Review
Copyright ©2011 Baishideng Publishing Group Co., Limited. All rights reserved.
World J Gastrointest Oncol. Jan 15, 2011; 3(1): 14-18
Published online Jan 15, 2011. doi: 10.4251/wjgo.v3.i1.14
Primary colorectal lymphoma: An overview
Goran Z Stanojevic, Milica D Nestorovic, Branko R Brankovic, Miroslav P Stojanovic, Milan M Jovanovic, Milan D Radojkovic
Goran Z Stanojevic, Milica D Nestorovic, Branko R Brankovic, Miroslav P Stojanovic, Milan M Jovanovic, Milan D Radojkovic, Clinic for General Surgery, Clinical Center Nis, Bul Zorana Djindjica 48, 18000 Nis, Serbia
Author contributions: Stanojevic GZ contributed substantially to conception and design; Nestorovic MD and Brankovic BR contributed to data acquisition; Nestorovic MD and Radojkovic MD contributed to analysis and interpretation of data; Stojanovic MP and Jovanovic MM drafted the article and revised it critically for important intellectual content; Stanojevic GP gave final approval of the version to be published.
Correspondence to: Goran Z Stanojevic, MD, PhD, Professor, Clinic for General Surgery, Medical Faculty, University of Nis, Bul Zorana Djindjica 48, 18000 Nis, Serbia. stgoran64@gmail.com
Telephone: +381-18-506946 Fax: +381-18-596006
Received: September 15, 2010
Revised: December 20, 2010
Accepted: December 27, 2010
Published online: January 15, 2011

Abstract

Lymphomas represent common hematological malignancies with increasing incidence in recent years. The major site of extranodal non-Hodgkin lymphoma is the gastrointestinal tract. Involvement of the large intestine is rare in comparison to the stomach or small bowel. The disease appears later in life, predominantly in the male population. Complaints are nonspecific, requiring a high index of suspicion in order to establish the diagnosis. The treatment varies from chemotherapy alone to multimodal therapies combining surgery, chemotherapy and radiotherapy. The small number of patients with various histological subtypes and different stage at presentation results in unclear protocol for the treatment of primary colorectal lymphoma. The purpose of this paper is to review current data on primary lymphoma of the colon and rectum while analyzing reported case series and published material on the subject.

Key Words: Lymphoma non-Hodgkin, Extranodal lymphoma, Large intestine, Colorectal surgery, Chemotherapy


Citation: Stanojevic GZ, Nestorovic MD, Brankovic BR, Stojanovic MP, Jovanovic MM, Radojkovic MD. Primary colorectal lymphoma: An overview. World J Gastrointest Oncol 2011; 3(1): 14-18
INTRODUCTION

Thomas Hodgkin was the first to introduce lymphomas into medical science in 1832. Subsequent to his report, two decades later, Virchow divided leukemia into the leukemic and “aleukemic” types, employing the term “lymphosarcoma”. At about the same time, a probable case of acute leukemia was published by Cohnheim in 1865 under the term “pseudoleukemia”. Pseudoleukemia was to become a catch-all for a variety of conditions with lymphadenopathy and splenomegaly in common. In 1893, Kundrat and colleagues again used the term lymphosarcoma. The first one to clearly describe follicular or nodular lymphomas was Brill et al in 1925 followed by Symmers in 1927. In 1942, Gall and Mallory introduced a lymphoma classification based on clinicopathological criteria, the first systematic attempt to bring order into the non-Hodgkin’s lymphoma (NHL) situation[1]. Over years, various classification systems have been used to differentiate lymphomas including the Rappaport Classification (used until the 70s)[2], Kiel System[3], Working Formulation[4] and Revised European-American Classification of Lymphoid Neoplasms (REAL)[5]. The latest WHO classification[6] recognizes 5 histological subtypes of B cell lineage: Extranodal marginal lymphoma (MALT lymphoma), follicular lymphoma, mantle cell lymphoma, diffuse large B-cell lymphoma and Burkitt’s lymphoma. According to REAL classification, intestinal T cell lymphomas were subdivided into enteropathy-associated T cell lymphoma and non-enteropathy associated T cell lymphoma that are now considered peripheral T cell derived lymphomas by the WHO classification[7]. All histological subtypes of nodal lymphomas may arise in the gastrointestinal tract but the major two appearing in more than 90% of cases are diffuse large B-cell NHL and mucosa-associated lymphoid tissue (MALT) NHL[8].

Lymphoma is the sixth most common cause of cancer death in the United States with increasing incidence in recent years[9]. It is a common malignancy affecting more than 58 000 patients in the United States[10]. In 40% of cases, the major site of extranodal NHL is the gastrointestinal tract. Involvement of the large intestine is rare (10%-20% of all gastrointestinal lymphomas) in comparison to the stomach or small bowel[11]. Primary NHL accounts for 0.1%-0.5% of all malignant tumors of the colon and rectum which makes it the third most common large bowel malignancy after adenocarcinoma and carcinoid[12].

DEFINITION, TYPES AND ETIOLOGY

Dawson et al[13] established criteria for the diagnosis of primary colorectal lymphomas in 1961. These are: (1) no enlarged superficial lymph nodes when the patient is first seen; (2) chest radiographs without obvious enlargement of the mediastinal nodes; (3) the white blood cell counts, both total and differential, are within normal range and bone marrow biopsy is also normal; (4) at laparotomy only regional nodes are affected by disease; and (5) the liver and spleen seem free of tumor. In the modern era, these criteria have been expanded to new diagnostic tools. Krol et al[14] in a paper from 2003 described three alternative definitions of primary nodal and extranodal NHL, exploring their effect on the percentage of the patients considered to have primary extranodal disease, their treatment outcome and survival in a population-based cohort of NHL patients. Their analysis showed that in nearly 10% of patients, a distinction between nodal or extranodal origin could not be made. When using a strict definition of extranodal lymphomas, better response rates and overall survival are found due to patient selection. With inclusion of disseminated disease in the extra nodal group, one can find no differences between response rate and overall survival in patients with nodal lymphomas compared to extranodal lymphomas. They proposed a more liberal definition of primary extranodal NHL that includes all patients who present with NHL that apparently originated from an extranodal site, even in the presence of disseminated disease, as long as the extranodal component is clinically dominant[14].

The most common histological subtype occurring in the colon and rectum is diffuse large B-cell lymphoma with frequency ranging from 47%-81% depending on the geographical location[12,15,16]. In the study conducted in 4 continents with 1378 patients, Anderson et al[17] have shown that the distribution of NHL subtypes differs in various geographical areas and suggested that this could be a reflection of differences in etiological factors or the host response to these factors. Unlike western countries, frequency of T cell lymphoma in the East is reported to be 17.9%-42%[18,19]. Primary colorectal lymphoma differs from its gastric counterpart. The stomach is the most frequent site of origin of primary gastrointestinal lymphomas. The most common histological type found is MALT lymphoma[20]. Gastric MALT associated lymphoma can be successfully treated by Helicobacter pylori (H. Pylori) eradication. The same histological subtype localized in the large intestine does not have the same connection with H. pylori infection[21].

Staging of the lymphomas is also going through some changes. The widely used Ann Arbor classification for extranodal lymphomas modified by Musshoff[22] has its limitations in terms of tailoring the treatment of each specific lymphoma entity. Several modifications have been developed[23]. The European Gastro-Intestinal Lymphoma Study Group (EGILS) proposed a modified TNM staging system adjusted for gastrointestinal lymphoma, taking into consideration the histopathological characteristics of extranodal B and T-cell lymphomas[24].

Etiological factors involved in the development of primary colorectal lymphoma are unknown. However, high frequency has been observed in conditions of immunosuppression such as inflammatory bowel disease-ulcerative colitis, HIV infection and conditions following organ transplantation[12]. In small series conducted by Doolabh et al[25], 3 out of 7 patients were HIV positive. Since the incidence of infection continues to rise, it would seem that HIV serology in all patients presenting with primary lymphoma of colon is warranted[25].

For the purposes of this overview, the data from the published studies of the primary colorectal lymphoma were analyzed (Table 1).

Table 1 Published studies on primary colorectal lymphoma.
AuthorPatientsMale:femaleAnalyzed periodStage
Therapy
Follow up in months (mo)Overall survival
 IIIIIIIVMult.Chem.Surg.
Cai et al[15]4329:141973-200541042526133Mean 64.8Rate 42%
Bairey et al[16]1712:513 yr52010962Median 75Median 44 mo
Kim et al[18]9564:311986-200234540757239Mean 29.55 yr rate 55.2%
Doolabh et al[25]74:31989-19981600601--
Stanojević et al[27]2420:141991-20050111212404Mean 30.3Mean 41.9 mo
Fan et al[28]3722:151980-19969230522213Median 50.4Median 24 mo
Cho et al[29]2317:61946-1993157011443Median 14410 yr rate 61%
Gonzalez et al[30]155:101990-2002150001503Median 28Median 60 mo
Wong et al[31]1413:11989-199905721103Median 20Rate 57.1%
Busch et al[32]1916:31972-198856081431-Median 45 mo
PRESENTATION AND DIAGNOSIS

The mean age at diagnosis is 55 years. Men are affected twice as often as women[16,26-28]. The most common symptoms in more than half of patients are abdominal pain and weight loss or changing in bowel habits[16,27,28]. Lower gastrointestinal bleeding can be found in 13%-82% of patients[15,28,29]. Infrequency of these complaints suggests that, despite of the large size of the lymphoma, mucosal ulceration does not usually occur[28].

The cecum is the most frequent location for primary colorectal lymphoma[16,27,28,30], probably due to the larger amount of lymphoid tissue in this region[31]. In different series, the data on the frequency in the rectum varies from 8.3% to 35%[27,29,31,32].

The lack of specific complaints makes the diagnosis hard to establish. Unfortunately, for some patients, a surgical procedure is the only diagnostic tool. As a rare lesion, it requires a high index of suspicion. Due to a delay in diagnosis in 33%-65% of patients, operative procedure is either urgent or emergent[12,15,16]. In more than half of patients, lymphoma is a bulky disease (Figure 1), reaching over 5 cm in diameter[16,27,28]. These bulky masses can usually be palpated by simple physical examination and can be viewed by ultrasonography[16].

Figure 1
Figure 1 Primary lymphoma of the cecum.

Colonoscopy is valuable in the diagnosis of primary lymphoma of the colon in a non-urgent setting but it is not always possible to determine this type of tumor due to an inadequate biopsy and the need for time consuming immunohistochemical staining. The growth patterns that can be seen in the colon vary. Usually colorectal lymphomas are large, polypoid lesions but mucosal ulceration can also be found (Figure 2). Lymphomatous polyposis can appear similar to familial adenomatous polyposis[33]. Plain radiographs of the abdomen are not helpful. Barium enema can be useful but it cannot distinguish adenocarcinoma or polyposis from lymphoma (Figure 3).

Figure 2
Figure 2 Colonoscopy findings of mantle cell lymphoma.
Figure 3
Figure 3 Barium enema showing lymphomatous polyposis.

Radiographical findings associated with colorectal lymphoma can be localized or diffuse. Computerized tomography (CT) shows the focal form of NHL characterized by infiltrative spread rising from the submucosa, resulting in uniform thickening of the intestinal wall, usually without associated desmoplastic reaction. Infiltration of the muscularis propria and the autonomic plexus may result in atonic, aneurismal dilatation of the lumen. Sometimes, lymphoma may form an annular napkin-ring lesion that mimics carcinoma[34]. When CT reveals the presence of an infiltrative process accompanied by enlarge lymph nodes in the abdomen or pelvis, lymphoma should be the primary consideration in the differential diagnosis and must be excluded by endoscopic biopsy. However, without the presence of enlarged lymph nodes it might be difficult to distinguish this type of tumor from a primary adenocarcinoma. This difficulty arises predominantly in cases with solitary mass lesions[35]. The role of PET (positron emission tomography) in the diagnosis and follow up of patients with lymphoma is yet to be established[36].

Disease stage at the time of diagnosis varies in publications. In 2008, in a retrospective study of 15 patients with colorectal lymphoma, Gonzales et al[30] reported all stage IE. Similar results were published in a German study of 371 patients by Koch et al[26] from 2001. On the contrary, other papers reported that than 54.2% of patients were treated in stage IIIE and IVE[15,27]. In a recent paper by Bairey et al[16], seven patients out of seventeen were reported to have stage I or II at diagnosis whereas all others had stage IV. In a study by Fan et al[28], 13.5% of the patients were stage IVE while 24.3% were stage IE and 62.3% were stage IIE.

MANAGEMENT

Although the role of surgery in the treatment of gastrointestinal lymphoma is debatable, the majority of the reported patients were operated on irrespective of the disease stage. There are no controlled randomized trials due to the low incidence of the disease. According to some series, since the rate of spontaneous perforation is high (5 out of 17 patients), it is beneficial to perform a hemicolectomy in order to prevent this complication[16]. Some authors argue that early diagnosis and timely onset of chemotherapy might do the job for such patients, thus avoiding a surgical procedure. There is tacit agreement that in the absence of disseminated disease, surgical resection is generally performed[25,27,28,30,37]. It is believed that surgery may provide important prognostic information, including history, tumor extent and stage, could prevent complications and may offer a chance for cure with or without chemotherapy[28].

In the published studies, treatment varies from chemotherapy alone to multimodal therapies combining surgery, chemotherapy and radiotherapy. Chemotherapy remains the basis of treatment for the rapidly proliferating aggressive lymphomas because these malignancies almost always extend beyond local fields, encompassed by surgery or radiation. The CHOP chemotherapeutic regimen (cyclophosphamide, doxorubicin, vincristine and prednisone) remains the first line therapy for all moderate and high-grade B-cell lymphomas. Several prospective trials have shown that adding rituximab to standard CHOP regiment (R-CHOP) resulted in higher response rates and better progression-free, event-free, disease-free and overall survival[38]. Fan et al[28] found significant improvement in the survival of patients with stage IIE who received adjuvant chemotherapy. However, the analysis of the subgroup of patients with high grade lymphoma in stage I and II showed that adding chemotherapy did not significantly impact survival. In 2005, Bilsel et al[35] reported the case of primary lymphoma of the rectum with complete clinical response after combination of radiation and chemotherapy. Similar results were published by other authors[39]. In case series published in 2002, Pricolo et al[40] treated patients with surgical resection and adjuvant chemo and radiotherapy, while Shimono et al[41] from Japan suggested preoperative radiotherapy. Some authors proposed the so called preventive chemotherapy in patients with stage IE, reaching five year survival of 80%[42]. In cases of indolent lymphomas (mantle cell, follicular cell and T cell lymphomas), complete surgical resection and radiation are recommended because of decreased chemoresponsiveness[43]. The median survival in reported series is generally low. Patient with stage IV disease demonstrates poor survival (up to 8 mo)[16].

Factors affecting survival differ among authors. Stage at the diagnosis has impact on survival[15,16,27]. According to Fan et al[28], only histological grade seems to be an adverse factor for prognosis. Urgency of the surgical procedure is also found to be an important factor affecting survival[16,27].

CONCLUSION

The vast majority of patients with primary colorectal lymphoma underwent some form of resection although the role of surgery and its extent is yet to be established. After resection, most patients undergo CHOP or other multiagent therapy. The optimal management of primary lymphoma of the colon and rectum has never been determined by randomized trials. The small number of patients with various histological subtypes and different stage at presentation results in unclear treatment protocol. Since all the published studies are retrospective, their scientific validity is partially diminished, imposing the need for conducting prospective multicentric studies. Meanwhile, systematized clinical experiences contribute usefully to the knowledge of clinicians.

Footnotes

Peer reviewers: Tatsuo Kanda, MD, PhD, Division of Digestive and General Surgery, Graduate School of Medical and Dental Sciences, Niigata University, Niigata City 951-8510, Japan; Jaw Yuan Wang, Professor, MD, PhD, Department of Surgery, Kaohsiung Medical University and Hospital, 100, Tzyou 1st Road, Kaohsiung 807, Taiwan, China; Ioannis A Voutsadakis, MD, PhD, Department of Medical Oncology, University Hospital of Larissa, Larissa 41110, Greece

S- Editor Wang JL L- Editor Roemmele A E- Editor Ma WH

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