Deep learning-based prediction of lymph node metastasis and occult tumor cells in gastric cancer using histopathological images: a retrospective study

Machine Learning


  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71:209–49.

    PubMed 

    Google Scholar 

  • Siegel RL, Miller KD, Wagle NS, Jemal A. Cancer statistics, 2023. CA Cancer J Clin. 2023;73:17–48.

    PubMed 

    Google Scholar 

  • Ajani JA, D’Amico TA, Bentrem DJ, Chao J, Cooke D, Corvera C, et al. Gastric cancer, Version 2.2022, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2022;20:167–92.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Shi RL, Chen Q, Ding JB, Yang Z, Pan G, Jiang D, et al. Increased number of negative lymph nodes is associated with improved survival outcome in node positive gastric cancer following radical gastrectomy. Oncotarget. 2016;7:35084–91.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sano T, Coit DG, Kim HH, Roviello F, Kassab P, Wittekind C, et al. Proposal of a new stage grouping of gastric cancer for TNM classification: International Gastric Cancer Association staging project. Gastric Cancer. 2017;20:217–25.

    Article 
    PubMed 

    Google Scholar 

  • de Burlet KJ, van den Hout MFCM, Putter H, Smit VTHBM, Hartgrink HH. Total number of lymph nodes in oncologic resections, is there more to be found? J Gastrointest Surg. 2015;19:943–8.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Seeruttun SR, Xu L, Wang F, Yi X, Fang C, Liu Z, et al. A homogenized approach to classify advanced gastric cancer patients with limited and adequate number of pathologically examined lymph nodes. Cancer Commun (Lond). 2019;39:32.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Arigami T, Uenosono Y, Yanagita S, Nakajo A, Ishigami S, Okumura H, et al. Clinical significance of lymph node micrometastasis in gastric cancer. Ann Surg Oncol. 2013;20:515–21.

    Article 
    PubMed 

    Google Scholar 

  • Lee CM, Cho JM, Jang YJ, Park SS, Park SH, Kim SJ, et al. Should lymph node micrometastasis be considered in node staging for gastric cancer? the significance of lymph node micrometastasis in gastric cancer. Ann Surg Oncol. 2015;22:765–71.

    Article 
    PubMed 

    Google Scholar 

  • Sekiguchi M, Oda I, Taniguchi H, Suzuki H, Morita S, Fukagawa T, et al. Risk stratification and predictive risk-scoring model for lymph node metastasis in early gastric cancer. J Gastroenterol. 2016;51:961–70.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Li Y, Wang D, Li Y, Liu X, Chen D, Yuan C, et al. Clinical significance of lymph node micrometastasis in pN0 gastric cancer patients. Gastroenterol Res Pract. 2021;2021:6854646.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Wang X, Yang X, Cai F, Cai M, Liu Y, Zhang L, et al. The key role of tumor budding in predicting the status of lymph node involvement in early gastric cancer patients: a clinical multicenter validation in China. Ann Surg Oncol. 2024;31:4224–35.

    Article 
    PubMed 

    Google Scholar 

  • Kim JY, Kim CH, Lee Y, Lee JH, Chae YS. Tumour infiltrating lymphocytes are predictors of lymph node metastasis in early gastric cancers. Pathology. 2017;49:589–95.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Chen D, Chen G, Jiang W, Fu M, Liu W, Sui J, et al. Association of the collagen signature in the tumor microenvironment with lymph node metastasis in early gastric cancer. JAMA Surg. 2019;154:e185249.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kather JN, Pearson AT, Halama N, Jäger D, Krause J, Loosen SH, et al. Deep learning can predict microsatellite instability directly from histology in gastrointestinal cancer. Nat Med. 2019;25:1054–6.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Huang B, Tian S, Zhan N, Ma J, Huang Z, Zhang C, et al. Accurate diagnosis and prognosis prediction of gastric cancer using deep learning on digital pathological images: a retrospective multicentre study. EBiomedicine. 2021;73:103631.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zheng X, Wang R, Zhang X, Sun Y, Zhang H, Zhao Z, et al. A deep learning model and human-machine fusion for prediction of EBV-associated gastric cancer from histopathology. Nat Commun. 2022;13:2790.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Flinner N, Gretser S, Quaas A, Bankov K, Stoll A, Heckmann LE, et al. Deep learning based on hematoxylin-eosin staining outperforms immunohistochemistry in predicting molecular subtypes of gastric adenocarcinoma. J Pathol. 2022;257:218–26.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wei Z, Zhao X, Chen J, Sun Q, Wang Z, Wang Y, et al. Deep learning-based stratification of gastric cancer patients from hematoxylin and eosin-stained whole slide images by predicting molecular features for immunotherapy response. Am J Pathol. 2023;193:1517–27.

    Article 
    PubMed 

    Google Scholar 

  • Brockmoeller S, Echle A, Ghaffari Laleh N, Eiholm S, Malmstrøm ML, Plato Kuhlmann T, et al. Deep learning identifies inflamed fat as a risk factor for lymph node metastasis in early colorectal cancer. J Pathol. 2022;256:269–81.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Krogue JD, Azizi S, Tan F, Flament-Auvigne I, Brown T, Plass M, et al. Predicting lymph node metastasis from primary tumor histology and clinicopathologic factors in colorectal cancer using deep learning. Commun Med (Lond). 2023;3:59.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zheng Q, Jian J, Wang J, Wang K, Fan J, Xu H, et al. Predicting lymph node metastasis status from primary muscle-invasive bladder cancer histology slides using deep learning: a retrospective multicenter study. Cancers (Basel). 2023;15:3000.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Guo Q, Qu L, Zhu J, Li H, Wu Y, Wang S, et al. Predicting lymph node metastasis from primary cervical squamous cell carcinoma based on deep learning in histopathologic images. Mod Pathol. 2023;36:100316.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Chen S, Xiang J, Wang X, Zhang J, Yang S, Yang W, et al. Deep learning-based pathology signature could reveal lymph node status and act as a novel prognostic marker across multiple cancer types. Br J Cancer. 2023;129:46–53.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Gao F, Jiang L, Guo T, Lin J, Xu W, Yuan L, et al. Deep learning-based pathological prediction of lymph node metastasis for patient with renal cell carcinoma from primary whole slide images. J Transl Med. 2024;22:568.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Muti HS, Röcken C, Behrens HM, Löffler CML, Reitsam NG, Grosser B, et al. Deep learning trained on lymph node status predicts outcome from gastric cancer histopathology: a retrospective multicentric study. Eur J Cancer. 2023;194:113335.

    Article 
    PubMed 

    Google Scholar 

  • Guo Z, Lan J, Wang J, Hu Z, Wu Z, Quan J, et al. Prediction of lymph node metastasis in primary gastric cancer from pathological images and clinical data by multimodal multiscale deep learning. Biomed Signal Process Control. 2023;86:105336.

    Article 

    Google Scholar 

  • Zeng YJ, Zhang CD, Dai DQ. Impact of lymph node micrometastasis on gastric carcinoma prognosis: a meta-analysis. World J Gastroenterol. 2015;21:1628–35.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mpallas KD, Lagopoulos VI, Kamparoudis AG. Prognostic significance of solitary lymphnode metastasis and micrometastasis in gastric cancer. Front Surg. 2018;5:63.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Tavares A, Wen X, Maciel J, Carneiro F, Dinis-Ribeiro M. Occult tumour cells in lymph nodes from gastric cancer patients: should isolated tumour cells also be considered?. Ann Surg Oncol. 2020;27:4204–15.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wang X, Chen Y, Gao Y, Zhang H, Guan Z, Dong Z, et al. Predicting gastric cancer outcome from resected lymph node histopathology images using deep learning. Nat Commun. 2021;12:1637.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Huang SC, Chen CC, Lan J, Hsieh TY, Chuang HC, Chien MY, et al. Deep neural network trained on gigapixel images improves lymph node metastasis detection in clinical settings. Nat Commun. 2022;13:3347.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • WHO Classification of Tumours Editorial Board. WHO classification of tumours: digestive system tumours. 5th ed. Lyon: International Agency for Research on Cancer; 2019.

  • Amin MB, Edge SB, Greene FL (ed.). AJCC Cancer Staging Manual. 8th ed (Springer, New York, 2017).

  • Jiang Y, Liang X, Han Z, Wang W, Xi S, Li T, et al. Radiographical assessment of tumour stroma and treatment outcomes using deep learning: a retrospective, multicohort study. Lancet Digit Health. 2021;3:e371–82.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Lu MY, Williamson DFK, Chen TY, Chen RJ, Barbieri M, Mahmood F. Data-efficient and weakly supervised computational pathology on whole-slide images. Nat Biomed Eng. 2021;5:555–70.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Kang M, Song H, Park S, Yoo D, Pereira S. Benchmarking self-supervised learning on diverse pathology datasets, (2023). http://arxiv.org/abs/2212.04690.

  • Agnes A, Biondi A, Cananzi FM, Rausei S, Reddavid R, Laterza V, et al. Ratio-based staging systems are better than the 7th and 8th editions of the TNM in stratifying the prognosis of gastric cancer patients: a multicenter retrospective study. J Surg Oncol. 2019;119:948–57.

    Article 
    PubMed 

    Google Scholar 

  • Wang W, Yang YJ, Zhang RH, Deng JY, Sun Z, Seeruttun SR, et al. Standardizing the classification of gastric cancer patients with limited and adequate number of retrieved lymph nodes: an externally validated approach using real-world data. Mil Med Res. 2022;9:15.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhou Y, Zhang GJ, Wang J, Zheng KY, Fu W. Current status of lymph node micrometastasis in gastric cancer. Oncotarget. 2017;8:51963–9.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nakajo A, Natsugoe S, Ishigami S, Matsumoto M, Nakashima S, Hokita S, et al. Detection and prediction of micrometastasis in the lymph nodes of patients with pN0 gastric cancer. Ann Surg Oncol. 2001;8:158–62.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Fukagawa T, Sasako M, Mann GB, Sano T, Katai H, Maruyama K, et al. Immunohistochemically detected micrometastases of the lymph nodes in patients with gastric carcinoma. Cancer. 2001;92:753–60.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Jeuck TLA, Wittekind C. Gastric carcinoma: stage migration by immunohistochemically detected lymph node micrometastases. Gastric Cancer. 2015;18:100–8.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Tavares A, Monteiro-Soares M, Viveiros F, Maciel Barbosa J, Dinis-Ribeiro M. Occult tumor cells in lymph nodes of patients with gastric cancer: a systematic review on their prevalence and predictive role. Oncology. 2015;89:245–54.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Wei T, Yuan X, Gao R, Johnston L, Zhou J, Wang Y, et al. Survival prediction of stomach cancer using expression data and deep learning models with histopathological images. Cancer Sci. 2023;114:690–701.

    Article 
    CAS 
    PubMed 

    Google Scholar 

  • Veldhuizen GP, Röcken C, Behrens HM, Cifci D, Muti HS, Yoshikawa T, et al. Deep learning-based subtyping of gastric cancer histology predicts clinical outcome: a multi-institutional retrospective study. Gastric Cancer. 2023;26:708–20.

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhao K, Li Z, Yao S, Wang Y, Wu X, Xu Z, et al. Artificial intelligence quantified tumour-stroma ratio is an independent predictor for overall survival in resectable colorectal cancer. EBiomedicine. 2020;61:103054.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bokhorst JM, Ciompi F, Öztürk SK, Oguz Erdogan AS, Vieth M, Dawson H, et al. Fully automated tumor bud assessment in hematoxylin and eosin-stained whole slide images of colorectal cancer. Mod Pathol. 2023;36:100233.

    Article 
    CAS 
    PubMed 

    Google Scholar 



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