• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information

NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.

Holzheimer RG, Mannick JA, editors. Surgical Treatment: Evidence-Based and Problem-Oriented. Munich: Zuckschwerdt; 2001.

Cover of Surgical Treatment

Surgical Treatment: Evidence-Based and Problem-Oriented.

Show details

Primary gastric lymphoma

and .

Author Information

1 and 2.

1 Clinica Chirurgica II, Università degli Studi “La Sapienza”, Policlinico Umberto I°, Rome, Italy
2 Department of Surgery - MISC, National University of Singapore, Singapore

The stomach is the site most commonly involved by extranodal lymphomas, and in 15–20% of diffuse non-Hodgkin`s lymphomas involvement of the stomach has been described. Recently, in patients with gastric tumors an increasing incidence of lymphomas has been described, seemingly not related only to the decreasing incidence of gastric adenocarcinoma or to the improvement of diagnostic procedures. According to Dawson gastric lymphomas are considered as primary when predominantly the stomach is involved, and the intra-abdominal lymphadenopathy, if present, corresponds to the expected lymphatic drainage of the stomach. In recent years, Isaacson and Spencer (8) introduced the concept of mucosa-associated lymphoid tissue (MALT) and MALT-type lymphomas which has been adopted and incorporated into a new classification scheme, the Revised European-American Lymphomas (REAL) classification. MALT lymphomas have been demonstrated to be closely associated with Helicobacter pylori (HP) infection. Its symptoms are mostly upper GI tract symptoms and resemble gastritis up to peptic ulcer syndrome. The most frequent findings were epigastric or diffuse abdominal pain, weight loss, vomiting, bleeding, dysphagia, perforation. For diagnosis, imaging techniques as angio CT-scan, spiral-CT or MRI are mandatory to show the gastric lesions and the extent of the disease. Management of gastric lymphoma is still being discussed and as yet the value of different treatment modalities is not well defined. Results of the literature support both chemo- or radiotherapy, and surgery. We conclude that patients must be staged by non-invasive techniques; for stages I and II until now surgery represents the most rational approach to the management of primary gastric lymphoma, either for curative resection or for correct staging, although different studies could show that chemotherapy and radiotherapy seem to have the same survival rate as surgery. Surgery is indicated to treat complications; it must be conservative and is not indicated in stages III or IV; chemotherapy and/or radio-chemotherapy are indicated as adjuvant therapy not only to manage, but also to prevent relapses in patients with a high risk of recurrence and negative prognostic factors.

Introduction

Non-Hodgkin's lymphoma (NHL) occurs more often than Hodgkin's disease and may be of the nodal or extranodal type. 25% of the non-Hodgkin's lymphomas in North America and about 50% in Europe and the Far East are primary extranodal NHL. The stomach most commonly involved by extra-nodal lymphomas, and in 15–20% of diffuse non-Hodgkin's lymphomas involvement of the stomach has been described (1). Nevertheless, primary gastric lymphoma is uncommon, accounting for only 2–8% of all gastric malignancies in Western countries (25). Some recent studies, however, report that the incidence of primary gastric lymphoma is increasing over the last two decades (3).

Recently, however, an increasing incidence of lymphoma has been described in patients with gastric tumors, which does not seem to be related only to the decreasing incidence of gastric adenocarcinoma or to the improvement of diagnostic procedures (4). The reasons of this trend are not clear and further epidemiologic studies are necessary .

According to Dawson (6) gastric lymphomas are considered as primary when predominantly the stomach is involved, and the intra-abdominal lymphadenopathy, if present, corresponds to the expected lymphatic drainage of the stomach. This definition excludes patients with palpable subcutaneous lymph nodes, mediastinal lymphadenopathy and bone marrow, liver or spleen involvement. In 1994 the Danish Lymphoma Study Group, defined all patients with more than 75% of the volume of the stomach involved as primary gastric lymphoma (7).

Pathology

Macroscopic features

In gastric lymphomas the primary lesion is in the submucosa, originating from the lymphoid tissue of the lamina propria (polypoidal masses or small mucosal ulcerations). In 30% of the cases the lesions are larger than 10 cm. Usually the serosa is invaded first followed by the mucosa. Regional lymph node metastasis (63%) precedes the involvement of distant organs. In 5–23% of all cases the entire stomach is affected or a multifocal localization is present; the distal portion of the stomach (excluding the pylorus) is the most frequent site of the tumor. Rarely the disease is a diffuse infiltrative process like a “linitis plastica”. Adjacent organs are infiltrated between 7 and 30%; pancreas, omentum and spleen are more frequently involved while the colon is only occasionally affected.

Microscopic features

This B-cell lymphoma is the characterized by the presence of lymphoepithelial lesions with lymphoid follicles and plasmacellular infiltration. The cells resemble centrocytes with small, dense, granular nuclei with clear cytoplasm and irregular borders. Chronic inflammation and immunostimulation (Helicobacter pylori?) could precede the polyclonal lymphocyte proliferation until one clone acquires malignant properties, and lymphoma develops. Histologically gastric lymphomas are divided into four groups (table I).

Table I. Classification by histologic type.

Table I

Classification by histologic type.

Histological classification

Histological classification of lymphoid neoplasms has been frustrating for both clinicians and pathologists. Since 1970 different and divergent classifications have been proposed. Originally, gastric lymphomas were classified according to criteria developed for nodal-based lymphomas. In recent years the concept of mucosa-associated lymphoid tissue (MALT) and MALT-type lymphomas introduced by Isaacson and Spencer (8) has been adopted and incorporated into a new classification scheme, the Revised European-American Lymphomas (REAL) classification. This classification contains the entity of extranodal marginal zone-B cell lymphoma (low-grade B-cell lymphoma of MALT-type). Transformation to a large cell lymphoma is recognized in this new classification scheme. Low-grade gastric B-cell lymphomas of MALT-type have been well characterized clinically, histologically and immunophenotypically. Transformation to the high-grade (large cell) lymphomas has been described; however, the criteria for distinguishing high-grade MALT-type lymphomas from other large cell lymphomas have not been widely addressed. Previous studies of patients with primary gastrointestinal and gastric lymphoma yielded conflicting results regarding the clinical significance of histologic type and clinical stage. Some studies have emphasized the importance of the clinical stage rather than the histologic type for the prognosis and clinical outcome, while other studies found histological grade to be significant; however, many of these studies were done before the low and high-grade gastric MALT-lymphomas classification was developed.

Histological lesions and Helicobacter pylori

MALT lymphomas have been demonstrated to be closely associated with Helicobacter pylori (HP) infection. The influence of HP was first postulated by Wotherspoon in 1991 (9). He found HP infection in 92% of patients with primary gastric lymphoma. In 1992 Hussell showed that the proliferation of low-grade B-cell primary gastric lymphoma is dependent on the activation of T-cells by Helicobacter pylori (10). But the important role of chronic HP infection was demonstrated by different studies describing the regression of low-grade MALT lymphomas one year after HP eradication in 70–90% of these tumors. Moreover, HP reinfection is mainly associated with recurrence of gastric lymphoma. For this reason a long-term follow-up is necessary.

Staging

According to the American Joint Committee on Cancer (AJCC), the TNM classification is not suitable, especially for primary gastric lymphomas. In this disease, the correct staging includes clinical, radiological and surgical parameters in order to accurately establish the stage of each patient. Following a modification of the Ann Arbor classification by Mushoff (table II), during the 5th International Conference on Malignant Lymphoma (11) a new classification was proposed and recommended in 1993 (table III).

Table II. Staging Ann Arbor Classification a.

Table II

Staging Ann Arbor Classification a.

Table III. Staging Classification (5th International Conference on Malignant Lymphoma)a.

Table III

Staging Classification (5th International Conference on Malignant Lymphoma)a.

Clinical signs and diagnosis

The disease is most common in the sixth decade, men are affected more often than women, and Caucasians more than individuals of Afro-American origin. Most patients show symptoms of the upper GI tract resembling gastritis up to peptic ulcer syndrome. Only a small number of patients in the series were asymptomatic (3%) while the most frequently occurring symptoms were epigastric or diffuse abdominal pain (60–95%), weight loss of more than 2 kg (15–40%), nausea (12–14%), vomiting (14–32%), bleeding (8–30%), dysphagia (4–9%), anorexia (6–10%), perforation (3%) and lymphadenopathy (10–15%). Many patients reported vague and non-specific symptoms four to ten months prior to diagnosis. Preoperative diagnosis of lymphoma is very important because it permits a correct preoperative work up of the patients to establish the correct stage in order to plan therapy. Preoperative blood chemistry, chest X-ray and bone marrow aspiration are fundamental to exclude metastatic disease. In 75% of cases, the barium meal shows a malignant gastric lesion with the most common finding of enlarged gastric folds. Subsequently, endoscopy demonstrates a diffuse infiltrative process with thick, rigid folds, ulcerative lesions or a polypoid mass. Due to the submucosal origin, bioptic diagnosis is difficult to establish but now, with the improvement of histologic and endoscopic technique (deep and multiple biopsies, cytology), diagnoses have become more accurate (85–90%). Imaging techniques as angio CT-scan, spiral-CT or MRI are mandatory to show the gastric lesion and the extent of the disease; but they can not reliably distinguish reactive from metastatic lymph nodes. The advent of endoscopic ultrasonography remarkably improved the local staging of the disease as the depth of invasion, and the presence of perigastric lymphadenopathy. Studies report that sensitivity and specificity are 89% and 97%, respectively, while accuracy for depth of invasion and perigastric nodes was 92% and 77%. Moreover, by echogenic patterns it is possible to distinguish gastric lymphoma from other tumors.

Prognostic factors

To date, many aspects of primary gastric lymphoma need to be stated: preoperative diagnosis is improving and this is very important not only for staging but also to plan a correct therapy. In fact, the prognosis is better than for other gastric tumors (12), because primary gastric lymphoma tends to remain localized for a long time. This has been attributed to its homing phenomenon in which the MALT lymphoma cells return to the original mucosal site rather than disseminate elsewhere.

Stage of the disease and grade of the lesion are the most important prognostic factors. In fact, depth of the invasion of the wall and size of the tumor measured at the intervention are important survival factors, as reported in previous studies (1) (80.8% of five-year survival for tumors smaller than 5 cm vs. 44.4% for larger lesions, p < 0.05). Moreover, histologic type of the tumor and the stage of the illness confirm that Ann Arbor Classification with Musshoff's modified criteria is the most reliable system (13); in fact the involvement of non-contiguous regional lymph nodes significantly influences prognosis. In many studies, the five-year survival rate decreases from 68.6% in stage II 1E to 44.4% in stage II 2E. Even greater is the difference in disease-free survival falling from 57.1% in stage II 1E to 16.7% in stage II 2E, showing an important decrease (p < 0.2). The five-year survival rate for low-grade and high-grade tumors was 91% and 56%, respectively. Depth of invasion and serosal penetration are other negative prognostic factors, as the five-year survival rate decreases for the stages T1 to T3 from 82% to 24%. Other negative survival factors described in the literature are old age, T-cell lymphoma, nodular type, lesions with a higher cell proliferation index measured by monoclonal antibody Ki67 or MIB1, and aneuploid lymphoma.

Therapeutic modalities

Management of gastric lymphoma is still being discussed and as yet the value of the respective treatment modalities is not well defined. Actually, results from the literature support both, chemo- or radiotherapy, and surgery (1, 4, 1419). The role of each modality in the treatment of primary gastric lymphoma is not well defined due to the infrequency of the disease and the small number of cases for each single study. Staging and histological classification are not uniformly referred to and several types and different grades of the disease exist. For these reasons it is difficult to conduct prospective controlled, randomized studies.

Surgery

In the past surgical excision of gastric lymphomas has been the treatment of choice. Several studies report the superior outcome of surgery, especially in the early stages (2022, 24). As observed also by Rackner (17) and others (22), in our opinion surgery plays an important role in the management of gastric lymphoma for the following reasons: 1. removing the lesion relieves symptoms and improves survival; 2. surgery allows not only a correct histological diagnosis but also the accurate staging of the disease; 3. it prevents severe complications such as bleeding or perforation. In the literature, incidence of these complications range from 0 and 25%; however, we emphasize, that independently of the real incidence the prognosis of these complications is very poor with an almost 100% mortality (1, 17). At the present time, there is no evidence suggesting that surgery can be avoided; when the disease has not spread (no unresectable para-aortic nodes, liver involvement, free nodules in the abdomen) or when there are no general contraindications to surgery, surgical resection of the tumor is the most rational approach to the management of gastric lymphoma. A review of our experience and of the literature shows that there are no differences of survival between total and partial gastrectomy. In all cases examined in our report, the gastric lesion was isolated; furthermore, positivity of surgical margins of resection does not seem to influence survival or recurrence rates in patients treated with adjuvant therapy (17). Positive microscopic margins can be controlled later with adjuvant therapy. A French prospective, randomized, multicentric study confirms that the incomplete resection status did not influence survival, relapse, or disease-free survival because all patients received adjuvant chemotherapy (25). For these reasons we think that, whenever possible, subtotal gastrectomy is preferable to total gastrectomy or more radical operations considering morbidity and the better quality of life. Also accurate lymphadenectomy of contiguous or regional nodes plays an important role both for curative resection and for correct staging. Recent reports have also suggested liver biopsies during surgery. Splenectomy does not seem to be mandatory, since in 84% of cases surgical resection of the tumor was ”curative” and standard lymphadenectomy (R > N+) was accurate in all patients.

Stages I and II are usually amenable for curative resection whereas, regardless of stage, the resection rate in all patients ranges from 52% to 76%. The main criterion for considering a tumor as not resectable is metastatic disease.

Adjuvant therapy

Because of their origin from lymphatic tissue of the gastric mucosa and submucosa, gastric lymphomas are highly sensitive to radiotherapy and chemotherapy.

Many authors reported on multimodal treatment with surgery, chemotherapy and/or radiotherapy as adjuvant therapy, but also treatment based only on chemotherapy or radiotherapy has been described (14, 16, 17). It is very difficult to evaluate and compare the efficacy of these therapies because there are no prospective controlled studies (1517). Chemotherapy plays an important role as adjuvant therapy after surgical resection; however the selection of patients for this treatment is still matter of debate. In our experience, in accordance to other reports (12, 17, 23) adjuvant therapy should be given to all patients with stage II E, III and IV gastric lymphoma, and in cases with stages IE and II 1E with negative prognostic factors, such as histologically high-grade lymphomas or large tumors (> 5 cm) in which the incidence of subclinical metastases is high. Most authors recommend radiotherapy in residual low-grade disease and when adjacent organs are involved. Shimm et al. (24) demonstrated that radiotherapy did not affect overall survival, but in patients with negative prognostic factors, such as positive lymph nodes and/or margins or serosal involvement, survival improved from 25 to 38%. Various authors (26, 27) confirm the role of radiotherapy in stage II patients with an increase of survival rate. Analyzing the literature we can affirm that adjuvant chemotherapy is mandatory in stage I patients with positive surgical resection margins, whereas in stage II combined chemo- and radiotherapy significantly improved the survival rate especially in patients with negative prognostic factors. Recently, the most controversial issue is if chemo- and/ or radiotherapy can replace surgery as primary treatment. The criteria pro surgery are that the excision is necessary for histological classification and staging, but today we must taking into account that with the advanced endoscopic and imaging techniques it is possible to allow an acceptable staging without surgery. Moreover, some authors describe that chemoradiotherapy can lead to necrosis of the tumor with resultant gastric perforation and bleeding (3 to 25%) (17, 28), whereas in a review of 17 studies, Mittal et al. (29) found no increased risk of perforation associated with adjuvant therapy. The Danish Lymphoma Study Group (7) concludes that surgery did not significantly influence survival rates in stages I and II. At the same time, in another study of 50 patients with gastric lymphoma treated with radiotherapy, surgery or both, the five-year survival rate for radiotherapy alone or in combination with surgery was equivalent, whereas the results of patients treated by radiotherapy and radiotherapy plus surgery were better than forsurgery alone.

Controversies

Recently, since systemic chemotherapy has been the treatment of choice for most nodal and extra nodal lymphomas, some suthors suggest that also in primary gastric lymphoma, chemo and/or radiotherapy can replace surgery as primary treatment.

The surgeons advocate that prognosis of gastric MALT lymphoma depend from the staging, grading and local infiltration and the gastric resection is necessary at this purpose. But, today we must taking into account that with the advancement of endoscopic, especially with endosonography that is a very accurate method to identify the layers of the gastric wall, and imaging technique is possible to allow an accurate staging by non-invasive methods. Moreover, some authors describe that chemo-radiotherapy can lead to necrosis of the tumor with resultant gastric perforation and bleeding (3 to 25%) [17,28], while in a review of 17 studies, Mittal at al. [29] found that the risk of perforation is not increased by adjuvant therapy. The Danish Lymphoma Study group [7] concludes that surgery did not significantly influence survival rate in stage I and II. At the same time, analyzing the data of 50 patients uderwent different therapeutic modalities, the author shows that: 5-year survival rate in patients treated with radiotherapy alone or in combination with surgery was equivalent while, the results of both these group, compared with surgery alone are better.

Eradication Therapy

In 1991, Waterspoon et al. [9] described firstly a consistent association of low-grade gastric MALToma with Helicobacter Pylori (HP) infection. The data was confirmed by other histopathological studies that suggest that HP is strongly involved in the pathogenesis of the primary gastric lymphoma. HP probably causes an initial follicular gastritis together with genetic alterations, formation of autoantibody, cell-mediated epithelial damage (T-helper cells). This results in gradual compromisation of the immunological regulated process with a subsequent development of a proliferative disease. Successive in-vitro studies have showed the role of HP influencing the MALT low-grade cells modulating their growth through infection-related factors. This is observed mainly in the initial stage (IE1) of the MALToma and only an accurate morphological study can recognize patient with a simple follicular gastritis from patients with low-grade gastric lymphoma. Based on these observations, several clinical trials worldwide have shown a 60–80% success rate of HP eradication with omeprazole (40 mg three times per day for 14 days) and amoxicillin (750 mg times per day for 14 days) in patient with gastric lymphoma with a remission of the disease especially in patients with localized low grade disease (stage IE) [30, 31, 32].

The eradication of H. pylori is a promising therapeutic approach for localized low grade mucosa-associated lymphoid tissue lymphoma and cure of this infection may lead to complete remission of the MALT lymphoma as showed in several studies with different follow-up.

However, in the small proportion of patients in whom treatment failed, surgery or alternative treatment as radio or chemotherapy must be done. We conclude that in early stages of the disease HP eradication must be utilized only after an accurate histo-morphological diagnosis supported if possible by molecular studies and a staging of the disease by endoluminal ultrasonography. This suggests that randomized trials are needed to clarify wheter medical or surgical management of localized gastric lymphoma or a combination of two is the best treatment modality and such treatment strategies should be only conducted in specialized Centers.

Conclusions

Due to the numerous variables reportedin the literature, such as different staging, several histological classifications and different therapeutic options, and considering the low incidence of the disease, it has been very difficult to establish well-defined guidelines for the best therapeutic options of primary gastric lymphoma. On the basis of our experience and the review of the literature we can conclude that 1) patients must be staged by non-invasive techniques; 2) in low-grade B-cell MALT-type lymphoma with HP infection, antibiotics and careful follow-up are recommended; 3) in stages I and II, surgery represents until now the most rational approach to the management of primary gastric lymphoma, either for curative resection or for correct staging, although different studies showed that chemotherapy and radiotherapy seem to have a survival rate equivalent to surgery; 4) surgery is indicated for the treatment of complications (perforation and bleeding); 5) surgery must be conservative since residual disease can be managed by adjuvant therapy; 6) subtotal gastrectomy (with accurate lymphadenectomy), charged with lesser complications and better quality of life, is preferable to total gastrectomy; 7) surgery is not indicated in stages III or IV; 8) chemotherapy and/or radio-chemotherapy as adjuvant therapy are indicated not only to manage, but also to prevent relapses in patients with a high risk of recurrence and with negative prognostic factors (stages II2E–IV, large tumors, histologically high-grade T-lymphomas).

To better define indications for accurate staging, classification and treatment modalities prospective, randomized trials are needed.

References

1.
Schutze W P, Halpern N B. Gastric lymphoma. Surg Gynecol Obstet. (1991);172:33–38. [PubMed: 1985339]
2.
Sandler R S. Primary gastric lymphoma: a review. Am J Gastroenterol. (1984);79(1):21–25. [PubMed: 6362400]
3.
Cogliatti S B, Schmid U, Schumacher U. et al. Primary B-cell gastric lymphoma: a clinicopathological study of 145 pts. Gastroenterology. (1991);101:1159–1170. [PubMed: 1936785]
4.
Hayes J, Dunn E. Has the incidence of primary gastric lymphoma increased? Cancer. (1989);63:2073–2076. [PubMed: 2702577]
5.
Rosen C B, Van Heerden J A, Martin J K. et al. Is an aggressive surgical approach to the patient with gastric lymphoma warranted? Ann Surg. (1987);205(6):634–640. [PMC free article: PMC1493050] [PubMed: 3592805]
6.
Dawson I M P, Cornes J S, Morrison B C. Primary malignant lymphoid tumours of the intestinal tract. Br J Surg. (1961);49:80–89. [PubMed: 13884035]
7.
D'Amore F, Brincker H, Gronbaek K. et al. Non-Hodgkin's lymphoma of the gastrointestinal tract: a population-based analysis of incidence, geographic distribution, clinicopathologic presentation features, and prognosis. Danish Lymphoma Study Group. J Clin Oncol. (1994);12:1673–1684. [PubMed: 8040680]
8.
Isaacson P G, Spencer J. Malignant lymphoma of mucosa-associated lymphoid tissue. Histopathology. (1987);11:445–462. [PubMed: 3497084]
9.
Waterspoon A C, Ortiz-Hidalgo C, Falson M R. et al. Helicobacter pylori associated gastritis and primary B-cell gastric lymphoma. Lancet. (1991);338:1175–1176. [PubMed: 1682595]
10.
Hussell T, Isaacson P G, Crabtree J E. et al. The response of cells from low-grade B-cell gastric lymphomas of mucosa-associated lymphoid tissue to Helicobacter pylori. Lancet. (1993);42:571–574. [PubMed: 8102718]
11.
Rohaitner A, dÕAmore F, Coiffer B. et al. Report on a workshop convened to discuss the pathological and staging classifications of gastrointestinal tract lymphoma. Ann Oncol. (1994);5:397–400. [PubMed: 8075046]
12.
Dworkin B, Lightdale C J, Weingrad D N. et al. Primary gastric lymphoma. A review of 50 cases. Dig Dis Sci. (1982);27(11):986–992. [PubMed: 7140495]
13.
Smithers D W. Summary of papers delivered at the conference on staging in Hodgkin's disease (Ann Arbor). Cancer Res. (1971);31:1869–1870. [PubMed: 5121698]
14.
Gobbi P G, Dionigi P, Barbieri F. et al. The role of surgery in the multimodal treatment of primary gastric non-Hodgkin lymphomas. A report of 76 cases and review of the literature. Cancer. (1990);65:2528–2536. [PubMed: 2186852]
15.
Jones R E, Willis S, Innes D J. et al. Primary gastric lymphoma. Problems in staging and management. Am J Surg. (1988);155:118–123. [PubMed: 2449090]
16.
Maor M H, Maddux B, Osborne B M. et al. Stages IE and IIE non-Hodgkin's lymphomas of the stomach. Cancer. (1984);54:2330–2337. [PubMed: 6208989]
17.
Rackner V L, Thirlby R C, Ryan J A. Role of surgery in multimodalty therapy for gastrointestinal lymphoma. Am J Surg. (1991);161(5):570–575. [PubMed: 2031540]
18.
Sheridan W P, Medley G, Brodie G N. Non-Hodgkin's lymphoma of the stomach: a prospective pilot study of surgery plus chemotherapy in early and advanced disease. J Clin Oncol. (1985);3(4):495–500. [PubMed: 3981224]
19.
Weingrad D N, Decosse J L, Sherlock P. et al. Primary gastric lymphoma: a 30 year review. Cancer. (1982);49:1258–1265. [PubMed: 7059947]
20.
Lim F E, Hartman A S, Tan E G. et al. Factors in the prognosis of gastric lymphoma. Cancer. (1977);39:1715–1720. [PubMed: 322839]
21.
Paulson S, Sheehan RG, Stone MJ et al (1983) Large cell lymphomas of the stomac: improved prognosis with complete resection of all intrinsic gastrointestinal disease. J Clin Oncol: 263–269 . [PubMed: 6668500]
22.
Rossini F, Pogliani E M, Pioltelli P. et al. Surgery and chemotherapy in the treatment of gastric non-Hodgkin's lymphoma. Rec Prog Med. (1990);81(6):448–452. [PubMed: 2251455]
23.
Aozasa K, Ueda T, Kurata A. et al. Prognostic evaluate of histologic and clinical factors in 56 patients with gastrointestinal lymphomas. Cancer. (1988);61:309–315. [PubMed: 3334966]
24.
Shimm D S, Dodoretz D E, Anderson T. et al. Primary gastric lymphoma. An analysis with emphasis on prognostic factors and radiation therapy. Cancer. (1983);52:2044–2048. [PubMed: 6627215]
25.
Salles G, Herbrecht R, Tilly H. et al. Aggresive primary gastrointestinal lymphomas: review of 91 patients treated with the LNH-84 regimen. A study of the groupe d'etude des lymphomes agressifs. Am J Med. (1991);90:77–84. [PubMed: 1702581]
26.
Weingrad D N, Decosse J J, Sherlock P. et al. Primary gastrointestinal lymphoma: a 30-year review. Cancer. (1982);49:1258–1265. [PubMed: 7059947]
27.
Bozzetti F, Audisio R A, Giardini R. et al. Role of surgery in patients with primary non-Hodgkin's lymphoma of the stomach: an old problem revisited. Br J Surg. (1993);80:1101–1106. [PubMed: 8402104]
28.
Brooks J J, Enterline H T. Primary gastric lymphomas: a clinicopathologic study of 58 cases with long-term follow-up and literature review. Cancer. (1983);51:701–711. [PubMed: 6336982]
29.
Mittal B, Wasserman T H, Griffith R C. Non-Hodgkin's lymphoma of the stomach. Am J Gastroenterol. (1983);78:780–787. [PubMed: 6650467]
Copyright © 2001, W. Zuckschwerdt Verlag GmbH.
Bookshelf ID: NBK6966
PubReader format: click here to try

Views

  • PubReader
  • Print View
  • Cite this Page

Related information

  • PMC
    PubMed Central citations
  • PubMed
    Links to pubmed

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...