Effect of COX-2 inhibitors and other non-steroidal inflammatory drugs on breast cancer risk: a meta-analysis

Breast Cancer Research and Treatment

Volumn 149, Issue 2, 2015, Pages 525-536

  de Pedro, María ^a,f   Baeza, Sara ^b   Escudero, María Teresa ^c   Dierssen Sotos, Trinidad ^d   Gómez Acebo, Inés ^d   Pollán, Marina ^e   Llorca, Javier ^d  

^a Nuevo Belén University Hospital   (Spain)

^b HOSPITAL NUESTRA SEÑORA DE SONSOLES   (Spain)

^c HOSPITAL UNIVERSITARIO MARQUÉS DE VALDECILLA   (Spain)

^d UNIVERSITY OF CANTABRIA   (Spain)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

^f UNIVERSITY OF CANTABRIA   (Spain)

Author keywords

Anti inflammatory drugs; Aspirin; Breast cancer; COX 2 inhibitor; Ibuprofen; NSAID

Indexed keywords

ACETYLSALICYLIC ACID; CELECOXIB; CYCLOOXYGENASE 2 INHIBITOR; IBUPROFEN; PARACETAMOL; ROFECOXIB; VALDECOXIB; NONSTEROID ANTIINFLAMMATORY AGENT;

ARTICLE; CANCER INCIDENCE; CANCER RISK; CHEMOPROPHYLAXIS; DRUG EFFECT; DRUG USE; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; HUMAN; META ANALYSIS; PRIORITY JOURNAL; RISK REDUCTION; SYSTEMATIC REVIEW; BREAST NEOPLASMS; CASE CONTROL STUDY; COHORT ANALYSIS; FEMALE; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK;

ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BREAST NEOPLASMS; CASE-CONTROL STUDIES; COHORT STUDIES; CYCLOOXYGENASE 2 INHIBITORS; FEMALE; HUMANS; ODDS RATIO; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK;

EID: 84925482290     PISSN: 01676806     EISSN: 15737217     Source Type: Journal    
DOI: 10.1007/s10549-015-3267-9     Document Type: Article

References (93)

1. Carter CA, Milholland RJ, Shea W, Ip MM (1983) Effect of the prostaglandin synthetase inhibitor indomethacin on 7,12-dimethylbenz(a)anthracene-induced mammary tumorigenesis in rats fed different levels of fat. Cancer Res 43(8):3559–3562
2. Hwang D, Scollard D, Byrne J, Levine E (1998) Expression of cyclooxygenase-1 and cyclooxygenase-2 in human breast cancer. J Natl Cancer Inst 90(6):455–460
3. Shiff SJ, Rigas B (1999) The role of cyclooxygenase inhibition in the antineoplastic effects of nonsteroidal antiinflammatory drugs (NSAIDs). J Exp Med 190(4):445–450
4. Williams CS, Mann M, DuBois RN (1999) The role of cyclooxygenases in inflammation, cancer, and development. Oncogene 18(55):7908–7916
5. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420(6917):860–867
6. Thun MJ, Henley SJ, Patrono C (2002) Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 94(4):252–266
7. Dubé C, Rostom A, Lewin G, Tsertsvadze A, Barrowman N, Code C, Sampson M, Moher D (2007) U.S. preventive services task force. The use of aspirin for primary prevention of colorectal cancer: a systematic review prepared for the U.S. preventive services task force. Ann Intern Med 146(5):365–375
8. Rostom A, Dubé C, Lewin G, Tsertsvadze A, Barrowman N, Code C, Sampson M, Moher D (2007) U.S. preventive services task force. Nonsteroidal anti-inflammatory drugs and cyclooxygenase-2 inhibitors for primary prevention of colorectal cancer: a systematic review prepared for the U.S. preventive services task force. Ann Intern Med 146(5):376–389
9. Harris RE, Alshafie GA, Seibert K (2000) Chemoprevention of breast cancer in rats by celecoxib, a cyclooxygenase 2 inhibitor. Cancer Res 20(8):2101–2103
10. Harris RE, Beebe-Donk J, Doss H, Burr Doss D (2005) Aspirin, ibuprofen, and other non-steroidal anti-inflammatory drugs in cancer prevention: a critical review of non-selective COX-2 blockade (review). Oncol Rep 13(4):559–583
11. Howe LR (2007) Inflammation and breast cancer. Cyclooxygenase/prostaglandin signaling and breast cancer. Breast Cancer Res 9(4):210
12. Singh-Ranger G, Salhab M, Mokbel K (2008) The role of cyclooxygenase-2 in breast cancer: review. Breast Cancer Res Treat 109(2):189–198
13. Howe LR, Lippman SM (2008) Modulation of breast cancer risk by nonsteroidal anti-inflammatory drugs. J Natl Cancer Inst 100(20):1420–1423
14. Rahme E, Ghosn J, Dasgupta K, Rajan R, Hudson M (2005) Association between frequent use of nonsteroidal anti-inflammatory drugs and breast cancer. BMC Cancer 5:159
15. Harris RE, Namboodiri K, Stellman SD, Wynder EL (1995) Breast cancer and NSAID use: heterogeneity of effect in a case-control study. Prev Med 24(2):119–120
16. Harris R, Namboodiri K, Farrar W (1995) Epidemiologic-study of nonsteroidal antiinflammatory drugs and breast-cancer. Oncol Rep 2(4):591–592
17. Rosenberg L (1995) Nonsteroidal anti-inflammatory drugs and cancer. Prev Med 24(2):107–109
18. Harris RE, Namboodiri KK, Farrar WB (1996) Nonsteroidal antiinflammatory drugs and breast cancer. Epidemiology 7(2):203–205
19. Neugut AI, Rosenberg DJ, Ahsan H, Jacobson JS, Wahid N, Hagan M, Rahman MI, Khan ZR, Chen L, Pablos-Mendez A, Shea S (1998) Association between coronary heart disease and cancers of the breast, prostate, and colon. Cancer Epidemiol Biomark Prev 7(10):869–873
20. Coogan PF, Rao SR, Rosenberg L, Palmer JR, Strom BL, Zauber AG, Stolley PD, Shapiro S (1999) The relationship of nonsteroidal anti-inflammatory drug use to the risk of breast cancer. Prev Med 29(2):72–76
21. Langman MJ, Cheng KK, Gilman EA, Lancashire RJ (2000) Effect of anti-inflammatory drugs on overall risk of common cancer: case-control study in general practice research database. BMJ 320(7250):1642–1646
22. Cotterchio M, Kreiger N, Sloan M, Steingart A (2001) Nonsteroidal anti-inflammatory drug use and breast cancer risk. Cancer Epidemiol Biomark Prev 10(11):1213–1217
23. Meier CR, Schmitz S, Jick H (2002) Association between acetaminophen or nonsteroidal antiinflammatory drugs and risk of developing ovarian, breast, or colon cancer. Pharmacotherapy 22(3):303–309
24. Moorman PG, Grubber JM, Millikan RC, Newman B (2003) Association between non-steroidal anti-inflammatory drugs (NSAIDs) and invasive breast cancer and carcinoma in situ of the breast. Cancer Causes Control 14(10):915–922
25. Terry MB, Gammon MD, Zhang FF, Tawfik H, Teitelbaum SL, Britton JA, Subbaramaiah K, Dannenberg AJ, Neugut AI (2004) Association of frequency and duration of aspirin use and hormone receptor status with breast cancer risk. JAMA 291(20):2433–2440
26. Swede H, Mirand AL, Menezes RJ, Moysich KB (2005) Association of regular aspirin use and breast cancer risk. Oncology 68(1):40–47
27. Zhang Y, Coogan PF, Palmer JR, Strom BL, Rosenberg L (2005) Use of nonsteroidal antiinflammatory drugs and risk of breast cancer: the case–control surveillance study revisited. Am J Epidemiol 162(2):165–170
28. Harris RE, Beebe-Donk J, Alshafie GA (2006) Reduction in the risk of human breast cancer by selective cyclooxygenase-2 (COX-2) inhibitors. BMC Cancer 30(6):27
29. Shen J, Gammon MD, Terry MB, Teitelbaum SL, Neugut AI, Santella RM (2006) Genetic polymorphisms in the cyclooxygenase-2 gene, use of nonsteroidal anti-inflammatory drugs, and breast cancer risk. Breast Cancer Res 8(6):R71
30. Vogel U, Christensen J, Nexø BA, Wallin H, Friis S, Tjønneland A (2007) Peroxisome proliferator-activated [corrected] receptor-gamma2 [corrected] Pro12Ala, interaction with alcohol intake and NSAID use, in relation to risk of breast cancer in a prospective study of Danes. Carcinogenesis 28(2):427–434
31. Chan AT, Manson JE, Feskanich D, Stampfer MJ, Colditz GA, Fuchs CS (2007) Long-term aspirin use and mortality in women. Arch Intern Med 167(6):562–572
32. Davis S, Mirick DK (2007) Medication use and the risk of breast cancer. Eur J Epidemiol 22(5):319–325
33. Kirsh VA, Kreiger N, Cotterchio M, Sloan M, Theis B (2007) Nonsteroidal antiinflammatory drug use and breast cancer risk: subgroup findings. Am J Epidemiol 166(6):709–716
34. Slattery ML, Curtin K, Baumgartner R, Sweeney C, Byers T, Giuliano AR, Baumgartner KB, Wolff RR (2007) IL6, aspirin, nonsteroidal anti-inflammatory drugs, and breast cancer risk in women living in the southwestern United States. Cancer Epidemiol Biomark Prev 16(4):747–755
35. Brasky TM, Bonner MR, Moysich KB, Ambrosone CB, Nie J, Tao MH, Edge SB, Kallakury BV, Marian C, Trevisan M, Shields PG, Freudenheim JL (2010) Non-steroidal anti-inflammatory drug (NSAID) use and breast cancer risk in the Western New York exposures and breast cancer (WEB) Study. Cancer Causes Control 21(9):1503–1512
36. Cronin-Fenton DP, Pedersen L, Lash TL, Friis S, Baron JA, Sørensen HT (2010) Prescriptions for selective cyclooxygenase-2 inhibitors, non-selective non-steroidal anti-inflammatory drugs, and risk of breast cancer in a population-based case-control study. Breast Cancer Res 12(2):R15
37. Ashok V, Dash C, Rohan TE, Sprafka JM, Terry PD (2011) Selective cyclooxygenase-2 (COX-2) inhibitors and breast cancer risk. Breast 20(1):66–70
38. Brasky TM, Bonner MR, Moysich KB, Ochs-Balcom HM, Marian C, Ambrosone CB, Nie J, Tao MH, Edge SB, Trevisan M, Shields PG, Freudenheim JL (2011) Genetic variants in COX-2, non-steroidal anti-inflammatory drugs, and breast cancer risk: the Western New York exposures and breast cancer (WEB) study. Breast Cancer Res Treat 126(1):157–165
39. Brasky TM, Bonner MR, Moysich KB, Ambrosone CB, Nie J, Tao MH, Edge SB, Kallakury BV, Marian C, Goerlitz DS, Trevisan M, Shields PG, Freudenheim JL (2011) Non-steroidal anti-inflammatory drugs (NSAIDs) and breast cancer risk: differences by molecular subtype. Cancer Causes Control 22(7):965–975
40. Vinogradova Y, Coupland C, Hippisley-Cox J (2011) Exposure to cyclooxygenase-2 inhibitors and risk of cancer: nested case-control studies. Br J Cancer 105(3):452–459
41. Jonsson F, Yin L, Lundholm C, Smedby KE, Czene K, Pawitan Y (2013) Low-dose aspirin use and cancer characteristics: a population-based cohort study. Br J Cancer 109(7):1921–1925
42. Ou SM, Chen YT, Chao PW, Lee YJ, Liu CJ, Yeh CM, Chen TJ, Chen TW, Yang WC, Li SY (2013) Nonsteroidal anti-inflammatory drug use is associated with cancer risk reduction in chronic dialysis patients. Kidney Int 84(1):198–205
43. Friedman GD, Ury HK (1980) Initial screening for carcinogenicity of commonly used drugs. J Natl Cancer Inst 65(4):723–733
44. Paganini-Hill A, Chao A, Ross RK, Henderson BE (1989) Aspirin use and chronic diseases: a cohort study of the elderly. BMJ 299(6710):1247–1250
45. Thun MJ, Namboodiri MM, Calle EE, Flanders WD, Heath CW Jr (1993) Aspirin use and risk of fatal cancer. Cancer Res 53(6):1322–1327
46. Schreinemachers DM, Everson RB (1994) Aspirin use and lung, colon, and breast cancer incidence in a prospective study. Epidemiology 5(2):138–146
47. Egan KM, Stampfer MJ, Giovannucci E, Rosner BA, Colditz GA (1996) Prospective study of regular aspirin use and the risk of breast cancer. J Natl Cancer Inst 88(14):988–993
48. Harris RE, Kasbari S, Farrar WB (1999) Prospective study of nonsteroidal anti-inflammatory drugs and breast cancer. Oncol Rep 6(1):71–73
49. Sharpe CR, Collet JP, McNutt M, Belzile E, Boivin JF, Hanley JA (2000) Nested case-control study of the effects of non-steroidal anti-inflammatory drugs on breast cancer risk and stage. Br J Cancer 83(1):112–120
50. Friis S, Nielsen GL, Mellemkjaer L, McLaughlin JK, Thulstrup AM, Blot WJ, Lipworth L, Vilstrup H, Olsen JH (2002) Cancer risk in persons receiving prescriptions for paracetamol: a Danish cohort study. Int J Cancer 97(1):96–101
51. Johnson TW, Anderson KE, Lazovich D, Folsom AR (2002) Association of aspirin and nonsteroidal anti-inflammatory drug use with breast cancer. Cancer Epidemiol Biomark Prev 11(12):1586–1591
52. Friis S, Sørensen HT, McLaughlin JK, Johnsen SP, Blot WJ, Olsen JH (2003) A population-based cohort study of the risk of colorectal and other cancers among users of low-dose aspirin. Br J Cancer 88(5):684–688
53. Harris RE, Chlebowski RT, Jackson RD, Frid DJ, Ascenseo JL, Anderson G, Loar A, Rodabough RJ, White E, McTiernan A (2003) Women’s health initiative. Breast cancer and nonsteroidal anti-inflammatory drugs: prospective results from the women’s health initiative. Cancer Res 63(18):6096–6101
54. Sørensen HT, Friis S, Nørgård B, Mellemkjaer L, Blot WJ, McLaughlin JK, Ekbom A, Baron JA (2003) Risk of cancer in a large cohort of nonaspirin NSAID users: a population-based study. Br J Cancer 88(11):1687–1692
55. Ratnasinghe LD, Graubard BI, Kahle L, Tangrea JA, Taylor PR, Hawk E (2004) Aspirin use and mortality from cancer in a prospective cohort study. Anticancer Res 24(5B):3177–3184
56. García Rodríguez LA, González-Pérez A (2004) Risk of breast cancer among users of aspirin and other anti-inflammatory drugs. Br J Cancer 91(3):525–529
57. Jacobs EJ, Thun MJ, Connell CJ, Rodriguez C, Henley SJ, Feigelson HS, Patel AV, Flanders WD, Calle EE (2005) Aspirin and other nonsteroidal anti-inflammatory drugs and breast cancer incidence in a large US cohort. Cancer Epidemiol Biomark Prev 14(1):261–264
58. Marshall SF, Bernstein L, Anton-Culver H, Deapen D, Horn-Ross PL, Mohrenweiser H, Peel D, Pinder R, Purdie DM, Reynolds P, Stram D, West D, Wright WE, Ziogas A, Ross RK (2005) Nonsteroidal anti-inflammatory drug use and breast cancer risk by stage and hormone receptor status. J Natl Cancer Inst 97(11):805–812
59. Gallicchio L, McSorley MA, Newschaffer CJ, Thuita LW, Huang HY, Hoffman SC, Helzlsouer KJ (2006) Nonsteroidal antiinflammatory drugs, cyclooxygenase polymorphisms, and the risk of developing breast carcinoma among women with benign breast disease. Cancer 106(7):1443–1452
60. Gallicchio L, Visvanathan K, Burke A, Hoffman SC, Helzlsouer KJ (2007) Nonsteroidal anti-inflammatory drugs and the risk of developing breast cancer in a population-based prospective cohort study in Washington County, MD. Int J Cancer 121(1):211–215
61. Gill JK, Maskarinec G, Wilkens LR, Pike MC, Henderson BE, Kolonel LN (2007) Nonsteroidal antiinflammatory drugs and breast cancer risk: the multiethnic cohort. Am J Epidemiol 166(10):1150–1158
62. Jacobs EJ, Thun MJ, Bain EB, Rodriguez C, Henley SJ, Calle EE (2007) A large cohort study of long-term daily use of adult-strength aspirin and cancer incidence. J Natl Cancer Inst 99(8):608–615
63. Bardia A, Ebbert JO, Vierkant RA, Limburg PJ, Anderson K, Wang AH, Olson JE, Vachon CM, Cerhan JR (2007) Association of aspirin and nonaspirin nonsteroidal anti-inflammatory drugs with cancer incidence and mortality. J Natl Cancer Inst 99(11):881–889
64. Friis S, Thomassen L, Sørensen HT, Tjønneland A, Overvad K, Cronin-Fenton DP, Vogel U, McLaughlin JK, Blot WJ, Olsen JH (2008) Nonsteroidal anti-inflammatory drug use and breast cancer risk: a Danish cohort study. Eur J Cancer Prev 17(2):88–96
65. Ready A, Velicer CM, McTiernan A, White E (2008) NSAID use and breast cancer risk in the VITAL cohort. Breast Cancer Res Treat 109(3):533–543
66. Gierach GL, Lacey JV Jr, Schatzkin A, Leitzmann MF, Richesson D, Hollenbeck AR, Brinton LA (2008) Nonsteroidal anti-inflammatory drugs and breast cancer risk in the national institutes of health-AARP diet and health study. Breast Cancer Res 10(2):R38
67. Siemes C, Visser LE, Coebergh JW, Hofman A, Uitterlinden AG, Stricker BH (2008) Protective effect of NSAIDs on cancer and influence of COX-2 C(-765G) genotype. Curr Cancer Drug Targets 8(8):753–764
68. Eliassen AH, Chen WY, Spiegelman D, Willett WC, Hunter DJ, Hankinson SE (2009) Use of aspirin, other nonsteroidal anti-inflammatory drugs, and acetaminophen and risk of breast cancer among premenopausal women in the Nurses’ Health Study II. Arch Intern Med 169(2):115–121
69. Bardia A, Olson JE, Vachon CM, Lazovich D, Vierkant RA, Wang AH, Limburg PJ, Anderson KE, Cerhan JR (2011) Effect of aspirin and other NSAIDs on postmenopausal breast cancer incidence by hormone receptor status: results from a prospective cohort study. Breast Cancer Res Treat 126(1):149–155
70. Bosco JL, Palmer JR, Boggs DA, Hatch EE, Rosenberg L (2011) Regular aspirin use and breast cancer risk in US Black women. Cancer Causes Control 22(11):1553–1561
71. Zhang X, Smith-Warner SA, Collins LC, Rosner B, Willett WC, Hankinson SE (2012) Use of aspirin, other nonsteroidal anti-inflammatory drugs, and acetaminophen and postmenopausal breast cancer incidence. J Clin Oncol 30(28):3468–3477
72. Cook NR, Lee IM, Gaziano JM, Gordon D, Ridker PM, Manson JE, Hennekens CH, Buring JE (2005) Low-dose aspirin in the primary prevention of cancer: the women’s health study: a randomized controlled trial. JAMA 294(1):47–55
73. Zhang SM, Cook NR, Manson JE, Lee IM, Buring JE (2008) Low-dose aspirin and breast cancer risk: results by tumour characteristics from a randomised trial. Br J Cancer 98(5):989–991
74. Bulun SE, Lin Z, Imir G et al (2005) Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev 57(3):359–383
75. Asaga S, Jinno H, Sakata M, Kitajima M (2007) Current perspective of chemoprevention in breast cancer. Nihon Rinsho 65(Suppl 3):627–632
76. Algra AM, Rothwell PM (2012) Effects of regular aspirin on long-term cancer incidence and metastasis: a systematic comparison of evidence from observational studies versus randomised trials. Lancet Oncol 13(5):518–527
77. Bosetti C, Gallus S, La Vecchia C (2006) Aspirin and cancer risk: an updated quantitative review to 2005. Cancer Causes Control 17(7):871–888
78. Bosetti C, Rosato V, Gallus S, Cuzick J, La Vecchia C (2012) Aspirin and cancer risk: a quantitative review to 2011. Ann Oncol 23(6):1403–1415
79. González-Pérez A, García Rodríguez LA, López-Ridaura R (2003) Effects of non-steroidal anti-inflammatory drugs on cancer sites other than the colon and rectum: a meta-analysis. BMC Cancer 3:28
80. Harris RE (2009) Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 17(2):55–67
81. Khuder SA, Mutgi AB (2001) Breast cancer and NSAID use: a meta-analysis. Br J Cancer 84(9):1188–1192
82. Luo T, Yan HM, He P, Luo Y, Yang YF, Zheng H (2012) Aspirin use and breast cancer risk: a meta-analysis. Breast Cancer Res Treat 131(2):581–587
83. Mangiapane S, Blettner M, Schlattmann P (2008) Aspirin use and breast cancer risk: a meta-analysis and meta-regression of observational studies from 2001 to 2005. Pharmacoepidemiol Drug Saf 17(2):115–124
84. Takkouche B, Regueira-Méndez C, Etminan M (2008) Breast cancer and use of nonsteroidal anti-inflammatory drugs: a meta-analysis. J Natl Cancer Inst 100(20):1439–1447
85. Tolentino Silva M, Freire Galvao T, Ricardo Zimmerman I, Gomes Pereira M, Cruz Lopes L (2012) Non-aspirin non-steroidal anti-inflammatory drugs for the primary chemoprevention of non-gastrointestinal cancer: summary of evidence. Curr Pharm Des 18(26):4047–4070
86. Zhao YS, Zhu S, Li XW, Wang F, Hu FL, Li DD, Zhang WC, Li X (2009) Association between NSAIDs use and breast cancer risk: a systematic review and meta-analysis. Breast Cancer Res Treat 117(1):141–150
87. Brockwell SE, Gordon IR (2001) A comparison of statistical methods for metaanalysis. StatMed 20:825–840
88. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7:177–188
89. Higgins JP, Thompson SG (2002) Quantifying heterogeneity in a meta-analysis. Stat Med 21:1539–1558
90. Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. Brit Med J 315:629–634
91. Light RJ, Pillemer DB (1984) Summing up: The science of reviewing research. Harvard University Press, Cambridge, MA
92. Duval S, Tweedie R (2000) Trim and fill: a simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics 56:455–463
93. Jin ZC, Zhou XH, He J (2014) Statistical methods for dealing with publication bias in meta-analysis. Stat Med. doi:10.1002/sim.6342