Insights Through the Endoscope: A Retrospective Study Unraveling the Macroscopic Features of Primary Colorectal Lymphoma

Abstract

Introduction: Primary colorectal lymphoma (PCL) is a very rare disease with limited information regarding its macroscopic features. This retrospective descriptive study aims to identify the macroscopic characteristics of PCL and explore treatment trends and outcomes with respect to histopathologic subtypes. Methods: This IRB-approved study from a large academic medical center identified 66 patients with colorectal lymphoma from 1998 to 2022 from a tumor registry. Thirty-four patients met the inclusion criteria of having PCL with available endoscopic data. The macroscopic features of each lesion were identified. Treatment trends and outcomes were examined at the patient level. Data were described using frequency and percentages for categorical characteristics and the median and interquatile range (IQR) for continuous outcomes. Results: A total of 77 PCL lesions were identified. Most were identified on screening or surveillance colonoscopies or colonoscopies performed after abnormal imaging (61.8%). Diffuse large B cell lymphoma (DLBCL) had the highest prevalence (N = 24), followed by follicular lymphoma (n = 21), mantle cell (n = 16), mucosa-associated lymphoid tissue (MALT) (n = 14), then Burkitt’s (n = 2). More mantle cell (93.8%) and follicular (90.5%) lymphomas were sessile. More MALT lymphomas were ulcerated (71.4%). A higher proportion of follicular (76.2%) and mantle cell (71.4%) lymphomas were diminutive (≤5 mm). More MALT (78.6%), DLBCL (75.0%), and Burkitt’s (100%) were large (≥20 mm). More lesions were found in the sigmoid colon (26.0%), followed by the rectum (22.1%), transverse colon (18.2%), cecum (18.2%), descending colon (10.4%), and ascending colon (5.2%). Overall, most underwent immunotherapy (61.3%) and did not have radiation therapy (81.3%), endoscopic resection (75.0%), and surgery (68.8%). Patients with DLBCL demonstrated higher rates of chemotherapy (70.6%), immunotherapy (87.5%), and remission after intervention (52.9%). Conclusions: Primary colorectal lymphomas display distinct macroscopic features and appear in different locations depending on the histopathologic subtype. Most cases are identified at early stages on screening colonoscopies and demonstrate a 75% two-year survival rate.

1. Introduction

Lymphomas are hematological malignancies with various histological subtypes and a broad spectrum of clinical behavior, aggressiveness, and prognosis. Non-Hodgkin lymphoma (NHL) is the seventh most common cancer in the United States, and Hodgkin lymphoma is the 27th most common [1]. Up to 40% of lymphoma cases can have extranodal metastases, with the gastrointestinal tract as the most common target [2]. Gastrointestinal tract lymphomas account for approximately 10–15% of all non-Hodgkin lymphomas [2]. Primary colorectal lymphomas (PCLs) are even rarer and account for only 0.2–0.6% of all colorectal malignancies and 15–20% of primary gastrointestinal lymphomas [3]. The incidence of PCL increased steadily from the 1970s to 2005 but has since been annually trending downward [4,5]. The survival outcome has increased over the past forty years, independent of age, marital status, pathological subtype, staging, or treatment modalities [4,5].

PCL is typically diagnosed on surveillance or routine colonoscopy and has an indolent course [6]. Its clinical presentation also varies from asymptomatic to vague symptoms such as diffuse abdominal pain to severe with intussusception. Diagnosis with colonoscopy and biopsy is the gold standard [7]. Limited existing studies have suggested various macroscopic features, including polypoid, ulcerative, multiple lymphomatous polyposes, diffuse, and mixed, as well as the location [8,9,10,11]. The common histological subtypes include mantle cell lymphoma, Burkitt lymphoma, follicular lymphoma, and diffuse large B cell lymphoma [11].

The current literature on PCL is limited primarily due to its rarity. This retrospective descriptive study aims to identify these characteristics and explore treatment trends and outcomes with respect to histopathologic subtypes.

2. Results

A total of 66 adult patients with colorectal lymphoma were extracted from the tumor registry. A total of 77 PCL lesions were identified from 34 patients meeting the inclusion criteria (Figure 1). Thirty-three patients had synchronous lesions, and one patient had both synchronous and metachronous lesions. Most were identified on screening or surveillance colonoscopies or colonoscopies performed after abnormal imaging (61.8%). All imaging modalities were computed tomography (CT) scans. Four abdominal CT scans were performed for abdominal pain, one abdominal CT scan for chronic diarrhea, one abdominal CT scan for weight loss, fatigue, and supraclavicular lymphadenopathy, and one lung CT scan for shortness of breath. Diffuse large B cell lymphoma (DLBCL) had the highest prevalence (n = 24), followed by follicular lymphoma (n = 21), mantle cell (n = 16), mucosa-associated lymphoid tissue (MALT) (n = 14), then Burkitt’s (n = 2). More cases of mantle cell lymphoma (93.8%) and follicular lymphoma (90.5%) were sessile (Table 1; Figure 1). More cases of MALT lymphoma were ulcerated (71.4%) (Figure 2). A higher proportion of follicular (76.2%) and mantle cell (71.4%) lymphoma were diminutive (≤5 mm). More MALT (78.6%), DLBCL (75.0%), and Burkitt’s (100%) were large (≥20 mm). More lesions were found in the sigmoid colon (26.0%), followed by the rectum (22.1%), transverse colon (18.2%), cecum (18.2%), descending colon (10.4%), and ascending colon (5.2%).

Most cases were identified at early stages on screening colonoscopies (41.2%), followed by colonoscopies due to symptoms (32.4%), abnormal imaging (20.6%), or positive stool DNA-based screening tests (5.9%) (Table 2). Most lymphomas were caught early in stages I and II (75%) rather than the late stage (25%). Most patients underwent some form of intervention following diagnosis rather than surveillance (78.1% vs. 21.9%). Most patients underwent immunotherapy (61.3%) and did not have radiation therapy (81.3%), endoscopic resection (75.0%), and surgery (68.8%). Patients with DLBCL demonstrated higher rates of chemotherapy (70.6%), immunotherapy (87.5%), and remission after intervention (52.9%). Following the initial intervention or surveillance, most patients entered remission (48.5%), while others progressed (39.4%), were stable (6.1%), or relapsed (6.1%). Most cancers were under surveillance at one- and two-year follow-ups (71.9% vs. 65.6%) with 82.2% and 75% survival rates, respectively. Three patients (9.4%) were undergoing active therapy at one- and two-year follow-ups.

3. Materials and Methods

This was an IRB-approved study from a large academic medical center. We retrospectively collected data from the tumor registry of patients aged ≥18 who were diagnosed with colorectal lymphoma between 1998 and 2022. Additional inclusion criteria included the diagnosis of primary colorectal lymphoma and the availability of endoscopic data for manual review; macroscopic features of each lesion were identified, including size, location, and Paris polyp classification. Treatment trends and outcomes were examined at the patient level. One patient was counted twice due to the diagnosis of a different histopathologic subtype on separate surveillance colonoscopies. Data were described using frequency and percentages for categorical characteristics and the median and interquartile range (IQR) for continuous outcomes. Analyses were conducted in SAS Enterprise Guide v8.3.

4. Discussion

Largely due to its rarity, much of the known information about PCL is synthesized from collections of smaller retrospective studies, case reports, or case series. As expected, due to the known indolent course of PCL, most lesions were detected through routine screening or surveillance colonoscopies. Approximately one-third of the lesions in our study were found because of active symptoms. The clinical presentation of PCL varies, with the most common presenting symptoms being abdominal pain, anorexia, nausea, diarrhea, night sweats, a palpable abdominal mass, and/or weight loss [7,12]. In rare instances, hematochezia, intussusception, or bowel obstruction may prompt the investigation and eventual diagnosis of PCL [7]. The average age of diagnosis is 55, with a 2:1 male-to-female ratio [13]. While the etiology and risk factors for PCL are unknown, it is reasonable to suspect that the risk factors of extra-gastrointestinal tract lymphomas may be similar. These include a family history of lymphoma, previous personal radiation exposure, exposure to certain infectious agents (Epstein–Barr virus, human T cell leukemia virus type 1, hepatitis C virus, human herpesvirus 8, etc.), drugs (phenytoin, digoxin, tumor necrosis factor (TNF) antagonists, etc.), autoimmune conditions (Sjogren syndrome, rheumatoid arthritis, Hashimoto thyroiditis, etc.), or congenital immunodeficiency diseases (Wiskott–Aldrich syndrome, severe combined immunodeficiency disease, etc.) [14].

Abnormal imaging prompted the colonoscopy that identified PCL lesions in approximately 20% of our cases. CT and double-contrast barium enemas (DCBEs) are the most employed imaging modalities for the workup of colorectal malignancies; however, they are often unnecessary, as tissue specimens are required for diagnosis [15,16]. A retrospective study recently evaluated the usefulness of DCBEs and CT in diagnosing PCL against its histological subtypes [15]. The diagnostic accuracy of PCL with CT was 26.3% and improved to 33.3% when combined with DCBEs [15]. The imaging features of PCL on DCBEs were subtle and non-specific but included giant mucosal rugae, superficial submucosal filling defects, and changing lesion forms with compression on fluoroscopy [15]. Concentric wall thickening and regional lymphadenopathy were the common CT imaging features [15]. While this study suggests that imaging may be useful in staging PCL, its role in diagnosis is limited, as colonoscopy with biopsies is the gold standard [15].

Limited information regarding the macroscopic characteristics of PCL lesions is available during colonoscopy. Polypoid types located in the cecum or ileocecal region have been most commonly described, occurring in 30–60% of patients [8,17]. Overall, the PCL lesions in our study were more likely to be large, sessile, and located in the sigmoid colon and rectal regions in contrast to the literature. Our retrospective study is one of the few to analyze the macroscopic features of PCL by histopathological subtypes, while most other studies focus on features and outcomes of one major subtype [8,9,17]. DLBCL had the highest prevalence in our study, followed by follicular lymphoma, mantle cell lymphoma, MALT lymphoma, and Burkitt’s. A similar retrospective study by Yachida et al., which consisted of 117 PCL lesions, also found DLBCL to be the most prevalent [8]. Our study found more mantle cell and follicular lymphomas to be sessile, while more MALT lymphomas were ulcerated. Yachida et al. determined polypoid types to be most common in DLBCL, mantle cell lymphoma, and MALT lymphoma (56%), whereas follicular lymphoma was macroscopically variant [8]. The differences in our data compared to Yachida et al. are likely due to small sample sizes; however, more studies are needed to determine if other factors affect the macroscopic characteristics of PCL lesions. Larger studies are also required to determine the macroscopic feature likelihoods for each histopathological subtype.

Our study is also unique in that we collected data on intervention trends and outcomes for each histopathological subtype. Most PCL lesions were identified in stages I or II, regardless of histopathological subtype. Chemotherapy and immunotherapy were the primary treatment modalities, while approximately one-third underwent surgical intervention. DLBCL lesions were more likely to be treated with chemotherapy and immunotherapy and enter remission following intervention. Most cancers were under surveillance at one- and two-year follow-ups (71.9% vs. 65.6%) with 82.2% and 75% survival rates, respectively. A meta-analysis by Lightner et al. found that most patients undergo surgery followed by adjuvant chemotherapy, a trend not observed in our study [17]. A large propensity score-matched retrospective analysis from the Surveillance, Epidemiology, and End Results (SEER) database by Zhang et al. found chemotherapy plus surgery to significantly improve overall survival and cancer-specific survival compared to chemotherapy alone [18]. However, a larger proportion of their cohort had more advanced stages (Ann Arbor stage III or IV) compared to our study.

A recent multicenter retrospective cohort study found the overall 5-year survival of PCL to be 58.4%, which was higher for rectal (61.0%) than colonic tumors (57.8%). A better prognosis was noted with age <70 years, female sex, and right-sided tumors. Aggressive histological subtypes and stage III or IV found on presentation were associated with worse survival. However, a limitation of this study was the lack of subgroup analysis by treatment modality, including chemotherapy, surgery, or surveillance [19]. Another recent retrospective cohort study suggested that marginal zone lymphoma has the longest median survival rate (164 months) of all histopathological subtypes and that DLBCL has the shortest, with only 70 months. Survival rates of those with right-sided disease, left-sided disease, and rectal disease were 117, 82, and 149 months, respectively. Younger married patients and those who underwent combination surgery, radiotherapy, and chemotherapy also showed better survival rates [3].

4.1. Limitations

Our study had several limitations. First, the rarity of the disease significantly limited our sample size. Based on the limited numbers, clinically relevant relationships between histopathological subtypes and the location, size, and macroscopic classification of the lesions are limited. However, this information may be useful for systematic reviews and meta-analyses to draw more conclusions. Second, information regarding the types of immunotherapy, chemotherapy, and radiotherapy was not collected largely based on the availability of information and was outside of the scope of this project. Further studies could address how PCL responds to different therapies compared to secondary colorectal lymphomas to determine optimal therapeutic strategies. Thirdly, the retrospective nature of this study may be prone to recall or misclassification biases. Prospective studies are needed to infer likelihood ratios between subtypes and macroscopic findings or outcomes.

4.2. Future Directions

Primary colorectal lymphomas display distinct macroscopic features and appear in different locations depending on the histopathologic subtype. The identification of common macroscopic features by subtype could aid in early recognition during routine colonoscopy. In addition, our findings support the value of screening colonoscopies for early detection, as most cases are identified at early stages with screening colonoscopies and highlight the importance of biopsies for definitive diagnosis.

To the best of our knowledge, no randomized controlled trials or clinical trials exist comparing treatment approaches and modalities and their efficacies in patients with primary colorectal lymphoma. Its rarity likely precludes a single-institution study and necessitates multicenter collaboration and coordination to pool a large enough cohort to achieve adequate study power. Large meta-analyses are needed to draw correlations between the macroscopic features and location tendencies of each histopathologic subtype. Furthermore, randomized controlled trials are needed to compare the efficacy of different treatment approaches and their respective survival rates. Studies assessing the molecular and/or genetic characterization of the subtypes could also be investigated. Finally, cost-effectiveness analyses could be employed for different treatment strategies.

4.3. Conclusions

Primary colorectal lymphomas display distinct macroscopic features and appear in different locations depending on the histopathologic subtype. The identification of common macroscopic features by subtype could aid in early recognition during routine colonoscopy. Our findings also support the value of screening colonoscopies for early detection, as most cases are identified at early stages with screening colonoscopies and exhibit a 75% two-year survival, highlighting the importance of biopsies for definitive diagnosis. While more studies are needed to determine the optimal treatment strategy, there may be potential for less aggressive approaches in select cases with chemotherapy/immunotherapy as the primary treatment.

Author Contributions

Conceptualization, J.J.G., B.C. and D.E.D.; methodology, J.J.G., B.C. and D.E.D.; formal analysis, J.J.G., B.C., S.M.N., I.U. and D.E.D.; investigation, J.J.G., B.C. and D.E.D.; data curation, J.J.G., B.C., S.M.N., I.U. and D.E.D.; writing—original draft preparation, J.J.G., B.C. and D.E.D.; writing—review and editing, J.J.G., B.C. and D.E.D.; visualization, J.J.G.; supervision, D.E.D. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Review Board (or Ethics Committee) of Geisinger Health System (protocol code #2023-1653; approval date 25 October 2024).

Informed Consent Statement

Patient consent was waived due to the retrospective study design.

Data Availability Statement

The original contributions presented in this study are included in the article. Further inquiries can be directed to the corresponding author(s).

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Figures and Tables

Table 1

Macroscopic description of lesions by histopathological subtype.

		Histopathological Subtype
	Overalln = 77	MALT lymphoman = 14	Follicular lymphoman = 21	Mantle cell lymphoman = 16	Diffuse large B cell lymphoman = 24	Burkitt’s lymphoman = 2
Macroscopic Classification, N (%)
Pedunculated	2 (2.6%)	0 (0%)	0 (0%)	0 (0%)	2 (8.3%)	0 (0%)
Sessile	40 (51.9%)	3 (21.4%)	19 (90.5%)	15 (93.8%)	3 (12.5%)	0 (0%)
Minimally elevated	0 (0%)	(0%)	(0%)	(0%)	(0%)	(0%)
Truly flat	1 (1.3%)	(0%)	1 (4.8%)	(0%)	(0%)	(0%)
Minimally depressed	0 (0%)	(0%)	(0%)	(0%)	(0%)	(0%)
Ulcerated	16 (20.8%)	10 (71.4%)	1 (4.8%)	(0%)	5 (20.8%)	(0%)
Mass	18 (23.4%)	1 (7.1%)	(0%)	1 (6.3%)	14 (58.3%)	2 (100%)
Size, N (%)
Diminutive	28 (41.2%)	2 (14.3%)	16 (76.2%)	5 (71.4%)	5 (20.8%)	0 (0%)
Small	4 (5.9%)	0 (0%)	3 (14.3%)	1 (14.3%)	0 (0%)	0 (0%)
Intermediate	3 (4.4%)	1 (7.1%)	1 (4.8%)	0 (0%)	1 (4.2%)	0 (0%)
Large	33 (48.5%)	11 (78.6%)	1 (4.8%)	1 (14.3%)	18 (75.0%)	2 (100%)
Location, N (%)
Ileocecal valve	0 (0%)	0 (0%)	0 (0%)	0 (0%)	0 (0%)	0 (0%)
Cecum	14 (18.2%)	0 (0%)	6 (28.6%)	2 (12.5%)	5 (20.8%)	1 (50.0%)
Ascending colon	4 (5.2%)	1 (7.1%)	0 (0%)	0 (0%)	3 (12.5%)	0 (0%)
Transverse colon	14 (18.2%)	4 (28.6%)	3 (14.3%)	2 (12.5%)	5 (20.8%)	0 (0%)
Descending colon	8 (10.4%)	3 (21.4%)	3 (14.3%)	1 (6.3%)	1 (4.2%)	0 (0%)
Sigmoid colon	20 (26.0%)	4 (28.6%)	5 (23.8%)	2 (12.5%)	8 (33.3%)	1 (50.0%)
Rectum	17 (22.1%)	2 (14.3%)	4 (19.0%)	9 (56.3%)	2 (8.3%)	0 (0%)

Table 2

Primary colorectal lymphoma outcomes.

		Histopathological Subtype
	Overall	MALT lymphoma	Follicular lymphoma	Mantle cell lymphoma	DLBCL	Burkitt’s lymphoma
	(n = 34)	(n = 7)	(n = 5)	(n = 2)	(n = 18)	(n = 2)
Disease after intervention, n (%)
Remission	16 (48.5%)	4 (57.1%)	2 (40.0%)	0 (0%)	9 (52.9%)	1 (50.0%)
Relapse	2 (6.1%)	0 (0%)	0 (0%)	1 (50.0%)	1 (5.9%)	0 (0%)
Progression	13 (39.4%)	2 (28.6%)	3 (60.0%)	1 (50.0%)	6 (35.3%)	1 (50.0%)
Stable	2 (6.1%)	1 (14.3%)	0 (0%)	0 (0%)	1 (5.9%)	0 (0%)
Missing	1	0	0	0	1	0
Treatment strategies
Surveillance, n (%)	7 (21.9%)	3 (50.0%)	3 (60.0%)	1 (50.0%)	0 (0%)	0 (0%)
Missing	2	1	0	0	1	0
Chemotherapy, n (%)	16 (50.0%)	0 (0%)	1 (20.0%)	1 (50.0%)	12 (70.6%)	2 (100.0%)
Missing	2	1	0	0	1	0
Radiation, n (%)	6 (18.8%)	1 (16.7%)	0 (0%)	1 (50.0%)	4 (23.5%)	0 (0%)
Missing	2	1	0	0	1	0
Immunotherapy, n (%)	19 (61.3%)	2 (33.3%)	1 (20.0%)	1 (50.0%)	14 (87.5%)	1 (50.0%)
Missing	3	1	0	0	2	0
Endoscopic Resection, n (%)	8 (25.0%)	2 (33.3%)	3 (60.0%)	2 (100.0%)	1 (5.9%)	0 (0%)
Missing	2	1	0	0	1	0
Surgery, n (%)	10 (31.3%)	2 (33.3%)	0 (0%)	0 (0%)	7 (41.2%)	1 (50.0%)
Missing	2	1	0	0	1	0
One-year outcome, n (%)
Surveillance	23 (71.9%)	6 (100.0%)	4 (80.0%)	1 (50.0%)	11 (64.7%)	1 (50.0%)
Active therapy	3 (9.4%)	0 (0%)	1 (20.0%)	1 (50.0%)	1 (5.9%)	0 (0%)
Hospice/death	6 (18.8%)	0 (0%)	0 (0%)	0 (0%)	5 (29.4%)	1 (50.0%)
Missing	2	1	0	0	1	0
Two-year outcome, n (%)
Surveillance	21 (65.6%)	6 (100.0%)	4 (80.0%)	1 (50.0%)	9 (52.9%)	1 (50.0%)
Active therapy	3 (9.4%)	0 (0%)	1 (20.0%)	1 (50.0%)	1 (5.9%)	0 (0%)
Hospice/death	8 (25.0%)	0 (0%)	0 (0%)	0 (0%)	7 (41.2%)	1 (50.0%)
Missing	2	1	0	0	1	0
Status, n (%)
Alive	19 (55.9%)	5 (71.4%)	4 (80.0%)	2 (100.0%)	7 (38.9%)	1 (50.0%)
Deceased	15 (44.1%)	2 (28.6%)	1 (20.0%)	0 (0%)	11 (61.1%)	1 (50.0%)
Stage at diagnosis, n (%)
IAE	2 (6.3%)	0 (0%)	0 (0%)	1 (50.0%)	1 (5.9%)	0 (0%)
IE	17 (53.1%)	5 (83.3%)	2 (40.0%)	1 (50.0%)	7 (41.2%)	2 (100.0%)
IIE	5 (15.6%)	0 (0%)	2 (40.0%)	0 (0%)	3 (17.6%)	0 (0%)
III	3 (9.4%)	0 (0%)	0 (0%)	0 (0%)	3 (17.6%)	0 (0%)
IV	3 (9.4%)	0 (0%)	1 (20.0%)	0 (0%)	2 (11.8%)	0 (0%)
IVAE	1 (3.1%)	1 (16.7%)	0 (0%)	0 (0%)	0 (0%)	0 (0%)
IVB	1 (3.1%)	0 (0%)	0 (0%)	0 (0%)	1 (5.9%)	0 (0%)
Missing	2	1	0	0	1	0
Colonoscopy referral indication, n (%)
Screening/surveillance	14 (41.2%)	4 (57.1%)	4 (80.0%)	1 (50.0%)	5 (27.8%)	0 (0%)
Symptoms	11 (32.4%)	2 (28.6%)	0 (0%)	0 (0%)	8 (44.4%)	1 (50.0%)
Abnormal imaging	7 (20.6%)	1 (14.3%)	0 (0%)	0 (0%)	5 (27.8%)	1 (50.0%)
Positive DNA-based CRC screening test	2 (5.9%)	0 (0%)	1 (20.0%)	1 (50.0%)	0 (0%)	0 (0%)
Observational time
Median (IQR)	55.0 (36.0, 95.0)	77.0 (55.0, 111.0)	56.0 (54.0, 89.0)	52.5 (51.0, 54.0)	39.5 (7.0, 76.0)	225.0 (225.0, 225.0)
Missing	1	0	0	0	0	1

References

1. SEER*Explorer: An Interactive Website for SEER Cancer Statistics [Internet]. Surveillance Research Program, National Cancer Institute. 17 April 2024; Available online: https://Seer.cancer.gov/statistics-network/explorer/ (accessed on 25 April 2024).

2. Alvarez-Lesmes, J.; Chapman, J.R.; Cassidy, D.; Zhou, Y.; Garcia-Buitrago, M.; Montgomery, E.A.; Lossos, I.S.; Sussman, D.; Poveda, J. Gastrointestinal tract lymphomas: A review of the most commonly encountered lymphomas. Arch. Pathol. Lab. Med.; 2021; 145, pp. 1585-1596. [DOI: https://dx.doi.org/10.5858/arpa.2020-0661-RA] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33836528]

3. Chen, Q.; Feng, Y.; Yang, J.; Li, R. Development and validation of a population-based prognostic nomogram for primary colorectal lymphoma patients. Front. Oncol.; 2022; 12, 991560. [DOI: https://dx.doi.org/10.3389/fonc.2022.991560] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/36353557]

4. Zhao, F.; Huang, L.; Chen, J.; Mei, S.; Wang, Z.; Wei, F.; Li, J.; Xiao, T.; Zhao, W.; Liu, Q. Incidence, survival of primary colorectal lymphoma over 40 years and a nomogram based on SEER database and independent validation. Res. Sq.; 2022; preprint [DOI: https://dx.doi.org/10.21203/rs.3.rs-1707515/v1]

5. Li, Q.; Mo, S.; Dai, W.; Li, Y.; Xu, Y.; Li, X.; Cai, G.; Cai, S. Changes in incidence and survival by decade of patients with primary colorectal lymphoma: A SEER analysis. Front. Public Health; 2020; 8, 486401. [DOI: https://dx.doi.org/10.3389/fpubh.2020.486401] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/33178655]

6. Gay, N.D.; Chen, A.; Okada, C.Y. Colorectal lymphoma: A review. Clin. Colon Rectal Surg.; 2018; 31, pp. 309-316. [DOI: https://dx.doi.org/10.1055/s-0038-1642048] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30186053]

7. Freedman, A.S. Clinical presentation and diagnosis of primary gastrointestinal lymphomas. UpToDate; post-TW ed. Wolters Kluwer: Alphen aan den Rhein, The Netherlands, 2011; Available online: https://www.uptodate.com/contents/clinical-presentation-and-diagnosis-of-primary-gastrointestinal-lymphomas (accessed on 25 April 2024).

8. Yachida, T.; Matsuda, T.; Sakamoto, T.; Nakajima, T.; Kakugawa, Y.; Maeshima, A.M.; Taniguchi, H.; Kushima, R.; Tobinai, K.; Kobara, H. et al. Endoscopic features of colorectal lymphoma according to histological type. JGH Open; 2022; 6, pp. 257-262. [DOI: https://dx.doi.org/10.1002/jgh3.12738] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/35475204]

9. Iwamuro, M.; Okada, H.; Takata, K.; Takenaka, R.; Inaba, T.; Mizuno, M.; Kobashi, H.; Tanaka, S.; Yoshioka, M.; Kondo, E. et al. Colorectal manifestation of follicular lymphoma. Intern. Med.; 2016; 55, pp. 1-8. [DOI: https://dx.doi.org/10.2169/internalmedicine.55.5393] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26726078]

10. Ghai, S.; Pattison, J.; Ghai, S.; O’Malley, M.E.; Khalili, K.; Stephens, M. Primary gastrointestinal lymphoma: Spectrum of imaging findings with pathologic correlation. Radiographics; 2007; 27, pp. 1371-1388. [DOI: https://dx.doi.org/10.1148/rg.275065151] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/17848697]

11. Mendelson, R.M.; Fermoyle, S. Primary gastrointestinal lymphomas: A radiological–pathological review. part 1: Stomach, oesophagus and colon. Australas. Radiol.; 2005; 49, pp. 353-364. [DOI: https://dx.doi.org/10.1111/j.1440-1673.2005.01457.x] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/16174173]

12. Fan, C.-W.; Changchien, C.R.; Wang, J.-Y.; Chen, J.-S.; Hsu, K.-C.; Tang, R.; Chiang, J.-M. Primary colorectal lymphoma. Dis. Colon Rectum; 2000; 43, pp. 1277-1282. [DOI: https://dx.doi.org/10.1007/BF02237436] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/11005497]

13. Porter, M.G.; Stoeger, S.M. Atypical colorectal neoplasms. Surg. Clin.; 2017; 97, pp. 641-656. [DOI: https://dx.doi.org/10.1016/j.suc.2017.01.011] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/28501252]

14. Sapkota, S.; Shaikh, H. Non-hodgkin lymphoma [updated 24 February 2023]. StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2024.

15. Li, M.; Zhang, L.; Liang, X.; Huang, W.T.; Ma, J.W.; Wan, Y.; Wu, N. Primary colorectal lymphoma: Computed tomography and double-contrast barium enema examination findings with histopathological correlation in 19 patients. Ann. Transl. Med.; 2019; 7, 308. [DOI: https://dx.doi.org/10.21037/atm.2019.06.32] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/31475178]

16. Green, B.; Raman, S. Colorectal lymphoma. Semin. Colon Rectal Surg.; 2015; 26, pp. 64-67. [DOI: https://dx.doi.org/10.1053/j.scrs.2015.01.003]

17. Lightner, A.L.; Shannon, E.; Gibbons, M.M.; Russell, M.M. Primary gastrointestinal non-hodgkin’s lymphoma of the small and large intestines: A systematic review. J. Gastrointest. Surg.; 2016; 20, pp. 827-839. [DOI: https://dx.doi.org/10.1007/s11605-015-3052-4] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/26676930]

18. Zhang, C.; Zhang, X.; Liu, Z.; Tao, J.; Lin, L.; Zhai, L. The impact of surgery on long-term survival of patients with primary intestinal non-hodgkin lymphomas based on SEER database. Sci. Rep.; 2021; 11, 23047. [DOI: https://dx.doi.org/10.1038/s41598-021-02597-1] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/34845308]

19. Hangge, P.; Calderon, E.; Habermann, E.; Glasgow, A.; Mishra, N. Primary colorectal lymphoma: Institutional experience and review of a national database. Dis. Colon Rectum; 2019; 62, pp. 1167-1176. [DOI: https://dx.doi.org/10.1097/DCR.0000000000001279] [PubMed: https://www.ncbi.nlm.nih.gov/pubmed/30489325]