Study on the relationship between TLS maturity in colon cancer tissues and clinical pathological characteristics as well as prognosis

doi:10.3877/cma.j.issn.1674-3946.2026.06.009

Abstract

Abstract:

Objective

To investigate the relationship between the maturity of tertiary lymphoid structures (TLS) in colon cancer tissues and clinical pathological features as well as prognosis.

Methods

The clinical data of 162 patients with colon cancer from January 2022 to January 2024 were retrospectively analyzed. The patients were divided into the TLS-positive group (n=124) and the TLS-negative group (n=38) based on the presence or absence of TLS in the tumor stroma. The TLS-positive group was further divided into the mature TLS (SFL-TLS) group (n=65) and the immature TLS (non-SFL-TLS) group (n=59) according to the histological morphology and functional structure integrity of TLS. Baseline data of the patients were collected, and the TLS structure was evaluated by histopathology and immunohistochemistry. Survival differences were analyzed using the Kaplan-Meier method and Log-Rank test. Independent factors affecting overall survival (OS) were analyzed using multivariate Cox proportional hazards regression.

Results

Before surgery, there was a statistically significant difference in the preoperative carcinoembryonic antigen (CEA) levels between the TLS-positive group and the TLS-negative group (P<0.05); there were statistically significant differences in microsatellite instability (MSI) status and extranodal lymph node invasion between the SFL-TLS group and the non-SFL-TLS group (P<0.05). The effector immune cells (CD8+ T cells, NK cells, CD8+ cytotoxic T cells, CD20+ B cells) and CXCL13 chemokine levels in the SFL-TLS group were significantly higher than those in the non-SFL-TLS group, while the inhibitory Treg cell levels were significantly lower than those in the non-SFL-TLS group (P<0.001); the 3-year OS of the TLS-positive group was 63.7% (79/124), and that of the TLS-negative group was 42.1% (16/38), with a statistically significant difference between the two groups (Log-Rank χ²=6.785, P=0.009); the 3-year OS of the SFL-TLS group was 76.9% (50/65), and that of the non-SFL-TLS group was 49.2% (29/59), with a statistically significant difference (Log-Rank χ²=10.422, P=0.001); Cox univariate analysis showed that the preoperative cancer antigen (CEA) level and extranodal lymph node invasion were risk factors for OS; the MSI status and maturity of TLS were protective factors for the overall survival of patients; multivariate Cox analysis further indicated that the preoperative CEA level (HR: 1.027, 95%CI: 1.000~1.055), extranodal lymph node invasion (HR: 2.583, 95%CI: 1.382~4.825) were independent risk factors for OS; the MSI status (HR: 0.452, 95%CI: 0.239~0.853), TLS maturity (HR: 0.372, 95%CI: 0.192~0.713) were independent protective factors for OS, while the TLS presence status did not show an independent prognostic impact.

Conclusion

The maturity of TLS is related to the high microsatellite instability status and is an independent protective factor for OS in patients with colon cancer, and it can be used as a potential biomarker for evaluating the prognosis of colon cancer patients.

Key words: Colonic Neoplasms, Tertiary Lymphoid Structures, Maturity, Clinicopathological Features, Prognosis

Jianxin Yang, Ninghua Yao, Feifei Zheng. Study on the relationship between TLS maturity in colon cancer tissues and clinical pathological characteristics as well as prognosis[J]. Chinese Journal of Operative Procedures of General Surgery(Electronic Edition), 2026, 20(06): 541-546.

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Figures/Tables 6

组别	例数	性别（例）		年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
组别	例数	男	女	年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
TLS阳性组	124	72	52	60.3±7.5	23.2±3.2	4.3±1.2
TLS阴性组	38	22	16	62.5±8.2	23.8±2.8	4.5±1.2
统计值		χ²=0.003		t=1.544	t=1.033	t=0.977
P值		0.955		0.125	0.303	0.330
组别	TNM分期（例）		肿瘤部位（例）		淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
组别	Ⅰ~Ⅱ	Ⅲ	左半	右半	淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
TLS阳性组	55	69	62	62	1.8±1.3	43.9±9.8	12.3±8.7
TLS阴性组	15	23	22	16	2.3±1.5	45.2±10.3	18.5±10.2
统计值	χ²=2.003		χ²=0.726		t=1.883	t=0.730	t=3.687
P值	0.157		0.394		0.062	0.466	<0.001

组别	例数	性别（例）		年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
组别	例数	男	女	年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
TLS阳性组	124	72	52	60.3±7.5	23.2±3.2	4.3±1.2
TLS阴性组	38	22	16	62.5±8.2	23.8±2.8	4.5±1.2
统计值		χ²=0.003		t=1.544	t=1.033	t=0.977
P值		0.955		0.125	0.303	0.330
组别	TNM分期（例）		肿瘤部位（例）		淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
组别	Ⅰ~Ⅱ	Ⅲ	左半	右半	淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
TLS阳性组	55	69	62	62	1.8±1.3	43.9±9.8	12.3±8.7
TLS阴性组	15	23	22	16	2.3±1.5	45.2±10.3	18.5±10.2
统计值	χ²=2.003		χ²=0.726		t=1.883	t=0.730	t=3.687
P值	0.157		0.394		0.062	0.466	<0.001

组别	例数	性别（例）		年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
组别	例数	男	女	年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
SFL-TLS组	65	36	29	60.2±7.4	23.2±3.0	4.3±1.1
非SFL-TLS组	59	34	25	60.4±7.7	23.2±3.3	4.3±1.2
统计值		χ²=0.063		t=0.141	t=0.071	t=0.097
P值		0.801		0.889	0.944	0.923
组别	TNM分期（例）		肿瘤部位（例）		淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
组别	Ⅰ~Ⅱ	Ⅲ	左半	右半	淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
SFL-TLS组	29	36	26	39	1.8±1.3	43.8±9.6	12.3±8.6
非SFL-TLS组	33	26	32	27	1.8±1.4	43.9±10.0	12.4±8.8
统计值	χ²=1.584		χ²=2.518		t=0.171	t=0.063	t=0.064
P值	0.280		0.113		0.864	0.950	0.949

组别	例数	性别（例）		年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
组别	例数	男	女	年龄（岁， $x ¯$ ±s）	BMI（kg/m²， $x ¯$ ±s）	肿瘤最大径（cm， $x ¯$ ±s）
SFL-TLS组	65	36	29	60.2±7.4	23.2±3.0	4.3±1.1
非SFL-TLS组	59	34	25	60.4±7.7	23.2±3.3	4.3±1.2
统计值		χ²=0.063		t=0.141	t=0.071	t=0.097
P值		0.801		0.889	0.944	0.923
组别	TNM分期（例）		肿瘤部位（例）		淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
组别	Ⅰ~Ⅱ	Ⅲ	左半	右半	淋巴结转移数（枚， $x ¯$ ±s）	Ki-67指数（%， $x ¯$ ±s）	术前CEA水平（ng/ml， $x ¯$ ±s）
SFL-TLS组	29	36	26	39	1.8±1.3	43.8±9.6	12.3±8.6
非SFL-TLS组	33	26	32	27	1.8±1.4	43.9±10.0	12.4±8.8
统计值	χ²=1.584		χ²=2.518		t=0.171	t=0.063	t=0.064
P值	0.280		0.113		0.864	0.950	0.949

因素	分类	SFL-TLS组（n=65）	非SFL-TLS组（n=59）	统计值	P值
组织学类型[例（%）]	腺癌	58(89.2)	52(88.1)	χ²=0.037	0.848
组织学类型[例（%）]	黏液腺癌/印戒细胞癌	7(10.8)	7(11.9)	χ²=0.037	0.848
分化程度[例（%）]	高/中分化	56(86.2)	48(81.4)	χ²=0.526	0.468
分化程度[例（%）]	低分化/未分化	9(13.8)	11(18.6)	χ²=0.526	0.468
脉管浸润[例（%）]	有	16(24.6)	22(37.3)	χ²=2.337	0.126
脉管浸润[例（%）]	无	49(75.4)	37(62.7)	χ²=2.337	0.126
肿瘤出芽[例（%）]	低级别	45(69.2)	38(64.4)	χ²=0.325	0.569
肿瘤出芽[例（%）]	高级别	20(30.8)	21(35.6)	χ²=0.325	0.569
神经侵犯[例（%）]	有	18(27.7)	25(42.4)	χ²=2.943	0.086
神经侵犯[例（%）]	无	47(72.3)	34(57.6)	χ²=2.943	0.086
肿瘤浸润深度[例（%）]	T₁~T₂	28(43.1)	28(47.5)	χ²=0.240	0.624
肿瘤浸润深度[例（%）]	T₃~T₄	37(56.9)	31(52.5)	χ²=0.240	0.624
淋巴结包膜外侵犯[例（%）]	有	10(15.4)	28(47.5)	χ²=14.969	<0.001
淋巴结包膜外侵犯[例（%）]	无	55(84.6)	31(52.5)	χ²=14.969	<0.001
MSI状态[例（%）]	MSS/MSI-L MSI-H	40(61.5) 25(38.5)	52(88.1) 7(11.9)	χ²=11.427	<0.001
CD8+T细胞比例（%， $x ¯$ ±s）		30.3±3.9	22.2±4.2	t=9.872	<0.001
NK细胞比例（%， $x ¯$ ±s）		15.7±3.0	11.3±3.1	t=7.985	<0.001
Treg细胞比例（%， $x ¯$ ±s）		5.1±1.1	7.9±1.3	t=12.354	<0.001
CD8+细胞毒性T细胞(个/高倍视野， $x ¯$ ±s)		0.7±0.2	0.4±0.1	t=14.256	<0.001
CD20+B细胞(个/高倍视野， $x ¯$ ±s)		0.7±0.1	0.4±0.1	t=15.897	<0.001
CXCL13趋化因子相对表达量（ $x ¯$ ±s）		0.9±0.2	0.4±0.1	t=16.982	<0.001

因素	分类	SFL-TLS组（n=65）	非SFL-TLS组（n=59）	统计值	P值
组织学类型[例（%）]	腺癌	58(89.2)	52(88.1)	χ²=0.037	0.848
组织学类型[例（%）]	黏液腺癌/印戒细胞癌	7(10.8)	7(11.9)	χ²=0.037	0.848
分化程度[例（%）]	高/中分化	56(86.2)	48(81.4)	χ²=0.526	0.468
分化程度[例（%）]	低分化/未分化	9(13.8)	11(18.6)	χ²=0.526	0.468
脉管浸润[例（%）]	有	16(24.6)	22(37.3)	χ²=2.337	0.126
脉管浸润[例（%）]	无	49(75.4)	37(62.7)	χ²=2.337	0.126
肿瘤出芽[例（%）]	低级别	45(69.2)	38(64.4)	χ²=0.325	0.569
肿瘤出芽[例（%）]	高级别	20(30.8)	21(35.6)	χ²=0.325	0.569
神经侵犯[例（%）]	有	18(27.7)	25(42.4)	χ²=2.943	0.086
神经侵犯[例（%）]	无	47(72.3)	34(57.6)	χ²=2.943	0.086
肿瘤浸润深度[例（%）]	T₁~T₂	28(43.1)	28(47.5)	χ²=0.240	0.624
肿瘤浸润深度[例（%）]	T₃~T₄	37(56.9)	31(52.5)	χ²=0.240	0.624
淋巴结包膜外侵犯[例（%）]	有	10(15.4)	28(47.5)	χ²=14.969	<0.001
淋巴结包膜外侵犯[例（%）]	无	55(84.6)	31(52.5)	χ²=14.969	<0.001
MSI状态[例（%）]	MSS/MSI-L MSI-H	40(61.5) 25(38.5)	52(88.1) 7(11.9)	χ²=11.427	<0.001
CD8+T细胞比例（%， $x ¯$ ±s）		30.3±3.9	22.2±4.2	t=9.872	<0.001
NK细胞比例（%， $x ¯$ ±s）		15.7±3.0	11.3±3.1	t=7.985	<0.001
Treg细胞比例（%， $x ¯$ ±s）		5.1±1.1	7.9±1.3	t=12.354	<0.001
CD8+细胞毒性T细胞(个/高倍视野， $x ¯$ ±s)		0.7±0.2	0.4±0.1	t=14.256	<0.001
CD20+B细胞(个/高倍视野， $x ¯$ ±s)		0.7±0.1	0.4±0.1	t=15.897	<0.001
CXCL13趋化因子相对表达量（ $x ¯$ ±s）		0.9±0.2	0.4±0.1	t=16.982	<0.001

因素	赋值	单因素Cox		多因素Cox
因素	赋值	HR （95%置信区间）	P值	HR （95%置信区间）	P值
术前CEA水平（ng/ml）	实测值	1.032(1.006~1.059)	0.008	1.027(1.000~1.055)	0.042
MSI状态	MSS/MSI-L=1；MSI-H=2	0.423(0.228~0.788)	0.007	0.452(0.239~0.853)	0.014
淋巴结包膜外侵犯	无=1；有=2	2.852(1.563~5.205)	0.010	2.583(1.382~4.825)	0.003
TLS存在状态	TLS阴性=1；TLS阳性=2	0.532(0.312~0.913)	0.022	0.612(0.342~1.093)	0.093
TLS成熟度	TLS阴性=1；TLS阳性-非SFL=2；TLS阳性-SFL=3	0.382(0.212~0.693)	0.002	0.372(0.192~0.713)	0.003

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