Decreased serum thrombospondin-1 levels in pancreatic cancer patients up to 24 months prior to clinical diagnosis: association with diabetes mellitus
Open accessPublished version of a preprint
Abstract
PURPOSE: Identification of serum biomarkers enabling earlier diagnosis of pancreatic ductal adenocarcinoma (PDAC) could improve outcome. Serum protein profiles in patients with preclinical disease and at diagnosis were investigated. EXPERIMENTAL DESIGN: Serum from cases up to 4 years prior to PDAC diagnosis and controls (UKCTOCS,n= 174) were studied, alongside samples from patients diagnosed with PDAC, chronic pancreatitis, benign biliary disease, type 2 diabetes mellitus, and healthy subjects (n= 298). Isobaric tags for relative and absolute quantification (iTRAQ) enabled comparisons of pooled serum from a test set (n= 150). Validation was undertaken using multiple reaction monitoring (MRM) and/or Western blotting in all 472 human samples and samples from a KPC mouse model. RESULTS: iTRAQ identified thrombospondin-1 (TSP-1) as reduced preclinically and in diagnosed samples. MRM confirmed significant reduction in levels of TSP-1 up to 24 months prior to diagnosis. A combination of TSP-1 and CA19-9 gave an AUC of 0.86, significantly outperforming both markers alone (0.69 and 0.77, respectively;P< 0.01). TSP-1 was also decreased in PDAC patients compared with healthy controls (P< 0.05) and patients with benign biliary obstruction (P< 0.01). Low levels of TSP-1 correlated with poorer survival, preclinically (P< 0.05) and at clinical diagnosis (P< 0.02). In PDAC patients, reduced TSP-1 levels were more frequently observed in those with confirmed diabetes mellitus (P< 0.01). Significantly lower levels were also observed in PDAC patients with diabetes compared with individuals with type 2 diabetes mellitus (P= 0.01). CONCLUSIONS: Circulating TSP-1 levels decrease up to 24 months prior to diagnosis of PDAC and significantly enhance the diagnostic performance of CA19-9. The influence of diabetes mellitus on biomarker behavior should be considered in future studies.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Siegel, R., Naishadham, D., & Jemal, A. (2013) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21166 · Cited by 11,825 · see citing works
Ross, P. L., Huang, Y. N., Marchese, J. N., Williamson, B., Parker, K., Hattan, S., Khainovski, N., Pillai, S., Dey, S., Daniels, S., et al. (2004) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m400129-mcp200 · Cited by 4,401 · see citing works
ASCO 2006 Update of Recommendations for the Use of Tumor Markers in Gastrointestinal Cancer
Locker, G. Y., Hamilton, S. R., Harris, J. E., Jessup, J. M., Kemeny, N. E., Macdonald, J. S., Somerfield, M. R., Hayes, D. F., & Bast, R. C. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2006.08.2644 · Cited by 1,592 · see citing works
Addona, T. A., Abbatiello, S. E., Schilling, B., Skates, S. J., Mani, D. R., Bunk, D. M., Spiegelman, C. H., Zimmerman, L. J., Ham, A.-J. L., Keshishian, H., et al. (2009) · Nature Biotechnology · doi:10.1038/nbt.1546 · Cited by 1,037 · see citing works
Menon, U., Gentry‐Maharaj, A., Hallett, R., Ryan, A., Burnell, M., Sharma, A., Lewis, S., Davies, S., Philpott, S., Lopes, A. D. B., et al. (2009) · The Lancet Oncology · doi:10.1016/s1470-2045(09)70026-9 · Cited by 829 · see citing works
Self-citationPrevalence and Clinical Profile of Pancreatic Cancer–Associated Diabetes Mellitus
Pannala, R., Leirness, J. B., Bamlet, W. R., Basu, A., Petersen, G. M., & Chari, S. T. (2008) · Gastroenterology · doi:10.1053/j.gastro.2008.01.039 · Cited by 621 · see citing works
Isolation and characterization of a high molecular weight glycoprotein from human blood platelets.
Lawler, J., Slayter, H. S., & Coligan, J. E. (1978) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)34336-3 · Cited by 434 · see citing works
CA19-9 serum levels in obstructive jaundice: clinical value in benign and malignant conditions
Marrelli, D., Caruso, S., Pedrazzani, C., Neri, A., Fernandes, E., Marini, M., Pinto, E., & Roviello, F. (2009) · The American Journal of Surgery · doi:10.1016/j.amjsurg.2008.12.031 · Cited by 241 · see citing works
Serum Biomarker Panels for the Detection of Pancreatic Cancer
Brand, R. E., Nolen, B. M., Zeh, H. J., Allen, P. J., Eloubeidi, M. A., Goldberg, M. J., Elton, E., Arnoletti, J. P., Christein, J. D., Vickers, S. M., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-0248 · Cited by 240 · see citing works
O'Brien, D. P., Sandanayake, N. S., Jenkinson, C., Gentry-Maharaj, A., Apostolidou, S., Fourkala, E.-O., Camuzeaux, S., Blyuss, O., Gunu, R., Dawnay, A., et al. (2015) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-14-0365 · Cited by 200 · see citing works
Self-citationVarma, V., Yao-Borengasser, A., Bodles, A. M., Rasouli, N., Phanavanh, B., Nolen, G. T., Kern, E. M., Nagarajan, R., Spencer, H. J., Lee, M.-J., et al. (2008) · Diabetes · doi:10.2337/db07-0840 · Cited by 194 · see citing works
New biomarkers and targets in pancreatic cancer and their application to treatment
Costello, E., Greenhalf, W., & Neoptolemos, J. P. (2012) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2012.119 · Cited by 192 · see citing works
Self-citationAggarwal, G., Ramachandran, V., Javeed, N., Arumugam, T., Dutta, S. K., Klee, G. G., Klee, E. W., Smyrk, T. C., Bamlet, W. R., Han, J., et al. (2012) · Gastroenterology · doi:10.1053/j.gastro.2012.08.044 · Cited by 170 · see citing works
Recruitment to multicentre trials—lessons from UKCTOCS: descriptive study
Menon, U., Gentry-Maharaj, A., Ryan, A., Sharma, A., Burnell, M., Hallett, R., Lewis, S., Lopez, A., Godfrey, K., Oram, D., et al. (2008) · BMJ · doi:10.1136/bmj.a2079 · Cited by 151 · see citing works
Self-citationGlycoprotein biomarker panel for pancreatic cancer discovered by quantitative proteomics analysis
Nie, S., Lo, A., Wu, J., Zhu, J., Tan, Z., Simeone, D. M., Anderson, M. A., Shedden, K. A., Ruffin, M. T., & Lubman, D. M. (2014) · Journal of Proteome Research · doi:10.1021/pr400967x · Cited by 128 · see citing works
Dudek, A. Z., & Mahaseth, H. (2005) · Cancer Investigation · doi:10.1081/cnv-200055949 · Cited by 99 · see citing works
Wong, D., Ko, A. H., Hwang, J. J., Venook, A. P., Bergsland, E. K., & Tempero, M. A. (2008) · Pancreas · doi:10.1097/mpa.0b013e31816d8185 · Cited by 89 · see citing works
Bigbee, W. L., Gopalakrishnan, V., Weissfeld, J. L., Wilson, D. O., Đačić, S., Lokshin, A. E., & Siegfried, J. M. (2012) · Journal of Thoracic Oncology · doi:10.1097/jto.0b013e31824ab6b0 · Cited by 84 · see citing works
Thrombospondin-1: An Islet Endothelial Cell Signal of Importance for β-Cell Function
Olerud, J., Mokhtari, D., Johansson, M., Christoffersson, G., Lawler, J., Welsh, N., & Carlsson, P. (2011) · Diabetes · doi:10.2337/db10-0277 · Cited by 84 · see citing works
Menon, R., Zhang, Q. H., Zhang, Y., Fermin, D., Bardeesy, N. M., DePinho, R. A., Lü, C., Hanash, S., Omenn, G. S., & States, D. J. (2008) · Cancer Research · doi:10.1158/0008-5472.can-08-2145 · Cited by 74 · see citing works
Walsh, J., Jenkins, R. E., Wong, M. H. L., Olayanju, A., Powell, H., Copple, I. M., O’Neill, P. M., Goldring, C. E., Kitteringham, N. R., & Park, B. K. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.05.007 · Cited by 71 · see citing works
Self-citationTonack, S., Jenkinson, C., Cox, T., Elliott, V, Jenkins, R. E., Kitteringham, N. R., Greenhalf, W., Shaw, V, Michalski, C. W., Friess, H., et al. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.150 · Cited by 70 · see citing works
Self-citationTherapies using anti-angiogenic peptide mimetics of thrombospondin-1
Henkin, J., & Volpert, O. V. (2011) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2011.640319 · Cited by 58 · see citing works
Suh, E. J., Kabir, M. H., Kang, U., Lee, J. W., Yu, J., Noh, D., & Lee, C. (2012) · Experimental & Molecular Medicine · doi:10.3858/emm.2012.44.1.003 · Cited by 56 · see citing works
Jenkinson, C., Elliott, V., Menon, U., Apostolidou, S., Fourkala, O. E., Gentry‐Maharaj, A., Pereira, S. P., Jacobs, I. J., Cox, T. F., Greenhalf, W., et al. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.10.001 · Cited by 51 · see citing works
Self-citationA technically detailed and pragmatic protocol for quantitative serum proteomics using iTRAQ
Tonack, S., Aspinall-O’Dea, M., Jenkins, R. E., Elliot, V., Murray, S., Lane, C. S., Kitteringham, N. R., Neoptolemos, J. P., & Costello, E. (2009) · Journal of Proteomics · doi:10.1016/j.jprot.2009.07.009 · Cited by 51 · see citing works
Self-citationMiyata, Y., & Sakai, H. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140612249 · Cited by 49 · see citing works
Function‐blocking antithrombospondin‐1 monoclonal antibodies
Annis, D. S., Murphy-Ullrich, J. E., & Mosher, D. F. (2006) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2006.01723.x · Cited by 47 · see citing works
Yan, L., Tonack, S., Smith, R., Dodd, S., Jenkins, R. E., Kitteringham, N., Greenhalf, W., Ghaneh, P., Neoptolemos, J. P., & Costello, E. (2009) · Journal of Proteome Research · doi:10.1021/pr800451h · Cited by 44 · see citing works
Self-citationBiomarkers for early diagnosis of pancreatic cancer
Jenkinson, C., Earl, J., Ghaneh, P., Halloran, C., Carrato, A., Greenhalf, W., Neoptolemos, J., & Costello, E. (2015) · Expert Review of Gastroenterology & Hepatology · doi:10.1586/17474124.2015.965145 · Cited by 42 · see citing works
Self-citation[Supplemental role of thrombospondin-1 in the diagnosis of prostate cancer].
Lü, J., Ye, D. W., Li, W. Z., Du, L.-H., Jin, W., Lu, X. Q., Zhang, J. H., & Chen, G. (2013) · PubMed · Cited by 2 · see citing works
Flagged first, then by citations
2 of the 33 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Goggins, M., Overbeek, K. A., Brand, R., Syngal, S., Del Chiaro, M., Bartsch, D. K., Bassi, C., Carrato, A., Farrell, J., Fishman, E. K., et al. (2020) · Gut · doi:10.1136/gutjnl-2019-319352 · Cited by 659 · see citing works
Early detection of pancreatic cancer
Pereira, S. P., Oldfield, L., Ney, A., Hart, P. A., Keane, M. G., Pandol, S. J., Li, D., Greenhalf, W., Jeon, C. Y., Koay, E. J., et al. (2020) · The Lancet Gastroenterology & Hepatology · doi:10.1016/s2468-1253(19)30416-9 · Cited by 482 · see citing works
Self-citationRoles 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 · see citing works
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 · see citing works
Analysis of the plasma proteome using iTRAQ and TMT-based Isobaric labeling.
Moulder, R., Bhosale, S. D., Goodlett, D., & Lahesmaa, R. (2018) · Mass spectrometry reviews (Print) · doi:10.1002/mas.21550 · Cited by 131 · see citing works
Serum biomarker signature-based liquid biopsy for diagnosis of early-stage pancreatic cancer
Mellby, L. D., Nyberg, A. P., Johansen, J. S., Wingren, C., Nordestgaard, B. G., Bojesen, S. E., Mitchell, B. L., Sheppard, B. C., Sears, R. C., & Borrebaeck, C. A. K. (2018) · Journal of Clinical Oncology · doi:10.1200/jco.2017.77.6658 · Cited by 159 · see citing works
Biomarkers 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 · see citing works
Diabetes and pancreatic cancer: Exploring the two-way traffic
Roy, A., Sahoo, J., Kamalanathan, S., Naik, D., Mohan, P., & Kalayarasan, R. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i30.4939 · Cited by 104 · see citing works
Therapeutic trends in pancreatic ductal adenocarcinoma (PDAC)
Chandana, S. R., Babiker, H. M., & Mahadevan, D. (2018) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2019.1557145 · Cited by 98 · see citing works
Extracellular Vesicle Analysis Allows for Identification of Invasive IPMN
Yang, K. S., Ciprani, D., O’Shea, A., Liss, A. S., Yang, R., Fletcher-Mercaldo, S., Mino-Kenudson, M. A., Castillo, C. F. F.-D., & Weissleder, R. (2020) · Gastroenterology · doi:10.1053/j.gastro.2020.11.046 · Cited by 97 · see citing works
for the European Study Group for Pancreatic Cancer, Kleeff, J. H., Costello, E., Jackson, R., Halloran, C. M., Greenhalf, W., Ghaneh, P., Lamb, R. F., Lerch, M. M., Mayerle, J. V., et al. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.277 · Cited by 78 · see citing works
Self-citationYao, K., Wang, Q., Jia, J., & Zhao, H. (2017) · Tumor Biology · doi:10.1177/1010428317707882 · Cited by 61 · see citing works
Honda, K., Katzke, V. A., Hüsing, A., Okaya, S., Shoji, H., Onidani, K., Olsen, A., Tjønneland, A. M., Overvad, K., Weiderpass, E., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31900 · Cited by 59 · see citing works
Abbruzzese, J. L., Andersen, D. K., Borrebaeck, C. A. K., Chari, S. T., Costello, E., Cruz‐Monserrate, Z., Eibl, G., Engleman, E. G., Fisher, W. E., Habtezion, A., et al. (2018) · Pancreas · doi:10.1097/mpa.0000000000001037 · Cited by 54 · see citing works
Self-citationValidation 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 · see citing works
Lam, B., Shrivastava, S. K., Shrivastava, A., Shankar, S., & Srivastava, R. K. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15413 · Cited by 53 · see citing works
Familial Pancreatic Cancer: Current Perspectives
Llach, J., Carballal, S., & Moreira, L. (2020) · Cancer Management and Research · doi:10.2147/cmar.s172421 · Cited by 48 · see citing works
Brand, R. E., Persson, J., Bratlie, S. O., Chung, D. C., Katona, B. W., Carrato, A., Castillo, M., Earl, J., Kokkola, A., Lucas, A. L., et al. (2022) · Clinical and Translational Gastroenterology · doi:10.14309/ctg.0000000000000468 · Cited by 45 · see citing works
Lu, W., Li, N., & Liao, F. (2019) · Genes · doi:10.3390/genes10080612 · Cited by 44 · see citing works
Non-Invasive Biomarkers for Earlier Detection of Pancreatic Cancer—A Comprehensive Review
Brezgyte, G., Shah, V. M., Jach, D., & Crnogorac‐Jurcevic, T. (2021) · Cancers · doi:10.3390/cancers13112722 · Cited by 43 · see citing works
Bennike, T. B., Bellin, M. D., Xuan, Y., Stensballe, A., Møller, F. T., Beilman, G. J., Levy, O., Cruz‐Monserrate, Z., Andersen, V. C., Steen, J. A. J., et al. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.8b00111 · Cited by 41 · see citing works
Urine biomarkers enable pancreatic cancer detection up to 2 years before diagnosis
Debernardi, S., Blyuss, O. B., Rycyk, D., Srivastava, K., Jeon, C. Y., Cai, H., Cai, Q., Shu, X., & Crnogorac‐Jurcevic, T. (2022) · International Journal of Cancer · doi:10.1002/ijc.34287 · Cited by 39 · see citing works
Oldfield, L. S., Evans, A., Rao, R. G., Jenkinson, C., Purewal, T. S., Psarelli, E. E., Menon, U., Timms, J. F., Pereira, S. P., Ghaneh, P., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2021.103802 · Cited by 42 · see citing works
Self-citationProteomic biomarkers in body fluids associated with pancreatic cancer
Jiménez‐Luna, C., Torres, C., Ortíz, R., Diéguez-Castillo, C., Martínez-Galán, J., Melguizo, C., Prados, J. C., & Caba, O. (2018) · Oncotarget · doi:10.18632/oncotarget.24654 · Cited by 33 · see citing works
de Oliveira, G., Freire, P. P., Cury, S. S., de Moraes, D., Oliveira, J. S., Dal‐Pai‐Silva, M., Reis, P. P., & Carvalho, R. F. (2020) · Cancers · doi:10.3390/cancers12030716 · Cited by 32 · see citing works
Pang, Y., Holmes, M. V., Chen, Z., & Kartsonaki, C. (2018) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.14576 · Cited by 28 · see citing works
Hanna-Sawires, R. G., Schiphuis, J. H., Wuhrer, M., Vasen, H. F. A., van Leerdam, M. E., Bonsing, B. A., Mesker, W. E., van der Burgt, Y. E. M., & Tollenaar, R. A. �. �. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22052655 · Cited by 27 · see citing works
Lucas, A. L., Simeone, D. M., Katona, B. W., Paiella, S., Zogopoulos, G., Sears, R. C., Grindedal, E. M., Wadlow, R. C., Borazanci, E. H., Gordon, O. K., et al. (2025) · Gastroenterology · doi:10.1053/j.gastro.2025.08.034 · Cited by 25 · see citing works
Matsumura, K., Hayashi, H., Uemura, N., Ogata, Y., Liu, Z., Sato, H., Shiraishi, Y., Kuroki, H., Kitamura, F., Kaida, T., et al. (2022) · Translational Oncology · doi:10.1016/j.tranon.2022.101533 · Cited by 25 · see citing works
Jia, K., Li, W., Wang, F., Qu, H., Qiao, Y., Zhou, L., Sun, Y., Ma, Q., & Zhao, X. (2016) · Oncotarget · doi:10.18632/oncotarget.8123 · Cited by 25 · see citing works
A metabolomics-based biomarker signature discriminates pancreatic cancer from chronic pancreatitis
Costello, E. (2017) · Gut · doi:10.1136/gutjnl-2016-313665 · Cited by 25 · see citing works
Self-citationRisk factors of pancreatic cancer and their possible uses in diagnostics
Lang, J., Kunovský, L., Kala, Z., & Trna, J. (2020) · Neoplasma · doi:10.4149/neo_2020_200706n699 · Cited by 20 · see citing works
The next “sweet” spot for pancreatic ductal adenocarcinoma: Glycoprotein for early detection
Xu, Y., Wang, Y., Höti, N., Clark, D. J., Chen, S., & Zhang, H. (2021) · Mass Spectrometry Reviews · doi:10.1002/mas.21748 · Cited by 22 · see citing works
Timms, J. F., Hale, O. J., & Cramer, R. (2016) · Expert Review of Proteomics · doi:10.1080/14789450.2016.1182431 · Cited by 18 · see citing works
Self-citationLiu, 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 · see citing works
Association of breast carcinoma growth with a non-canonical axis of IFNγ/IDO1/TSP1
Lopes-Bastos, B., Jin, L., Ruge, F., Owen, S., Sanders, A. J., Cogle, C. R., Chester, J. D., Jiang, W. G., & Cai, J. (2017) · Oncotarget · doi:10.18632/oncotarget.18781 · Cited by 17 · see citing works
Omics Approaches in Pancreatic Adenocarcinoma
González‐Borja, I., Viúdez, A., Goñi, S., Santamaría, E., Carrasco‐García, E., Pérez‐Sanz, J., Hernández-García, I., Elarre, P. S., Arrazubi, V., Oyaga-Iriarte, E., et al. (2019) · Cancers · doi:10.3390/cancers11081052 · Cited by 16 · see citing works
Cintas, C., Douché, T., Therville, N., Arcucci, S., Ramos‐Delgado, F., Basset, C., Thibault, B., & Guillermet‐Guibert, J. (2018) · Cancers · doi:10.3390/cancers10060174 · Cited by 15 · see citing works
Pekarek, L., Fraile‐Μartinez, O., Montero, C. G., Álvarez-Mon, M. Á., Acero, J., Ruiz‑Llorente, L., García‐Honduvilla, N., Albillos, A., Buján, J., Álvarez‐Mon, M., et al. (2021) · Oncology Letters · doi:10.3892/ol.2021.13070 · Cited by 15 · see citing works
Proteomics in pancreatic cancer
Cai, F., Gu, Y., Ling, Y., Yi, G., Zang, S., Su, T., Liu, Y., Li, A., Wang, D., Zhao, W., et al. (2025) · Biomarker Research · doi:10.1186/s40364-025-00805-y · Cited by 14 · see citing works
Pancreatic Cancer–Associated Diabetes is Clinically Distinguishable From Conventional Diabetes
Yoon, B. H., Ang, S. M., Alabd, A., Furlong, K., Yeo, C. J., Lavu, H., & Winter, J. M. (2021) · Journal of Surgical Research · doi:10.1016/j.jss.2020.12.015 · Cited by 13 · see citing works
Nakao, Y., Nakagawa, S., Yamashita, Y., Umezaki, N., Okamoto, Y., Ogata, Y., Yasuda‐Yoshihara, N., Itoyama, R., Yusa, T., Yamashita, K., et al. (2021) · Annals of Surgical Oncology · doi:10.1245/s10434-020-09383-9 · Cited by 14 · see citing works
Matricellular proteins and survival in patients with pancreatic cancer: A systematic review
Fiorino, S., Reggiani, M. L. B., Birtolo, C., Acquaviva, G., Visani, M., Fornelli, A., Masetti, M., Tura, A., Sbrignadello, S., Grizzi, F., et al. (2017) · Pancreatology · doi:10.1016/j.pan.2017.11.001 · Cited by 11 · see citing works
The Past, Present, and Future of Biomarkers for the Early Diagnosis of Pancreatic Cancer
Vitale, F., Verme, L. Z. D., Paratore, M., Negri, M., Nista, E. C., Ainora, M. E., Esposto, G., Mignini, I., Borriello, R., Galasso, L., et al. (2024) · Biomedicines · doi:10.3390/biomedicines12122840 · Cited by 12 · see citing works
Palma, N. A., Lucas, A. L., Katona, B. W., Athanasiou, A., Kureshi, N. M., Ford, L., Keller, T., Weber, S., Schiess, R., King, T. C., et al. (2025) · Cancers · doi:10.3390/cancers17111866 · Cited by 10 · see citing works
Xu, T., Xu, X., Liu, P., Mao, H. Z., & Ju, S. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.563527 · Cited by 10 · see citing works
Juthani, R., & Manne, A. (2025) · Frontiers in Oncology · doi:10.3389/fonc.2025.1555963 · Cited by 11 · see citing works
Liu, J., Wang, S., Hou, J., Cai, H., Pan, W., Dong, H., Sun, R., Dong, H., Fang, S., & Yu, B. (2020) · Circulation Journal · doi:10.1253/circj.cj-19-1206 · Cited by 9 · see citing works
Zhang, Z., Qin, W., & Sun, Y. (2018) · Pathology - Research and Practice · doi:10.1016/j.prp.2018.10.003 · Cited by 9 · see citing works
Biliary Obstruction: Endoscopic Approaches
Davee, T. R., & Lee, J. (2017) · Seminars in Interventional Radiology · doi:10.1055/s-0037-1608828 · Cited by 8 · see citing works
Coleman, O., Henry, M. A., McVey, G., CLYNES, M. M., Moriarty, M. J., & Meleady, P. (2016) · Expert Review of Proteomics · doi:10.1586/14789450.2016.1167601 · Cited by 8 · see citing works
miR-1246 Promotes Laryngeal Squamous Cell Carcinoma Progression by Interacting with THBS1
Wu, L., Zuo, N., Pan, S., Wang, Y., Wang, Q., & Ma, J. (2022) · Journal of Environmental Pathology Toxicology and Oncology · doi:10.1615/jenvironpatholtoxicoloncol.2022040516 · Cited by 7 · see citing works
Recent advances in proteomic profiling of pancreatic ductal adenocarcinoma and the road ahead
Kim, H., Park, J., Wang, J. I., & Kim, Y. (2017) · Expert Review of Proteomics · doi:10.1080/14789450.2017.1382356 · Cited by 7 · see citing works
Proteomic analysis of psoriatic skin lesions in a Chinese population
Wang, W., Xu, Q., Li, B., Li, H., Shen, S., Wu, J., Ge, H., Zhang, H., Chen, S., Chen, W., et al. (2021) · Journal of Proteomics · doi:10.1016/j.jprot.2021.104207 · Cited by 7 · see citing works
Proteomic analysis of pancreatic ductal adenocarcinoma
Meleady, P., Rahman, R. A., Henry, M. A., Moriarty, M. J., & CLYNES, M. M. (2020) · Expert Review of Proteomics · doi:10.1080/14789450.2020.1803743 · Cited by 6 · see citing works
Rao, R., Gulfishan, M., Kim, M., & Kashyap, M. K. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-4152-1_12 · Cited by 5 · see citing works
Yousefli, Z., Rafiee, N., Nourollahian, T., Alipour, A., Haghshenas, Z., Islampanah, M., Khazaei, M., Fiuji, H., Hassanian, S. M., Ferns, G. A., et al. (2025) · Pathology - Research and Practice · doi:10.1016/j.prp.2025.156045 · Cited by 5 · see citing works
Polanco, P. M., Gonda, T. A., Borazanci, E. H., Glazer, E. S., Trevino, J. G., DeMuth, G., Ford, L. A., King, T. C., Palma, N. A., & Brand, R. E. (2025) · Current Oncology · doi:10.3390/curroncol32110638 · Cited by 5 · see citing works
Blood-Based Biomarkers in the Diagnosis and Risk Stratification of Pancreatic Cysts
Peller, M. T., & Das, K. K. (2023) · Gastrointestinal Endoscopy Clinics of North America · doi:10.1016/j.giec.2023.03.009 · Cited by 5 · see citing works
Xia, H., Feng, L., Lin, L., Jiang, Z., Chen, J., Shi, W., Ying, S., Yu, M., Ju, L., Zhu, L., et al. (2020) · Environmental Research · doi:10.1016/j.envres.2020.110467 · Cited by 5 · see citing works
Pescatore, R., Milliken, N., King, T. C., Josey, D., Palma, N. A., & Ford, L. A. (2025) · Diagnostics · doi:10.3390/diagnostics15243177 · Cited by 4 · see citing works
Biomarkers for the Early Detection of Pancreatic Ductal Adenocarcinoma
Borrebaeck, C. A. K., Mellby, L. D., & King, T. C. (2022) · Exon Publications eBooks · doi:10.36255/exon-publications-gastrointestinal-cancers-biomarkers-pancreatic-cancer · Cited by 4 · see citing works
Buanes, T. A. (2016) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i48.10502 · Cited by 4 · see citing works
Jallod, I. M. S., Abbas, A. K., Yaqoob, F. I., & Aziz, A.-A. A. (2025) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-025-04209-5 · Cited by 3 · see citing works
BTNL9 exerts anti-cancer effects by inhibiting CDC20 to induce G2/M arrest in pancreatic cancer
Xiao, M., Luo, Z., Yu, A.-R., Xu, K., & Zhou, W. (2025) · World Journal of Gastrointestinal Oncology · doi:10.4251/wjgo.v17.i7.108274 · Cited by 3 · see citing works
Pancreatic Cancer Screening in Patients with Type 2 Diabetes Mellitus: A Narrative Review
Danilă, M., Ghiuchici, A.-M., Bende, R., Rațiu, I., & Bende, F. (2025) · Medicina · doi:10.3390/medicina62010067 · Cited by 3 · see citing works
The endoscopist’s role in the diagnosis and management of pancreatic cancer
Lee, J. H., Cassani, L. S., Bhosale, P., & Ross, W. A. (2016) · Expert Review of Gastroenterology & Hepatology · doi:10.1080/17474124.2016.1176910 · Cited by 3 · see citing works
Mass spectrometry–based proteomics technology in pancreatic cancer research
Sun, X. J., Wang, S., & Wong, C. C. L. (2023) · Journal of Pancreatology · doi:10.1097/jp9.0000000000000152 · Cited by 3 · see citing works
Development of Novel Diagnostic Pancreatic Tumor Biomarkers
Oldfield, L. S., Rao, R. G., Barrera, L. N., & Costello, E. (2018) · Springer eBooks · doi:10.1007/978-1-4939-7193-0_86 · Cited by 3 · see citing works
Self-citationPrediagnostic blood biomarkers for pancreatic cancer: meta-analysis
Bengtsson, A., Draus, T., Andersson, R., & Ansari, D. (2024) · BJS Open · doi:10.1093/bjsopen/zrae046 · Cited by 2 · see citing works
Primary and Secondary Prevention of Pancreatic Cancer
Yu, A., Romero, T., & Genkinger, J. M. (2019) · Current Epidemiology Reports · doi:10.1007/s40471-019-00189-2 · Cited by 2 · see citing works
Kahlert, C., Distler, M., Aust, D. E., Gieldon, L., Weitz, J., & Welsch, T. (2017) · Der Chirurg · doi:10.1007/s00104-017-0569-y · Cited by 2 · see citing works
Mahajan, D., & Pandey, A. K. (2024) · Asian Pacific Journal of Cancer Biology · doi:10.31557/apjcb.2024.9.1.61-66 · Cited by 2 · see citing works
New‐onset Diabetes as a Harbinger of Pancreatic Cancer: is Early Diagnosis Possible?
Andersen, D. K., Chari, S. T., Costello, E., Crnogorac‐Jurcevic, T., Hart, P. A., Maitra, A., & Pandol, S. J. (2021) · doi:10.1002/9781119570097.ch51 · Cited by 2 · see citing works
Self-citationCarrara, S., Archibugi, L., Terrin, M., Secchettin, E., Luca, R. D., & Paiella, S. (2026) · Digestive and Liver Disease · doi:10.1016/j.dld.2026.04.007 · Cited by 1 · see citing works
Development of Novel Diagnostic Pancreatic Tumor Biomarkers 2nd ed
Oldfield, L. S., Rao, R. G., Barrera, L. N., & Costello, E. (2017) · Springer eBooks · doi:10.1007/978-1-4939-6631-8_86-1 · Cited by 1 · see citing works
Self-citationSecondary Screening for Inherited Pancreatic Ductal Adenocarcinoma
Sheel, A., Nicholson, J., Sarantitis, I., Neoptolemos, J. P., & Greenhalf, W. (2018) · Springer eBooks · doi:10.1007/978-1-4939-7193-0_63 · Cited by 1 · see citing works
Self-citationPancreatic cancer, pancreatogenic diabetes, type 2 diabetes mellitus
Друк, И. В. (2022) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-205-9-171-182 · Cited by 1 · see citing works
Metabolic Biomarkers of Pancreatic Cancer
Mahajan, U. M., Li, Q., Kamlage, B., Lerch, M. M., & Mayerle, J. V. (2020) · Molecular and translational medicine · doi:10.1007/978-3-030-49476-6_5 · Cited by 1 · see citing works
Secondary Screening for Inherited Pancreatic Ductal Adenocarcinoma
Sheel, A., Nicholson, J., Sarantitis, I., Neoptolemos, J. P., & Greenhalf, W. (2017) · Springer eBooks · doi:10.1007/978-1-4939-6631-8_63-1
Self-citationCintas, C., Douché, T., & Guillermet‐Guibert, J. (2018) · Preprints.org · doi:10.20944/preprints201802.0013.v1
Challenges and Opportunities for Early Pancreatic Cancer Detection: Role for Protein Biomarkers
Oldfield, L. S., Barrera, L. N., Williams, D., Evans, A., Neoptolemos, J. P., & Costello, E. (2020) · Molecular and translational medicine · doi:10.1007/978-3-030-49476-6_4
Self-citationComputer-Aided Diagnosis of Pancreatic Ductal Adenocarcinoma Using Machine Learning Techniques
Saraswathi, H. S., Rafi, M., Manjunath, K., & Raju, C. K. (2021) · Advances in intelligent systems and computing · doi:10.1007/978-981-16-5157-1_74
Cintas, C., Douché, T., & Guillermet‐Guibert, J. (2018) · Preprints.org · doi:10.20944/preprints201802.0011.v1
A Machine Learning Prediction Model for Type 2 Diabetes Mellitus Associated Pancreatic CancerPreprint
Seth, S., Chaudhary, K., & Ramachandran, S. (2024) · SSRN Electronic Journal · doi:10.2139/ssrn.5036037
Les cellules sénecentes comme niche de survie : rôle de la voie TSP1-CD47
Moreau, M. (2017) · theses.fr (ABES) · doi:10.70675/e62d69b6z1f00z4f88z817bzda54e624150f
- Authors
- Jenkinson, C., Elliott, V. L., Evans, A., Oldfield, L., Jenkins, R. E., O'Brien, D. P., Apostolidou, S., Gentry-Maharaj, A., Fourkala, E.-O., Jacobs, I. J., Menon, U., Cox, T., Campbell, F., Pereira, S. P., Tuveson, D. A., Park, B. K., Greenhalf, W., Sutton, R., Timms, J. F., Neoptolemos, J. P., & Costello, E.
- Affiliations
- University of Liverpool (GB)
- University College London (GB)
- 4Department of Women's Cancer, Institute for Women's Health, University College London, United Kingdom.
- University of Manchester (GB)
- Cold Spring Harbor Laboratory (US)
- Corresponding author
- Costello, Eithne
- ORCID
- Venue
- Clinical Cancer Research
- Published
- 2016-03-31
- Volume
- 22
- Issue
- 7
- Pages
- 1734-1743
- ISSN
- 1078-0432 (ISSN-L)
- 1557-3265
- PMC
- PMC4820087
- OpenAlex
- W2173639106
- Cited by
- 87
- References
- 33
- Citations by year
- 2026: 1 · 2025: 10 · 2024: 5 · 2023: 2 · 2022: 7 · 2021: 11 · 2020: 14 · 2019: 4 · 2018: 14 · 2017: 13 · 2016: 6
- FWCI
- 4.80
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Clinical Cancer Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (submittedVersion)
- Funders
- Northwest Cancer Research Fund, UK, grant CR976, The National Institute for Health Research Pancreas Biomedical Research Unit, Cancer Research UK (FP7/2007-2013)
- Topics
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Health Sciences › Medicine › Surgery › Pancreatitis Pathology and Treatment
- Health Sciences › Medicine › Surgery › Cholangiocarcinoma and Gallbladder Cancer Studies
- Keywords
- thrombospondin-1, pancreatic ductal adenocarcinoma, early diagnosis, serum biomarkers, CA19-9, type 2 diabetes, preclinical disease, survival, chronic pancreatitis, benign biliary obstruction, KPC mouse model
- MeSH terms
- Aged, Animals, Diabetes Mellitus, Type 2, Disease Models, Animal, Female, Humans, Male, Middle Aged, Neoplasm Staging, Pancreatic Neoplasms, Platelet Count, Time Factors, Biomarkers, Tumor, Reproducibility of Results, Case-Control Studies, Thrombospondin 1, Carcinoma, Pancreatic Ductal, Proteomics, Mice, Early Detection of Cancer, Patient Outcome Assessment
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
