Aspirin and the risk of Hodgkin's lymphoma in a population-based case-control study

Journal of the National Cancer Institute

Volumn 96, Issue 4, 2004, Pages 305-315

  Chang, Ellen T ^a   Zheng, Tongzhang ^b   Weir, Edward G ^c   Borowitz, Michael ^c   Mann, Risa B ^c   Spiegelman, Donna ^a   Meuller, Nancy E ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DEPARTMENT OF PATHOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NONSTEROID ANTIINFLAMMATORY AGENT; PARACETAMOL; PROSTAGLANDIN; PROSTAGLANDIN SYNTHASE; TRANSCRIPTION FACTOR;

ADOLESCENT; ADULT; AGED; ARTICLE; CANCER RISK; CARCINOGENESIS; CASE CONTROL STUDY; CELL SURVIVAL; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; DRUG USE; FEMALE; GEOGRAPHY; HODGKIN DISEASE; HUMAN; IMMUNITY; LYMPHOMA CELL; MAJOR CLINICAL STUDY; MALE; POPULATION RESEARCH; PRIORITY JOURNAL; PROSTAGLANDIN SYNTHESIS INHIBITION; PROTEIN FUNCTION; RISK ASSESSMENT; SIGNAL TRANSDUCTION; STATISTICAL SIGNIFICANCE; UNITED STATES;

EID: 1342312264     PISSN: 00278874     EISSN: None     Source Type: Journal    
DOI: 10.1093/jnci/djh038     Document Type: Article

References (87)

1. IARC Working Group on the Evaluation of Cancer Preventive Agents. Non-steroidal anti-inflammatory drugs. IARC Handbooks of Cancer Prevention. Vol. 1. New York (NY): Oxford University Press; 1997. p. 1-214.
2. Thun MJ, Henley SJ, Patrono C. Nonsteroidal anti-inflammatory drugs as anticancer agents: mechanistic, pharmacologic, and clinical issues. J Natl Cancer Inst 2002;94:252-66.
3. Kune GA, Kune S, Watson LF. Colorectal cancer risk, chronic illnesses, operations, and medications: case control results from the Melbourne Colorectal Cancer Study. Cancer Res 1988;48:4399-404.
4. Isomaki HA, Hakulinen T, Joutsenlahti U. Excess risk of lymphomas, leukemia and myeloma in patients with rheumatoid arthritis. J Chronic Dis 1978;31:691-6.
5. Gann PH, Manson JE, Glynn RJ, Buring JE, Hennekens CH. Low-dose aspirin and incidence of colorectal tumors in a randomized trial. J Natl Cancer Inst 1993;85:1220-4.
6. Garcia-Rodríguez LA, Huerta-Alvarez C. Reduced risk of colorectal cancer among long-term users of aspirin and nonaspirin nonsteroidal antiinflammatory drugs. Epidemiology 2001;12:88-93.
7. Giovannucci E, Rimm EB, Stampfer MJ, Colditz GA, Ascherio A, Willett WC. Aspirin use and the risk for colorectal cancer and adenoma in male health professionals. Ann Intern Med 1994;121:241-6.
8. Giovannucci E, Egan KM, Hunter DJ, Stampfer MJ, Colditz GA, Willett WC, et al. Aspirin and the risk of colorectal cancer in women. New Engl J Med 1995;333:609-14.
9. Giovannucci E. The prevention of colorectal cancer by aspirin use. Biomed Pharmacother 1999;53:303-8.
10. Greenberg ER, Baron JA, Freeman DH Jr, Mandel JS, Haile R. Reduced risk of large-bowel adenomas among aspirin users. The Polyp Prevention Study Group. J Natl Cancer Inst 1993;85:912-6.
11. Gridley G, McLaughlin JK, Ekbom A, Klareskog L, Adami HO, Hacker DG, et al. Incidence of cancer among patients with rheumatoid arthritis. J Natl Cancer Inst 1993;85:307-11.
12. Suh O, Mettlin C, Petrelli NJ. Aspirin use, cancer, and polyps of the large bowel. Cancer 1993;72:1171-7.
13. Thun MJ, Namboodiri MM, Calle EE, Flanders WD, Heath CW Jr. Aspirin use and risk of fatal cancer. Cancer Res 1993;53:1322-7.
14. Sandler RS, Halabi S, Baron JA, Budinger S, Paskett E, Keresztes R, et al. A randomized trial of aspirin to prevent colorectal adenomas in patients with previous colorectal cancer [published erratum appears in N Engl J Med 2003;348:1939]. N Engl J Med 2003;348:883-90.
15. Baron JA, Cole BF, Sandler RS, Haile RW, Ahnen D, Bresalier R, et al. A randomized trial of aspirin to prevent colorectal adenomas. N Engl J Med 2003;348:891-9.
16. Schreinemachers DM, Everson RB. Aspirin use and lung, colon, and breast cancer incidence in a prospective study. Epidemiology 1994;5:138-46.
17. Sharp L, Chilvers CE, Cheng KK, McKinney PA, Logan RF, Cook-Mozaffari P, et al. Risk factors for squamous cell carcinoma of the oesophagus in women: a case-control study. Br J Cancer 2001;85:1661-70.
18. Farrow DC, Vaughan TL, Hansten PD, Stanford JL, Risch HA, Gammon MD, et al. Use of aspirin and other nonsteroidal anti-inflammatory drugs and risk of esophageal and gastric cancer. Cancer Epidemiol Biomarkers Prev 1998;7:97-102.
19. Funkhouser EM, Sharp GB. Aspirin and reduced risk of esophageal carcinoma. Cancer 1995;76:1116-9.
20. Ohki S, Ogino N, Yamamoto S, Hayaishi O. Prostaglandin hydroperoxidase, an integral part of prostaglandin endoperoxide synthetase from bovine vesicular gland microsomes. J Biol Chem 1979;254:829-36.
21. Picot D, Loll PJ, Garavito RM. The X-ray crystal structure of the membrane protein prostaglandin H2 synthase-1. Nature 1994;367:243-9.
22. Loll PJ, Picot D, Garavito RM. The structural basis of aspirin activity inferred from the crystal structure of inactivated prostaglandin H2 synthase. Nat Struct Biol 1995;2:637-43.
23. Lupulescu A. Effect of prostaglandins on protein, RNA, DNA and collagen synthesis in experimental wounds. Prostaglandins 1975;10:573-9.
24. Lupulescu AP. Cytologic and metabolic effects of prostaglandins on rat skin. J Invest Dermatol 1977;68:138-45.
25. Lupulescu A. Enhancement of carcinogenesis by Prostaglandins in male albino Swiss mice. J Natl Cancer Inst 1978;61:97-106.
26. Lupulescu A. Enhancement of carcinogenesis by Prostaglandins. Nature 1978;272:634-6.
27. Goodwin JS, Messner RP, Bankhurst AD, Peake GT, Saiki JH, Williams RC Jr. Prostaglandin-producing suppressor cells in Hodgkin's disease. N Engl J Med 1977;297:963-8.
28. Sébahoun G, Maraninchi D, Carcassonne Y. Increased prostaglandin E production in malignant lymphomas. Acta Haematol 1985;74:132-6.
29. Cayeux SJ, Beverley PC, Schulz R, Dorken B. Elevated plasma prostaglandin E2 levels found in 14 patients undergoing autologous bone marrow or stem cell transplantation. Bone Marrow Transplant 1993;12:603-8.
30. Hsu SM, Hsu PL, Lo SS, Wu KK. Expression of prostaglandin H synthase (cyclooxygenase) in Hodgkin's mononuclear and Reed-Sternberg cells. Functional resemblance between H-RS cells and histiocytes or interdigitating reticulum cells. Am J Pathol 1988;133:5-12.
31. Santoro MG, Philpott GW, Jaffe BM. Inhibition of tumour growth in vivo and in vitro by prostaglandin E. Nature 1976;263:777-9.
32. Tutton PJ, Barkla DH. Influence of prostaglandin analogues on epithelial cell proliferation and xenograft growth. Br J Cancer 1980;41:47-51.
33. Craven PA, Saito R, DeRubertis FR. Role of local prostaglandin synthesis in the modulation of proliferative activity of rat colonic epithelium. J Clin Invest 1983;72:1365-75.
34. de Mello MC, Bayer BM, Beaven MA. Evidence that prostaglandins do not have a role in the cytostatic action of anti-inflammatory drugs. Biochem Pharmacol 1980;29:311-8.
35. Elder DJ, Hague A, Hicks DJ, Paraskeva C. Differential growth inhibition by the aspirin metabolite salicylate in human colorectal tumor cell lines: enhanced apoptosis in carcinoma and in vitro-transformed adenoma relative to adenoma relative to adenoma cell lines. Cancer Res 1996;56: 2273-6.
36. Hanif R, Pittas A, Feng Y, Koutsos MI, Qiao L, Staiano-Coico L, et al. Effects of nonsteroidal anti-inflammatory drugs on proliferation and on induction of apoptosis in colon cancer cells by a prostaglandin-independent pathway. Biochem Pharmacol 1996;52:237-45.
37. Amann R, Peskar BA. Anti-inflammatory effects of aspirin and sodium salicylate. Eur J Pharmacol 2002;447:1-9.
38. Ebisuzaki K. Aspirin and methylsulfonylmethane (MSM): a search for common mechanisms, with implications for cancer prevention. Anticancer Res 2003;23:453-8.
39. Baeuerle PA, Baltimore D. NF-kappa B: ten years after. Cell 1996;87:13-20.
40. Baldwin AS Jr. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu Rev Immunol 1996;14:649-83.
41. Degitz K, Li LJ, Caughman SW. Cloning and characterization of the 5′-transcriptional regulatory region of the human intercellular adhesion molecule 1 gene. J Biol Chem 1991;266:14024-30.
42. Neish AS, Williams AJ, Palmer HJ, Whitley MZ, Collins T. Functional analysis of the human vascular cell adhesion molecule 1 promoter. J Exp Med 1992;176:1583-93.
43. Caamano J, Hunter CA. NF-kappaB family of transcription factors: central regulators of innate and adaptive immune functions. Clin Microbiol Rev 2002;15:414-29.
44. Karin M, Cao Y, Greten FR, Li ZW. NF-kappaB in cancer: from innocent bystander to major culprit. Nat Rev Cancer 2002;2:301-10.
45. Bargou RC, Emmerich F, Krappmann D, Bommert K, Mapara MY, Arnold W, et al. Constitutive nuclear factor-kappaB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J Clin Invest 1997;100:2961-9.
46. Izban KF, Ergin M, Huang Q, Qin JZ, Martinez RL, Schnitzer B, et al. Characterization of NF-kappaB expression in Hodgkin's disease: inhibition of constitutively expressed NF-kappaB results in spontaneous caspase-independent apoptosis in Hodgkin and Reed-Sternberg cells. Mod Pathol 2001;14:297-310.
47. Hinz M, Loser P, Mathas S, Krappmann D, Dorken B, Scheidereit C. Constitutive NF-kappaB maintains high expression of a characteristic gene network, including CD40, CD86, and a set of antiapoptotic genes in Hodgkin/Reed-Sternberg cells. Blood 2001;97:2798-807.
48. Anagnostopoulos I, Herbst H, Niedobitek G, Stein H. Demonstration of monoclonal EBV genomes in Hodgkin's disease and Ki-1-positive anaplastic large cell lymphoma by combined Southern blot and in situ hybridization. Blood 1989;74:810-6.
49. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Epstein-Barr virus and Kaposi's sarcoma herpesvirus/human herpesvirus 8. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Vol. 70. Lyon (France): IARC Press; 1997. p. 1-524.
50. Weiss LM, Movahed LA, Warnke RA, Sklar J. Detection of Epstein-Barr viral genomes in Reed-Sternberg cells of Hodgkin's disease. N Engl J Med 1989;320:502-6.
51. Rickinson AB, Kieff E. Epstein-Barr virus. In: Fields BN, Knipe DM, Howley PM, editors. Fields virology. 3rd ed. Philadelphia (PA): Lippencott-Raven; 1996. p. 2397-446.
52. Murray PG, Young LS. The role of the Epstein-Barr virus in human disease. Front Biosci 2002;7:d519-40.
53. Sugano N, Chen W, Roberts ML, Cooper NR. Epstein-Barr virus binding to CD21 activates the initial viral promoter via NF-kappaB induction. J Exp Med 1997;186:731-7.
54. Bargou RC, Leng C, Krappmann D, Emmerich F, Mapara MY, Bommert K, et al. High-level nuclear NF-kappa B and Oct-2 is a common feature of cultured Hodgkin/Reed-Sternberg cells. Blood 1996;87:4340-7.
55. Horie R, Higashihara M, Watanabe T. Hodgkin's lymphoma and CD30 signal transduction. Int J Hematol 2003;77:37-47.
56. Staudt LM. The molecular and cellular origins of Hodgkin's disease. J Exp Med 2000;191:207-12.
57. Bohlke K, Harlow BL, Cramer DW, Spiegelman D, Mueller NE. Evaluation of a population roster as a source of population controls: the Massachusetts Resident Lists. Am J Epidemiol 1999;150:354-8.
58. United States Census Bureau. Census 2000 Data for the State of Connecticut. 20 August 2002. Vol 2002: U.S. Department of Commerce; 2002. Available at http://www.census.gov/census2000/states/ct.html. [Last accessed: December 24, 2002.]
59. Waksberg J. Sampling methods for random digit dialing. J Am Stat Assoc 1978;73:40-6.
60. United States Federal Financial Institutions Examination Council (FFIEC). FFIEC Geocoding System. 26 July 2002. Available at http://www.ffiec.gov/geocode/default.htm. [Last accessed: December 24, 2002.]
61. Harris NL, Jaffe ES, Diebold J, Flandrin G, Muller-Hermelink HK, Vardiman J, et al. The World Health Organization classification of hematological malignancies report of the Clinical Advisory Committee Meeting, Airlie House, Virginia, November 1997. Mod Pathol 2000;13:193-207.
62. Pathology and genetics of tumours of haematopoietic and lymphoid tissues. World Health Organization Classification of Tumours. Jaffe ES, Harris NL, Stein H, Voordiman JN, editors. Lyon (France): IARC Press; 2001. p. 237-53.
63. Staal SP, Ambinder R, Beschorner WE, Hayward GS, Mann R. A survey of Epstein-Barr virus DNA in lymphoid tissue. Frequent detection in Hodgkin's disease. Am J Clin Pathol 1989;91:1-5.
64. Ambinder RF, Mann RB. Epstein-Barr-encoded RNA in situ hybridization: diagnostic applications. Hum Pathol 1994;25:602-5.
65. Gulley ML, Glaser SL, Craig FE, Borowitz M, Mann RB, Shema SJ, et al. Guidelines for interpreting EBER in situ hybridization and LMP1 immunohistochemical tests for detecting Epstein-Barr virus in Hodgkin lymphoma. Am J Clin Pathol 2002;117:259-67.
66. Greenland S. Modeling and variable selection in epidemiologic analysis. Am J Public Health 1989;79:340-9.
67. Kleinbaum DG, Kupper LL, Morgenstern H. Epidemiologic research: principles and quantitative methods. Belmont (CA): Lifetime Learning Publications; 1992. p. 194-219.
68. Gutensohn NM. Social class and age at diagnosis of Hodgkin's disease: new epidemiologic evidence for the "two-disease hypothesis". Cancer Treat Rep 1982;66:689-95.
69. Alexander FE, McKinney PA, Williams J, Ricketts TJ, Cartwright RA. Epidemiological evidence for the 'two-disease hypothesis' in Hodgkin's disease. Int J Epidemiol 1991;20:354-61.
70. Grilli M, Pizzi M, Memo M, Spano P. Neuroprotection by aspirin and sodium salicylate through blockade of NF-kappaB activation. Science 1996;274:1383-5.
71. Kopp E, Ghosh S. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 1994;265:956-9.
72. Yin MJ, Yamamoto Y, Gaynor RB. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta. Nature 1998; 396:77-80.
73. Van Der Ouderaa FJ, Buytenhek M, Nugteren DH, Van Dorp DA. Acetylation of prostaglandin endoperoxide synthetase with acetylsalicylic acid. Eur J Biochem 1980;109:1-8.
74. Meade EA, Smith WL, DeWitt DL. Differential inhibition of prostaglandin endoperoxide synthase (cyclooxygenase) isozymes by aspirin and other non-steroidal anti-inflammatory drugs. J Biol Chem 1993;268:6610-4.
75. Laneuville O, Breuer DK, Dewitt DL, Hla T, Funk CD, Smith WL. Differential inhibition of human prostaglandin endoperoxide H synthases-1 and -2 by nonsteroidal anti-inflammatory drugs. J Pharmacol Exp Ther 1994;271:927-34.
76. Gierse JK, Hauser SD, Creely DP, Koboldt C, Rangwala SH, Isakson PC, et al. Expression and selective inhibition of the constitutive and inducible forms of human cyclo-oxygenase. Biochem J 1995;305:479-84.
77. Nelson M. Childhood nutrition and poverty. Proc Nutr Soc 2000;59:307-15.
78. Hess FI, Nukuro E, Judson L, Rodgers J, Nothdurft HD, Rieckmann KH. Anti-malarial drug resistance, malnutrition and socio-economic status. Trop Med Int Health 1997;2:721-8.
79. Signorello LB, McLaughlin JK, Lipworth L, Friis S, Sorensen HT, Blot WJ. Confounding by indication in epidemiologic studies of commonly used analgesics. Am J Ther 2002;9:199-205.
80. McLaughlin JK, Blot WJ, Mehl ES, Fraumeni JF Jr. Relation of analgesic use to renal cancer: population-based findings. Natl Cancer Inst Monogr 1985;69:217-22.
81. Piper JM, Tonascia J, Matanoski GM. Heavy phenacetin use and bladder cancer in women aged 20 to 49 years. N Engl J Med 1985;313:292-5.
82. Derby LE, Jick H. Acetaminophen and renal and bladder cancer. Epidemiology 1996;7:358-62.
83. Gago-Dominguez M, Yuan JM, Castelao JE, Ross RK, Yu MC. Regular use of analgesics is a risk factor for renal cell carcinoma. Br J Cancer 1999;81:542-8.
84. Kaye JA, Myers MW, Jick H. Acetaminophen and the risk of renal and bladder cancer in the general practice research database. Epidemiology 2001;12:690-4.
85. Friis S, Nielsen GL, Mellemkjaer L, McLaughlin JK, Thulstrup AM, Blot WJ, et al. Cancer risk in persons receiving prescriptions for paracetamol: a Danish cohort study. Int J Cancer 2002;97:96-101.
86. Cramer DW, Harlow BL, Titus-Ernstoff L, Bohlke K, Welch WR, Greenberg ER. Over-the-counter analgesics and risk of ovarian cancer. Lancet 1998;351:104-7.
87. Moysich KB, Mettlin C, Piver MS, Natarajan N, Menezes RJ, Swede H. Regular use of analgesic drugs and ovarian cancer risk. Cancer Epidemiol Biomarkers Prev 2001;10:903-6.