Computational discovery of tissue morphology biomarkers in very long-term survivors with pancreatic ductal adenocarcinoma

Pancreatic ductal adenocarcinoma (PDAC) is one of the deadliest forms of cancer, with an average 5-year survival rate of only 8%. Within PDAC patients, however, there is a small subset of patients who survive >10 years. Deciphering underlying reasons behind prolonged survival could potentially provide new opportunities to treat PDAC; however, no genomic, transcriptomic, proteomic, or clinical signatures have been found to robustly separate this subset of patients. Digital pathology, in combination with machine learning, provides an opportunity to computationally search for tissue morphology patterns associated with disease outcomes. Here, we developed a computational framework to analyze whole-slide images (WSI) of PDAC patient tissue and identify tissue-morphology signatures for very long term surviving patients. Our results indicate that less tissue morphology heterogeneity is significantly linked to better patient survival and that the extra-tumoral space encodes prognostic information for survival. Based on information from morphological heterogeneity in the tumor and its adjacent area, we established a machine learning model with an AUC of 0.94. Our analysis workflow highlighted a quantitative visual-based tissue phenotype analysis that also allows direct interaction with pathology. This study demonstrates a pathway to accelerate the discovery of undetermined tissue morphology associated with pathogenesis states and prognosis and diagnosis of patients by utilizing new computational approaches.

[1]  H. Kocher,et al.  Pancreatic Cancer , 2019, Methods in Molecular Biology.

[2]  D. Edwards,et al.  Generation of an in vitro 3D PDAC stroma rich spheroid model. , 2016, Biomaterials.

[3]  Kevin W. Eliceiri,et al.  Highly aligned stromal collagen is a negative prognostic factor following pancreatic ductal adenocarcinoma resection , 2016, Oncotarget.

[4]  Ce Zhang,et al.  Predicting non-small cell lung cancer prognosis by fully automated microscopic pathology image features , 2016, Nature Communications.

[5]  A. Jemal,et al.  Cancer treatment and survivorship statistics, 2016 , 2016, CA: a cancer journal for clinicians.

[6]  Francesco Bianconi,et al.  Multi-class texture analysis in colorectal cancer histology , 2016, Scientific Reports.

[7]  J. Tomlinson,et al.  Long-term survival in patients with pancreatic ductal adenocarcinoma. , 2016, Surgery.

[8]  Eva Budinska,et al.  Joint analysis of histopathology image features and gene expression in breast cancer , 2016, BMC Bioinformatics.

[9]  C. Verbeke,et al.  Morphological heterogeneity in ductal adenocarcinoma of the pancreas - Does it matter? , 2016, Pancreatology : official journal of the International Association of Pancreatology (IAP) ... [et al.].

[10]  Adrien Depeursinge,et al.  Automated classification of brain tumor type in whole-slide digital pathology images using local representative tiles , 2016, Medical Image Anal..

[11]  Predicting survival of pancreatic cancer patients treated with gemcitabine using longitudinal tumour size data , 2016, Cancer Chemotherapy and Pharmacology.

[12]  S. Curley,et al.  Generation of Homogenous Three-Dimensional Pancreatic Cancer Cell Spheroids Using an Improved Hanging Drop Technique. , 2016, Tissue engineering. Part C, Methods.

[13]  L. Wood,et al.  A robust non-linear tissue-component discrimination method for computational pathology , 2015, Laboratory Investigation.

[14]  A. Jemal,et al.  Cancer statistics, 2016 , 2016, CA: a cancer journal for clinicians.

[15]  J. Iovanna,et al.  Long‐term survivors after pancreatectomy for cancer: the TNM classification is outdated , 2015, ANZ journal of surgery.

[16]  Jen Jen Yeh,et al.  Virtual microdissection identifies distinct tumor- and stroma-specific subtypes of pancreatic ductal adenocarcinoma , 2015, Nature Genetics.

[17]  M. McCarter,et al.  Characteristics of 10-Year Survivors of Pancreatic Ductal Adenocarcinoma. , 2015, JAMA surgery.

[18]  Very long-term survival in pancreatic cancer , 2015, Aging.

[19]  L. Wood,et al.  Very Long-term Survival Following Resection for Pancreatic Cancer Is Not Explained by Commonly Mutated Genes: Results of Whole-Exome Sequencing Analysis , 2015, Clinical Cancer Research.

[20]  Damon H. May,et al.  Proteins associated with pancreatic cancer survival in patients with resectable pancreatic ductal adenocarcinoma , 2014, Laboratory Investigation.

[21]  Shai Dekel,et al.  Computer-aided diagnostics in digital pathology: automated evaluation of early-phase pancreatic cancer in mice , 2015, International Journal of Computer Assisted Radiology and Surgery.

[22]  H. Kocher,et al.  Pancreatic cancer organotypics: High throughput, preclinical models for pharmacological agent evaluation. , 2014, World journal of gastroenterology.

[23]  C. Guerra,et al.  Galectin-1 drives pancreatic carcinogenesis through stroma remodeling and Hedgehog signaling activation. , 2014, Cancer research.

[24]  Benjamin D. Smith,et al.  Projecting cancer incidence and deaths to 2030: the unexpected burden of thyroid, liver, and pancreas cancers in the United States. , 2014, Cancer research.

[25]  B. Dörken,et al.  Does long‐term survival in patients with pancreatic cancer really exist?—Results from the CONKO‐001 study , 2013, Journal of surgical oncology.

[26]  Ju-Hong Lee,et al.  New Morphological Features for Grading Pancreatic Ductal Adenocarcinomas , 2013, BioMed research international.

[27]  C. S. Ki,et al.  The influence of matrix properties on growth and morphogenesis of human pancreatic ductal epithelial cells in 3D. , 2013, Biomaterials.

[28]  F. Di Maggio,et al.  Imbalance of desmoplastic stromal cell numbers drives aggressive cancer processes , 2013, The Journal of pathology.

[29]  J. Willmann,et al.  Stromal galectin-1 expression is associated with long-term survival in resectable pancreatic ductal adenocarcinoma , 2012, Cancer biology & therapy.

[30]  K. Polyak,et al.  Intra-tumour heterogeneity: a looking glass for cancer? , 2012, Nature Reviews Cancer.

[31]  P. Mazur,et al.  Genetically engineered mouse models of pancreatic cancer: unravelling tumour biology and progressing translational oncology , 2011, Gut.

[32]  Y. Miao,et al.  Galectin-1 Secreted by Activated Stellate Cells in Pancreatic Ductal Adenocarcinoma Stroma Promotes Proliferation and Invasion of Pancreatic Cancer Cells: An In Vitro Study on the Microenvironment of Pancreatic Ductal Adenocarcinoma , 2011, Pancreas.

[33]  Fabio A. González,et al.  Visual pattern mining in histology image collections using bag of features , 2011, Artif. Intell. Medicine.

[34]  F. Real,et al.  Galectin-1 is a novel functional receptor for tissue plasminogen activator in pancreatic cancer. , 2009, Gastroenterology.

[35]  Kunio Doi,et al.  Computer-aided diagnosis in medical imaging: Historical review, current status and future potential , 2007, Comput. Medical Imaging Graph..

[36]  H. Iwase,et al.  [Breast cancer]. , 2006, Nihon rinsho. Japanese journal of clinical medicine.

[37]  Corinna Cortes,et al.  Support-Vector Networks , 1995, Machine Learning.

[38]  Trevor Hastie,et al.  Regularized Discriminant Analysis and Its Application in Microarrays , 2004 .

[39]  Pong C. Yuen,et al.  Regularized discriminant analysis and its application to face recognition , 2003, Pattern Recognit..

[40]  Eric R. Ziegel,et al.  Generalized Linear Models , 2002, Technometrics.

[41]  T P Speed,et al.  A score test for the linkage analysis of qualitative and quantitative traits based on identity by descent data from sib-pairs. , 2000, Biostatistics.

[42]  D. Opitz,et al.  Popular Ensemble Methods: An Empirical Study , 1999, J. Artif. Intell. Res..

[43]  Xiaoou Tang,et al.  Texture information in run-length matrices , 1998, IEEE Trans. Image Process..

[44]  R. Tibshirani Regression Shrinkage and Selection via the Lasso , 1996 .

[45]  N. Dubrawsky Cancer statistics , 1989, CA: a cancer journal for clinicians.

[46]  Robert M. Haralick,et al.  Textural Features for Image Classification , 1973, IEEE Trans. Syst. Man Cybern..

[47]  Peter E. Hart,et al.  Nearest neighbor pattern classification , 1967, IEEE Trans. Inf. Theory.

[48]  C. Dunnett A Multiple Comparison Procedure for Comparing Several Treatments with a Control , 1955 .