Indian Journal of Pathology and Microbiology

: 2011  |  Volume : 54  |  Issue : 4  |  Page : 712--719

Gastrointestinal lymphomas: Pattern of distribution and histological subtypes: 10 years experience in a tertiary centre in South India

Neeraj Arora1, Marie Therese Manipadam1, Anna Pulimood1, BS Ramakrishna2, Ashok Chacko3, Susy S Kurian1, Sheila Nair1,  
1 Department of Pathology, Christian Medical College, Vellore, Tamil Nadu, India
2 Department of Medical Gastroenterology, Christian Medical College, Vellore, Tamil Nadu, India
3 Department of Gastrointestinal Sciences, Christian Medical College, Vellore, Tamil Nadu, India

Correspondence Address:
Neeraj Arora
Department of Pathology, Christian Medical College, Vellore - 632 004, Tamil Nadu


Background and Aim: Gastrointestinal tract (GIT) is one of the major sites of extra-nodal lymphomas constituting 10-15% of all non-Hodgkin«SQ»s lymphoma cases and about 30-40% of extra-nodal lymphomas. Considerable variation exists in the literature with respect to incidence of the various histological subtypes and sites of involvement. This study was undertaken to ascertain the anatomic distribution, histological subtypes and sites of all GIT lymphomas presenting to a tertiary referral hospital in southern India. Materials and Methods: The histological material of 361 patients over a period of 10 years (2001-2010), with histopathological diagnosis of lymphoma involving the GIT (both primary and secondary), was analyzed retrospectively. All lymphomas were reclassified according to the World Health Organization 2008 classification. Results: These 361 cases include 336 primary and 25 cases of lymphomas, where the involvement was secondary. Primary lymphomas consisted of 267 males (79.64%) and 68 females (20.24%) with a male:female ratio of 3.93:1. The mean age was 45 years (range 3-88). Diffuse large B-cell lymphoma (DLBCL) was the commonest subtype (222 cases; 66.71%), followed by low-grade marginal zone lymphoma of the mucosa associated lymphoid tissue (MALT) type (34 cases; 10.12%) and Burkitt«SQ»s lymphoma (35 cases; 10.48%). The commonest site was stomach (180 cases; 53.57%), followed by small intestine (79 cases; 23.51%) and large intestine (68 cases; 20.23%), respectively. There were some uncommon types of GIT lymphomas documented during the study. Conclusion: In this largest retrospective single centre study from India, we establish that the pattern of distribution of primary GIT lymphomas (PGLs) in India is similar to the western literature in that the stomach is the commonest site of PGL and DLBCL is the commonest histological subtype. Immunoproliferative small intestinal disease cases were seen in this study, which is uncommon in the west.

How to cite this article:
Arora N, Manipadam MT, Pulimood A, Ramakrishna B S, Chacko A, Kurian SS, Nair S. Gastrointestinal lymphomas: Pattern of distribution and histological subtypes: 10 years experience in a tertiary centre in South India.Indian J Pathol Microbiol 2011;54:712-719

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Arora N, Manipadam MT, Pulimood A, Ramakrishna B S, Chacko A, Kurian SS, Nair S. Gastrointestinal lymphomas: Pattern of distribution and histological subtypes: 10 years experience in a tertiary centre in South India. Indian J Pathol Microbiol [serial online] 2011 [cited 2020 Jul 11 ];54:712-719
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The gastrointestinal tract (GIT) is the commonest site for extra-nodal non-Hodgkin's lymphomas (NHL), which show an increasing incidence worldwide. GIT lymphoma is a heterogeneous entity and constitutes approximately 10-15% of all NHL cases and 30%-40% of all extra-nodal lymphomas. [1]

The involvement of GIT by lymphomas can be primary or secondary, as a part of the dissemination. Primary GIT lymphomas (PGLs) have been defined as those in which involvement of the alimentary tract predominates or those with symptoms of GIT involvement on presentation. [2] This is a more liberal definition than described by Dawson et al. who defined PGL as a tumor that predominantly involves the GIT with lymph node involvement confined to the drainage area of the primary tumor site, when there is no liver or spleen involvement or palpable lymph nodes, when the chest radiograph is normal and the peripheral white cells are normal. [3]

Considerable variation exists in the literature with respect to incidence of the various histological subtypes and sites of involvement of gastrointestinal (GI) lymphomas. [4] The most common site of PGL in Western countries is the stomach (approximately 35-75%), followed by the small intestine (30%) and large intestine (10%). [1] These proportions differ geographically and small intestinal lymphomas are more common than other PGL in the Middle East and North Africa. [5]

This study was undertaken to ascertain the anatomic distribution, histological subtypes, and sites of all GIT lymphomas (both primary and secondary lymphomas) in southern India since there are no large studies documented in the literature from this region which look into the pattern of distribution and histological subtypes. [6]

 Materials and Methods

This was a retrospective study carried out in Department of Pathology, Christian Medical College, Vellore, India covering a period of 10 years from 2001 to 2010 and included 361 patients with histopathological diagnosis of lymphoma involving the GIT (both primary and secondary). All the data were obtained from the computer database at the Department of Pathology.

The study included biopsy material of patients registered with the hospital (n = 318) and from those referred from outside (n = 43). There were 314 mucosal biopsies and 47 resected surgical specimens including total/subtotal colectomy/gastrectomy/ileal resection specimens. All the repeat/multiple biopsies from a single case were excluded from the analysis. Tissue was processed routinely in 10% formalin and 5μ paraffin sections were stained with hematoxylin and eosin (H and E). Immunostaining along with appropriate positive and negative controls was performed manually on paraffin sections with the conventional avidin-biotin peroxidase technique and developed with diaminobenzidine (DAB) with pretreatment by heating in a Pascal pressure cooker in 0.01 M citrate buffer (pH 6.0)/l mM EDTA buffer (pH 8.0) or the proteolytic enzymes, trypsin or pepsin. The antibodies used for IHC included CD3, CD5, CD4, CD7, CD8, CD15, CD20, CD21, CD23, CD30, CD34, CD43, CD45, CD79a, CD99, CD117, CD138, VS38, Kappa, Lambda, Cyclin D1, Bcl-2, TdT, ALK, MUM1, Granzyme B, EBV-LMP1, and MIB-1 (all from DAKO, Glostrup, Denmark); CD10, PAX5, CD56, CD57, H. pylori (Novocastra, Newcastle, UK), and TIA1 (Abcam, Cambridge, UK). The panel of antibodies used in a given case was dependent on morphologic evaluation.

All the cases were reviewed and reclassified based on morphological and immunophenotypic criteria according to the World Health Organization (WHO) 2008 classification. [7] Additional immunostains were studied if necessary. Karyotyping/Fluorescence in situ hybridization (FISH was not available in any of these cases.

Patients were diagnosed as primary or secondary GIT lymphoma. PGL was defined as the presence of GI symptoms or predominant lesions in the GIT as defined by Lewin et al.[2] Site of origin in GIT lymphomas was described as in an earlier study by Koch et al.[4] Patients were considered Heliobacter Pylori (H. pylori) positive if the histology including special stains and/or immunohistochemistry were positive for H. pylori. Serology for H. pylori was not available.


361 cases of lymphoma involving GIT (including 336 PGL) diagnosed over a period of 10 years were included in the study. PGLs included 267 males (79.64%) and 68 female (20.24%) patients, with a male:female ratio of 3.93:1. Males predominated in all subtypes. Majority of the patients were from the higher age groups with peak incidence seen in the 6 th decade (mean age 45 years, range of 3-88 years). The frequency of various histological subtypes, site, and age distribution of both primary and secondary lymphomas are listed in [Table 1], [Table 2], [Table 3] and [Table 4]. The 361 patients included post transplant (n = 9), HIV positive (n = 13), hepatitis C virus (HCV) positive (n = 2), and a single case which was positive for both HIV and HCV.{Table 1}{Table 2}{Table 3}{Table 4}

All the lymphomas involving GIT were NHL except for one case of secondary involvement of GIT by Hodgkin lymphoma (HL). The distribution of PGLs by histological subtype is shown in [Table 1], while [Table 2] shows the distribution of secondary GIT lymphoma. The predominant PGLs were B-cell lymphomas (n = 325; 96.73%). T-cell lymphomas were infrequent and constituted only 3.27 % (n = 11). Diffuse large B-cell lymphoma (DLBCL) was the commonest PGL subtype forming 66.71% of all lymphomas. 6.76% (n = 15) of the DLBCL showed a component of MALT lymphoma. Low-grade marginal zone lymphoma of the MALT type (10.12%) and Burkitt's lymphoma (BL) (10.48%) were the other common subtypes of lymphoma. H. pylori were documented only in 44% (11/25) of the gastric low-grade MALT.

BL constituted 10.48%, was seen commonly in children with a median age of 12 years and commonly involved the small intestine (51.3%) and ileocaecal region (25.71%). HIV was associated with 57.14% (4/7) of the adult BL. There were five cases classified as DLBCL/BL gray zone lymphoma according to the WHO 2008 classification based on the morphology and immunophenotype. Karyotyping/FISH were not available in any of these cases. Mantle cell lymphoma (MCL) accounted for 2.68% of all the patients studied (n = 9) and 44 % (n = 4) of them presented as multiple polyps in the intestine. Other B-cell histological subtypes were found in seven cases, including four cases of immunoproliferative small intestinal disease (IPSID) and three case of plasmablastic lymphoma (PBL). Gastric mucosal biopsies were available in two cases of IPSID and none of these had any H. pylori infection. [Table 2] shows the distribution of various secondary GIT lymphomas. All these cases were high-grade lymphomas. There was a single case of secondary involvement of stomach by grade III follicular lymphoma in a 56-year male. There was not a single case of lymphoblastic lymphoma involving GIT in this series.

Eleven cases (03.27%) were diagnosed as T-cell PGLs, which included one case each of enteropathy-associated T-cell lymphoma (EATCL) and extra-nodal NK/T-cell lymphoma, three cases of anaplastic large cell lymphoma (ALCL) and six cases of peripheral T-cell lymphoma, not other wise specified (PTCL-NOS).

The commonest site for PGL was the stomach (n = 180; 53.57%) followed by the small intestine (n = 79; 23.51%). Large intestine lymphomas constituted 20.23% (n = 68) of the PGLs and included lymphomas of ileocecum (n = 34), colon (n = 23), and rectum (n = 12).

Post transplant lymphoproliferative disorders (PTLPDs) including both B-cell and T-cell NHLs, constituted 02.68% (n = 9) of the PGLs [Table 5]. Majority of these cases were seen in males. DLBCL was the commonest PTLPD (n = 6) followed by PTCL NOS (n = 3). All cases of PTLPD involving the GIT were postrenal transplant (5 months to 14 years post transplant) and predominantly involved jejunum (n = 5; 55%) and stomach (n = 4; 45%).{Table 5}

HIV infection was associated with 04.65% of the PGLs (n = 13), with a male predominance (85.17%; n = 11) [Table 6]. All the cases were high-grade B-cell NHLs. DLBCL was the commonest subtype (n = 6; 46.15%) and other lymphomas included BL (n = 4; 30.77%) and PBL (n = 3; 23.07%). The stomach was the commonest site involved in 53.84% of the cases (n = 7).{Table 6}

There were five PGLs which had an associated synchronous (two cases)/metachronous (three cases) secondary malignancy. These included three cases with secondary malignancies in the GIT [Table 7]. According to Gluckman's definition "synchronous carcinomas" include carcinomas that present either simultaneously or within a 6-month period of identification of the original tumor. Carcinomas diagnosed beyond the 6-month interval are referred to as "metachronous carcinoma." [8]{Table 7}

Some other rare cases documented in this study included a case of lymphocyte depleted CD 20+ HL (CD20+, CD15+ CD30+, and EBV-LMP+) presenting with hepatosplenomegaly and secondarily involving stomach and colon in a 23-year-old male. There was another case of a 51-year-old male having immunohistologic features consistent with B-prolymphocytic leukaemia on cervical lymph node involving ileum. This patient had peripherFal blood lymphocytosis (TLC-69,000, 87% lymphocytes) and 24% prolymphocytes. Flow cytometry also revealed an immunophenotype consistent with CLL/PLL [CD19 +, CD20 (bright), CD22 +, CD23 (dim), CD5 (dim), CD43 +, FMC7 (bright), Kappa (bright), IgD + and IgM+].


GIT lymphomas represent approximately 1-10% of all GI malignancies. [9],[10] It is an uncommon heterogeneous disease in terms of site of involvement, histological subtypes, and treatments offered. [4],[9],[10] The site of involvement and the histological subtypes have been described as independent prognostic factors in many studies so it is important to determine the pattern of distribution and the various histological subtypes common in one particular region. [4] Generally, the most common location for PGL is the stomach (37-86%), followed by the small intestine and large intestine. [4] The proportions may differ geographically with some Turkish and Indian studies suggesting that small intestinal lymphomas are more common than gastric lymphomas. [6],[11]

In this large series on GIT lymphomas from a single centre in India, the stomach was the commonest PGL site, involved in 53.57% of the cases, while the intestines [Figure 1] (both large and small) were involved in 43.75% of the cases. These values are similar to various other studies from UK, [12] Netherlands, [13] and Saudi Arabia [14] but different from two other studies in India which report the intestine as the commonest site [6],[15] . In these studies stomach was involved in 29 [6] and 46.8% [15] of the cases. However, most of these studies analyzed smaller number of cases. [Table 8] and [Table 9] compare the data from our study with the western and Indian studies, respectively.{Table 8}{Table 9}{Figure 1}

Intestinal lymphomas differ significantly from their gastric counterparts, not only in pathology but also with regard to clinical features, management, and prognosis. [16] Small intestine was involved in 23.51% (n = 79) of our cases and large intestine in 20.23% (n = 68), which is similar to the published literature from India and worldwide. In Middle Eastern countries, the frequency of intestinal lymphoma is high (range, 49-81%). This may be partly explained by the high prevalence of IPSID in these areas. [11],[14],[17]

DLBCL, a morphologically heterogeneous type of lymphoma, is the commonest histological subtype of PGL in most of the studies. [4],[18],[19],[20],[21] Similar to these studies, DLBCL was the commonest histological subtype (n = 222; 66.71%) in this study, followed by low-grade marginal zone lymphoma of the MALT (n = 34; 10.12%) type and BL (n = 35; 10.48%). In fact as shown in [Figure 1], DLBCL was the commonest histological subtype seen in stomach, small intestine, and large intestine. A low-grade component of MALT lymphoma was seen in 6.76% (n = 15) of the DLBCL, which is much lower than 33% reported by Koch et al.[4] He also reported that 40% of primary gastric lymphomas were of low-grade MALT type, [4] but in our study we observed that only 14.44% (n = 26) of the gastric lymphomas were of low-grade MALT type. The stomach was the commonest site for MALT lymphomas (n = 26; 76.47%) similar to what has been reported in literature (85%). [22] H. pylori were seen in only 44% of the gastric low-grade MALT, which is much lower than reported in the literature (92%), [23] but these values are based only on histology and serology studies were not available in these cases. Serology studies though are mandatory when results of histology are negative as they increase the sensitivity. There is no large study from India looking at the association between H. pylori and gastric MALT lymphomas. Sood et al. were able to demonstrate H. pylori in 10% (1/10) [1] of the low-grade gastric MALT lymphoma (only light microscopy), whereas Shukla et al.[24] reported H. pylori in 75% (3/4) of the low-grade gastric MALT. These numbers are too small for any meaningful comparison.

IPSID a variant of MALT, commonly seen in the Middle East countries and very rarely from the western countries has only been reported very sporadically in India. [25],[26] IPSID accounted for only 1.2% (n = 4) of our PGLs [Figure 2], which is significantly lower than 23 % (20/85) reported by Salem et al.[11] in the Middle East, but it does suggest that IPSID does occur in this part of the world. All the cases of IPSID were males, with two cases each in third and sixth decade. The small intestine was involved in all the four cases with involvement extending uptill rectum in one case and stomach in one. BL constituted 19.72% (n = 29) of our intestinal lymphomas and was seen predominantly in the children. DLBCL/BL gray zone has been reported to involve GIT and was seen in 1.49 % (n = 5) of the lymphomas. PBL is a recently described entity with a unique immunophenotype and a predilection for the oral cavity of patients with HIV. [7] GIT has been described as one of the common sites. [7] We had three cases (0.83%) of PBL involving GIT with a case each involving colon and rectum.{Figure 2}

Primary GIT T-cell lymphomas are rare. [27],[28] It has been shown T-cell NHL formed 1.5% of all the GIT lymphomas by Koch et al.[4] and 3.5% of the total GIT lymphomas (excluding ALCL) by Shet et al.[28] In this study we were able to document that T-cell lymphomas formed 3.27% (n = 11) of the PGLs and this includes cases of primary ALCL. EATCL is a T-cell lymphoma associated with celiac disease and has been described more in the western literature rather than Asia. [28],[29] We documented a single case of EATCL (CD3+, CD8+, CD56+) involving ileum [Figure 3] in a 53-year-old male who presented with complaints of diarrhea, weight loss, and insignificant past history.{Figure 3}

Lymphomas that occur in immunodeficiency conditions are clinically and pathologically very heterogeneous. GIT involvement is described in up to 30% of patients with PTLPD. [30] PTLPD was noted in 2.68% of the PGLs in this study (n = 9). In HIV-associated lymphomas, GIT is one of the most frequent extra-nodal sites [7],[30] and similar to this series (84.61%) male predominance is described in the literature. [31] Stomach was the commonest site which is similar what has been reported to Imrie et al.[32] and Heise et al.[33] but different from Srinivasan et al.[31] who documented small bowel as the commonest site (30%). DLBCL (6/13) was the commonest PGL associated with HIV infection which is similar to the experience of Srinivasan et al.[31] The other histological subtypes included BL (n = 4) and PBL (n = 3) [Figure 4].{Figure 4}

Second malignancies including both synchronous and metachronous gastric adenocarcinoma and MALT lymphomas although rare have been well documented. [34],[35],[36],[37],[38] Metachronous gastric adenocarcinoma following gastric MALT has been reported in seven cases in a series. [35] Lee et al.[36] reported five cases of synchronous gastric adenocarcinoma and MALT lymphoma among 6012 gastric adenocarcinoma patients (8.3%) and a higher frequency among 25 primary gastric MALT lymphoma patients (20.0%). We had five GIT lymphomas which had an associated synchronous (two cases)/metachronous (three cases) secondary malignancy. The case of synchronous BL with renal cell carcinoma is the first case to be reported in the literature and has been published. [37]

In conclusion, this retrospective single centre largest study of patients with GIT lymphoma from south India illustrates the pattern of distribution of various common and rare histological subtypes in a tertiary centre. The pattern of distribution was similar to the western reports in that stomach is the commonest site for GIT lymphoma and DLBCL the commonest histological subtype. IPSID though not as common in the Middle East does occur in our country, whereas EATCL of the GIT are rare as compared to the West.[42]


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