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Breast Cancer Risk Among Women Who Start Smoking as Teenagers

¹ Institute of Community Medicine, University of Tromsö, ² NIEHS, Epidemiology Branch, Research Triangle Park, North Carolina; ³ International Agency for Research on Cancer, ⁴ Institut National de la Santé et de la Recherche Médicale, Lyon, France; ⁵ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden; ⁶ Finish Cancer Registry, Liisankatu, Helsinki, Finland

Inger T. Gram, Institute of Community Medicine, University of Tromsö, N-9037 Tromsö, Norway. Phone: +47-7764-4816; Fax: +47-7764-4831. E-mail: inger.gram{at}ism.uit.no

	Abstract

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Objective: To examine the effect of smoking on breast cancer risk in a large population-based cohort of women, many of whom started smoking as teenagers.

Methods: We followed 102,098 women, ages 30 to 50 years, completing a mailed questionnaire at recruitment to the Norwegian-Swedish Cohort Study in 1991/1992, through December 2000. We used Cox proportional hazard regression models to estimate relative risk (RR) of breast cancer associated with different measures of smoking initiation, duration, and intensity adjusting for confounding variables. We conducted analyses on the entire study population, among women who had smoked for at least 20 years, among nondrinkers, and separately for each country.

Results: Altogether, 1,240 women were diagnosed with incident, invasive breast cancer. Compared with never smokers, women who smoked for at least 20 years and who smoked 10 cigarettes or more daily had a RR of 1.34 (95% CI, 1.06-1.70). Likewise, those who initiated smoking prior to their first birth (1.27, 1.00-1.62), before menarche (1.39, 1.03-1.87), or before age 15 (1.48, 1.03-2.13) had an increased risk. In contrast, women who had smoked for at least 20 years, but started after their first birth, did not experience an increased breast cancer risk. The increased RR associated with smoking was observed among nondrinkers of alcohol, women with and without a family history of breast cancer, premenopausal and postmenopausal women, and in both countries.

Conclusion: Our results support the notion that women who start smoking as teenagers and continue to smoke for at least 20 years may increase their breast cancer risk.

Key Words: Smoking • breast cancer • incidence • cohort • teenager • age at first birth • alcohol • risk factors • epidemiology • women • Norway • Sweden

	Introduction

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The relationship between smoking and the risk of breast cancer has been unclear for several decades, and whether or not young women should be warned about smoking as a possible cause of breast cancer remains controversial (1-4). In 1982, MacMahon et al. (5) first suggested a protective effect, whereas Hiatt and Fireman, 4 years later, proposed a detrimental effect of smoking on breast cancer risk (6). Since then, studies have continued to show positive, inverse, or null associations (4, 7-9).

In 2002, a pooled analysis of 53 epidemiologic studies found that the positive relationship between smoking and breast cancer was likely due to confounding by alcohol consumption, an established cause of breast cancer (10). However, this study used crude smoking measures, e.g. ever versus never smokers and also including passive smokers in the reference group, possibly diluting a weak effect. From a public health perspective, even a small increase in the risk of breast cancer among women who smoke may account for a substantial number of cancer cases in populations where the prevalence of smoking is high.

In 1982, Russo et al. (11) hypothesized that the mammary tissue is particularly susceptible to carcinogenic exposures during the years from pre-puberty to the first birth, when the mammary cells differentiate. Therefore, we examined the association between cigarette smoking and breast cancer risk in a large population-based cohort of women who were teenagers when smoking prevalence increased markedly among young Scandinavian women.

	Materials and Methods

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Study Population
The Norwegian-Swedish Women's Lifestyle and Health Cohort Study was initiated in 1991/1992. In Norway, a nationwide random sample of 100,000 women, born between 1943 and 1957, was drawn from the National Population Register at Statistics Norway. In Sweden, a random sample of 96,000 women, born between 1943 and 1962, residing in the Uppsala Health Care Region, was drawn from the National Population Register at Statistics Sweden.

All women received a letter inviting them to participate in the study. The letter requested that they provide written informed consent, and contained a comprehensive questionnaire that was to be completed and returned in a prestamped envelope. The common set of questions included detailed assessment of smoking habits, alcohol consumption, contraceptive use, reproductive history, history of breast cancer in the mother and sister(s), height and current weight [allowing us to calculate body mass index (BMI) as weight in kilograms divided by the square of height in meters], and other aspects of lifestyle habits. In both countries, the national Data Inspection Boards and the regional Medical Ethical Committees approved the study. All women gave written informed consent to participate.

Smoking Assessment
The questionnaire elicited information on current and previous smoking history, and asked if the women lived with a smoker or had done so during childhood. We categorized women who had never smoked, but been exposed to passive smoke at home as "passive smokers" and those reporting neither as "never smokers".

We categorized the ever-active smokers according to current and past smoking status, smoking duration; number of cigarettes smoked daily, pack-years of smoking (i.e., number of cigarettes smoked per day, divided by 20, multiplied by the number of years smoked), and years of smoking latency (i.e., age at cohort enrollment minus age of smoking initiation). We further separated them into three descriptors of timing of smoking initiation: (a) age they started smoking, (b) whether they started smoking before or around menarche, and (c) before their first birth.

We classified women who had smoked for at least 20 years as long-term smokers, and calculated their average smoking duration, according to the three descriptors of timing of smoking initiation. We categorized past smokers according to smoking recency, i.e., years since they stopped smoking.

Other Exposures
Women who reported a natural menopause or a bilateral oophorectomy at cohort enrollment were considered postmenopausal, regardless of age at hysterectomy, or use of hormone replacement therapy. Women were classified as postmenopausal when they reached 50 years of age during follow-up. We calculated average daily consumption of alcohol in grams based on the content of pure alcohol in the different sorts of beverages among drinkers. Women who reported to be teetotalers, and those answering "seldom" or "never" in the frequency table, are from hereon referred to as nondrinkers. Their alcohol consumption was set to 0.

Follow-up
In Norway, 57,584 (57.6%) and in Sweden 49,259 (51.3%) women returned completed questionnaires, resulting in an overall response rate of 54.5%. The cohort data were linked to the national registries of cancer and statistics in Norway and Sweden, to identify all incident cancer cases and deaths/emigrations, respectively. Woman-years were calculated from the start of follow-up to the date of diagnosis of primary invasive breast cancer, the date of emigration, death, or the end of follow-up, i.e., December 31, 2000, whichever occurred first.

Among the 106,841 women included, 789 emigrated and 1,360 died during follow-up. We excluded 5 women due to missing vital status information (whether they were alive, dead, or emigrated) in the available register files, 15 women who had emigrated or died before the start of follow-up, and 1,681 women who were diagnosed with any invasive cancer prior to the start of follow-up for a total of 1,701. We excluded 3,042 women with no information on smoking history, leaving 102,098 subjects in the analytic cohort.

Statistical Analysis
We obtained crude breast cancer incidence rates by dividing the number of cases by the total number of woman-years in that exposure category. The rates were then age-adjusted to the world standard population (12). We estimated the relative risk (RR) of breast cancer associated with different measures of smoking exposure as described by Cox (13). We tested for trends across categories of smoking variables by assigning equally spaced scores to the categories and treating the variable as continuous in the analyses. The trend test analyses did not include passive smokers. Unless otherwise specified, the reference group is designated as never smokers throughout the paper.

Potential confounding variables for the smoking and breast cancer association were examined and, those of importance, i.e., age at enrollment, age at menarche, age at first birth, number of children, menopausal status, family history of breast cancer, hormonal contraceptive use, consumption of alcohol, and BMI, were included in the final models. Age at first birth (<21, 21-24, 25+) and parity (0, 1, 2, 3+) were considered as a set of indicator variables. The multivariate analyses presented here are based on 91,125 women with information on the above listed variables. We repeated all analyses excluding 60 women diagnosed with breast cancer during the first 12 months of follow-up. The RR estimates obtained in this way were not materially different from the results presented in the paper (data not shown).

We conducted analyses on the entire study population, among long-term ever smokers, among nondrinkers, and separately for each country. We also compared the RR of breast cancer among long-term smokers stratified by country and by two categories (high/low risk) of established breast cancer risk factors. Subsequently, we conducted analyses including passive smokers in the reference group. Because smoking influences BMI and age at menopause, we also conducted analyses excluding BMI and age at menopause from the models, one by one, and both at the same time, as well as setting menopause at 54 years for never smokers and 52 years for current smokers.

We did the Cox proportional hazards analyses with the PHREG procedure in the SAS statistical package (14). We entered multiplicative terms between smoking and possible effect modifiers in the proportional hazards model to evaluate interaction, and tested for heterogeneity between strata with Wald ² statistics. RRs are given with 95% CIs. Results were considered as statistically significant if the P value was 0.05 or less, and 95% CIs are reported throughout the paper. All P values are two-sided.

	Results

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During the 924,768 person-years of observation, 1,240 incident cases of primary invasive breast cancer, confirmed by histology, were identified. Altogether, 64% of the women were reported to be ever smokers, whereas 13% were classified as never smokers. Table 1 shows that Norwegian women were more likely to be past or current smokers than Swedish women (P < 0.001).

The age-adjusted incidence rates of breast cancer were 114 per 100,000 woman-years among never smokers, 120 among past-smokers, and 135 among current smokers. The corresponding rate among women who had been exposed to passive smoking at home was 134 per 100,000 woman-years. A multivariate model based on 1,130 cases with complete information on the potential confounders yielded a nonsignificant increased RR for past 1.15 (95% CI, 0.94-1.41), current 1.17 (95% CI, 0.95-1.45), and passive 1.21 (95% CI, 0.98-1.50) smokers compared with never smokers. An ordinal trend test across three smoking groups (never, past, and current) was not statistically significant. We also collapsed past and current smokers and used both passive and never smokers as the reference group. This model yielded a RR estimate for ever smokers of 1.0 (95% CI, 0.98-1.50). We further examined the association between the time since subjects quit smoking (and different combinations of childhood and current exposures at home among passive smokers) and breast cancer risk. No meaningful results were revealed (data not shown).

Table 3 shows the RR of breast cancer according to various measures of smoking exposure among current and long-term smokers compared with never smokers. In the analysis including all women, current smokers who began smoking before 15 years of age, those who smoked >10 cigarettes a day, or had smoked at least 20 pack-years all had increased risk. Trend tests across the four exposure categories (including the reference group) for number of cigarettes smoked daily (P = 0.03), duration of smoking (P = 0.05), and number of pack-years (P = 0.01) were significant. We observed even stronger associations between smoking and breast cancer risk when the models included only long-term smokers. Those who began smoking before or around menarche had a 39%, and those starting before their first birth had a 27% statistically significant increased risk of developing breast cancer. When these models were restricted to nondrinkers, women who started smoking before their first birth, or had a smoking latency period of >25 years, presented a significantly increased risk of developing breast cancer by about 75%. The results among the nondrinkers are based on a small number of cases, and have wide confidence intervals (Table 3).

Among long-term smokers, those who started before the age of 15 had a 20% nonsignificant increased risk when those who started between ages 15 and 19 were the reference group. The former group had on average smoked 1.4 years longer than the comparison group (P = 0.001). Likewise, those who started before or around menarche had smoked 1.2 years longer (P = 0.001) and had a 15% increased risk compared with long-term smokers who started after menarche. Similarly, long-term smokers who started before their first birth, had smoked 0.8 years longer (P = 0.001) and had an almost 40% increased risk when the reference group was those who started smoking after their first birth.

The RR of breast cancer among ever smokers compared with never smokers were the same in Norway and Sweden when stratified by country, i.e., 1.24 (95% CI, 0.90-1.70). Table 4 shows the RR estimates among long-term smokers compared with never smokers, after stratification by different risk factors for breast cancer. All risk estimates, except for menarche before age 13, were above unity. The test for heterogeneity was not significant for any of the risk factors. The results from Table 4 stayed materially the same when we included passive smokers in the reference group or did country-specific analyses (data not shown).

	Discussion

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Our study has several strengths. The smoking histories were obtained at enrollment and, hence, are not subject to recall bias. We have the ability to separate current and past smokers, and to exclude women exposed to passive smoking at home from the reference group. We have a large proportion of current smokers at enrollment, and have the ability to stratify long-term smokers according to descriptors of smoking initiation, and compare the different groups of long-term smokers. We have detailed information on, and can control for established breast cancer risk factors: many of which vary according to smoking status. Additional strengths include the large size of the cohort, that it is sampled from a general population, and has virtually complete follow-up. The cohort shows the expected association between oral contraceptive use and breast cancer, and between hormonal contraceptive use and ovarian cancer (15, 16). We have shown that the study participants are similar to nonparticipants with respect to several breast cancer risk factors (17). Furthermore, the cumulated incidence rates during follow-up for all cancer sites as well as for breast cancer sites are almost identical as those reported to the national cancer registry in the same period, suggesting that our findings may be valid in the general population (18). Indeed, the smoking habits among our Norwegian and Swedish women reflect known smoking patterns in the respective countries.

Our study has several limitations. We have only crude and limited information about passive smoking. Also, because time of smoking initiation and duration are highly correlated, in this relatively young cohort, it is very difficult to separate the effects. Furthermore, we do not have updated information on changes in smoking habits, hormonal contraceptive use, hormonal replacement therapy, BMI, menopausal status, and alcohol consumption during follow-up, nor lifetime alcohol consumption. However, few Scandinavian women start to smoke after the age of 30, which is the lowest age of enrollment in our study. If current smokers quit smoking during follow-up, this may have diluted our results. We already show that by setting the same age at menopause for smokers and never smokers, we have biased the displayed results towards the null. In a recent study by Horn-Ross et al. (19), elevated breast cancer risk was most evident for recent drinking with no clear pattern for consumption during earlier periods of life. The lack of lifetime alcohol consumption in our study may still be a concern. Because the distribution of established risk factors for breast cancer vary according to smoking status in our cohort, unknown risk factors may do the same. There may be some residual confounding in both directions due to the factors listed above.

Due to smoking trends in Norway and Sweden, women in our cohort have a higher smoking prevalence during their teenage years than women included in the three previous population-based studies from the Scandinavian countries (20-22). Nevertheless, in our Norwegian-Swedish case-control study including women <45 years old at the time of the data collection in 1985, we did find a 30% nonsignificant increased breast cancer risk among those who started smoking before 15 years old (20). Similarly, the Swedish follow-up study, where the youngest women were 18 years old at the time of the data collection in 1963, revealed a 20% nonsignificant increased risk among those who began smoking before the age of 19 (22). The Norwegian follow-up study, where the youngest women were 35 years old at enrollment in the mid-1970s, found no association with breast cancer risk (21).

To date, 13 cohort studies (6, 21, 23-32) have examined the association between smoking and breast cancer risk. The results of these studies are mixed, but generally show no association. However, the four most recent studies and the only ones including >500 breast cancer cases do find a positive association with either long-term smoking (30), smoking prior to a first birth (29), or both (31, 32).

In contrast to the women in the studies by Egan et al. (29) and Terry et al. (30), our women were aged <50 years at enrollment, thus belonging to birth cohorts with different smoking habits than the two North American studies. The most recently published studies (31, 32) recruited participants during the 1990s, as we did. However, there were only 5% and 13% current smokers at enrollment in the California Teachers Study (31) and in the Nurses' Health Study II (32), respectively. In comparison, we have 28% current smokers in our sample from the general population. This may explain the consistency of our results.

The present study shows a consistent dose-response, which enhances the biological plausibility of an increased breast cancer risk due to smoking. Plasma lipoproteins may transport the carcinogens in the tobacco smoke to the breast (33) where they can be stored in breast adipose tissue (34, 35) and could then be metabolized and activated by human mammary epithelial cells. Furthermore, the breast tissue of smokers have a higher prevalence of smoking-specific DNA adducts and p53 gene mutations compared with that in nonsmokers (7). This all supports the likelihood of a positive association between cigarette smoking and breast cancer risk. The increased risk associated with smoking prior to a first birth is in accordance with data from epidemiologic and animal studies (7, 11, 36, 37). One important result from our study is that we find no increased risk among women who initiate smoking after the first birth. This supports the notion that breast tissue becomes more resistant to the carcinogens in tobacco smoke after differentiation.

Our study finds that women who start smoking at young ages, and continue to smoke for at least 20 years increase their breast cancer risk. The fact that teenagers who smoke today tend to initiate smoking at earlier ages than in previous generations may have implications for targeted efforts to reduce breast cancer risk. Teenage girls and adult women should be given yet another reason to avoid, and to quit smoking.

	Footnotes

 
Grant support: In Norway, the study was supported by grants from the National CancerInstitute of the USA (grant CA 52449), the Norwegian Cancer Society (grant DNK 90050),the Aakre Foundation, and the Norwegian Research Council (Visiting Scientist Award grant 148365/300) for Dr. Gram's work at the IARC, Lyon, France. In Sweden, the Swedish Council supported the study for Planning and Coordination of Research, Swedish Cancer Society,Organon, Pharmacia, Medical Products Agency, AFA, US Army Breast Cancer Research Program, and Schering-Plough.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 5/19/04; revised 7/ 8/04; accepted 7/20/04.

	References

Top Abstract Introduction Materials and Methods Results Discussion References

 

1. Kuper H, Boffetta P, Adami HO. Tobacco use and cancer causation: association by tumour type. J Intern Med 2002;252:206–24.[CrossRef][Medline]
2. Chaturvedi P. Does smoking increase the risk of breast cancer? Lancet Oncol 2003;4:657–8.
3. Beral V, Doll R, Peto R, Reeves G. Does smoking increase the risk of breast cancer? Lancet Oncol 2003;4:658.
4. Vineis P, Alavanja M, Buffler P, et al. Tobacco and cancer: recent epidemiological evidence. J Natl Cancer Inst 2004;96:99–106.[Free Full Text]
5. MacMahon B, Trichopoulos D, Cole P, Brown J. Cigarette smoking and urinary estrogens. N Engl J Med 1982;307:1062–5.[Medline]
6. Hiatt RA, Fireman BH. Smoking, menopause, and breast cancer. J Natl Cancer Inst 1986;76:833–8.
7. Terry PD, Rohan TE. Cigarette smoking and the risk of breast cancer in women: a review of the literature. Cancer Epidemiol Biomarkers Prev 2002;11:953–71.[Abstract/Free Full Text]
8. Morabia A. Active and passive smoking in breast cancer. Epidemiology 2002;13:744–5.[Medline]
9. IARC Working Group. Tobacco Smoke and involuntary smoking (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans).IARC Monogr 2004;83:11452.
10. Hamajima N, Hirose K, Tajima K, et al. Alcohol, tobacco and breast cancer-collaborative reanalysis of individual data from 53 epidemiological studies, including 58,515 women with breast cancer and 95,067 women without the disease. Br J Cancer 2002;87:1234–45.[CrossRef][Medline]
11. Russo J, Tay LK, Russo IH. Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat 1982;2:5–73.[CrossRef][Medline]
12. Parkin DM, Whelan SL, Ferlay J, Teppo L, Thomas DB. Cancer incidence in five continents. Vol. VIII. Lyon: IARC;2002.
13. Cox D. Regression models and life-tables.J R Stat Soc, Ser B Stat Methodol. 1972;34:187–220.
14. SAS/STAT®. User's Guide Version. 8th ed. Cary (NC): SAS Institute, Inc.; 1999.
15. Kumle M, Weiderpass E, Braaten T, Persson I, Adami HO, Lund E. Use of oral contraceptives and breast cancer risk: The Norwegian-Swedish Women's Lifestyle and Health Cohort Study. Cancer Epidemiol Biomarkers Prev 2002;11:1375–81.[Abstract/Free Full Text]
16. Kumle M, Weiderpass E, Braaten T, Adami HO, Lund E. Risk for invasive and borderline epithelial ovarian neoplasias following use of hormonal contraceptives: the Norwegian-Swedish Women's Lifestyle and Health Cohort Study. Br J Cancer 2004;90:1386–91.[Medline]
17. Lund E, Gram IT. Response rate according to title and length of questionnaire.Scand J Soc Med, Suppl. 1998;26:154–60.
18. Lund E, Kumle M, Braaten T, et al. External validity in a population-based national prospective study—the Norwegian Women and Cancer Study (NOWAC). Cancer Causes Control 2003;14:1001–8.[CrossRef][Medline]
19. Horn-Ross PL, Canchola AJ, West DW, et al. Patterns of alcohol consumption and breast cancer risk in the California Teachers Study cohort. Cancer Epidemiol Biomarkers Prev 2004;13:405–11.[Abstract/Free Full Text]
20. Adami HO, Lund E, Bergstrom R, Meirik O. Cigarette smoking, alcohol consumption and risk of breast cancer in young women. Br J Cancer 1988;58:832–7.[Medline]
21. Vatten LJ, Kvinnsland S. Cigarette smoking and risk of breast cancer: a prospective study of 24,329 Norwegian women. Eur J Cancer 1990;26:830–3.
22. Nordlund LA, Carstensen JM, Pershagen G. Cancer incidence in female smokers: a 26-year follow-up. Int J Cancer 1997;73:625–8.[CrossRef][Medline]
23. Hiatt RA, Klatsky AL, Armstrong MA. Alcohol consumption and the risk of breast cancer in a prepaid health plan. Cancer Res 1988;48:2284–7.[Abstract/Free Full Text]
24. Schatzkin A, Carter CL, Green SB, et al. Is alcohol consumption related to breast cancer? Results from the Framingham Heart Study. J Natl Cancer Inst 1989;81:31–5.[Abstract/Free Full Text]
25. London SJ, Colditz GA, Stampfer MJ, Willett WC, Rosner BA, Speizer FE. Prospective study of smoking and the risk of breast cancer. J Natl Cancer Inst 1989;81:1625–31.[Abstract/Free Full Text]
26. Hunter DJ, Hankinson SE, Hough H, et al. A prospective study of NAT2 acetylation genotype, cigarette smoking, and risk of breast cancer. Carcinogenesis 1997;18:2127–32.[Abstract/Free Full Text]
27. Zheng W, Deitz AC, Campbell DR, et al. N-acetyltransferase 1 genetic polymorphism, cigarette smoking, well-done meat intake, and breast cancer risk. Cancer Epidemiol Biomarkers Prev 1999;8:233–9.[Abstract/Free Full Text]
28. Manjer J, Malina J, Berglund G, Bondeson L, Garne JP, Janzon L. Breast cancer incidence in ex-smokers in relation to body mass index, weight gain and blood lipid levels. Eur J Cancer Prev 2001;10:281–7.[Medline]
29. Egan KM, Stampfer MJ, Hunter D, et al. Active and passive smoking in breast cancer: prospective results from the Nurses' Health Study. Epidemiology 2002;13:138–45.[CrossRef][Medline]
30. Terry PD, Miller AB, Rohan TE. Cigarette smoking and breast cancer risk: a long latency period? Int J Cancer 2002;100:723–8.
31. Reynolds P, Hurley S, Goldberg DE, et al. Active smoking, household passive smoking, and breast cancer: evidence from the California Teachers Study. J Natl Cancer Inst 2004;96:29–37.[Abstract/Free Full Text]
32. Al Delaimy WK, Cho E, Chen WY, Colditz G, Willet WC. A prospective study of smoking and risk of breast cancer in young adult women. Cancer Epidemiol Biomarkers Prev 2004;13:398–404.[Abstract/Free Full Text]
33. Plant AL, Benson DM, Smith LC. Cellular uptake and intracellular localization of benzo(a)pyrene by digital fluorescence imaging microscopy. J Cell Biol 1985;100:1295–308.[Abstract/Free Full Text]
34. Morris JJ, Seifter E. The role of aromatic hydrocarbons in the genesis of breast cancer. Med Hypotheses 1992;38:177–84.[CrossRef][Medline]
35. Obana H, Hori S, Kashimoto T, Kunita N. Polycyclic aromatic hydrocarbons in human fat and liver. Bull Environ Contam Toxicol 1981;27:23–7.[CrossRef][Medline]
36. Band PR, Le ND, Fang R, Deschamps M. Carcinogenic and endocrine disrupting effects of cigarette smoke and risk of breast cancer. Lancet 2002;360:1044–9.[CrossRef][Medline]
37. Morabia A. Smoking (active and passive) and breast cancer: epidemiologic evidence up to June 2001. Environ Mol Mutagen 2002;39:89–95.[CrossRef][Medline]

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