Abstract
Previous studies investigating the association between glutathione S-transferase M1 (GSTM1) null genotype and laryngeal cancer risk reported controversial results. Thus, a meta-analysis was performed to clarify the effect of GSTM1 null genotype on laryngeal cancer risk. A literature search was performed for all possible studies. We estimated summary odd ratio (OR) with its 95 % confidence interval (95 % CI) to assess the association. Subgroup analyses were performed by ethnicity or the sample size. 24 individual case–control studies involving a total of 2,809 laryngeal cancer cases and 4,478 controls were finally included into this meta-analysis. Meta-analyses of total 24 studies showed the GSTM1 null genotype was significantly associated with increased laryngeal cancer risk (random-effects OR = 1.44, 95 % CI 1.19–1.73, P < 0.001). Subgroup analyses by ethnicity showed that the GSTM1 null genotype was associated with increased laryngeal cancer risk in both Caucasians (fixed-effects OR = 1.17, 95 % CI 1.04–1.33, P = 0.012) and Asians (random-effects OR = 1.89, 95 % CI 1.28–2.77, P = 0.001). Also, subgroup analyses by sample size also further identified this association above. The cumulative meta-analyses showed a trend of more obvious association between GSTM1 null genotype and increased risk of laryngeal cancer as information accumulated by year. Meta-analysis of available data suggests that GSTM1 null genotype contributes to increased laryngeal cancer risk in both Caucasians and East Asians.
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Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2):69–90
Bosetti C, Garavello W, Gallus S, La Vecchia C (2006) Effects of smoking cessation on the risk of laryngeal cancer: an overview of published studies. Oral Oncol 42(9):866–872
Sadri M, McMahon J, Parker A (2006) Laryngeal dysplasia: aetiology and molecular biology. J Laryngol Otol 120(3):170–177
Nadal A, Cardesa A (2003) Molecular biology of laryngeal squamous cell carcinoma. Virchows Arch 442(1):1–7
Ha PK, Califano JA 3rd (2002) The molecular biology of laryngeal cancer. Otolaryngol Clin North Am 35(5):993–1012
Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88
Hayes JD, Strange RC (2000) Glutathione S-transferase polymorphisms and their biological consequences. Pharmacology 61(3):154–166
Ruwali M, Singh M, Pant MC, Parmar D (2011) Polymorphism in glutathione S-transferases: susceptibility and treatment outcome for head and neck cancer. Xenobiotica 41(12):1122–1130
Lourenco GJ, Silva EF, Rinck-Junior JA, Chone CT, Lima CS (2011) CYP1A1, GSTM1 and GSTT1 polymorphisms, tobacco and alcohol status and risk of head and neck squamous cell carcinoma. Tumour Biol 32(6):1209–1215
Risch A, Ramroth H, Raedts V, Rajaee-Behbahani N, Schmezer P, Bartsch H, Becher H, Dietz A (2003) Laryngeal cancer risk in Caucasians is associated with alcohol and tobacco consumption but not modified by genetic polymorphisms in class I alcohol dehydrogenases ADH1B and ADH1C, and glutathione-S-transferases GSTM1 and GSTT1. Pharmacogenetics 13(4):225–230
Matthias C, Bockmuhl U, Jahnke V, Jones PW, Hayes JD, Alldersea J, Gilford J, Bailey L, Bath J, Worrall SF, Hand P, Fryer AA, Strange RC (1998) Polymorphism in cytochrome P450 CYP2D6, CYP1A1, CYP2E1 and glutathione S-transferase, GSTM1, GSTM3, GSTT1 and susceptibility to tobacco-related cancers: studies in upper aerodigestive tract cancers. Pharmacogenetics 8(2):91–100
Gronau S, Koenig-Greger D, Jerg M, Riechelmann H (2003) Gene polymorphisms in detoxification enzymes as susceptibility factor for head and neck cancer? Otolaryngol Head Neck Surg 128(5):674–680
Gajecka M, Rydzanicz M, Jaskula-Sztul R, Kujawski M, Szyfter W, Szyfter K (2005) CYP1A1, CYP2D6, CYP2E1, NAT2, GSTM1 and GSTT1 polymorphisms or their combinations are associated with the increased risk of the laryngeal squamous cell carcinoma. Mutat Res 574(1–2):112–123
Chatzimichalis M, Xenellis J, Tzagaroulakis A, Sarof P, Banis K, Gazouli M, Bibas A (2010) GSTT1, GSTM1, GSTM3 and NAT2 polymorphisms in laryngeal squamous cell carcinoma in a Greek population. J Laryngol Otol 124(3):318–323
Bardakci F, Canbay E, Degerli N, Coban L, Canbay EI (2003) Relationship of tobacco smoking with GSTM1 gene polymorphism in laryngeal cancer. J Cell Mol Med 7(3):307–312
Morita S, Yano M, Tsujinaka T, Akiyama Y, Taniguchi M, Kaneko K, Miki H, Fujii T, Yoshino K, Kusuoka H, Monden M (1999) Genetic polymorphisms of drug-metabolizing enzymes and susceptibility to head-and-neck squamous-cell carcinoma. Int J Cancer 80(5):685–688
Cabelguenne A, Loriot MA, Stucker I, Blons H, Koum-Besson E, Brasnu D, Beaune P, Laccourreye O, Laurent-Puig P, De Waziers I (2001) Glutathione-associated enzymes in head and neck squamous cell carcinoma and response to cisplatin-based neoadjuvant chemotherapy. Int J Cancer 93(5):725–730
Coutelle C, Ward PJ, Fleury B, Quattrocchi P, Chambrin H, Iron A, Couzigou P, Cassaigne A (1997) Laryngeal and oropharyngeal cancer, and alcohol dehydrogenase 3 and glutathione S-transferase M1 polymorphisms. Hum Genet 99(3):319–325
Jahnke V, Strange R, Matthias C, Fryer A (1997) Glutathione S-transferase and cytochrome P450 genotypes as risk factors for laryngeal carcinoma. Eur Arch Otorhinolaryngol 254(Suppl 1):S147–S149
Hong YJ, Lee JK, Lee GH, Hong SI (2000) Influence of glutathione S-transferase M1 and T1 genotypes on larynx cancer risk among Korean smokers. Clin Chem Lab Med 38(9):917–919
To-Figueras J, Gene M, Gomez-Catalan J, Pique E, Borrego N, Caballero M, Cruellas F, Raya A, Dicenta M, Corbella J (2002) Microsomal epoxide hydrolase and glutathione S-transferase polymorphisms in relation to laryngeal carcinoma risk. Cancer Lett 187(1–2):95–101
Acar H, Ozturk K, Muslumanoglu MH, Yildirim MS, Cora T, Cilingir O, Ozer B (2006) Relation of glutathione S-transferase genotypes (GSTM1 and GSTT1) to laryngeal squamous cell carcinoma risk. Cancer Genet Cytogenet 169(2):89–93
Peters ES, McClean MD, Marsit CJ, Luckett B, Kelsey KT (2006) Glutathione S-transferase polymorphisms and the synergy of alcohol and tobacco in oral, pharyngeal, and laryngeal carcinoma. Cancer Epidemiol Biomarkers Prev 15(11):2196–2202
Jourenkova N, Reinikainen M, Bouchardy C, Dayer P, Benhamou S, Hirvonen A (1998) Larynx cancer risk in relation to glutathione S-transferase M1 and T1 genotypes and tobacco smoking. Cancer Epidemiol Biomarkers Prev 7(1):19–23
Nosheen M, Ishrat M, Malik FA, Baig RM, Kayani MA (2010) Association of GSTM1 and GSTT1 gene deletions with risk of head and neck cancer in Pakistan: a case control study. Asian Pac J Cancer Prev 11(4):881–885
Attia J, Thakkinstian A, D’Este C (2003) Meta-analyses of molecular association studies: methodologic lessons for genetic epidemiology. J Clin Epidemiol 56(4):297–303
Petitti DB (2000) Meta-analysis, decision analysis, and cost effectiveness analysis: methods for quantitative synthesis in medicine, 2nd edn. Oxford University Press, New York
Burchard EG, Ziv E, Coyle N, Gomez SL, Tang H, Karter AJ, Mountain JL, Perez-Stable EJ, Sheppard D, Risch N (2003) The importance of race and ethnic background in biomedical research and clinical practice. N Engl J Med 348(12):1170–1175
Bhopal R (2004) Glossary of terms relating to ethnicity and race: for reflection and debate. J Epidemiol Community Health 58(6):441–445
Mantel N, Haenszel W (1959) Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst 22(4):719–748
DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560
Cochran WG (1954) The combination of estimates from different experiments. Biometrics 10(1):101–129
Thompson SG, Higgins J (2002) How should meta-regression analyses be undertaken and interpreted? Stat Med 21(11):1559–1573
Lau J, Antman EM, Jimenez-Silva J, Kupelnick B, Mosteller F, Chalmers TC (1992) Cumulative meta-analysis of therapeutic trials for myocardial infarction. N Engl J Med 327(4):248–254
Zintzaras E, Lau J (2008) Synthesis of genetic association studies for pertinent gene-disease associations requires appropriate methodological and statistical approaches. J Clin Epidemiol 61(7):634–645
Muellerleile P, Mullen B (2006) Sufficiency and stability of evidence for public health interventions using cumulative meta-analysis. Am J Public Health 96(3):515–522
Coon CS (1972) The races of Europe. Greenwood Press, New York
Stuck AE, Rubenstein LZ, Wieland D (1998) Bias in meta-analysis detected by a simple, graphical test. Asymmetry detected in funnel plot was probably due to true heterogeneity. BMJ 316(7129):469 (author reply 470–461)
Egger M, Davey Smith G, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634
Li L, Lin P, Deng YF, Zhu ZL, Lu HH (2004) Relationship between susceptibility and prognosis of laryngeal cancer and genetic polymorphisms in CYP1A1 and GSTM1. Zhonghua Er Bi Yan Hou Ke Za Zhi 39(1):2–7
Yan Y, Zhou W (2003) GSTM1 null genotype and susceptibility of laryngeal carcinoma. Nantong Yi Xue Yuan Bao 23(3):255–257
Tian S, Zhang J, Xiao Q, Zhai J, Yan X, Huang M, Chen F, Li Q, Guan Z (2011) The association between genetic polymorphisms of GSTM1, GSTT1, GSTP1 and susceptibility to laryngeal carcinoma from the Han people in Guangdong zone. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 25(5):204–210
Li Q, Wang L, Chen Y, Du Y, Kong P, Li Y, Xu X (2009) Polymorphisms of GSTM1, GSTT1 and susceptibility of laryngeal and hypopharyngeal carcinomas. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 23(24):1105–1107, 1111
Lei DP, Pan X, Guo CH, Xu F, Zhang L, Liu D, Luan X (2002) Larynx cancer risk in relation to glutathione S-transferase M1 null genotype. Chin J Med Genet 19(6):74–76
Unal M, Tamer L, Ates NA, Akbas Y, Pata YS, Vayisoglu Y, Ercan B, Gorur K, Atik U (2004) Glutathione S-transferase M1, T1, and P1 gene polymorphism in laryngeal squamous cell carcinoma. Am J Otolaryngol 25(5):318–322
Canova C, Richiardi L, Merletti F, Pentenero M, Gervasio C, Tanturri G, Garzino-Demo P, Pecorari G, Talamini R, Barzan L, Sulfaro S, Franchini G, Muzzolini C, Bordin S, Pugliese GN, Macri E, Simonato L (2010) Alcohol, tobacco and genetic susceptibility in relation to cancers of the upper aerodigestive tract in northern Italy. Tumori 96(1):1–10
Leme CV, Raposo LS, Ruiz MT, Biselli JM, Galbiatti AL, Maniglia JV, Pavarino-Bertelli EC, Goloni-Bertollo EM (2010) GSTM1 and GSTT1 genes analysis in head and neck cancer patients. Rev Assoc Med Bras 56(3):299–303
Sharma R, Panda NK, Khullar M (2010) Hypermethylation of carcinogen metabolism genes, CYP1A1, CYP2A13 and GSTM1 genes in head and neck cancer. Oral Dis 16(7):668–673
Matthias C, Jahnke V, Hand P, Fryer AA, Strange RC (1999) Immunohistologic and molecular genetic studies of the effect of glutathione-S-transferases on the development of squamous epithelial carcinomas in the area of the head-neck. Laryngorhinootologie 78(4):182–188
Matthias C, Jahnke V, Fryer AA, Strange RC (2002) Influence of glutathione s-transferase and cytochrome p450 polymorphisms on prognosis of head and neck cancer. Laryngorhinootologie 81(6):406–412
Gronau S, Konig-Greger D, Rettinger G, Riechelmann H (2000) GSTM1 gene polymorphism in patients with head and neck tumors. Laryngorhinootologie 79(6):341–344
Jahnke V, Matthias C, Fryer A, Strange R (1996) Glutathione S-transferase and cytochrome-P-450 polymorphism as risk factors for squamous cell carcinoma of the larynx. Am J Surg 172(6):671–673
Zhuo WL, Wang Y, Zhuo XL, Zhu B, Zhu Y, Chen ZT (2009) Polymorphisms of CYP1A1 and GSTM1 and laryngeal cancer risk: evidence-based meta-analyses. J Cancer Res Clin Oncol 135(8):1081–1090
Kumar V, Murthy AK, Suresh K (2011) Glutathione S-transferase M1 and T1 Status and the Risk of Laryngeal Cancer: a Meta-analysis. Asian Pac J Cancer Prev 12(9):2221–2226
Ioannidis JP, Patsopoulos NA, Evangelou E (2007) Uncertainty in heterogeneity estimates in meta-analyses. BMJ 335(7626):914–916
Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, Brozek J, Norris S, Falck-Ytter Y, Glasziou P, DeBeer H, Jaeschke R, Rind D, Meerpohl J, Dahm P, Schunemann HJ (2011) GRADE guidelines: 1. Introduction-GRADE evidence profiles and summary of findings tables. J Clin Epidemiol 64(4):383–394
Zhang R, Xu G, Chen W, Zhang W (2011) Genetic polymorphisms of glutathione S-transferase M1 and bladder cancer risk: a meta-analysis of 26 studies. Mol Biol Rep 38(4):2491–2497
Wang B, Huang G, Wang D, Li A, Xu Z, Dong R, Zhang D, Zhou W (2010) Null genotypes of GSTM1 and GSTT1 contribute to hepatocellular carcinoma risk: evidence from an updated meta-analysis. J Hepatol 53(3):508–518
Economopoulos KP, Sergentanis TN (2010) GSTM1, GSTT1, GSTP1, GSTA1 and colorectal cancer risk: a comprehensive meta-analysis. Eur J Cancer 46(9):1617–1631
Qiu LX, Wang K, Lv FF, Chen ZY, Liu X, Zheng CL, Li WH, Zhu XD, Guo WJ, Li J (2011) GSTM1 null allele is a risk factor for gastric cancer development in Asians. Cytokine 55(1):122–125
Qiu LX, Yuan H, Yu KD, Mao C, Chen B, Zhan P, Xue K, Zhang J, Hu XC (2010) Glutathione S-transferase M1 polymorphism and breast cancer susceptibility: a meta-analysis involving 46,281 subjects. Breast Cancer Res Treat 121(3):703–708
Economopoulos KP, Sergentanis TN, Vlahos NF (2010) Glutathione S-transferase M1, T1, and P1 polymorphisms and ovarian cancer risk: a meta-analysis. Int J Gynecol Cancer 20(5):732–737
Economopoulos KP, Choussein S, Vlahos NF, Sergentanis TN (2010) GSTM1 polymorphism, GSTT1 polymorphism, and cervical cancer risk: a meta-analysis. Int J Gynecol Cancer 20(9):1576–1580
Thier R, Brüning T, Roos PH, Rihs HP, Golka K, Ko Y, Bolt HM (2003) Markers of genetic susceptibility in human environmental hygiene and toxicology: the role of selected CYP, NAT and GST genes. Int J Hyg Environ Health 206(3):149–171
Reszka E, Wasowicz W, Gromadzinska J (2006) Genetic polymorphism of xenobiotic metabolising enzymes, diet and cancer susceptibility. Br J Nutr 96(4):609–619
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H. Xiao and M. Li contributed equally to this work.
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Xiao, H., Li, M., Tian, L. et al. Quantitative assessment of the association between GSTM1 null genotype and laryngeal cancer risk. Eur Arch Otorhinolaryngol 270, 615–622 (2013). https://doi.org/10.1007/s00405-012-2148-7
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DOI: https://doi.org/10.1007/s00405-012-2148-7