Currently, much effort is put into the development of specific therapeutical approaches that are tailored to specific lymphoma entities. As a consequence, more specific information needs to be collected to support the choice of therapy. In gastric marginal zone B cell lymphoma of MALT-type, the need for specialised documentation of tumour extent in the organ wall has been stressed by the high predictive value for failure of response after Helicobacter pylori eradication of infiltration beyond the mucosa, a predictive parameter irrespective of the presence of the t(11;18) translocation.1–5 With new techniques such as endosonography, this infiltration depth can be assessed with improving accuracy. However, the information cannot be translated into the current staging systems. The dissemination patterns of extranodal lymphomas are also essentially different from primary nodal lymphomas.6 As tumour stage is one of the most important guidelines in the choice of local therapy (surgery, radiotherapy) and chemotherapy, adequate documentation of tumour localisation in the organ related lymph nodes and beyond is essential.
The Ann Arbor staging system, developed for and routinely used in nodal non-Hodgkin’s lymphoma, is not optimal for documentation of the specific relevant features of primary extranodal lymphoma in the gastrointestinal tract. Several modifications and alternatives have been proposed. However, neither differentiation of stage I1 (confinement of lymphoma to the mucosa and submucosa) from stage I2 (tumour extension beyond the submucosa according to Radaszkiewicz and colleagues7) nor discrimination of stage II1 (involvement of regional lymph nodes) from stage II2 (node involvement beyond the regional area, as assessed in the Musshoff modification8) is sufficiently serving the demand for documenting all features of lymphoma. To meet these shortcomings, the Lugano classification was constructed by Rohatiner and colleagues9 introducing stage IIE for “serosa penetration” without lymph node involvement into the Ann Arbor system. This represents a change in meaning of stage II that originally indicated lymph node involvement. Therefore, the Lugano system is causing more confusion than benefit.
TNM staging for tumours of epithelial origin has also been proposed as an alternative in gastrointestinal lymphoma to describe localised disease. The “T” part of this system pertains to the anatomical structure of the organs and sufficiently fulfills the requirements for staging of local extent of the disease.
The European Gastro-Intestinal Lymphoma Study Group (EGILS) is a multidisciplinary group of investigators, including clinical investigators such as gastroenterologists, medical oncologists, radiotherapists, and pathologists, as well as basic researchers such as cellular and molecular biologists. Several groups from the UK, France, Germany, the Netherlands, Spain, and Austria now take part and have come together regularly since 1999 to discuss and study subjects in epidemiology and molecular and cell biology of gastrointestinal lymphoma. Clinical protocols and trials have been developed and performed as a collaborative effort. As a result of discussions on staging protocols and reporting systems over the past years, we would like to propose a modified TNM staging system, named after the first venue of the group in Paris. The staging system adequately records: (1) depth of tumour infiltration; (2) extent of nodal involvement; as well as (3) specific lymphoma spreading (table 1▶). It is adjusted to the gastrointestinal origin of the lymphoma, considering histopathological characteristics of extranodal B and T cell lymphomas. The use of this system in future studies will permit accurate comparison of the reported cohorts and should allow rapid accumulation of good data for proper stratification of patients for risk assessment and treatment options.
Table 1 .
Paris staging system for primary gastrointestinal lymphomas*†
| TX | Lymphoma extent not specified |
| TO | No evidence of lymphoma |
| T1 | Lymphoma confined to the mucosa/submucosa |
| T1m | Lymphoma confined to mucosa |
| T1sm | Lymphoma confined to submucosa |
| T2 | Lymphoma infiltrates muscularis propria or subserosa |
| T3 | Lymphoma penetrates serosa (visceral peritoneum) without invasion of adjacent structures |
| T4 | Lymphoma invades adjacent structures or organs |
| NX | Involvement of lymph nodes not assessed |
| NO | No evidence of lymph node involvement |
| N1‡ | Involvement of regional lymph nodes |
| N2 | Involvement of intra-abdominal lymph nodes beyond the regional area |
| N3 | Spread to extra-abdominal lymph nodes |
| MX | Dissemination of lymphoma not assessed |
| MO | No evidence of extranodal dissemination |
| M1 | Non-continuous involvement of separate site in gastrointestinal tract (eg, stomach and rectum) |
| M2 | Non-continuous involvement of other tissues (eg, peritoneum, pleura) or organs (eg, tonsils, parotid gland, ocular adnexa, lung, liver, spleen, kidney, breast etc.) |
| BX | Involvement of bone marrow not assessed |
| B0 | No evidence of bone marrow involvement |
| B1 | Lymphomatous infiltration of bone marrow |
| TNM | Clinical staging: status of tumour, node, metastasis, bone marrow |
| pTNMB | Histopathological staging: status of tumor, node, metastasis, bone marrow |
| pN | The histological examination will ordinarily include 6 or more lymph nodes |
*Valid for lymphomas originating from the gastro-oesophageal junction to the anus (as defined by identical histomorphological structure).
†In case of more than one visible lesion synchronously originating in the gastrointestinal tract, give the characteristics of the more advanced lesion.
‡Anatomical designation of lymph nodes as “regional” according to site: (a) stomach: perigastric nodes and those located along the ramifications of the coeliac artery (that is, left gastric artery, common hepatic artery, splenic artery) in accordance with compartments I and II of the Japanese Research Society for Gastric Cancer (1995); (b) duodenum: pancreaticoduodenal, pyloric, hepatic, and superior mesenteric nodes; (c) jejunum/ileum: mesenteric nodes and, for the terminal ileum only, the ileocolic as well as the posterior caecal nodes; (d) colorectum: pericolic and perirectal nodes and those located along the ileocolic, right, middle, and left colic, inferior mesenteric, superior rectal, and internal iliac arteries.
References
- 1.Sackman M, Morgner A, Rudolph, B et al. Regression of gastric MALT lymphoma after eradication of Helicobacter pylori is predicted by endosonographic staging. Gastroenterology 1997;113:1087–90. [DOI] [PubMed] [Google Scholar]
- 2.Steinbach G, Ford R, Glober G, et al. Antibiotic treatment of gastric lymphoma of mucosa-associated lymphoid tissue. an uncontrolled trial. Ann Intern Med 1999;131:88–95. [DOI] [PubMed] [Google Scholar]
- 3.Ruskone-Fourmestraux A, Lavergne A, Aegerter PH, et al. Predictive factors for regression of gastric MALT lymphoma after anti-Helicobacter pylori treatment. Gut 2001;48:297–303. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Nakamura S, Matsumoto T, Suekane H, et al. Predictive value of endoscopic ultrasonography for regression of gastric low grade and high grade MALT lymphomas after eradication of Helicobacter pylori. Gut 2001;48:454–60 [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Liu H, Ye H, Ruskone-Fourmestraux A, et al. T(11;18) is a marker for all stage gastric MALT lymphomas that will not respond to H. pylori eradication.Gastroenterology 2002;22:1286–94, [DOI] [PubMed] [Google Scholar]
- 6.Krol AD, Herman J, Kramer MH, et al. Gastric lymphomas compared with lymph node lymphomas in a population-based registry differ in stage distribution and dissimination but not in patient survival. Cancer 1997;79:390–7. [DOI] [PubMed] [Google Scholar]
- 7.Radaszkiewicz T, Dragosics B, Bauer P. Gastrointestinal malignant lymphomas of the mucosa-associated lymphoid tissue: factors relevant to prognosis. Gastroenterology 1992;102:1628–38. [DOI] [PubMed] [Google Scholar]
- 8.Musshoff K. Klinische Stadieneinteilung der nicht-Hodgkin Lymphome (Clinical staging classification of non-Hodgkin’s lymphomas (author’s transl)). Strahlentherapie 1977;153:218–21. [PubMed] [Google Scholar]
- 9.Rohatiner A, D’Amore F, Coiffier 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. [DOI] [PubMed] [Google Scholar]