Progress of enrichment technology of circulating tumor cells in primary liver cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

HUO Chenyu ,  JIANG Li

Department of Liver Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

JIANG Li, Email: jl339@126.com

Keywords：

primary liver cancer; circulating tumor cell; separation; enrichment

DOI：

10.7507/1007-9424.202210034

Video：

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Objective To understand the latest progress of enrichment technology of circulating tumor cells (CTCs), and summarize the principle, advantages and disadvantages of various enrichment technologies and their applications in primary liver cancer (PLC). Method The literature relevant to the enrichment methods of CTCs in the PLC was reviewed and summarized. Results The clinical significances of CTCs in the early diagnosis and staging, hierarchical diagnosis and treatment, and efficacy monitoring of patients with PLC had been recognized. There were many separation and enrichment technologies for CTC, which were mainly based on the differences of physical and biochemical characteristics, as well as the combination of enrichment methods with various principles. Each enrichment method had corresponding advantages and disadvantages, and few enrichment methods for CTC was applied to PLC. Conclusions Although many problems need to be solved in enrichment method of CTCs at present, it is believed that the existing problems will be solved one by one with continuous improvement of technology. And CTC detection is expected to apply in clinical, so as to provide more efficient diagnosis and treatment methods for patients with PLC.

Citation： HUO Chenyu, JIANG Li. Progress of enrichment technology of circulating tumor cells in primary liver cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2023, 30(4): 494-500. doi: 10.7507/1007-9424.202210034 Copy

1.	McGlynn KA, Petrick JL, El-Serag HB. Epidemiology of hepatocellular carcinoma. Hepatology, 2021, 73 Suppl 1 (Suppl 1): 4-13.
2.	Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
3.	陈万青, 郑荣寿, 张思维, 等. 2013年中国恶性肿瘤发病和死亡分析. 中国肿瘤, 2017, 26(1): 1-7.
4.	Klotz R, Thomas A, Teng T, et al. Circulating tumor cells exhibit metastatic tropism and reveal brain metastasis drivers. Cancer Discov, 2020, 10(1): 86-103.
5.	Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin, 2018, 68(1): 7-30.
6.	Lin D, Shen L, Luo M, et al. Circulating tumor cells: biology and clinical significance. Signal Transduct Target Ther, 2021, 6(1): 404. doi: 10.1038/s41392-021-00817-8.
7.	穆洪, 林凯璇, 赵宏, 等. 肝细胞肝癌外周血循环肿瘤细胞的检测. 中华肿瘤杂志, 2014, 36(4): 276-281.
8.	齐鲁楠, 向邦德, 吴飞翔, 等. 肝细胞癌患者循环血肿瘤细胞的检测、分型鉴定及其临床意义. 中国癌症防治杂志, 2017, 9(1): 55-60.
9.	Liu S, Li N, Yu X, et al. Expression of intercellular adhesion molecule 1 by hepatocellular carcinoma stem cells and circulating tumor cells. Gastroenterology, 2013, 144(5): 1031-1041. e10. doi: 10.1053/j.gastro.2013.01.046.
10.	Attard G, de Bono JS. Utilizing circulating tumor cells: challenges and pitfalls. Curr Opin Genet Dev, 2011, 21(1): 50-58.
11.	Alix-Panabières C, Pantel K. Challenges in circulating tumour cell research. Nat Rev Cancer, 2014, 14(9): 623-631.
12.	沈素雅, 黄建钊, 李小怀. 循环肿瘤细胞富集技术研究进展. 检验医学, 2022, 37(1): 91-96.
13.	Gertler R, Rosenberg R, Fuehrer K, et al. Detection of circulating tumor cells in blood using an optimized density gradient centrifugation. Recent Results Cancer Res, 2003, 162: 149-155.
14.	Yoo CE, Moon HS, Kim YJ, et al. Highly dense, optically inactive silica microbeads for the isolation and identification of circulating tumor cells. Biomaterials, 2016, 75: 271-278.
15.	Li X, Li Y, Shao W, et al. Strategies for enrichment of circulating tumor cells. Transl Cancer Res, 2020, 9(3): 2012-2025.
16.	Huang Q, Wang FB, Yuan CH, et al. Gelatin nanoparticle-coated silicon beads for density-selective capture and release of heterogeneous circulating tumor cells with high purity. Theranostics, 2018, 8(6): 1624-1635.
17.	Hu D, Liu H, Tian Y, et al. Sorting technology for circulating tumor cells based on microfluidics. ACS Comb Sci, 2020, 22(12): 701-711.
18.	Vona G, Sabile A, Louha M, et al. Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulatingtumor cells. Am J Pathol, 2000, 156(1): 57-63.
19.	Monterisi S, Castello A, Toschi L, et al. Preliminary data on circulating tumor cells in metastatic NSCLC patients candidate to immunotherapy. Am J Nucl Med Mol Imaging, 2019, 9(6): 282-295.
20.	Zhao Y, Zhao S, Chen Y, et al. Isolation of circulating tumor cells in patients undergoing surgery for esophageal cancer and a specific confirmation method. Oncol Lett, 2019, 17(4): 3817-3825.
21.	Kim TH, Lim M, Park J, et al. FAST: size-selective, clog-free isolation of rare cancer cells from whole blood at a liquid-liquid interface. Anal Chem, 2017, 89(2): 1155-1162.
22.	Cheng IF, Huang WL, Chen TY, et al. Antibody-free isolation of rare cancer cells from blood based on 3D lateral dielectrophoresis. Lab Chip, 2015, 15(14): 2950-2959.
23.	Loutherback K, D’Silva J, Liu L, et al. Deterministic separation of cancer cells from blood at 10 mL/min. AIP Adv, 2012, 2(4): 42107. doi: 10.1063/1.4758131.
24.	侯铁英, 张玉, 周典蓉. 循环肿瘤细胞富集技术研究进展. 中华肿瘤防治杂志, 2022, 29(11): 859-864.
25.	Altay R, Yapici MK, Koşar A. A hybrid spiral microfluidic platform coupled with surface acoustic waves for circulating tumor cell sorting and separation: a numerical study. Biosensors (Basel), 2022, 12(3): 171. doi: 10.3390/bios12030171.
26.	Kulasinghe A, Zhou J, Kenny L, et al. Capture of circulating tumour cell clusters using straight microfluidic chips. Cancers (Basel), 2019, 11(1): 89. doi: 10.3390/cancers11010089.
27.	Renier C, Pao E, Che J, et al. Label-free isolation of prostate circulating tumor cells using Vortex microfluidic technology. NPJ Precis Oncol, 2017, 1(1): 15. doi: 10.1038/s41698-017-0015-0.
28.	Antfolk M, Antfolk C, Lilja H, et al. A single inlet two-stage acoustophoresis chip enabling tumor cell enrichment from white blood cells. Lab Chip, 2015, 15(9): 2102-2109.
29.	Gascoyne PR, Noshari J, Anderson TJ, et al. Isolation of rare cells from cell mixtures by dielectrophoresis. Electrophoresis, 2009, 30(8): 1388-1398.
30.	Le Du F, Fujii T, Kida K, et al. EpCAM-independent isolation of circulating tumor cells with epithelial-to-mesenchymal transition and cancer stem cell phenotypes using ApoStream® in patients with breast cancer treated with primary systemic therapy. PLoS One, 2020, 15(3): e0229903. doi: 10.1371/journal.pone.0229903.
31.	Yamato M, Kimura T. Magnetic processing of diamagnetic materials. Polymers (Basel), 2020, 12(7): 1491. doi: 10.3390/polym12071491.
32.	Hofman V, Ilie MI, Long E, et al. Detection of circulating tumor cells as a prognostic factor in patients undergoing radical surgery for non-small-cell lung carcinoma: comparison of the efficacy of the CellSearch Assay™ and the isolation by size of epithelial tumor cell method. Int J Cancer, 2011, 129(7): 1651-1660.
33.	Wu S, Zhao S, Cui D, et al. Advances in the biology, detection techniques, and clinical applications of circulating tumor cells. J Oncol, 2022, 2022: 7149686. doi: 10.1155/2022/7149686.
34.	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. doi: 10.1186/1479-5876-10-138.
35.	Drucker A, Teh EM, Kostyleva R, et al. Comparative performance of different methods for circulating tumor cell enrichment in metastatic breast cancer patients. PLoS One, 2020, 15(8): e0237308. doi: 10.1371/journal.pone.0237308.
36.	Miltenyi S, Müller W, Weichel W, et al. High gradient magnetic cell separation with MACS. Cytometry, 1990, 11(2): 231-238.
37.	Talasaz AH, Powell AA, Huber DE, et al. Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc Natl Acad Sci USA, 2009, 106(10): 3970-3975.
38.	Lu NN, Xie M, Wang J, et al. Biotin-triggered decomposable immunomagnetic beads for capture and release of circulating tumor cells. ACS Appl Mater Interfaces, 2015, 7(16): 8817-8826.
39.	Wu X, Bai Z, Wang L, et al. Magnetic cell centrifuge platform performance study with different microsieve pore geometries. Sensors (Basel), 2019, 20(1): 48. doi: 10.3390/s20010048.
40.	Xiong K, Wei W, Jin Y, et al. Biomimetic immuno-magnetosomes for high-performance enrichment of circulating tumor cells. Adv Mater, 2016, 28(36): 7929-7935.
41.	Rushton AJ, Nteliopoulos G, Shaw JA, et al. A review of circulating tumour cell enrichment technologies. Cancers (Basel), 2021, 13(5): 970. doi: 10.3390/cancers13050970.
42.	Stott SL, Hsu CH, Tsukrov DI, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci USA, 2010, 107(43): 18392-18397.
43.	Song Y, Shi Y, Huang M, et al. Bioinspired engineering of a multivalent aptamer-functionalized nanointerface to enhance the capture and release of circulating tumor cells. Angew Chem Int Ed Engl, 2019, 58(8): 2236-2240.
44.	Green NM. Avidin. Adv Protein Chem, 1975, 29: 85-133.
45.	Chen L, Luo S, Ge Z, et al. Unbiased enrichment of circulating tumor cells via DNAzyme-catalyzed proximal protein biotinylation. Nano Letters, 2022, 22(4): 1618-1625.
46.	Wu Z, Pan Y, Wang Z, et al. A PLGA nanofiber microfluidic device for highly efficient isolation and release of different phenotypic circulating tumor cells based on dual aptamers. J Mater Chem B, 2021, 9(9): 2212-2220.
47.	Chen K, Dopico P, Varillas J, et al. Integration of lateral filter arrays with immunoaffinity for circulating-tumor-cell isolation. Angew Chem Int Ed Engl, 2019, 58(23): 7606-7610.
48.	Karabacak NM, Spuhler PS, Fachin F, et al. Microfluidic, marker-free isolation of circulating tumor cells from blood samples. Nat Protoc, 2014, 9(3): 694-710.
49.	Fachin F, Spuhler P, Martel-Foley JM, et al. Monolithic chip for high-throughput blood cell depletion to sort rare circulating tumor cells. Sci Rep, 2017, 7(1): 10936. doi: 10.1038/s41598-017-11119-x.
50.	欧洋, 高德海, 王振丹, 等. CTC-Biopsy系统检测肿瘤患者外周血CTC临床应用可行性研究. 中华肿瘤防治杂志, 2019, 26(1): 56-60.

1. McGlynn KA, Petrick JL, El-Serag HB. Epidemiology of hepatocellular carcinoma. Hepatology, 2021, 73 Suppl 1 (Suppl 1): 4-13.
2. Bray F, Ferlay J, Soerjomataram I, et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin, 2018, 68(6): 394-424.
3. 陈万青, 郑荣寿, 张思维, 等. 2013年中国恶性肿瘤发病和死亡分析. 中国肿瘤, 2017, 26(1): 1-7.
4. Klotz R, Thomas A, Teng T, et al. Circulating tumor cells exhibit metastatic tropism and reveal brain metastasis drivers. Cancer Discov, 2020, 10(1): 86-103.
5. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2018. CA Cancer J Clin, 2018, 68(1): 7-30.
6. Lin D, Shen L, Luo M, et al. Circulating tumor cells: biology and clinical significance. Signal Transduct Target Ther, 2021, 6(1): 404. doi: 10.1038/s41392-021-00817-8.
7. 穆洪, 林凯璇, 赵宏, 等. 肝细胞肝癌外周血循环肿瘤细胞的检测. 中华肿瘤杂志, 2014, 36(4): 276-281.
8. 齐鲁楠, 向邦德, 吴飞翔, 等. 肝细胞癌患者循环血肿瘤细胞的检测、分型鉴定及其临床意义. 中国癌症防治杂志, 2017, 9(1): 55-60.
9. Liu S, Li N, Yu X, et al. Expression of intercellular adhesion molecule 1 by hepatocellular carcinoma stem cells and circulating tumor cells. Gastroenterology, 2013, 144(5): 1031-1041. e10. doi: 10.1053/j.gastro.2013.01.046.
10. Attard G, de Bono JS. Utilizing circulating tumor cells: challenges and pitfalls. Curr Opin Genet Dev, 2011, 21(1): 50-58.
11. Alix-Panabières C, Pantel K. Challenges in circulating tumour cell research. Nat Rev Cancer, 2014, 14(9): 623-631.
12. 沈素雅, 黄建钊, 李小怀. 循环肿瘤细胞富集技术研究进展. 检验医学, 2022, 37(1): 91-96.
13. Gertler R, Rosenberg R, Fuehrer K, et al. Detection of circulating tumor cells in blood using an optimized density gradient centrifugation. Recent Results Cancer Res, 2003, 162: 149-155.
14. Yoo CE, Moon HS, Kim YJ, et al. Highly dense, optically inactive silica microbeads for the isolation and identification of circulating tumor cells. Biomaterials, 2016, 75: 271-278.
15. Li X, Li Y, Shao W, et al. Strategies for enrichment of circulating tumor cells. Transl Cancer Res, 2020, 9(3): 2012-2025.
16. Huang Q, Wang FB, Yuan CH, et al. Gelatin nanoparticle-coated silicon beads for density-selective capture and release of heterogeneous circulating tumor cells with high purity. Theranostics, 2018, 8(6): 1624-1635.
17. Hu D, Liu H, Tian Y, et al. Sorting technology for circulating tumor cells based on microfluidics. ACS Comb Sci, 2020, 22(12): 701-711.
18. Vona G, Sabile A, Louha M, et al. Isolation by size of epithelial tumor cells: a new method for the immunomorphological and molecular characterization of circulatingtumor cells. Am J Pathol, 2000, 156(1): 57-63.
19. Monterisi S, Castello A, Toschi L, et al. Preliminary data on circulating tumor cells in metastatic NSCLC patients candidate to immunotherapy. Am J Nucl Med Mol Imaging, 2019, 9(6): 282-295.
20. Zhao Y, Zhao S, Chen Y, et al. Isolation of circulating tumor cells in patients undergoing surgery for esophageal cancer and a specific confirmation method. Oncol Lett, 2019, 17(4): 3817-3825.
21. Kim TH, Lim M, Park J, et al. FAST: size-selective, clog-free isolation of rare cancer cells from whole blood at a liquid-liquid interface. Anal Chem, 2017, 89(2): 1155-1162.
22. Cheng IF, Huang WL, Chen TY, et al. Antibody-free isolation of rare cancer cells from blood based on 3D lateral dielectrophoresis. Lab Chip, 2015, 15(14): 2950-2959.
23. Loutherback K, D’Silva J, Liu L, et al. Deterministic separation of cancer cells from blood at 10 mL/min. AIP Adv, 2012, 2(4): 42107. doi: 10.1063/1.4758131.
24. 侯铁英, 张玉, 周典蓉. 循环肿瘤细胞富集技术研究进展. 中华肿瘤防治杂志, 2022, 29(11): 859-864.
25. Altay R, Yapici MK, Koşar A. A hybrid spiral microfluidic platform coupled with surface acoustic waves for circulating tumor cell sorting and separation: a numerical study. Biosensors (Basel), 2022, 12(3): 171. doi: 10.3390/bios12030171.
26. Kulasinghe A, Zhou J, Kenny L, et al. Capture of circulating tumour cell clusters using straight microfluidic chips. Cancers (Basel), 2019, 11(1): 89. doi: 10.3390/cancers11010089.
27. Renier C, Pao E, Che J, et al. Label-free isolation of prostate circulating tumor cells using Vortex microfluidic technology. NPJ Precis Oncol, 2017, 1(1): 15. doi: 10.1038/s41698-017-0015-0.
28. Antfolk M, Antfolk C, Lilja H, et al. A single inlet two-stage acoustophoresis chip enabling tumor cell enrichment from white blood cells. Lab Chip, 2015, 15(9): 2102-2109.
29. Gascoyne PR, Noshari J, Anderson TJ, et al. Isolation of rare cells from cell mixtures by dielectrophoresis. Electrophoresis, 2009, 30(8): 1388-1398.
30. Le Du F, Fujii T, Kida K, et al. EpCAM-independent isolation of circulating tumor cells with epithelial-to-mesenchymal transition and cancer stem cell phenotypes using ApoStream® in patients with breast cancer treated with primary systemic therapy. PLoS One, 2020, 15(3): e0229903. doi: 10.1371/journal.pone.0229903.
31. Yamato M, Kimura T. Magnetic processing of diamagnetic materials. Polymers (Basel), 2020, 12(7): 1491. doi: 10.3390/polym12071491.
32. Hofman V, Ilie MI, Long E, et al. Detection of circulating tumor cells as a prognostic factor in patients undergoing radical surgery for non-small-cell lung carcinoma: comparison of the efficacy of the CellSearch Assay™ and the isolation by size of epithelial tumor cell method. Int J Cancer, 2011, 129(7): 1651-1660.
33. Wu S, Zhao S, Cui D, et al. Advances in the biology, detection techniques, and clinical applications of circulating tumor cells. J Oncol, 2022, 2022: 7149686. doi: 10.1155/2022/7149686.
34. 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. doi: 10.1186/1479-5876-10-138.
35. Drucker A, Teh EM, Kostyleva R, et al. Comparative performance of different methods for circulating tumor cell enrichment in metastatic breast cancer patients. PLoS One, 2020, 15(8): e0237308. doi: 10.1371/journal.pone.0237308.
36. Miltenyi S, Müller W, Weichel W, et al. High gradient magnetic cell separation with MACS. Cytometry, 1990, 11(2): 231-238.
37. Talasaz AH, Powell AA, Huber DE, et al. Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device. Proc Natl Acad Sci USA, 2009, 106(10): 3970-3975.
38. Lu NN, Xie M, Wang J, et al. Biotin-triggered decomposable immunomagnetic beads for capture and release of circulating tumor cells. ACS Appl Mater Interfaces, 2015, 7(16): 8817-8826.
39. Wu X, Bai Z, Wang L, et al. Magnetic cell centrifuge platform performance study with different microsieve pore geometries. Sensors (Basel), 2019, 20(1): 48. doi: 10.3390/s20010048.
40. Xiong K, Wei W, Jin Y, et al. Biomimetic immuno-magnetosomes for high-performance enrichment of circulating tumor cells. Adv Mater, 2016, 28(36): 7929-7935.
41. Rushton AJ, Nteliopoulos G, Shaw JA, et al. A review of circulating tumour cell enrichment technologies. Cancers (Basel), 2021, 13(5): 970. doi: 10.3390/cancers13050970.
42. Stott SL, Hsu CH, Tsukrov DI, et al. Isolation of circulating tumor cells using a microvortex-generating herringbone-chip. Proc Natl Acad Sci USA, 2010, 107(43): 18392-18397.
43. Song Y, Shi Y, Huang M, et al. Bioinspired engineering of a multivalent aptamer-functionalized nanointerface to enhance the capture and release of circulating tumor cells. Angew Chem Int Ed Engl, 2019, 58(8): 2236-2240.
44. Green NM. Avidin. Adv Protein Chem, 1975, 29: 85-133.
45. Chen L, Luo S, Ge Z, et al. Unbiased enrichment of circulating tumor cells via DNAzyme-catalyzed proximal protein biotinylation. Nano Letters, 2022, 22(4): 1618-1625.
46. Wu Z, Pan Y, Wang Z, et al. A PLGA nanofiber microfluidic device for highly efficient isolation and release of different phenotypic circulating tumor cells based on dual aptamers. J Mater Chem B, 2021, 9(9): 2212-2220.
47. Chen K, Dopico P, Varillas J, et al. Integration of lateral filter arrays with immunoaffinity for circulating-tumor-cell isolation. Angew Chem Int Ed Engl, 2019, 58(23): 7606-7610.
48. Karabacak NM, Spuhler PS, Fachin F, et al. Microfluidic, marker-free isolation of circulating tumor cells from blood samples. Nat Protoc, 2014, 9(3): 694-710.
49. Fachin F, Spuhler P, Martel-Foley JM, et al. Monolithic chip for high-throughput blood cell depletion to sort rare circulating tumor cells. Sci Rep, 2017, 7(1): 10936. doi: 10.1038/s41598-017-11119-x.
50. 欧洋, 高德海, 王振丹, 等. CTC-Biopsy系统检测肿瘤患者外周血CTC临床应用可行性研究. 中华肿瘤防治杂志, 2019, 26(1): 56-60.

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Progress of enrichment technology of circulating tumor cells in primary liver cancer

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