Improving pancreatic cancer diagnosis using circulating tumor cells: Prospects for staging and single-cell analysis

Expert Review of Molecular Diagnostics

Volumn 15, Issue 11, 2015, Pages 1491-1504

  Court, Colin M ^a,b   Ankeny, Jacob S ^a,b   Hou, Shuang ^a   Tseng, Hsian Rong ^c   Tomlinson, James S ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

biomarker; circulating tumor cells; diagnosis; liquid biopsy; pancreatic cancer; personalized medicine; precision medicine; single cell sequencing; staging

Indexed keywords

ANTINEOPLASTIC AGENT; TUMOR MARKER;

ARTICLE; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RESEARCH; CANCER SCREENING; CANCER STAGING; CANCER SURGERY; CIRCULATING TUMOR CELL; CLINICAL TRIAL (TOPIC); HUMAN; IMMUNOCYTOCHEMISTRY; META ANALYSIS (TOPIC); MOLECULAR BIOLOGY; MOLECULAR DIAGNOSIS; MULTIMODALITY CANCER THERAPY; NONHUMAN; PANCREAS CANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE CELL ANALYSIS; TUMOR BIOPSY; EARLY CANCER DIAGNOSIS; GENETICS; METABOLISM; PANCREATIC NEOPLASMS; PATHOLOGY; PERSONALIZED MEDICINE; PROCEDURES; PROGNOSIS; TUMOR EMBOLISM;

BIOMARKERS, TUMOR; EARLY DETECTION OF CANCER; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; NEOPLASM STAGING; NEOPLASTIC CELLS, CIRCULATING; PANCREATIC NEOPLASMS; PRECISION MEDICINE; PROGNOSIS; SINGLE-CELL ANALYSIS;

EID: 84947129864     PISSN: 14737159     EISSN: 17448352     Source Type: Journal    
DOI: 10.1586/14737159.2015.1091311     Document Type: Article

References (81)

1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. Cancer J Clin 2015; 65 (1): 5-29
2. Howlader N, Noone A, Krapcho M, et al. SEER cancer statistics review, 1975-2011. National Cancer Institute; Bethesda, MD, USA: 2014
3. Porta M, Fabregat X, Malats N, et al. Exocrine pancreatic cancer: symptoms at presentation and their relation to tumour site and stage. Clin Transl Oncol 2005; 7 (5): 189-97
4. Merchea A, Cullinane DC, Sawyer MD, et al. Esophagogastroduodenoscopy-associated gastrointestinal perforations: a single-center experience. Surgery 2010; 148 (4): 876-80; discussion 881-872
5. Bournet B, Selves J, Grand D, et al. Endoscopic ultrasound-guided fine-needle aspiration biopsy coupled with a KRAS mutation assay using allelic discrimination improves the diagnosis of pancreatic cancer. J Clin Gastroenterol 2015; 49 (1): 50-6
6. Edge SBB, Compton CC, Fritz AG, et al. AJCC cancer staging manual. Springer, NY; 2010
7. Tempero MA, Arnoletti JP, Behrman S, et al. Pancreatic adenocarcinoma. JNCCN 2010; 8 (9): 972-1017
8. Winter JM, Cameron JL, Campbell KA, et al. 1423 pancreaticoduodenectomies for pancreatic cancer: A single-institution experience. J Gastrointestinal surg 2006; 10 (9): 1199-210; discussion 1210-1191
9. Rochefort MM, Ankeny JS, Kadera BE, et al. Impact of tumor grade on pancreatic cancer prognosis: validation of a novel TNMG staging system. Ann Surg Oncol 2013; 20 (13): 4322-9
10. Girgis MD, Olafsen T, Kenanova V, et al. CA19-9 as a potential target for radiolabeled antibody-based positron emission tomography of pancreas cancer. Int J Mol Imaging 2011; 2011: 834515
11. Collisson E, Tempero M. Blinded by the light: molecular imaging in pancreatic adenocarcinoma. Clin Cancer Res 2011; 17 (2): 203-5
12. Merkow RP, Bilimoria KY, Tomlinson JS, et al. Postoperative complications reduce adjuvant chemotherapy use in resectable pancreatic cancer. Ann Surg 2014; 260 (2): 372-7
13. Conroy T, Desseigne F, Ychou M, et al. FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. N Engl J Med 2011; 364 (19): 1817-25
14. Von Hoff DD, Ervin T, Arena FP, et al. Increased survival in pancreatic cancer with nab-paclitaxel plus gemcitabine. N Engl J Med 2013; 369 (18): 1691-703
15. Donahue TR, Isacoff WH, Hines OJ, et al. Downstaging chemotherapy and alteration in the classic computed tomography/magnetic resonance imaging signs of vascular involvement in patients with pancreaticobiliary malignant tumors: influence on patient selection for surgery. Arch Surg 2011; 146 (7): 836-43
16. Matthaei H, Hong SM, Mayo SC, et al. Presence of pancreatic intraepithelial neoplasia in the pancreatic transection margin does not influence outcome in patients with R0 resected pancreatic cancer. Ann Surg Oncol 2011; 18 (12): 3493-9
17. Becker AE, Hernandez YG, Frucht H, Lucas AL. Pancreatic ductal adenocarcinoma: risk factors, screening, and early detection. World J Gastroenterol 2014; 20 (32): 11182-98
18. Langer P, Kann PH, Fendrich V, et al. Five years of prospective screening of high-risk individuals from families with familial pancreatic cancer. Gut 2009; 58 (10): 1410-18
19. Jones S, Zhang X, Parsons DW, et al. Core signaling pathways in human pancreatic cancers revealed by global genomic analyses. Science 2008; 321 (5897): 1801-6
20. Bardeesy N, DePinho RA. Pancreatic cancer biology and genetics. Nat Rev Cancer 2002; 2 (12): 897-909
21. Vincent A, Herman J, Schulick R, et al. Pancreatic cancer. Lancet 2011; 378 (9791): 607-20
22. Harsha HC, Kandasamy K, Ranganathan P, et al. A compendium of potential biomarkers of pancreatic cancer. PLoS Med 2009; 6 (4): e1000046
23. Winter JM, Yeo CJ, Brody JR. Diagnostic, prognostic, and predictive biomarkers in pancreatic cancer. J Surg Oncol 2013; 107 (1): 15-22
24. Pleskow DK, Berger HJ, Gyves J, et al. Evaluation of a serologic marker, CA19-9, in the diagnosis of pancreatic cancer. Ann Intern Med 1989; 110 (9): 704-9
25. Yachida S, Jones S, Bozic I, et al. Distant metastasis occurs late during the genetic evolution of pancreatic cancer. Nature 2010; 467 (7319): 1114-17
26. Campbell PJ, Yachida S, Mudie LJ, et al. The patterns and dynamics of genomic instability in metastatic pancreatic cancer. Nature 2010; 467 (7319): 1109-13
27. Boadas J, Mora J, Urgell E, et al. Clinical usefulness of K-ras gene mutation detection and cytology in pancreatic juice in the diagnosis and screening of pancreatic cancer. Eur J Gastroenterol Hepatol 2001; 13 (10): 1153-9
28. Parkinson DR, Dracopoli N, Petty BG, et al. Considerations in the development of circulating tumor cell technology for clinical use. J Transl Med 2012; 10: 138
29. Altman DG, McShane LM, Sauerbrei W, Taube SE. Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK): explanation and elaboration. PLoS Med 2012; 9 (5): e1001216
30. Ashworth T. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Aust Med J 1869; 14 (3): 146-9
31. Allard WJ, Matera J, Miller MC, et al. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin Can Res 2004; 10 (20): 6897-904
32. Liu S, Li N, Yu X, et al. on of intercellular adhesion molecule 1 by hepatocellular carcinoma stem cells and circulating tumor cells. Gastroenterology 2013; 144 (5): 1031-1041 e1010
33. Alix-Panabieres C. EPISPOT assay: detection of viable DTCs/CTCs in solid tumor patients. Recent results in cancer research. Fortschritte der Krebsforschung. Prog dans les recherches sur le cancer 2012; 195: 69-76
34. Adams DL, Stefansson S, Haudenschild C, et al. Cytometric characterization of circulating tumor cells captured by microfiltration and their correlation to the cellsearch((R)) CTC test. J Inter Soci Analy Cytol 2015; 87 (2): 137-44
35. Fidler IJ. Metastasis: guantitative analysis of distribution and fate of tumor embolilabeled with 125 I-5-iodo-2-deoxyuridine. J Natl Cancer Inst 1970; 45 (4): 773-82
36. Luzzi KJ, MacDonald IC, Schmidt EE, et al. Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am J Pathol 1998; 153 (3): 865-73
37. Haber DA, Velculescu VE. Blood-based analyses of cancer: circulating tumor cells and circulating tumor DNA. Cancer Discov 2014; 4 (6): 650-61
38. Balic M, Lin H, Williams A, et al. Progress in circulating tumor cell capture and analysis: implications for cancer management. Expert Rev Mol Diagn 2012; 12 (3): 303-12
39. Satelli A, Mitra A, Brownlee Z, et al. Epithelial-mesenchymal transitioned circulating tumor cells capture for detecting tumor progression. Clin Cancer Res 2015; 21 (4): 899-906
40. Xu W, Cao L, Chen L, et al. Isolation of circulating tumor cells in patients with hepatocellular carcinoma using a novel cell separation strategy. Clin Cancer Res 2011; 17 (11): 3783-93
41. Saucedo-Zeni N, Mewes S, Niestroj R, et al. A novel method for the in vivo isolation of circulating tumor cells from peripheral blood of cancer patients using a functionalized and structured medical wire. Int J Oncol 2012; 41 (4): 1241-50
42. Stott SL, Hsu CH, Tsukrov DI, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Nat Acad Sci USA 2010; 107 (43): 18392-7
43. Lustberg MB, Balasubramanian P, Miller B, et al. Heterogeneous atypical cell populations are present in blood of metastatic breast cancer patients. Breast Cancer Res 2014; 16 (2): R23
44. Pantel K, Deneve E, Nocca D, et al. Circulating epithelial cells in patients with benign colon diseases. Clin Chem 2012; 58 (5): 936-40
45. Van der Auwera I, Peeters D, Benoy IH, et al. Circulating tumour cell detection: a direct comparison between the CellSearch System, the AdnaTest and CK-19/mammaglobin RT-PCR in patients with metastatic breast cancer. Br J Cancer 2010; 102 (2): 276-84
46. Chausovsky G, Luchansky M, Figer A, et al. Expression of cytokeratin 20 in the blood of patients with disseminated carcinoma of the pancreas, colon, stomach, and lung. Cancer 1999; 86 (11): 2398-405
47. Soeth E, Grigoleit U, Moellmann B, et al. Detection of tumor cell dissemination in pancreatic ductal carcinoma patients by CK 20 RT-PCR indicates poor survival. J Cancer Res Clin Oncol 2005; 131 (10): 669-76
48. Hoffmann K, Kerner C, Wilfert W, et al. Detection of disseminated pancreatic cells by amplification of cytokeratin-19 with quantitative RT-PCR in blood, bone marrow and peritoneal lavage of pancreatic carcinoma patients. World J Gastroenterol 2007; 13 (2): 257-63
49. Uchikura K, Takao S, Nakajo A, et al. Intraoperative molecular detection of circulating tumor cells by reverse transcription-polymerase chain reaction in patients with biliary-pancreatic cancer is associated with hematogenous metastasis. Ann Surg Oncol 2002; 9 (4): 364-70
50. Mataki Y, Takao S, Maemura K, et al. Carcinoembryonic antigen messenger RNA expression using nested reverse transcription-PCR in the peripheral blood during follow-up period of patients who underwent curative surgery for biliary-pancreatic cancer: longitudinal analyses. Clin Cancer Res 2004; 10 (11): 3807-14
51. Zhou J, Hu L, Yu Z, et al. Marker expression in circulating cancer cells of pancreatic cancer patients. J Surg Res 2011; 171 (2): 631-6
52. de Albuquerque A, Kubisch I, Breier G, et al. Multimarker gene analysis of circulating tumor cells in pancreatic cancer patients: a feasibility study. Oncol 2012; 82 (1): 3-10
53. Kurihara T, Itoi T, Sofuni A, et al. Detection of circulating tumor cells in patients with pancreatic cancer: a preliminary result. J Hepatobiliary Pancreat Surg 2008; 15 (2): 189-95
54. Bidard FC, Huguet F, Louvet C, et al. Circulating tumor cells in locally advanced pancreatic adenocarcinoma: the ancillary CirCe 07 study to the LAP 07 trial. Ann Oncol 2013; 24 (8): 2057-61
55. ZGraggen K, Centeno BA, Fernandez-del Castillo C, et al. Biological implications of tumor cells in blood and bone marrow of pancreatic cancer patients. Surgery 2001; 129 (5): 537-46
56. Nagrath S, Sequist LV, Maheswaran S, et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature 2007; 450 (7173): 1235-9
57. Yu M, Ting DT, Stott SL, et al. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature 2012; 487 (7408): 510-13
58. Sheng W, Ogunwobi OO, Chen T, et al. Capture, release and culture of circulating tumor cells from pancreatic cancer patients using an enhanced mixing chip. Lab Chip 2014; 14 (1): 89-98
59. Rhim AD, Thege FI, Santana SM, et al. Detection of circulating pancreas epithelial cells in patients with pancreatic cystic lesions. Gastroenterology 2014; 146 (3): 647-51
60. Zhang Y, Wang F, Ning N, et al. Patterns of circulating tumor cells identified by CEP8, CK and CD45 in pancreatic cancer. Inter J Can 2015; 136 (5): 1228-33
61. Kamande JW, Hupert ML, Witek MA, et al. Modular microsystem for the isolation, enumeration, and phenotyping of circulating tumor cells in patients with pancreatic cancer. Anal Chem 2013; 85 (19): 9092-100
62. Khoja L, Backen A, Sloane R, et al. A pilot study to explore circulating tumour cells in pancreatic cancer as a novel biomarker. Br J Cancer 2012; 106 (3): 508-16
63. Iwanicki-Caron I, Basile P, Toure E, et al. Usefulness of circulating tumor cell detection in pancreatic adenocarcinoma diagnosis. Am J Gastroenterol 2013; 108 (1): 152-5
64. Kulemann B, Pitman MB, Liss AS, et al. Circulating tumor cells found in patients with localized and advanced pancreatic cancer. Pancreas 2015; 44 (4): 547-50
65. Bobek V, Gurlich R, Eliasova P, Kolostova K. Circulating tumor cells in pancreatic cancer patients: enrichment and cultivation. World J Gastroenterol 2014; 20 (45): 17163-70
66. Ren C, Han C, Zhang J, et al. Detection of apoptotic circulating tumor cells in advanced pancreatic cancer following 5-fluorouracil chemotherapy. Cancer Biol Ther 2011; 12 (8): 700-6
67. Ankeny J, Hou S, Lin M, et al. Pancreatic circulating tumor cells as a diagnostic adjunct in pancreatic cancer. In: Gastrointestinal cancers symposium. ASCO; 2014. p. 175
68. Eloubeidi MA, Chen VK, Eltoum IA, et al. Endoscopic ultrasound-guided fine needle aspiration biopsy of patients with suspected pancreatic cancer: diagnostic accuracy and acute and 30-day complications. Am J Gastroenterol 2003; 98 (12): 2663-8
69. Navin NE. Cancer genomics: one cell at a time. Genome Biol 2014; 15 (8): 452
70. Milos PM. Emergence of single-molecule sequencing and potential for molecular diagnostic applications. Expert Rev Mol Diagn 2009; 9 (7): 659-66
71. Heitzer E, Auer M, Gasch C, et al. Complex tumor genomes inferred from single circulating tumor cells by array-CGH and next-generation sequencing. Cancer Res 2013; 73 (10): 2965-75
72. Lohr JG, Adalsteinsson VA, Cibulskis K, et al. Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer. Nat Biotechnol 2014; 32 (5): 479-84
73. Ni X, Zhuo M, Su Z, et al. Reproducible copy number variation patterns among single circulating tumor cells of lung cancer patients. Proc Nat Acad Sci USA 2013; 110 (52): 21083-8
74. Hou S, Zhao L, Shen Q, et al. Polymer nanofiber-embedded microchips for detection, isolation, and molecular analysis of single circulating melanoma cells. Angewandte Chemie (International ed.in English) 2013; 52 (12): 3379-83
75. Polzer B, Medoro G, Pasch S, et al. Molecular profiling of single circulating tumor cells with diagnostic intention. EMBO molecular medicine 2014; 6 (11): 1371-86
76. Court C, Ankeny JS, Hou S, et al. Single cell mutational analysis of isolated circulating tumor cells in pancreatic cancer. Ann Surg Oncol 2015; 22 (1s): 1534-4681
77. Okada G, Watanabe H, Ohtsubo K, et al. Multiple factors influencing the release of hTERT mRNA from pancreatic cancer cell lines in in vitro culture. Cell Biol Int 2012; 36 (6): 545-53
78. Harewood GC, Wiersema MJ. A cost analysis of endoscopic ultrasound in the evaluation of pancreatic head adenocarcinoma. Am J Gastroenterol 2001; 96 (9): 2651-6
79. Medicaid CfMa. 2015 Medicare Clinical Laboratory Fee Schedule. (Ed.^(Eds) Center for Medicare and Medicaid, 2015
80. Brenner H, Gondos A, Arndt V. Recent major progress in long-term cancer patient survival disclosed by modeled period analysis. J Clin Oncol 2007; 25 (22): 3274-80
81. Coates RJ, Kolor K, Stewart SL, Richardson LC. Diagnostic markers for ovarian cancer screening: not ready for routine clinical use. Clin Cancer Res 2008; 14 (22): 7575-6; author reply 7577-7579