Skip to main content
Log in

A case–control study of tobacco use and other non-occupational risk factors for t(14;18) subtypes of non-Hodgkin's lymphoma (United States)

  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

Abstract

Objective: Non-Hodgkin's lymphoma (NHL) encompasses diverse subtypes, and analyzing NHL as a single outcome may mask associations. In a new approach we evaluated associations with subtypes defined by the t(14;18) translocation, reasoning that cases within these subtypes would have more common risk factors than all NHL Combined. Methods: Archival biopsies from cases in a population-based NHL study were assayed for t(14;18) using polymerase chain reaction amplification. Exposures in 68 t(14;18)-positive and 114-negative cases were compared with 1245 controls. The expectation–maximization algorithm was used to fit polytomous regression models based on all available information, including data from 440 unclassified cases. Results: Family history of hemolymphatic cancer was associated with t(14;18)-negative NHL (odds ratio (OR) 2.4, 95% confidence interval (CI) 1.4–3.9), but not t(14;18)-positive NHL. Cigarette smoking was weakly associated with t(14;18)-positive NHL (OR 1.7, CI 0.9–3.3), but ORs decreased as smoking increased. Chewing tobacco was associated with t(14;18)-positive NHL, particularly when used before age 18 (OR 2.5, CI 1.0–6.0, 13 exposed cases). Odds ratios for both case-subtypes were doubled among hair-dye users. Conclusions: Cigarette smoking was not clearly associated with t(14;18)-positive NHL. Family history may be a marker for factors that act specifically through t(14;18)-negative pathogenic mechanisms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Magrath I (1992) Molecular basis of lymphomagenesis. Cancer Res 52s: 5529s.

    Google Scholar 

  2. Jaffe ES, Raffeld M, Medeiros L, Stetler-Stevenson M (1992) An overview of the classification of non-Hodgkin's lymphomas: an integration of morphological and phenotypical concepts. Cancer Res 52s: 5447s-5452s.

    Google Scholar 

  3. Weisenburger D (1992) Pathological classification of non-Hodgkin's lymphoma for epidemiological studies. Cancer Res 52s: 5456s.

    Google Scholar 

  4. Herrinton L (1998) Epidemiology of the Revised European-American Lymphoma classification subtypes. Epidemiol Rev 20: 187–203.

    Google Scholar 

  5. Potter M (1992) Pathogenetic mechanisms in B-cell non-Hodgkin's lymphoma in humans. Cancer Res 52s: 5522s-5528s.

    Google Scholar 

  6. Weiss N, Liff J (1983) Accounting for the multicausal nature of disease in the design and analysis of epidemiologic studies. Am J Epidemiol 117: 14–18.

    Google Scholar 

  7. Brown L, Everett G, Gibson R, Burmeister L, Schuman L, Blair A (1992) Smoking and risk of non-Hodgkin's lymphoma and multiple myeloma. Cancer Causes Control 3: 49–55.

    Google Scholar 

  8. Herrinton L, Friedman G (1998) Cigarette smoking and risk of non-Hodgkin's lymphoma subtypes. Cancer Epidemiol Biomarkers Prev 7: 25–28.

    Google Scholar 

  9. Freedman D, Tolbert P, Coates R, Brann E, Kjeldsberg C (1998) Relation of cigarette smoking to non-Hodgkin's lymphoma among middle-aged men. Am J Epidemiol 148: 833–841.

    Google Scholar 

  10. Zahm S, Weisenburger D, Holmes F, Cantor K, Blair A (1998) Tobacco and non-Hodgkin's lymphoma: combined analysis of three case-control studies (United States). Cancer Causes Control 8: 159–166.

    Google Scholar 

  11. Tatham L, Tolbert P, Kjeldsberg C (1997) Occupational risk factors for subgroups of non-Hodgkin's lymphoma. Epidemiology 8: 551–558.

    Google Scholar 

  12. Scherr PA, Hutchinson G, Neiman R (1992) Non-Hodgkin's lymphoma and occupational exposure. Cancer Res 52s: 5503s-5509s.

    Google Scholar 

  13. Cleary M, Smith S, Sklar J (1986) Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2/immunoglobulin transcript resulting from the t(14;18) translocation. Cell 47: 19–28.

    Google Scholar 

  14. Tsujimoto Y, Croce C (1986) Analysis of the structure, transcripts, and protein products of bcl-2, the gene involved in human follicular lymphoma. Proc Natl Acad Sci USA 83: 5214–5218.

    Google Scholar 

  15. Bakhshi A, Wright J, Graininger W, et al. (1987) Mechanism of the t(14;18) chromosomal translocation: structural analysis of both derivative 14and 18 reciprocal partners. Proc Natl Acad Sci USA 84: 2396–2400.

    Google Scholar 

  16. McDonnell T, Deane N, Platt F, et al. (1989) bcl-2–immunoglobulin transgenic mice demonstrate extended B-cell survival and follicular lymphoproliferation. Cell 57: 79–88.

    Google Scholar 

  17. Cantor K, Blair A, Everett G, et al. (1992) Pesticides and other agricultural risk factors for non-Hodgkin's lymphoma among men in Iowa and Minnesota. Cancer Res 52: 2447.

    Google Scholar 

  18. Blair A, Linos A, Stewart P, et al. (1993) Evaluation of risks for non-Hodgkin's lymphoma by occupation and industry exposures from a case-control study. Am J Ind Med 23: 301–312.

    Google Scholar 

  19. Harris N, Jaffe E, Stein H, et al. (1994) A revised European-American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood 84: 1361–1392.

    Google Scholar 

  20. Crescenzi M, Seto M, Herzig G, Weiss P, Griffith R, Korsmeyer S (1988) Thermostable DNA polymerase chain amplification of t(14;18) chromosome breakpoints and detection of minimal residual disease. Proc Natl Acad Sci USA 85: 4869–4873.

    Google Scholar 

  21. Liu J, Johnson R, Traweek S (1993) Rearrangement of the BCL-2 gene in follicular lymphoma. Detection by PCR in both fresh and fixed tissue samples. Diag Mol Pathol 2: 241–247.

    Google Scholar 

  22. StataCorp (1999) Stata Statistical Software, 6.0 ed. College Station, TX: Stata Corporation.

  23. Rubin D (1976) Inference and missing data. Biometrika 63: 581–592.

    Google Scholar 

  24. Dempster A, Laird N, Rubin D (1977) Maximum likelihood from incomplete data via the EM algorithm. J R Stat Soc B 39: 1–38.

    Google Scholar 

  25. Schroeder J, Weinberg C (2001) Use of missing-data methods to correct bias and improve precision in case-control studies where cases are subtyped but subtype information is incomplete. Am J Epidemiol 154: 954–962.

    Google Scholar 

  26. Dubin N, Pasternack B (1986) Risk assessment for case-control subgroups by polychotomous logistic regression. Am J Epidemiol 123: 1101–1017.

    Google Scholar 

  27. Greenland S (1995) Dose-response and trend analysis in epidemiology: alternatives to categorical analysis. Epidemiology 6: 356–365.

    Google Scholar 

  28. Schroeder J, Olshan A, Baric R, et al. (2001) Agricultural risk factors for t(14;18) subtypes of non-Hodgkin's lymphoma. Epidemiology 12: 701–709.

    Google Scholar 

  29. Greenland S, Rothman K (1998) Concepts of interaction. In: Rothman K, Greenland S, eds. Modern Epidemiology, 2nd edn. Philadelphia: Lippincott-Raven, pp. 329–342.

    Google Scholar 

  30. Fifth International Workshop on Chromosomes in Leukemia-Lymphoma (1987) Correlation of chromosome abnormalities with histologic and immunologic characteristics in non-Hodgkin's lymphoma and adult T cell leukemia-lymphoma. Blood 70: 1554–1564.

    Google Scholar 

  31. Pezzella F, Ralfkiaer E, Gatter K, Mason D (1990) The 14;18 translocation in European cases of follicular lymphoma: compar-Non-occupational factors and t(14;18) NHL subtypes 167 ison of Southern blotting and the polymerase chain reaction. Br J Haematol 76: 58–64.

    Google Scholar 

  32. Pottern LM, Linet M, Blair A, et al. (1991) Familial cancers associated with subtypes of leukemia and non-Hodgkin's lymphoma. Leuk Res 15: 305–314.

    Google Scholar 

  33. Cantor K, Blair A, Everett G, et al. (1988) Hair dye use and risk of leukemia and lymphoma. Am J Public Health 78: 570–571.

    Google Scholar 

  34. Paffenbarger R, Wing A, Hyde R (1978) Characteristics in youth predictive of adult-onset malignant lymphomas, melanomas, and leukemias: brief communication. J Natl Cancer Inst 60: 89–92.

    Google Scholar 

  35. Linet MS, McLaughlin JK, Hsing AW, et al. (1992) Is cigarette smoking a risk factor for non-Hodgkin's lymphoma or multiple myeloma? Results from the Lutheran Brotherhood Cohort Study. Leuk Res 16: 621–624.

    Google Scholar 

  36. Franceschi A, Serraino D, Bidoli E, et al. (1989) The epidemiology of non-Hodgkin's lymphoma in the north-east of Italy: a hospitalbased case-control study. Leuk Res 13: 465–472.

    Google Scholar 

  37. Parker AS, Cerhan JR, Dick F, et al. (2000) Smoking and risk of non-Hodgkin lymphoma subtypes in a cohort of older women. Leuk Lymphoma 37: 341–349.

    Google Scholar 

  38. Bell D, Liu Y, Cortopassi G (1995) Occurrence of bcl-2 oncogene translocation with increased frequency in the peripheral blood of heavy smokers. J Natl Cancer Inst 87: 223–224.

    Google Scholar 

  39. Gordis L (1982) Should dead cases be matched to dead controls? Am J Epidemiol 115: 1–5.

    Google Scholar 

  40. McLaughlin J, Blot W, Mehl E, Mandel J (1985) Problems in the use of dead controls in case-control studies. I. General results. Am J Epidemiol 121: 131–139.

    Google Scholar 

  41. Centers for Disease Control and Prevention (2000) Youth Risk Behavior Surveillance-United States, 1999. MMWR 49(SS-5).

  42. Zahm SH, Weisenburger D, Babbitt P, Saal R, Vaught J, Blair A (1992) Use of hair coloring products and the risk of lymphoma, multiple myeloma, and chronic lymphocytic leukemia. Am J Public Health 82: 990–997.

    Google Scholar 

  43. Altekruse SF, Henley SJ, Thun MJ (1999) Deaths from hematopoietic and other cancers in relation to permanent hair dye use in a large prospective study (United States). Cancer Causes Control 10: 617–625.

    Google Scholar 

  44. Grodstein F, Hennekens C, Colditz G, Hunter D, Stampfer M (1994) A prospective study of permanent hair dye use and hematopoeitic cancer. J Natl Cancer Inst 86: 1466–1470.

    Google Scholar 

  45. La Vecchia C, Tavani A (1995) Epidemiological evidence on hair dyes and the risk of cancer in humans. Eur J Cancer Prevention 4: 31–43.

    Google Scholar 

  46. Linet MS, Pottern L (1992) Familial aggregation of hematopoietic malignancies and risk of non-Hodgkin's lymphoma. Cancer Res 52s: 5468s-5473s.

    Google Scholar 

  47. Filipovich A, Mathur A, Kamat D, Shapiro R (1992) Primary immunodeficiencies: genetic risk factors for lymphoma. Cancer Res 52s: 5645s-5467s.

    Google Scholar 

  48. Levine A (1992) Acquired immunodeficiency syndrome-related lymphoma. Blood 80: 8–20.

    Google Scholar 

  49. Ho M, Miller G, Atchison RW, et al. (1985) Epstein-Barr virus infections and DNA hybridization studies in posttransplantation lymphoma and lymphoproliferative lesions: the role of primary infection. J Infect Dis 152: 876–886.

    Google Scholar 

  50. Henderson S, Rowe M, Gregory C, et al. (1991) Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 65: 1107–1115.

    Google Scholar 

  51. Cantor K (1982) Farming and mortality from non-Hodgkin's lymphoma: a case-control study. Int J Cancer 29: 239–247.

    Google Scholar 

  52. Biggar R, Melbye M (1996) Marital status in relation to Kaposi's sarcoma, non-Hodgkin's lymphoma, and anal cancer in the pre-AIDS era. J Acquired Immune Def Syndromes Human Retrovirol 11: 178–182.

    Google Scholar 

  53. Nelson RA, Levine AM, Marks G, Bernstein L (1997) Alcohol, tobacco, and recreational drug use and the risk of non-Hodgkin's lymphoma. Br J Cancer 76: 1532–1537.

    Google Scholar 

  54. Gail M, Pluda J, Rabkin C, et al. (1991) Projections of the incidence of non-Hodgkin's lymphoma related to acquired immunodeficiency syndrome. J Natl Cancer Inst 83: 695–701.

    Google Scholar 

  55. Harnly M, Swan S, Holly E, Kelter A, Padian N (1988) Temporal trends in the incidence of non-Hodgkin's lymphoma and selected malignancies in a population with a high incidence of acquired immunodeficiency syndrome (AIDS).AmJ Epidemiol 128: 261–267.

    Google Scholar 

  56. Horsman D, Gascoyne R, Coupland R, Coldman A, Adomat S (1995) Comparison of cytogenetic analysis Southern analysis, and polymerase chain reaction for the detection of t(14;18) in follicular lymphoma. Am J Clin Pathol 103: 472–478.

    Google Scholar 

  57. Turner GE, Ross F, Krajewski A (1995) Detection of t(14;18) in British follicular lymphoma using cytogenetics, Southern blotting, and the polymerase chain reaction. Br J Haematol 89: 223–225.

    Google Scholar 

  58. Pezzella F, Jones M, Ralfkiaer E, Ersboll J, Gatter K, Mason D (1992) Evaluation of bcl-2 protein expression and 14;18 translocation as prognostic markers in follicular lymphoma. Br J Cancer 65: 87–89.

    Google Scholar 

  59. Galoin S, Al Saati T, Schlaifer D, Huynh A, Attal M, Delsol G (1996) Oligonucleotide clonospecific probes directed against the functional sequence of t(14;18): a new tool for the assessment of minimal residual disease in follicular lymphomas. Br J Hematol 94: 676–684.

    Google Scholar 

  60. Miettinen M, Lasota J (1997) Polymerase chain reaction based gene rearrangement studies in the diagnosis of follicular lymphoma-performance in formaldehyde-fixed tissue and application in clinical problem cases. Pathol Res Pract 193: 9–19.

    Google Scholar 

  61. Corbally N, Grogan L, Devan P, Carney D (1992) The detection of specific gene rearrangements in non-Hodgkin's lymphoma using the polymerase chain reaction. Br J Cancer 66: 805–809.

    Google Scholar 

  62. Clark HM, Jones DB, Wright DH (1992) Cytogenetic and molecular studies of t(14;18) and t(14;19) in nodal and extra-nodal B-cell lymphoma. J Pathol 166: 129–137.

    Google Scholar 

  63. Lee K (1993) Investigation of bcl-2 rearrangements in a United Kingdom series of low and high grade non-Hodgkin's lymphomas. Leuk Lymphoma 11: 91.

    Google Scholar 

  64. Levine E, Arthur D, Frizzera G, Peterson B, Hurd D, Bloomfield C (1985) There are differences in cytogenetic abnormalities among histologic subtypes of the non-Hodgkin's lymphomas. Blood 66: 1414–1422.

    Google Scholar 

  65. Yunis J, Frizzera G, Oken M, McKenna J, Theologides A, Arnesen M (1987) Multiple recurrent genomic defects in follicular lymphoma. N Engl J Med 316: 79–84.

    Google Scholar 

  66. Blair A, Zahm S (1993) Patterns of pesticide use among farmers: implications for epidemiologic research. Epidemiology 4: 55–62.

    Google Scholar 

  67. Blair A, Zahm SH (1990) Methodologic issues in exposure assessment for case-control studies of cancer and herbicides. Am J Ind Med 18: 285–293.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schroeder, J., Olshan, A., Baric, R. et al. A case–control study of tobacco use and other non-occupational risk factors for t(14;18) subtypes of non-Hodgkin's lymphoma (United States). Cancer Causes Control 13, 159–168 (2002). https://doi.org/10.1023/A:1014397920185

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014397920185

Navigation