原发性胃淋巴瘤的内镜特征分析及疗效预测

doi:10.19723/j.issn.1671-167X.2026.02.019

摘要/Abstract

摘要：

目的: 系统总结北京大学第三医院原发性胃淋巴瘤(primary gastric lymphoma, PGL)患者的内镜特征，探索基于补体受体2/B细胞淋巴瘤-6蛋白(complement receptor type 2/B-cell lymphoma 6 protein, CD21/BCL6)的淋巴滤泡破坏程度分级在胃黏膜相关淋巴组织(mucosa associated lymphoid tissue, MALT)淋巴瘤根除幽门螺杆菌(Helicobacter pylori, Hp)疗效中的预测价值。方法: 连续选择2010年1月至2025年1月北京大学第三医院确诊的100例PGL患者的病例资料进行回顾性分析，按病理类型分为惰性与侵袭性两组，比较其临床及内镜特征；采用Kaplan-Meier法绘制生存曲线并以Log-rank检验比较总生存率(overall survival, OS)和无进展生存率(progression free survival, PFS)；另外选择同期根除Hp疗效明确的25例胃MALT淋巴瘤患者初诊活检标本行CD21/BCL6免疫组化染色并进行G0~G4分级，比较根除有效/无效亚组分级差异，并通过Logistic回归分析根除无效相关因素。结果: 共纳入100例PGL患者，平均年龄63.0(55.8, 71.0)岁，男性47例，女性53例；侵袭性组的B症状发生率高于惰性组(49.0% vs. 19.6%, P=0.004)。内镜方面，侵袭性组以溃疡型/混合型为主(P < 0.001)，糜烂(98.0% vs. 49.0%, P < 0.001)、溃疡/白苔(96.0% vs. 37.3%, P < 0.001)、病灶“质脆”(47.0% vs. 11.9%, P < 0.001)、出血倾向(P=0.008)、胃腔狭窄(38.8% vs. 0, P < 0.001)及蠕动差(49.0% vs. 9.8%, P < 0.001)更常见；生存分析显示侵袭性组OS与PFS均劣于惰性组(OS: P=0.009；PFS: P=0.003)。在25例胃MALT淋巴瘤亚队列中，无效组Hp阴性比例更高(P=0.049)，且淋巴滤泡破坏程度分级显著高于有效组(P=0.015)；多因素Logistic回归提示破坏程度分级与根除无效独立相关(AOR=3.63，95%CI: 1.14~11.58，P=0.021)，Hp感染状态未见独立相关(P=0.240)。结论: PGL内镜表现具有显著异质性，溃疡型/混合型、病灶脆性、出血倾向、腔狭窄及蠕动差更提示侵袭性淋巴瘤，并且与较差生存相关；在胃MALT淋巴瘤中，初诊活检基于CD21/BCL6的淋巴滤泡破坏程度分级可用于早期识别根除Hp无效高风险人群，为分层治疗与随访决策提供依据。

关键词: 原发性胃淋巴瘤, 内镜特征, MALT淋巴瘤, 幽门螺杆菌根除疗效, 淋巴滤泡破坏程度分级

Abstract:

Objective: Primary gastric lymphoma (PGL) is a rare form of lymphoma that arises within the gastric mucosa-associated lymphoid tissue (MALT), often linked to Helicobacter pylori (Hp) infection. The endoscopic features of PGL are heterogeneous, and understanding these characteristics could help distinguish between different lymphoma subtypes. This study aims to systematically assess the endoscopic features of PGL and explore the role of complement receptor type 2/B-cell lymphoma 6 protein (CD21/BCL6)-based grading of lymphoid follicular disruption in predicting the effectiveness of Hp eradication (HPE) treatment in gastric MALT lymphoma. Methods: A retrospective study was conducted involving 100 patients diagnosed with PGL at Peking University Third Hospital between January 2010 and January 2025. Patients were divided into two groups based on histopathological findings: indolent and aggressive lymphoma. The clinical and endoscopic characteristics of these two groups were compared. Survival analysis, including overall survival (OS) and progression-free survival (PFS), was performed using Kaplan-Meier curves and Log-rank tests. A subgroup of 25 patients with gastric MALT lymphoma and known HPE outcomes was selected for further analysis. Diagnostic biopsies were immunohistochemically stained with CD21 and BCL6 and graded from G0 to G4 based on follicular disruption. Logistic regression analysis was used to identify factors associated with HPE failure. Results: Among the 100 patients, the average age was 63.0 (55.8, 71.0) years, with 47 men and 53 women. Aggressive lymphoma showed a significantly higher incidence of B symptoms compared with indolent lymphoma (49.0% vs. 19.6%, P= 0.004). Endoscopically, aggressive lymphoma presented more frequently with ulcerative or mixed morphologies (P < 0.001) and exhibited higher rates of mucosal erosion, ulceration with white slough, lesion friability, bleeding tendency, gastric stenosis, and impaired peristalsis (P < 0.001 for all). Aggressive lymphoma also had significantly worse OS and PFS (OS: P=0.009; PFS: P=0.003). In the subgroup of 25 MALT lymphoma patients, those with ineffective HPE were more likely to be Hp-negative (P=0.049) and had a significantly higher degree of follicular disruption (P=0.015). Multivariable Logistic regression revealed that follicular disruption grading was independently associated with HPE failure (AOR=3.63, 95%CI: 1.14-11.58, P=0.021), while Hp infection status was not (P=0.240). Conclusion: PGL demonstrates considerable variability in its endoscopic presentation. Features, such as ulcerative/mixed morphology, friability, bleeding tendency, stenosis, and impaired peristalsis are indicative of more aggressive disease and correlate with poorer survival outcomes. The CD21/BCL6-based grading of lymphoid follicular disruption provides a valuable tool for identifying patients at high risk of HPE failure, supporting early intervention and risk stratification for gastric MALT lymphoma treatment.

Key words: Primary gastric lymphoma, Endoscopic features, Mucosa-associated lymphoid tissue (MALT) lymphoma, Helicobacter pylori eradication response, Lymphoid follicular disruption grading

中图分类号:

R735.2

魏竞尧, 叶菊香, 周美玲, 付伟伟, 刘鑫, 翟康乐, 石岩岩, 丁士刚, 张静. 原发性胃淋巴瘤的内镜特征分析及疗效预测[J]. 北京大学学报（医学版）, 2026, 58(2): 342-350.

Jingyao WEI, Juxiang YE, Meiling ZHOU, Weiwei FU, Xin LIU, Kangle ZHAI, Yanyan SHI, Shigang DING, Jing ZHANG. Endoscopic characteristics of primary gastric lymphoma and prediction of treatment response[J]. Journal of Peking University (Health Sciences), 2026, 58(2): 342-350.

图/表 9

图1

表1

表2

图2

表3

100例PGL患者的内镜结果"

Indicator	Indolent lymphoma (n=51)	Aggressive lymphoma (n=49)	P
Lesion location^b			0.104
Cardia	0 (0.0)	1 (1.2)
Fundus	7 (8.8)	5 (6.0)
Upper gastric body	18 (22.5)	9 (10.8)
Middle gastric body	22 (27.5)	19 (22.9)
Lower gastric body	22 (27.5)	27 (32.5)
Antrum	11 (13.7)	22 (26.6)
Lesion orientation			0.103
Anterior wall	13 (25.5)	8 (16.3)
Posterior wall	6 (11.8)	9 (18.4)
Lesser curvature	7 (13.7)	15 (30.6)
Greater curvature	25 (49.0)	17 (34.7)
Gross morphology			< 0.001
Ulcerative type	11 (21.6)	35 (71.4)
Infiltrative type	12 (23.5)	0 (0.0)
Nodular type	19 (37.3)	1 (2.0)
Polypoid type	4 (7.8)	1 (2.0)
Mixed type	5 (9.8)	12 (24.6)
Number of lesions			0.568
Solitary	19 (37.3)	21 (42.9)
Multiple	32 (62.7)	28 (57.1)
Long diameter/cm^c			0.178^a
＜1	7 (23.3)	4 (12.9)
1-＜3	16 (53.4)	13 (41.9)
≥3	7 (23.3)	14 (45.2)
Short diameter/cm^c			0.131^a
＜1	11 (36.7)	8 (25.8)
1-＜3	15 (50.0)	12 (38.7)
≥3	4 (13.3)	11 (35.5)
Erosion			< 0.001
Absent	26 (51.0)	1 (2.0)
Present	25 (49.0)	48 (98.0)
Ulceration/white slough			< 0.001
Absent	32 (62.7)	2 (4.0)
Present	19 (37.3)	47 (96.0)
Consistency			< 0.001
Soft	32 (62.7)	8 (16.3)
Hard	4 (7.8)	5 (10.2)
Tough/firm	9 (17.6)	13 (26.5)
Brittle	6 (11.9)	23 (47.0)
Bleeding			0.008
Active bleeding	4 (7.8)	9 (18.4)
Easy bleeding on biopsy	40 (78.4)	40 (81.6)
Not prone to bleeding	7 (13.8)	0 (0.0)
Perilesional mucosa			0.550
Normal mucosa	1 (2.0)	0 (0.0)
Erythema/edema	21 (41.2)	16 (32.7)
Converging folds	6 (11.8)	5 (10.2)
Uneven mucosa	23 (45.0)	28 (57.1)
Background mucosa			0.259
Normal mucosa	4 (7.8)	2 (4.1)
Erythema/edema	5 (9.8)	5 (10.2)
Mottled mucosa	32 (62.7)	24 (49.0)
Uneven mucosa	10 (19.7)	18 (36.7)
Gastric lumen			< 0.001
Patent	51 (100.0)	30 (61.2)
Stenosis	0 (0.0)	19 (38.8)
Peristalsis			< 0.001
Good	46 (90.2)	25 (51.0)
Poor	5 (9.8)	24 (49.0)

表3

表4

图3

图4

表5

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Grade	Name	Histomorphological features
G0	Architecture-intact type	A continuous, dense CD21 meshwork surrounds a well-defined BCL6-positive germinal center; The follicular contour is intact, with no disruption
G1	Marginal thinning/eccentric type	The CD21 meshwork remains continuous but shows peripheral “crescent-shaped” condensation toward the outer margin or focal thinning; The germinal center remains intact
G2	Disrupted with preserved outline type	The CD21 meshwork shows breaks and/or gaps; The follicular outline is still preserved. Features suggestive of tumor cell “follicular colonization” are present (BCL6-positive areas are intercalated by non-germinal-center cells)
G3	Outline-loss type	The follicular contour is indistinct or largely lost; Only scattered fragmentary CD21 meshwork persists, and BCL6-positive germinal-center cells are no longer detectable
G4	Absent/disintegrated type	The CD21 meshwork is almost completely unrecognizable/absent; Germinal centers are lost, or only rare scattered BCL6-positive cells are seen

Indicator	Indolent lymphoma (n=51)	Aggressive lymphoma (n=49)	P
Gender			0.680
Male	25 (49.0)	22 (44.9)
Female	26 (51.0)	27 (55.1)
Age/years
Male	63.52±8.71^a	60.68±14.34^a	0.410
Female	59.88±12.90^a	65.26±11.84^a	0.120
Presenting symptoms			0.137
Abdominal pain	13 (25.5)	22 (44.9)
Abdominal distension	8 (15.7)	5 (10.2)
Acid reflux/heartburn	3 (5.9)	3 (6.1)
Nausea/vomiting	4 (7.8)	4 (8.2)
Hematemesis/melena	8 (15.7)	10 (20.4)
Asymptomatic	15 (29.4)	5 (10.2)
Hypertension			0.790
No	32 (62.7)	32 (65.3)
Yes	19 (37.3)	17 (34.7)
Diabetes mellitus			0.716
No	44 (86.3)	41 (83.7)
Yes	7 (13.7)	8 (16.3)
Smoking			0.722
No	38 (74.5)	38 (77.6)
Yes	13 (25.5)	11 (22.4)
Alcohol consumption			0.315
No	41 (80.4)	43 (87.8)
Yes	10 (19.6)	6 (12.2)
B symptoms			0.004
No	40 (80.4)	25 (51.0)
Yes	11 (19.6)	24 (49.0)

Indicator	Indolent lymphoma (n=51)	Aggressive lymphoma (n=49)	P
Lugano classification			< 0.001^a
Stage Ⅰ	37 (72.5)	8 (16.3)
Stage Ⅱ	9 (17.6)	9 (18.4)
Stage Ⅲ	0 (0.0)	2 (4.1)
Stage Ⅳ	5 (9.9)	30 (61.2)
Therapeutic regimen			< 0.001
Untreated	6 (11.8)	4 (8.2)
HPE only	16 (31.4)	0 (0.0)
Radiotherapy/chemotherapy/surgery	7 (13.7)	42 (85.7)
HPE+Radiotherapy/chemotherapy	22 (43.1)	3 (6.1)
Follow-up effect			0.007
Remission after treatment	31 (60.7)	30 (61.2)
Residual/ineffective	8 (15.7)	1 (2.0)
Progress/death	6 (11.8)	16 (32.7)
Untreated and alive	6 (11.8)	2 (4.1)

Indicator	HPE effective (n=10)	HPE ineffective (n=15)	P
Gender			0.099
Male	2 (20.0)	9 (60.0)
Female	8 (80.0)	6 (40.0)
Age/years	61.1 (52.8, 68.0)	62.9 (59.0, 69.0)	0.453
Hypertension			>0.999
No	6 (60.0)	9 (60.0)
Yes	4 (40.0)	6 (40.0)
Diabetes mellitus			>0.999
No	8 (80.0)	13 (86.7)
Yes	2 (20.0)	2 (13.3)
Smoking			0.179
No	9 (90.0)	9 (60.0)
Yes	1 (10.0)	6 (40.0)
Alcohol			0.615
No	9 (90.0)	11 (73.3)
Yes	1 (10.0)	4 (26.7)
B symptoms			0.499
No	7 (70.0)	13 (86.7)
Yes	3 (30.0)	2 (13.3)
Lesion orientation			>0.999
Anterior wall	2 (20.0)	2 (13.3)
Posterior wall	1 (10.0)	1 (6.7)
Lesser curvature	2 (20.0)	3 (20.0)
Greater curvature	5 (50.0)	9 (60.0)
Gross morphology			0.912
Ulcerative type	1 (10.0)	2 (13.3)
Infiltrative type	2 (20.0)	2 (13.3)
Nodular type	6 (60.0)	8 (53.5)
Polypoid type	0 (0.0)	2 (13.3)
Mixed type	1 (10.0)	1 (6.7)
Number of lesions			>0.999
Solitary	3 (30.0)	5 (33.3)
Multiple	7 (70.0)	10 (66.7)
Erosion			>0.999
Absent	6 (60.0)	9 (60.0)
Present	4 (40.0)	6 (40.0)
Ulceration			>0.999
Absent	7 (70.0)	11 (73.3)
Present	3 (30.0)	4 (26.7)
Consistency			0.510
Soft	5 (50.0)	11 (73.3)
Hard	1 (10.0)	0 (0.0)
Tough	1 (10.0)	2 (13.3)
Brittle	3 (30.0)	2 (13.3)
Peristalsis			0.400
Good	9 (90.0)	15 (100.0)
Poor	1 (10.0)	0 (0.0)
Hp infection status			0.049
Positive	7 (70.0)	4 (26.7)
Negative	3 (30.0)	11 (73.3)
Disruption grading			0.015
G0	3 (30.0)	0 (0.0)
G1	1 (10.0)	0 (0.0)
G2	4 (40.0)	3 (20.0)
G3	0 (0.0)	8 (53.3)
G4	2 (20.0)	4 (26.7)

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