Consensus criteria for sensitive detection of minimal neuroblastoma cells in bone marrow, blood and stem cell preparations by immunocytology and QRT-PCR: Recommendations by the International Neuroblastoma Risk Group Task Force

British Journal of Cancer

Volumn 100, Issue 10, 2009, Pages 1627-1637

  Beiske, K ^a,i   Burchill, S A ^b   Cheung, I Y ^c   Hiyama, E ^d   Seeger, R C ^e   Cohn, S L ^f   Pearson, A D J ^g   Matthay, K K ^h  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^d HIROSHIMA UNIVERSITY   (Japan)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^f UNIVERSITY OF CHICAGO   (United States)

^g INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Immunocytology; INRG; Minimal disease; Neuroblastoma; QRT PCR

Indexed keywords

GANGLIOSIDE GD2; MESSENGER RNA; TUMOR ANTIGEN; TYROSINE 3 MONOOXYGENASE;

ARTICLE; BLOOD SAMPLING; BONE MARROW BIOPSY; CANCER CYTODIAGNOSIS; CANCER DIAGNOSIS; DIAGNOSTIC VALUE; DISSEMINATED CANCER; FLOW CYTOMETRY; FLUORESCENCE IN SITU HYBRIDIZATION; HUMAN; IMMUNOCYTOCHEMISTRY; LABORATORY DIAGNOSIS; MINIMAL RESIDUAL DISEASE; MYELOABLATIVE CONDITIONING; NEUROBLASTOMA; NEUROBLASTOMA CELL; NUCLEIC ACID ANALYSIS; PERIPHERAL BLOOD STEM CELL; PRACTICE GUIDELINE; PRIORITY JOURNAL;

ADVISORY COMMITTEES; ALGORITHMS; BONE MARROW; CONSENSUS; HEALTH PLANNING GUIDELINES; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASM, RESIDUAL; NEOPLASTIC CELLS, CIRCULATING; NEOPLASTIC STEM CELLS; NEUROBLASTOMA; REFERENCE STANDARDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SPECIMEN HANDLING;

EID: 67349179161     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605029     Document Type: Article

References (84)

1. Athale UH, Shurtleff SA, Jenkins JJ, Poquette CA, Tan M, Downing JR, Pappo AS (2001) Use of reverse transcriptase polymerase chain reaction for diagnosis and staging of alveolar rhabdomyosarcoma, Ewing sarcoma family of tumors, and desmoplastic small round cell tumor. J Pediatr Hematol Oncol 23: 99-104
2. Avigad S, Cohen IJ, Zilberstein J, Liberzon E, Goshen Y, Ash S, Meller I, Kollender Y, Issakov J, Zaizov R, Yaniv I (2004) The predictive potential of molecular detection in the nonmetastatic Ewing family of tumors. Cancer 100: 1053-1058
3. Beck D, Maritaz O, Gross N, Favrot M, Vultier N, Bailly C, Villa I, Gentilhomme O, Philip T (1988) Immunocytochemical detection of neuroblastoma cells infiltrating clinical bone marrow samples. Eur J Pediatr 147: 609-612
4. Beillard E, Pallisgaard N, van der Velden VH, Bi W, Dee R, van der Schoot E, Delabesse E, Macintyre E, Gottardi E, Saglio G, Watzinger F, Lion T, van Dongen JJ, Hokland P, Gabert J (2003) Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using 'real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe Against Cancer program. Leukemia 17: 2474-2486
5. Beiske K, Ambros PK, Burchill SA, Cheung IY, Swerts K (2005) Detecting minimal residual disease in neuroblastoma patients - the present state of the art. Cancer Lett 228: 229-240
6. Brenner MK (1995) The contribution of marker gene studies to hemopoietic stem cell therapies. Stem Cells 13: 453-461
7. Brenner MK, Rill DR, Moen RC, Krance RA, Heslop HE, Mirro Jr J, Anderson WF, Ihle JN (1994) Gene marking and autologous bone marrow transplantation. Ann NY Acad Sci 716: 204-214
8. Brodeur G, Pritchard J, Berthold F, Carlsen NL, Castel V, Castelberry RP, De Bernardi B, Evans AE, Favrot M, Hedborg F, Kaneko M, Kemshead J, Lampert F, Lee REJ, Look T, Pearson ADJ, Philip T, Roald B, Sawada T, Seeger RC, Tsuchida Y, Voute PA (1993) Revisions of the international criteria for neuroblastoma diagnosis, staging and response to treatment. J Clin Oncol 11: 1466-1477
9. Brodeur G, Seeger RC, Barrett A, Berthold F, Castleberry RP, D'Angio G, De Bernadi B, Evans AE, Favrot M, Freeman AI, Haase G, Hartmann O, Hayes FA, Helson L, Kemshead J, Lampert F, Ninane J, Ohkawa H, Philip T, Pinkerton CR, Pritchard J, Sawada T, Siegel S, Ide Smith E, Tsuchida Y, Voute PA (1988) International criteria for diagnosis, staging, and response to treatment in patients with neuroblastoma. J Clin Oncol 6: 1874-1881
10. Brodeur GM (2003) Neuroblastoma: biological insights into a clinical enigma. Nat Rev Cancer 3: 203-216
11. Burchill SA, Bradbury FM, Selby P, Lewis IJ (1995) Early clinical evaluation of neuroblastoma cell detection by reverse transcriptase-polymerase chain reaction (RT-PCR) for tyrosine hydroxylase mRNA. Eur J Cancer 31: 553-556
12. Burchill SA, Bradbury FM, Smith B, Lewis IJ, Selby P (1994) Neuroblastoma cell detection by reverse transcriptase-polymerase chain reaction (RT-PCR) for tyrosine hydroxylase mRNA. Int J Cancer 57: 671-675
13. Burchill SA, Kinsey SE, Picton S, Roberts P, Pinkerton CR, Selby P, Lewis IJ (2001b) Minimal residual disease at the time of peripheral blood stem cell harvest in patients with advanced neuroblastoma. Med Pediatr Oncol 36: 213-219
14. Burchill SA, Lewis IJ, Abrams KR, Riley R, Imeson J, Pearson AD, Pinkerton R, Selby P (2001a) Circulating neuroblastoma cells detected by reverse transcriptase polymerase chain reaction for tyrosine hydroxylase mRNA are an independent poor prognostic indicator in stage 4 neuroblastoma in children over 1 year. J Clin Oncol 19: 1795-1801
15. Burchill SA, Selby P (1999) Early detection of small volume disease using molecular technology. Cancer Top 10: 1-4
16. Burchill SA, Selby PJ (2000) Molecular detection of low-level disease in patients with cancer. J Pathol 190: 6-14
17. Campana D, Coustan-Smith E (2002) Advances in the immunological monitoring of childhood acute lymphoblastic leukaemia. Best Pract Res Clin Haematol 15: 1-19
18. Campana D, Neale GA, Coustan-Smith E, Pui CH (2001) Detection of minimal residual disease in acute lymphoblastic leukemia: the St Jude experience. Leukemia 15: 278-279
19. Cheung IY, Barber D, Cheung NK (1998) Detection of microscopic neuroblastoma in marrow by histology, immunocytology, and reverse transcription-PCR of multiple molecular markers. Clin Cancer Res 4: 2801-2805
20. Cheung IY, Cheung NK (2001) Quantitation of marrow disease in neuroblastoma by real-time reverse transcription-PCR. Clin Cancer Res 7: 1698-1705
21. Cheung IY, Feng Y, Gerald W, Cheung NK (2008) Exploiting gene expression profiling to identify novel minimal residual disease markers of neuroblastoma. Clin Cancer Res 14: 7020-7027
22. Cheung IY, Feng Y, Vickers A, Gerald W, Cheung NK (2007) Cyclin D1, a novel molecular marker of minimal residual disease, in metastatic neuroblastoma. J Mol Diagn 9: 237-241
23. Cheung IY, Lo Piccolo MS, Kushner BH, Cheung NK (2003) Quantitation of GD2 synthase mRNA by real-time reverse transcriptase polymerase chain reaction: clinical utility in evaluating adjuvant therapy in neuroblastoma. J Clin Oncol 21: 1087-1093
24. Cheung IY, Sahota A, Cheung NK (2004) Measuring circulating neuro-blastoma cells by quantitative reverse transcriptase-polymerase chain reaction analysis. Correlation with its paired bone marrow and standard disease markers. Cancer 101: 2303-2308
25. Cheung NK, Heller G, Kushner BH, Liu C, Cheung IY (1997) Detection of metastatic neuroblastoma in bone marrow: when is routine marrow histology insensitive? J Clin Oncol 15: 2807-2817
26. Cheung NK, Saarinen UM, Neely JE, Landmeier B, Donovan D, Coccia PF (1985) Monoclonal antibodies to a glycolipid antigen on human neuroblastoma cells. Cancer Res 45: 2642-2649
27. Cheung NK, Van Hoff DD, Strandjord SE, Coccia PF (1986) Detection of neuroblastoma cells in bone marrow using GD2 specific monoclonal antibodies. J Clin Oncol 4: 363-369
28. Cohn SL, Pearson ADJ, London WB, Monclair T, Ambros PF, Brodeur GM, Faldum A, Hero B, Iehara T, Machin D, Mosseri V, Simon T, Garaventa A, Castel V, Matthay KK, for the INRG Task Force (2009) The International Neuroblastoma Risk Group (INRG) Classification System. J Clin Oncol 27: 289-297
29. Combaret V, Favrot MC, Kremens B, Philip I, Bailly C, Fontaniere B, Gentilhomme O, Chauvin F, Zucker JM, Bernard JL, Philip T (1989) Immunological detection of neuroblastoma cells in bone marrow harvested for autologous transplantation. Br J Cancer 59: 844-847
30. Corrias MV, Dallorso S, Kagedal B, Soler S, Swerts K, Tchirkov A, Vicha A, Viprey V, Ladenstein R, Burchill S (2008) TR110 high frequency of minimal disease detected in bone marrow and peripheral blood from children with high risk neuroblastoma by QRT-PCR. A SIOPEN study. Proceedings of the ANR 2008. www.anrmeeting.org Japan 2008
31. Corrias MV, Haupt R, Carlini B, Parodi S, Rivabella L, Garaventa A, Pistoia V, Dallorso S (2006) Peripheral blood stem cell tumor cell contamination and survival of neuroblastoma patients. Clin Cancer Res 12: 5680-5685
32. de Alava E, Lozano MD, Patino A, Sierrasesumaga L, Pardo-Mindan FJ (1998) Ewing family tumors: potential prognostic value of reverse-transcriptase polymerase chain reaction detection of minimal residual disease in peripheral blood samples. Diagn Mol Pathol 7: 152-157
33. Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369: 1742-1757
34. Faderl S, Talpaz M, Kantarjian HM, Estrov Z (1999) Should polymerase chain reaction analysis to detect minimal residual disease in patients with chronic myelogenous leukemia be used in clinical decision making? Blood 93: 2755-2759
35. Faulkner LB, Tintori V, Tamburini A, Paoli A, Garaventa A, Viscardi E, Tucci F, Lippi AA, De Bernadi B, Bernini G (1998) High-sensitivity immunocytologic analysis of neuroblastoma cells in paired blood and marrow samples. J Hematother 7: 361-366
36. Favrot MC, Frappaz D, Maritaz O, Phiip I, Fontaniere B, Gentilhomme O, Bailly C, Zucker JM, Gentet JC, Kemshead J, Philip T (1986) Histological, cytological and immunological analyses are complementary for the detection of neuroblastoma cells in bone marrow. Br J Cancer 54: 637-641
37. Foroni L, Harrison CJ, Hoffbrand AV, Potter MN (1999) Investigation of minimal residual disease in childhood and adult acute lymphoblastic leukaemia by molecular analysis. Br J Haematol 105: 7-24
38. Fukuda M, Miyajima Y, Miyashita Y, Horibe K (2001) Disease outcome may be predicted by molecular detection of minimal residual disease in bone marrow in advanced neuroblastoma: a pilot study. J Pediatr Hematol Oncol 23: 10-13
39. Gallego S, Llort A, Roma J, Sabado C, Gros L, de Toledo JS (2006) Detection of bone marrow micrometastasis and microcirculating disease in rhabdomyosarcoma by a real-time RT-PCR assay. J Cancer Res Clin Oncol 132: 356-362
40. Gilbert J, Norris MD, Marshall GM, Haber M (1997) Low specificity of PGP9.5 expression for detection of micrometastatic neuroblastoma. Br J Cancer 75: 1779-1781
41. Grau E, Oltra S, Mart́inez F, Orellana C, Cañete A, Fernández JM, Hernández-Mart́i M, Castel V (2009) MAGE-A1 expression is associated with good prognosis in neuroblastoma tumors. J Cancer Res Clin Oncol 135: 523-531
42. Gunn J, McCall JL, Yun K, Wright PA (1996) Detection of micrometastases in colorectal cancer patients by K19 and K20 reverse-transcription polymerase chain reaction. Lab Invest 75: 611-616
43. Gussetis ES, Ebener U, Wehner S, Kornhuber B (1989) Immunological detection and definition of minimal residual neuroblastoma disease in bone marrow samples obtained during or after therapy. Eur J Cancer Clin Oncol 25: 1745-1753
44. Hochhaus A, Weisser A, La Rosée P, Emig M, Müller MC, Saussele S, Reiter A, Kuhn C, Berger U, Hehlmann R, Cross NC (2000) Detection and quantification of residual disease in chronic myelogenous leukemia. Leukemia 14: 998-1005
45. Horibe K, Fukuda M, Miyajima Y, Matsumoto K, Kondon M, Inaba J, Miyashita Y (2001) Outcome prediction by molecular detection of minimal residual disease in bone marrow for advanced neuroblastoma. Med Pediatr Oncol 36: 203-204
46. Ito R, Asami S, Kagawa S, Motohashi S, Shichino H, Chin M, Yoshida Y, Nemoto N, Mugishima H, Suzuki T (2004) Usefulness of tyrosine hydroxylase mRNA for diagnosis and detection of minimal residual disease in neuroblastoma. Biol Pharm Bull 27: 315-318
47. Kramer K, Gerald WL, Kushner BH, Larson SM, Hameed M, Cheung NK (1998) Disialoganglioside GD2 loss following monoclonal antibody therapy is rare in neuroblastoma. Clin Cancer Res 4: 2135-2139
48. Kuroda T, Saeki M, Nakano M, Mizutani S (1997) Clinical application of minimal residual neuroblastoma cell detection by reverse transcriptase- polymerase chain reaction. J Pediatr Surg 32: 69-72
49. Ladisch S, Wu ZL, Feig S, Ulsh L, Schwartz E, Floutsis G, Wiley F, Lenarsky C, Seeger R (1987) Shedding of GD2 ganglioside by human neuroblas-toma. Int J Cancer 39: 73-76
50. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408
51. Maris JM, Hogarty MD, Bagatell R, Cohn SL (2007) Neuroblastoma. Lancet 369: 2106-2120
52. Medic S, Pearce RL, Heenan PJ, Ziman M (2007) Molecular markers of circulating melanoma cells. Pigment Cell Res 20: 80-91
53. Méhes G, Lörch T, Ambros PF (2000) Quantitative analysis of disseminated tumour cells in the bone marrow by automated fluorescence image analysis. Cytometry 42: 357-362
54. Méhes G, Luegmayr A, Hattinger CM, Lörch T, Ambros IM, Gadner H, Ambros PF (2001) Automatic detection and genetic profiling of disseminated neuroblastoma cells. Med Pediatr Oncol 36: 205-209
55. Miyajima Y, Horibe K, Fukuda M, Matsumoto K, Numata S, Mori H, Kato K (1996) Sequential detection of tumour cells in the peripheral blood and bone marrow of patients with stage IV neuroblastoma by the reverse transcription-polymerase chain reaction for tyrosine hydroxylase mRNA. Cancer 77: 1214-1219
56. Miyajima Y, Kato K, Numata S, Kudo K, Horibe K (1995) Detection of neuroblastoma cells in bone marrow and peripheral blood at diagnosis by the reverse transcriptase-polymerase chain reaction for tyrosine hydroxylase mRNA. Cancer 75: 2757-2761
57. Monclair T, Brodeur GM, Ambros PF, Brisse H, Cecchetto G, Holmes K, Kaneko M, London WB, Matthay KK, Nuchtern JG, Schweinitz DV, Simon T, Cohn SL, Pearson ADJ, for the INRG Task Force (2009) The International Neuroblastoma Risk Grouping (INRG) Staging System. J Clin Oncol 27: 298-303
58. Moss TJ, Reynolds CP, Sather HN, Romansky SG, Hammond D, Seeger RC (1991) Prognostic value of immunocytologic detection of bone marrow metastases in neuroblastoma. N Engl J Med 324: 219-226
59. Mujoo K, Cheresh DA, Rosenberg J, Hirschowitz L, Reisfeld RA (1987) Disialoganglioside GD2 on human neuroblastoma cells: target antigen for monoclonal antibody-mediated cytolysis and suppression of tumour growth. Cancer Res 47: 1098-1104
60. O'Driscoll L (2007) Extracellular nucleic acids and their potential as diagnostic, prognostic and predictive biomarkers. Anticancer Res 27: 1257-1265
61. Ootsuka S, Asami S, Sasaki T, Yoshida Y, Nemoto N, Shichino H, Chin M, Mugishima H, Suzuki T (2008) Useful markers for detecting minimal residual disease in cases of neuroblastoma. Biol Pharm Bull 31: 1071-1074
62. Riley RD, Burchill SA, Abrams KR, Heney D, Sutton AJ, Jones DR, Lambert PC, Young B, Wailoo AJ, Lewis IJ (2003) A systematic review of molecular and biological tumour markers in neuroblastoma. Clin Cancer Res 10: 4-12
63. Roman J, Alvarez MA, Torres A (2000) Molecular basis for therapeutic decisions in chronic myeloid leukemia patients after allogeneic bone marrow transplantation. Haematologica 85: 1072-1082
64. Schleiermacher G, Peter M, Oberlin O, Philip T, Rubie H, Mechinaud F (2003) Increased risk of systemic relapses associated with bone marrow micrometastasis and circulating tumor cells in localized Ewing tumor. J Clin Oncol 21: 85-91
65. Schulz G, Cheresh DA, Varki NM, Yu A, Staffileno LK, Reisfeld RA (1984) Detection of ganglioside GD2 in tumour tissues and sera of neuro-blastoma patients. Cancer Res 44: 5914-5920
66. Schumacher-Kuckelkorn R, Hero B, Ernestus K, Berthold F (2005) Lacking immunocytological GD2 expression in neuroblastoma: report of three cases. Pediatr Blood Cancer 45: 195-202
67. Seeger RC, Reynolds CP, Gallego R, Stram DO, Gerbing RB, Matthay KK (2000) Quantitative tumour cell content of bone marrow and blood as a predictor of outcome in stage IV neuroblastoma: a Children's Cancer Group Study. J Clin Oncol 18: 4067-4076
68. Shochat SJ, Abt AB, Schengrund CL (1988) VCN-releasable sialic acid and gangliosides in human neuroblastomas. J Pediatr Surg 12: 413-418
69. Shono K, Tajiri T, Fujii Y, Suita S (2000) Clinical implications of minimal disease in the bone marrow and peripheral blood in neuroblastoma. J Pediatr Surg 35: 1415-1420
70. Sugimoto T, Sawada T, Matsumura T, Kemshead JT, Horii Y, Saida T, Imashuku S, Takeuchi Y (1988) Diagnosis of neuroblastoma metastasis in bone marrow with a panel of monoclonal antibodies. Med Pediatr Oncol 16: 190-196
71. Swerts K, Ambros PF, Brouzes C, Navarro JM, Gross N, Rampling D, Schumacher-Kuckelkorn R, Sementa AR, Ladenstein R, Beiske K (2005) Standardization of the immunocytochemical detection of neuroblastoma cells in bone marrow. J Histochem Cytochem 53: 1433-1440
72. Swerts K, De Moerloose B, Dhooge C, Vandesompele J, Hoyoux C, Beiske K, Benoit Y, Laureys G, Philippé J (2006) Potential application of ELAVL4 real-time quantitative reverse transcription-PCR for detection of disseminated neuroblastoma cells. Clin Chem 52: 438-445
73. Swerts K, Moerloose BD, Dhooge C, Brichard B, Benoit Y, Laureys G, Philippé J (2004) Detection of residual neuroblastoma cells in bone marrow: comparison of flow cytometry with immunocytochemistry. Cytometry 61: 9-19
74. Taback B, Hoon DS (2004) Circulating nucleic acids in plasma and serum: past, present and future. Curr Opin Mol Ther 6: 273-278
75. Tchirkov A, Paillard C, Halle P, Bernard F, Bordigoni P, Vago P, Deméocq F, Kanold J (2003) Significance of molecular quantification of minimal residual disease in metastatic neuroblastoma. J Hematother Stem Cell Res 12: 435-442
76. Thomson B, Hawkins D, Felgenhauer J, Radich J (1999) RT-PCR evaluation of peripheral blood, bone marrow and peripheral blood stem cells in children and adolescents undergoing VACIME chemotherapy for Ewing's sarcoma and alveolar rhabdomyosarcoma. Bone Marrow Transplant 24: 527-533
77. Trager C, Kogner P, Lindskog M, Ponthan F, Kullman A, Kagedal B (2003) Quantitative analysis of tyrosine hydroxylase mRNA for sensitive detection of neuroblastoma cells in blood and bone marrow. Clin Chem 49: 104-112
78. Träger C, Vernby A, Kullman A, Ora I, Kogner P, Kågedal B (2008) mRNAs of tyrosine hydroxylase and dopa decarboxylase but not of GD2 synthase are specific for neuroblastoma minimal disease and predicts outcome for children with high-risk disease when measured at diagnosis. Int J Cancer 123: 2849-2855
79. Viprey VF, Corrias MV, Kagedal B, Oltra S, Swerts K, Vicha A, Ladenstein R, Burchill SA (2007) Standardisation of operating procedures for detection of minimal disease by QRT-PCR in children with neuroblas-toma: quality assurance on behalf of SIOPEN-R-NET. Eur J Cancer 43: 341-350
80. Viprey VF, Lastowska MA, Corrias MV, Swerts K, Jackson MS, Burchill SA (2008) Minimal disease monitoring by QRT-PCR: guidelines for identification and systematic validation of molecular markers prior to evaluation in prospective clinical trials. J Pathol 216: 245-252
81. Wagner LM, Burger RA, Guichard SM, Raimondi SC, Santana VM, Furman WL, Barnette P, Danks MK (2006) Pilot study to evaluate MYCN expression as a neuroblastoma cell marker to detect minimal residual disease by RT-PCR. J Pediatr Hematol Oncol 28: 635-641
82. Warzynski MJ, Graham DM, Axtell RA, Higgins JV, Hammers Ya (2002) Flow cytometric immunophenotyping test for staging/monitoring neuroblastoma patients. Cytometry 50: 298-304
83. Zeerleder S (2006) The struggle to detect circulating DNA. Crit Care 10: 142
84. Zoubek A, Ladenstein R, Windhager R, Amann G, Fischmeister G, Kager L, Jugovic D, Ambros PF, Gadner H, Kovar H (1998) Predictive potential of testing for bone marrow involvement in Ewing tumor patients by RT-PCR: a preliminary evaluation. Int J Cancer 79: 56-60