erosions in the antrum. On pathological examination of the partially resected stomach, the depressed lesion was found to be a type IIc early poorly differentiated adenocarcinoma, measuring 1.5 × 1 cm, and the discolored area was a coexisting gastric malignant lymphoma of diffuse lymphocytic cell type. The patient was progressing favorably in out-patient clinics, but died of gastric stump cancer in 1985.

Case 4

A 77-year-old male was referred to our hospital for treatment of gastric malignant lymphoma in July 1994. An endoscopic examination showed a Bormann 2-like lesion and a small elevated lesion independently located in the middle body of the stomach. Histological examination of biopsy specimens revealed the former as malignant lymphoma, diffuse large cell type, and the latter as a well differentiated adenocarcinoma. Considering his great age, total gastrectomy was inadvisable and 10 courses of VEPA chemotherapy (vincristin, endoxan, predonine, adriamicin) were given, followed by an endoscopic mucosectomy for the type IIa early gastric cancer. Thegastric lymphoma responded completely to chemotherapy, and the intramucosal cancerous lesion was resected succesfully.

Since gastric carcinoma and gastric lymphoma have been linked to infection with Helicobacter pylori (H. pylori),serological tests for H. pylori infection were done and revealed that our four cases wereallpositive.

REVIEW OF THE JAPANESE LITERATURE

Since the first description of synchronous coexisting gastric carcinoma and malignant lymphomaby Azeyanagi et al. (4),62 cases have thus far been reportedin the Japanese literature. Thus, including our four cases, we reviewed the clinicopathological features of 66 cases. The subjects consisted of 48 males with a mean age of 63.8 years (range 24-81), and 18 females with a mean age of 58.6 (28-81). Patients, of either sex, were most often in their sixth decade, and the male:female ratio was 2.7:1.

Clinical details are summarized in Table 2 and Table 3. When the macroscopic appearances of the gastric malignant lymphomas (62 cases) were classified into five types according to the General Rules for the Gastric Cancer Study in Japan, 71% (44/62) were of advanced type. Twenty of these were of the protruded type, six of the ulcerative type, 13 of the excavative type and five of the giant fold type. However, 76% (44/58) of the adenocarcinomas were macroscopically of the early type. There was no specific distribution in the location of either lymphomas or adenocarcinomas.

Although, due to the application of a variety of classification systems, we could not determine in detail the histological types of the malignant lymphomas, most cases were of the diffuse type according to the Working Formulation classification. Seventy-five per cent of adenocarcinomas associated with lymphomas were of histologically differentiated type (papillary, 12%; well, 33% and moderately, 30%).

The relative locations of lymphoma and carcinoma were investigated in 63 cases. Nineteen cases (30%) showed collision tumors, five cases (8%) showed contiguous tumors and 39 cases (62%) showed independent tumors. A correct preoperative diagnosis was obtained in only 27% of cases, in which the tumors were located independently.

DISCUSSION

A primary gastrointestinal lymphoma is one that involves only the bowel at presentation or one in which the primary presenting systems are gastrointestinal. The stomach is the most common site of lymphoma, and yet gastric lymphoma comprises only 1% of all gastric malignancies (5). Few reports have been published regarding the simultaneous presence of gastric carcinoma and gastric malignant lymphoma (6-8).


Figure 6. Histological findings of biopsy specimens from the malingant lymphoma in Case2. (a) Medium-power view shows diffuse infiltration of the lymphoma cells in the submucosal layer. (b) Most of the tumor cells were large, of high nuclear:cytoplasmic ratio and classified as diffuse large cell type.

Table 1. Clinicopathological data of four patients with gastric malignant lymphoma coexisting with gastric adenocarcinoma in NCCH
      Malignant Lymphoma Adenocarcinoma  
Case

 Age

 Sex

 Macroscopic type Histology

 Location

 Macroscopic type Histology

 Depth

 Location

 Relationship
1

 68

 Male

 Superficial

 D, small cleaved M

 I

 Poor

 sm

 C

 Independent
2 61 Male Superficial D, large M IIc Well m A Independent
3

 61

 Female

 Superficial

 D, lymphocytic A

 IIc

 Poor

 m

 M

 Independent
4 62 Male Advanced D, large M IIa Well m M Independent
Both tumors were classified according to the General Rules for the Gastric Cancer Study in Japan and the Working Formulation classification. D, diffuse; C, upper third of the stomach; M, middle third of the stomach; A, lower third of the stomach; m, mucosal invasion; sm, submucosal invasion; Well, well differentiated adenocarcinoma; Poor, poorly differentiated adenocarcinoma

Table 2. Clinicopathological features of gastric malignant lymphoma coexisting with gastric adenocarcinoma
Malignant Lymphoma
Type No. of cases (%)
Macroscopic type
Total 62  
Superficial 18 (29%)
Protruded 20 (32%)
Ulcerative 6 (10%)
Excavated 13 (21%)
Giant fold 5 (8%)
Histological type
Total 38  
Diffuse large 20 (54%)
Diffuse small cleaved 7 (18%)
Diffuse lymphocytic 2 (5%)
Diffuse mixed 5 (13%)
Follicular small cleaved 4 (11%)
Location
Total 62  
C 12 (19%)
M 24 (39%)
A 15 (24%)
Multiple
areas		 11

 (18%)
Lymphomas were classified according to Working Formaulation classification and the General Rules for the Gastric Cancer Study in Japan. C, upper third of the stomach; M, middle third of the stomach; A, lower third of the stomach

In this paper, we summarize their coexistence in our hospital and review 62 similar cases in the Japanese literature from 1962 to 1994. The incidence of gastric carcinoma was 3.3% in patients with gastric lymphoma in the National Cancer Center Hospital, a much higher figure than for the Japanese population in general (about 0.05%).

The precise mechanism of the coexistence of these neoplasms is unclear. However, H. pylori,a gram-negative bacterium, is thought to contribute to the development of both carcinoma and lymphoma. There have been many reports that H. pylori infection, which is thought to be causallyrelated to chronic gastritis, may also be associated with an increased risk of gastric carcinoma (9-13). Tatsuta et al. demonstrated that H. pylori infection was closely associated with differentiated type gastric carcinoma (14). Recently, several authors have stronglysuggested that H. pylori infection may play an important role inthe pathogenesis of gastric lymphoma (17-20). In the present review study, therate of H. pylori infection was unclear except in our 4 positive cases.However, a high incidence of differentiated type gastric carcinoma associated with lymphoma might be due to H. pylori infection.

Table 3. Clinicopathological features of gastric adenocarcinoma coexisting with gastric malignant lymphoma
Adenocarcinoma
Type No. of cases (%)
Macroscopic
Total 58  
Early carcinoma 44 (76%)
I 3 (5%)
IIa 3 (5%)
IIb 3 (5%)
IIc 25 (43%)
Others 10 (17%)
Advanced carcinoma 14 (24%)
B-1 2 (3%)
B-2 6 (9%)
B-3 1 (2%)
B-4 2 (3%)
others 3 (5%)
Histological 43  
Total    
Pap 5 (12%)
Well 14 (32%)
Mod 13 (30%)
Poor 5 (12%)
Sig 6 (14%)
Location 63  
Total    
C 9 (14%)
M 25 (40%)
A 25 (40%)
Multiple areas 4 (6%)
Gastric carcinomas were classified according to the General Rules for the Gastric Cancer Study in Japan. Pap, papillary; Sig, signet ring cell; Well, well differentiated; Mod, moderately differentiated; Poor, poorly differentiated adenocarcinoma; C, upper third; M, middle third; A, lower third of the stomach

However, in a review of 7130 consecutive cases of resected gastric adenocarcinoma over 32 years in our hospital, the coexistence of gastric malignant lymphoma was detected in only four cases (0.06%). This is consistent with a report by Noda et al. (21), showing that the incidence of adenocarcinoma of the stomach which has coexisting primary malignant lymphoma is only 0.08% (2 of 2438 cases). Whilst in the authors' experience gastric lymphoma seems to carry an increased risk of gastric carcinoma, the converse seems not to hold, suggesting that factors other than H. pylori affect the tumorigenesis in both of these tumors. It is generally known that immunologically compromised patients, such as those with lymphoma, have a tendency for occurrence of secondary neoplasms. In our review of the simultaneous presence of lymphoma and adenocarcinoma of the stomach, most of the lymphomas were of advanced type (71%) and most carcinomas were of early type (76%). We do not know, of course, how fast each neoplasm grows, but it is likely that malignant lymphoma preceeded adenocarcinoma and that the lymphoma-associated immunosupressive state may be a key to the subsequent development of gastric carcinoma.

Because preoperative differential diagnosis between gastric carcinoma and lymphoma isextremely difficult because of their resemblance in macroscopic appearance (22,23), pathological information is indispensable. However, the accuracy of endoscopic biopsies from gastric lymphoma are notsatisfactory, ranging from 52% to 88% (24). Sampling may be problematic where there is a considerable reactive lymphoid infiltration adjoining the lymphoma. Errors may also occur in distinguishing lymphoma from poorly differentiated carcinoma. These could explain the low rate of correct diagnosis for the presence of both tumors. However, there is no way to improve diagnostic accuracy except by careful endoscopy and scrupulous biopsy examination.

From the point of view of clinical management, it is also important when considering a patient with gastric lymphoma not to overlook coexistent gastric carcinoma. In Western countries, total gastrectomy is inadvisable ordinarily because of its greater risk to the patients and because any residual tumor responds well to chemotherapy. In this situation, coexisting adenocarcinoma must be diagnosed correctly and resected surgically, since chemotherapy is not effective for carcinoma. The 5-year survival rate in patients with lymphoma is undoubtedly better than the 5-year survival rate for patients with gastric carcinoma in Western countries. Therefore, specific indication of surgery should be considered for coexisting gastric carcinoma, although operation is usually avoided in a patient with generalized diseases of gastric lymphoma.

In Japan, on the contrary, diagnosis of coexisting gastric carcinoma has less meaning for a patient with gastric lymphoma, since total gastrectomy is routinely performed. However, thinking of options of treatment for gastric lymphoma such as surgery, chemotherapy and radiation, preoperative diagnosis for the presence of both neoplasms would be of importance.

ACKNOWLEDGEMENTS

This work was supported in part by Grants-in-Aid for Cancer Research and for the 2nd Term Comprehensive 10-year Strategy for Cancer Control from the Ministry of Health and Welfare of Japan.

References

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Received July 12, 1996; accepted October 30, 1996
For reprints and all correspondence: Hitoshi Kondo, Department of Gastrointestinal Oncology, National Cancer Center Hospital, 5-1-1 Tsukiji, Chuo-ku, Tokyo 104, Japan

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