Tumor Budding as a Risk Factor for Lymph Node Metastasis and Local Recurrence in pT1 Colorectal Cancer: A Systematic Review and Meta-Analysis

Gastro hep advances Pub Date : 2025-01-01 DOI:10.1016/j.gastha.2025.100713

Heng Zhang , Femke Simmer , Alessandro Lugli , Iris D. Nagtegaal

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Abstract

Background and Aims

Implementation of population screening programs resulted in an increase in early colorectal cancer (CRC, pT1). For these small CRC, endoscopic local resection is the preferred treatment. However, the presence of lymph node metastasis (LNM) and risk of local recurrence might require additional surgery. Tumor budding (TB) is a well-known biomarker for adverse outcomes in pT1 CRC. This study aims to further explore the relationship between TB and in pT1 CRC and to clarify the relationship between TB and local recurrence, to provide more strategies for the selection of surgical treatment.

Methods

A systematic review was conducted using the MEDLINE and EMBASE databases to investigate the relationship between TB and LNM and local recurrence in pT1 CRC. Meta-analysis based on a random-effects model was performed to evaluate the relationship between TB and these 2 factors.

Results

A total of 57 observational studies were included in the meta-analysis, with a total of 24,956 patients. High-grade TB was significantly associated with both LNM (risk ratio (RR) = 4.04, 95% confidence interval (CI), 3.52–4.64, I² = 56.11%, P < .001) and local recurrence (RR = 2.35, 95% CI, 1.21–4.54, I² = 26.18%, P = .01). Sensitivity analysis confirmed the robustness of our pooled results. Subgroup analysis also explored possible sources of heterogeneity. For LNM, geographical location (Asia: RR = 4.22, 95% CI, 3.64–4.89; Others: RR = 2.72, 95% CI, 2.08–3.57, P = .01) and year of publication (<2015: RR = 4.96, 95% CI, 4.01–6.15; ≥2015: RR = 3.58, 95% CI, 2.99–4.29, P = .02) showed significant differences in the subgroup analysis. We cannot rule out publication bias for LNM risk.

Conclusion

Our findings confirm that TB is a strong predictor of local recurrence, but in particular of LNM in pT1 CRC and offers effective guidance for selecting further surgical treatment strategies.

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肿瘤出芽是pT1期结直肠癌淋巴结转移和局部复发的危险因素：一项系统综述和荟萃分析

背景与目的人群筛查项目的实施导致早期结直肠癌（CRC, pT1）的增加。对于这些小的结直肠癌，内镜下局部切除是首选的治疗方法。然而，淋巴结转移（LNM）的存在和局部复发的风险可能需要额外的手术。肿瘤出芽（TB）是pT1型结直肠癌不良结局的一个众所周知的生物标志物。本研究旨在进一步探讨结核与pT1期结直肠癌的关系，明确结核与局部复发的关系，为手术治疗的选择提供更多的策略。方法采用MEDLINE和EMBASE数据库进行系统评价，探讨结核和LNM与pT1期结直肠癌局部复发的关系。采用随机效应模型进行meta分析，评价结核与这两个因素之间的关系。结果meta分析共纳入57项观察性研究，共纳入24,956例患者。高级别结核病与LNM均显著相关(风险比(RR) = 4.04, 95%可信区间（CI）， 3.52 ~ 4.64, I2 = 56.11%, P <；.001)和局部复发率（RR = 2.35, 95% CI, 1.21 ~ 4.54, I2 = 26.18%, P = 0.01）。敏感性分析证实了合并结果的稳健性。亚组分析还探讨了异质性的可能来源。对于LNM，地理位置(亚洲：RR = 4.22, 95% CI, 3.64-4.89；其他：RR = 2.72, 95% CI, 2.08-3.57, P = 0.01)和发表年份(<2015: RR = 4.96, 95% CI, 4.01-6.15；≥2015:RR = 3.58, 95% CI, 2.99 ~ 4.29, P = 0.02)在亚组分析中有显著性差异。我们不能排除LNM风险的发表偏倚。结论我们的研究结果证实，结核病是局部复发的一个强有力的预测因子，尤其是pT1 CRC的LNM，并为选择进一步的手术治疗策略提供了有效的指导。

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