Efficacy of clodronate, pamidronate, and zoledronate in reducing morbidity and mortality in cancer patients with bone metastasis: A meta-analysis of randomized clinical trials

Clinical Therapeutics

Volumn 31, Issue 5, 2009, Pages 962-979

  Machado, Márcio ^a   Cruz, Lorena Souza ^b   Tannus, Gabriela ^c   Fonseca, Marcelo ^c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

bisphosphonates; meta analysis; mortality; skeletal related events

Indexed keywords

CALCIUM; CLODRONIC ACID; PAMIDRONIC ACID; PLACEBO; ZOLEDRONIC ACID;

BONE METASTASIS; BREAST CANCER; CANCER RADIOTHERAPY; CLINICAL TRIAL; COCHRANE LIBRARY; CONTROLLED CLINICAL TRIAL; DRUG EFFICACY; EMBASE; HEAD AND NECK CANCER; HUMAN; HYPERCALCEMIA; KIDNEY CANCER; LUNG NON SMALL CELL CANCER; LUNG SMALL CELL CANCER; MEDLINE; META ANALYSIS; MORBIDITY; MORTALITY; MULTIPLE CYCLE TREATMENT; MYELOMA; ORTHOPEDIC SURGERY; PATHOLOGIC FRACTURE; PROSTATE CANCER; QUALITY CONTROL; RANDOMIZED CONTROLLED TRIAL; REVIEW; SPINAL CORD COMPRESSION; THYROID CANCER;

ADULT; ANTINEOPLASTIC AGENTS; BONE DENSITY CONSERVATION AGENTS; BONE NEOPLASMS; CLODRONIC ACID; DIPHOSPHONATES; FEMALE; HUMANS; IMIDAZOLES; MALE; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK; SURVIVAL ANALYSIS; TREATMENT OUTCOME;

EID: 66949136282     PISSN: 01492918     EISSN: 1879114X     Source Type: Journal    
DOI: 10.1016/j.clinthera.2009.05.009     Document Type: Review

References (86)

1. Diel I.J., Kaufmann M., and Bastert G. Metastatic Bone Disease: Fundamental and Clinical Aspects (1994), Springer-Verlag, New York, NY 1-11
2. British Association of Surgical Oncology Guidelines. The management of metastatic bone disease in the United Kingdom. The Breast Specialty Group of the British Association of Surgical Oncology. Eur J Surg Oncol. 25 (1999) 3-23
3. Coleman R.E. Skeletal complications of malignancy. Cancer 80 Suppl (1997) 1588-1594
4. Greenlee R.T., Hill-Harmon M.B., Murray T., and Thun M. Cancer statistics, 2001 [published correction appears in CA Cancer J Clin. 2001;51:144]. CA Cancer J Clin. 51 (2001) 15-36
5. Coleman R.E. Metastatic bone disease: Clinical features, pathophysiology and treatment strategies. Cancer Treat Rev. 27 (2001) 165-176
6. Zekri J., Ahmed N., Coleman R.E., and Hancock B.W. The skeletal meta-static complications of renal cell carcinoma. Int J Oncol 19 (2001) 379-382
7. Donato J. Tumores ósseos. Metástase de carcinoma (2001), Rocca, Rio de Janeiro, Brazil 211-216
8. Healey J.H., and Brown H.K. Complications of bone metastases: Surgical management. Cancer 88 (2000) 2940-2951
9. Hungria V.T. Doença óssea em mieloma múltiplo. Rev Bras Hematol Hemoter 29 (2007) 60-66
10. Russell R.G., and Rogers M.J. Bisphosphonates: From the laboratory to the clinic and back again. Bone 25 (1999) 97-106
11. The Cochrane Collaboration. Review Manager (RevMan). http://www.cc-ims.net/revman Accessed January 1, 2009
12. Cochran W.G. The combination of estimates from different experiments. Biometrics 10 (1954) 101-129
13. Higgins J.P., Thompson S.G., Deeks J.J., and Altman D.G. Measuring inconsistency in meta-analyses. BMJ 327 (2003) 557-560
14. Begg C.B., and Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics 50 (1994) 1088-1101
15. Jadad A.R., Moore R.A., Carroll D., et al. Assessing the quality of reports of randomized clinical trials: Is blinding necessary?. Control Clin Trials 17 (1996) 1-12
16. Berenson J.R., Rosen L.S., Howell A., et al. Zoledronic acid reduces skeletalrelated events in patients with osteolytic metastases [published correction appears in Cancer. 2001;91:1956]. Cancer 91 (2001) 1191-1200
17. Cascinu S., Casadei V., Del Ferro E., et al. Pamidronate in patients with painful bone metastases, who failed initial treatment with hormones and/or chemotherapy. Support Care Cancer 4 (1996) 31-33
18. Clemons M.J., Dranitsaris G., Ooi W.S., et al. Phase II trial evaluating the palliative benefit of second-line zoledronic acid in breast cancer patients with either a skeletal-related event or progressive bone metastases despite first-line bisphospho-nate therapy. J Clin Oncol 30 (2006) 4895-4900
19. Coleman R.E., Houston S., Purohit O.P., et al. A randomised phase II study of oral pamidronate for the treatment of bone metastases from breast cancer. Eur J Cancer 34 (1998) 820-824
20. Glover D., Lipton A., Keller A., et al. Intravenous pamidronate disodium treatment of bone metastases in patients with breast cancer. A doseseeking study. Cancer 74 (1994) 2949-2955
21. Heindenreich A., Hofmann R., and Engelmann U.H. The use of biphos-phonate for the palliative treatment of painful bone metastasis due to hormone refractory prostate cancer. J Urol 165 (2001) 136-140
22. Ibrahim A., Scher N., Williams G., et al. Approval summary for zoledronic acid for treatment of multiple myeloma and cancer bone metastases. Clin Cancer Res 9 (2003) 2394-2399
23. Lipton A. Bisphosphonates and metastatic breast carcinoma. Cancer 97 Suppl (2002) 848-853
24. Rosen L.S., Gordon D., Kaminski M., et al. Zoledronic acid versus pamid-ronate in the treatment of skeletal metastases in patients with breast cancer or osteolytic lesions of multiple myeloma: A phase III, doubleblind, comparative trial. Cancer J 7 (2001) 377-387
25. van Holten-Verzantvoort A.T., Kroon H.M., Bijvoet O.L., et al. Palliative pamidronate treatment in patients with bone metastases from breast cancer. J Clin Oncol 11 (1993) 491-498
26. Diel I.J., Jaschke A., Solomayer E.F., et al. Adjuvant oral clodronate improves the overall survival of primary breast cancer patients with micrometastases to the bone marrow: A long-term follow-up. Ann Oncol 19 (2008) 2007-2011
27. Adami S., and Mian M. Clodronate therapy of metastatic bone disease in patients with prostatic carcinoma. Recent Results Cancer Res. 116 (1989) 65-72
28. Chern B., Joseph D., Joshua D., et al. Bisphosphonate infusion: Patient preference, safety and clinic use. Support Care Cancer 12 (2004) 463-466
29. Jagdev S.P., Purohit P., Heatley S., et al. Comparison of the effects of intravenous pamidronate and oral clodronate on symptoms and bone resorption in patients with meta-static bone disease. Ann Oncol 12 (2001) 1433-1438
30. Kylmälä T., Tammela T., Risteli L., et al. Evaluation of the effect of oral clodronate on skeletal metastases with type 1 collagen metabolites. A controlled trial of the Finnish Prostate Cancer Group. Eur J Cancer 29A (1993) 821-825
31. O'Rourke N., McCloskey E., Houghton F., et al. Double-blind, placebo-controlled, dose-response trial of oral clodronate in patients with bone metastases. J Clin Oncol 13 (1995) 929-934
32. Robertson A.G., Reed N.S., and Ralston S.H. Effect of oral clodronate on metastatic bone pain: A doubleblind, placebo-controlled study. J Clin Oncol 13 (1995) 2427-2430
33. Saarto T., Vehmanen L., Virkkunen P., and Blomqvist C. Ten-year follow-up of a randomized controlled trial of adjuvant clodronate treatment in node-positive breast cancer patients. Acta Oncol 43 (2004) 650-656
34. Delmas P.D., Charhon S., Chapuy M.C., et al. Long-term effects of dichloromethylene diphosphonate (CI2MDP) on skeletal lesions in multiple myeloma. Metab Bone Dis Relat Res 4 (1982) 163-168
35. Terpos E., Palermos J., Tsionos K., et al. Effect of pamidronate administration on markers of bone turnover and disease activity in multiple myeloma. Eur J Haematol 65 (2000) 331-336
36. Tyrrell C.T., Bruning P.F., May-Levin F., et al. Pamidronate infusions as single-agent therapy for bone metastases: A phase II trial in patients with breast cancer. Eur J Cancer 31A (1995) 1976-1980
37. Coleman R.E. Efficacy of zoledronic acid and pamidronate in breast cancer patients: A comparative analysis of randomized phase III trials. J Clin Oncol 25 Suppl 1 (2002) S25-S31
38. Harvey H.A., and Lipton A. The role of bisphosphonates in the treatment of bone metastases-the U.S. experience. Support Care Cancer 4 (1996) 213-217
39. Li E.C., and Davis L.E. Zoledronic acid: A new parenteral bisphosphonate. Clin Ther. 25 (2003) 2669-2708
40. Lipton A., Theriault R.L., Hortobagyi G.N., et al. Pamidronate prevents skeletal complications and is effective palliative treatment in women with breast carcinoma and osteo-lytic bone metastases: Long term follow-up of two randomized, placebo-controlled trials. Cancer 88 (2000) 1082-1090
41. Pavlakis N., Schmidt R., and Stockler M. . Bisphosphonates for breast cancer. Cochrane Database Syst Rev. (2005) CD003474
42. Saad F., Lipton A., Cook R., et al. Pathologic fractures correlate with reduced survival in patients with malignant bone disease. Cancer 110 (2007) 1860-1867
43. Small E.J., Smith M.R., Seaman J.J., et al. Combined analysis of two multicenter, randomized, placebo-controlled studies of pamidronate disodium for the palliation of bone pain in men with metastatic prostate cancer. J Clin Oncol. 21 (2003) 4277-4284
44. Saad F., and Lipton A. Zoledronic acid is effective in preventing and delaying skeletal events in patients with bone metastases secondary to genitourinary cancers. BJU Int. 96 (2005) 964-969
45. Lipton A., Cook R., Saad F., et al. Normalization of bone markers is associated with improved survival in patients with bone metastases from solid tumors and elevated bone resorption receiving zoledron-ic acid. Cancer 113 (2008) 193-201
46. Saad F. Bisphosphonates can prevent skeletal complications of malignant bone disease from prostate cancer and renal cell carcinoma. Eur Urol Suppl. 6 (2007) 683-688
47. Biermann W.A., Cantor R.I., Fellin F.M., et al. An evaluation of the potential cost reductions resulting from the use of clodronate in the treatment of metastatic carcinoma of the breast to bone. Bone 12 Suppl 1 (1991) S37-S42
48. De Cock E., Hutton J., Canney P., et al. Cost-effectiveness of oral iban-dronate compared with intravenous (i.v.) zoledronic acid or i.v. generic pamidronate in breast cancer patients with metastatic bone disease undergoing i.v. chemotherapy. Support Care Cancer. 13 (2005) 975-986
49. De Cock E., Hutton J., Canney P., et al. Cost-effectiveness of oral iban-dronate versus IV zoledronic acid or IV pamidronate for bone metastases in patients receiving oral hormonal therapy for breast cancer in the United Kingdom. Clin Ther. 27 (2005) 1295-1310
50. Gessner U., Koeberle D., Thuerlimann B., et al. Economic analysis of terminal care for patients with malignant osteolytic bone disease and pain treated with pamidronate. Support Care Cancer. 8 (2000) 115-122
51. Romanus D., Iscoe N., Deangelis C., et al. Cost analysis of secondary prophylaxis with oral clodronate versus pamidronate in metastatic breast cancer patients. Support Care Cancer 12 (2004) 844-851
52. Ali S.M., Esteva F.J., Hortobagyi G., et al. Safety and efficacy of bisphos-phonates beyond 24 months in cancer patients. J Clin Oncol. 19 (2001) 3434-3437
53. Bamias A., Kastritis E., Bamia C., et al. Osteonecrosis of the jaw in cancer after treatment with bis-phosphonates: Incidence and risk factors. J Clin Oncol. 23 (2005) 8580-8587
54. Hirsh V., Major P.P., Lipton A., et al. Zoledronic acid and survival in patients with metastatic bone disease from lung cancer and elevated markers of osteoclast activity. J Thorac Oncol. 3 (2008) 228-236
55. Hultborn R., Gundersen S., Rydén S., et al. Efficacy of pamidronate in breast cancer with bone metastases: A randomized double-blind placebo controlled multicenter study. Acta Oncol. 35 Suppl 5 (1996) 73-74
56. Lipton A., Colombo-Berra A., Bukowski R.M., et al. Skeletal complications in patient with bone metastases from renal cell carcinoma and therapeutic benefits of zoledronic acid. Clin Cancer Res. 10 (2004) 6397S-6403S
57. Paterson A.H., Ernst D.S., Powles T.J., et al. Treatment of skeletal disease in breast cancer with clodronate. Bone 12 Suppl 1 (1991) S25-S30
58. Saad F., Gleason D.M., Murray R., et al., the Zoledronic Acid Prostate Cancer Study Group. Long-term efficacy of zoledronic acid for the prevention of skeletal complications in patients with metastatic hormone-refractory prostate cancer. J Natl Cancer Inst. 96 (2004) 879-882
59. Schulman C.C. Efficacy of zoledronic acid in the treatment of bone metastases secondary to renal cell carcinoma. Eur Urol Suppl. 3 (2004) 40-45
60. Berenson J.R., Lichtenstein A., Porter L., et al., the Myeloma Aredia Study Group. Efficacy of pamid-ronate in reducing skeletal events in patients with advanced multiple myeloma. N Engl J Med. 334 (1996) 488-493
61. Brincker H., Westin J., Abildgaard N., et al., the Danish-Swedish Cooperative Study Group. Failure of oral pamidronate to reduce skeletal morbidity in multiple myeloma: A double-blind placebo-controlled trial. Br J Haematol. 101 (1998) 280-286
62. Conte P.F., Latreille J., Mauriac L., et al., the Aredia Multinational Cooperative Group. Delay in progression of bone metastases in breast cancer patients treated with intravenous pamidronate: Results from a multinational randomized controlled trial. J Clin Oncol. 14 (1996) 2552-2559
63. Dearnaley D.P., Sydes M.R., Mason M.D., et al., the Mrc Pr05 Collaborators. A double-blind, placebo-controlled, randomized trial of oral sodium clodronate for metastatic prostate cancer (MRC PR05 Trial). J Natl Cancer Inst. 95 (2003) 1300-1311
64. Hortobagyi G.N., Theriault R.L., Porter L., et al., the Protocol 19 Aredia Breast Cancer Study Group. Efficacy of pamidronate in reducing skeletal complications in patients with breast cancer and lytic bone metastases. N Engl J Med. 335 (1996) 1785-1791
65. Hultborn R., Gundersen S., Ryden S., et al. Efficacy of pamidronate in breast cancer with bone metastases: A randomized, double-blind placebo controlled multicenter study. Anticancer Res. 19 (1999) 3383-3392
66. Kanis J.A., Powles T., Paterson A.H., et al. Clodronate decreases the frequency of skeletal metastases in women with breast cancer. Bone 19 (1996) 663-667
67. Kohno N., Aogi K., Minami H., et al. Zoledronic acid significantly reduces skeletal complications compared with placebo in Japanese women with bone metastases from breast cancer: A randomized, placebo-controlled trial. J Clin Oncol. 15 (2005) 3314-3321
68. Kristensen B., Ejlertsen M., Groenvold M., et al. Oral clodronate in breast cancer patients with bone metastases: A randomized study. J Intern Med. 246 (1999) 67-74
69. Lahtinen R., Laakso M., Palva I., et al., the Finnish Leukaemia Group. Randomised, placebo-controlled multicentre trial of clodronate in multiple myeloma [published correction appears in Lancet. 1992; 340: 1420]. Lancet 340 (1992) 1049-1052
70. Lipton A., Zheng M., and Seaman J. Zoledronic acid delays the onset of skeletal-related events and progression of skeletal disease in patients with advanced renal cell carcinoma. Cancer. 98 (2003) 962-969
71. McCloskey E.V., McLennan I.C., Drayson M.T., et al. A randomized trial of the effect of clodronate on skeletal morbidity in multiple myeloma. MRC Working Party on Leukaemia in Adults. Br J Haematol 100 (1998) 317-325
72. Paterson A.H., Powles T.J., Kanis J.A., et al. Double-blind controlled trial of oral clodronate in patients with bone metastases from breast cancer. J Clin Oncol. 11 (1993) 59-65
73. Rosen L.S., Gordon D., Tchekmedyian S., et al. Zoledronic acid versus placebo in the treatment of skeletal metastases in patients with lung cancer and other solid tumors: A phase III, double-blind, randomized trial-the Zoledronic Acid Lung Cancer and Other Solid Tumors Study Group. J Clin Oncol. 21 (2003) 3150-3157
74. Saad F., Gleason D.M., Murray R., et al., the Zoledronic Acid Prostate Cancer Study Group. A randomized, placebo-controlled trial of zoledronic acid in patients with hormone-refractory metastatic prostate carcinoma. J Natl Cancer Inst. 94 (2002) 1458-1468
75. Theriault R.L., Lipton A., Hortobagyi G.N., et al., the Protocol 18 Aredia Breast Cancer Study Group. Pamidronate reduces skeletal morbidity in women with advanced breast cancer and lytic bone lesions: A randomized, placebo-controlled trial. J Clin Oncol. 17 (1999) 846-854
76. Tubiana-Hulin M., Beuzeboc P., Mauriac L., et al. Double-blinded controlled study comparing clo- dronate versus placebo in patients with breast cancer bone metastases [in French]. Bull Cancer. 88 (2001) 701-707
77. van Holten-Verzantvoort A.T., Hermans J., Beex L.V., et al. Does supportive pamidronate treatment prevent or delay the first manifestation of bone metastases in breast cancer patients?. Eur J Cancer 327 (1996) 450-454
78. Yuen K.K., Shelley M., Sze W.M., et al. Bisphosphonates for advanced prostate cancer. Cochrane Database Syst Rev. (2006) CD006250
79. Djulbegovic B., Wheatley K., Ross J., et al. Bisphosphonates in multiple myeloma. Cochrane Database Syst Rev. (2002) CD003188
80. Menssen H.D., Sakalová A., Fontana A., et al. Effects of long-term intravenous ibandronate therapy on skeletal-related events, survival, and bone resorption markers in patients with advanced multiple myeloma. J Clin Oncol. 20 (2002) 2353-2359
81. Heidenreich A., Elert A., and Hofmann R. Ibandronate in the treatment of prostate cancer associated painful osseous metastases. Prostate Cancer Prostatic Dis. 5 (2002) 231-235
82. Heras P., Karagiannis S., Kritikos K., et al. Ibandronate is effective in preventing skeletal events in patients with bone metastases from colorectal cancer. Eur J Cancer Care (Engl). 16 (2007) 539-542
83. Tripathy D., Lichinitzer M., Lazarev A., et al., the MF 4434 Study Group. Oral ibandronate for the treatment of metastatic disease in breast cancer: Efficacy and safety results from a randomized, doubleblind, placebo-controlled trial. Ann Oncol. 15 (2004) 743-750
84. Body J.J., Diel I.J., Lichinitzer M., et al. Oral ibandronate reduces the risk of skeletal complications in breast cancer patients with metastatic bone disease: Results from two randomised, placebo-controlled phase III studies. Br J Cancer 90 (2004) 1133-1137
85. Body J.J., Diel I.J., Lichnitser M.R., et al., the MF 4265 Study Group. Intravenous ibandronate reduces the incidence of skeletal complications in patients with breast cancer and bone metastases. Ann Oncol. 14 (2003) 1399-1405
86. Tripathy D., Body J.J., and Bergström B. Review of ibandronate in the treatment of metastatic bone disease: Experience from phase III trials. Clin Ther. 26 (2004) 1947-1959