Abstract
Purpose
Hormonal factors may play a role in the development of lung cancer in women. This study examined the relationship between lung cancer and reproductive factors in a large cohort of women, most of whom never smoked (97 %).
Methods
A cohort of 267,400 female textile workers in Shanghai, China, enrolled in a trial of breast self-examination provided information on reproductive history, demographical factors, and cigarette smoking at enrollment in 1989–91. The cohort was followed until July of 2000 for incidence of lung cancer; 824 cases were identified. Hazard ratios (HR) and 95 % confidence intervals (CI) associated with selected reproductive factors were calculated using Cox proportional hazards modeling, adjusting for smoking, age, and also parity when relevant.
Results
Nulliparous women were at increased risk compared to parous women (HR = 1.33, 95 % CI 1.00–1.77). Women who had gone through menopause at baseline were at increased risk compared to women of the same age who were still menstruating. Risk was higher in women with a surgical menopause (HR = 1.64, 95 % CI 0.96–2.79) than in those with a natural menopause (HR = 1.35, 95 % CI 0.84–2.18), and risk was highest in those postmenopausal women with a hysterectomy and bilateral oophorectomy at baseline (HR = 1.39, 95 % CI 0.96–2.00), although the risk estimates were not statistically significant.
Conclusions
These results support experimental data that demonstrate a biological role for hormones in lung carcinogenesis.
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References
Siegfried JM, Hershberger PA, Stabile LP (2009) Estrogen receptor signaling in lung cancer. Semin Oncol 36(6):524–531. doi:10.1053/j.seminoncol.2009.10.004
Wakelee HA, Chang ET, Gomez SL, Keegan TH, Feskanich D, Clarke CA, Holmberg L, Yong LC, Kolonel LN, Gould MK, West DW (2007) Lung Cancer Incidence in Never Smokers. J Clin Oncol 25(5):472–478. doi:10.1200/jco.2006.07.2983
Seow A, Koh WP, Wang R, Lee HP, Yu MC (2009) Reproductive variables, soy intake, and lung cancer risk among nonsmoking women in the Singapore Chinese Health Study. Cancer Epidemiol Biomarkers Prev 18(3):821–827. doi:10.1158/1055-9965.EPI-08-0892
Weiss JM, Lacey JV Jr, Shu XO, Ji BT, Hou L, Yang G, Li H, Rothman N, Blair A, Gao YT, Chow WH, Zheng W (2008) Menstrual and reproductive factors in association with lung cancer in female lifetime nonsmokers. Am J Epidemiol 168(11):1319–1325. doi:10.1093/aje/kwn257
Meinhold CL, Berrington de Gonzalez A, Bowman ED, Brenner AV, Jones RT, Lacey JV Jr, Loffredo CA, Perlmutter D, Schonfeld SJ, Trivers GE, Harris CC (2011) Reproductive and hormonal factors and the risk of nonsmall cell lung cancer. Int J Cancer 128(6):1404–1413. doi:10.1002/ijc.25434
Baik CS, Strauss GM, Speizer FE, Feskanich D (2010) Reproductive factors, hormone use, and risk for lung cancer in postmenopausal women, the Nurses’ Health Study. Cancer Epidemiol Biomarkers Prev 19(10):2525–2533. doi:10.1158/1055-9965.EPI-10-0450
Paulus JK, Asomaning K, Kraft P, Johnson BE, Lin X, Christiani DC (2010) Parity and risk of lung cancer in women. Am J Epidemiol 171(5):557–563. doi:10.1093/aje/kwp441
Liu Y, Inoue M, Sobue T, Tsugane S (2005) Reproductive factors, hormone use and the risk of lung cancer among middle-aged never-smoking Japanese women: a large-scale population-based cohort study. Int J Cancer 117(4):662–666. doi:10.1002/ijc.21229
Brinton LA, Gierach GL, Andaya A, Park Y, Schatzkin A, Hollenbeck A, Spitz MR (2011) Reproductive and hormonal factors and lung cancer risk in the NIH-AARP Diet and Health Study cohort. Cancer Epidemiol Biomarkers Prev. doi:10.1158/1055-9965.epi-10-1325
Kabat GC, Miller AB, Rohan TE (2007) Reproductive and hormonal factors and risk of lung cancer in women: a prospective cohort study. Int J Cancer 120(10):2214–2220. doi:10.1002/ijc.22543
Kreuzer M, Gerken M, Heinrich J, Kreienbrock L, Wichmann HE (2003) Hormonal factors and risk of lung cancer among women? Int J Epidemiol 32(2):263–271. doi:10.1093/ije/dyg064
Koushik A, Parent ME, Siemiatycki J (2009) Characteristics of menstruation and pregnancy and the risk of lung cancer in women. Int J Cancer 125(10):2428–2433. doi:10.1002/ijc.24560
Parker WH, Broder MS, Chang E, Feskanich D, Farquhar C, Liu Z, Shoupe D, Berek JS, Hankinson S, Manson JE (2009) Ovarian conservation at the time of hysterectomy and long-term health outcomes in the Nurses’ Health Study. Obstet Gynecol 113(5):1027–1037. doi:10.1097/AOG.0b013e3181a11c64
Chlebowski RT, Anderson GL, Manson JE, Schwartz AG, Wakelee H, Gass M, Rodabough RJ, Johnson KC, Wactawski-Wende J, Kotchen JM, Ockene JK, O’Sullivan MJ, Hubbell FA, Chien JW, Chen C, Stefanick ML (2010) Lung cancer among postmenopausal women treated with estrogen alone in the women’s health initiative randomized trial. J Natl Cancer Inst 102(18):1413–1421. doi:10.1093/jnci/djq285
Chlebowski RT, Schwartz AG, Wakelee H, Anderson GL, Stefanick ML, Manson JE, Rodabough RJ, Chien JW, Wactawski-Wende J, Gass M, Kotchen JM, Johnson KC, O’Sullivan MJ, Ockene JK, Chen C, Hubbell FA (2009) Oestrogen plus progestin and lung cancer in postmenopausal women (Women’s Health Initiative trial): a post hoc analysis of a randomised controlled trial. Lancet 374(9697):1243–1251. doi:10.1016/S0140-6736(09)61526-9
Vessey M, Painter R, Yeates D (2003) Mortality in relation to oral contraceptive use and cigarette smoking. Lancet 362(9379):185–191. doi:10.1016/S0140-6736(03)13907-4
Dorjgochoo T, Shu XO, Li HL, Qian HZ, Yang G, Cai H, Gao YT, Zheng W (2009) Use of oral contraceptives, intrauterine devices and tubal sterilization and cancer risk in a large prospective study, from 1996 to 2006. Int J Cancer 124(10):2442–2449. doi:10.1002/ijc.24232
Wu-Williams AH, Dai XD, Blot W, Xu ZY, Sun XW, Xiao HP, Stone BJ, Yu SF, Feng YP, Ershow AG et al (1990) Lung cancer among women in north-east China. Br J Cancer 62(6):982–987. doi:10.1038/bjc.1990.421
Elliott AM, Hannaford PC (2006) Use of exogenous hormones by women and lung cancer: evidence from the Royal College of General Practitioners’ Oral Contraception Study. Contraception 73(4):331–335. doi:10.1016/j.contraception.2005.10.003
Rosenblatt KA, Gao DL, Ray RM, Nelson ZC, Wernli KJ, Li W, Thomas DB (2007) Monthly injectable contraceptives and the risk of all cancers combined and site-specific cancers in Shanghai. Contraception 76(1):40–44. doi:10.1016/j.contraception.2007.03.004
Rosenblatt KA, Gao DL, Ray RM, Nelson ZC, Wernli KJ, Li W, Thomas DB (2009) Oral contraceptives and the risk of all cancers combined and site-specific cancers in Shanghai. Cancer Causes Control 20(1):27–34. doi:10.1007/s10552-008-9213-y
Thomas DB, Gao DL, Ray RM, Wang WW, Allison CJ, Chen FL, Porter P, Hu YW, Zhao GL, Pan LD, Li W, Wu C, Coriaty Z, Evans I, Lin MG, Stalsberg H, Self SG (2002) Randomized trial of breast self-examination in Shanghai: final results. J Natl Cancer Inst 94(19):1445. doi:10.1093/jnci/94.19.1445
Rothman KJ, Greenland S (1998) Modern Epidemiology, 2nd edn. Lippincott-Raven, Philadelphia, PA
Rosenblatt KA, Gao DL, Ray RM, Rowland MR, Nelson ZC, Wernli KJ, Li W, Thomas DB (2006) Induced abortions and the risk of all cancers combined and site-specific cancers in Shanghai. Cancer Causes Control 17(10):1275–1280. doi:10.1007/s10552-006-0067-x
Astrakianakis G, Seixas NS, Ray R, Camp JE, Gao DL, Feng Z, Li W, Wernli KJ, Fitzgibbons ED, Thomas DB, Checkoway H (2007) Lung cancer risk among female textile workers exposed to endotoxin. J Natl Cancer Inst 99(5):357. doi:10.1093/jnci/djk063
Checkoway H, Ray RM, Lundin JI, Astrakianakis G, Seixas NS, Camp JE, Wernli KJ, Fitzgibbons ED, Li W, Feng Z, Gao DL, Thomas DB (2011) Lung cancer and occupational exposures other than cotton dust and endotoxin among women textile workers in Shanghai, China. Occup Environ Med 68:425–429. doi:10.1136/oem.2010.059519
Astrakianakis G, Seixas NS, Ray R, Camp JE, Gao DL, Feng Z, Li W, Wernli KJ, Fitzgibbons ED, Thomas DB, Checkoway H (2010) Re: lung cancer risk among female textile workers exposed to endotoxin. J Natl Cancer Inst 102(12):913–914. doi:10.1093/jnci/djq155
Borgan O, Langholz B, Samuelsen SO, Goldstein L, Pogoda J (2000) Exposure stratified case-cohort designs. Lifetime Data Anal 6(1):39–58. doi:10.1023/A:1009661900674
Langholz B, Jiao J (2007) Computational methods for case-cohort studies. Comput Stat Data An 51(8):3737–3748. doi:10.1016/j.csda.2006.12.028
Stabile LP, Davis ALG, Gubish CT, Hopkins TM, Luketich JD, Christie N, Finkelstein S, Siegfried JM (2002) Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor α and β and show biological responses to estrogen. Cancer Res 62(7):2141–2150
Sun S, Schiller JH, Gazdar AF (2007) Lung cancer in never smokers- a different disease. Nat Rev Cancer 7(10):778–790. doi:10.1038/nrc2190
Stabile LP, Lyker JS, Gubish CT, Zhang W, Grandis JR, Siegfried JM (2005) Combined targeting of the estrogen receptor and the epidermal growth factor receptor in non-small cell lung cancer shows enhanced antiproliferative effects. Cancer Res 65(4):1459–1470. doi:10.1158/0008-5472.CAN-04-1872
Márquez-Garbán DC, Chen H-W, Goodglick L, Fishbein MC, Pietras RJ (2009) Targeting aromatase and estrogen signaling in human non-small cell lung cancer. Ann N Y Acad Sci 1155(1):194–205. doi:10.1111/j.1749-6632.2009.04116.x
Lim WY, Chen Y, Chuah KL, Eng P, Leong SS, Lim E, Lim TK, Ng A, Poh WT, Tee A, Teh M, Salim A, Seow A (2012) Female reproductive factors, gene polymorphisms in the estrogen metabolism pathway, and risk of lung cancer in Chinese women. Am J Epidemiol 175(6):492–503. doi:10.1093/aje/kwr332
Zhou BS, Wang TJ, Guan P, Wu JM (2000) Indoor air pollution and pulmonary adenocarcinoma among females: a case–control study in Shenyang, China. Oncol Rep 7:1253–1260
Brenner AV, Wang Z, Kleinerman RA, Lei S, Metayer C, Wang W, Lubin JH (2003) Menstrual and reproductive factors and risk of lung cancer among Chinese women, Eastern Gansu Province, 1994–1998. J Epidemiol 13(1):22–28. doi:10.2188/jea.13.22
Gao YT, Blot WJ, Zheng W, Ershow AG, Hsu CW, Levin LI, Zhang R, Fraumeni JF Jr (1987) Lung cancer among Chinese women. Int J Cancer 40(5):604–609. doi:0.1002/ijc.2910400505
Dahabreh IJ, Trikalinos TA, Paulus JK (2012) Parity and risk of lung cancer in women: systematic review and meta-analysis of epidemiological studies. Lung Cancer 76(2):150–158. doi:10.1016/j.lungcan.2011.10.014
Wernli KJ, Ray RM, Gao DL, Fitzgibbons ED, Camp JE, Astrakianakis G, Seixas N, Li W, De Roos AJ, Feng Z, Thomas DB, Checkoway H (2008) Occupational risk factors for endometrial cancer among textile workers in Shanghai. China. Am J Ind Med 51(9):673–679. doi:10.1002/ajim.20614
de Kleijn MJ, van der Schouw YT, Verbeek AL, Peeters PH, Banga JD, van der Graaf Y (2002) Endogenous estrogen exposure and cardiovascular mortality risk in postmenopausal women. Am J Epidemiol 155(4):339–345. doi:10.1093/aje/155.4.339
Henderson BE, Feigelson HS (2000) Hormonal carcinogenesis. Carcinogenesis 21(3):427–433. doi:10.1093/carcin/21.3.427
Lin Y, Cai L (2012) Environmental and dietary factors and lung cancer risk among Chinese women: a case–control study in southeast China. Nutr Cancer 64(4):508–514. doi:10.1080/01635581.2012.668743
Schwartz AG, Wenzlaff AS, Prysak GM, Murphy V, Cote ML, Brooks SC, Skafar DF, Lonardo F (2007) Reproductive factors, hormone use, estrogen receptor expression and risk of non small-cell lung cancer in women. J Clin Oncol 25(36):5785–5792. doi:10.1200/JCO.2007.13.3975
Liao ML, Wang JH, Wang HM, Ou AQ, Wang XJ, You WQ (1996) A study of the association between squamous cell carcinoma and adenocarcinoma in the lung, and history of menstruation in Shanghai women. China. Lung Cancer 14(Suppl 1):S215–S221. doi:10.1016/S0169-5002(96)90224-X
Wu AH, Yu MC, Thomas DC, Pike MC, Henderson BE (1988) Personal and family history of lung disease as risk factors for adenocarcinoma of the lung. Cancer Res 48(24 Pt 1):7279–7284
Taioli E, Wynder EL (1994) Re: endocrine factors and adenocarcinoma of the lung in women. J Natl Cancer Inst 86(11):869–870. doi:10.1093/jnci/86.11.869
Seow A, Poh W-T, Teh M, Eng P, Wang Y-T, Tan W-C, Yu MC, Lee H-P (2000) Fumes from meat cooking and lung cancer risk in Chinese women. Cancer Epidemiol Biomarkers Prev 9(11):1215–1221
Acknowledgments
The authors would like to acknowledge the Shanghai study manager (Wen Wan Wang), industrial hygienists and Shanghai field workers for their extensive efforts as well as George Astrakianakis, Noah Seixas, Janice Camp, Karen Wernli, and Dawn Fitzgibbons for their work on the endotoxin exposure assessment. Funding provided from the National Cancer Institute at the National Institutes of Health (R01CA80180). Dr. Applebaum was supported by K01OH009390.
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The authors declare that they have no conflict of interests.
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Gallagher, L.G., Rosenblatt, K.A., Ray, R.M. et al. Reproductive factors and risk of lung cancer in female textile workers in Shanghai, China. Cancer Causes Control 24, 1305–1314 (2013). https://doi.org/10.1007/s10552-013-0208-y
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DOI: https://doi.org/10.1007/s10552-013-0208-y