Prognostic significance of micrometastatic bone marrow involvement

Breast Cancer Research and Treatment

Volumn 52, Issue 1-3, 1998, Pages 201-216

  Braun, Stephan ^a   Pantel, Klaus ^a,b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

Author keywords

Bone marrow; Breast cancer; Cytokeratin; Immunocytochemistry; Micrometastasis; Monoclonal antibodies; Mucin; Prognosis

Indexed keywords

CELL ADHESION MOLECULE; CELL MEMBRANE PROTEIN; CYTOKERATIN; GROWTH FACTOR RECEPTOR; KI 67 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MESSENGER RNA; MONOCLONAL ANTIBODY; TUMOR ANTIGEN;

AUTOLOGOUS BONE MARROW TRANSPLANTATION; BONE MARROW METASTASIS; BREAST CANCER; CANCER DIAGNOSIS; CANCER IMMUNOTHERAPY; CANCER STAGING; CLINICAL TRIAL; CYTODIAGNOSIS; DIAGNOSTIC PROCEDURE; HUMAN; IMMUNOCYTOCHEMISTRY; PRIORITY JOURNAL; PROGNOSIS; REVIEW;

BONE MARROW; BREAST NEOPLASMS; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOHISTOCHEMISTRY; KI-67 ANTIGEN; NEOPLASM METASTASIS; POLYMERASE CHAIN REACTION; PROGNOSIS; RECEPTOR, ERBB-2;

EID: 0032412620     PISSN: 01676806     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006164914610     Document Type: Review

References (93)

1. Black RJ, Bray F, Ferlay J, Parkin DM: Cancer incidence and mortality in the European Union: cancer registry data and estimates of national incidence for 1990. Eur J Cancer 33:1075-1107, 1997
2. Pantel K: Detection of minimal disease in patients with solid tumors. J Hematother 5:359-367, 1996
3. Fidler IJ, Radinsky R: Genetic control of cancer metastasis. J Natl Cancer Inst 82:166-168, 1990
4. Liotta LA, Steeg PS, Stetler-Stevenson WG: Cancer metastasis and angiogenesis: an imbalance of positive and negative regulation. Cell 64:327-336, 1991
5. Schlimok G, Funke I, Holzmann B, Göttlinger HG, Schmidt G, Häuser H, Swierkot S, Warnecke HH, Schneider B, Koprowski H, Riethmüller G: Micrometastatic cancer cells in bone marrow: in vitro detection with anti-cytokeratin and in vivo labeling with anti-17-1A monoclonal antibodies. Proc Natl Acad Sci USA 84:8672-8676, 1987
6. Mansi JL, Berger U, Easton D, McDonnell T, Redding WH, Gazet JC, McKinna A, Powles TJ, Coombes RC: Micrometastases in bone marrow in patients with primary breast cancer: evaluation as an early predictor of bone metastases. Br Med J 295: 1093-1096, 1987
7. Mansi JL, Easton D, Berger U, Gazet JC, Ford HT, Dearnaley D, Coombes RC: Bone marrow micrometastases in primary breast cancer: prognostic significance after 6 years' follow-up. Eur J Cancer 27:1552-1555, 1991
8. Harbeck N, Untch M, Pache L, Eiermann W: Tumour cell detection in the bone marrow of breast cancer patients at primary therapy: results of a 3-year median follow-up. Br J Cancer 69:566-571, 1994
9. Diel IJ, Kaufmann M, Costa SD, Holle R, von Minckwitz G, Solomayer EF, Kaul S, Bastert G: Micrometastatic breast cancer cells in bone marrow at primary surgery: prognostic value in comparison with nodal status. J Natl Cancer Inst 88:1652-1664, 1996
10. Cote RJ, Rosen PP, Lesser ML, Old LJ, Osborne MP: Prediction of early relapse in patients with operable breast cancer by detection of occult bone marrow micrometastases. J Clin Oncol 9:1749-1756, 1991
11. Schlimok G, Lindemann F, Holzmann K, Witte J, Renner D, Riethmüller G: Prognostic significance of disseminated tumor cells detected in bone marrow of patients with breast and colorectal cancer: a multivariate analysis. Proc Am Soc Clin Oncol 11:102 (abstract), 1992
12. Salvadori B, Squicciarini P, Rovini D, Orefice S, Andreola S, Rilke F, Barletta L, Menard S, Colnaghi MI: Use of monoclonal antibody MBrl to detect micrometastases in bone marrow specimens of breast cancer patients. Eur J Cancer 26:865-867, 1990
13. Courtemanche DJ, Worth AJ, Coupland RW, Rowell JL, MacFarlane JK: Monoclonal antibody LICR-LON-M8 does not predict the outcome of operable breast cancer. Can J Surg 34:21-26, 1991
14. Mathieu MC, Friedman S, Bosq J, Caillou B, Spielmann M, Travagli JP, Contesso G: Immunohistochemical staining of bone marrow biopsies for detection of occult metastasis in breast cancer. Breast Cancer Res Treat 15:21-26, 1990
15. Gogas H, Mansi JL, Bliss J, Coombes RC: Can the presence of micrometastases in primary breast cancer predict outcome? Long-term (median 12.5 yrs) followup. Proc ASCO 16:153a (abstract #537), 1997
16. Kirk SJ, Cooper GG, Hoper M, Watt PC, Roy AD, Olding-Smee W: The prognostic significance of marrow micrometastases in women with early breast cancer. Eur J Surg Oncol 16:481-485, 1990
17. Singletary SE, Larry L, Trucker SL, Spitzer G: Detection of micrometastatic tumor cells in bone marrow of breast carcinoma patients. J Surg Oncol 47:32-36, 1991
18. Osborne M, Rosen P: Detection and management of bone marrow micrometastases in breast cancer. Oncology 8:25-36, 1994
19. Mansi JL, Berger U, Wilson P, Shearer R, Coombes RC: Detection of tumor cells in bone marrow of patients with prostatic carcinoma by immunocytochemical techniques. J Urology 139:545-548, 1988
20. Braun S, Müller M, Hepp F, Schlimok G, Riethmüller G, Pantel K: Re: Micrometastatic breast cancer cells in bone marrow at primary surgery: Prognostic value in comparison with nodal status. J Natl Cancer Inst, in press
21. Pantel K, Izbicki JR, Passlick B, Angstwurm M, Häussinger K, Thetter O, Riethmüller G: Frequency and prognostic significance of isolated tumour cells in bone marrow of patients with non-small cell lung cancer without overt metastases. Lancet 347:649-653, 1996
22. Schlimok G, Funke I, Bock B, Schweiberer B, Witte J, Riethmüller G: Epithelial tumor cells in bone marrow of patients with colorectal cancer: immunocytochemical detection, phenotypic characterization, and prognostic significance. J Clin Oncol 8:831-837, 1990
23. Braun S, Pantel K: Biological characteristics of micrometastatic carcinoma cells in bone marrow. In: Günthert U, Birchmeier W (eds) Attempts to understand metastasis formation, Vol 213/I, pp 163-177. Springer, Berlin-New York-Tokyo, 1996
24. Pantel K, Schlimok G, Angstwurm M, Weckermann C, Schmaus W, Gath H, Passlick B, Izbicki J, Riethmüller G: Methodological analysis of immunocytochemical screening for disseminated epithelial tumor cells in bone marrow. J Hematother 3:165-173, 1994
25. Gallee MPW, van Vroonhoven CCJ, van der Korput HAGM, van der Kwast TH, ten Kate FJW, Romijn JC, Trapman J: Characterization of monoclonal antibodies raised against prostatic cell line PC-82. Prostate 9:33-45, 1986
26. Osborne M, Wong G, Asina S, Old L, Cote R, Rosen P: Sensitivity of immunocytochemical detection of breast cancer cells in human bone marrow. Cancer Res 51:2706-2709, 1991
27. Molino A, Colombatti M, Bonetti F, Zardini M, Pasini F, Perini A, Pelosi G, Tridente G, Veneri D, Cetto GL: A comparative analysis of three different techniques for the detection of breast cancer cells in bone marrow. Cancer 67:1033-1036, 1991
28. Jauch KW, Heiss MM, Gruetzner KU, Funke I, Pantel K, Babic R, Eissner HJ, Riethmüller G, Schildberg FW: Prognostic significance of bone marrow micrometastases in patients with gastric cancer. J Clin Oncol 14:1810-1817, 1996
29. Diel IJ, Kaufmann M, Goerner R, Costa SD, Kaul S, 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
30. Schwarz G: Cytomorphology and cell yield in a new cytocentrifugal technique allowing the collection of the cell-free supernatant. Lab Med 15:45-50, 1991
31. Gribben JG, Freedman AS, Neuberg D: Immunologic purging of marrow assessed by PCR before autologous bone marrow transplantation of B-cell lymphoma. N Engl J Med 325:1525-1533, 1991
32. Bos IL: Ras oncogenes in human cancer: a review. Cancer Res 49:4682-4689, 1989
33. Harris CC, Hollstein M: Clinical implications of the p53 tumor-suppressor gene. N Engl J Med 329:1318-1327, 1993
34. Hayashi N, Arakawa H, Nagase H, Yanagisawa A, Kato Y, Ohta H, Takano S, Ogawa M, Nakamura Y: Genetic diagnosis identifies occult lymph node metastases undetectable by the histopathological method. Cancer Res 54:3853-3856, 1994
35. Hayashi N, Ito I, Yanagisawa A, Kato Y, Nakamori S, Imaoka S, Watanabe H, Ogawa M, Nakamura K: Genetic diagnosis of lymph-node metastasis in colorectal cancer. Lancet 345:1257-1259, 1995
36. Zippelius A, Kufer P, Honold G, Köllermann MW, Oberneder R, Schlimok G, Riethmüller G, Pantel K: Limitations of reverse transcriptase-polymerase chain reaction for detection of micrometastatic epithelial cancer cells in bone marrow. J Clin Oncol 15:2701-2708, 1997
37. de Graaf H, Mælandssmo GM, Ruud P, Forus A, Øyjord T, Fodstad Ø, Hovig E: Ectopic expression of target genes may represent an inherent limitation of RT-PCR assays used for micrometastasis detection: studies on the epithelial glycoprotein gene EGP-2. Int J Cancer 722:191-196, 1997
38. Krismann M, Todt B, Schröder J, Gareis D, Müller KM, Seeber S, Schütte 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
39. Schoenfeld A, Luqmani Y, Smith D, O'Reilly S, Shousha S, Sinnett HD, Coombes RC: Detection of breast cancer micrometastases in axillary lymph nodes by using Polymerase Chain Reaction. Cancer Res 54: 2986-2990, 1994
40. Traweek ST, Liu J, Battifora H: Keratin gene expression in non-epithelial tissues. Detection with polymerase chain reaction. Am J Pathol 142:1111-1118, 1993
41. Datta YH, Adams PT, Drobyski WR: Sensitive detection of occult breast cancer by the reverse-transcriptase polymerase chain reaction. J Clin Oncol 12:475-482, 1994
42. Fields KK, Elfenbein GJ, Trudeau WL, Perlinss JB, Jansen WE, Moscinski LC: Clinical significance of bone marrow metastases as detected using polymerase chain reaction in patients with breast cancer undergoing high-dose chemotherapy and autologous bone marrow transplantation. J Clin Oncol 14:1868-1876, 1996
43. Gerhard M, Juhl H, Kalthoff H, Schreiber HW, Wagener C, 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
44. Kamby K, Guldhammer B, Vejborg I, Rossing N, Dirksen H, Daugaard S, Mouridsen HT: The presence of tumor cells in bone marrow at the time of first recurrence of breast cancer. Cancer 60:1306-1312, 1987
45. Ridell B, Landys K: Incidence and histopathology of metastases of mammary carcinoma in biopsies from the posterior iliac crest. Cancer 44:1782-1788, 1979
46. Redding HW, Coombes RC, Monagham P, Clink HMD, Imrie SF, Dearnaley DP, Ormerod MG, Sloane JP, Gazet JC, Powles TJ, Neville AM: Detection of micrometastases in patients with primary breast cancer. Lancet ii:1271-1274, 1983
47. Taylor-Papadimitriou J, Burchell J, Moss F, Beverly P: Monoclonal antibodies to epithelial membrane antigen and human milk fat globule mucin define epitopes expressed on other molecules. Lancet i:458, 1985
48. Heyderman E, Macartney JC: Epithelial membrane antigen and lymphoid cells. Lancet i:109, 1985
49. Delsol G, Gatter KC, Stein H, Erber WN, Pulfod KAF, Zinne K, Mason DY: Human lymphoid cells express epithelial membrane antigen. Lancet ii: 1124-1128, 1984
50. Berger U, Bettelheim R, Mansi JL, Easton D, Coombes RC, Neville AM: The relationship between micrometastases in the bone marrow, histopathologic features of the primary tumor in breast cancer and prognosis. Am J Clin Pathol 90:1-6, 1988
51. Cote RJ, Rosen PP, Hakes TB, Sedira M, Bazinet M, Kinne DW, Old LJ, Osborne MP: Monoclonal antibodies detect occult breast carcinoma metastases in the bone marrow of patients with early stage disease. Am J Surg Pathol 12:333-340, 1988
52. Pantel K, Braun S, Schlimok G, Janni W, Hepp F, Kentenich C, Müller M, Sommer HL, Riethmüller G: Association of cytokeratin(CK)-positive breast cancer (BC) micrometastases with early recurrence and poor overall survival. Proc ASCO, submitted, 1998
53. Fox SB, Leek RD, Bliss J, Mansi JL, Gusterson B, Gatter KC, Harris AL: Association of tumor angiogenesis with bone marrow micrometastases in breast cancer. J Natl Cancer Inst 89:1044-1049, 1997
54. Schlimok G, Lindemann F, Holzmann K, Witte J, Pantel K, Riethmüller G: Prognostic significance of tumor cells detected in bone marrow of breast cancer patients. In: The Lancet Conference, 1994, Brugge, Belgium, p 47
55. Pantel K, Schlimok G, Kutter D, Schaller G, Genz T, Wiebecke B, Backmann R, Funke I, Riethmüller G: Frequent down-regulation of major histocompatibility class I antigen expression on individual micrometastatic carcinoma cells. Cancer Res 51:4712-4715, 1991
56. Pantel K, Schlimok G, Braun S, Kutter D, Schaller G, Funke I, Izbicki J, Riethmüller G: Differential expression of proliferation-associated molecules in individual micrometastatic carcinoma cells. J Natl Cancer Inst 85:1419-1424, 1993
57. Gerdes J, Lemke H, Baisch H, Wacker HH, Schwab U, Stein H: Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67. J Immunol 133:1710-1715, 1984
58. Freeman JW, Busch RK, Gyorkey F, Gyorkey P, Ross BE, Busch H: Identification and characterization of a human proliferation-associated nucleolar antigen with a molecular weight of 120,000 expressed in early G1 phase. Cancer Res 48:1244-1251, 1988
59. Ochs RL, Reilly MT, Freeman JW, Busch H: Intranucleolar localization of human proliferating cell nucleolar antigen p120. Cancer Res 48:6523-6529, 1988
60. Schlimok G, Riethmüller G: Detection, characterization and tumorigenicity of tumor cells in human bone marrow. Semin Cancer Biol 1:207-215, 1990
61. Slamon JD, Godolphin W, Jones LA, Holt JA, Wong SG, Keith DE, Levin WJ, Stuart SG, Udove J, Ullrich A, Press MF: Studies of the HER-2/neu proto-oncogene in human breast cancer and ovarian cancer. Science 244:707-712, 1989
62. Bianchi S, Paglierani M, Zampi G, Cardona G, Cataliotti L, Bonardi R, Ciatto S: Prognostic significance of c-erbB-2 expression in node negative breast cancer. Br J Cancer 67:625-629, 1993
63. Berger MS, Locher GW, Saurer S, Gullick WJ, Waterfield MD, Groner B, Hynes NE: Correlation of c-erbB-2 gene amplification and protein expression in human breast carcinoma with nodal status and nuclear grading. Cancer Res 48:1238-1243, 1988
64. Tiwari RK, Borgen PI, Wong GY, Cordon CC, Osborne MP: HER-2/neu amplification and overexpression in primary human breast cancer is associated with early metastasis. Anticancer Res 12:419-425, 1992
65. Varley JM, Swallow JE, Brammar WJ, Whittaker JL, Walker RA: Alterations to either c-erbB-2(neu) or c-myc proto-oncogenes in breast carcinomas correlate with poor short-term prognosis. Oncogene 1:423-430, 1987
66. Venter DJ, Tuzi NL, Kumar S, Gullick WJ: Overexpression of the c-erb-B-2 oncoprotein in human breast carcinomas: immunohistochemical assessment correlates with gene amplification. Lancet ii: 69-72, 1987
67. Taylor-Papadimitriou J: Oncogene signalling, epithelial polarity, and metastatic phenotype. In: The Lancet Conference, 1994, Brugge, Belgium, p 7
68. Hoffman M: New clue found to oncogene's role in breast cancer. Science 256:1129, 1992
69. Lupu R, Colomer R, Kannan B, Lippman ME: Characterization of a growth factor that binds exclusively to the erbB2 receptor and induces cellular responses. Proc Natl Acad Sci USA 89:2287-2291, 1992
70. Peles E, Bacus SS, Koski RA, Lu HS, Wen D, Ogden SG, Levy RB, Yarden Y: Isolation of the neu/HER-2 stimulatory ligand: a 44 kD glycoprotein that induces differentiation of mammary tumor cells. Cell 69:205-216, 1992
71. Riethmüller G, Johnson JP: Monoclonal antibodies in the detection and therapy of micrometastatic epithelial cancer. Curr Opin Immunol 4:647-655, 1992
72. Hämmerling G, Maschek V, Sturmhöfel K, Momburg F: Regulation and functional role of MHC expression on tumors. In: Melchers F (ed) Prog Immunol. Springer, Berlin, 1989, pp 1071-1078
73. Pardoll DM: Cancer vaccines. Immunol Today 14: 310-316, 1993
74. Nabel GJ, Felgner PL: Direct gene transfer for immunotherapy and immunization. In: Robinson C, Watson F (eds) Trends in Biotechnology: Gene Therapy - Therapeutic Strategies and Commercial Prospects. Bousfield, Cambridge, 1993, pp 211-214
75. Behrens J, Frixen U, Schipper I, Weidner M, Birchmeier W: Cell adhesion in invasion and metastasis. Semin Cell Biol 3:169-178, 1992
76. Hart IR, Goode NT, Wilson RE: Molecular aspects of the metastatic cascade. Biochim Biophys Acta 989: 65-84, 1989
77. Schwarz MA, Owaribe K, Kartenbeck J, Franke WW: Desmosomes and hemidesmosomes: Constitutive molecular components. Annu Rev Cell Biol 6:461-491, 1990
78. Göttlinger HG, Funke I, Johnson JP, Gokel JM, Riethmüller G: The epithelial cell surface antigen 17-1A, a target for antibody-mediated tumor therapy: Its biochemical nature, tissue distribution and recognition by different monoclonal antibodies. Int J Cancer 38:47-53, 1986
79. Litvinov SV, Velders MP, Bakker HAM, Fleuren GJ, Warnaar SO: Ep-CAM: a human epithelial antigen is a homophilic cell-cell adhesion molecule. J Cell Biol 125:437-446, 1994
80. Riethmüller G, Schneider-Gädicke E, Schlimok G, Schmiegel W, Raab R, Höffken K, Gruber R, Pichlmaier H, Hirche H, Pichlmayr R, Buggisch P, Witte J, The German Cancer Aid 17-1A Study Group: Randomised trial of monoclonal antibody for adjuvant therapy of resected Dukes C colorectal carcinoma. Lancet 343:1177-1183, 1994
81. Schlimok G, Pantel K, Loibner H, Fackler-Schwalbe I, Riethmüller G: Reduction of metastatic carcinoma cells in bone marrow by intravenously administered monoclonal antibody: towards a novel surrogate test to monitor adjuvant therapies of solid tumours. Eur J Cancer 31A:1799-1803, 1995
82. Scholz D, Lubeck M, Loibner H: Biological activity in the human system of isotype variants of oligosaccharide Y-specific murine monoclonal antibodies. Cancer Immunol Immunother 33:153-157, 1991
83. Hempel D, Müller P, Oruzio D, Ehnle S, Schlimok G: Adoptive immunotherapy with monoclonal antibody 17-1A to reduce minimal residual disease in breast cancer patients after high-dose chemotherapy. Blood 90 Suppl 1:379B, abstract #4454, 1997
84. Hohaus S, Funk L, Brehm M, Abdallah A, Murea S, Kaul S, Haas R: Persistence of isolated tumor cells in patients with breast cancer after sequential high-dose therapy with peripheral blood stem cell transplantation. Blood 88 suppl 10:128A, abstract #501, 1996
85. Baselga J, Tripathy D, Mendelsohn J, Baughman S, Benz CC, Dantis L, Sklarin NT, Seidman AD, Hudis CA, Moore J, Rosen PP, Twaddell T, Henderson IC, Norton N: Phase II study of weekly intravenous recombinant humanized anti-p185Her2 monoclonal antibody in patients with Her2/neu-overexpressing metastatic breast cancer. J Clin Oncol 14:737-744, 1996
86. Jain RK: Physiological barriers to delivery of monoclonal antibodies and other macromolecules in tumors. Cancer Res 50:2741-2451, 1990
87. Dillman RO: Antibodies as cytotoxic therapy. J Clin Oncol 12:1497-1515, 1994
88. Braun S, Hepp F, Sommer HL, Pantel K: Tumor antigen heterogeneity of disseminated breast cancer cells: Implications for immunotherapy of minimal residual disease. Int J Cancer, in press
89. Scott AM, Welt S: Antibody-based immunological therapies. Curr Opin Immunol 9:717-722, 1997
90. Funke I, Schraut W: Meta-analysis of studies on bone marrow micrometastases: An independent prognostic impact remains to be substantiated. J Clin Oncol, in press, 1997
91. Roberts WM, Estrov Z, Ouspenskaia MV, Johnston DA, McClain KL, Zipf TF: Measurement of residual leukemia during remission in childhood acute lymphoblastic leukemia. N Engl J Med 336:317-323, 1997
92. Pantel K, Dickmanns A, Zippelius A, Klein C, Shi J, Hoechtlen-Vollmar W, Schlimok G, Weckermann D, Oberneder R, Fanning E, Riethmüller G: Establishment of micrometastatic carcinoma cell lines: a novel source of tumor cell vaccines. J Natl Cancer Inst 87:1162-1168, 1995
93. Pantel K, Putz E, Riethmüller G: Identification of new therapeutic targets on bone marrow micrometastases. Blood 90, Suppl 1:421A, abstract #1871, 1997