Risk for second malignancies in non-Hodgkin's lymphoma survivors: A meta-analysis

Annals of Oncology

Volumn 22, Issue 8, 2011, Pages 1845-1858

  Pirani, M ^a   Marcheselli, R ^a   Marcheselli, L ^a   Bari, A ^a   Federico, M ^a   Sacchi, S ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

Meta analysis; NHL; Relative risk; Secondary malignancies

Indexed keywords

CYCLOPHOSPHAMIDE; DOXORUBICIN; PREDNISONE; VINCRISTINE;

AGE; ARTICLE; CANCER RADIOTHERAPY; CANCER RISK; CANCER SURVIVOR; DISEASE ASSOCIATION; EMBASE; ENVIRONMENTAL EXPOSURE; GENETIC SUSCEPTIBILITY; HUMAN; MEDLINE; NONHODGKIN LYMPHOMA; PRIORITY JOURNAL; REGRESSION ANALYSIS; RISK ASSESSMENT; SECOND CANCER; SYSTEMATIC ERROR; SYSTEMATIC REVIEW; WHOLE BODY RADIATION;

EID: 79961006848     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdq697     Document Type: Article

References (94)

1. Fisher RI, LeBlanc M, Press OW et al. New treatment options have changed the survival of patients with follicular lymphoma. J Clin Oncol 2005; 23: 8447-8452.
2. Marcus R, Imrie K, Solal-Celigny P et al. Phase III study of R-CVP compared with cyclophosphamide, vincristine, and prednisone alone in patients with previously untreated advanced follicular lymphoma. J Clin Oncol 2008; 26: 4579-4586.
3. Sacchi S, Pozzi S, Marcheselli L et al. Introduction of rituximab in front-line and salvage therapies has improved outcome of advanced-stage follicular lymphoma patients. Cancer 2007; 109: 2077-2082.
4. Coiffier B, Lepage E, Briere J et al. CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. N Engl J Med 2002; 346: 235-242.
5. Habermann TM, Weller EA, Morrison VA et al. Rituximab-CHOP versus CHOP alone or with maintenance rituximab in older patients with diffuse large B-cell lymphoma. J Clin Oncol 2006; 24: 3121-3127.
6. Pfreundschuh M, Trumper L, Osterborg A et al. CHOP-like chemotherapy plus rituximab versus CHOP-like chemotherapy alone in young patients with good-prognosis diffuse large-B-cell lymphoma: a randomised controlled trial by the MabThera International Trial (MInT) Group. Lancet Oncol 2006; 7: 379-391.
7. Sehn LH, Donaldson J, Chhanabhai M et al. Introduction of combined CHOP plus rituximab therapy dramatically improved outcome of diffuse large B-cell lymphoma in British Columbia. J Clin Oncol 2005; 23: 5027-5033.
8. Fu K, Weisenburger DD, Choi WW et al. Addition of rituximab to standard chemotherapy improves the survival of both the germinal center B-cell-like and non-germinal center B-cell-like subtypes of diffuse large B-cell lymphoma. J Clin Oncol 2008; 26: 4587-4594.
9. Philip T, Guglielmi C, Hagenbeek A et al. Autologous bone marrow transplantation as compared to salvage chemotherapy in relapses of chemotherapy sensitive non-Hodgkin's lymphoma. N Engl J Med 1995; 333: 1540-1545.
10. Bierman PJ, Vose JM, Anderson JR et al. High-dose therapy with autologous hematopoietic rescue for follicular low-grade non-Hodgkin's lymphoma. J Clin Oncol 1997; 15: 445-450.
11. Apostolidis J, Gupta RK, Grenzelias D et al. High-dose therapy with autologous bone marrow support as consolidation of remission in follicular lymphoma: long term clinical and molecular follow up. J Clin Oncol 2000; 18: 527-536.
12. Haioun C, Lepage E, Gisselbrecht C et al. Benefit of autologous bone marrow transplantation over sequential chemotherapy in poor-risk aggressive non-Hodgkin's lymphoma: updated results of the prospective study LNH87-2. Groupe d'Etude des Lymphomes de l'Adulte. J Clin Oncol 1997; 15: 1131-1137.
13. Pedersen-Bjergaard J, Ersboll J, Sorensen HM et al. Risk of acute nonlymphocytic leukaemia and preleukemia in patients treated with cyclophosphamide for non-Hodgkin's lymphomas: comparison with results obtained in patients treated for Hodgkin's disease and ovarian carcinoma with other alkylating agents. Ann Intern Med 1985; 103: 195-200.
14. Pedersen-Bjergaard J, Ersboll J, Hansen VL et al. Carcinoma of the urinary bladder after treatment with cyclophosphamide for non-Hodgkin's lymphoma. N Engl J Med 1988; 318: 1028-1032.
15. Travis LB, Curtis RE, Boice JD Jr et al. Second cancers following non-Hodgkin's lymphoma. Cancer 1991; 67: 2002-2009.
16. Travis LB, Curtis RE, Glimelius B et al. Bladder and kidney cancer following cyclophosphamide therapy for non-Hodgkin's lymphoma. J Natl Cancer Inst 1995; 87: 524-530.
17. André M, Mounier N, Leleu X et al. Second cancers and late toxicities after treatment of aggressive non-Hodgkin lymphoma with the ACVBP regimen: a GELA cohort study on 2837 patients. Blood 2004; 103: 1222-1228.
18. Mudie NY, Swerdlow AJ, Higgins CD et al. Risk of second malignancy after non-Hodgkin's lymphoma: a British Cohort Study. J Clin Oncol 2006; 24: 1568-1574.
19. Tward JD, Wendland MM, Shrieve DC et al. The risk of secondary malignancies over 30 years after the treatment of non-Hodgkin lymphoma. Cancer 2006; 107: 108-115.
20. Teta MJ, Lau E, Sceurman BK, Wagner ME. Therapeutic radiation for lymphoma: risk of malignant mesothelioma. Cancer 2007; 109: 1432-1438.
21. Bluhm EC, Ronckers C, Hayashi R et al. Cause-specific mortality and second cancer incidence after non-Hodgkin lymphoma: a report from the Childhood Cancer Survivor Study. Blood 2008; 111: 4014-4021.
22. Greene MH, Young RC, Merrill JM, DeVita VT. Evidence of a treatment dose response in acute nonlymphocytic leukemias which occur after therapy of non-Hodgkin's lymphoma. Cancer Res 1983; 43: 1891-1898.
23. Travis LB, Weeks J, Curtis RE et al. Leukemia following low-dose total body irradiation and chemotherapy for non-Hodgkin's lymphoma. J Clin Oncol 1996; 14: 565-571.
24. Darrington DL, Vose JM, Anderson JR et al. Incidence and characterization of secondary myelodysplastic syndrome and acute myelogenous leukemia following high-dose chemoradiotherapy and autologous stem-cell transplantation for lymphoid malignancies. J Clin Oncol 1994; 12: 2527-2534.
25. Stone RM, Neuberg D, Soiffer R et al. Myelodysplastic syndrome as a late complication following autologous bone marrow transplantation for non-Hodgkin's lymphoma. J Clin Oncol 1994; 12: 2535-2542.
26. Pedersen-Bjergaard J, Pedersen M, Myhre J, Geisler C. High risk of therapy-related leukemia after BEAM chemotherapy and autologous stem cell transplantation for previously treated lymphomas is mainly related to primary chemotherapy and not to the BEAM-transplantation procedure. Leukemia 1997; 11: 1654-1660.
27. Brown JR, Yeckes H, Friedberg JW et al. Increasing incidence of late second malignancies after conditioning with cyclophosphamide and total body irradiation and autologous bone marrow transplantation for non-Hodgkin's lymphoma. J Clin Oncol 2005; 23: 2208-2214.
28. Zarrabi MH. Association of non-Hodgkin's lymphoma (NHL) and second neoplasms. Semin Oncol 1980; 17: 340-351.
29. Ellis M, Lishner M. Second malignancies following treatment in non-Hodgkin's lymphoma. Leuk Lymphoma 1993; 9: 337-342.
30. Dores GM, Miller ME, Schwartz S, Benditt JO. Review of Hodgkin's disease and lung cancer following non-Hodgkin's lymphoma in Rhode Island and review of the literature. R I Med 1995; 78: 317-319.
31. Epelbaum R. Non-Hodgkin's lymphoma: long-term survivors and adverse effects. Ann Oncol 2000; 11 (Suppl 3): 123-128.
32. Armitage JO, Carbone PP, Connors JM et al. Treatment-related myelodysplasia and acute leukemia in non-Hodgkin's lymphoma patients. J Clin Oncol 2003; 21: 897-906.
33. Lens MB, Newton-Bishop JA. An association between cutaneous melanoma and non-Hodgkin's lymphoma: pooled analysis of published data with a review. Ann Oncol 2005; 16: 460-465.
34. Tward J, Glenn M, Pulsipher M et al. Incidence, risk factors, and pathogenesis of second malignancies in patients with non-Hodgkin lymphoma. Leuk Lymphoma 2007; 48: 1482-1495.
35. Ng AK, Travis LB. Second primary cancers: an overview. Hematol Oncol Clin North Am 2008; 22: 271-289.
36. Stroup DF, Berlin JA, Morton SC et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 2000; 283: 2008-2012.
37. Bonovas S, Filioussi K, Tsavaris N, Sitaras NM. Use of statins and breast cancer: a meta-analysis of seven randomized clinical trials and nine observational studies. J Clin Oncol 2005; 23: 8606-8612.
38. Jüni P, Witschi A, Bloch R, Egger M. The hazards of scoring the quality of clinical trials for meta-analysis. JAMA 1999; 282: 1054-1060.
39. Alder N, Fenty J, Warren F et al. Meta-analysis of mortality and cancer incidence among workers in the synthetic rubber-producing industry. Am J Epidemiol 2006; 164: 405-420.
40. Cochran WG. The combination of estimates from different experiments. Biometrics 1954; 10: 101-129.
41. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21: 1539-1558.
42. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ 2003; 327: 557-560.
43. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials 1986; 7: 177-188.
44. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 1959; 22: 719-748.
45. Higgins JPT, Green S. Cochrane Handbook for Systematic Reviews of Interventions, Section 9.5.4. Version 5.0.2 [updated September 2009]. The Cochrane Collaboration 2009; www.cochrane-handbook.org.
46. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 1994; 50: 1088-1101.
47. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629-634.
48. Tobias A. Assessing the influence of a single study in the meta-analysis estimate. Stata Tech Bull 1999; 8: 15-17.
49. Higgins JP, Thompson SG. Controlling the risk of spurious findings from meta-regression. Stat Med 2004; 23: 1663-1682.
50. Storm HH, Prener A. Second cancer following lymphatic and hematopoietic cancers in Denmark, 1943-80. Natl Cancer Inst Monogr 1985; 68: 389-409.
51. Kantor AF, Curtis RE, Vonderheid EC et al. Risk of second malignancy after cutaneous T-cell lymphoma. Cancer 1989; 63: 1612-1615.
52. Travis LB, Gonzalez CL, Hankey BF, Jaffe ES. Hodgkin's disease following non-Hodgkin's lymphoma. Cancer 1992; 69: 2337-2342.
53. Rabbani F, Russo P. Lack of association between renal cell carcinoma and non-Hodgkin's lymphoma. Urology 1999; 54: 28-33.
54. Cannon MJ, Flanders WD, Pellett PE. Occurrence of primary cancers in association with multiple myeloma and Kaposi's sarcoma in the United States, 1973-1995. Int J Cancer 2000; 85: 453-456.
55. Dong C, Hemminki K. Second primary neoplasms among 53159 haematolymphoproliferative malignancy patients in Sweden, 1958-1996: a search for common mechanisms. Br J Cancer 2001; 85: 997-1005.
56. Huang KP, Weinstock MA, Clarke CA et al. Lymphomas and other malignant neoplasms in patients with mycosis fungoides and Sezary syndrome: evidence from population-based and clinical cohorts. Arch Dermatol 2007; 143: 45-50.
57. Maule M, Scélo G, Pastore G et al. Risk of second malignant neoplasms after childhood central nervous system malignant tumours: an international study. Eur J Cancer 2008; 44: 830-839.
58. Inskip PD, Curtis RE. New malignancies following childhood cancer in the United States, 1973-2002. Int J Cancer 2007; 121: 2233-2240.
59. Travis LB, Curtis RE, Glimelius B et al. Second cancers among long-term survivors of non Hodgkin's lymphoma. J Natl Cancer Inst 1993; 85: 1932-1937.
60. Brennan P, Coates M, Armstrong B et al. Second primary neoplasms following non-Hodgkin's lymphoma in New South Wales, Australia. Br J Cancer 2000; 82: 1344-1347.
61. Väkevä L, Pukkala E, Ranki A. Increased risk of secondary cancers in patients with primary cutaneous T cell lymphoma. J Invest Dermatol 2000; 115: 62-65.
62. Teppo L, Pukkala E, Saxén E. Multiple cancer-an epidemiologic exercise in Finland. J Natl Cancer Inst 1985; 7: 207-217.
63. Hall P, Rosendahl I, Mattsson A, Einhorn S. Non-Hodgkin's lymphoma and skin malignancies-shared etiology? Int J Cancer 1995; 62: 519-522.
64. Adami J, Frisch M, Yuen J et al. Evidence of an association between non-Hodgkin's lymphoma and skin cancer. BMJ 1995; 310: 1491-1495.
65. Goggins WB, Finkelstein DM, Tsao H. Evidence for an association between cutaneous melanoma and non-Hodgkin lymphoma. Cancer 2001; 91: 874-880.
66. Hemminki K, Jiang Y, Steineck G. Skin cancer and non-Hodgkin's lymphoma as second malignancies: markers of impaired immune function? Eur J Cancer 2003; 39: 223-229.
67. McKenna DB, Stockton D, Brewster DH, Doherty VR. Evidence for an association between cutaneous malignant melanoma and lymphoid malignancy: a population-based retrospective cohort study in Scotland. Br J Cancer 2003; 88: 74-78.
68. Montalbàn C, Castrillo JM, López-Abente et al. Other cancers in patients with gastric MALT lymphoma. Leuk Lymphoma 1999; 33: 161-168.
69. Au WY, Gascoyne RD, Le N et al. Incidence of second neoplasms in patients with MALT lymphoma: no increase in risk above the background population. Ann Oncol 1999; 10: 317-321.
70. Amadori D, Ronconi S. Secondary lung tumors in hematological patients. Semin Respir Crit Care Med 2005; 26: 520-526.
71. Barista I, Cabanillas F, Romaguera JE et al. Is there an increased rate of additional malignancies in patients with mantle cell lymphoma? Ann Oncol 2002; 13: 318-322.
72. Moser EC, Noordijk EM, van Leeuwen FE et al. Risk of second cancer after treatment of aggressive non-Hodgkin's lymphoma; an EORTC cohort study. Haematologica 2006; 91: 1481-1488.
73. Sacchi S, Marcheselli L, Bari A et al. Secondary malignancies after treatment for indolent non-Hodgkin's lymphoma: a 16-year follow-up study. Haematologica 2008; 93: 398-404.
74. Sacchi S, Marcheselli L, Bari A et al. Second malignancies after treatment of diffuse large B-cell non-Hodgkin's lymphoma: a GISL cohort study. Haematologica. 2008; 93: 1335-1342.
75. Takenaka T, Konda C, Sakano T et al. Second primary malignancies in lymphoma patients. Jpn J Clin Oncol 1985; 15: 443-449.
76. Lavey RS, Eby NL, Prosnitz LR. Impact on second malignancy risk of the combined use of radiation and chemotherapy for lymphomas. Cancer 1990; 66: 80-88.
77. Lishner M, Slingerland J, Barr J et al. Second malignant neoplasms in patients with non-Hodgkin's lymphoma. Hematol Oncol 1991; 9: 169-179.
78. Tanaka H, Tsukuma H, Teshima H et al. Second primary cancers following non-Hodgkin's lymphoma in Japan: increased risk of hepatocellular carcinoma. Jpn J Cancer Res 1997; 88: 537-542.
79. Leung W, Sandlund JT, Hudson MM et al. Second malignancy after treatment of childhood non-Hodgkin lymphoma. Cancer 2001; 92: 1959-1966.
80. Guadagnolo BA, Li S, Neuberg D et al. Long-term outcome and mortality trends in early-stage, Grade 1-2 follicular lymphoma treated with radiation therapy. Int J Radiat Oncol Biol Phys 2006; 64: 928-934.
81. Iannitto E, Minardi V, Callea V et al. Assessment of the frequency of additional cancers in patients with splenic marginal zone lymphoma. Eur J Haematol 2006; 76: 134-140.
82. Arcaini L, Burcheri S, Rossi A et al. Risk of second cancer in nongastric marginal zone B-cell lymphomas of mucosa-associated lymphoid tissue: a population-based study from northern Italy. Clin Cancer Res 2007; 13: 182-186.
83. Greene MH, Wilson J. Second cancer following lymphatic and hematopoietic cancers in Connecticut, 1935-1982. Natl Cancer Inst Monogr 1985; 68: 191-217.
84. Brennan P, Scélo G, Hemminki K et al. Second primary cancers among 109 000 cases of non-Hodgkin's lymphoma. Br J Cancer 2005; 93: 159-166.
85. Hemminki K, Lenner P, Sundquist J, Bermejo JL. Risk of subsequent solid tumors after non-Hodgkin's lymphoma: effect of diagnostic age and time since diagnosis. J Clin Oncol 2008; 26: 1850-1857.
86. Levi F, Randimbison L, Te VC, La Vecchia C. Non-Hodgkin's lymphomas, chronic lymphocytic leukaemias and skin cancers. Br J Cancer 1996; 74: 1847-1850.
87. Dores GM, Coté TR, Travis LB. New malignancies following Hodgkin lymphoma, non-Hodgkin lymphoma and myeloma. In Curtis RE, Freedman DM, Ron E et al. (eds), New Malignancies among Cancer Survivors: SEER Cancer Registries, 1973-2000. Bethesda, MD: National Cancer Institute 2006; 397-428. NIH Publ. No. 05-5302.
88. Droitcour J, Silberman G, Chelimsky E. Cross-design synthesis: a new form of meta-analysis for combining results from randomized clinical trials and medical-practice databases. Int J Technol Assess Health Care 1993; 9: 440-449.
89. Allan JM, Travis LB. Mechanisms of therapy-related carcinogenesis. Nat Rev Cancer 2005; 5(12): 943-955.
90. Friedman DL, Kadan-Lottick NS, Whitton J et al. Increased risk of cancer among siblings of long-term childhood cancer survivors: a report from the childhood cancer survivor study. Cancer Epidemiol Biomarkers Prev 2005; 14: 1922-1927.
91. Landgren O, Pfeiffer RM, Stewart L et al. Risk of second malignant neoplasms among lymphoma patients with a family history of cancer. Int J Cancer 2007; 120: 1099-1102.
92. Travis LB, Gospodarowicz M, Curtis RE et al. Lung cancer following chemotherapy and radiotherapy for Hodgkin's disease. J Natl Cancer Inst 2002; 94: 182-192.
93. van Leeuwen FE, Klokman WJ, Stovall M et al. Roles of radiotherapy and smoking in lung cancer following Hodgkin's disease. J Natl Cancer Inst 1995; 87: 1530-1537.
94. Bhatia S, Sklar C. Second cancers in survivors of childhood cancer. Nat Rev Cancer 2002; 2: 124-132.