Ki-67 is a valuable prognostic predictor of lymphoma but its utility varies in lymphoma subtypes: Evidence from a systematic meta-analysis

BMC Cancer

Volumn 14, Issue 1, 2014, Pages

  He, Xin ^a   Chen, Zhigang ^a   Fu, Tao ^a   Jin, Xueli ^a   Yu, Teng ^a   Liang, Yun ^a   Zhao, Xiaoying ^a   Huang, Liansheng ^a  

^a THE SECOND AFFILIATED HOSPITAL OF ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Ki 67; Lymphoma; Meta analysis; Prognostic value

Indexed keywords

BLEOMYCIN; CHLORAMBUCIL; CHLORMETHINE; CYCLOPHOSPHAMIDE; DACARBAZINE; DOXORUBICIN; ETOPOSIDE; KI 67 ANTIGEN; METHOTREXATE; MITOXANTRONE; MONOCLONAL ANTIBODY; NUCLEAR PROTEIN; PREDNISONE; PROCARBAZINE; RITUXIMAB; VINBLASTINE; VINCRISTINE; ANTINEOPLASTIC AGENT; TUMOR MARKER; LACTATE DEHYDROGENASE;

ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CELL PROLIFERATION; CLINICAL DECISION MAKING; CLINICAL FEATURE; DISEASE FREE SURVIVAL; HODGKIN DISEASE; HUMAN; LARGE CELL LYMPHOMA; LYMPHOMA; MANTLE CELL LYMPHOMA; META ANALYSIS; NONHODGKIN LYMPHOMA; OVERALL SURVIVAL; PREDICTION; PROTEIN EXPRESSION; SCORING SYSTEM; SYSTEMATIC REVIEW; GENE EXPRESSION; GENETICS; METABOLISM; MORTALITY; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; PUBLISHING; RISK; ANTIGEN EXPRESSION; CANCER CLASSIFICATION; CANCER STAGING; FUNCTIONAL STATUS; INTERNATIONAL PROGNOSTIC INDEX; NK T CELL LYMPHOMA; RISK ASSESSMENT; TUMOR LOCALIZATION;

ANTIBODIES, MONOCLONAL, MURINE-DERIVED; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; GENE EXPRESSION; HUMANS; KI-67 ANTIGEN; LYMPHOMA; ODDS RATIO; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; PUBLICATION BIAS; TUMOR MARKERS, BIOLOGICAL;

EID: 84899474728     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-14-153     Document Type: Article

References (45)

1. A clinical evaluation of the International Lymphoma Study Group classification of non-Hodgkin's lymphoma. The Non-Hodgkin's Lymphoma Classification Project. Blood 1997, 89(11):3909-3918.
2. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012, 62(1):10-29. 10.3322/caac.20138, 22237781.
3. Sattar T, Griffeth LK, Latifi HR, Glass J, Munker R, Lilien DL. PET imaging today: contribution to the initial staging and prognosis of patients with non-Hodgkin's lymphomas. J La State Med Soc 2006, 158(4):193-201.
4. Schluter C, Duchrow M, Wohlenberg C, Becker MH, Key G, Flad HD, Gerdes J. The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 1993, 123(3):513-522. 10.1083/jcb.123.3.513, 2200129, 8227122.
5. Li S, Feng X, Li T, Zhang S, Zuo Z, Lin P, Konoplev S, Bueso-Ramos CE, Vega F, Medeiros LJ, Yin CC. Extranodal NK/T-cell lymphoma, nasal type: a report of 73 cases at MD Anderson Cancer Center. Am J Surg Pathol 2013, 37(1):14-23. 10.1097/PAS.0b013e31826731b5, 23232851.
6. Geisler CH, Kolstad A, Laurell A, Jerkeman M, Raty R, Andersen NS, Pedersen LB, Eriksson M, Nordstrom M, Kimby E, Bentzen H, Kuittinen O, Lauritzsen GF, Nilsson-Ehle H, Ralfkiaer E, Ehinger M, Sundstrom C, Delabie J, Karjalainen-Lindsberg ML, Brown P, Elonen E. Nordic MCL2 trial update: six-year follow-up after intensive immunochemotherapy for untreated mantle cell lymphoma followed by BEAM or BEAC + autologous stem-cell support: still very long survival but late relapses do occur. Br J Haematol 2012, 158(3):355-362. 10.1111/j.1365-2141.2012.09174.x, 22640180.
7. Li ZM, Huang JJ, Xia Y, Zhu YJ, Zhao W, Wei WX, Jiang WQ, Lin TY, Huang HQ, Guan ZZ. High Ki-67 expression in diffuse large B-cell lymphoma patients with non-germinal center subtype indicates limited survival benefit from R-CHOP therapy. Eur J Haematol 2012, 88(6):510-517. 10.1111/j.1600-0609.2012.01778.x, 22413767.
8. Goy A, Bernstein SH, McDonald A, Pickard MD, Shi H, Fleming MD, Bryant B, Trepicchio W, Fisher RI, Boral AL, Mulligan G. Potential biomarkers of bortezomib activity in mantle cell lymphoma from the phase 2 PINNACLE trial. Leuk Lymphoma 2010, 51(7):1269-1277. 10.3109/10428194.2010.483302, 20572799.
9. Jerkeman M, Anderson H, Dictor M, Kvaloy S, Akerman M, Cavallin-Stahl E. Assessment of biological prognostic factors provides clinically relevant information in patients with diffuse large B-cell lymphoma-a Nordic Lymphoma Group study. Ann Hematol 2004, 83(7):414-419. 10.1007/s00277-004-0855-x, 15085385.
10. Hasselblom S, Ridell B, Sigurdardottir M, Hansson U, Nilsson-Ehle H, Andersson PO. Low rather than high Ki-67 protein expression is an adverse prognostic factor in diffuse large B-cell lymphoma. Leuk Lymphoma 2008, 49(8):1501-1509. 10.1080/10428190802140055, 18766962.
11. Sehn LH, Berry B, Chhanabhai M, Fitzgerald C, Gill K, Hoskins P, Klasa R, Savage KJ, Shenkier T, Sutherland J, Gascoyne RD, Connors JM. The revised International Prognostic Index (R-IPI) is a better predictor of outcome than the standard IPI for patients with diffuse large B-cell lymphoma treated with R-CHOP. Blood 2007, 109(5):1857-1861. 10.1182/blood-2006-08-038257, 17105812.
12. Pfreundschuh M, Ho AD, Cavallin-Stahl E, Wolf M, Pettengell R, Vasova I, Belch A, Walewski J, Zinzani PL, Mingrone W, Kvaloy S, Shpilberg O, Jaeger U, Hansen M, Corrado C, Scheliga A, Loeffler M, Kuhnt E. Prognostic significance of maximum tumour (bulk) diameter in young patients with good-prognosis diffuse large-B-cell lymphoma treated with CHOP-like chemotherapy with or without rituximab: an exploratory analysis of the MabThera International Trial Group (MInT) study. Lancet Oncol 2008, 9(5):435-444. 10.1016/S1470-2045(08)70078-0, 18400558.
13. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 2009, 62(10):1006-1012. 10.1016/j.jclinepi.2009.06.005, 19631508.
14. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 2010, 25(9):603-605. 10.1007/s10654-010-9491-z, 20652370.
15. Parmar MK, Torri V, Stewart L. Extracting summary statistics to perform meta-analyses of the published literature for survival endpoints. Stat Med 1998, 17(24):2815-2834. 10.1002/(SICI)1097-0258(19981230)17:24<2815::AID-SIM110>3.0.CO;2-8, 9921604.
16. Handoll HH. Systematic reviews on rehabilitation interventions. Arch Phys Med Rehabil 2006, 87(6):875. 10.1016/j.apmr.2006.04.006, 16731227.
17. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003, 327(7414):557-560. 10.1136/bmj.327.7414.557, 192859, 12958120.
18. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959, 22(4):719-748.
19. Salles G, de Jong D, Xie W, Rosenwald A, Chhanabhai M, Gaulard P, Klapper W, Calaminici M, Sander B, Thorns C, Campo E, Molina T, Lee A, Pfreundschuh M, Horning S, Lister A, Sehn LH, Raemaekers J, Hagenbeek A, Gascoyne RD, Weller E. Prognostic significance of immunohistochemical biomarkers in diffuse large B-cell lymphoma: a study from the Lunenburg Lymphoma Biomarker Consortium. Blood 2011, 117(26):7070-7078. 10.1182/blood-2011-04-345256, 21536860.
20. Gaudio F, Giordano A, Perrone T, Pastore D, Curci P, Delia M, Napoli A, De' Risi C, Spina A, Ricco R, Liso V, Specchia G. High Ki67 index and bulky disease remain significant adverse prognostic factors in patients with diffuse large B cell lymphoma before and after the introduction of rituximab. Acta Haematol 2011, 126(1):44-51. 10.1159/000324206, 21430371.
21. Song MK, Chung JS, Joo YD, Lee SM, Oh SY, Shin DH, Yun EY, Kim SG, Seol YM, Shin HJ, Choi YJ, Cho GJ. Clinical importance of Bcl-6-positive non-deep-site involvement in non-HIV-related primary central nervous system diffuse large B-cell lymphoma. J Neurooncol 2011, 104(3):825-831. 10.1007/s11060-011-0555-z, 21380743.
22. Ott G, Ziepert M, Klapper W, Horn H, Szczepanowski M, Bernd HW, Thorns C, Feller AC, Lenze D, Hummel M, Stein H, Muller-Hermelink HK, Frank M, Hansmann ML, Barth TF, Moller P, Cogliatti S, Pfreundschuh M, Schmitz N, Trumper L, Loeffler M, Rosenwald A. Immunoblastic morphology but not the immunohistochemical GCB/nonGCB classifier predicts outcome in diffuse large B-cell lymphoma in the RICOVER-60 trial of the DSHNHL. Blood 2010, 116(23):4916-4925. 10.1182/blood-2010-03-276766, 20736456.
23. Barros MH, Scheliga A, De Matteo E, Minnicelli C, Soares FA, Zalcberg IR, Hassan R. Cell cycle characteristics and Epstein-Barr virus are differentially associated with aggressive and non-aggressive subsets of Hodgkin lymphoma in pediatric patients. Leuk Lymphoma 2010, 51(8):1513-1522. 10.3109/10428194.2010.489243, 20687799.
24. Yoon DH, Choi DR, Ahn HJ, Kim S, Lee DH, Kim SW, Park BH, Yoon SO, Huh J, Lee SW, Suh C. Ki-67 expression as a prognostic factor in diffuse large B-cell lymphoma patients treated with rituximab plus CHOP. Eur J Haematol 2010, 85(2):149-157.
25. Chung R, Peters AC, Armanious H, Anand M, Gelebart P, Lai R. Biological and clinical significance of GSK-3beta in mantle cell lymphoma-an immunohistochemical study. Int J Clin Exp Pathol 2010, 3(3):244-253. 2836502, 20224723.
26. Garcia M, Romaguera JE, Inamdar KV, Rassidakis GZ, Medeiros LJ. Proliferation predicts failure-free survival in mantle cell lymphoma patients treated with rituximab plus hyperfractionated cyclophosphamide, vincristine, doxorubicin, and dexamethasone alternating with rituximab plus high-dose methotrexate and cytarabine. Cancer 2009, 115(5):1041-1048. 10.1002/cncr.24141, 19170236.
27. Hsi ED, Jung SH, Lai R, Johnson JL, Cook JR, Jones D, Devos S, Cheson BD, Damon LE, Said J. Ki67 and PIM1 expression predict outcome in mantle cell lymphoma treated with high dose therapy, stem cell transplantation and rituximab: a Cancer and Leukemia Group B 59909 correlative science study. Leuk Lymphoma 2008, 49(11):2081-2090. 10.1080/10428190802419640, 19021050.
28. Szczuraszek K, Mazur G, Jelen M, Dziegiel P, Surowiak P, Zabel M. Prognostic significance of Ki-67 antigen expression in non-Hodgkin's lymphomas. Anticancer Res 2008, 28(2A):1113-1118.
29. Determann O, Hoster E, Ott G, Wolfram Bernd H, Loddenkemper C, Leo Hansmann M, Barth TE, Unterhalt M, Hiddemann W, Dreyling M, Klapper W. Ki-67 predicts outcome in advanced-stage mantle cell lymphoma patients treated with anti-CD20 immunochemotherapy: results from randomized trials of the European MCL Network and the German Low Grade Lymphoma Study Group. Blood 2008, 111(4):2385-2387. 10.1182/blood-2007-10-117010, 18077791.
30. Kim SJ, Kim BS, Choi CW, Choi J, Kim I, Lee YH, Kim JS. Ki-67 expression is predictive of prognosis in patients with stage I/II extranodal NK/T-cell lymphoma, nasal type. Ann Oncol 2007, 18(8):1382-1387. 10.1093/annonc/mdm183, 17693651.
31. Bahnassy AA, Zekri AR, Asaad N, El-Houssini S, Khalid HM, Sedky LM, Mokhtar NM. Epstein-Barr viral infection in extranodal lymphoma of the head and neck: correlation with prognosis and response to treatment. Histopathology 2006, 48(5):516-528. 10.1111/j.1365-2559.2006.02377.x, 16623777.
32. Martinez A, Bellosillo B, Bosch F, Ferrer A, Marce S, Villamor N, Ott G, Montserrat E, Campo E, Colomer D. Nuclear survivin expression in mantle cell lymphoma is associated with cell proliferation and survival. Am J Pathol 2004, 164(2):501-510. 10.1016/S0002-9440(10)63140-9, 1602245, 14742256.
33. Seki R, Okamura T, Koga H, Yakushiji K, Hashiguchi M, Yoshimoto K, Ogata H, Imamura R, Nakashima Y, Kage M, Ueno T, Sata M. Prognostic significance of the F-box protein Skp2 expression in diffuse large B-cell lymphoma. Am J Hematol 2003, 73(4):230-235. 10.1002/ajh.10379, 12879424.
34. Provencio M, Corbacho C, Salas C, Millan I, Espana P, Bonilla F, Ramon Cajal S. The topoisomerase IIalpha expression correlates with survival in patients with advanced Hodgkin's lymphoma. Clin Cancer Res 2003, 9(4):1406-1411.
35. Raty R, Franssila K, Joensuu H, Teerenhovi L, Elonen E. Ki-67 expression level, histological subtype, and the International Prognostic Index as outcome predictors in mantle cell lymphoma. Eur J Haematol 2002, 69(1):11-20. 10.1034/j.1600-0609.2002.01677.x, 12270057.
36. Sanchez E, Chacon I, Plaza MM, Munoz E, Cruz MA, Martinez B, Lopez L, Martinez-Montero JC, Orradre JL, Saez AI, Garcia JF, Piris MA. Clinical outcome in diffuse large B-cell lymphoma is dependent on the relationship between different cell-cycle regulator proteins. J Clin Oncol 1998, 16(5):1931-1939.
37. Morente MM, Piris MA, Abraira V, Acevedo A, Aguilera B, Bellas C, Fraga M, Garcia-Del-Moral R, Gomez-Marcos F, Menarguez J, Oliva H, Sanchez-Beato M, Montalban C. Adverse clinical outcome in Hodgkin's disease is associated with loss of retinoblastoma protein expression, high Ki67 proliferation index, and absence of Epstein-Barr virus-latent membrane protein 1 expression. Blood 1997, 90(6):2429-2436.
38. Miller TP, Grogan TM, Dahlberg S, Spier CM, Braziel RM, Banks PM, Foucar K, Kjeldsberg CR, Levy N, Nathwani BN. Prognostic significance of the Ki-67-associated proliferative antigen in aggressive non-Hodgkin's lymphomas: a prospective Southwest Oncology Group trial. Blood 1994, 83(6):1460-1466.
39. Slymen DJ, Miller TP, Lippman SM, Spier CM, Kerrigan DP, Rybski JA, Rangel CS, Richter LC, Grogan TM. Immunobiologic factors predictive of clinical outcome in diffuse large-cell lymphoma. J Clin Oncol 1990, 8(6):986-993.
40. Salek D, Vesela P, Boudova L, Janikova A, Klener P, Vokurka S, Jankovska M, Pytlik R, Belada D, Pirnos J, Moulis M, Kodet R, Michal M, Janousova E, Muzik J, Mayer J, Trneny M. Retrospective analysis of 235 unselected patients with mantle cell lymphoma confirms prognostic relevance of Mantle Cell Lymphoma International Prognostic Index and Ki-67 in the era of rituximab: long-term data from the Czech Lymphoma Project Database. Leuk Lymphoma 2013,
41. Gerdes J, Li L, Schlueter C, Duchrow M, Wohlenberg C, Gerlach C, Stahmer I, Kloth S, Brandt E, Flad HD. Immunobiochemical and molecular biologic characterization of the cell proliferation-associated nuclear antigen that is defined by monoclonal antibody Ki-67. Am J Pathol 1991, 138(4):867-873. 1886092, 2012175.
42. Dziegiel P, Salwa-Zurawska W, Zurawski J, Wojnar A, Zabel M. Prognostic significance of augmented metallothionein (MT) expression correlated with Ki-67 antigen expression in selected soft tissue sarcomas. Histol Histopathol 2005, 20(1):83-89.
43. Urruticoechea A, Smith IE, Dowsett M. Proliferation marker Ki-67 in early breast cancer. J Clin Oncol 2005, 23(28):7212-7220. 10.1200/JCO.2005.07.501, 16192605.
44. Spyratos F, Ferrero-Pous M, Trassard M, Hacene K, Phillips E, Tubiana-Hulin M, Le Doussal V. Correlation between MIB-1 and other proliferation markers: clinical implications of the MIB-1 cutoff value. Cancer 2002, 94(8):2151-2159. 10.1002/cncr.10458, 12001111.
45. Wilson WH, Teruya-Feldstein J, Fest T, Harris C, Steinberg SM, Jaffe ES, Raffeld M. Relationship of p53, bcl-2, and tumor proliferation to clinical drug resistance in non-Hodgkin's lymphomas. Blood 1997, 89(2):601-609.