Abstract
Colon lymphoma is a rare type of gastrointestinal lymphoma and represents 0.2% to –1.2% of all primary colon cancers. This study aimed to retrospectively examine the general characteristics, treatment methods, and survival characteristics of patients with colon lymphoma who were followed-up at our center. This retrospective study included patients diagnosed with colon lymphoma who were followed up at Ankara Numune Training and Research Hospital and Ankara Bilkent City Hospital between December 2005 and June 2023. Clinicopathological features, radiological findings, treatments, and modalities of patients were obtained from their medical records. Fourteen patients with primary colon lymphoma were included in the study. Thirteen patients (92.9%) were diagnosed with diffuse large B-cell lymphoma. The median age of the patients was 55 (28–84) years. The tumor location was the terminal ileum/cecum in 50% of the patients. At the time of diagnosis, 10 patients (7 with stage 1E-2E disease, 2 with stage 3E disease, and 1 with stage 4E disease due to tumor obstruction) underwent surgery. Twelve patients received chemotherapy (6 patients as adjuvant and 6 patients as first-line treatment). The median overall survival (OS) was 10 years (0.1–21.5) years, the 5-year median OS was 71%, and the 10-year median OS was 53%. Primary colon lymphoma is a rare disease and its optimal treatment is not clearly defined. The primary treatment for primary colon lymphoma is a combination of surgery and chemotherapy. A clear consensus on the treatment can be established through prospective studies.
Keywords: colon lymphomas, gastrointestinal lymphoma, primary colon cancers, rare disease
1. Introduction
Lymphoproliferative diseases are classified into Hodgkin lymphoma and non-Hodgkin lymphoma (NHL). Gastrointestinal lymphoma is the most common type of extranodal infiltration, with a rate of 15% to 20%, as the mesenteric or retroperitoneal lymph nodes are common origins that can share lymphatic drainage with the gastrointestinal tract.[1] Primary extranodal NHL represents lymphomas that arise in any organ outside the lymph nodes or spleen and can involve the gastrointestinal tract at any site from the oropharynx to the rectum, with the most common sites of involvement being the stomach (50–75%), small intestines (20–30%), and colon and rectum (10–20%).[2]
Colon lymphoma is a rare type of gastrointestinal lymphoma and the third most common malignancy of the colon, after carcinomas and carcinoids. It represents 0.2% to 1.2% of all primary colon cancers.[2,3] It may be primary or secondary to systemic lymphoma. NHL is the most common histological subtype, and the most common NHL subtype in the colon and rectum is diffuse large B-cell lymphoma (DLBCL).[4] Males is most commonly affected, with a peak incidence in the sixth and seventh decades of life.[5] The presentation is usually nonspecific, leading to a delay in diagnosis.[6] Treatment involves either chemotherapy alone or multiple modalities, including surgery, chemotherapy, and radiotherapy.[7] Despite advances in cancer treatment in recent years, colon lymphomas have a worse prognosis than other gastrointestinal lymphomas, with a 5-year survival rate of approximately 50%.
This study aimed to retrospectively examine the general characteristics, treatment methods, survival characteristics, and factors affecting the characteristics of patients with colon lymphoma followed up at our center.
2. Materials and methods
This retrospective study included patients diagnosed with colon lymphoma who were followed up at Ankara Numune Training and Research Hospital and Ankara Bilkent City Hospital between December 2005 and June 2023. The files of 14 patients with colon lymphoma aged ≥ 18 years were accessed.
Age at diagnosis, symptoms at presentation, ECOG performance status, comorbidities, tumor location, disease stage, and treatment regimens received were obtained from the patients’ files. Clinicopathological features, radiological findings, treatments, and modalities of patients were obtained from their medical records. Overall survival (OS) was defined as the time interval from the time of the first metastatic disease to death due to any reason or last follow-up. Data were retrospectively analyzed.
The study was approved by the Ethics Committee of Ankara Bilkent City Hospital in accordance with the Declaration of Helsinki (decision number E1-22-2386) and the approval date of February 09, 2022.
2.1. Statistical analysis
SPSS Statistics (version 24.0; IBM Corp., Chicago, IL) was used for the statistical analysis. Continuous variables are presented as median (minimum–maximum), and categorical variables are presented as percentages. The Kaplan–Meier method was used for the survival analysis. Statistical significance was set at P < .05.
3. Results
Fourteen patients were included in the study. All the patients had non-Hodgkin subtypes. The clinical and pathological characteristics of the patients are summarized in Table 1. One patient (7.1%) had follicular lymphoma, and 13 (92.9%) had DLBCL. Pathological grade information was obtained for 10 patients. Seven patients were grade 3, one patient was grade 2, and 2 patients were grade 1. The median age of the patients was 55 (28–84) years. Nine patients (64.3%) were male, and 5 patients (35.7%) were female. Eleven (78.6%) patients presented with abdominal pain, 1 (7.1%) with rectal bleeding, 1 (7.1%) with nausea and vomiting, and 1 (7.1%) with weight loss. Four (28.6%) patients had comorbidities (1 patient had diabetes mellitus, 1 patient had hypertension, 1 patient had hypothyroidism, and 1 patient had asthma bronchiale). Nine patients (64.1%) had an Eastern Cooperative Oncology Group Performance Status (ECOG PS) of 1, 4 patients had an ECOG PS of 2, and 1 patient had an ECOG PS of 3. None of the patients had B symptoms. The Follicular Lymphoma International Prognostic Index score of patients diagnosed with follicular lymphoma was 2 (intermediate-risk group). The International Prognostic Index score of patients diagnosed with DLBCL was 0–1 (low risk) in 4 (30.8%) patients, 2 (low-intermediate risk) in 4 (30.8%) patients, 3 (high-intermediate risk) in 3 (23.1%) patients, and 4–5 (high risk) in 2 (15.3%) patients.
Table 1.
Clinical and pathological characteristics of patients.
| Variables N (%) Median (minimum; maximum) | |||
|---|---|---|---|
| Age of diagnosis (years) |
|
55 (28;84) | |
| Gender | Female | 5 (35.7%) | |
| Male | 9 (64.3%) | ||
| Compliant | Abdominal pain | 11 (78.6%) | |
| Lower gastrointestinal bleeding | 1 (7.1%) | ||
| Nausea—vomiting | 1 (7.1%) | ||
| Weight loss | 1 (7.1%) | ||
| Comorbidity | No | 10 (71.4%) | |
| Yes | 4 (28.6%) | ||
| B symptom | No | 3 (21.4%) | |
| Yes | 11 (78.6%) | ||
| ECOG PS | 0–2 | 13 (92.9%) | |
| 3 | 1 (7.1%) | ||
| Alcohol | No | 13 (92.9%) | |
| Yes | 1 (7.1%) | ||
| Smoking | No | 7 (50%) | |
| Yes | 7 (50%) | ||
| IBD | No | 13 (92.9%) | |
| Yes | 1 (7.1%) | ||
| Bulky disease | No | 9 (64.3%) | |
| Yes | 5 (35.7%) | ||
| Colonoscopic finding | Diffuse infiltration | 5 (35.7%) | |
| Tumor or mass | 8 (57.1%) | ||
| Polyps | 1 (7.1%) | ||
| Tumor location | Ascending colon | 3 (21.4%) | |
| Descending—sigmoid colon | 3 (21.4%) | ||
| Multiple segments | 1 (7.1%) | ||
| Terminal ileum—caecum | 7 (50%) | ||
| Tumor size (cm) |
5 (4;15) | ||
| Tumor obstruction | No | 4 (28.6%) | |
| Yes | 10 (71.4%) | ||
| NHL subtype | Diffuse large B cell lymphoma | 13 (92.9%) | |
| Follicular lymphoma | 1 (7.1%) | ||
| CNS risk score | Low risk | 6 (42.9%) | |
| Intermediate risk | 5 (35.7%) | ||
| High risk | 3 (21.4%) | ||
| IPI score | Low risk | 4 (28.6%) | |
| Low intermediate risk | 5 (35.7%) | ||
| High intermediate risk | 3 (21.4%) | ||
| High risk | 2 (14.3%) | ||
| Treatment response of patients receiving first-line chemotherapy | CR | 2 (33%) | |
| SD | 4 (67%) | ||
CNS = central nervous system, CR = complete response, ECOG PS = Eastern Cooperative Oncology Group Performance Status, IBD = inflammatory bowel disease, IPI = The International Prognostic Index, N = number of patients, SD = stable disease.
Tumor location was terminal ileum/cecum localization in 7 patients (50%), ascending colon localization in 3 (21.4%), descending colon localization in 3 (21.4%), and multisegmentary localization in 1 (7.1%). The median primary tumor diameter was 5 (4–15) cm. The following results were detected in the colonoscopic findings of the patients: mass formation in 8 (57.1%) patients, diffuse infiltration in 5 (35.7%) patients, and polyp in 1 (7.1%) patient. Two patients were stage 1E (14.3%), 5 were stage 2E (35.2%), 2 were stage 3E (14.3%), and 5 were stage 4E (35.7%). At the time of diagnosis, 10 patients (7 patients with stage 1E–2E disease; 2 patients with stage 3E and developing tumor obstruction; 1 patient with stage 4E disease and developing tumor obstruction) underwent surgery, while 4 patients with stage 4E disease did not undergo surgery. Five patients (35.7%) had bulky disease (tumor size ≥ 7.5 cm). One patient was diagnosed with stage 3E DLBCL, underwent surgery due to tumor obstruction, and died of COVID-19 pneumonia 2 weeks after the operation. One patient diagnosed with stage 1E DLBCL did not receive any postoperative chemotherapy. In total, 12 patients received chemotherapy (6 patients as adjuvant, 6 patients as first-line treatment). The chemotherapy regimens received by the patients were as follows: 9 (75%) patients received rituximab, cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP); 1 (8.3%) patient received rituximab; 1 (8.3%) patient received CHOP; and 1 (8.3%) patient received cyclophosphamide, epirubicin, vincristine, and prednisone (CEOP).
The mean follow-up period was 4.5 years. The median OS was 10 years (0.1–21.5) years. The 5-year median OS was 71%, and the 10-year median OS was 53%.
4. Discussion
In this study, the average age at diagnosis was 50 years and 64.3% of the patients were male. Studies have found that primary colon lymphoma affects the 5th to 7th decades of life and has a male-to-female ratio of 1.5–2:1.[8]
Gastrointestinal lymphomas are predominantly of the B-cell type, with DLBCL being the most prevalent histological subtype, followed by mucosa-associated lymphoid tissue lymphoma.[4] NHL is the most prevalent histological subtype, with DLBCL being the most common NHL subtype in the colon and rectum, accounting for 47% to 81% of cases.[4,9,10] In our study, all our patients had NHL. Most patients (92.9%) had DLBCL, and one patient (7.1%) had follicular lymphoma.
The most commonly used staging system for colon lymphomas is the Lugano classification, which is based on the Ann Arbor system modification.[11] The Lugano classification focuses on the number of tumor sites (nodal and extranodal) and their location. In stage 1 disease, there is involvement of a single lymph node region (stage I) or a single extra-lymphatic organ or region without nodal involvement (stage IE). In stage 2, there is involvement of 2 or more nodal regions on the same side of the diaphragm (stage II), or stage I or II by nodal involvement with limited contiguous extranodal involvement (stage IIE). In Stage 3, lymph node involvement was observed on both sides of the diaphragm. In stage 4, there is diffuse involvement of one or more lymphatic organs with or without nodal involvement. In our study, 2 patients were stage 1E (14.3%), 5 patients were stage 2E (35.2%), 2 patients were stage 3E (14.3%), and 5 patients were stage 4E (35.7%). 50% of the patients had stage 3–4 disease. In a retrospective study including 15 colorectal lymphoma patients, all patients had stage IE disease.[5] Conversely, other studies found that more than 54.2% of patients were stage IIIE and IVE.[9,12] Bairey et al[4] reported that 7 out of 17 patients were in stage I or II, and 10 were in stage 4. In a study of 37 cases of colorectal lymphoma, 24.3% of patients were stage IE, 62.2% were stage IIE, and 13.5% had stage 4E.[8]
Clinical symptoms vary depending on the lesion site, and abdominal pain, weight loss, and diarrhea are the most common symptoms.[13] In the present study, abdominal pain was the most prevalent symptom, affecting 78.6% of patients, followed by rectal bleeding, nausea and vomiting, and weight loss. These findings are consistent with those of previous studies in which abdominal pain was reported in 62% and 56% of patients, whereas weight loss was observed in 43% and 29% of patients, respectively.[4,5]
The median primary tumor diameter in our study was 5 cm (range: 4–15 cm). This aligns with previous studies indicating that over 50% of patients presented with a primary tumor mass > 5 cm.[8,12] In a study involving 14 primary and 3 secondary colon lymphomas, the tumor diameter exceeded 5 cm in 3 patients and 10 cm in 8 patients, with DLBCL detected in 11 of the 14 primary cases.[4]
The cecum is the most common site of primary lymphoma, with frequent involvement of the ileocecal valve because of the abundance of lymphoid tissue in this region.[3,14] This is consistent with the findings of Gonzalez et al, in which the cecum was the most frequently involved region (60%) in primary colon lymphomas, followed by the right colon (27%), and the sigmoid colon (13%).[5] Similarly, in our study, the tumor was located in the terminal ileum/cecum in 50% of the patients.
Due to the rarity of primary colon lymphoma, the optimal treatment approach remains undefined. Existing literature consists mainly of retrospective case series with limited patient numbers and individual case reports. The primary treatment for primary colon lymphoma is a combination of surgery and chemotherapy.[15] While some studies advocate surgical intervention for early stage disease and chemotherapy in advanced cases, others suggest that chemotherapy should be the mainstay of treatment for patients with nodal involvement.[10,14,16] Surgery also plays a role in alleviating pain and managing emergency situations such as obstruction, perforation, and bleeding. Although complete tumor obstruction is uncommon at diagnosis in intestinal lymphomas, partial obstruction may occur.[17] In a study evaluating 43 patients diagnosed with colorectal lymphoma, 56% of the patients required emergency surgery.[9] In another series in which 46 patients diagnosed with ileocecal lymphoma were evaluated, 13 patients required emergency surgery.[18] In our study, 71.4% of the patients underwent surgery due to tumor obstruction. The initial presenting symptoms and signs may vary and are influenced by the location of the tumor within the intestine.
CHOP chemotherapy remains the first-line treatment for intermediate- and high-grade B-cell lymphoma. Studies have demonstrated improved response rates and survival outcomes with the addition of rituximab to standard CHOP chemotherapy.[19] In a retrospective analysis of 52 colorectal lymphomas, 36 cases underwent surgery.[20] Better OS results were obtained in patients who underwent radical surgery than in patients who received only chemotherapy or in the palliative surgery group. In a study involving 14 patients with colorectal lymphoma (DLBCL) who received R-CHOP adjuvant chemotherapy following surgical resection, the disease-free survival rate was 88.2% after a median follow-up of 55 months[21] Bilsel et al reported a case of rectal DLBCL with bulky disease, where a loop colostomy was performed followed by ProMACE chemotherapy (doxorubicin, cyclophosphamide, etoposide, prednisone, and methotrexate) and involved-field radiation therapy, resulting in a complete response.[22] In cases of indolent lymphomas (e.g., mantle cells and follicular cells), complete surgical resection and radiotherapy may be recommended because of their lower responsiveness to chemotherapy.[23]
The literature suggests that survival outcomes are improved in stage 1E and 2E patients who undergo surgery followed by chemotherapy.[6,24,25] Studies have demonstrated a 10-year overall survival rate of 83% in stage IE patients who received adjuvant chemotherapy after surgery.[24] Additionally, surgery has been shown to provide good local control in early stage primary colon lymphoma.[5,6] Therefore, early stage tumors can be effectively treated with surgery followed by adjuvant chemotherapy, whereas advanced-stage tumors are typically managed with multi-agent chemotherapy, often avoiding surgery.[4,26,27] The primary reason for avoiding nonsurgical chemotherapy in early-stage cases is the potential risk of tumor perforation as a response to chemotherapy.
In our study, the median overall survival (OS) was 10 years (range: 0.1–21.5 years), with a 5-year OS of 71% and a 10-year OS of 53%. The 5-year median overall survival (OS) in colorectal lymphoma was 71% in a study by Huang et al involving 52 patients, whereas Zhai et al reported a 5-year median OS of 64.2% in a study of 46 colorectal lymphoma patients.[18–20] Kim et al observed a 5-year OS of 55.2%, and Cho et al reported a 10-year median OS of 61% in their study of 23 patients.[28,29]
This study had certain limitations. The fact that this was a retrospective study is a significant limitation. Our number of patients was relatively small, but in the literature review, we came across a case series with a small number of patients, since primary colon lymphoma is very rare. As this was a retrospective study, we could not assess the pathological staining characteristics of some patients from patient files.
5. Conclusions
In conclusion, primary colon lymphoma is a rare disease, and its optimal treatment has not been clearly defined. A retrospective case series with a small number of patients and case reports is available in the literature. Although no consensus has been reached, the primary treatment for primary colon lymphoma involves a combination of surgery and chemotherapy. Prospective studies are warranted to establish a clear consensus regarding treatment.
Author contributions
Conceptualization: Denizcan Hasturk, Selin Akturk Esen.
Data curation: Muge Buyukaksoy.
Formal analysis: Ismet Seven.
Investigation: Ismet Seven.
Methodology: Burak Civelek.
Project administration: Dogan Uncu.
Resources: Denizcan Hasturk.
Software: Muge Buyukaksoy.
Supervision: Dogan Uncu.
Validation: Selin Akturk Esen, Muge Buyukaksoy, Burak Civelek.
Visualization: Ismet Seven.
Writing – original draft: Selin Akturk Esen.
Writing – review & editing: Denizcan Hasturk.
Abbreviations:
- DLBCL
- diffuse large B-cell lymphoma
- ECOG PS
- Eastern Cooperative Oncology Group Performance Status
- NHL
- non-Hodgkin lymphoma
- OS
- overall survival
The study was conducted in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of Ankara Bilkent City Hospital (protocol number E1-22-2386 and approval date February 09, 2022).
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
The authors have no funding and conflicts of interest to disclose.
How to cite this article: Hasturk D, Akturk Esen S, Buyukaksoy M, Civelek B, Seven I, Uncu D. Primary colon lymphomas: An analysis of our experience over the last 18 years. Medicine 2024;103:19(e38013).
Contributor Information
Selin Akturk Esen, Email: drselin16@hotmail.com.
Muge Buyukaksoy, Email: mugebuyukaksoy@gmail.com.
Burak Civelek, Email: drburak@hotmail.com.
Ismet Seven, Email: sevenismet84@gmail.com.
Dogan Uncu, Email: doganuncu@yahoo.com.
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