1,000
Views
22
CrossRef citations to date
0
Altmetric
Review

Liquid biopsies in pancreatic cancer

ORCID Icon, &
Pages 869-878 | Received 28 May 2019, Accepted 16 Sep 2019, Published online: 26 Sep 2019

References

  • Ionescu-Tirgoviste C, Gagniuc PA, Gubceac E, et al. A 3D map of the islet routes throughout the healthy human pancreas. Sci Rep. 2015 Sep 29;5:14634.
  • Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019 Jan;69(1):7–34.
  • Gillen S, Schuster T, Meyer Zum Buschenfelde C, et al. Preoperative/neoadjuvant therapy in pancreatic cancer: a systematic review and meta-analysis of response and resection percentages. PLoS Med. 2010 Apr 20;7(4):e1000267.
  • Kamisawa T, Wood LD, Itoi T, et al. Pancreatic cancer. Lancet. 2016 Jul 2;388(10039):73–85.
  • Chan A, Prassas I, Dimitromanolakis A, et al. Validation of biomarkers that complement CA19.9 in detecting early pancreatic cancer. Clin Cancer Res. 2014 Nov 15;20(22):5787–5795.
  • Kleeff J, Korc M, Apte M, et al. Pancreatic cancer. Nat Rev Dis Primers. 2016 Apr 21;2:16022.
  • Tang S, Huang G, Liu J, et al. Usefulness of 18F-FDG PET, combined FDG-PET/CT and EUS in diagnosing primary pancreatic carcinoma: a meta-analysis. Eur J Radiol. 2011 Apr;78(1):142–150.
  • Crowley E, Di Nicolantonio F, Loupakis F, et al. Liquid biopsy: monitoring cancer-genetics in the blood. Nat Rev Clin Oncol. 2013 Aug;10(8):472–484.
  • Glantz MJ, Cole BF, Glantz LK, et al. Cerebrospinal fluid cytology in patients with cancer: minimizing false-negative results. Cancer. 1998 Feb 15;82(4):733–739.
  • Gorgannezhad L, Umer M, Islam MN, et al. Circulating tumor DNA and liquid biopsy: opportunities, challenges, and recent advances in detection technologies. Lab Chip. 2018 Apr 17;18(8):1174–1196.
  • Anker P, Stroun M, Maurice PA. Spontaneous release of DNA by human blood lymphocytes as shown in an in vitro system. Cancer Res. 1975 Sep;35(9):2375–2382.
  • Stroun M, Lyautey J, Lederrey C, et al. About the possible origin and mechanism of circulating DNA apoptosis and active DNA release. Clin Chim Acta. 2001 Nov;313(1–2):139–142.
  • Schwarzenbach H, Hoon DS, Pantel K. Cell-free nucleic acids as biomarkers in cancer patients. Nat Rev Cancer. 2011 Jun;11(6):426–437.
  • Jahr S, Hentze H, Englisch S, et al. DNA fragments in the blood plasma of cancer patients: quantitations and evidence for their origin from apoptotic and necrotic cells. Cancer Res. 2001 Feb 15;61(4):1659–1665.
  • Diehl F, Li M, Dressman D, et al. Detection and quantification of mutations in the plasma of patients with colorectal tumors. Proc Natl Acad Sci U S A. 2005 Nov 8;102(45):16368–16373.
  • Thierry AR, Mouliere F, Gongora C, et al. Origin and quantification of circulating DNA in mice with human colorectal cancer xenografts. Nucleic Acids Res. 2010 Oct;38(18):6159–6175.
  • Sorenson GD, Pribish DM, Valone FH, et al. Soluble normal and mutated DNA sequences from single-copy genes in human blood. Cancer Epidemiol Biomarkers Prev. 1994 Jan-Feb;3(1):67–71.
  • Abbosh C, Birkbak NJ, Wilson GA, et al. Phylogenetic ctDNA analysis depicts early-stage lung cancer evolution. Nature. 2017 Apr 26;545(7655):446–451.
  • Beaver JA, Jelovac D, Balukrishna S, et al. Detection of cancer DNA in plasma of patients with early-stage breast cancer. Clin Cancer Res. 2014 May 15;20(10):2643–2650.
  • Diehl F, Schmidt K, Choti MA, et al. Circulating mutant DNA to assess tumor dynamics. Nat Med. 2008 Sep;14(9):985–990.
  • Kinugasa H, Nouso K, Miyahara K, et al. Detection of K-ras gene mutation by liquid biopsy in patients with pancreatic cancer. Cancer. 2015 Jul 1;121(13):2271–2280.
  • Jiang P, Lo YMD. The long and short of circulating cell-free DNA and the ins and outs of molecular diagnostics. Trends Genet. 2016 Jun;32(6):360–371.
  • Zhou Q, Zheng J, Qing Z, et al. Detection of circulating tumor DNA in human blood via DNA-mediated surface-enhanced Raman spectroscopy of single-walled carbon nanotubes. Anal Chem. 2016 May 3;88(9):4759–4765.
  • Shapiro B, Chakrabarty M, Cohn EM, et al. Determination of circulating DNA levels in patients with benign or malignant gastrointestinal disease. Cancer. 1983 Jun 1;51(11):2116–2120.
  • Sausen M, Phallen J, Adleff V, et al. Clinical implications of genomic alterations in the tumour and circulation of pancreatic cancer patients. Nat Commun. 2015 Jul 7;6:7686.
  • Pietrasz D, Pecuchet N, Garlan F, et al. Plasma circulating tumor DNA in pancreatic cancer patients is a prognostic marker. Clin Cancer Res. 2017 Jan 1;23(1):116–123.
  • Kulemann B, Pitman MB, Liss AS, et al. Circulating tumor cells found in patients with localized and advanced pancreatic cancer. Pancreas. 2015 May;44(4):547–550.
  • Tjensvoll K, Lapin M, Buhl T, et al. Clinical relevance of circulating KRAS mutated DNA in plasma from patients with advanced pancreatic cancer. Mol Oncol. 2016 Apr;10(4):635–643.
  • Cohen JD, Javed AA, Thoburn C, et al. Combined circulating tumor DNA and protein biomarker-based liquid biopsy for the earlier detection of pancreatic cancers. Proc Natl Acad Sci U S A. 2017 Sep 19;114(38):10202–10207.
  • Lee B, Lipton LR, Cohen J, et al. Circulating tumor DNA as a prognostic biomarker in early stage pancreatic cancer. J Clin Oncol. 2018;36(15_suppl):e16206–e16206.
  • Xu R, Rai A, Chen M, et al. Extracellular vesicles in cancer - implications for future improvements in cancer care. Nat Rev Clin Oncol. 2018 May 23;15:617–638.
  • Zhang L, Zhang S, Yao J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015 Nov 5;527(7576):100–104.
  • van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018 Apr;19(4):213–228.
  • Witwer KW, Buzas EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2:20360.
  • Maas SLN, Breakefield XO, Weaver AM. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol. 2017 Mar;27(3):172–188.
  • Consortium E-T, Van Deun J, Mestdagh P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017 Feb 28;14(3):228–232.
  • Pariset E, Agache V, Millet A. Extracellular vesicles: isolation methods. Adv Biosyst. 2017;1(5):1700040.
  • Coumans FA, van der Pol E, Boing AN, et al. Reproducible extracellular vesicle size and concentration determination with tunable resistive pulse sensing. J Extracell Vesicles. 2014;3:25922.
  • Woo HK, Sunkara V, Park J, et al. Exodisc for rapid, size-selective, and efficient isolation and analysis of nanoscale extracellular vesicles from biological samples. ACS Nano. 2017 Feb 28;11(2):1360–1370.
  • Liu F, Vermesh O, Mani V, et al. The Exosome Total Isolation Chip. ACS Nano. 2017 Nov 28;11(11):10712–10723.
  • Grant R, Ansa-Addo E, Stratton D, et al. A filtration-based protocol to isolate human plasma membrane-derived vesicles and exosomes from blood plasma. J Immunol Methods. 2011 Aug 31;371(1–2):143–151.
  • Davies RT, Kim J, Jang SC, et al. Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip. 2012 Dec 21;12(24):5202–5210.
  • Ibsen SD, Wright J, Lewis JM, et al. Rapid isolation and detection of exosomes and associated biomarkers from plasma. ACS Nano. 2017 Jul 25;11(7):6641–6651.
  • Chen C, Skog J, Hsu CH, et al. Microfluidic isolation and transcriptome analysis of serum microvesicles. Lab Chip. 2010 Feb 21;10(4):505–511.
  • Kanwar SS, Dunlay CJ, Simeone DM, et al. Microfluidic device (ExoChip) for on-chip isolation, quantification and characterization of circulating exosomes. Lab Chip. 2014 Jun 7;14(11):1891–1900.
  • Ko J, Bhagwat N, Yee SS, et al. Combining machine learning and nanofluidic technology to diagnose pancreatic cancer using exosomes. ACS Nano. 2017 Nov 28;11(11):11182–11193.
  • Castillo J, Bernard V, San Lucas FA, et al. Surfaceome profiling enables isolation of cancer-specific exosomal cargo in liquid biopsies from pancreatic cancer patients. Ann Oncol. 2018 Jan 1;29(1):223–229.
  • Reategui E, van der Vos KE, Lai CP, et al. Engineered nanointerfaces for microfluidic isolation and molecular profiling of tumor-specific extracellular vesicles. Nat Commun. 2018 Jan 12;9(1):175.
  • Wu M, Ouyang Y, Wang Z, et al. Isolation of exosomes from whole blood by integrating acoustics and microfluidics. Proc Natl Acad Sci U S A. 2017 Oct 3;114(40):10584–10589.
  • Zhang P, Zhou X, He M, et al. Ultrasensitive detection of circulating exosomes with a 3D-nanopatterned microfluidic chip. Nat Biomed Eng. 2019 Feb 25;3:438–451.
  • Melo SA, Luecke LB, Kahlert C, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015 Jul 9;523(7559):177–182.
  • Hu J, Sheng Y, Kwak KJ, et al. A signal-amplifiable biochip quantifies extracellular vesicle-associated RNAs for early cancer detection. Nat Commun. 2017 Nov 22;8(1):1683.
  • Lewis JM, Vyas AD, Qiu Y, et al. Integrated Analysis of Exosomal Protein Biomarkers on Alternating Current Electrokinetic Chips Enables Rapid Detection of Pancreatic Cancer in Patient Blood. ACS Nano. 2018 Apr 24;12(4):3311–3320.
  • Lai X, Wang M, McElyea SD, et al. A microRNA signature in circulating exosomes is superior to exosomal glypican-1 levels for diagnosing pancreatic cancer. Cancer Lett. 2017 May 1;393:86–93.
  • Allenson K, Castillo J, San Lucas FA, et al. High prevalence of mutant KRAS in circulating exosome-derived DNA from early-stage pancreatic cancer patients. Ann Oncol. 2017 Apr 1;28(4):741–747.
  • Yang S, Che SP, Kurywchak P, et al. Detection of mutant KRAS and TP53 DNA in circulating exosomes from healthy individuals and patients with pancreatic cancer. Cancer Biol Ther. 2017 Mar 4;18(3):158–165.
  • Bernard V, Kim DU, San Lucas FA, et al. Circulating nucleic acids are associated with outcomes of patients with pancreatic cancer. Gastroenterology. 2019 Jan;156(1):108–118 e4.
  • Ashworth TR. A case of cancer in which cells similar to those in the tumors were seen in the blood after death. Australasi Med J. 1869;14:146–149.
  • O’Flaherty JD, Gray S, Richard D, et al. Circulating tumour cells, their role in metastasis and their clinical utility in lung cancer. Lung Cancer. 2012 Apr;76(1):19–25.
  • DiPardo BJ, Winograd P, Court CM, et al. Pancreatic cancer circulating tumor cells: applications for personalized oncology. Expert Rev Mol Diagn. 2018 Sep;18(9):809–820.
  • Plaks V, Koopman CD, Werb Z. Circulating tumor cells. Science. 2013 Sep 13;341(6151):1186–1188.
  • Chaffer CL, Weinberg RA. A perspective on cancer cell metastasis. Science. 2011 Mar 25;331(6024):1559–1564.
  • Kamyabi N, Huang J, Lee JJ, et al. A microfluidic device for label-free isolation of tumor cell clusters from unprocessed blood samples. Biomicrofluidics. 2019 Jul;13(4):044111.
  • Fabisiewicz A, Grzybowska E. CTC clusters in cancer progression and metastasis. Med Oncol. 2017 Jan;34(1):12.
  • Arnoletti JP, Fanaian N, Reza J, et al. Pancreatic and bile duct cancer circulating tumor cells (CTC) form immune-resistant multi-cell type clusters in the portal venous circulation. Cancer Biol Ther. 2018 Aug;19(10):887–897.
  • Gall TM, Jacob J, Frampton AE, et al. Reduced dissemination of circulating tumor cells with no-touch isolation surgical technique in patients with pancreatic cancer. JAMA Surg. 2014 May;149(5):482–485.
  • Rhim AD, Mirek ET, Aiello NM, et al. EMT and dissemination precede pancreatic tumor formation. Cell. 2012 Jan 20;148(1–2):349–361.
  • Rhim AD, Thege FI, Santana SM, et al. Detection of circulating pancreas epithelial cells in patients with pancreatic cystic lesions. Gastroenterology. 2014 Mar;146(3):647–651.
  • Alix-Panabieres C, Pantel K. Circulating tumor cells: liquid biopsy of cancer. Clin Chem. 2013 Jan;59(1):110–118.
  • Blassl C, Kuhlmann JD, Webers A, et al. Gene expression profiling of single circulating tumor cells in ovarian cancer - Establishment of a multi-marker gene panel. Mol Oncol. 2016 Aug;10(7):1030–1042.
  • Yu M, Bardia A, Aceto N, et al. Cancer therapy. Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility. Science. 2014 Jul 11;345(6193):216–220.
  • Yu M, Ting DT, Stott SL, et al. RNA sequencing of pancreatic circulating tumour cells implicates WNT signalling in metastasis. Nature. 2012 Jul 26;487(7408):510–513.
  • Nagrath S, Sequist LV, Maheswaran S, et al. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature. 2007 Dec 20;450(7173):1235–1239.
  • Stott SL, Hsu CH, Tsukrov DI, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci U S A. 2010 Oct 26;107(43):18392–18397.
  • Khojah R, Stoutamore R, Di Carlo D. Size-tunable microvortex capture of rare cells. Lab Chip. 2017 Jul 25;17(15):2542–2549.
  • O’Shannessy DJ, Davis DW, Anderes K, et al. Isolation of circulating tumor cells from multiple epithelial cancers with apostream((R)) for detecting (or monitoring) the expression of folate receptor alpha. Biomark Insights. 2016;11:7–18.
  • Ozkumur E, Shah AM, Ciciliano JC, et al. Inertial focusing for tumor antigen-dependent and -independent sorting of rare circulating tumor cells. Sci Transl Med. 2013 Apr 3;5(179):179ra47.
  • Jan YJ, Chen JF, Zhu Y, et al. NanoVelcro rare-cell assays for detection and characterization of circulating tumor cells. Adv Drug Deliv Rev. 2018 Feb 1;125:78–93.
  • Poruk KE, Valero V 3rd, Saunders T, et al. Circulating tumor cell phenotype predicts recurrence and survival in pancreatic adenocarcinoma. Ann Surg. 2016 Dec;264(6):1073–1081.
  • de Albuquerque A, Kubisch I, Breier G, et al. Multimarker gene analysis of circulating tumor cells in pancreatic cancer patients: a feasibility study. Oncology. 2012;82(1):3–10.
  • Kim TH, Wang Y, Oliver CR, et al. A temporary indwelling intravascular aphaeretic system for in vivo enrichment of circulating tumor cells. Nat Commun. 2019 Apr 1;10(1):1478.
  • 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 Cancer Res. 2004 Oct 15;10(20):6897–6904.
  • 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):189–195.
  • 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 Aug;24(8):2057–2061.
  • 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 Jan 31;106(3):508–516.
  • Okubo K, Uenosono Y, Arigami T, et al. Clinical impact of circulating tumor cells and therapy response in pancreatic cancer. Eur J Surg Oncol. 2017 Jun;43(6):1050–1055.
  • Effenberger KE, Schroeder C, Hanssen A, et al. Improved risk stratification by circulating tumor cell counts in pancreatic cancer. Clin Cancer Res. 2018 Jun 15;24(12):2844–2850.
  • Kulemann B, Rosch S, Seifert S, et al. Pancreatic cancer: circulating tumor cells and primary tumors show heterogeneous KRAS mutations. Sci Rep. 2017 Jul 3;7(1):4510.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.