Clinicopathological Features, Treatment Strategy, and Prognosis of Primary Non-Hodgkin's Lymphoma of the Duodenum: A SEER Database Analysis.
The most predominant extranodal site in non-Hodgkin's lymphoma (NHL) is the gastrointestinal (GI) tract , accounting for 5% to 20% of all NHL cases and 30% to 45% of all extranodal cases . The lesion can occur in any part of the digestive tract from the mouth to the anus, of which stomach is the most common pathogenic sites (60%-75%) .
As primary duodenum lymphomas (PDLs) are exceedingly rare, the current researches about PDLs are based on anecdotal reports [4-23]. In the present study, we retrospectively reviewed the clinical and pathological manifestations of lymphomas of duodenum lymphoma for cases based on the largest sample size so far to identify prognostic factors and to clarify the value of treatment modalities in the management of these malignancies.
2. Materials and Methods
2.1. Data Source and Patient Selection. We queried the SEER database (SEER, 18 November 2017) with SEER Stat version 8.3.5 software to identify 14872 patients who were diagnosed with lymphoma from 1998 to 2015, including 1060 PDLs, 10573 primary gastric lymphomas (PGLs), and 3239 primary small intestinal lymphomas (PSILs). The codes used for lymphoma in the coding system of the International Classification of Diseases for Oncology (ICD-O)-3 were 9590-9729. The search was limited to adult patients ([greater than or equal to] 18 years old) with the type of follow-up equal to "active follow-up." The exclusion criteria were as follows: (i) patients without definitely histological confirmation; (ii) patients with only autopsy or death certificate records; (iii) patients with incomplete survival data and follow-up information; (iv) patients without Ann Arbor stage record; and (v) patients without the information of surgery. After screening, we got a total of 10321 patients.
Clinical and pathological variables (e.g., age, gender, race, sex, age at diagnosis, marital status, year of diagnosis, histological type, Ann Arbor stage, whole body symptom of lymphoma based on the AJCC (6th edition) staging system, treatment modalities employed and information of "cause of death and follow-up," and "multiple primary field") were extracted from the SEER.
Since the SEER cause-specific death classification variable is defined by taking into account cause of death in conjunction with sequence of tumor occurrence (ie, only one tumor or the first of multiple tumors) and comorbidities (e.g., AIDS and/or site-related diseases), we excluded the patients except that lymphoma was the only one primary cancer or the 1st cancer of 2 or more primaries to avoid the ambiguity of the lymphoma-specific survival .
The survival data were available in the measurement unit of months, without precise days. Considering the preconditions that no precise survival days were available and that patients with only autopsy or death certificate records were excluded, a survival time of 0 months was recorded as 0.5 months to include patients who died within 1 month of diagnosis but who did not reach the 1-month threshold [25,26].
Since this study only involves analysis of the publically available database (SEER) and does not contain any identifying patient information, the ethical approval of this study by the institutional review board (IRB) is not required.
2.2. Statistical Analyses. Statistical analyses were performed using the statistical software SPSS 22.0 for Apple (SPSS Inc., Chicago, IL). Numerical variables were expressed as mean [+ or -] SD and were analyzed by the t-test. Discrete variables were analyzed using the chi-square test or Fisher's exact test. Risk factors for survival were identified by univariate analysis, and COX regression was employed for multivariate analysis. Disease-specific survival (DSS) was analyzed by the Kaplan-Meier method and differences between the curves were compared using the log-rank test. All P values were two-sided, and P values < 0.05 were considered statistically significant.
3.1. Baseline Demographic Characteristics. Clinical and pathological features of primary duodenum lymphoma (PDL) are summarized in Table 1. In total, 1060 eligible PDL patients were recognized during the 18-year study period (between 1998 and 2015). There was no obvious sex trend: 604 were male and 456 were female. Age was from 7 to 99 years (median, 62 years; mean, 60.96 [+ or -] 15.205 years). Most patients were married (611; 57.65%) and white (878; 82.83%). 55.66% of the patients had clear symptoms, of which the symptoms of A were 463 (43.68%) and B were 127 (11.98%). Out of 1060 PDL specimens, follicular lymphoma (FL) was observed in 436 (41.13%) of them, and diffuse large B-cell lymphoma (DLBCL) in 348 of the tumor specimens (32.83%) was observed. The majority of patients (949, 89.85%) had single tumor, and only 111 (10.47%) patients had multiple tumors. Among 1060 patients, 92 underwent surgery alone or associated with conservative treatment (chemotherapy alone, radiotherapy alone, chemotherapy + radiotherapy, or Helicobacter pylori eradication only), and the other 968 received conservative treatment.
Next, clinical and pathological features of 1060 PDLs were compared with those of 10573 PGLs and 3239 PSILs (Table 2). The results showed that there were no significant differences in age, gender, marital status, race, and other cancers between the surgery and conservative groups. However, primary site, Ann Arbor staging, symptoms, and histological type were significantly different between the two groups (all P < 0.05); that is, incidence of cancers with I stage or A symptoms was significantly higher in the conservative group compared to that in the surgery group.
The results showed that age, gender, symptom, and histological type were significantly different between PDLs and PGLs (all P < 0.05); that is, incidence of tumors with younger patients or more follicular lymphoma was significantly higher in the PDL group compared to that in the PGL group. The PDL group also showed younger patients, earlier Ann Arbor staging, more follicular lymphoma, and more surgery treatment in comparison with those of the PSIL group (all P < 0.05).
3.2. Survival and Prognostic Factors. In order to analyze the prognosis among duodenum, gastric, and small intestinal lymphomas, survivals of 1060 PDLs were compared to those of 10573 PGLs and 3239 PSILs (Figure 1). The results showed that the DSS of PDLs were significantly better than those of PGLs and PSILs (10-year survival rate: 21.24% vs. 20.40%, P = 0.027; 10-year survival rate: 21.24% vs. 16.79%, P = 0.001).
Furthermore, univariate and multivariate analyses were performed to evaluate the prognosis of PDLs (Table 3). Age, gender, Ann Arbor staging, and histological type were regarded as independent prognostic factors for the DSS (all P < 0.05). Symptom was regarded as a significant risk factor for the DSS by univariate analysis (P = 0.002), while it is not an independent prognostic factor for DSS by multivariate analysis.
3.3. Stratified Analysis. We showed stratified analysis according to several prognostic variables based on multivariate analyses (Figure 2). Patients with <65 years, female, stage I, and FL were found to be significantly associated with good DSS. However, patients with >60 years, male, stage IV, and TCL were found to be significantly associated with poor DSS (all P < 0.05).
Figure 3 shows the changing trend of treatment modalities to PGL. The changing trends of treatment modalities to PDL were analyzed in 4 consecutive time periods: from 1998 to 2000 (period 1), from 2001 to 2005 (period 2), from 2006 to 2010 (period 3), and from 2011 to 2015 (period 4). The proportion of patients who received conservative treatment increased from 84.40% in period 2 to 94.74% in period 4, whereas patients who received surgical treatment gradually decreased from 15.60% in period 2 to 5.26% in period 4.
To the best of our knowledge, the current study represented the largest number of PDLs. In this study, we summarized clinical and pathological features of 1060 cases of PDLs. We further analyzed prognosis of PDLs in comparison with that of PDLs and PSILs. It was found that tumors with younger patients or more follicular lymphoma was significantly higher in PDLs. In addition, PDLs had poorer prognosis compared to PGLs and PSILs. These observations indicate that surgery treatment may not play a role in improving survival in patients as compared to conservative treatment. Since 2000, the proportion of PDL patients undergoing surgery has declined.
We know that follicular lymphoma (FL) is primarily a nodal disease and primary FL of the gastrointestinal (GI) tract is rare . However, the most common histological subtype is FL, followed by DLBCL among of PDLs . Our study showed that the proportion of FL was the highest (44.13%) and significantly higher than that of stomach (2.23%) and small intestine (22.97%). Therefore, the predominance of the follicular histology in PDL was interesting. The high proportion of follicular lymphoma in duodenal lymphoma might be an important reason why the prognosis was better than that of the stomach and small intestine.
Our study showed that the mean age (60.96 [+ or -] 15.205) of patients with PDL was younger than that of the stomach and small intestine, and that the proportion of stage I was also higher than that of the stomach and small intestine. The duodenal anatomy site is special, the tumor growth space is small, and the patient presents the discomfort symptom earlier than the stomach and small intestinal. At the same time, EUS can not only clarify the lesions on the mucosal surface of the gastrointestinal tract but also understand the changes in the hierarchical structure of the gastrointestinal wall and its relationship with adjacent tissues and organs. It might relate to lower age and tumor staging.
Based on the assumption that gastrointestinal tract lymphoma is a localised disease, the surgical treatment was traditionally considered the cornerstone of the therapeutical strategy showing impressive results in terms of long survival. Nowadays, this approach has been extensively revised, and the management of gastrointestinal tract lymphoma is centred on systemic treatments such as chemo- and radiotherapy. From the EER data, the proportion of patients undergoing surgery gradually decreased from 2000 to 2015. From our study, the treatment of PDLs was also in line with the current treatment trend, but interestingly, the proportion of PDLs treated by surgery was lower than that of the stomach (9.64%) and the small intestine (35.13%), among which it was significantly lower than that of the small intestine. The reason maybe that the duodenal lesion is mostly found in the descending segment [4-23], which has a complex anatomical structure and a small possibility of local resection, unlike the small intestine which can be directly resected, so conservative treatment is more preferred. Once a larger operation is performed, it is bound to cause complications and affect the quality of life. Meanwhile, multivariate analysis confirmed that the treatment modality was unrelated to DSS; that is, surgical treatment did not bring a survival advantage. The results were similar to previous reports (Table 4) [28-31] that the survival results of nonsurgical treatment were similar or even better than those of surgical treatment. Surgery, thus, is restricted to the treatment of complications such as occlusion, bleeding or perforation. Preventive surgery is sometimes advocated in bulky tumors, when rapid tumor necrosis secondary to chemo/radiotherapy may be associated with a high risk of life-threatening complications . Surgery is also required for removal of residual disease after medical debulking . Since the SEER database does not list the complications, this paper cannot discuss the complications.
Although there was no statistically significant difference in survival by treatment modalities in the multivariate analysis, there are other multiple factors that contribute to survival. In previous studies, female, low-grade histology and good PS have been reported to be associated with high OS. However, age >60 years, advanced stage, poor performance status (PS), and elevated lactic dehydrogenase (LDH) were associated with poor outcome [3, 32-34]. In our study, age, gender, Ann Arbor staging, and histological type retained independent prognostic factors in the multivariate analysis. Patients with <65 years, female, stage I, and FL were found to be significantly associated with good DSS. LDH and PS are not mentioned in the SEER database, so statistical analysis cannot be made in this paper.
Although it is an excellent resource for comparative outcome analysis for all malignancies involving the gastrointestinal tract, SEER has its limitations. Since the database provides passive follow-up for its registered cases, incomplete data reporting remains a problem. First, much information could not be obtained from the SEER database, such as PS and LDH. Second, the SEER database also did not describe postoperative complications and quality of life score, so we were unable to assess the complications and quality of life associated with surgery.
Abbreviations CHOP: cyclophosphamide, doxorubicin, vincristine, and prednisolone COPD: chronic obstructive pulmonary disease CVP: cyclophosphamide, vincristine, and prednisone D: died DLBCL: diffuse large B-cell lymphoma DSS: disease-specific survival ETCL: enteropathy-type T-cell lymphoma F: female FL: follicular lymphoma JGCA: Japanese Gastric Cancer Association L: live LDH: lactic dehydrogenase M: male MALT: mucosa-associated lymphoid tissue MCL: mantle cell lymphoma NHL: non-Hodgkin's lymphoma NR: no recurrence PDL: primary duodenum lymphoma PGIL: primary gastrointestinal PGLs: primary gastric lymphoma PS: performance status PSILs: primary small intestinal lymphoma R: recurrence R- rituximab with CHOP CHOP: SEER: Surveillance, Epidemiology, and End Results
No additional data are available.
Conflicts of Interest
The authors declare that they have no conflicts of interest to this work.
ZGL conceived the study and drafted the manuscript. WY and ZY participated in drafting the manuscript. ZZC designed and supervised the study. All authors contributed to the writing of the manuscript and provided final approval of the manuscript. All authors have read and approved the final version of this manuscript. All authors agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
The authors acknowledge the efforts of the Surveillance, Epidemiology, and End Results (SEER) Program tumor registries in the creation of the SEER database.
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Guoliang Zheng, Yue Wang, Yan Zhao, and Zhichao Zheng [ID]
Department of Gastric Surgery, Cancer Hospital of China Medical University (Liaoning Cancer Hospital and Institute), No. 44 Xiaoheyan Road, Dadong District, Shenyang, Liaoning 110042, China
Correspondence should be addressed to Zhichao Zheng; email@example.com
Received 27 June 2019; Accepted 26 December 2019; Published 13 January 2020
Academic Editor: Quirino Lai
Caption: Figure 1: Comparison of DSS among PDLs, PGLs, and PSILs. The results showed that the DSS of PDLs were significantly better than those of PGLs and PSILs (10-year survival rate: 21.24% vs. 20.40%, P = 0.027; 10-year survival rate: 21.24% vs. 16.79%, P = 0.001). PDLs vs. PGLs: P < 0.05; PDLs vs. PSILs: P < 0.05. PGL, primary gastric lymphoma; PSIL, primary small intestinal lymphoma; PDL, primary duodenum lymphoma.
Caption: Figure 2: The stratified analysis according to (a) age, (b) gender, (c) Ann Arbor staging, and (d) histological type in the PDLs. Patients with <65 years, female, stage I, and FL were found to be significantly associated with good DSS. However, patients with [greater than or equal to] 60 years, male, stage IV, and TCL were found to be significantly associated with poor DSS (all P < 0.05).
Caption: Figure 3: Trend of treatment modality (surgery vs. conservative treatment) to PGLs over the 18-year period from 1998 to 2015. The proportion of patients who received conservative treatment increased from 84.40% in period 2 to 94.74% in period 4, whereas patients who received surgical treatment gradually decreased from 15.60% in period 2 to 5.26% in period 4.
Table 1: Demographics and characteristics of PDLs. Clinicopathologic features Number of assessable patients (%) Age (years) Mean [+ or -] SD 60.96 [+ or -] 15.205 [greater than or equal to] 60 578 (54.53) <60 482 (45.47) Gender Male 604 (56.98) Female 456 (43.02) Marital status Married 611 (57.65) Unmarried 349 (32.92) Unknown 100 (9.43) Race White 878 (82.83) Black 69 (6.51) Others 93 (8.77) Unknown 20 (1.89) Ann Arbor staging I 564 (53.21) II 182 (17.17) III 40 (3.77) IV 173 (16.32) Unknown 101 (9.53) Symptoms A 463 (43.68) B 127 (11.98) Unknown 470 (44.34) Histological type DBCLC 348 (32.83) MALT 146 (13.77) T-cell 28 (2.64) FL 436 (41.13) MCL 29 (2.74) Unknown 73 (6.89) Combined with other cancers Yes 111 (10.47) No 949 (89.53) Treatment modality Only surgery 41 (3.87) Surgery + conservative 51 (4.81) Conservative 968 (91.32) DLBCL = diffuse large B-cell lymphoma; ETCL = T-cell lymphoma; FL = follicular lymphoma; MALT = mucosa-associated lymphoid tissue; MCL = mantle cell lymphoma. Table 2: Comparison of clinicopathological parameters among PSLs, PGLs, and PSILs. Clinicopathologic PDLs features n = 1060 Age (years) Mean [+ or -] SD 60.96 [+ or -] 15.205 [greater than or 578 (54.53) equal to] 60 <60 482 (45.47) Gender Male 604 (56.98) Female 456 (43.02) Ann Arbor staging I 564 (53.21) II 182 (17.17) III 40 (3.77) IV 173 (16.32) Unknown 101 (9.53) Symptoms A 463 (43.68) B 127 (11.98) Unknown 470 (44.34) Histological type DLBCL 348 (32.83) MALT 146 (13.77) T-cell 28 (2.64) FL 436 (41.13) MCL 29 (2.74) Unknown 73 (6.89) Treatment modality Only surgery 41 (3.87) Surgery + conservative 51 (4.81) Conservative 968 (91.32) Clinicopathologic PGLs features n =10573 P value Age (years) Mean [+ or -] SD 66.08 [+ or -] 14.957 <0.001 [greater than or 7205 (68.15) <0.001 equal to] 60 <60 3368 (31.85) Gender 0.016 Male 5617 (53.13) Female 4956 (46.87) Ann Arbor staging 0.071 I 5616 (53.12) II 1541 (14.58) III 482 (4.56) IV 1731 (16.37) Unknown 1203 (11.37) Symptoms <0.001 A 3260 (30.83) B 1313 (12.42) Unknown 6000 (56.75) Histological type <0.001 DLBCL 5168 (48.88) MALT 4323 (40.89) T-cell 78 (0.74) FL 236 (2.23) MCL 131 (1.24) Unknown 637 (6.02) Treatment modality 0.38 Only surgery 401 (3.79) Surgery + conservative 619 (5.85) Conservative 9553 (90.36) Clinicopathologic PSILs features n = 3239 P value Age (years) Mean [+ or -] SD 62.41 [+ or -] 16.779 0.013 [greater than or 1927 (59.49) 0.004 equal to] 60 <60 1312 (40.51) Gender 0.065 Male 1931 (59.62) Female 1308 (40.38) Ann Arbor staging <0.001 I 1239 (38.25) II 1047 (32.32) III 143 (4.41) IV 567 (17.52) Unknown 243 (7.50) Symptoms <0.001 A 1174 (36.25) B 432 (13.33) Unknown 1633 (50.42) Histological type <0.001 DLBCL 1778 (54.89) MALT 265 (8.18) T-cell 185 (5.71) FL 744 (22.97) MCL 51 (1.57) Unknown 216 (6.68) Treatment modality <0.001 Only surgery 928 (28.65) Surgery + conservative 1173 (36.22) Conservative 1138 (35.13) DLBCL = diffuse large B-cell lymphoma; ETCL = T-cell lymphoma; FL = follicular lymphoma; MALT = mucosa-associated lymphoid tissue; MCL = mantle cell lymphoma. Table 3: Univariate and multivariate analysis for DSS in the PGLs. Characteristics Univariate analysis HR 95% CI P value Age (years) 1.026 1.017-1.035 <0.001 Gender 0.636 0.491-0.824 0.001 Marital status 1.136 0.950-1.358 0.162 Symptom 1.239 1.083-1.417 0.002 Ann Arbor staging 1.189 1.099-1.286 <0.001 Histological type 0.696 0.638-0.759 <0.001 Combined with other cancers 0.724 0.483-1.087 0.119 Treatment modality 1.158 0.993-1.349 0.061 Characteristics Multivariate analysis HR 95% CI P value Age (years) 1.027 1.018-1.036 <0.001 Gender 0.633 0.487-0.823 0.001 Marital status Symptom Ann Arbor staging 1.202 1.107-1.306 <0.001 Histological type 0.718 0.656-0.786 <0.001 Combined with other cancers Treatment modality 1.034 0.906-1.182 0.618 Table 4: Previously reported cases of PDLs. Reference Num Age Sex Location Zheng et al.  1 58 M -- Linnik et al.  1 51 M -- Iwamuro et al.  2 52 M Descendant duodenum 96 F Descendant duodenum Mejia et al.  1 56 M Papilla Iwamuro 1 60 M Descendant et al.  duodenum Trivedi et al.  1 36 F Ampulla of Vater Tari et al.  1 66 F Ampulla of Vater Du et al.  1 65 M Descendant duodenum Cho et al.  1 68 M Duodenal bulb Kondo et al.  1 78 F Ampulla of Vater Nakase et al.  1 57 F Papilla Born et al.  1 75 F -- Woo et al.  1 71 F Descendant duodenum Chim et al.  1 73 M Ampulla of Vater Jabr  1 71 F Ampulla of Vater Zenda et al.  1 49 F Papilla Yildirim et al.  3 33 M Ampulla of Vater 24 M Ampulla of Vater 38 M Ampulla of Vater Isomoto et al.  1 46 M Ampulla of Vater Nadal et al.  1 55 M Ampulla of Vater Ventrucci et al.  1 65 F Ampulla of Vater Reference Type Stage Zheng et al.  MCL -- Linnik et al.  DLBCL -- Iwamuro et al.  FL IV FL IV Mejia et al.  FL -- Iwamuro FL IV et al.  Trivedi et al.  DLBCL -- Tari et al.  FL II2 Du et al.  DLBCL and TCL -- Cho et al.  MALT -- Kondo et al.  DLBCL -- Nakase et al.  FL I Born et al.  FL -- Woo et al.  MALT EII2 Chim et al.  DLBCL II1 Jabr  DLBCL -- Zenda et al.  FL I Yildirim et al.  DLBCL -- DLBCL -- DLBCL -- Isomoto et al.  MALT IE Nadal et al.  FL -- Ventrucci et al.  MALT -- Reference CD markers Surgery Zheng et al.  CD20, CD21, CD5, BCL-2 None Linnik et al.  CD20, CD45, BCL2, BCL6 None Iwamuro et al.  CD20, CD10, BCL2 -- CD20, CD10, BCL2 -- Mejia et al.  CD-20, CD10, BCL-2, BCL-6 None Iwamuro CD20, CD10, None et al.  BCL2 Trivedi et al.  CD20 YES Tari et al.  CD20, CD10, BCL-2 None Du et al.  CD20, CD3, CD45 YES Cho et al.  -- YES Kondo et al.  CD20, CD10, CD79a, BCL-2 YES Nakase et al.  CD10, Bcl-2 None Born et al.  -- None Woo et al.  CD20 None Chim et al.  CD20, BCL-6 None Jabr  CD20, CD10, CD45, BCL-2 None Zenda et al.  CD20, CD10, CD79a, BCL-2 None Yildirim et al.  CD20 None CD20, CD45 None CD20, LCA None Isomoto et al.  BCL-2 None Nadal et al.  CD10, Bcl-2 None Ventrucci et al.  CD20, CD79a, BCL-2 None Reference Conservation Zheng et al.  None Linnik et al.  Chemotherapy Iwamuro et al.  -- -- Mejia et al.  R Iwamuro Bendamustine et al.  and R Trivedi et al.  Chemotherapy Tari et al.  None Du et al.  R-CHOP Cho et al.  -- Kondo et al.  R-CHOP Nakase et al.  None Born et al.  None Woo et al.  CVP Chim et al.  CHOP Jabr  Chemotherapy Zenda et al.  R-CHOP Yildirim et al.  CHOP CHOEP CHOP Isomoto et al.  Radiation Nadal et al.  CHOP Ventrucci et al.  CVP Reference Follow-up Zheng et al.  -- Linnik et al.  60 mo/L Iwamuro et al.  -- -- Mejia et al.  -- Iwamuro -- et al.  Trivedi et al.  2 y/L Tari et al.  -- Du et al.  30 mo/R Cho et al.  -- Kondo et al.  19mo/NR Nakase et al.  1 mo/NR Born et al.  -- Woo et al.  1 y/NR Chim et al.  Died due to COPD Jabr  -- Zenda et al.  -- Yildirim et al.  1 y/NR Died due to sepsis and multiorgan failure Died due to suspected perforation Isomoto et al.  4 y/NR Nadal et al.  2 y/NR Ventrucci et al.  15mo/NR
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|Title Annotation:||Research Article|
|Author:||Zheng, Guoliang; Wang, Yue; Zhao, Yan; Zheng, Zhichao|
|Publication:||Canadian Journal of Gastroenterology and Hepatology|
|Date:||Jan 1, 2020|
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