Cancer Res Treat.  2019 Oct;51(4):1392-1399. 10.4143/crt.2018.612.

Active and Passive Smoking, BRAF(V600E) Mutation Status, and the Risk of Papillary Thyroid Cancer: A Large-Scale Case-Control and Case-Only Study

• Kim KN
• Hwang Y
• Kim K
• Lee KE
• Park YJ
• Choi JY
• Park DJ
• Cho B
• Kang D
• Park SK

• KMID: 2460588
• DOI: http://doi.org/10.4143/crt.2018.612

Abstract

PURPOSE
The association between tobacco smoking and thyroid cancer remains uncertain. We evaluated the associations of active and passive smokingwith the risk of papillary thyroid cancer (PTC), the most common type of thyroid cancer, and with the BRAF(V600E) mutation, the most common oncogenic mutation in PTC related to poor prognosis.
MATERIALS AND METHODS
We conducted this study with newly diagnosed PTC patients (n=2,142) and community controls (n=21,420) individually matched to cases for age and sex. Information on active and passive smoking and potential confounders were obtained from structured questionnaires, anthropometric measurements, and medical records. BRAF(V600E) mutation status was assessed in PTC patients. We evaluated the associations of active and passive smoking with PTC and BRAF(V600E) mutation risk using conditional and unconditional logistic regression models, respectively.
RESULTS
We did not find associations between exposure indices of active and passive smoking and PTC risk in both men and women, except for the association between current smoking and lower PTC risk. Cumulative smoking ≥ 20 pack-years was associated with lower BRAF(V600E) mutation risk in male PTC patients (odds ratio [OR], 0.55; 95% confidence interval [CI], 0.30 to 1.00). The CI for the association was wider in female PTC patients (OR, 0.23; 95% CI, 0.02 to 2.62), possibly owing to a smaller sample size in this stratum.
CONCLUSION
We did not find consistent associations between active and passive smoking and PTC risk. Cumulative smoking ≥ 20 pack-years was associated with lower BRAF(V600E) mutation risk in male PTC patients.

Keyword

Smoking; Passive smoking; Papillary thyroid cancer; BRAF mutation; Case-control studies; Case-only studies

MeSH Terms

Case-Control Studies*
Female
Humans
Logistic Models
Male
Medical Records
Prognosis
Sample Size
Smoke
Smoking
Thyroid Gland*
Thyroid Neoplasms*
Tobacco Smoke Pollution*
Smoke
Tobacco Smoke Pollution

Reference

References

1. Pellegriti G, Frasca F, Regalbuto C, Squatrito S, Vigneri R. Worldwide increasing incidence of thyroid cancer: update on epidemiology and risk factors. J Cancer Epidemiol. 2013; 2013:965212.

2. Jung KW, Won YJ, Kong HJ, Lee ES; Community of Population-Based Regional Cancer Registries. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2015. Cancer Res Treat. 2018; 50:303–16.

3. Li N, Du XL, Reitzel LR, Xu L, Sturgis EM. Impact of enhanced detection on the increase in thyroid cancer incidence in the United States: review of incidence trends by socioeconomic status within the surveillance, epidemiology, and end results registry, 1980-2008. Thyroid. 2013; 23:103–10.

4. Cramer JD, Fu P, Harth KC, Margevicius S, Wilhelm SM. Analysis of the rising incidence of thyroid cancer using the Surveillance, Epidemiology and End Results national cancer data registry. Surgery. 2010; 148:1147–52.

5. Vigneri R, Malandrino P, Vigneri P. The changing epidemiology of thyroid cancer: why is incidence increasing? Curr Opin Oncol. 2015; 27:1–7.

6. Mack WJ, Preston-Martin S, Bernstein L, Qian D. Lifestyle and other risk factors for thyroid cancer in Los Angeles County females. Ann Epidemiol. 2002; 12:395–401.

7. Navarro Silvera SA, Miller AB, Rohan TE. Risk factors for thyroid cancer: a prospective cohort study. Int J Cancer. 2005; 116:433–8.

8. Xhaard C, Ren Y, Clero E, Maillard S, Brindel P, Rachedi F, et al. Differentiated thyroid carcinoma risk factors in French Polynesia. Asian Pac J Cancer Prev. 2014; 15:2675–80.

9. Iribarren C, Haselkorn T, Tekawa IS, Friedman GD. Cohort study of thyroid cancer in a San Francisco Bay area population. Int J Cancer. 2001; 93:745–50.

10. Cho A, Chang Y, Ahn J, Shin H, Ryu S. Cigarette smoking and thyroid cancer risk: a cohort study. Br J Cancer. 2018; 119:638–45.

11. Kitahara CM, Linet MS, Beane Freeman LE, Check DP, Church TR, Park Y, et al. Cigarette smoking, alcohol intake, and thyroid cancer risk: a pooled analysis of five prospective studies in the United States. Cancer Causes Control. 2012; 23:1615–24.

12. Moura MA, Bergmann A, Aguiar SS, Thuler LC. The magnitude of the association between smoking and the risk of developing cancer in Brazil: a multicenter study. BMJ Open. 2014; 4:e003736.

13. Zivaljevic V, Slijepcevic N, Sipetic S, Paunovic I, Diklic A, Zoric G, et al. Risk factors for well-differentiated thyroid cancer in men. Tumori. 2013; 99:458–62.

14. Myung SK, Lee CW, Lee J, Kim J, Kim HS. Risk factors for thyroid cancer: a hospital-based case-control study in Korean adults. Cancer Res Treat. 2017; 49:70–8.

15. Kabat GC, Kim MY, Wactawski-Wende J, Rohan TE. Smoking and alcohol consumption in relation to risk of thyroid cancer in postmenopausal women. Cancer Epidemiol. 2012; 36:335–40.

16. Sokic SI, Adanja BJ, Vlajinac HD, Jankovic RR, Marinkovic JP, Zivaljevic VR. Risk factors for thyroid cancer. Neoplasma. 1994; 41:371–4.

17. Xing M. BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocr Rev. 2007; 28:742–62.

18. Xing M, Alzahrani AS, Carson KA, Viola D, Elisei R, Bendlova B, et al. Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. JAMA. 2013; 309:1493–501.

19. Kim TH, Park YJ, Lim JA, Ahn HY, Lee EK, Lee YJ, et al. The association of the BRAF(V600E) mutation with prognostic factors and poor clinical outcome in papillary thyroid cancer: a meta-analysis. Cancer. 2012; 118:1764–73.

20. Lee KE, Park YJ, Cho B, Hwang Y, Choi JY, Kim SJ, et al. Protocol of a thyroid cancer longitudinal study (T-CALOS): a prospective, clinical and epidemiological study in Korea. BMJ Open. 2015; 5:e007234.

21. Health Examinees Study Group. The Health Examinees (HEXA) study: rationale, study design and baseline characteristics. Asian Pac J Cancer Prev. 2015; 16:1591–7.

22. Kim SJ, Lee KE, Myong JP, Park JH, Jeon YK, Min HS, et al. BRAF V600E mutation is associated with tumor aggressiveness in papillary thyroid cancer. World J Surg. 2012; 36:310–7.

23. Stansifer KJ, Guynan JF, Wachal BM, Smith RB. Modifiable risk factors and thyroid cancer. Otolaryngol Head Neck Surg. 2015; 152:432–7.

24. Paoff K, Preston-Martin S, Mack WJ, Monroe K. A case-control study of maternal risk factors for thyroid cancer in young women (California, United States). Cancer Causes Control. 1995; 6:389–97.

25. Marchetti A, Felicioni L, Malatesta S, Grazia Sciarrotta M, Guetti L, Chella A, et al. Clinical features and outcome of patients with non-small-cell lung cancer harboring BRAF mutations. J Clin Oncol. 2011; 29:3574–9.

26. Samowitz WS, Albertsen H, Sweeney C, Herrick J, Caan BJ, Anderson KE, et al. Association of smoking, CpG island methylator phenotype, and V600E BRAF mutations in colon cancer. J Natl Cancer Inst. 2006; 98:1731–8.

27. Asvold BO, Bjoro T, Vatten LJ. Association of serum TSH with high body mass differs between smokers and never-smokers. J Clin Endocrinol Metab. 2009; 94:5023–7.

28. Kleiman DA, Buitrago D, Crowley MJ, Beninato T, Veach AJ, Zanzonico PB, et al. Thyroid stimulating hormone increases iodine uptake by thyroid cancer cells during BRAF silencing. J Surg Res. 2013; 182:85–93.

29. Kim HJ, Park HK, Byun DW, Suh K, Yoo MH, Min YK, et al. Iodine intake as a risk factor for BRAF mutations in papillary thyroid cancer patients from an iodine-replete area. Eur J Nutr. 2018; 57:809–15.

30. Khoury MJ, Flanders WD. Nontraditional epidemiologic approaches in the analysis of gene-environment interaction: case-control studies with no controls! Am J Epidemiol. 1996; 144:207–13.

31. Jarvis MJ, Russell MA, Benowitz NL, Feyerabend C. Elimination of cotinine from body fluids: implications for noninvasive measurement of tobacco smoke exposure. Am J Public Health. 1988; 78:696–8.