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Current Cancer Drug Targets


ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Review Article

The Clinical Application of Circulating Tumor Cells and DNAs as Prognostic and Predictive Biomarkers in Gastrointestinal Cancer

Author(s): Sara Memarpour*, Ghazaleh Khalili-Tanha*, Awa Alizadeh Ghannad, Masoud Sharifian Razavi, Mona Joudi, Marjan Joodi, Gordon A. Ferns, Seyed Mahdi Hassanian, Majid Khazaei and Amir Avan*

Volume 21, Issue 8, 2021

Published on: 11 March, 2021

Page: [676 - 688] Pages: 13

DOI: 10.2174/1568009621666210311090531

Price: $65


Gastrointestinal (GI) cancer is one of the most common cancers globally. Genetic and epigenetic mechanisms are involved in its pathogenesis. The conventional methods for diagnosis and screening for GI cancers are often invasive and have other limitations. In the era of personalized medicine, a novel non-invasive approach called liquid biopsy has been introduced for the detection and management of GI cancers, which focuses on the analysis of Circulating Tumor Cells (CTCs) and circulating cell-free tumor DNA (ctDNA). Several studies have shown that this new approach allows for an improved understanding of GI tumor biology and will lead to an improvement in clinical management. The aim of the current review is to explore the clinical applications of CTCs and ctDNA in patients with GI cancer.

Keywords: Gastrointestinal cancer, liquid biopsy, CTCs, ctDNA, biomarkers, tumor biology.

Graphical Abstract
Parkin, D.M.; Bray, F.; Ferlay, J.; Pisani, P. Global cancer statistics, 2002. CA Cancer J. Clin., 2005, 55(2), 74-108.
[] [PMID: 15761078]
Herszényi, L.; Tulassay, Z. Epidemiology of gastrointestinal and liver tumors. Eur. Rev. Med. Pharmacol. Sci., 2010, 14(4), 249-258.
[PMID: 20496531]
Sitarz, R.; Skierucha, M.; Mielko, J.; Offerhaus, G.J.A.; Maciejewski, R.; Polkowski, W.P. Gastric cancer: epidemiology, prevention, classification, and treatment. Cancer Manag. Res., 2018, 10, 239-248.
[] [PMID: 29445300]
Hundahl, S.A.; Phillips, J.L.; Menck, H.R. The National Cancer Data Base Report on poor survival of U.S. gastric carcinoma patients treated with gastrectomy; , 2000.
Amin, M.B.; Greene, F.L.; Edge, S.B.; Compton, C.C.; Gershenwald, J.E.; Brookland, R.K.; Meyer, L.; Gress, D.M.; Byrd, D.R.; Winchester, D.P. , 2017.
Hyman, D.M.; Taylor, B.S.; Baselga, J. Implementing genome-driven oncology. Cell, 2017, 168(4), 584-599.
[] [PMID: 28187282]
Matsuoka, T.; Yashiro, M. Precision medicine for gastrointestinal cancer: Recent progress and future perspective. World J. Gastrointest. Oncol., 2020, 12(1), 1-20.
[] [PMID: 31966910]
Alix-Panabières, C.; Pantel, K. Clinical applications of circulating tumor cells and circulating tumor DNA as liquid biopsy. Cancer Discov., 2016, 6(5), 479-491.
[] [PMID: 26969689]
Diaz, L.A., Jr; Bardelli, A. Liquid biopsies: genotyping circulating tumor DNA. J. Clin. Oncol., 2014, 32(6), 579-586.
[] [PMID: 24449238]
Siravegna, G.; Marsoni, S.; Siena, S.; Bardelli, A. Integrating liquid biopsies into the management of cancer. Nat. Rev. Clin. Oncol., 2017, 14(9), 531-548.
[] [PMID: 28252003]
Marrugo-Ramírez, J.; Mir, M.; Samitier, J. Blood-based cancer biomarkers in liquid biopsy: a promising non-invasive alternative to tissue biopsy. Int. J. Mol. Sci., 2018, 19(10), 2877.
[] [PMID: 30248975]
Marcuello, M.; Vymetalkova, V.; Neves, R.P.L.; Duran-Sanchon, S.; Vedeld, H.M.; Tham, E.; van Dalum, G.; Flügen, G.; Garcia-Barberan, V.; Fijneman, R.J.; Castells, A.; Vodicka, P.; Lind, G.E.; Stoecklein, N.H.; Heitzer, E.; Gironella, M. Circulating biomarkers for early detection and clinical management of colorectal cancer. Mol. Aspects Med., 2019, 69, 107-122.
[] [PMID: 31189073]
Paget, S. The distribution of secondary growths in cancer of the breast. Lancet, 1889, 133(3421), 571-573.
Alix-Panabières, C.; Pantel, K. Circulating tumor cells: liquid biopsy of cancer. Clin. Chem., 2013, 59(1), 110-118.
[] [PMID: 23014601]
Ferreira, M.M.; Ramani, V.C.; Jeffrey, S.S. Circulating tumor cell technologies. Mol. Oncol., 2016, 10(3), 374-394.
[] [PMID: 26897752]
Khamenehfar, A.; Li, P.C. Microfluidic devices for circulating tumor cells isolation and subsequent analysis. Curr. Pharm. Biotechnol., 2016, 17(9), 810-821.
[] [PMID: 26927214]
Zhe, X.; Cher, M.L.; Bonfil, R.D. Circulating tumor cells: finding the needle in the haystack. Am. J. Cancer Res., 2011, 1(6), 740-751.
[PMID: 22016824]
Myung, J.H.; Hong, S. Microfluidic devices to enrich and isolate circulating tumor cells. Lab Chip, 2015, 15(24), 4500-4511.
[] [PMID: 26549749]
Nagrath, S.; Sequist, L.V.; Maheswaran, S.; Bell, D.W.; Irimia, D.; Ulkus, L.; Smith, M.R.; Kwak, E.L.; Digumarthy, S.; Muzikansky, A.; Ryan, P.; Balis, U.J.; Tompkins, R.G.; Haber, D.A.; Toner, M. Isolation of rare circulating tumour cells in cancer patients by microchip technology. Nature, 2007, 450(7173), 1235-1239.
[] [PMID: 18097410]
Song, K-M.; Lee, S.; Ban, C. Aptamers and their biological applications. Sensors (Basel), 2012, 12(1), 612-631.
[] [PMID: 22368488]
Zhang, J.; Sheng, W.; Fan, Z.H. An ensemble of aptamers and antibodies for multivalent capture of cancer cells. Chem. Commun. (Camb.), 2014, 50(51), 6722-6725.
[] [PMID: 24827472]
Kowalik, A.; Kowalewska, M.; Góźdź, S. Current approaches for avoiding the limitations of circulating tumor cells detection methods-implications for diagnosis and treatment of patients with solid tumors. Trans. Res., 2017, 185, 58-84.e15.
Zieglschmid, V.; Hollmann, C.; Mannel, J.; Albert, W.; Jaeschke-Melli, S.; Eckstein, B.; Hillemann, T.; Greten, T.F.; Gross, E.; Böcher, O. Tumor-associated gene expression in disseminated tumor cells correlates with disease progression and tumor stage in colorectal cancer. Anticancer Res., 2007, 27(4A), 1823-1832.
[PMID: 17649779]
Alix-Panabières, C. EPISPOT assay: detection of viable DTCs/CTCs in solid tumor patients. Minimal Residual Disease and Circulating Tumor Cells in Breast Cancer; Springer, 2012, pp. 69-76.
Werner, S.L.; Graf, R.P.; Landers, M.; Valenta, D.T.; Schroeder, M.; Greene, S.B.; Bales, N.; Dittamore, R.; Marrinucci, D. Analytical validation and capabilities of the epic CTC platform: enrichment-free circulating tumour cell detection and characterization. J. Circ. Biomark., 2015, 4, 3.
[] [PMID: 28936239]
Shen, Z.; Wu, A.; Chen, X. Current detection technologies for circulating tumor cells. Chem. Soc. Rev., 2017, 46(8), 2038-2056.
[] [PMID: 28393954]
Crowley, E.; Di Nicolantonio, F.; Loupakis, F.; Bardelli, A. Liquid biopsy: monitoring cancer-genetics in the blood. Nat. Rev. Clin. Oncol., 2013, 10(8), 472-484.
[] [PMID: 23836314]
Bardelli, A.; Pantel, K. Liquid biopsies, what we do not know (yet). Cancer Cell, 2017, 31(2), 172-179.
[] [PMID: 28196593]
Dawson, S-J.; Tsui, D.W.; Murtaza, M.; Biggs, H.; Rueda, O.M.; Chin, S-F.; Dunning, M.J.; Gale, D.; Forshew, T.; Mahler-Araujo, B.; Rajan, S.; Humphray, S.; Becq, J.; Halsall, D.; Wallis, M.; Bentley, D.; Caldas, C.; Rosenfeld, N. Analysis of circulating tumor DNA to monitor metastatic breast cancer. N. Engl. J. Med., 2013, 368(13), 1199-1209.
[] [PMID: 23484797]
Spindler, K-L.G.; Pallisgaard, N.; Vogelius, I.; Jakobsen, A. Quantitative cell-free DNA, KRAS, and BRAF mutations in plasma from patients with metastatic colorectal cancer during treatment with cetuximab and irinotecan. Clin. Cancer Res., 2012, 18(4), 1177-1185.
[] [PMID: 22228631]
McBride, D.J.; Orpana, A.K.; Sotiriou, C.; Joensuu, H.; Stephens, P.J.; Mudie, L.J.; Hämäläinen, E.; Stebbings, L.A.; Andersson, L.C.; Flanagan, A.M.; Durbecq, V.; Ignatiadis, M.; Kallioniemi, O.; Heckman, C.A.; Alitalo, K.; Edgren, H.; Futreal, P.A.; Stratton, M.R.; Campbell, P.J. Use of cancer-specific genomic rearrangements to quantify disease burden in plasma from patients with solid tumors. Genes Chromosomes Cancer, 2010, 49(11), 1062-1069.
[] [PMID: 20725990]
Bettegowda, C.; Sausen, M.; Leary, R.J.; Kinde, I.; Wang, Y.; Agrawal, N.; Bartlett, B.R.; Wang, H.; Luber, B.; Alani, R.M. Detection of circulating tumor DNA in early- and late-stage human malignancies Sci. Transl. Med., 2014, 6(224), 224ra24.
[] [PMID: 24553385]
Zhang, B.O.; Xu, C.W.; Shao, Y.; Wang, H.T.; Wu, Y.F.; Song, Y.Y.; Li, X.B.; Zhang, Z.; Wang, W.J.; Li, L.Q.; Cai, C.L. Comparison of droplet digital PCR and conventional quantitative PCR for measuring EGFR gene mutation. Exp. Ther. Med., 2015, 9(4), 1383-1388.
[] [PMID: 25780439]
García-Foncillas, J.; Alba, E.; Aranda, E.; Díaz-Rubio, E.; López-López, R.; Tabernero, J.; Vivancos, A. Incorporating BEAMing technology as a liquid biopsy into clinical practice for the management of colorectal cancer patients: an expert taskforce review. Ann. Oncol., 2017, 28(12), 2943-2949.
[] [PMID: 28945877]
Ottesen, E.A.; Hong, J.W.; Quake, S.R.; Leadbetter, J.R. Microfluidic digital PCR enables multigene analysis of individual environmental bacteria. Science., 2006, 314(5804), 1464-1467.
[] [PMID: 17138901]
Kinde, I.; Wu, J.; Papadopoulos, N.; Kinzler, K.W.; Vogelstein, B. Detection and quantification of rare mutations with massively parallel sequencing. Proc. Natl. Acad. Sci. USA, 2011, 108(23), 9530-9535.
[] [PMID: 21586637]
Forshew, T.; Murtaza, M.; Parkinson, C.; Gale, D.; Tsui, D. W.; Kaper, F.; Dawson, S.-J.; Piskorz, A. M.; Jimenez-Linan, M.; Bentley, D. Noninvasive identification and monitoring of cancer mutations by targeted deep sequencing of plasma DNA. Sci. Transl. Med., 2012, 4(136), 136ra68-136ra68.
Newman, A.M.; Bratman, S.V.; To, J.; Wynne, J.F.; Eclov, N.C.; Modlin, L.A.; Liu, C.L.; Neal, J.W.; Wakelee, H.A.; Merritt, R.E.; Shrager, J.B.; Loo, B.W., Jr; Alizadeh, A.A.; Diehn, M. An ultrasensitive method for quantitating circulating tumor DNA with broad patient coverage. Nat. Med., 2014, 20(5), 548-554.
[] [PMID: 24705333]
Torre, L.A.; Bray, F.; Siegel, R.L.; Ferlay, J.; Lortet-Tieulent, J.; Jemal, A. Global cancer statistics, 2012. CA Cancer J. Clin., 2015, 65(2), 87-108.
[] [PMID: 25651787]
Pennathur, A.; Gibson, M.K.; Jobe, B.A.; Luketich, J.D. Oesophageal carcinoma. Lancet, 2013, 381(9864), 400-412.
[] [PMID: 23374478]
Hoeppner, J.; Kulemann, B. Circulating tumor cells in esophageal cancer. Oncol. Res. Treat., 2017, 40(7-8), 417-422.
[] [PMID: 28693013]
Wang, S.; Du, H.; Li, G. Significant prognostic value of circulating tumor cells in esophageal cancer patients: A meta-analysis. Oncotarget, 2017, 8(9), 15815-15826.
[] [PMID: 28178659]
Sclafani, F.; Smyth, E.; Cunningham, D.; Chau, I.; Turner, A.; Watkins, D. A pilot study assessing the incidence and clinical significance of circulating tumor cells in esophagogastric cancers. Clin. Colorectal Cancer, 2014, 13(2), 94-99.
[] [PMID: 24332356]
Matsushita, D.; Uenosono, Y.; Arigami, T.; Yanagita, S.; Nishizono, Y.; Hagihara, T.; Hirata, M.; Haraguchi, N.; Arima, H.; Kijima, Y.; Kurahara, H.; Maemura, K.; Okumura, H.; Ishigami, S.; Natsugoe, S. Clinical significance of circulating tumor cells in peripheral blood of patients with esophageal squamous cell carcinoma. Ann. Surg. Oncol., 2015, 22(11), 3674-3680.
[] [PMID: 25652049]
Li, H.; Song, P.; Zou, B.; Liu, M.; Cui, K.; Zhou, P.; Li, S.; Zhang, B. Circulating tumor cell analyses in patients with esophageal squamous cell carcinoma using epithelial marker-dependent and -independent approaches. Medicine (Baltimore), 2015, 94(38), e1565.
[] [PMID: 26402816]
Hoeppner, J.; Lordick, F.; Brunner, T.; Glatz, T.; Bronsert, P.; Röthling, N.; Schmoor, C.; Lorenz, D.; Ell, C.; Hopt, U.T.; Siewert, J.R. ESOPEC: prospective randomized controlled multicenter phase III trial comparing perioperative chemotherapy (FLOT protocol) to neoadjuvant chemoradiation (CROSS protocol) in patients with adenocarcinoma of the esophagus (NCT02509286). BMC Cancer, 2016, 16, 503.
[] [PMID: 27435280]
Ferlay, J.; Soerjomataram, I.; Dikshit, R.; Eser, S.; Mathers, C.; Rebelo, M.; Parkin, D.M.; Forman, D.; Bray, F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer, 2015, 136(5), E359-E386.
[] [PMID: 25220842]
Marrelli, D.; De Stefano, A.; de Manzoni, G.; Morgagni, P.; Di Leo, A.; Roviello, F. Prediction of recurrence after radical surgery for gastric cancer: a scoring system obtained from a prospective multicenter study. Ann. Surg., 2005, 241(2), 247-255.
[] [PMID: 15650634]
Tang, L.; Zhao, S.; Liu, W.; Parchim, N.F.; Huang, J.; Tang, Y.; Gan, P.; Zhong, M. Diagnostic accuracy of circulating tumor cells detection in gastric cancer: systematic review and meta-analysis. BMC Cancer, 2013, 13, 314.
[] [PMID: 23806209]
Lee, M.W.; Kim, G.H.; Jeon, H.K.; Park, S.J. Clinical application of circulating tumor cells in gastric cancer. Gut Liver, 2019, 13(4), 394-401.
[] [PMID: 30970448]
Li, Y.; Gong, J.; Zhang, Q.; Lu, Z.; Gao, J.; Li, Y.; Cao, Y.; Shen, L. Dynamic monitoring of circulating tumour cells to evaluate therapeutic efficacy in advanced gastric cancer. Br. J. Cancer, 2016, 114(2), 138-145.
[] [PMID: 26784122]
Kang, H.M.; Kim, G.H.; Jeon, H.K.; Kim, D.H.; Jeon, T.Y.; Park, D.Y.; Jeong, H.; Chun, W.J.; Kim, M-H.; Park, J.; Lim, M.; Kim, T-H.; Cho, Y-K. Circulating tumor cells detected by lab-on-a-disc: Role in early diagnosis of gastric cancer. PLoS One, 2017, 12(6), e0180251-e0180251.
[] [PMID: 28662130]
Yang, C.; Zhang, N.; Wang, S.; Shi, D.; Zhang, C.; Liu, K.; Xiong, B. Wedge-shaped microfluidic chip for circulating tumor cells isolation and its clinical significance in gastric cancer. J. Transl. Med., 2018, 16(1), 139-139.
[] [PMID: 29792200]
Van Cutsem, E.; Cervantes, A.; Nordlinger, B.; Arnold, D. Metastatic colorectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol., 2014, 25(Suppl. 3), iii1-iii9.
[] [PMID: 25190710]
Labianca, R.; Nordlinger, B.; Beretta, G.D.; Mosconi, S.; Mandalà, M.; Cervantes, A.; Arnold, D. Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol., 2013, 24(Suppl. 6), vi64-vi72.
[] [PMID: 24078664]
Hamzehzadeh, L.; Yousefi, M.; Ghaffari, S.H. Colorectal cancer screening: A comprehensive review to recent non-invasive methods. Int. J. Hematol. Oncol. Stem Cell Res., 2017, 11(3), 250-261.
[PMID: 28989593]
Tappenden, P.; Chilcott, J.; Eggington, S.; Patnick, J.; Sakai, H.; Karnon, J. Option appraisal of population-based colorectal cancer screening programmes in England. Gut, 2007, 56(5), 677-684.
[] [PMID: 17142648]
Cristofanilli, M.; Budd, G.T.; Ellis, M.J.; Stopeck, A.; Matera, J.; Miller, M.C.; Reuben, J.M.; Doyle, G.V.; Allard, W.J.; Terstappen, L.W.; Hayes, D.F. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med., 2004, 351(8), 781-791.
[] [PMID: 15317891]
Miller, M.C.; Doyle, G.V.; Terstappen, L.W. Significance of circulating tumor cells detected by the cell search system in patients with metastatic breast colorectal and Prostate cancer. J. Oncol., 2010, 2010, 617421.
[] [PMID: 20016752]
Miyamoto, D.T.; Sequist, L.V.; Lee, R.J. Circulating tumour cells-monitoring treatment response in prostate cancer. Nat. Rev. Clin. Oncol., 2014, 11(7), 401-412.
[] [PMID: 24821215]
Huang, M.Y.; Tsai, H.L.; Huang, J.J.; Wang, J.Y. Clinical implications and future perspectives of circulating tumor cells and biomarkers in clinical outcomes of colorectal cancer. Transl. Oncol., 2016, 9(4), 340-347.
[] [PMID: 27567958]
Fang, C.; Fan, C.; Wang, C.; Huang, Q.; Meng, W.; Yu, Y.; Yang, L.; Peng, Z.; Hu, J.; Li, Y.; Mo, X.; Zhou, Z. CD133+CD54+CD44+ circulating tumor cells as a biomarker of treatment selection and liver metastasis in patients with colorectal cancer. Oncotarget, 2016, 7(47), 77389-77403.
[] [PMID: 27764803]
Burz, C.; Pop, V-V.; Buiga, R.; Daniel, S.; Samasca, G.; Aldea, C.; Lupan, I. Circulating tumor cells in clinical research and monitoring patients with colorectal cancer. Oncotarget, 2018, 9(36), 24561-24571.
[] [PMID: 29849961]
Kidess-Sigal, E.; Liu, H.E.; Triboulet, M.M.; Che, J.; Ramani, V.C.; Visser, B.C.; Poultsides, G.A.; Longacre, T.A.; Marziali, A.; Vysotskaia, V.; Wiggin, M.; Heirich, K.; Hanft, V.; Keilholz, U.; Tinhofer, I.; Norton, J.A.; Lee, M.; Sollier-Christen, E.; Jeffrey, S.S. Enumeration and targeted analysis of KRAS, BRAF and PIK3CA mutations in CTCs captured by a label-free platform: Comparison to ctDNA and tissue in metastatic colorectal cancer. Oncotarget, 2016, 7(51), 85349-85364.
[] [PMID: 27863403]
Gasch, C.; Bauernhofer, T.; Pichler, M.; Langer-Freitag, S.; Reeh, M.; Seifert, A.M.; Mauermann, O.; Izbicki, J.R.; Pantel, K.; Riethdorf, S. Heterogeneity of epidermal growth factor receptor status and mutations of KRAS/PIK3CA in circulating tumor cells of patients with colorectal cancer. Clin. Chem., 2013, 59(1), 252-260.
[] [PMID: 23136247]
Wan, L.; Pantel, K.; Kang, Y. Tumor metastasis: moving new biological insights into the clinic. Nat. Med., 2013, 19(11), 1450-1464.
[] [PMID: 24202397]
Satelli, A.; Batth, I.S.; Brownlee, Z.; Rojas, C.; Meng, Q.H.; Kopetz, S.; Li, S. Potential role of nuclear PD-L1 expression in cell-surface vimentin positive circulating tumor cells as a prognostic marker in cancer patients. Sci. Rep., 2016, 6, 28910.
[] [PMID: 27363678]
Sugimachi, K.; Yokobori, T.; Iinuma, H.; Ueda, M.; Ueo, H.; Shinden, Y.; Eguchi, H.; Sudo, T.; Suzuki, A.; Maehara, Y.; Mori, M.; Mimori, K. Aberrant expression of plastin-3 via copy number gain induces the epithelial-mesenchymal transition in circulating colorectal cancer cells. Ann. Surg. Oncol., 2014, 21(11), 3680-3690.
[] [PMID: 24217791]
Mouliere, F.; El Messaoudi, S.; Pang, D.; Dritschilo, A.; Thierry, A.R. Multi-marker analysis of circulating cell-free DNA toward personalized medicine for colorectal cancer. Mol. Oncol., 2014, 8(5), 927-941.
[] [PMID: 24698732]
Zhu, Y.; Guo, Z.; Liu, Y.; Zheng, X.; Yang, G.; Zheng, G. A novel ARMS-based assay for the quantification of EGFR mutations in patients with lung adenocarcinoma. Oncol. Lett., 2018, 15(3), 2905-2912.
[PMID: 29435017]
Sanmamed, M.F.; Fernández-Landázuri, S.; Rodríguez, C.; Zárate, R.; Lozano, M.D.; Zubiri, L.; Perez-Gracia, J.L.; Martín-Algarra, S.; González, A. Quantitative cell-free circulating BRAFV600E mutation analysis by use of droplet digital PCR in the follow-up of patients with melanoma being treated with BRAF inhibitors. Clin. Chem., 2015, 61(1), 297-304.
[] [PMID: 25411185]
Taniguchi, K.; Uchida, J.; Nishino, K.; Kumagai, T.; Okuyama, T.; Okami, J.; Higashiyama, M.; Kodama, K.; Imamura, F.; Kato, K. Quantitative detection of EGFR mutations in circulating tumor DNA derived from lung adenocarcinomas. Clin. Cancer Res., 2011, 17(24), 7808-7815.
[] [PMID: 21976538]
Heitzer, E.; Ulz, P.; Belic, J.; Gutschi, S.; Quehenberger, F.; Fischereder, K.; Benezeder, T.; Auer, M.; Pischler, C.; Mannweiler, S.; Pichler, M.; Eisner, F.; Haeusler, M.; Riethdorf, S.; Pantel, K.; Samonigg, H.; Hoefler, G.; Augustin, H.; Geigl, J.B.; Speicher, M.R. Tumor-associated copy number changes in the circulation of patients with prostate cancer identified through whole-genome sequencing. Genome Med., 2013, 5(4), 30.
[] [PMID: 23561577]
Manier, S.; Park, J.; Capelletti, M.; Bustoros, M.; Freeman, S.S.; Ha, G.; Rhoades, J.; Liu, C.J.; Huynh, D.; Reed, S.C.; Gydush, G.; Salem, K.Z.; Rotem, D.; Freymond, C.; Yosef, A.; Perilla-Glen, A.; Garderet, L.; Van Allen, E.M.; Kumar, S.; Love, J.C.; Getz, G.; Adalsteinsson, V.A.; Ghobrial, I.M. Whole-exome sequencing of cell-free DNA and circulating tumor cells in multiple myeloma. Nat. Commun., 2018, 9(1), 1691.
[] [PMID: 29703982]
Setoyama, T.; Natsugoe, S.; Okumura, H.; Matsumoto, M.; Uchikado, Y.; Ishigami, S.; Owaki, T.; Takao, S.; Aikou, T. Carcinoembryonic antigen messenger RNA expression in blood predicts recurrence in esophageal cancer. Clin. Cancer Res., 2006, 12(20 Pt 1), 5972-5977.
[] [PMID: 17062668]
Tanaka, K.; Yano, M.; Motoori, M.; Kishi, K.; Miyashiro, I.; Shingai, T.; Gotoh, K.; Noura, S.; Takahashi, H.; Ohue, M.; Yamada, T.; Ohigashi, H.; Yamamoto, T.; Yamasaki, T.; Doki, Y.; Ishikawa, O. CEA-antigen and SCC-antigen mRNA expression in peripheral blood predict hematogenous recurrence after resection in patients with esophageal cancer. Ann. Surg. Oncol., 2010, 17(10), 2779-2786.
[] [PMID: 20411433]
Reeh, M.; Effenberger, K.E.; Koenig, A.M.; Riethdorf, S.; Eichstädt, D.; Vettorazzi, E.; Uzunoglu, F.G.; Vashist, Y.K.; Izbicki, J.R.; Pantel, K.; Bockhorn, M. Circulating tumor cells as a biomarker for preoperative prognostic staging in patients with esophageal cancer. Ann. Surg., 2015, 261(6), 1124-1130.
[] [PMID: 25607767]
Su, P-J.; Wu, M-H.; Wang, H-M.; Lee, C-L.; Huang, W-K.; Wu, C-E.; Chang, H-K.; Chao, Y-K.; Tseng, C-K.; Chiu, T-K.; Lin, N.M-J.; Ye, S-R.; Lee, J.Y-C.; Hsieh, C-H. Circulating tumour cells as an independent prognostic factor in patients with advanced oesophageal squamous cell carcinoma undergoing chemoradiotherapy. Sci. Rep., 2016, 6(1), 31423.
[] [PMID: 27530152]
Han, D.; Chen, K.; Che, J.; Hang, J.; Li, H. Detection of epithelial-mesenchymal transition status of circulating tumor cells in patients with esophageal squamous carcinoma. BioMed Res. Int., 2018, 2018, 7610154.
[] [PMID: 30046606]
Zhang, Y.; Li, J.; Wang, L.; Meng, P.; Zhao, J.; Han, P.; Xia, J.; Xu, J.; Wang, L.; Shen, F.; Zheng, A.; Zhou, F.; Fan, R. Clinical significance of detecting circulating tumor cells in patients with esophageal squamous cell carcinoma by EpCAM‑independent enrichment and immunostaining‑fluorescence in situ hybridization. Mol. Med. Rep., 2019, 20(2), 1551-1560.
[] [PMID: 31257510]
Kuvendjiska, J.; Bronsert, P.; Martini, V.; Lang, S.; Pitman, M.B.; Hoeppner, J.; Kulemann, B. Non-Metastatic esophageal adenocarcinoma: circulating tumor cells in the course of multimodal tumor treatment. Cancers (Basel), 2019, 11(3), 397.
[] [PMID: 30901891]
Pituch-Noworolska, A.; Kolodziejczyk, P.; Kulig, J.; Drabik, G.; Szczepanik, A.; Czupryna, A.; Popiela, T.; Zembala, M. Circulating tumour cells and survival of patients with gastric cancer. Anticancer Res., 2007, 27(1B), 635-640.
[PMID: 17348453]
Hiraiwa, K.; Takeuchi, H.; Hasegawa, H.; Saikawa, Y.; Suda, K.; Ando, T.; Kumagai, K.; Irino, T.; Yoshikawa, T.; Matsuda, S.; Kitajima, M.; Kitagawa, Y. Clinical significance of circulating tumor cells in blood from patients with gastrointestinal cancers. Ann. Surg. Oncol., 2008, 15(11), 3092-3100.
[] [PMID: 18766405]
Koga, T.; Tokunaga, E.; Sumiyoshi, Y.; Oki, E.; Oda, S.; Takahashi, I.; Kakeji, Y.; Baba, H.; Maehara, Y. Detection of circulating gastric cancer cells in peripheral blood using real time quantitative RT-PCR. Hepatogastroenterology, 2008, 55(84), 1131-1135.
[PMID: 18705345]
Mimori, K.; Fukagawa, T.; Kosaka, Y.; Kita, Y.; Ishikawa, K.; Etoh, T.; Iinuma, H.; Sasako, M.; Mori, M. Hematogenous metastasis in gastric cancer requires isolated tumor cells and expression of vascular endothelial growth factor receptor-1. Clin. Cancer Res., 2008, 14(9), 2609-2616.
[] [PMID: 18451223]
Matsusaka, S.; Chìn, K.; Ogura, M.; Suenaga, M.; Shinozaki, E.; Mishima, Y.; Terui, Y.; Mizunuma, N.; Hatake, K. Circulating tumor cells as a surrogate marker for determining response to chemotherapy in patients with advanced gastric cancer. Cancer Sci., 2010, 101(4), 1067-1071.
[] [PMID: 20219073]
Kutun, S.; Celik, A.; Cem Kockar, M.; Erkorkmaz, U.; Eroğlu, A.; Cetin, A.; Erkosar, B.; Yakicier, C. Expression of CK-19 and CEA mRNA in peripheral blood of gastric cancer patients. Exp. Oncol., 2010, 32(4), 263-268.
[PMID: 21270756]
Uenosono, Y.; Arigami, T.; Kozono, T.; Yanagita, S.; Hagihara, T.; Haraguchi, N.; Matsushita, D.; Hirata, M.; Arima, H.; Funasako, Y.; Kijima, Y.; Nakajo, A.; Okumura, H.; Ishigami, S.; Hokita, S.; Ueno, S.; Natsugoe, S. Clinical significance of circulating tumor cells in peripheral blood from patients with gastric cancer. Cancer, 2013, 119(22), 3984-3991.
[] [PMID: 23963829]
Okabe, H.; Tsunoda, S.; Hosogi, H.; Hisamori, S.; Tanaka, E.; Tanaka, S.; Sakai, Y. Circulating tumor cells as an independent predictor of survival in advanced gastric cancer. Ann. Surg. Oncol., 2015, 22(12), 3954-3961.
[] [PMID: 25777087]
Kolostova, K.; Matkowski, R.; Gürlich, R.; Grabowski, K.; Soter, K.; Lischke, R.; Schützner, J.; Bobek, V. Detection and cultivation of circulating tumor cells in gastric cancer. Cytotechnology, 2016, 68(4), 1095-1102.
[] [PMID: 25862542]
Pernot, S.; Badoual, C.; Terme, M.; Castan, F.; Cazes, A.; Bouche, O.; Bennouna, J.; Francois, E.; Ghiringhelli, F.; De La Fouchardiere, C.; Samalin, E.; Bachet, J. B.; Borg, C.; Ducreux, M.; Marcheteau, E.; Stanbury, T.; Gourgou, S.; Malka, D.; Taieb, J. Dynamic evaluation of circulating tumour cells in patients with advanced gastric and oesogastric junction adenocarcinoma: Prognostic value and early assessment of therapeutic effects. Eur J Cancer., 2017, 79, 15-22.
[] [PMID: 28456090]
Bessa, X.; Elizalde, J.I.; Boix, L.; Piñol, V.; Lacy, A.M.; Saló, J.; Piqué, J.M.; Castells, A. Lack of prognostic influence of circulating tumor cells in peripheral blood of patients with colorectal cancer. Gastroenterology, 2001, 120(5), 1084-1092.
[] [PMID: 11266372]
Ito, S.; Nakanishi, H.; Hirai, T.; Kato, T.; Kodera, Y.; Feng, Z.; Kasai, Y.; Ito, K.; Akiyama, S.; Nakao, A.; Tatematsu, M. Quantitative detection of CEA expressing free tumor cells in the peripheral blood of colorectal cancer patients during surgery with real-time RT-PCR on a LightCycler. Cancer Lett., 2002, 183(2), 195-203.
[] [PMID: 12065095]
Cohen, S.J.; Punt, C.J.; Iannotti, N.; Saidman, B.H.; Sabbath, K.D.; Gabrail, N.Y.; Picus, J.; Morse, M.; Mitchell, E.; Miller, M.C.; Doyle, G.V.; Tissing, H.; Terstappen, L.W.; Meropol, N.J. Relationship of circulating tumor cells to tumor response, progression-free survival, and overall survival in patients with metastatic colorectal cancer. J. Clin. Oncol., 2008, 26(19), 3213-3221.
[] [PMID: 18591556]
Tol, J.; Koopman, M.; Miller, M.C.; Tibbe, A.; Cats, A.; Creemers, G.J.; Vos, A.H.; Nagtegaal, I.D.; Terstappen, L.W.; Punt, C.J. Circulating tumour cells early predict progression-free and overall survival in advanced colorectal cancer patients treated with chemotherapy and targeted agents. Ann. Oncol., 2010, 21(5), 1006-1012.
[] [PMID: 19861577]
Iinuma, H.; Watanabe, T.; Mimori, K.; Adachi, M.; Hayashi, N.; Tamura, J.; Matsuda, K.; Fukushima, R.; Okinaga, K.; Sasako, M.; Mori, M. Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes’ stage B and C colorectal cancer. J. Clin. Oncol., 2011, 29(12), 1547-1555.
[] [PMID: 21422427]
Sastre, J.; Maestro, M.L.; Gómez-España, A.; Rivera, F.; Valladares, M.; Massuti, B.; Benavides, M.; Gallén, M.; Marcuello, E.; Abad, A.; Arrivi, A.; Fernández-Martos, C.; González, E.; Tabernero, J.M.; Vidaurreta, M.; Aranda, E.; Díaz-Rubio, E. Circulating tumor cell count is a prognostic factor in metastatic colorectal cancer patients receiving first-line chemotherapy plus bevacizumab: a Spanish Cooperative Group for the Treatment of Digestive Tumors study. Oncologist, 2012, 17(7), 947-955.
[] [PMID: 22643538]
Aggarwal, C.; Meropol, N.J.; Punt, C.J.; Iannotti, N.; Saidman, B.H.; Sabbath, K.D.; Gabrail, N.Y.; Picus, J.; Morse, M.A.; Mitchell, E.; Miller, M.C.; Cohen, S.J. Relationship among circulating tumor cells, CEA and overall survival in patients with metastatic colorectal cancer. Ann. Oncol., 2013, 24(2), 420-428.
[] [PMID: 23028040]
Gazzaniga, P.; Raimondi, C.; Gradilone, A.; Biondi Zoccai, G.; Nicolazzo, C.; Gandini, O.; Longo, F.; Tomao, S.; Lo Russo, G.; Seminara, P.; Vincenzi, B.; Chimenti, I.; Cristofanilli, M.; Frati, L.; Cortesi, E. Circulating tumor cells in metastatic colorectal cancer: do we need an alternative cutoff? J. Cancer Res. Clin. Oncol., 2013, 139(8), 1411-1416.
[] [PMID: 23736274]
Sotelo, M.J.; Sastre, J.; Maestro, M.L.; Veganzones, S.; Viéitez, J.M.; Alonso, V.; Grávalos, C.; Escudero, P.; Vera, R.; Aranda, E.; García-Alfonso, P.; Gallego-Plazas, J.; Lopez, C.; Pericay, C.; Arrivi, A.; Vicente, P.; Ballesteros, P.; Elez, E.; López-Ladrón, A.; Díaz-Rubio, E. Role of circulating tumor cells as prognostic marker in resected stage III colorectal cancer. Ann. Oncol., 2015, 26(3), 535-541.
[] [PMID: 25515656]
Seeberg, L.T.; Waage, A.; Brunborg, C.; Hugenschmidt, H.; Renolen, A.; Stav, I.; Bjørnbeth, B.A.; Brudvik, K.W.; Borgen, E.F.; Naume, B.; Wiedswang, G. Circulating tumor cells in patients with colorectal liver metastasis predict impaired survival. Ann. Surg., 2015, 261(1), 164-171.
[] [PMID: 24509211]
Gorges, T.M.; Stein, A.; Quidde, J.; Hauch, S.; Röck, K.; Riethdorf, S.; Joosse, S.A.; Pantel, K. Improved detection of circulating tumor cells in metastatic colorectal cancer by the combination of the CellSearch® system and the AdnaTest®. PLoS One, 2016, 11(5), e0155126.
[] [PMID: 27182774]
Le, U.T.; Bronsert, P.; Picardo, F.; Riethdorf, S.; Haager, B.; Rylski, B.; Czerny, M.; Beyersdorf, F.; Wiesemann, S.; Pantel, K.; Passlick, B.; Kaifi, J.T.; Schmid, S. Intraoperative detection of circulating tumor cells in pulmonary venous blood during metastasectomy for colorectal lung metastases. Sci Rep., 2018, 8(1), 8751.
[] [PMID: 29884810]

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