Skip to main content

Advertisement

Log in

Characteristics of cigarette smoking without alcohol consumption and laryngeal cancer: overall and time-risk relation. A meta-analysis of observational studies

  • Laryngology
  • Published:
European Archives of Oto-Rhino-Laryngology Aims and scope Submit manuscript

Abstract

Tobacco smoking was one of the risk factors for upper aerodigestive tract cancer, but exclusive quantification of the impact of cigarette smoking on laryngeal cancer had not been investigated. A meta-analysis of researches that had reported quantitative estimates of cigarette smoking and risk of laryngeal cancer by March 2016 was performed. Pooled estimates of relative risks and their 95% confidence intervals were obtained and summarized. Sensitivity analysis and subgroup analysis were implemented to find out sources of research heterogeneity and the effect of potential confounders. Publication bias was investigated and corrected if found to be present through Egger’s and Begg’s test, and trim and fill algorithm. Thirty researches based on a total of 14,292 cases from three cohort and fifteen case–control studies were included and pooled estimate for the correlation between cigarette smoking and the risk of laryngeal cancer was 7.01 (95% confidence interval 5.56–8.85), with moderate heterogeneity across the researches (I 2 = 56.7%, p = 0.002). The RRs were 5.04 (95% CI 3.09–8.22) for cohort studies (p = 0.121), 7.59 (95% CI 5.86–9.82) for case–control studies (p = 0.005). The risk kept elevated within the first fifteen years of quitting smoking(RR 3.62, 95% CI 1.88–7.00) but dropped in the 16 years and more after smoking cessation(RR 1.88, 95% CI 1.16–3.05). Individuals who smoked with 40 or more pack-years had nine times the risk of laryngeal cancer(RR 9.14; 95% CI 6.24–13.39). Subjects who smoked 30 or more cigarettes a day had sevenfolds the risk of laryngeal cancer (RR 7.02; 95% CI 4.47–11.02) and who smoked 40 or more years had five times the risk versus never smokers (RR 5.76; 95% CI 3.69–8.99). Evidence of publication bias was not detected for the correlation between current cigarette smoking and risk of laryngeal cancer (p = 0.225 with Begg’s test, p = 0.317 with Egger’s test). The results demonstrated strong correlation referring to dose–response and time–response between cigarette smoking and risk of laryngeal cancer for both men and women. The probability of developing laryngeal cancer was decreased by quitting smoking, particularly among former cigarette smokers who had stopped smoking for 15 or more years. The subgroup analysis demonstrated that study type influenced the RRs estimates of the studies.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Ahrens W, Jockel KH, Patzak W, Elsner G (1991) Alcohol, smoking, and occupational factors in cancer of the larynx: a case–control study. Am J Ind Med 20(4):477–493

    Article  CAS  PubMed  Google Scholar 

  2. Applebaum KM, Furniss CS, Zeka A, Posner MR, Smith JF, Bryan J, Eisen EA, Peters ES, McClean MD, Kelsey KT (2007) Lack of association of alcohol and tobacco with HPV16-associated head and neck cancer. J Natl Cancer Inst 99(23):1801–1810

    Article  PubMed  Google Scholar 

  3. Bosetti C, Gallus S, Franceschi S, Levi F, Bertuzzi M, Negri E, La Vecchia C (2002) Cancer of the larynx in non-smoking alcohol drinkers and in non-drinking tobacco smokers. (Comparative Study Research Support, Non-U.S. Gov’t). Br J Cancer 87(5):516–518. doi:10.1038/sj.bjc.6600469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Bosetti C, Gallus S, Peto R, Negri E, Talamini R, Tavani A, La Vecchia C (2008) Tobacco smoking, smoking cessation, and cumulative risk of upper aerodigestive tract cancers (Multicenter Study Research Support, Non-U.S. Gov’t). Am J Epidemiol 167(4):468–473. doi:10.1093/aje/kwm318

    Article  PubMed  Google Scholar 

  5. Dai Q, Ji BT, Xu M, Gao YT (1994) Analysis of population attributable risk proportion (PARP) of some commonly seen cancer due to smoking in urban Shanghai. Tumor 14(4):208–211 (Chinese)

  6. Dosemeci M, Gokmen I, Unsal M, Hayes RB, Blair A (1997) Tobacco, alcohol use, and risks of laryngeal and lung cancer by subsite and histologic type in Turkey. Cancer Causes Control 8(5):729–737

    Article  CAS  PubMed  Google Scholar 

  7. Durán de Alba LM, Roa Castro FM (2008) Risk factors for developing laryngeal cancer in adult population at the Hospital Español in Mexico City. Acta Otorrinolaringol Esp 59(8):367–370

    Article  PubMed  Google Scholar 

  8. Egger M, Davey SG, Schneider M, Minder C (1997) Bias in metaanalysis detected by a simple, graphical test. BMJ 315(7109):629–634

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Falk RT, Pickle LW, Brown LM, Mason MJ, Buffler PA, Fraumeni Jr JF (1989) Effect of smoking and alcohol consumption on laryngeal cancer risk in coastal Texas. Cancer Res 49:4024–4029

    CAS  PubMed  Google Scholar 

  10. Feng J, Li L, Zhao YS, Tang SQ, Yang HB, Liu SX (2011) Interaction between CYP 2C19*3 polymorphism and smoking in relation to laryngeal carcinoma in the Chinese Han population (Research Support, Non-U.S. Gov’t). Genet Mol Res 10(4):3331–3337. doi:10.4238/2011.December.5.9

    Article  CAS  PubMed  Google Scholar 

  11. Feng S, Guo X, Wang Y, Li XT (2010). Risk factors of laryngeal carcinoma: a case–control analysis. J China Med Univ 39(6):474–475 (Chinese)

  12. Franceschi S, Talamini R, Barra S, Baron AE, Negri E, Bidoli E, La Vecchia C (1990) Smoking and drinking in relation to cancers of the oral cavity, pharynx, larynx, and esophagus in Northern Italy. Cancer Res 50(20):6502–6507

    CAS  PubMed  Google Scholar 

  13. Freudenheim JL, Graham S, Byers TE, Marshall JR, Haughey BP, Swanson MK, Wilkinson G (1992) Diet, smoking, and alcohol in cancer of the larynx: a case–control study (Research Support, U.S. Gov’t, P.H.S.). Nutr Cancer 17(1):33–45. doi:10.1080/01635589209514171

    Article  CAS  PubMed  Google Scholar 

  14. Gallus S, Bosetti C, Franceschi S, Levi F, Negri E, Vecchia CL (2003) Laryngeal cancer in women: tobacco, alcohol, nutritional, and hormonal factors. Cancer Epidemiol Biomark Prev 12:514–517

    Google Scholar 

  15. Gandini S, Botteri E, Iodice S, Boniol M, Lowenfels AB, Maisonneuve P, Boyle P (2008) Tobacco smoking and cancer: a meta-analysis. Int J Cancer 122:155–164. doi:10.1002/ijc.23033

    Article  CAS  PubMed  Google Scholar 

  16. Gandini S, Botteri E, Iodice S, Boniol M, Lowenfels AB, Maisonneuve P, Boyle P (2008) Tobacco smoking and cancer: a meta-analysis (Meta-Analysis Research Support, Non-U.S. Gov’t). Int J Cancer 122(1):155–164. doi:10.1002/ijc.23033

    Article  CAS  PubMed  Google Scholar 

  17. Guo X (1993) A case–control study of the etiology of laryngeal cancer in Liaoning Province. Zhonghua er bi yan hou ke za zhi 28(4):219–221 (252)

  18. Hashibe M, Boffetta P, Zaridze D, Shangina O, Szeszenia-Dabrowska N, Mates D, Brennan P (2007) Contribution of tobacco and alcohol to the high rates of squamous cell carcinoma of the supraglottis and glottis in Central Europe (Multicenter Study Research Support, Non-U.S. Gov’t). Am J Epidemiol 165(7):814–820. doi:10.1093/aje/kwk066

    Article  PubMed  Google Scholar 

  19. Hashibe M, Brennan P, Benhamou S, Castellsague X, Chen C, Curado MP, Boffetta P (2007) Alcohol drinking in never users of tobacco, cigarette smoking in never drinkers, and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium (Multicenter Study Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.). J Natl Cancer Inst 99(10):777–789. doi:10.1093/jnci/djk179

    Article  PubMed  Google Scholar 

  20. Hashibe M, Brennan P, Chuang SC, Boccia S, Castellsague X, Chen C, Boffetta P (2009) Interaction between tobacco and alcohol use and the risk of head and neck cancer: pooled analysis in the International Head and Neck Cancer Epidemiology Consortium (Multicenter Study Research Support, N.I.H., Extramural Research Support, N.I.H., Intramural Research Support, Non-U.S. Gov’t Research Support, U.S. Gov’t, Non-P.H.S.). Cancer Epidemiol Biomark Prev 18(2):541–550. doi:10.1158/1055-9965.EPI-08-0347

    Article  CAS  Google Scholar 

  21. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ishiguro S, Sasazuki S, Inoue M, Kurahashi N, Iwasaki M, Tsugane S (2009) Effect of alcohol consumption, cigarette smoking and flushing response on esophageal cancer risk: a population-based cohort study (JPHC study) (Research Support, Non-U.S. Gov’t). Cancer Lett 275(2):240–246. doi:10.1016/j.canlet.2008.10.020

    Article  CAS  PubMed  Google Scholar 

  23. Jayalekshmi PA, Nandakumar A, Akiba S, Gangadharan P, Koriyama C (2013) Associations of tobacco use and alcohol drinking with laryngeal and hypopharyngeal cancer risks among men in Karunagappally, Kerala, India—Karunagappally Cohort Study. PLoS One 8:8

    Article  Google Scholar 

  24. Jee SH, Samet JM, Ohrr H, Kim JH, Kim S (2004) Smoking and cancer risk in Korean men and women. Cancer Causes Control 15:341–348

    Article  PubMed  Google Scholar 

  25. Lee KW, Kuo WR, Tsai SM, Wu DC, Wang WM, Fang FM, Ko YC (2005) Different impact from betel quid, alcohol and cigarette: risk factors for pharyngeal and laryngeal cancer (Research Support, Non-U.S. Gov’t). Int J Cancer 117(5):831–836. doi:10.1002/ijc.21237

    Article  CAS  PubMed  Google Scholar 

  26. Lu B, Li J, Gao Q, Yu W, Yang Q, Li X (2014) Laryngeal cancer risk and common single nucleotide polymorphisms in nucleotide excision repair pathway genes ERCC1, ERCC2, ERCC3, ERCC4, ERCC5 and XPA. Gene 542(1):64–68

    Article  CAS  PubMed  Google Scholar 

  27. Lubin JH, Purdue M, Kelsey K, Zhang ZF, Winn D, Wei Q, Hayes RB (2009) Total exposure and exposure rate effects for alcohol and smoking and risk of head and neck cancer: a pooled analysis of case–control studies (Meta-Analysis Research Support, N.I.H., Intramural). Am J Epidemiol 170(8):937–947. doi:10.1093/aje/kwp222

    Article  PubMed  PubMed Central  Google Scholar 

  28. Maasland DH, van den Brandt PA, Kremer B, Goldbohm RA, Schouten LJ (2014) Alcohol consumption, cigarette smoking and the risk of subtypes of head-neck cancer: results from the Netherlands Cohort Study (Research Support, Non-U.S. Gov’t). BMC Cancer 14:187. doi:10.1186/1471-2407-14-187

    Article  PubMed  PubMed Central  Google Scholar 

  29. Maurya SS, Katiyar T, Dhawan A, Singh S, Jain SK, Pant MC, Parmar D (2015) Gene–environment interactions in determining differences in genetic susceptibility to cancer in subsites of the head and neck. Environ Mol Mutagen 56(3):313–321

    Article  CAS  PubMed  Google Scholar 

  30. Moghaddam AA, Huxley RR, Lam TH, Woodward M (2009) Risk of upper aerodigestive tract cancer associated with smoking with and without concurrent alcohol consumption. Mt Sinai J Med 76:392–403. doi:10.1002/msj.2012510.1002/MSJ

    Article  Google Scholar 

  31. Moura MA, Bergmann A, Aguiar SS, Thuler LC (2014) The magnitude of the association between smoking and the risk of developing cancer in Brazil: a multicenter study. BMJ Open 4(2):e003736. doi:10.1136/bmjopen-2013-003736

    Article  PubMed  PubMed Central  Google Scholar 

  32. Norman RP (2002) Risk factors for oesophageal, lung, oral and laryngeal cancers in black South Africans. Br J Cancer 86:1751–1756

    Article  Google Scholar 

  33. Ramroth H, Dietz A, Becher H (2011) Intensity and inhalation of smoking in the aetiology of laryngeal cancer. Int J Environ Res Public Health 8(4):976–984

    Article  PubMed  PubMed Central  Google Scholar 

  34. Risch A, Ramroth H, Raedts V, Rajaee-Behbahani N, Schmezer P, Bartsch 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 (Research Support, Non-U.S. Gov’t). Pharmacogenetics 13(4):225–230. doi:10.1097/01.fpc.0000054081.64000.b8

    Article  CAS  PubMed  Google Scholar 

  35. Sterne JA, Egger M, Smith GD (2001) Investigating and dealing with publication and other biases in metaanalysis. BMJ 323(7304):101–105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Talamini R, Bosetti C, La Vecchia C, Dal Maso L, Levi F, Bidoli E, Franceschi S (2002) Combined effect of tobacco and alcohol on laryngeal cancer risk: a case–control study. Cancer Causes Control 13(10):957–964

    Article  CAS  PubMed  Google Scholar 

  37. Tavani A, Negri E, Franceschi S, Barbone F, La Vecchia C (1994) Attributable risk for laryngeal cancer in Northern Italy. Cancer Epidemiol Biomark Prev 3(2):121–125

    CAS  Google Scholar 

  38. Toporcov TN, Znaor A, Zhang ZF, Yu GP, Winn DM, Wei Q, Filho VW (2015) Risk factors for head and neck cancer in young adults: a pooled analysis in the INHANCE consortium. Int J Epidemiol 44(1):169–185

    Article  PubMed  PubMed Central  Google Scholar 

  39. Vaezi MF, Qadeer MA, Lopez R, Colabianchi N (2006) Laryngeal cancer and gastroesophageal reflux disease: a case–control study. Am J Med 119(9):768–776. doi:10.1016/j.amjmed.2006.01.019

    Article  PubMed  Google Scholar 

  40. Yun YH, Jung KW, Bae JM, Lee JS, Shin SA, Min Park S, Yul Huh B (2005) Cigarette smoking and cancer incidence risk in adult men: national Health Insurance Corporation Study. Cancer Detect Prev 29(1):15–24. doi:10.1016/j.cdp.2004.08.006

    Article  PubMed  Google Scholar 

  41. Zeka A, Gore R, Kriebel D (2003) Effects of alcohol and tobacco on aerodigestive cancer risks: a meta-regression analysis. Cancer Causes Control 14:897–906

    Article  PubMed  Google Scholar 

  42. Zhou J, Liu F, Zhang D, Chen B, Li Q, Zhou L, Tao L (2014) Significance of MDM2-309 polymorphisms and induced corresponding plasma MDM2 levels in susceptibility to laryngeal squamous cell carcinoma. DNA Cell Biol 33(2):88–94

    Article  CAS  PubMed  Google Scholar 

  43. Zvrko E, Gledović Z, Ljaljević A (2008) Risk factors for laryngeal cancer in Montenegro. Arh Hig Rada Toksikol 59(1):11–18

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jing-Jing Zuo or Ze-Zhang Tao.

Ethics declarations

Conflict of interest

Jing-Jing Zuo declares that he has no conflict of interest. Ze-Zhang Tao declares that he has no conflict of interest. Chen Chen declares that he has no conflict of interest. Zhang-Wei Hu declares that he has no conflict of interest. Ye-Xing Xu declares that she has no conflict of interest. An-Yuan Zheng declares that he has no conflict of interest. Yi Guo declares that he has no conflict of interest.

Funding

This study was funded by the National Natural Science Foundation of China (No. 81372880), and the Natural Science Foundation of Hubei Province of China (No. 2012FFA045).

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zuo, JJ., Tao, ZZ., Chen, C. et al. Characteristics of cigarette smoking without alcohol consumption and laryngeal cancer: overall and time-risk relation. A meta-analysis of observational studies. Eur Arch Otorhinolaryngol 274, 1617–1631 (2017). https://doi.org/10.1007/s00405-016-4390-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00405-016-4390-x

Keywords

Navigation