Skip to main content
Log in

Relationship among metabolizing genes, smoking and alcohol used as modifier factors on prostate cancer risk: Exploring some gene–gene and gene–environment interactions

  • Genetic Epidemiology
  • Published:
European Journal of Epidemiology Aims and scope Submit manuscript

Abstract

Background: Prostate cancer (PCa) is one of the most common male cancers, but the burden of this disease shows remarkable worldwide variation. The role of susceptibility low penetrance genes and environmental factors in the etiology of (PCa) is unclear, but may involve, in some cases, multiple alleles at multiple loci and environmental factors. Study Objectives: To assess whether CYP1A1, GSTM1, GSTT1 susceptibility genotypes, smoking status and alcohol consumption factors contribute to PCa risk, gene–gene and gene–environment interactions were analyzed. Design and Participants: We explored interactions on a multiplicative scale conducting a population-based case–control and a case–only study on 103 incident PCa patients and 132 unrelated controls. Main Results: The interaction odds ratios (IOR) for PCa risk were increased in men who had both susceptibility genotypes GST (M1; T1) null and CYP1A1-M1* in a case–control and case-only design (IORcc: 1.11; 95% CI: 0.12–10.02; IORcc: 6.23; 95%, CI: 0.51–75.89; IORco: 2.80; 95% CI: 0.44–17.45 and IORco: 2.65; 95%, CI: 0.30–25.40). No clear evidence for interaction on a multiplicative scale between smoking status, alcohol consumption and genetic polymorphisms in PCa risk was observed. Conclusions: Our findings suggest that the interaction between genetic polymorphisms in GST (T1; M1) and CYP1A1-M1* would play a significant role as a modifying factor on PCa risk in Chilean people. However, these preliminary exploratory results should be confirmed in a larger study.

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

  • KC Chu RE Tarone HP Freeman (2003) ArticleTitleTrends in prostate cancer mortality among black men and white men in the United States Cancer 97 1507–1516 Occurrence Handle10.1002/cncr.11212 Occurrence Handle12627516

    Article  PubMed  Google Scholar 

  • PH Gann (2002) ArticleTitleRisk factors for prostate cancer. Rev Urol 4 S3–S10 Occurrence Handle16986064

    PubMed  Google Scholar 

  • INE. Anuario de Estadísticas Vitales.: Instituto Nacional de Estadísticas, Gobierno de Chile, Ministerio de Salud. Servicio de Registro Civil e Identificación 2002; 246.

  • Trucco C. Tamizaje o Screening en Cancer de Prostata, Boletín Escuela de Medicina, Pontificia Universidad Católica de Chile 1998; 27: 94–96.

  • L Martínez (1995) ArticleTitleEvaluación longitudinal y predicción de tasas de defunción por cáncer prostático en Chile. Rev Chil Urol 60 56–59

    Google Scholar 

  • Corti D, Fonerón A, Troncoso L, Ebel L, Marchetti P, Muñoz N. Epidemiología del Cáncer de Próstata. Provincia de Valdivia, 1990–2000. Rev Chil Urol 2002: 67.

  • J Szot (2003) ArticleTitleAnálisis epidemiológico de la mortalidad por tumores sólidos en la Región Metropolitana, Chile, 1999. Rev Méd Chil 131 641–649 Occurrence Handle12942592

    PubMed  Google Scholar 

  • BA Verhage LA Kiemeney (2003) ArticleTitleInherited predisposition to prostate cancer Eur J Epidemiol 18 1027–1036 Occurrence Handle10.1023/A:1026101914592 Occurrence Handle14620936

    Article  PubMed  Google Scholar 

  • WG Nelson AM De Marzo WB Isaacs (2003) ArticleTitleProstate cancer N Engl J Med 349 366–381 Occurrence Handle10.1056/NEJMra021562 Occurrence Handle1:CAS:528:DC%2BD3sXls1Sntrg%3D Occurrence Handle12878745

    Article  CAS  PubMed  Google Scholar 

  • SS Coughlin IJ Hall (2002) ArticleTitleA review of genetic polymorphisms and prostate cancer risk. Ann Epidemiol 12 182–196 Occurrence Handle10.1016/S1047-2797(01)00310-6 Occurrence Handle11897176

    Article  PubMed  Google Scholar 

  • WW Au (2001) ArticleTitleLife style factors and acquired susceptibility to environmental disease Int J Hyg Environ Health 204 17–22 Occurrence Handle11725340 Occurrence Handle1:STN:280:DC%2BD3MnnvF2isg%3D%3D

    PubMed  CAS  Google Scholar 

  • P Lichtenstein NV Holm PK Verkasalo et al. (2000) ArticleTitleEnvironmental and heritable factors in the causation of cancer–analyses of cohorts of twins from Sweden, Denmark, and Finland N Engl J Med 343 78–85 Occurrence Handle10.1056/NEJM200007133430201 Occurrence Handle1:STN:280:DC%2BD3czjtFCiug%3D%3D Occurrence Handle10891514

    Article  CAS  PubMed  Google Scholar 

  • RB Hayes (2001) ArticleTitleGene–environment interrelations in prostate cancer Epidemiol Rev 23 163–167 Occurrence Handle11588843 Occurrence Handle1:STN:280:DC%2BD3Mrkt1Sksw%3D%3D

    PubMed  CAS  Google Scholar 

  • P Vineis (2002) ArticleTitleThe relationship between polymorphisms of xenobiotic metabolizing enzymes and susceptibility to cancer Toxicology 181–182 457–462 Occurrence Handle10.1016/S0300-483X(02)00450-X Occurrence Handle12505352

    Article  PubMed  Google Scholar 

  • DW Nebert RA McKinnon A Puga (1996) ArticleTitleHuman drug-metabolizing enzyme polymorphisms: Effects on risk of toxicity and cancer DNA Cell Biol 15 273–280 Occurrence Handle8639263 Occurrence Handle1:CAS:528:DyaK28XitlCms7k%3D Occurrence Handle10.1089/dna.1996.15.273

    Article  PubMed  CAS  Google Scholar 

  • A Hirvonen K Husgafvel-Pursiainen S Anttila A Karjalainen H Vainio (1993) ArticleTitlePolymorphism in CYP1A1 and CYP2D6 genes: Possible association with susceptibility to lung cancer. Environ Health Perspect 101 IssueID(Suppl 3) 109–112 Occurrence Handle7908263 Occurrence Handle1:CAS:528:DyaK2cXhs1Sitro%3D

    PubMed  CAS  Google Scholar 

  • FP Guengerich T Shimada KD Raney et al. (1992) ArticleTitleElucidation of catalytic specificities of human cytochrome P450 and glutathione S-transferase enzymes and relevance to molecular epidemiology. Environ Health Perspect 98 75–80 Occurrence Handle1486866 Occurrence Handle1:CAS:528:DyaK3sXnsVynsQ%3D%3D

    PubMed  CAS  Google Scholar 

  • SG Carmella A Borukhova SA Akerkar SS Hecht (1997) ArticleTitleAnalysis of human urine for pyridine-N-oxide metabolites of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone, a tobacco-specific lung carcinogen Cancer Epidemiol Biomarkers Prev 6 113–120 Occurrence Handle9037562 Occurrence Handle1:CAS:528:DyaK2sXhs1Khtbo%3D

    PubMed  CAS  Google Scholar 

  • AK Daly KS Fairbrother J Smart (1998) ArticleTitleRecent advances in understanding the molecular basis of polymorphisms in genes encoding cytochrome P450 enzymes Toxicol Lett 102–103 143–147 Occurrence Handle10.1016/S0378-4274(98)00299-9 Occurrence Handle10022246

    Article  PubMed  Google Scholar 

  • JA Agundez C Martínez M Olivera et al. (1998) ArticleTitleExpression in human prostate of drug- and carcinogen-metabolizing enzymes: Association with prostate cancer risk Br J Cancer 78 1361–1367 Occurrence Handle9823980 Occurrence Handle1:CAS:528:DyaK1cXns1WlsLY%3D

    PubMed  CAS  Google Scholar 

  • SJ Plummer DV Conti PL Paris AP Curran G Casey JS Witte (2003) ArticleTitleCYP3A4 and CYP3A5 genotypes, haplotypes, and risk of prostate cancer Cancer Epidemiol Biomarkers Prev 12 928–932 Occurrence Handle14504207 Occurrence Handle1:CAS:528:DC%2BD3sXnsValt7Y%3D

    PubMed  CAS  Google Scholar 

  • T Shimada CH Yun H Yamazaki JC Gautier PH Beaune FP Guengerich (1992) ArticleTitleCharacterization of human lung microsomal cytochrome P-450 1A1 and its role in the oxidation of chemical carcinogens Mol Pharmacol 41 856–864 Occurrence Handle1588920 Occurrence Handle1:CAS:528:DyaK38XmtVKrtL0%3D

    PubMed  CAS  Google Scholar 

  • Taioli E, Trachman J, Chen X, Toniolo P, Garte S. A CYP1A1 restriction fragment lengh polymorphism is associated with breast cancer in African-American women. Cancer Res 1995: 3757–3758.

  • A Hirvonen (1997) ArticleTitleCombinations of susceptible genotypes and individual responses to toxicants. Environ Health Perspect 105 IssueID(Suppl 4) 755–758 Occurrence Handle9255557 Occurrence Handle1:CAS:528:DyaK2sXls1emu7s%3D

    PubMed  CAS  Google Scholar 

  • Seidegard J, Vorachek WR, Pero RW, Pearson WR. Hereditary differences in the expression of the human glutathione transferasa active on trans-steilvene oxide are due to a gene deletion. Proc Natl Acad Sci USA 1988: 7293–7297.

  • S Pemble KR Schroeder SR Spencer et al. (1994) ArticleTitleHuman glutathione S-transferase theta (GSTT1): cDNA cloning and the characterization of a genetic polymorphism. Biochem J 300 IssueID(Pt 1) 271–276 Occurrence Handle1:CAS:528:DyaK2cXkt1yhtrk%3D Occurrence Handle8198545

    CAS  PubMed  Google Scholar 

  • C Steinhoff KH Franke K Golka et al. (2000) ArticleTitleGlutathione transferase isozyme genotypes in patients with prostate and bladder carcinoma Arch Toxicol 74 521–526 Occurrence Handle10.1007/s002040000161 Occurrence Handle11131031 Occurrence Handle1:CAS:528:DC%2BD3MXjslGisg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • TR Rebbeck AH Walker JM Jaffe DL White AJ Wein SB Malkowicz (1999) ArticleTitleGlutathione S-transferase-mu (GSTM1) and -theta (GSTT1) genotypes in the etiology of prostate cancer Cancer Epidemiol Biomarkers Prev 8 283–287 Occurrence Handle1:CAS:528:DyaK1MXislejs7k%3D Occurrence Handle10207629

    CAS  PubMed  Google Scholar 

  • C Acevedo JL Opazo C Huidobro J Cabezas J Iturrieta L Quinones Sepulveda (2003) ArticleTitlePositive correlation between single or combined genotypes of CYP1A1 and GSTM1 in relation to prostate cancer in Chilean people Prostate 57 111–117 Occurrence Handle10.1002/pros.10274 Occurrence Handle12949934 Occurrence Handle1:CAS:528:DC%2BD3sXosFKqt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • LF Wymenga K Groenier P Visser-van Brummen J Marrink HJ Mensink (2000) ArticleTitleReliability analysis of first and second generation PSA assays Can J Urol 7 1070–1076 Occurrence Handle11109077 Occurrence Handle1:STN:280:DC%2BD3MzitFejtw%3D%3D

    PubMed  CAS  Google Scholar 

  • L Quiñones D Lucas J Godoy et al. (2001) ArticleTitleCYP1A1, CYP2E1 and GSTM1 genetic polymorphisms. The effect of single and combined genotypes on lung cancer susceptibility in Chilean people Cancer Lett 174 35–44 Occurrence Handle10.1016/S0304-3835(01)00686-3 Occurrence Handle11675150

    Article  PubMed  Google Scholar 

  • Garte S, Boffetta P, Caporaso N, Vineis P. Metabolic gene allele nomenclature. Cancer Epidemiol Biomarkers Prev 2001; 10.

  • M Ingelman-Sundberg M Oscarson AK Daly S Garte DW Nebert (2001) ArticleTitleHuman cytocrome P-450 (CYP) genes: A web page for the nomenclature of alelles Cancer Epidemiol Biomarkers Prev 10 1307–1308 Occurrence Handle11751452 Occurrence Handle1:STN:280:DC%2BD38%2Fgt1SmsA%3D%3D

    PubMed  CAS  Google Scholar 

  • Korf B. Human genetics: A problem based approach, 2000.

  • LD Botto MJ Khoury (2001) ArticleTitleCommentary: Facing the challenge of gene–environment interaction: The two-by-four table and beyond. Am J Epidemiol 153 1016–1020 Occurrence Handle10.1093/aje/153.10.1016 Occurrence Handle11384958 Occurrence Handle1:STN:280:DC%2BD3Mzht1yitA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • Q Yang MJ Khoury (1997) ArticleTitleEvolving methods in genetic epidemiology. III. Gene–environment interaction in epidemiologic research Epidemiol Rev 19 33–43 Occurrence Handle9360900 Occurrence Handle1:STN:280:DyaK1c%2FisFektw%3D%3D

    PubMed  CAS  Google Scholar 

  • MJ Khoury WD Flanders (1996) ArticleTitleNontraditional epidemiologic approaches in the analysis of gene–environment interaction: Case–control studies with no controls! Am J Epidemiol 144 207–213 Occurrence Handle8686689 Occurrence Handle1:STN:280:DyaK28zgt1Wnsg%3D%3D

    PubMed  CAS  Google Scholar 

  • CB Begg ZF Zhang (1994) ArticleTitleStatistical analysis of molecular epidemiology studies employing case-series Cancer Epidemiol Biomarkers Prev 3 173–175 Occurrence Handle8049640 Occurrence Handle1:STN:280:DyaK2czisFyhsw%3D%3D

    PubMed  CAS  Google Scholar 

  • STATA. STATA Corporation. Intercooled STATA for Windows, 2000.

  • R el-Zein N Conforti-Froes WW Au (1997) ArticleTitleInteractions between genetic predisposition and environmental toxicants for development of lung cancer Environ Mol Mutagen 30 196–204 Occurrence Handle10.1002/(SICI)1098-2280(1997)30:2<196::AID-EM12>3.0.CO;2-8 Occurrence Handle9329644 Occurrence Handle1:CAS:528:DyaK2sXmvFCqt7Y%3D

    Article  PubMed  CAS  Google Scholar 

  • SN Kelada DL Eaton SS Wang NR Rothman MJ Khoury (2003) ArticleTitleThe role of genetic polymorphisms in environmental health. Environ Health Perspect 111 1055–1064 Occurrence Handle12826477 Occurrence Handle1:CAS:528:DC%2BD3sXlvF2ksr0%3D

    PubMed  CAS  Google Scholar 

  • K Kawajiri Y Fujii-Kuriyama (1991) ArticleTitleP450 and human cancer Jpn J Cancer Res 82 1325–1335 Occurrence Handle1778754 Occurrence Handle1:STN:280:DyaK387jvVehsw%3D%3D

    PubMed  CAS  Google Scholar 

  • H Raunio K Husgafvel-Pursiainen S Anttila E Hietanen A Hirvonen O Pelkonen (1995) ArticleTitleDiagnosis of polymorphisms in carcinogen-activating and inactivating enzymes and cancer susceptibility–A review Gene 159 113–121 Occurrence Handle10.1016/0378-1119(94)00448-2 Occurrence Handle7607565 Occurrence Handle1:CAS:528:DyaK2MXmvFWqsrw%3D

    Article  PubMed  CAS  Google Scholar 

  • M Murata T Shiraishi K Fukutome et al. (1998) ArticleTitleCytochrome P4501A1 and glutathione S-transferase M1 genotypes as risk factors for prostate cancer in Japan Jpn J Clin Oncol 28 657–660 Occurrence Handle10.1093/jjco/28.11.657 Occurrence Handle9861231 Occurrence Handle1:STN:280:DyaK1M%2FnvVahtg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • M Murata M Watanabe M Yamanaka et al. (2001) ArticleTitleGenetic polymorphisms in cytochrome P450 (CYP) 1A1, CYP1A2, CYP2E1, glutathione S-transferase (GST) M1 and GSTT1 and susceptibility to prostate cancer in the Japanese population Cancer Lett 165 171–177 Occurrence Handle1:CAS:528:DC%2BD3MXitF2ru7g%3D Occurrence Handle11275366

    CAS  PubMed  Google Scholar 

  • Z Kote-Jarai D Easton SM Edwards et al. (2001) ArticleTitleRelationship between glutathione S-transferase M1, P1 and T1 polymorphisms and early onset prostate cancer Pharmacogenetics 11 325–330 Occurrence Handle10.1097/00008571-200106000-00007 Occurrence Handle11434510 Occurrence Handle1:CAS:528:DC%2BD3MXkvFeis7o%3D

    Article  PubMed  CAS  Google Scholar 

  • T Beer A Evans K Hough B Lowe J McWilliams W Henner (2002) ArticleTitlePolymorphisms of GSTP1 and related genes and prostate cancer risk Prostate Cancer Prostatic Dis 5 22–27 Occurrence Handle10.1038/sj.pcan.4500549 Occurrence Handle15195126 Occurrence Handle1:CAS:528:DC%2BD38Xjt1Ogu70%3D

    Article  PubMed  CAS  Google Scholar 

  • SN Kelada SL Kardia AH Walker AJ Wein SB Malkowicz TR Rebbeck (2000) ArticleTitleThe glutathione S-transferase-mu and -theta genotypes in the etiology of prostate cancer: Genotype–environment interactions with smoking Cancer Epidemiol Biomarkers Prev 9 1329–1334 Occurrence Handle1:CAS:528:DC%2BD3MXktFaitw%3D%3D Occurrence Handle11142418

    CAS  PubMed  Google Scholar 

  • LH Lumey B Pittman EA Zang EL Wynder (1997) ArticleTitleCigarette smoking and prostate cancer: No relation with six measures of lifetime smoking habits in a large case–control study among U.S. whites Prostate 33 195–200 Occurrence Handle9365548 Occurrence Handle1:STN:280:DyaK1c%2Fjt1amsA%3D%3D

    PubMed  CAS  Google Scholar 

  • PA Lotufo IM Lee UA Ajani CH Hennekens JE Manson (2000) ArticleTitleCigarette smoking and risk of prostate cancer in the physicians’ health study (United States) Int J Cancer 87 141–144 Occurrence Handle10.1002/1097-0215(20000701)87:1<141::AID-IJC21>3.0.CO;2-A Occurrence Handle10861465 Occurrence Handle1:STN:280:DC%2BD3czitFCnsw%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • K Hickey KA Do A Green (2001) ArticleTitleSmoking and prostate cancer Epidemiol Rev 23 115–125 Occurrence Handle1:STN:280:DC%2BD3Mrkt1SlsQ%3D%3D Occurrence Handle11588835

    CAS  PubMed  Google Scholar 

  • F Levi Vecchia C La (2001) ArticleTitleTobacco smoking and prostate cancer: Time for an appraisal Ann Oncol 12 733–738 Occurrence Handle10.1023/A:1011124523984 Occurrence Handle11484946 Occurrence Handle1:STN:280:DC%2BD38%2FislSksQ%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • Signorello L, Adami H. Prostate cancer. In: Adami H-O, Hunter D, Trichopoulos D. (eds), Textbook of cancer epidemiology. New York: Oxford University Press, 2002: 400–428.

  • Sommer F, Klotz T, Schmitz-Drager BJ. Lifestyle issues and genitourinary tumours. World J Urol 2003.

  • LA Plaskon DF Penson TL Vaughan JL Stanford (2003) ArticleTitleCigarette smoking and risk of prostate cancer in middle-aged men Cancer Epidemiol Biomarkers Prev 12 604–609 Occurrence Handle12869398 Occurrence Handle1:CAS:528:DC%2BD3sXlsVymsb0%3D

    PubMed  CAS  Google Scholar 

  • SK Park KY Yoo SJ Lee et al. (2000) ArticleTitleAlcohol consumption, glutathione S-transaferase M1 and T1 genetic polymorphisms and breast cancer risk Theta. Pharmacogenetics 10 301–309 Occurrence Handle10.1097/00008571-200006000-00004 Occurrence Handle1:CAS:528:DC%2BD3cXksFSqsbg%3D

    Article  CAS  Google Scholar 

  • T Zheng T Holford S Zahm et al. (2003) ArticleTitleGlutathione S-transferase M1 and T1 genetic polymorphisms, alcohol consumption and breast cancer risk Br J Cancer 88 58–62 Occurrence Handle10.1038/sj.bjc.6600708 Occurrence Handle12556960 Occurrence Handle1:CAS:528:DC%2BD3sXntFSnsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • A Rundle D Tang L Mooney S Grumet F Perera (2003) ArticleTitleThe interaction between alcohol consumption and GSTM1 genotype on polycyclic aromatic hydrocarbon–DNA adduct levels in breast tissue Cancer Epidemiol Biomarkers Prev 12 911–914 Occurrence Handle14504203 Occurrence Handle1:CAS:528:DC%2BD3sXnsValt7s%3D

    PubMed  CAS  Google Scholar 

  • LK Dennis (2000) ArticleTitleMeta-analysis for combining relative risks of alcohol consumption and prostate cancer Prostate 42 56–66 Occurrence Handle10579799 Occurrence Handle1:STN:280:DC%2BD3c%2FkslWhsw%3D%3D

    PubMed  CAS  Google Scholar 

  • LK Dennis RB Hayes (2001) ArticleTitleAlcohol and prostate cancer Epidemiol Rev 23 110–114 Occurrence Handle11588834 Occurrence Handle1:STN:280:DC%2BD3Mrkt1SlsA%3D%3D

    PubMed  CAS  Google Scholar 

  • K Albertsen M Gronbaek (2002) ArticleTitleDoes amount or type of alcohol influence the risk of prostate cancer? Prostate 52 297–304 Occurrence Handle10.1002/pros.10120 Occurrence Handle12210490

    Article  PubMed  Google Scholar 

  • V Bagnardi M Blangiardo C La Vecchia G Corrao (2001) ArticleTitleA meta-analysis of alcohol drinking and cancer risk Br J Cancer 85 1700–1705 Occurrence Handle10.1054/bjoc.2001.2140 Occurrence Handle11742491 Occurrence Handle1:CAS:528:DC%2BD38XnsVChtg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  • P Brennan (2002) ArticleTitleGene-environment interaction and aetiology of cancer: What does it mean and how can we measure it? Carcinogenesis 23 381–387 Occurrence Handle10.1093/carcin/23.3.381 Occurrence Handle11895852 Occurrence Handle1:CAS:528:DC%2BD38Xis1Knt7c%3D

    Article  PubMed  CAS  Google Scholar 

  • Brennan P. Design and analysis issues in case–control studies addressing genetic susceptibility. IARC Sci Publ 1999: 123–132.

  • Botto L, Khoury M. PART II: Methods and approaches 1: Assessing disease associations and interactions. Facing the challenge of complex genotypes and gene–environment interaction: The basic epidemiologic units in case–control and case–only designs. In: Muin J, Khoury JL, Willie Burke (eds), Human genome epidemiology: A scientific foundation for using genetic information to improve health and prevent disease. Oxford University Press, 2004.

  • A Seidler H Heiskel R Bickeboller G Elsner (1998) ArticleTitleAssociation between diesel exposure at work and prostate cancer Scand J Work Environ Health 24 486–494 Occurrence Handle9988091 Occurrence Handle1:CAS:528:DyaK1MXnt1Ojtw%3D%3D

    PubMed  CAS  Google Scholar 

  • L Quiñones F Berthou N Varela B Simon L Gil D Lucas (1999) ArticleTitleEthnic susceptibility to lung cancer: Differences in CYP2E1, CYP1A1 and GSTM1 genetic polymorphisms between French Caucasian and Chilean populations Cancer Lett 141 167–171 Occurrence Handle10.1016/S0304-3835(99)00099-3 Occurrence Handle10454258

    Article  PubMed  Google Scholar 

  • S Wacholder NR Rothman N Caporaso (2002) ArticleTitleCounterpoint: Bias from population stratification is not a major threat to the validity of conclusions from epidemiological studies of common polymorphisms and cancer Cancer Epidemiol Biomarkers Prev 11 513–520 Occurrence Handle12050091

    PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luis Quiñones S.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cáceres L, D.D., Iturrieta G, J., Acevedo C, C. et al. Relationship among metabolizing genes, smoking and alcohol used as modifier factors on prostate cancer risk: Exploring some gene–gene and gene–environment interactions. Eur J Epidemiol 20, 79–88 (2005). https://doi.org/10.1007/s10654-004-1632-9

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10654-004-1632-9

Keywords

Navigation