Molecular detection of micrometastases and circulating tumor cells in solid tumors

Clinical Cancer Research

Volumn 5, Issue 8, 1999, Pages 1950-1960

  Ghossein, Ronald A ^a   Bhattacharya, Satyajit ^a   Rosai, Juan ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

CANCER SURVIVAL; HUMAN; INTERMETHOD COMPARISON; LABORATORY DIAGNOSIS; METASTASIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGNOSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SOLID TUMOR; TUMOR CELL;

FALSE NEGATIVE REACTIONS; FALSE POSITIVE REACTIONS; HUMANS; NEOPLASM CIRCULATING CELLS; NEOPLASM METASTASIS; NEOPLASMS; POLYMERASE CHAIN REACTION; PREDICTIVE VALUE OF TESTS; PROGNOSIS; SENSITIVITY AND SPECIFICITY;

EID: 0032772005     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (116)

1. Ashworth, T. R. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Australian Med. J., 14: 146, 1869.
2. Engell, H. C. Cancer cells in the circulating blood. Acta Chir. Scand. (Suppl.): 201, 1955.
3. Christopherson, W. Cancer cells in the peripheral blood: a second look. Acta Cytol., 9: 169-174, 1965.
4. Moss, T. J., and Sanders D. G. Detection of neuroblastoma cells in blood. J. Clin. Oncol., 8: 736-740, 1990.
5. Redding, W. H., Coombes, R. C., Monaghan, P., Clink, H. M., Imrie, S. F., Dearnaley, D. P., Ormerad, M. G., Sloane, J. P., Gazet, J. C., Powles, T. J., and Munro Neville, A. Detection of micrometastases in patients with primary breast cancer. Lancet, 2: 1271-1273, 1983.
6. Stahel, R. A., Mabry, M., Skarkin, A. T., Speak, J., and Bernal, S. D. Detection of bone marrow metastasis in small-cell lung cancer by monoclonal antibody. J. Clin. Oncol., 3: 455-456, 1985.
7. Diel, I. J., Kaufman, M., Goerner, R., Costa, S. D., Kaul, S., and Bastert, G. Detection of tumor cells in bone marrow of patients with primary breast cancer: a prognostic factor for distant metastasis. J. Clin. Oncol., 10: 1534-1539, 1992.
8. Pantel, K., Izbicki, J., Passlick, B., Angstwurm, M., Haussinger, K., Thetter, O., and Riethmuller, G. Frequency and prognostic significance of isolated tumor cells in bone marrow of patients with non-small cell lung cancer without overt metastases. Lancet, 347: 649-653, 1996.
9. Lindemann, F., Schlimock, G., Dirschedl, P., Witte, J., and Riethmuller, G. Prognostic significance of micrometastatic tumor cells in bone marrow of colorectal patients. Lancet, 340: 685-689, 1992.
10. Pelkey, T. J., Frierson, H. F., and Bruns, D. E. Molecular and immunological detection of circulating tumor cells and micrometastases from solid tumors. Clin. Chem., 42: 1369-1381, 1996.
11. Kirk, S. J., Cooper, G. G., Hoper, M., Watt, P. C., Roy, A. D., and Odling-Smee, W. The prognostic significance of marrow micrometastases in women with early breast cancer. Eur. J. Surg. Oncol., 16: 481-485, 1990.
12. Salvadori, B., Squicciarni, P., Rovini, D., Orefice S., Andreola, S., Rilke, F., Barletta, L., Menard, S., and Colnaghi, M. I. Use of monoclonal antibody Mbr1 to detect micrometastases in bone marrow specimens of breast cancer patients. Eur. J. Cancer, 26: 865-867, 1990.
13. Singletary, S. E., Larry, L., Tucker, S. L., and Spitzer, G. Detection of micrometastatic tumor cells in bone marrow of breast carcinoma patients. J. Surg. Oncol., 47: 32-36, 1991.
14. Courtemanche, D. J., Worth, A. J., Coupland, R. W., and MacFarlane, J. K. Detection of micrometastases from primary breast cancer. Can. J. Surg., 34: 15-19, 1991.
15. Miettinen, M. Keratin subsets in spindle cell sarcomas. Keratins are widespread but synovial sarcoma contains a distinctive keratin polypeptide pattern and desmoplakins. Am. J. Pathol., 138: 505-513, 1991.
16. Thomas, P., and Battifora, H. Keratins versus epithelial membrane antigen in tumor diagnosis: an immunohistochemical comparison of five monoclonal antibodies. Hum. Pathol., 18: 728-734, 1987.
17. Campana, D., and Pui, C. H. Detection of minimal residual disease in acute leukemias: methodological advances and clinical significance. Blood, 85: 1416-1434, 1995.
18. Cave, H., Guidal, P., Rohrlich, P., Delfau, M. H., Broyart, A., Lescoeur, B., Rahimy, C., Fenneteau, O., Monplaisir, N., d'Auriol, L., Elion, J., Vilmer, E., and Grandchamp, B. Prospective monitoring and quantitation of residual blasts in childhood acute leukemias by polymerase chain reaction of delta and gamma T-cell receptor genes. Blood, 83: 1892-1902, 1994.
19. Miyajama, Y., Kato, K., Numata, S., Kudo, K., and Horibe, K. Detection of neuroblastoma cells in bone marrow and peripheral blood at diagnosis by the reverse transcriptase-polymerase chain reaction for tyrosine hydroxylase mRNA. Cancer (Phila.), 75: 2757-2761, 1995.
20. Gerhard, M., Juhl, H., Kalthoff, H., Schreiber, H. W., Wagener, C., and Neumaier, M. Specific detection of carcinoembryonic antigen-expressing tumor cells in bone marrow aspirates by polymerase chain reaction. J. Clin. Oncol., 12: 725-729, 1994.
21. Lee, M. S., Chang, K. S., Cabanillas, F., Freireich, E. J., Trujillo, J. M., and Stass, S. A. Detection of minimal residual cells carrying the t(14;18) by DNA sequence amplification. Science (Washington DC), 237: 175-178, 1987.
22. Komeda, T., Fukuda, Y., Sando, T., Kita, R., Furukawa, M., Nishida, N., Amenomori, M., and Nakao, K. Sensitive detection of circulating hepatocellular carcinoma cells in peripheral venous blood. Cancer (Phila.), 75: 2214-2219, 1995.
23. Eeles, R. A., and Janssen, J. G. W. (eds.). Polymerase chain reaction. The technique and its applications. Austin, TX: R. G. Landes Cie, 1993.
24. Kawasaki, E. S., Clark, S. S., Coyne, M. Y., Smith, S. D., Champlin, R., Witte, O. N., and McCormick, F. P. Diagnosis of chronic myeloid and acute lymphocytic leukemias by detection of leukemia-specific mRNA sequences amplified in vitro. Proc. Natl. Acad. Sci. USA, 85: 5698-5702, 1988.
25. West, D. C., Grier, G. E., Swallow, M. M., Demetri, G. D., Granowetter, L., and Sklar, J. Detection of circulating tumor cells in patients with Ewing's sarcoma and peripheral primitive neuroectodermal tumor. J. Clin. Oncol., 15: 583-588, 1997.
26. Qiu, S. D., Young, C. Y., Bilhartz, D. L., Prescott, J. L., Farrow, G. M., He, W. W., and Tindall, D. J. In situ hybridization of prostatic-specific antigen mRNA in human prostate. J. Urol., 144: 1550-1556, 1990.
27. Ghossein, R. A., Scher, H. I., Gerald, W. L., Kelly, W. K., Curley, T., Amsterdam, A., Zhang, Z. F., and Rosai, J. Detection of circulating tumor cells in patients with localized and metastatic prostatic carcinoma prostatic carcinoma: clinical implications. J. Clin. Oncol., 13: 1195-1200, 1995.
28. Hughes, T., Janssen, J. G. W., Morgan, G., Mariatt, P., Saglio, G., Pignon, J. M., Pignatti, F. P., Mills, K., Keating, A., Gluckman, E., Bartram, C. R., and Goldman, J. M. False-positive results with PCR to detect leukemia-specific transcripts. Lancet, 335: 1037-1038, 1990.
29. Kaplan, J. C., Kahn, A., and Chelly, J. Illegitimate transcription: its use in the study of inherited disease. Hum. Mutat., 1: 357-360, 1992.
30. Mattano, L. A., Moss, T. J., and Emerson, S. G. Sensitive detection of rare circulating neuroblastoma cells by the reverse transcriptase-polymerase chain reaction. Cancer Res., 52: 4701-4705, 1992.
31. Smith, B., Selby, P., Southgate, J., Pittman, K., Bradley, C., and Blair, G. E. Detection of melanoma cells in peripheral blood by means of reverse transcriptase and polymerase chain reaction. Lancet, 338: 1227-1229, 1991.
32. Schoenfeld, A., Luqmani, Y., Smith, D., O'Reilly, S., Shousha, S., Sinnett, H. D., and Coombes, R. C. Detection of breast cancer micrometastases in axillary lymph nodes by using polymerase chain reaction. Cancer Res., 54: 2986-2990, 1994.
33. Olsson, C. A., de Vries, G. M., Buttyan, R., and Katz, A. E. Reverse transcriptase-polymerase chain reaction for prostate cancer. Urol. Clin. N. Am., 24: 367-378, 1997.
34. Ghossein, R. A., Coit, D., Brennan, M., Zhang, Z. F., Wang, Y., Bhattacharya, S., Houghton, A., and Rosai, J. Prognostic significance of peripheral blood and bone marrow tyrosinase mRNA in malignant melanoma. Clin. Cancer Res., 4: 419-428, 1998.
35. Young, C. Y. F., Montgomery, B. T., Andrews, P. E., Qui, S. D., Bilhartz, D. L., and Tindall, D. J. Hormonal regulation of prostate-specific antigen messenger RNA in human prostatic adenocarcinoma cell line LNCaP. Cancer Res., 51: 3748-3752, 1991.
36. Fukuhara, T., Hooper, W. C., Baylin, S. B., Benson, J., Pruckler, J., Olson, A. C., Evatt, B. L., and Vogler, W. R. Use of the polymerase chain reaction to detect hypermethylation in the calcitonin gene: a new, sensitive approach to monitor tumor cells in acute myelogenous leukemia. Leuk. Res., 16: 1031-1040, 1992.
37. Cross, N. C., Feng, L., Chase, A., Bungey, J., Hughes, T. P., and Goldman, J. M. Competitive polymerase chain reaction to estimate the number of bcr-abl transcripts in chronic myeloid leukemia patients after bone marrow transplantation. Blood, 82: 1929-1936, 1993.
38. Meijerink, J. P., Smetsers, T. F., Raemaekers, J. M., Bogman, M. J., De Witte, T., and Mensink, E. J. Quantitation of follicular non-Hodgkin's lymphoma cells carrying t(14;18) by competitive polymerase chain reaction. Br. J. Haematol., 84: 250-256, 1993.
39. Brisco, M. J., Condon, J., Hughes, E., Neoh, S. H., Sykes, P. J., Seshadri, R., Toogood, I., Waters, K., Tauro, G., Ekert, H., and Morley, A. A. Outcome prediction in childhood acute lymphoblastic leukemia by molecular quantification of residual disease at the end of induction. Lancet, 343: 196-200, 1994.
40. Johnson, P. W. M., Burchill, S. A., and Selby, P. J. The molecular detection of circulating tumor cells. Br. J. Cancer, 72: 268-276, 1995.
41. Israeli, R., Miller, W. H., Su, S. L., Samadi, D. S., Powell, C. T., Heston, W. D., Wise, G. J., and Fair, W. R. Sensitive nested reverse transcription polymerase chain reaction detection of circulating prostatic tumor cells: comparison of prostatic-specific membrane antigen and prostate-specific antigen-based assays. Cancer Res., 54: 6306-6310, 1994.
42. Katz, A. E., Olsson, C. A., Raffo, A. J., Cama, C., Perlman, H., Seaman, E., O'Toole, K. M., McMahon, D., Benson, M. C., and Buttyan, R. Molecular staging of prostate cancer with the use of an enhanced reverse transcriptase-PCR assay. Urology, 43: 765-775, 1994.
43. Seiden, M. V., Kantoff, P. W., Krithivas, K., Propert, K., Bryant, M., Haltom, E., Gagnes, L., Kaplan, I., Bubley, G., De Wolf, W., and Sklar, J. Detection of circulating tumor cells in men with localized prostate cancer. J. Clin. Oncol., 12: 2634-2639, 1995.
44. Sokoloff, M. H., Tso, C. L., Kaboo, R., Nelson, S., Ko, J., Dorey, F., Figlin, R. A., Pang, S., de Kernion, J., and Belldegrun, A. Quantitative polymerase chain reaction does not improve preoperative prostate cancer staging: a clinicopathological molecular analysis of 121 patients. J. Urol., 156: 1560-1566, 1996.
45. Corey, E., Arfman, E. W., Oswin, M. M., Melchior, S. W., Tindall, D. J., Young, C. Y., Ellis, W. J., and Vessella, R. L. Detection of circulating prostatic cells by reverse transcriptase-polymerase chain reaction of human glandular kallikrein (Hk2) and prostatic-specific antigen (PSA) messages. Urology, 50: 184-188, 1997.
46. Wood, D. P., and Banerjee, M. Presence of circulating prostate cells in the bone marrow of patients undergoing radical prostatectomy is predictive of disease free survival. J. Clin. Oncol., 15: 3451-3457, 1997.
47. Olsson, C. A., de Vries, G. M., Raffo, A. J., Benson, M. C., O'Toole, K., Cao, Y., Buttyan, R. E., and Katz, A. E. Preoperative reverse transcriptase polymerase chain reaction for prostatic specific antigen predicts treatment failure following radical prostatectomy. J. Urol., 155: 1557-1562, 1996.
48. Ghossein, R., Rosai, J., Scher, H. I., Seiden, M., Zhang, Z. F., Sun, M., Chang, G., Berlane, K., Krithivas, K., and Kantoff, P. W. Prognostic significance of detection of prostate specific antigen transcripts in the peripheral blood of patients with metastatic androgen independent prostatic carcinoma. Urology, 50: 100-105, 1997.
49. Deguchi, T., Doi, T., Ehara, H., Ito, S., Takahashi, Y., Nishino, Y., Fujihiro, S., Kawamura, T., Komeda, H., Horie, M., Kaji, H., Shimokawa, K., Tanaka, T., and Kawada, Y. Detection of micrometastatic prostate cancer cells in lymph nodes by reverse transcriptase-polymerase chain reaction. Cancer Res., 53: 5350-5354, 1993.
50. Meyers, F., de Vere, W. R. W., Larkin, E., Chi, S. G., Borchers, M., Soares, S., and Gumerlock, P. H. Bone marrow molecular staging of prostatic carcinoma: does it help? Proc. Am. Soc. Clin. Oncol., 14: 230, 1995.
51. Edelstein, R. A., Zietman, A. L., de las Morenas, A., Krane, R. J., Babayan, R. K., Dallow, K. C., Traish, A., and Moreland, R. B. Implication of prostatic micrometastases to the pelvic lymph nodes: an archival tissue study. Urology, 47: 370-375, 1996.
52. Price, D. K., Woodard, W. L., and Teigland, C. M. Simultaneous detection of prostate specific antigen-expressing and prostate-specific membrane antigen expressing cells by a multiplex reverse transcriptase polymerase chain reaction assay. Urol. Oncol., 1: 226-233, 1995.
53. Sun, Y., Lin, J., Katz, A. E., and Fisher, P. B. Human prostatic carcinoma PTI-1 is expressed in human tumor cell lines and prostate carcinoma patient blood samples. Cancer Res., 57: 18-23, 1997.
54. Wright, G. L., Jr., Haley, C., Beckett, M. L., and Schellhammer, P. F. Expression of the prostate biomarker 7E11-C5 in primary and metastatic prostatic carcinoma. Proc. Am. Assoc. Cancer Res., 35: 233, 1994.
55. Axelrod, H. R., Gilman, S. C., D'aleo, C. J., Petrylak, D., Reuter, V., Gulfo, J. V., Saad, A., Cordon-Cardo, C, and Scher, H. I. Preclinical results and immunohistochemical studies with 90Y-CYT-356:a new prostatic cancer therapeutic agent. J. Urol., 147: 361A, 1992.
56. Wright, G. L., Jr., Haley, C., Beckett, M, L., and Schellhammer, P. F. Expression of prostate-specific membrane antigen in normal, benign and malignant prostatic tissue. Urol. Oncol., 1: 18-28, 1995.
57. Shen, R., Su, Z., Olsson, C. A., and Fisher, P. B. Identification of the human prostatic carcinoma oncogene PTI-1 by rapid expression cloning and differential RNA display. Proc. Natl. Acad. Sci. USA, 92: 6778-6782, 1995.
58. Seiden, M., and Sklar, J. L. PCR and RT-PCR-based methods of tumor detection: potential applications and clinical implications. In: V. T. DeVita, S. Hellman, and S. A. Rosenberg (eds.), Important Advances in Oncology, pp. 191-204. Philadelphia: Lippincott, 1996.
59. Schlimock, G., and Riethmuller, G. Detection, characterization and tumorigenicity of disseminated tumor cells in human bone marrow. Semin. Cancer Biol., 1: 207, 1990.
60. Ghalie, R. The Osborne/Rosen article reviewed. Oncology, 8: 36-40, 1994.
61. Osborne, M. P., Asina, S., Wong, G. Y., Old, L. J., and Cote, R. J. Immunofluorescent monoclonal antibody detection of breast cancer in bone marrow: sensitivity in a model system. Cancer Res., 49: 2510-2513, 1989.
62. Cote, R. J., Rosen, P. P., Lesser, M. L., Old, L. J., and Osborne, M. P. Prediction of early relapse in patients with operable breast cancer by detection of occult bone marrow micrometastases. J. Clin. Oncol., 9: 1749-1756, 1991.
63. Fields, K. K., Elfenbein, G. J., Trudeau, W. L., Perkins, J. B., Janssen, W. E., and Moscinski, L. C. Clinical significance of bone marrow metastases as detected using the polymerase chain reaction in patients with breast cancer undergoing high-dose chemotherapy and autologous bone marrow transplantation. J. Clin. Oncol., 14: 1868-1876, 1996.
64. Datta, Y. H., Adams, P. T., Drobyski, W. R., Ethier, S. P., Terry, V. H., and Roth, M. S. Sensitive detection of occult breast cancer by the reverse-transcriptase polymerase chain reaction. J. Clin. Oncol., 12: 475-482, 1994.
65. Mori, M., Mimori, K., Inoue, H., Barnard, G. F., Tsuji, K., Nanbara, S., Ueo, H., and Akiyoshi, T. Detection of cancer micrometastases in lymph nodes by reverse transcriptase-polymerase chain reaction. Cancer Res., 55: 3417-3420, 1995.
66. Brown, D. C., Purushotam, A. D., Birnie, G. D., and George, W. D. Detection of intraoperative tumor cell dissemination in patients with breast cancer by use of the reverse transcription and polymerase chain reaction. Surgery, 117: 96-101, 1995.
67. Noguchi, S., Aihara, T., Nakamori, S., Motomura, K., Inaji, H., Imaoka, S., and Koyama, H. The detection of breast carcinoma micrometastases in axillary lymph nodes by means of reverse transcriptase-polymerase chain reaction. Cancer (Phila.), 74: 1595-1600, 1994.
68. Noguchi, S., Aihara, T., Motomura, K., Inaji, H., Imaoka, S., and Koyama, H. Detection of breast cancer micrometastases in axillary lymph nodes by means of reverse transcriptase polymerase chain reaction. Comparison between MUC1 mRNA and keratin 19 mRNA amplification. Am. J. Pathol., 148: 649-656, 1996.
69. Mori, M., Mimori, K., Ueo, H., Tsuji, K., Shirashi, T., Barnard, G. F., Sugimachi, K., and Akiyoshi, T. Clinical significance of molecular detection of carcinoma cells in lymph nodes and peripheral blood by reverse transcription-polymerase chain reaction in patients with gastrointestinal or breast carcinomas. J. Clin. Oncol., 16: 128-132, 1998.
70. Bostick, P. J., Chatterjee, S., Chi, D. D., Huynh, K. T., Giuliano, A. E., Cote, R., and Hoon, D. S. Limitations of specific reverse-transcriptase polymerase chain reaction markers in the detection of metastases in lymph nodes and blood of breast cancer patients. J. Clin. Oncol., 16: 2632-2640, 1998.
71. Krisman, M., Todt, B., Schroder, J., Gareis, D., Muller, K. M., Seeber, S., and Schutte, J. Low specificity of cytokeratin 19 reverse transcriptase polymerase chain reaction analyses for detection of hematogenous lung cancer dissemination. J. Clin. Oncol., 13: 2769-2775, 1995.
72. Battayani, Z., Grob, J. J., Xerri, L., Noe, C., Zarour, H., Houvaeneghel, G., Delpero, J. R., Birnbaum, D., Hassoun, J., and Bonerandi, J. J. Polymerase chain reaction detection of circulating melanocytes as a prognostic marker in patients with melanoma. Arch. Dermatol., 131: 443-447, 1995.
73. Buzaid, A. C., and Balch, C. M. Polymerase chain reaction for detection of melanoma in peripheral blood: too early to assess clinical value. J. Natl. Cancer Inst., 88: 569-570, 1996.
74. Hoon, D. S. B., Wang, Y., Dale, P. S., Conrad, A. J., Schmid, P., Garrison, D., Kuo, C., Foshag, L. J., Nizze, A. J., and Mortal, D. L. Detection of occult melanoma cells in blood with a multiple-marker polymerase chain reaction assay, J. Clin. Oncol., 13: 2109-2116, 1995.
75. Kunter, U., Buer, J., Probst, M., Duensing, S., Dallmann, I., Grosse, J., Kirchner, H., Schluepen, E. M., Volkenandt, M., Ganser, A., and Atzpodien, J. Peripheral blood tyrosinase messenger RNA detection and survival in malignant melanoma. J. Natl. Cancer Inst., 88: 590-594, 1996.
76. Brossart, P., Keiholz, U., Willhauck, M., Scheibenbogen, C., Mohler, T., and Hunstein, W. Hematogenous spread of malignant melanoma cells in different stages of disease. J. Invest. Dermatol., 101: 887-889, 1993.
77. Foss, A. J., Guille, M. J., Occleston, N. L., Hykin, P. G., Hungerford, J. L., and Lightman, S. The detection of melanoma cells in peripheral blood by reverse transcriptase polymerase chain reaction. Br. J. Cancer, 72: 155-159, 1995.
78. Pittman, K., Burchill, S., Smith, B., Southgate, J., Joffe, J., Gore, M., and Selby, P. Reverse transcriptase-polymerase chain reaction for expression of tyrosinase to identify malignant melanoma cells in peripheral blood. Ann. Oncol., 7: 297-301, 1996.
79. Mellado, B., Colomer, D., Castel, T., Munoz, M,. Carballo, E., Galan, M., Mascaro, J. M., Vives-Corrons, J. L., Grau, J. J., and Estape, J. Detection of circulating neoplastic cells by reverse transcriptase polymerase chain reaction in malignant melanoma: association with clinical stage and prognosis. J. Clin. Oncol., 14: 2091-2097, 1996.
80. Curry, B. J., Myers, K., and Hersey, P. Polymerase chain reaction detection of melanoma cells in the circulation: relation to clinical stage, surgical treatment, and recurrence from melanoma. J. Clin. Oncol., 16: 1760-1769, 1998.
81. Coit, D., Ghossein, R. A., Vlamis, V., Satagopan, J., Livingston, P., Rosai, J., and Houghton, A. Prognostic significance of detection of tyrosinase mRNA in the peripheral blood and/or bone marrow of melanoma patients rendered surgically free of disease. Proc. Am. Soc. Clin. Oncol. 17: 541a, 1998.
82. Wang, X., Heller, R., VanVoorhis, N., Cruse, C. W., Glass, F., Fenske, N., Berman, C., Leo-Messina, J., Rappaport, D., Wells, K., De Conti, R., Moscinski, L., Stankard, C., Puleo, C., and Reintgen, D. Detection of submicroscopic lymph node metastases with polymerase chain reaction in patients with malignant melanoma. Ann. Surg., 220: 768-774, 1994.
83. Biegliek, S. C., Ghossein, R. A., Rosai, J., Bhattacharya, S., and Coit, D. G. The detection of tyrosinase mRNA by reverse transcriptase polymerase chain reaction (RT-PCR) in melanoma sentinel nodes. Ann. Surg. Oncol., 6: 232-240, 1999.
84. Funaki, N. O., Tanaka, J., Kasamatsu, T., Ohshio, G., Hosotani, R., Okino, T., and Imamura, M. Identification of carcinoembryonic antigen mRNA in circulating peripheral blood of pancreatic carcinoma and gastric carcinoma patients. Life Sci., 59: 2187-2199, 1996.
85. Mori, M., Mimori, K., Ueo, H., Karimine, N., Barnard, G. F., Sugimachi, K., and Akiyoshi, T. Molecular detection of circulating solid carcinoma cells in the peripheral blood: the concept of early systemic disease. Int. J. Cancer, 68: 739-743, 1996.
86. Liefers, G. J., Cleton-Jansen, A. M., Van de Velde, C. J. H., Hermans, J., Van Krieken, J. H., Cornelisse, C. J., and Tollenaar, R. A. Micrometastases and survival in stage II colorectal cancer. N. Engl. J. Med., 339: 223-228, 1998.
87. Bostick, P. J., Hoon, D. S. B., and Cote, R. C. Detection of carcinoembryonic antigen messenger RNA in lymph nodes from patients with colorectal cancer. N. Engl. J. Med., 339: 1643, 1998.
88. Zippelius, A., Kufer, P., Honold, G., Kollermann, M. W., Oberneer, R., Schlimock, G., Riethmuller, G., and Pantel, K. Limitations of reverse transcriptase polymerase chain reaction analyses for detection of micrometastatic epithelial cancer cells in bone marrow. J. Clin. Oncol., 15: 2701-2708, 1997.
89. Hardingham, J. E., Kotasek, D., Sage, R. E., Gooley, L. T., Mi, J. X., Dobrovic, A., Norman, J. E., Bolton, A. E., and Dale, B. M. Detection of circulating tumor cells in colorectal cancer by immunobead-PCR is a sensitive prognostic marker for relapse of disease. Mol. Med., 1: 789-794, 1995.
90. Lode, H. N., Handgretinger, R., Schuermann, U., Seitz, G., Klingebiel, T., Niethammer, D., and Beck, J. Detection of neuroblastoma cells in CD34+ selected peripheral stem cells using a combination of tyrosine hydroxylase nested RT-PCR and anti-ganglioside GD2 immunocytochemistry. Eur. J. Cancer, 33: 2024-2030, 1997.
91. Cheung, I. Y., and Cheung, N. K. V. Molecular detection of GAGE expression in peripheral blood and bone marrow: utility as a tumor marker for neuroblastoma. Clin. Cancer Res., 3: 821-826, 1997.
92. Van den Eynde, B., Peeters, O., De Backer, O., Gaugler, B., Lucas, S., and Boon, T. A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma. J. Exp. Med., 182: 689-698, 1995.
93. Brenner, M. Gene marking. Hum. Gene Ther., 7: 1927-1936, 1996.
94. Rill, D. R., Santana, V. M., Roberts, W. M., Nilson, T., Bowman, L. C., Krance, R. A., Heslop, H. E., Moen, R. C., Ihle, J. N., and Brenner, M. K. Direct demonstration that autologous bone marrow transplantation for solid tumors can return a multiplicity of tumorigenic cells. Blood, 84: 380-383, 1994.
95. Pfleiderer, C., Zoubek, A., Gruber, B., Kronberger, M., Ambros, P. F., Lion, T., Fink, F. M., Gardner, H., and Kovar, H. Detection of tumor cells in peripheral blood and bone marrow from Ewing tumor patients by RT PCR. Int. J. Cancer, 64: 135-139, 1995.
96. Peter, M., Magdelenat, H., Michon, J., Melot, T., Oberlin, O., Zucker, J. M., Thomas, G., and Delattre, O. Sensitive detection of occult Ewing's cells by the reverse transcriptase polymerase chain reaction. Br. J. Cancer, 72: 96-100, 1995.
97. Fagnou, C., Michon, J., Peter, M., Bernoux, A., Oberlin, O., Zucker, J. M., Magdelenat, H., and Delattre, O. Presence of tumor cells in bone marrow but not in blood is associated with adverse prognosis in patients with Ewing's tumor. J. Clin. Oncol., 16: 1707-1711, 1998.
98. Zoubek, A., Ladenstein, R., Windhager, R., Amann, G., Fischmeister, G., Kager, L., Jugovic, D., Ambros, P. F., Gadner, H., and Kovar, H. Predictive potential of testing for bone marrow involvement in Ewing tumor patients by RT PCR: a preliminary evaluation. Int. J. Cancer, 79: 56-60, 1998.
99. Matsumura, M., Niwa, Y., Kato, N., Komatsu, Y., Shiina, S., Kawabe, T., Kawase, T., Toyoshima, H., Ihori, M., and Shiratori, Y. Detection of α-fetoprotein mRNA, an indicator of hematogenous spreading hepatocellular carcinoma, in the circulation: a possible predictor of metastatic hepatocellular carcinoma. Hepatology, 20: 1418-1425, 1994.
100. Kar, S., and Carr, B. I. Detection of liver cells in peripheral blood of patients with advanced stage hepatocellular carcinoma. Hepatology, 21: 403-407, 1995.
101. Lemoine, A., Le Bricon, T., Salvucci, M., Azoulay, D., Pham, P., Raccuia, J., Bismuth, H., and Debuire, B. Prospective evaluation of circulating hepatocytes by α-fetoprotein mRNA in humans during liver surgery. Ann. Surg., 226: 43-50, 1997.
102. Muller, C., Peterman, D., Pfeffel, F., Oesterreicher, C., and Fugger, R. Lack of specificity of albumin mRNA positive cells as a marker of circulating hepatoma cells. Hepatology, 25: 896-899, 1997.
103. Stenman, J., Lintula, S., Hotakainen, K., Vartiainen, J., Lehvaslaiho, H., and Stenman, U. H. Detection of squamous cell carcinoma antigen-expressing tumour cells in blood by reverse transcriptase-polymerase chain reaction in cancer of the uterine cervix. Int. J. Cancer, 74: 75-80, 1997.
104. Pao, C. C., Hor, J. J., Yang, F. P., Lin, C. Y., and Tseng, C. J. Detection of human papillomavirus mRNA and cervical cancer cells in peripheral blood of cervical cancer patients with metastasis. J. Clin. Oncol., 15: 1008-1012, 1997.
105. Ditkoff, B. A., Marvin, M. R., Yemul, S., Shi, Y. J., Chabot, J., Feind, C., and Lo Gerfo, P. L. Detection of circulating thyroid cells in peripheral blood. Surgery, 120: 959-965, 1996.
106. Tallini, G., Ghossein, R., Emanuel, J., Gill, J., Kinder, B., Dimich, A. B., Costa, J., Robbins, R., Burrow, G. N., and Rosai, J. Detection of thyroglobulin, thyroid peroxidase and RET/PTC1 mRNA in the peripheral blood of patients with thyroid disease. J. Clin. Oncol., 16: 1158-1166, 1998.
107. Ringel, M. D., Ladenson, P. W., and Levine, M. A. Molecular diagnosis of residual and recurrent thyroid cancer by amplification of thyroglobulin messenger ribonucleic acid in peripheral blood. J. Clin. Endocrinol. Metab., 83: 4435-4442, 1998.
108. Brennan, J. A., Mao, L,. Hruban, R. H., Boyle, J. O., Eby, Y. J., Koch, W. M., Goodman, S. N., and Sidransky, D. Molecular assessment of histopathological staging in squamous cell carcinoma of the head and neck. N. Engl. J. Med., 332: 429-435, 1995.
109. Brennan, J. A., and Sidransky, D. Molecular staging of head and neck squamous carcinoma. Cancer Metastasis Rev., 15: 3-10, 1996.
110. Weiss, L. Metastatic inefficiency. Adv. Cancer Res., 54: 159-211, 1990.
111. Glaves, D., Huben, R. P., and Weiss, L. Haematogenous dissemination of cells from human renal adenocarcinomas. Br. J. Cancer, 57: 32-35, 1988.
112. Sugarbaker, P. H. Metastatic inefficiency: the scientific basis for resection of liver metastases from colorectal cancer. J. Surg. Oncol., 3 (Suppl.): 158-160, 1993.
113. Martin, V. M., Siewert, C., Scharl, A., Harms, T., Heinze, R., Ohl, S., Radbruch, A., Miltenyi, S., and Schmitz, J. Immunomagnetic enrichment of disseminated epithelial tumor cells from peripheral blood by MACS. Exp. Hematol., 26: 252-264, 1998.
114. Racila, E., Euhus, D., Weiss, A. J., Rao, C., McConnell, J., Terstappen, L. W., and Uhr, J. W. Detection and characterization of carcinoma cells in blood. Proc. Natl. Acad. Sci. USA, 95: 4589-4594, 1998.
115. Ghossein, R. A., Osman, I., Bhattacharya, S., Ferrara, J., Fazzari, M., and Scher, H. I. Detection of circulating tumor cells in prostatic carcinoma using immunobead reverse transcriptase polymerase chain reaction for prostatic specific membrane antigen mRNA. Mod. Pathol., 12: 96A, 1999.
116. Johnson, P. W. M., Burchill, S. A., and Selby, P. J. The molecular detection of circulating tumor cells. Br. J. Cancer, 72: 268-276, 1995.