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The sTRA Plasma Biomarker: Blinded Validation of Improved Accuracy Over CA19-9 in Pancreatic Cancer Diagnosis
Open accessPublished version of a preprint
Abstract
Purpose: The CA19-9 biomarker is elevated in a substantial group of patients with pancreatic ductal adenocarcinoma (PDAC), but not enough to be reliable for the detection or diagnosis of the disease. We hypothesized that a glycan called sTRA (sialylated tumor-related antigen) is a biomarker for PDAC that improves upon CA19-9. Experimental Design: We examined sTRA and CA19-9 expression and secretion in panels of cell lines, patient-derived xenografts, and primary tumors. We developed candidate biomarkers from sTRA and CA19-9 in a training set of 147 plasma samples and used the panels to make case–control calls, based on predetermined thresholds, in a 50-sample validation set and a blinded, 147-sample test set. Results: The sTRA glycan was produced and secreted by pancreatic tumors and models that did not produce and secrete CA19-9. Two biomarker panels improved upon CA19-9 in the training set, one optimized for specificity, which included CA19-9 and 2 versions of the sTRA assay, and another optimized for sensitivity, which included 2 sTRA assays. Both panels achieved statistical improvement (P < 0.001) over CA19-9 in the validation set, and the specificity-optimized panel achieved statistical improvement (P < 0.001) in the blinded set: 95% specificity and 54% sensitivity (75% accuracy), compared with 97%/30% (65% accuracy). Unblinding produced further improvements and revealed independent, complementary contributions from each marker. Conclusions: sTRA is a validated serological biomarker of PDAC that yields improved performance over CA19-9. The new panels may enable surveillance for PDAC among people with elevated risk, or improved differential diagnosis among patients with suspected pancreatic cancer.
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Biomarker panels often build upon CA 19-9 and demonstrate improved performance in early-stage disease compared with CA 19-9 alone.
“Such biomarker “panels” often build upon CA 19-9 and demonstrate improved performance in early-stage disease compared with CA 19-9 alone.40–43”
From Artificial Intelligence and Early Detection of Pancreatic Cancer: 2020 Summative Review (2021) · cites this paper as [42]
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Citations
Cites
An Introduction to the Bootstrap
Efron, B., & Tibshirani, R. J. (1994) · doi:10.1201/9780429246593 · Cited by 40,500
An Introduction to the Bootstrap.
Buckland, S. T., Efron, B., & Tibshirani, R. J. (1994) · Biometrics · doi:10.2307/2532810 · Cited by 3,236
Detection and localization of surgically resectable cancers with a multi-analyte blood test
Cohen, J. D., Li, L., Wang, Y., Thoburn, C., Afsari, B., Danilova, L., Douville, C., Javed, A. A., Wong, F., Mattox, A., et al. (2018) · Science · doi:10.1126/science.aar3247 · Cited by 2,783
Self-citationPhases of Biomarker Development for Early Detection of Cancer
Pepe, M. S., Etzioni, R., Feng, Z., Potter, J. D., Thompson, M. L., Thornquist, M., Winget, M., & Yasui, Y. (2001) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/93.14.1054 · Cited by 1,686 · cited 1×
“For further validation, the sample size should be expanded; prospective sample collection at multiple sites should be used; and the measurements should be acquired using the clinical assay that would be used in practice (32).”
MethodMagnani, J. L., Nilsson, B., Brockhaus, M., Zopf, D., Steplewski, Z., Koprowski, H., & Ginsburg, V. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)45389-1 · Cited by 882 · cited 1×
“Both CA19-9 and sTRA appear on multiple glycoproteins and glycolipids (19, 20).”
BackgroundGoonetilleke, K. S., & Siriwardena, A. K. (2006) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2006.10.004 · Cited by 880 · cited 2×
“The CA19-9 performance was in agreement with previous reports (1) and our previous studies (4) on similar cohorts, yielding 70% to 75% sensitivity at 70% to 75% specificity (Fig.”
BackgroundResultPEPE, M. S., Feng, Z., Janes, H., Bossuyt, P. M., & Potter, J. D. (2008) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djn326 · Cited by 723 · cited 1×
“The samples were collected prior to knowledge of diagnosis, which is one of the PROBE design requirements (31), but they were not collected in prospective manner that mimicked clinical application.”
BackgroundColorectal carcinoma-specific antigen: detection by means of monoclonal antibodies.
Herlyn, M., Steplewski, Z., Herlyn, D., & Koprowski, H. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.3.1438 · Cited by 657 · cited 1×
“1A) is a tetrasaccharide detected by the CA19-9 monoclonal antibody (16).”
BackgroundProbability of Pancreatic Cancer Following Diabetes: A Population-Based Study
Chari, S. T., Leibson, C. L., Rabe, K. G., Ransom, J., de Andrade, M., & Petersen, G. M. (2005) · Gastroenterology · doi:10.1053/j.gastro.2005.05.007 · Cited by 603
Cohen, J. D., Javed, A. A., Thoburn, C. J., Wong, F., Tie, J., Gibbs, P., Schmidt, C. M., Yip-Schneider, M., Allen, P. J., Schattner, M. A., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1704961114 · Cited by 588 · cited 1×
“Given that combining CA19-9 with the PCR-based assay improved sensitivity (29), it is reasonable that the addition of sTRA would further improve sensitivity.”
BackgroundSelf-citation(1990) · PubMed · Cited by 579
A Monosialoganglioside Is a Monoclonal Antibody-Defined Antigen of Colon Carcinoma
Magnani, J. L., Brockhaus, M., Smith, D. F., Ginsburg, V., Blaszczyk, M., Mitchell, K. F., Steplewski, Z., & Koprowski, H. (1981) · Science · doi:10.1126/science.7209516 · Cited by 375 · cited 1×
“Both CA19-9 and sTRA appear on multiple glycoproteins and glycolipids (19, 20).”
BackgroundNew insights into pancreatic cancer-induced paraneoplastic diabetes
Sah, R. P., Nagpal, S. J. S., Mukhopadhyay, D., & Chari, S. T. (2013) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2013.49 · Cited by 339
Detection of early pancreatic ductal adenocarcinoma with thrombospondin-2 and CA19-9 blood markers
Kim, J., Bamlet, W. R., Oberg, A. L., Chaffee, K. G., Donahue, G., Cao, X.-J., Chari, S., Garcia, B. A., Petersen, G. M., & Zaret, K. S. (2017) · Science Translational Medicine · doi:10.1126/scitranslmed.aah5583 · Cited by 269 · cited 1×
“Plasma thrombospondin-2 was combined with CA19-9 to yield high specificity and sensitivity in multiple sample sets (25), and a drop in specific isoforms of apolipoprotein.”
MethodLennon, A. M., Wolfgang, C. L., Canto, M. I., Klein, A. P., Herman, J. M., Goggins, M., Fishman, E. K., Kamel, I. R., Weiss, M. J., Diaz, L. A., et al. (2014) · Cancer Research · doi:10.1158/0008-5472.can-14-0734 · Cited by 268
Antigens of human pancreatic adenocarcinoma cells defined by murine monoclonal antibodies.
Metzgar, R. S., Gaillard, M. T., Levine, S. J., Tuck, F. L., Bossen, E. H., & Borowitz, M. J. (1982) · PubMed · Cited by 246
Multiplexed analysis of glycan variation on native proteins captured by antibody microarrays
Chen, S., LaRoche, T., Hamelinck, D., Bergsma, D. P., Brenner, D. E., Simeone, D. M., Brand, R. E., & Haab, B. B. (2007) · Nature Methods · doi:10.1038/nmeth1035 · Cited by 239
Self-citationAndrews, P. W., Banting, G. S., Damjanov, I., Arnaud, D., & Avner, P. R. (1984) · Hybridoma · doi:10.1089/hyb.1984.3.347 · Cited by 232 · cited 3×
“A monoclonal antibody called TRA-1-60 (17) detects the presumed precursor of the CA19-9 antigen, a non-fucosylated and non-sialylated tetrasaccharide (Fig.”
BackgroundInfluentialPowers, T. W., Jones, E. E., Rodemich-Betesh, L., Romano, P. R., Gao, P., Copland, J. A., Mehta, A. S., & Drake, R. R. (2013) · Analytical Chemistry · doi:10.1021/ac402108x · Cited by 171 · cited 1×
“Therefore, new leads potentially could be found by analyzing tumors with a non-glandular histopathology using glycan-discovery methods such as wholetissue MALDI imaging (41).”
MethodSelf-citationSequential Validation of Blood-Based Protein Biomarker Candidates for Early-Stage Pancreatic Cancer
Capello, M., Bantis, L. E., Scélo, G., Zhao, Y., Peng, L., Dhillon, D. S., Patel, N. J., Kundnani, D. L., Wang, H., Abbruzzese, J. L., et al. (2016) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djw266 · Cited by 148
Self-citationYue, T., Goldstein, I. J., Hollingsworth, M. A., Kaul, K. L., Brand, R. E., & Haab, B. B. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900135-mcp200 · Cited by 132 · cited 1×
“In the blood of patients with pancreatic cancer, we previously detected the glycans primarily on the mucins MUC1, MUC5AC, and MUC16, and more rarely onMUC5BandMUC3A (7, 13, 21).”
BackgroundSelf-citationNatunen, S., Satomaa, T., Pitkänen, V., Salo, H., Mikkola, M. L., Natunen, J., Otonkoski, T., & Valmu, L. (2010) · Glycobiology · doi:10.1093/glycob/cwq209 · Cited by 92
Honda, K., Kobayashi, M., Okusaka, T., Rinaudo, J. A., Huang, Y., Marsh, T. L., Sanada, M., Sasajima, Y., Nakamori, S., Shimahara, M., et al. (2015) · Scientific Reports · doi:10.1038/srep15921 · Cited by 89 · cited 1×
“AII strongly discriminated pancreatic cancer from healthy controls, although not from benign diseases, in a blinded study (26).”
BackgroundSelf-citationPour, P. M., Tempero, M., Takasaki, H., Uchida, E., Takiyama, Y., Burnett, D. A., & Steplewski, Z. (1988) · PubMed · Cited by 82
Yue, T., Maupin, K. A., Fallon, B. P., Li, L., Partyka, K. A., Anderson, M. A., Brenner, D. E., Kaul, K. L., Zeh, H. J., Moser, A. J., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0029180 · Cited by 76
Self-citationYue, T., Partyka, K. A., Maupin, K. A., Hurley, M. C., Andrews, P., Kaul, K. L., Moser, A. J., Zeh, H. J., Brand, R. E., & Haab, B. B. (2011) · PROTEOMICS · doi:10.1002/pmic.201000827 · Cited by 70 · cited 1×
“In the blood of patients with pancreatic cancer, we previously detected the glycans primarily on the mucins MUC1, MUC5AC, and MUC16, and more rarely onMUC5BandMUC3A (7, 13, 21).”
BackgroundSelf-citationA Plasma Biomarker Panel to Identify Surgically Resectable Early-Stage Pancreatic Cancer
Balasenthil, S., Huang, Y., Liu, S., Marsh, T. L., Chen, J., Stass, S. A., Kukuruga, D. L., Brand, R. E., Chen, N., Frazier, M. L., et al. (2017) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djw341 · Cited by 69 · cited 1×
“Panels of biomarkers including metabolic markers (27) and protein indicators of a migratory signature (28) showed particularly encouraging results in recent studies.”
ResultSelf-citationTakasaki, H., Uchida, E., Tempero, M. A., Burnett, D. A., Metzgar, R. S., & Pour, P. M. (1988) · PubMed · Cited by 68
Haglund, C. H., Lindgren, J., Roberts, P., & Nordling, S. (1986) · British Journal of Cancer · doi:10.1038/bjc.1986.34 · Cited by 67 · cited 1×
“The elevation of CA19-9 in the blood potentially results from accumulations in the stroma followed by leakage into the capillaries or lymph (39, 40).”
BackgroundKawa, S., Tokoo, M., Oguchi, H., Furuta, S., Homma, T., Hasegawa, Y., Ogata, H., & Sakata, K. (1994) · Pancreas · doi:10.1097/00006676-199411000-00003 · Cited by 64 · cited 1×
“Other patients elevate a glycan detected by the DUPAN-2 monoclonal antibody (35, 36), identified primarily as type 1 sialyl-LacNAc (37, 38).”
BackgroundPartyka, K. A., Maupin, K. A., Brand, R. E., & Haab, B. B. (2012) · PROTEOMICS · doi:10.1002/pmic.201100676 · Cited by 60 · cited 1×
“Other patients elevate a glycan detected by the DUPAN-2 monoclonal antibody (35, 36), identified primarily as type 1 sialyl-LacNAc (37, 38).”
BackgroundSelf-citationBalmaña, M., Sarrats, A., Llop, E., Barrabés, S., Saldova, R., Ferri, M. J., Figueras, J., Fort, E., Llorens, R., Rudd, P. M., et al. (2015) · Clinica Chimica Acta · doi:10.1016/j.cca.2015.01.007 · Cited by 54 · cited 1×
“33), which we (5, 6) and others (34) found elevated in the circulation of many patients with pancreatic cancer.”
BackgroundValidation of Biomarkers for Early Detection of Pancreatic Cancer
Young, M. R., Wagner, P. D., Ghosh, S., Rinaudo, J. A., Baker, S. G., Zaret, K. S., Goggins, M., & Srivastava, S. (2018) · Pancreas · doi:10.1097/mpa.0000000000000973 · Cited by 53
Haab, B. B., Huang, Y., Balasenthil, S., Partyka, K. A., Tang, H., Anderson, M. A., Allen, P. J., Sasson, A. R., Zeh, H. J., Kaul, K. L., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0139049 · Cited by 47 · cited 2×
“The CA19-9 performance was in agreement with previous reports (1) and our previous studies (4) on similar cohorts, yielding 70% to 75% sensitivity at 70% to 75% specificity (Fig.”
BackgroundResultSelf-citationCharacterization of CA 19-9 bearing mucins as physiological exocrine pancreatic secretion products.
Kalthoff, H., Kreiker, C., Schmiegel, W.-H., Greten, H., & Thiele, H. G. (1986) · PubMed · Cited by 45
Tang, H., Singh, S. K., Partyka, K. A., Kletter, D., Hsueh, P. Y., Yadav, J., Ensink, E., Bern, M. W., Hostetter, G. H., Hartman, D. J., et al. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.047837 · Cited by 44
Self-citationMalesci, A., Montorsi, M., Mariani, A., Santambrogio, R., Bonato, C., Bissi, O., Tacconi, M., Wizemann, G., & Spina, G. (1992) · Pancreas · doi:10.1097/00006676-199207000-00012 · Cited by 42
Tang, H., Partyka, K. A., Hsueh, P. Y., Sinha, J. Y., Kletter, D., Zeh, H. J., Huang, Y., Brand, R. E., & Haab, B. B. (2015) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2015.12.003 · Cited by 41 · cited 2×
“Another glycan, referred to as sTRA, was elevated in up to half of the patientswith lowCA19-9, with very low false-positive rates (7).”
BackgroundSelf-citationThe CA19-9 and Sialyl-TRA Antigens Define Separate Subpopulations of Pancreatic Cancer Cells
Barnett, D., Liu, Y., Partyka, K. A., Huang, Y., Tang, H., Hostetter, G. H., Brand, R. E., Singhi, A. D., Drake, R. R., & Haab, B. B. (2017) · Scientific Reports · doi:10.1038/s41598-017-04164-z · Cited by 28 · cited 2×
“In subsequent research, we found that the cells producing sTRA are different in location,morphologies, andmolecular characteristics than the cells producingCA19-9 (8).”
BackgroundSelf-citationSingh, S. K., Pal, K., Yadav, J., Tang, H., Partyka, K. A., Kletter, D., Hsueh, P. Y., Ensink, E., Birendra, K. C., Hostetter, G. H., et al. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00142 · Cited by 27 · cited 2×
“One class of glycans we found is based on a structural isomer of the CA19-9 antigen called sialyl-Lewis X (5, 6).”
BackgroundSelf-citationKelly, K. A., Hollingsworth, M. A., Brand, R. E., Liu, C. H., Singh, V. K., Srivastava, S., Wasan, A. D., Yadav, D. K., & Andersen, D. K. (2015) · Pancreas · doi:10.1097/mpa.0000000000000552 · Cited by 17
Self-citationThe Marker State Space (MSS) Method for Classifying Clinical Samples
Fallon, B. P., Curnutte, B., Maupin, K. A., Partyka, K. A., Choi, S., Brand, R. E., LANGMEAD, C. J., Tembe, W., & Haab, B. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0065905 · Cited by 6 · cited 1×
“Using the MSS method (22), we identified 2 lead panels, one that provided high specificity for the detection of cancer (low false-positive rate), and another with high sensitivity (low false-negative rate).”
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Roles of CA19-9 in pancreatic cancer: Biomarker, predictor and promoter
Luo, G., Jin, K., Deng, S., Cheng, H., Fan, Z., Gong, Y., Qian, Y., Huang, Q., Ni, Q., Liu, C., et al. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2020.188409 · Cited by 446
Artificial Intelligence and Early Detection of Pancreatic Cancer: 2020 Summative Review
Kenner, B., Chari, S. T., Kelsen, D., Klimstra, D. S., Pandol, S. J., Rosenthal, M., Rustgi, A. K., Taylor, J. A., Yala, A., Abul-Husn, N., et al. (2021) · Pancreas · doi:10.1097/mpa.0000000000001762 · Cited by 158
Self-citationBiomarkers in the diagnosis of pancreatic cancer: Are we closer to finding the golden ticket?
O'Neill, R. S., & Stoita, A. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i26.4045 · Cited by 144
Blood biomarkers for differential diagnosis and early detection of pancreatic cancer
Al-Shaheri, F. N., Alhamdani, M. S. S., Bauer, A. S., Giese, N. A., Büchler, M. W., Hackert, T., & Hoheisel, J. D. (2021) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2021.102193 · Cited by 115
McDowell, C. T., Klamer, Z. L., Hall, J., West, C. A., Wisniewski, L., Powers, T. W., Angel, P. M., Mehta, A. S., Lewin, D., Haab, B. B., et al. (2020) · Molecular & Cellular Proteomics · doi:10.1074/mcp.ra120.002256 · Cited by 98
“The immunofluorescence data were overlaid onto MALDI mass and H&E images using the custom-built Overlay program (5) and Canvas 14.”
BackgroundMethodInfluentialSelf-citationApplications and continued evolution of glycan imaging mass spectrometry
McDowell, C. T., Lu, X., Mehta, A. S., Angel, P. M., & Drake, R. R. (2021) · Mass Spectrometry Reviews · doi:10.1002/mas.21725 · Cited by 76
Self-citationPancreatic Cancer in Chronic Pancreatitis: Pathogenesis and Diagnostic Approach
Cosquer, G. L., Maulat, C., Bournet, B., Cordelier, P., Buscail, É., & Buscail, L. (2023) · Cancers · doi:10.3390/cancers15030761 · Cited by 73
Reese, K.-L., Pantel, K., & Smit, D. J. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-024-03166-w · Cited by 56
A combination of circulating tumor cells and CA199 improves the diagnosis of pancreatic cancer
Chen, J., Wang, H., Zhou, L., Liu, Z., & Tan, X. (2022) · Journal of Clinical Laboratory Analysis · doi:10.1002/jcla.24341 · Cited by 48
Lu, X., McDowell, C. T., Blaschke, C. R. K., Liu, L., Grimsley, G., Wisniewski, L., Gao, C., Mehta, A. S., Haab, B. B., Angel, P. M., et al. (2023) · Analytical Chemistry · doi:10.1021/acs.analchem.2c04882 · Cited by 42
Self-citationBoyd, L. N. C., Ali, M., Kam, L., Puik, J. R., Rodrigues, S. M. F., Zwart, E. S., Daams, F. D., Zonderhuis, B. M., Meijer, L. L., Large, T. Y. S. L., et al. (2022) · Cancers · doi:10.3390/cancers14020344 · Cited by 42
“Two fairly recent publications which discuss the cost effectiveness of PDAC surveillance state that a biomarker with 96% specificity and 65% sensitivity could already result in an acceptable cost-benefit analysis [41] and that screening of high-risk pancreatic cancer patients could result in an increase of survival by…”
BackgroundWeng, W., Zhang, Z., Huang, W., Xu, X., Wu, B., Ye, T., Shan, Y., Shi, K., & Lin, Z. (2020) · Cancer Cell International · doi:10.1186/s12935-020-01243-6 · Cited by 40
Nanoparticle-enabled blood tests for early detection of pancreatic ductal adenocarcinoma
Caputo, D. D., & Caracciolo, G. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.11.030 · Cited by 38
Identification of Serum microRNA-25 as a novel biomarker for pancreatic cancer
Yu, Y., Tong, Y., Zhong, A., Wang, Y., Lu, R., & Guo, L. (2020) · Medicine · doi:10.1097/md.0000000000023863 · Cited by 37
“Meanwhile, previous researches have shown that the Lewis (-) individuals which take up the population of approximately 5% to 10%, have minimal or even no secretion of CA19-9, accounting for about 34% of PCa patients.([7,8]) In consideration of these conditions, the combination of CA19-9 and CA125 has been widely used…”
MethodAn Integrated Workflow for Global, Glyco-, and Phospho-proteomic Analysis of Tumor Tissues
Zhou, Y., Lih, T. M., Yang, G., Chen, S., Chen, L., Chan, D. W., Zhang, H., & Li, Q. K. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.9b03753 · Cited by 35
Haab, B. B., Qian, L., Staal, B., Jain, M., Fahrmann, J. F., Worthington, C., Prosser, D., Velokokhatnaya, L., Lopez, C., Tang, R., et al. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.217245 · Cited by 32
Self-citationMasterson, A. N., Chowdhury, N. N., Fang, Y., Yip-Schneider, M., Hati, S., Gupta, P., Cao, S., Wu, H., Schmidt, C. M., Fishel, M. L., et al. (2023) · ACS Sensors · doi:10.1021/acssensors.2c02105 · Cited by 26
Detection of Chemotherapy-resistant Pancreatic Cancer Using a Glycan Biomarker, sTRA
Gao, C., Wisniewski, L., Liu, Y., Staal, B., Beddows, I., Plenker, D., Aldakkak, M., Hall, J., Barnett, D., Gouda, M. K., et al. (2020) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-20-2475 · Cited by 26
“Immunoassays The immunoassays were based on the method described previously (15).”
BackgroundMethodInfluentialSelf-citationJiang, Z., Zheng, X., Li, M., & Liu, M. (2023) · Frontiers of Medicine · doi:10.1007/s11684-023-1050-6 · Cited by 24
Asar, M. C., Franco, A., & Soendergaard, M. (2020) · Biomolecules · doi:10.3390/biom10050714 · Cited by 23
Diagnostic biomarkers for pancreatic cancer: An update
Yang, M. J., & Zhang, C. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i45.7862 · Cited by 21
Biomolecular Recognition of the Glycan Neoantigen CA19-9 by Distinct Antibodies
Borenstein-Katz, A., Warszawski, S., Amon, R., Eilon-Ashkenazy, M., Cohen‐Dvashi, H., Ben‐Arye, S. L., Tasnima, N., Yu, H., Chen, X., Padler‐Karavani, V., et al. (2021) · Journal of Molecular Biology · doi:10.1016/j.jmb.2021.167099 · Cited by 20
Zhang, P., Wu, Z., Zhang, W.-B., He, Y., Chen, K., Wang, T., Li, H., Zheng, H., Li, D., Yang, D.-W., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36374-7 · Cited by 19
Liu, Y., Kaur, S., Huang, Y., Fahrmann, J. F., Rinaudo, J. A., Hanash, S. M., Batra, S. K., Singhi, A. D., Brand, R. E., Maitra, A., et al. (2020) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-20-0161 · Cited by 17
Self-citationElango, A., Nesam, V. D., Sukumar, P., Lawrence, I., & Radhakrishnan, A. (2024) · Archives of Microbiology · doi:10.1007/s00203-024-03914-8 · Cited by 14
“Staal and team proved that the combination of Sialylated tumor-related antigen and CA19–9 will be good enough for both accuracy and sensitivity (Staal et al. 2019).”
Wang, A., Sun, B., Wang, M., Shi, H., Huang, Z., He, T., Li, Q., Deng, J., Fu, W., & Jiang, Y. (2020) · PeerJ · doi:10.7717/peerj.8811 · Cited by 15
“Numerous studies have shown that tumor size, lymph node metastasis, vascular invasion and serum tumor markers (TMs) are vital prognostic factors for PC (Karamitopoulou et al., 2013; Staal et al., 2019; Winter, Yeo & Brody, 2013).”
BackgroundAdvances in the Discovery of Novel Biomarkers for Cancer: Spotlight on Protein N -Glycosylation
Zhang, W., Yang, Z., Gao, X., & Wu, Q. (2020) · Biomarkers in Medicine · doi:10.2217/bmm-2020-0185 · Cited by 15
Automated Identification and Quantification of Signals in Multichannel Immunofluorescence Images
Barnett, D., Hall, J., & Haab, B. B. (2019) · American Journal Of Pathology · doi:10.1016/j.ajpath.2019.03.011 · Cited by 14
Self-citationGlycosylation in cancer as a source of biomarkers
Khorami-Sarvestani, S., Hanash, S., Fahrmann, J. F., Léon-Letelier, R. A., & Katayama, H. (2024) · Expert Review of Proteomics · doi:10.1080/14789450.2024.2409224 · Cited by 13
Mottini, C., Auciello, F. R., Manni, I., Pilarsky, C. P., Caputo, D. D., Caracciolo, G., Rossetta, A., Gennaro, E. D., Budillon, A., Blandino, G., et al. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-024-03117-5 · Cited by 12
“…aiming to strengthen and validate traditional biomarkers, there are also some clinical trials that are trying to identify new biomarkers (i.e. trial ID NCT06041009 and NCT04549064), and some of the newly proposed molecules even showed superior performance over CA19-9 (trial ID: NCT04143152) [133].”
BackgroundPancreatic Cancer Surveillance and Novel Strategies for Screening
Dudley, B., & Brand, R. E. (2021) · Gastrointestinal Endoscopy Clinics of North America · doi:10.1016/j.giec.2021.08.008 · Cited by 10
Self-citationBinkowski, B., Klamer, Z. L., Gao, C., Staal, B., Repesh, A., Tran, H.-L., Brass, D. M., Bartlett, P., Gallinger, S., Blomqvist, M., et al. (2025) · Science Advances · doi:10.1126/sciadv.adt0029 · Cited by 6
“…significantly different between the groups (log-rank test), potentially owing to a small sample size, but the substantial difference in 50% and 2-year survival uniquely in the heterogeneous-uniform group suggests a link between clonal outgrowths of different PDAC subpopulations and poor survival.”
InfluentialSelf-citationKhakoo, S. S., Petrillo, A., Salati, M., Muhith, A., Evangelista, J., Seghezzi, S., Petrelli, F., Tomasello, G., & Ghidini, M. (2021) · Cancers · doi:10.3390/cancers13174396 · Cited by 6
Evaluation of Sialyl-Lactotetra as a Marker for Epithelial Ovarian Tumors
Barone, A., Linder, A., Mateoiu, C., Larsen, R. K., Blixt, O., Teneberg, S., & Sundfeldt, K. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.561888 · Cited by 5
Recent advances in molecular diagnostics and therapeutic targets for pancreatic cancer
Clay, R., & Siddiqi, S. A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-12-819457-7.00016-5 · Cited by 3
(2022) · Cancer Screening and Prevention · doi:10.14218/csp.2022.00015 · Cited by 3
The circadian gene Dec2 promotes pancreatic cancer progression and dormancy through immune evasion
Wang, L., Harris, C. R., Dudgeon, C., Prela, O., Cazarin, J., Shih, C.-H., Davidson, C., Casabianca, A., De, S., Narrow, W. C., et al. (2026) · Developmental Cell · doi:10.1016/j.devcel.2026.04.001 · Cited by 2
Self-citationRNA biosensors for detection of pancreatic cancer.
Zare-Mehrjardi, M.-J., Hatami-Araghi, M., Jafari-Khorchani, M., Roudsari, Z. O., Taheri-Anganeh, M., Abdolrahmat, M., Ghasemi, H., & Aiiashi, S. (2025) · Clinica chimica acta; international journal of clinical chemistry · doi:10.1016/j.cca.2025.120237 · Cited by 2
Detection of Chemotherapy-Resistant Pancreatic Cancer Using a Glycan BiomarkerPreprint
Gao, C., Wisniewski, L., Liu, Y., Staal, B., Beddows, I., Plenker, D., Aldakkak, M., Hall, J., Barnett, D., Gouda, M. K., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.01.128082
Self-citationAvanços no diagnóstico do Tumor Pancreático: o papel emergente do biomarcador CA 19-9
Barbosa, L. B. D. S., Lino, V. T., & Rodarte, R. W. (2024) · Brazilian Journal of Health Review · doi:10.34119/bjhrv7n2-466
Harris, C. R., Wang, L., Dudgeon, C., Prela, O., Cazarin, J., Shih, C.-H., Davidson, C., Casabianca, A., De, S., Narrow, W. C., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.12.623005
Self-citationYamamoto, T., Boku, S., Mitamura, K., & Taga, A. (2025) · Biomedicines · doi:10.3390/biomedicines13112631
Advances in metallomics for pancreatic cancer: Analytical strategies for biomarker discovery
Royle, O., McCauley, J. I., Lockwood, T. E., Doble, P., Cox, T. R., Chitty, J. L., & Bordin, D. M. (2026) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2026.118878
Wu, A. H. B., Ong, C. M., Alamillo, M., Clark, Z., Wong, C., & Jung, G. (2026) · Cancer Treatment and Research Communications · doi:10.1016/j.ctarc.2026.101328
Gui, S., Zhang, Y., Xia, T., Qian, J., Fang, Z., Ouyang, W., Wang, J., Chen, J., Ren, X., Lyu, J., et al. (2026) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2026.101642
“S8 A and Supplementary Data 6).”
Metadata
- Authors
- Staal, B., Liu, Y., Barnett, D., Hsueh, P., He, Z., Gao, C., Partyka, K., Hurd, M. W., Singhi, A. D., Drake, R. R., Huang, Y., Maitra, A., Brand, R. E., & Haab, B. B.
- Affiliations
- Van Andel Institute (US)
- Fred Hutch Cancer Center (US)
- The University of Texas MD Anderson Cancer Center (US)
- University of Pittsburgh Medical Center (US)
- Medical University of South Carolina (US)
- Corresponding author
- Haab, Brian B.
- ORCID
- Venue
- Clinical Cancer Research
- Published
- 2019-05-01
- Volume
- 25
- Issue
- 9
- Pages
- 2745-2754
- ISSN
- 1078-0432 (ISSN-L)
- 1557-3265
- PMC
- PMC7246054
- OpenAlex
- W2910639478
- Cited by
- 49
- References
- 46
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 7 · 2023: 5 · 2022: 3 · 2021: 9 · 2020: 14 · 2019: 4
- FWCI
- 3.13
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Clinical Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NCI (U01 CA152653, U01 CA200466, U01 CA200468, U01 CA168896, U01 CA196403, P30 CA138313)
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Health Sciences › Medicine › Surgery › Pancreatitis Pathology and Treatment
- Keywords
- strA, CA19-9, pancreatic ductal adenocarcinoma, plasma biomarkers, glycan biomarkers, diagnostic accuracy, biomarker panel, tumor-associated glycosylation, cancer surveillance, differential diagnosis
- MeSH terms
- Aged, Animals, Female, Follow-Up Studies, Humans, Male, Middle Aged, Pancreatic Neoplasms, Prognosis, Tumor Cells, Cultured, Biomarkers, Tumor, Antigens, Tumor-Associated, Carbohydrate, Case-Control Studies, CA-19-9 Antigen, N-Acetylneuraminic Acid, Carcinoma, Pancreatic Ductal, Xenograft Model Antitumor Assays, Mice
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