Non-steroidal anti-inflammatory drugs use is associated with reduced risk of inflammation-associated cancers: NIH-AARP study

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Shebl, Fatma M ^e   Hsing, Ann W ^c,f   Park, Yikyung ^g   Hollenbeck, Albert R ^b   Chu, Lisa W ^c,d   Meyer, Tamra E ^h   Koshiol, Jill ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b AARP   (United States)

^c CANCER PREVENTION INSTITUTE OF CALIFORNIA   (United States)

^d STANFORD CANCER INSTITUTE   (United States)

^e YALE UNIVERSITY   (United States)

^f Cancer Institute   (United States)

^g WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h Pharmacovigilance Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ANACIN; EXCEDRIN; FENOPROFEN; FENOPROFEN CALCIUM; IBUPROFEN; INDOMETACIN; KETOPROFEN; NABUMETONE; NAPROXEN; NONSTEROID ANTIINFLAMMATORY AGENT; PIROXICAM; SULINDAC;

ADULT; AGED; ALCOHOL CONSUMPTION; ANUS CANCER; ARTICLE; BREAST CANCER; CANCER INCIDENCE; CANCER RISK; COHORT ANALYSIS; COLORECTAL CANCER; CONTROLLED STUDY; DRUG USE; ENDOMETRIUM CANCER; ESOPHAGUS CANCER; ETHNICITY; FEMALE; FEMALE GENITAL TRACT CANCER; FOLLOW UP; GALLBLADDER CANCER; HEAD AND NECK CANCER; HUMAN; INFECTION; KIDNEY CANCER; LIFESTYLE; LIVER CANCER; LYMPHOMA; MALE; MALIGNANT NEOPLASTIC DISEASE; OBESITY; PANCREAS CANCER; POPULATION RESEARCH; PROPENSITY SCORE; PROSPECTIVE STUDY; RISK REDUCTION; SMOKING; STOMACH CANCER; THYROID CANCER; COMPLICATION; INCIDENCE; INFLAMMATION; MIDDLE AGED; NATIONAL HEALTH ORGANIZATION; NEOPLASMS; RISK; UNITED STATES;

AGED; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ASPIRIN; COHORT STUDIES; FEMALE; HUMANS; INCIDENCE; INFLAMMATION; MALE; MIDDLE AGED; NATIONAL INSTITUTES OF HEALTH (U.S.); NEOPLASMS; RISK; UNITED STATES;

EID: 84928568621     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114633     Document Type: Article

References (84)

1. Haas M, Buttner M, Rau TT, Fietkau R, Grabenbauer GG, et al. (2011) Inflammation in gastric adenocarcinoma of the cardia: how do EBV infection, Her2 amplification and cancer progression influence tumor-infiltrating lymphocytes? Virchows Arch 458: 403-411.
2. Mantovani A, Allavena P, Sica A, Balkwill F (2008) Cancer-related inflammation. Nature 454: 436-444.
3. Allavena P, Garlanda C, Borrello MG, Sica A, Mantovani A (2008) Pathways connecting inflammation and cancer. Curr Opin Genet Dev 18: 3-10.
4. Mantovani A, Pierotti MA (2008) Cancer and inflammation: A complex relationship. Cancer Lett 267: 180-181.
5. Daugherty SE, Pfeiffer RM, Sigurdson AJ, Hayes RB, Leitzmann M, et al. (2011) Nonsteroidal antiinflammatory drugs and bladder cancer: A pooled analysis. Am J Epidemiol 173: 721-730.
6. McCormack VA, Hung RJ, Brenner DR, Bickeboller H, Rosenberger A, et al. (2011) Aspirin and NSAID use and lung cancer risk: A pooled analysis in the International Lung Cancer Consortium (ILCCO). Cancer Causes Control 22: 1709-1720.
7. Ruder EH, Laiyemo AO, Graubard BI, Hollenbeck AR, Schatzkin A, et al. (2011) Non-steroidal antiinflammatory drugs and colorectal cancer risk in a large, prospective cohort. Am J Gastroenterol 106: 1340-1350.
8. Wernli KJ, Newcomb PA, Hampton JM, Trentham-Dietz A, Egan KM (2008) Inverse association of NSAID use and ovarian cancer in relation to oral contraceptive use and parity. Br J Cancer 98: 1781-1783.
9. Coogan PF, Kelly JP, Strom BL, Rosenberg L (2010) Statin and NSAID use and prostate cancer risk. Pharmacoepidemiol Drug Saf 19: 752-755.
10. Danforth KN, Gierach GL, Brinton LA, Hollenbeck AR, Katki HA, et al. (2009) Nonsteroidal antiinflammatory drug use and endometrial cancer risk in the NIH-AARP Diet and Health Study. Cancer Prev Res (Phila) 2: 466-472.
11. Daugherty SE, Moore SC, Pfeiffer RM, Inskip PD, Park Y, et al. (2011) Nonsteroidal Anti-inflammatory Drugs and Glioma in the NIH-AARP Diet and Health Study Cohort. Cancer Prev Res (Phila) 4: 2027-2034.
12. Legge F, Paglia A, D'Asta M, Fuoco G, Scambia G, et al. (2011) Phase II study of the combination carboplatin plus celecoxib in heavily pre-treated recurrent ovarian cancer patients. BMC Cancer 11: 214.
13. Chan AT, Hsu M, Zauber AG, Hawk ET, Bertagnolli MM (2011) The Influence of UGT1A6 Variants and Aspirin Use in a Randomized Trial of Celecoxib for Prevention of Colorectal Adenoma. Cancer Prev Res (Phila).
14. Burn J, Bishop DT, Chapman PD, Elliott F, Bertario L, et al. (2011) A randomized placebo-controlled prevention trial of aspirin and/or resistant starch in young people with familial adenomatous polyposis. Cancer Prev Res (Phila) 4: 655-665.
15. Sandler RS, Halabi S, Baron JA, Budinger S, Paskett E, et al. (2003) A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer. N Engl J Med 348: 883-890.
16. Schatzkin A, Subar AF, Thompson FE, Harlan LC, Tangrea J, et al. (2001) Design and serendipity in establishing a large cohort with wide dietary intake distributions: The National Institutes of Health-American Association of Retired Persons Diet and Health Study. Am J Epidemiol 154: 1119-1125.
17. Michaud DS, Midthune D, Hermansen S, Leitzmann M, Harlan LC, et al. (2005) Comparison of cancer registry case ascertainment with SEER estimates and self-reporting in a subset of the NIHAARP Diet and Health Study. J Registry Manage 32: 70-75.
18. de Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, et al. (2012) Global burden of cancers attributable to infections in 2008: A review and synthetic analysis. Lancet Oncol 13: 607-615.
19. Consumption and Ethyl Carbamate. Vol 96 Lyon, France: International Agency for Research on Cancer.
20. National Cancer Institute (2013) Fact Sheet Alcohol and Cancer Risk.
21. U.S. Department of Health and Human Services.(2004) The Health Consequences of Smoking: A Report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health.
22. Rosenbaum PR, Rubin DB (1984) Reducing Bias in Observational Studies Using Sub classification on the Propensity Score. Journal of the American Statistical Association 79: 516-524.
23. Austin PC (2009) Using the Standardized Difference to Compare the Prevalence of a Binary Variable Between Two Groups in Observational Research. Communications in Statistics-Simulation and Computation 38: 1228-1234.
24. Benjamini Y, Hochberg Y (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B 57: 289-300.
25. Sahasrabuddhe VV, Gunja MZ, Graubard BI, Trabert B, Schwartz LM, et al. (2012) Nonsteroidal antiinflammatory drug use, chronic liver disease, and hepatocellular carcinoma. J Natl Cancer Inst 104: 1808-1814.
26. Grosch S, Maier TJ, Schiffmann S, Geisslinger G (2006) Cyclooxygenase-2 (COX-2)-independent anticarcinogenic effects of selective COX-2 inhibitors. J Natl Cancer Inst 98: 736-747.
27. Janssen A, Maier TJ, Schiffmann S, Coste O, Seegel M, et al. (2006) Evidence of COX-2 independent induction of apoptosis and cell cycle block in human colon carcinoma cells after S-or R-ibuprofen treatment. Eur J Pharmacol 540: 24-33.
28. Khan Z, Khan N, Tiwari RP, Sah NK, Prasad GB, et al. (2011) Biology of Cox-2: A n application in cancer therapeutics. Curr Drug Targets 12: 1082-1093.
29. Schror K (2011) Pharmacology and cellular/molecular mechanisms of action of aspirin and Non-aspirin NSAIDs in colorectal cancer. Best Pract Res Clin Gastroenterol 25: 473-484.
30. Suh N, Reddy BS, Decastro A, Paul S, Lee HJ, et al. (2011) Combination of Atorvastatin with Sulindac or Naproxen Profoundly Inhibits Colonic Adenocarcinomas by Suppressing the p65/beta-Catenin/Cyclin D1 Signaling Pathway in Rats. Cancer Prev Res (Phila) 4: 1895-1902.
31. Zaric J, Joseph JM, Tercier S, Sengstag T, Ponsonnet L, et al. (2011) Identification of MAGI1 as a tumor-suppressor protein induced by cyclooxygenase-2 inhibitors in colorectal cancer cells. Oncogene.
32. Greenspan EJ, Madigan JP, Boardman LA, Rosenberg DW (2011) Ibuprofen inhibits activation of nuclear {beta}-catenin in human colon adenomas and induces the phosphorylation of GSK-3{beta}. Cancer Prev Res (Phila) 4: 161-171.
33. Jayaprakash V, Rigual NR, Moysich KB, Loree TR, Nasca MA, et al. (2006) Chemoprevention of head and neck cancer with aspirin: A case-control study. Arch Otolaryngol Head Neck Surg 132: 1231-1236.
34. Funkhouser EM, Sharp GB (1995) Aspirin and reduced risk of esophageal carcinoma. Cancer 76: 1116-1119.
35. Bosetti C, Gallus S, La Vecchia C (2009) Aspirin and cancer risk: A summary review to 2007. Recent Results Cancer Res 181: 231-251.
36. Macfarlane TV, Macfarlane GJ, Thakker NS, Benhamou S, Bouchardy C, et al. (2012) Role of medical history and medication use in the aetiology of upper aerodigestive tract cancers in Europe: The ARCAGE study. Ann Oncol 23: 1053-1060.
37. Bosetti C, Talamini R, Franceschi S, Negri E, Garavello W, et al. (2003) Aspirin use and cancers of the upper aerodigestive tract. Br J Cancer 88: 672-674.
38. Luo T, Yan HM, He P, Luo Y, Yang YF, et al. (2011) Aspirin use and breast cancer risk: A meta-analysis. Breast Cancer Res Treat.
39. Gonzalez-Perez A, Garcia Rodriguez LA, Lopez-Ridaura R (2003) Effects of non-steroidal antiinflammatory drugs on cancer sites other than the colon and rectum: A meta-analysis. BMC Cancer 3: 28.
40. Chang ET, Cronin-Fenton DP, Friis S, Hjalgrim H, Sorensen HT, et al. (2010) Aspirin and other nonsteroidal anti-inflammatory drugs in relation to Hodgkin lymphoma risk in northern Denmark. Cancer Epidemiol Biomarkers Prev 19: 59-64.
41. Xu J, Yin Z, Gao W, Liu L, Wang R, et al. (2011) Meta-Analysis on the Association Between Nonsteroidal Anti-Inflammatory Drug Use and Lung Cancer Risk. Clin Lung Cancer.
42. Sudbo J, Lee JJ, Lippman SM, Mork J, Sagen S, et al. (2005) Non-steroidal anti-inflammatory drugs and the risk of oral cancer: A nested case-control study. Lancet 366: 1359-1366.
43. Corley DA, Kerlikowske K, Verma R, Buffler P (2003) Protective association of aspirin/NSAIDs and esophageal cancer: A systematic review and meta-analysis. Gastroenterology 124: 47-56.
44. Anderson KE, Johnson TW, Lazovich D, Folsom AR (2002) Association between non steroidal antiinflammatory drug use and the incidence of pancreatic cancer. J Natl Cancer Inst 94: 1168-1171.
45. Wilson JC, Anderson LA, Murray LJ, Hughes CM (2011) Non-steroidal anti-inflammatory drug and aspirin use and the risk of head and neck cancer: A systematic review. Cancer Causes Control 22: 803-810.
46. Schreinemachers DM, Everson RB (1994) Aspirin use and lung, colon, and breast cancer incidence in a prospective study. Epidemiology 5: 138-146.
47. Jacobs EJ, Thun MJ, Bain EB, Rodriguez C, Henley SJ, et al. (2007) A large cohort study of long-term daily use of adult-strength aspirin and cancer incidence. J Natl Cancer Inst 99: 608-615.
48. Cole BF, Logan RF, Halabi S, Benamouzig R, Sandler RS, et al. (2009) Aspirin for the chemoprevention of colorectal adenomas: meta-analysis of the randomized trials. J Natl Cancer Inst 101: 256-266.
49. Flossmann E, Rothwell PM (2007) Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies. Lancet 369: 1603-1613.
50. Bosetti C, Gallus S, La Vecchia C (2006) Aspirin and cancer risk: A n updated quantitative review to 2005. Cancer Causes Control 17: 871-888.
51. Yang P, Zhou Y, Chen B, Wan HW, Jia GQ, et al. (2010) Aspirin use and the risk of gastric cancer: A meta-analysis. Dig Dis Sci 55: 1533-1539.
52. Sun L, Yu S (2011) Meta-analysis: non-steroidal anti-inflammatory drug use and the risk of esophageal squamous cell carcinoma. Dis Esophagus 24: 544-549.
53. Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Curhan GC, et al. (2005) Long-term use of aspirin and nonsteroidal anti-inflammatory drugs and risk of colorectal cancer. JAMA 294: 914-923.
54. Wang WH, Huang JQ, Zheng GF, Lam SK, Karlberg J, et al. (2003) Non-steroidal anti-inflammatory drug use and the risk of gastric cancer: A systematic review and meta-analysis. J Natl Cancer Inst 95: 1784-1791.
55. Gao J, Niwa K, Sun W, Takemura M, Lian Z, et al. (2004) Non-steroidal anti-inflammatory drugs inhibit cellular proliferation and upregulate cyclooxygenase-2 protein expression in endometrial cancer cells. Cancer Sci 95: 901-907.
56. Wu CY, Wu MS, Kuo KN, Wang CB, Chen YJ, et al. (2010) Effective reduction of gastric cancer risk with regular use of nonsteroidal anti-inflammatory drugs in Helicobacter pylori-infected patients. J Clin Oncol 28: 2952-2957.
57. Li GQ, Xia HH, Chen MH, Tsukamoto T, Tatematsu M, et al. (2008) Effects of aspirin on the development of Helicobacter pylori-induced gastric inflammation and heterotopic proliferative glands in Mongolian gerbils. Helicobacter 13: 20-29.
58. Bardou M, Barkun AN, Ghosn J, Hudson M, Rahme E (2004) Effect of chronic intake of NSAIDs and cyclooxygenase 2-selective inhibitors on esophageal cancer incidence. Clin Gastroenterol Hepatol 2: 880-887.
59. Vaughan TL, Dong LM, Blount PL, Ayub K, Odze RD, et al. (2005) Non-steroidal anti-inflammatory drugs and risk of neoplastic progression in Barrett's oesophagus: A prospective study. Lancet Oncol 6: 945-952.
60. Chan AT, Giovannucci EL, Meyerhardt JA, Schernhammer ES, Wu K, et al. (2008) Aspirin dose and duration of use and risk of colorectal cancer in men. Gastroenterology 134: 21-28.
61. Baron JA, Cole BF, Sandler RS, Haile RW, Ahnen D, et al. (2003) A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 348: 891-899.
62. Sorensen HT, Friis S, Norgard B, Mellemkjaer L, Blot WJ, et al. (2003) Risk of cancer in a large cohort of nonaspirin NSAID users: A population-based study. Br J Cancer 88: 1687-1692.
63. Berasain C, Castillo J, Perugorria MJ, Latasa MU, Prieto J, et al. (2009) Inflammation and liver cancer: new molecular links. Ann N Y Acad Sci 1155: 206-221.
64. Tsan YT, Lee CH, Ho WC, Lin MH, Wang JD, et al. (2013) Statins and the Risk of Hepatocellular Carcinoma in Patients With Hepatitis C Virus Infection. J Clin Oncol.
65. Hossain MA, Kim DH, Jang JY, Kang YJ, Yoon JH, et al. (2012) Aspirin induces apoptosis in vitro and inhibits tumor growth of human hepatocellular carcinoma cells in a nude mouse xenograft model. Int J Oncol 40: 1298-1304.
66. Cook NR, Lee IM, Gaziano JM, Gordon D, Ridker PM, et al. (2005) Low-dose aspirin in the primary prevention of cancer: The Women's Health Study: A randomized controlled trial. JAMA 294: 47-55.
67. Hernandez-Diaz S, Garcia Rodriguez LA (2007) Nonsteroidal anti-inflammatory drugs and risk of lung cancer. Int J Cancer 120: 1565-1572.
68. Van Dyke AL, Cote ML, Prysak G, Claeys GB, Wenzlaff AS, et al. (2008) Regular adult aspirin use decreases the risk of non-small cell lung cancer among women. Cancer Epidemiol Biomarkers Prev 17: 148-157.
69. Ross JA, Blair CK, Cerhan JR, Soler JT, Hirsch BA, et al. (2011) Nonsteroidal anti-inflammatory drug and acetaminophen use and risk of adult myeloid leukemia. Cancer Epidemiol Biomarkers Prev 20: 1741-1750.
70. Kasum CM, Blair CK, Folsom AR, Ross JA (2003) Non-steroidal anti-inflammatory drug use and risk of adult leukemia. Cancer Epidemiol Biomarkers Prev 12: 534-537.
71. Singh R, Cadeddu RP, Frobel J, Wilk CM, Bruns I, et al. (2011) The non-steroidal anti-inflammatory drugs Sulindac sulfide and Diclofenac induce apoptosis and differentiation in human acute myeloid leukemia cells through an AP-1 dependent pathway. Apoptosis 16: 889-901.
72. Harris RE, Beebe-Donk J, Namboodiri KK (2001) Inverse association of non-steroidal antiinflammatory drugs and malignant melanoma among women. Oncol Rep 8: 655-657.
73. Curiel-Lewandrowski C, Nijsten T, Gomez ML, Hollestein LM, Atkins MB, et al. (2011) Long-term use of nonsteroidal anti-inflammatory drugs decreases the risk of cutaneous melanoma: results of a United States case-control study. J Invest Dermatol 131: 1460-1468.
74. Joosse A, Koomen ER, Casparie MK, Herings RM, Guchelaar HJ, et al. (2009) Non-steroidal antiinflammatory drugs and melanoma risk: large Dutch population-based case-control study. J Invest Dermatol 129: 2620-2627.
75. Johannesdottir SA, Chang ET, Mehnert F, Schmidt M, Olesen AB, et al. (2012) Nonsteroidal antiinflammatory drugs and the risk of skin cancer: A population-based case-control study. Cancer.
76. Asgari MM, Maruti SS, White E (2008) A large cohort study of non steroidal anti-inflammatory drug use and melanoma incidence. J Natl Cancer Inst 100: 967-971.
77. Jeter JM, Bonner JD, Johnson TM, Gruber SB (2011) Non steroidal anti-inflammatory drugs and risk of melanoma. J Skin Cancer 2011: 598571.
78. Viswanathan AN, Feskanich D, Schernhammer ES, Hankinson SE (2008) Aspirin, NSAID, and acetaminophen use and the risk of endometrial cancer. Cancer Res 68: 2507-2513.
79. Moysich KB, Baker JA, Rodabaugh KJ, Villella JA (2005) Regular analgesic use and risk of endometrial cancer. Cancer Epidemiol Biomarkers Prev 14: 2923-2928.
80. Prizment AE, Folsom AR, Anderson KE (2010) Non steroidal anti-inflammatory drugs and risk for ovarian and endometrial cancers in the Iowa Women's Health Study. Cancer Epidemiol Biomarkers Prev 19: 435-442.
81. Bodelon C, Doherty JA, Chen C, Rossing MA, Weiss NS (2009) Use of non steroidal anti inflammatory drugs and risk of endometrial cancer. Am J Epidemiol 170: 1512-1517.
82. Gallicchio L, Visvanathan K, Burke A, Hoffman SC, Helzlsouer KJ (2007) Nonsteroidal antiinflammatory drugs and the risk of developing breast cancer in a population-based prospective cohort study in Washington County, MD. Int J Cancer 121: 211-215.
83. Jacobs EJ, Rodriguez C, Mondul AM, Connell CJ, Henley SJ, et al. (2005) A large cohort study of aspirin and other non steroidal anti-inflammatory drugs and prostate cancer incidence. J Natl Cancer Inst 97: 975-980.
84. Rothwell PM, Fowkes FG, Belch JF, Ogawa H, Warlow CP, et al. (2011) Effect of daily aspirin on longterm risk of death due to cancer: A nalysis of individual patient data from randomised trials. Lancet 377: 31-41.