Li Hui, Meng Lu, Wang Hongke, Cui Liang, Sheng Heyu, Zhao Peiyan, Hong Shuo, Du Xinhua, Yan Shi, Xing Yun, Feng Shicheng, Zhang Yan, Fang Huan, Bai Jing, Liu Yan, Lan Shaowei, Liu Tao, Guan Yanfang, Xia Xuefeng, Yi Xin, Cheng Ying
The Medical Oncology Translational Research Laboratory, Jilin Provincial Key Laboratory of Molecular Diagnostics for Lung Cancer, Jilin Cancer Hospital, No. 1066, Jinhu Road, Changchun, 130012, China.
Geneplus-Beijing Institute, 9th Floor, No. 6 Building, Peking University Medical Industrial Park, Zhongguancun Life Science Park, Beijing, 102206, China.
Brief Bioinform. 2024 Nov 22;26(1). doi: 10.1093/bib/bbae677.
Somatic variants play a crucial role in the occurrence and progression of cancer. However, in the absence of matched normal controls, distinguishing between germline and somatic variants becomes challenging in tumor samples. The existing tumor-only genomic analysis methods either suffer from limited performance or insufficient interpretability due to an excess of features. Therefore, there is an urgent need for an alternative approach that can address these issues and have practical implications. Here, we presented OncoTOP, a computational method for genomic analysis without matched normal samples, which can accurately distinguish somatic mutations from germline variants. Reference sample analysis revealed a 0% false positive rate and 99.7% reproducibility for variant calling. Assessing 2864 tumor samples across 18 cancer types yielded a 99.8% overall positive percent agreement and a 99.9% positive predictive value. OncoTOP can also accurately detect clinically actionable variants and subclonal mutations associated with drug resistance. For the prediction of mutation origins, the positive percent agreement stood at 97.4% for predicting somatic mutations and 95.7% for germline mutations. High consistency of tumor mutational burden (TMB) was observed between the results generated by OncoTOP and tumor-normal paired analysis. In a cohort of 97 lung cancer patients treated with immunotherapy, TMB-high patients had prolonged PFS (P = .02), proving the reliability of our approach in estimating TMB to predict therapy response. Furthermore, microsatellite instability status showed a strong concordance (97%) with polymerase chain reaction results, and leukocyte antigens class I subtypes and homozygosity achieved an impressive concordance rate of 99.3% and 99.9% respectively, compared to its tumor-normal paired analysis. Thus, OncoTOP exhibited high reliability in variant calling, mutation origin prediction, and biomarker estimation. Its application will promise substantial advantages for clinical genomic testing.
体细胞变异在癌症的发生和发展中起着至关重要的作用。然而,在缺乏匹配的正常对照的情况下,区分肿瘤样本中的种系变异和体细胞变异变得具有挑战性。现有的仅针对肿瘤的基因组分析方法要么由于特征过多而性能有限,要么解释性不足。因此,迫切需要一种能够解决这些问题并具有实际意义的替代方法。在此,我们提出了OncoTOP,一种无需匹配正常样本的基因组分析计算方法,它可以准确地区分体细胞突变和种系变异。参考样本分析显示变异检测的假阳性率为0%,重复性为99.7%。对18种癌症类型的2864个肿瘤样本进行评估,总体阳性百分比一致性为99.8%,阳性预测值为99.9%。OncoTOP还可以准确检测与耐药性相关的临床可操作变异和亚克隆突变。对于突变起源的预测,预测体细胞突变的阳性百分比一致性为97.4%,预测种系突变的为95.7%。OncoTOP生成的结果与肿瘤-正常配对分析生成的结果之间观察到肿瘤突变负荷(TMB)具有高度一致性。在一组接受免疫治疗的97例肺癌患者中,高TMB患者的无进展生存期延长(P = 0.02),证明了我们的方法在估计TMB以预测治疗反应方面的可靠性。此外,微卫星不稳定性状态与聚合酶链反应结果显示出很强的一致性(97%),与肿瘤-正常配对分析相比,白细胞抗原I类亚型和纯合性分别达到了令人印象深刻的99.3%和99.9%的一致性率。因此,OncoTOP在变异检测、突变起源预测和生物标志物估计方面表现出高度可靠性。其应用将为临床基因组检测带来实质性优势。