Chest ACCP Career Connection
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

Guest Access | Sign In via User Name/Password
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (17)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Khuder, S. A.
Right arrow Articles by Mutgi, A. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Khuder, S. A.
Right arrow Articles by Mutgi, A. B.
(Chest. 2001;120:1577-1583.)
© 2001 American College of Chest Physicians

Effect of Smoking Cessation on Major Histologic Types of Lung Cancer*

Sadik A. Khuder, PhD and Anand B. Mutgi, MD, MSc

* From the Department of Medicine, Medical College of Ohio, Toledo, OH.

Correspondence to: Sadik A. Khuder, PhD, Department of Medicine, Medical College of Ohio, 3120 Glendale Ave, Toledo, OH 43614-5809; e-mail: skhuder{at}mco.edu


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Study objectives: It is well-recognized that the risk of lung cancer declines after smoking cessation. However, the degree of decline in different histologic types of lung cancer is not well understood. We conducted a meta-analysis of peer-reviewed studies to assess the effect of smoking cessation on rates of major histologic types of lung cancer.

Design: Studies published in English between 1970 and 1999 were identified through searches of computerized databases (ie, MEDLINE and CANCERLIT). Combined estimates of relative risk and 95% confidence intervals were calculated for 27 studies using fixed and random effects models. Separate analyses were conducted for men and women.

Results: Smoking cessation was associated with a reduction in the risk of all the major histologic types of lung cancer. The highest reduction was in small cell lung carcinoma (SCLC) and squamous cell carcinoma (SQC), and the lowest reduction was seen in large cell cancer and adenocarcinoma. In women, the combined risks for SQC and SCLC were higher than those in men. The dose-response curve for intensity of smoking was steeper in women.

Conclusion: The findings of this study suggest that smoking cessation results in the greatest reductions for SCLC and SQC. This effect is most marked in heavy smokers, particularly among women.

Key Words: case-control • cessation • histology • lung cancer • odds ratio • smoking


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Lung cancer is the most common malignancy in the United States and is the leading cause of cancer deaths in men and women.1 The lung cancer incidence is leveling off in men but is continuing to rise at a steady rate among women.

The association between smoking and lung cancer has been studied extensively and is well-established. Eighty-seven to ninety percent of lung cancer cases are attributable to cigarette smoking, and smokers are 22 times more likely to die from lung cancer than nonsmokers.2

It is well-recognized that the risk of lung cancer declines after smoking cessation.3 4 However, it is not known whether this decline varies with the histologic type of lung cancer. Previous studies have shown that smoking is more often associated with squamous cell carcinoma (SQC) or small cell lung carcinoma (SCLC) than with adenocarcinoma (ADC).5 6 Consequently, it is expected that greater reductions would be seen in cases of SQC and SCLC after smoking cessation. The effect of quitting smoking on the risk of large cell carcinoma (LGC) is not well-understood. In this study, we examined the effects of the cessation of smoking on the risk for the major histologic types of lung cancer.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
The MEDLINE and CANCERLIT databases were searched using key words pertaining to smoking and to histologic type of lung cancer. In addition, the reference lists of identified studies as well as review articles were examined to identify additional studies. This search strategy identified over 600 articles on smoking and lung cancer. Only studies pertaining to lung histology and published in English were reviewed. We excluded case series studies from further review. The search was repeated until no additional articles were found prior to September 2000. Articles were examined, and studies were excluded from the meta-analysis for any one of the following reasons: (1) two or more histologic types were grouped together and no data were presented on the specific histologic type; (2) lack of measures for relative risk; (3) absence of risk comparison to nonsmokers; and (4) the group studied was included in another published study.

Articles were stratified into subgroups based on study design and year of publication. Studies were reviewed and data pertaining to estimator of relative risk were abstracted. A series of meta-analyses were conducted and the results were evaluated in the context of the published literature on the subject. The heterogeneity of the estimators of relative risk was tested using Cochran Q statistics.7 The fixed-effects model was used to obtain the combined estimator of relative risk (odds ratio [OR]) and its SE. The random-effects model8 was used in situations in which significant heterogeneity within the groups of studies was detected.

Stratified analyses were carried out according to the type of control used in case-control studies. Separate analyses were carried out for men and women. The dose-response relationship was evaluated for the number of years of abstinence from smoking. At each dose, the OR and 95% confidence interval (CI) were extracted. The SE was calculated from the 95% CI. For a few studies in which the 95% CI was not provided, the OR and SE were calculated using the number of exposed cases and controls.

An exponential random-effects approach9 was used to assess the effect of the number of years since smoking cessation on the risk reduction of lung cancer. For each study, a dose-response estimate was obtained by imposing a linear trend model for the natural logarithm of the OR (ln OR) at each exposure level. The midinterval score was assigned to a dose level at each exposure category. A combined slope or trend was obtained by combining individual slope estimates. The equality of the response across dose levels was tested using a t test.

Publication bias was investigated by constructing funnel plots for the ln OR vs study size for each histologic type. A rank correlation test10 was used to test for the statistical significance of publication bias.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
Forty-eight studies evaluating the association between smoking and major histologic types of lung cancer were reviewed. These studies were published between 1970 and 1999. Fifteen studies11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 were excluded because insufficient information was provided on the OR or the SE. Four studies26 27 28 29 were excluded because the histologic types were identified only as "Kreyberg I" and "Kreyberg II." One study30 presented a combined analysis of case-control studies in China and was excluded because the information on the original studies was not given.

The remaining 28 studies were included in the analysis. Information about these studies is presented in Table 1 . There were 27 case-control studies5 6 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 and one prospective cohort study.56 Population-based control subjects were used in 12 case-control studies.5 34 35 36 38 43 45 48 49 50 53 54 Eleven studies31 32 33 37 39 40 41 42 46 51 55 used hospital-based control subjects, and only 2 studies6 44 were autopsy-based. The study of Damber and Larsson47 used both population-based and autopsy-based control subjects, and data pertaining to population-based control subjects were used in the meta-analysis. The study of Ger et al52 used both hospital-based and population-based control subjects and was considered as a population-based study in the analysis. Nine studies5 6 33 44 45 47 51 53 54 were restricted to men, and four studies35 43 49 50 were restricted to women. Twelve studies32 34 36 37 38 39 40 41 42 46 48 55 reported data separately for both men and women. The most frequent histologic type of lung cancer was SQC, and the least frequent histologic type was LGC.


View this table:
[in this window]
[in a new window]

  		Table 1. Summary of Studies Used in Meta-analyses of Smoking Cessation and Lung Cancer*

 
The combined ORs for histologic types according to smoking status and study design are presented in Table 2 . Significant heterogeneity was detected among studies on current smokers and for all histologic types and study designs. For ex-smokers, the heterogeneity test was not significant for SQC and SCLC in studies utilizing population-based control subjects. For SCLC, the combined estimate for population-based control subjects was higher than that for other designs. The highest OR was 72.5 (95% CI, 13.8 to 379) for SCLC and current smokers. The lowest OR was 2.55 (95% CI, 0.82 to 7.89) for ADC and ex-smokers.


View this table:
[in this window]
[in a new window]

  		Table 2. Combined OR of Lung Cancer According to Smoking Status and Study Design

 
Table 3 presents combined ORs for different histologic types of lung cancer by smoking status and gender. In current smokers, the combined OR for SQC and SCLC in women was higher than that in men. This gender difference was less marked for ADC. We could not ascertain the gender differences in LGC due to the limited number of studies. Among ex-smokers, there was a consistent decline in combined ORs across all histologic types of lung cancer. In ex-smokers, women had greater reductions in risk for SQC and SCLC compared to men.


View this table:
[in this window]
[in a new window]

  		Table 3. Combined OR of Lung Cancer According to Smoking Status and Gender

 
Fourteen studies5 6 32 35 40 41 42 44 46 48 50 53 54 56 provided information on the number of years since smoking cessation. The pooled dose-response test was significant in all the four histologic types (Table 4 ). The reduction in risk was steeper in SCLC in comparison to other subtypes (Fig 1 ). Combined estimates for the number of years since the cessation of smoking are presented in Table 5 . Between 1 year and 4 years of cessation, there was a 19% reduction in the risk of SCLC. The lowest reduction was for ADC (12%). After >= 10 years, there was a 65% reduction in SCLC and only a 47% reduction in ADC.


View this table:
[in this window]
[in a new window]

  		Table 4. Dose-Response Analyses for Quitting Smoking

 


View larger version (12K):
[in this window]
[in a new window]
[Download PPT slide]
  		Figure 1. The ORs associated with different histologic types of lung cancer over the years since smoking cessation.

 

View this table:
[in this window]
[in a new window]

  		Table 5. Adjusted Risk Ratio for Year of Quitting for Major Histologic Types of Lung Cancer

 
A plot for the ln OR in ever-smokers vs the inverse of the SE was generated for each of the four histologic types. None of the plots showed a relationship between ln OR and study size. The test for publication bias by histologic type indicated no evidence of bias due to study size for all histologic types of lung cancer.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The findings of this study suggest that the risk of lung cancer decreases significantly after the cessation of smoking and for all histologic types of the disease. The magnitude of reduction varies among the histologic types of lung cancer. The cessation of smoking showed the greatest reduction in the risk of SQC or SCLC. The OR decreases progressively as the number of years of abstinence from smoking increases, and this is true for all histologic types. The risk reduction was most noticeable for SCLC followed by SQC. ADC displayed the least risk reduction. Our findings concerning risk reduction with abstinence are corollary to the effect of smoking on the occurrence of the major histologic types of lung cancer. The association between smoking and SCLC or SQC is stronger than that for ADC.5 6 32 40 42 44 46 48 50 54 We also noted that the effect of smoking cessation on LGC was greater than that on ADC.

The results of our meta-analysis affirm that cessation of smoking is effective in reducing the risk of lung cancer in both men and women and that this effect is significantly greater for SCLC and SQC. Interestingly, women appeared to experience greater reduction in the risk of SCLC and SQC compared to men. However, the difference between women and men is not significant for ADC. Recent epidemiologic studies suggest that, given the same level of lifelong exposure, women may be more susceptible to tobacco carcinogens than men.31 Mollerup et al57 found that women had significantly higher levels of pulmonary DNA adducts (ie, modified DNA resulting from the binding of polynuclear aromatic hydrocarbons to the p53 gene) per pack-year than did men. The gender difference may be related to circulating female steroid hormones. A recent study58 suggested that polymorphisms in CYP1A1 and GSTM1 contribute to an increased risk of lung cancer in women.

The steeper dose-response relationship with cessation of smoking was more noticeable for SCLC, particularly for women. This finding is clinically significant, as SCLC incidence appears to be increasing more rapidly in women than in men.59 60 61 Increased efforts toward smoking cessation in women would yield earlier and greater reductions in SCLC.

The dose-response for LGC was not calculated in women due to insufficient data, and therefore no conclusions can be drawn. Several morphologic features of LGC are shared with other cell types. In the Surveillance, Epidemiology, and End Results program, LGC was not categorized before 1978.62 We can only speculate that the reduction of risk in women is similar to that in men.

We noted that the progressive reduction in lung cancer incidence continued for > 10 years, suggesting a continued benefit with abstinence from smoking over time. Although the risk in ex-smokers was significantly reduced in comparison to current smokers, the risk never approached that in nonsmokers, even after > 10 years of smoking cessation. This finding reinforces the importance of the need for continued abstinence from smoking indefinitely. These findings also suggest that cigarette smoking can act as both an initiator and a promoter of lung carcinogenesis. The initiation and promotion of lung cancer is thought to result from a series of genetic mutations, including point mutations, chromosomal abnormalities, gene amplification, and altered gene expression.63 Tobacco smoke contains > 100 diverse mutagens and carcinogens, including polycyclic aromatic hydrocarbons, N-nitrosamines, and aromatic amines. The metabolites of these carcinogens are direct mutagens and may cause DNA damage.64 The promoting activity may be diminished immediately after the cessation of smoking and specifically for SCLC and SQC. However, the initiating activity remains for an extended period after the cessation of smoking and for all the histologic types of lung cancer.

There are several limitations that need to be taken into consideration before interpreting the findings of our analysis. These limitations stem from the studies included in the analysis and the inherent limitations of meta-analysis. Our meta-analysis involved studies from different parts of the world, and thus the accuracy of the classification of the histologic types of lung cancer may not be consistent. The diagnosis of lung cancer was not necessarily performed in a uniform manner across hospitals in different parts of the world. Most of the studies are retrospective and relied on recall information for exposure assessment leading to recall bias. The validity of the information on years of cessation from smoking (especially in the remote past) is difficult to determine. We limited our search to studies published in the English language, and we may have missed some published and unpublished work, particularly that stemming from smaller studies. However, this is unlikely to affect our results substantially since we have included studies from different continents.

Some studies were limited by the small number of cases for particular histologic type and gender. The accuracy of ORs may not be reliable, especially for LGC. Three types of control subjects were employed in case-control studies, and the OR probably reflected a design-specific bias. For deceased patients and control subjects, the data were collected from the next of kin. The use of proxy respondents as a source of data on smoking status may not be reliable. As smoking is also related to causes of death other than lung cancer, a comparison with deceased control subjects probably underestimated the true risk of lung cancer. Living control subjects may outlive the patients by many years and may, therefore, cause an overestimation of risk. The use of hospital control subjects may lead to an underestimation of an effect if the causes for hospitalization are also associated with smoking. Our meta-analysis also is limited by the degree of heterogeneity, as noted by the wide CIs. However, the decrease was consistent in the same direction, suggesting a stability for risk reduction with smoking cessation.

In conclusion, the findings of our meta-analysis suggest that abstinence from cigarette smoking is associated with a reduction of risk for all histologic types of lung cancer, with the reduction being greater for patients with SCLC and SQC. This reduction is more marked in women. Cohort studies are needed to corroborate our findings as the incidence of SCLC is leveling off in men but continues to increase in women. The continuous increase in the prevalence of smoking in developing countries demands the means to address this serious health problem. The findings also suggest that cigarette smoking has the strongest effect on SCLC and the weakest effect on ADC. It is possible that other exposures are involved in the etiology of ADC. Further studies are needed to delineate these other risk factors for ADC. Our study highlights the lack of data on the effect of smoking cessation on LGC risk reduction. We suggest that further studies be conducted to assess the effect of smoking cessation on the risk of LGC and that they be conducted in women particularly.


   Footnotes
 
Abbreviations: ADC = adenocarcinoma; CI = confidence interval; LGC = large cell carcinoma; ln OR = natural logarithm of the odds ratio; OR = odds ratio; SCLC = small cell lung carcinoma; SQC = squamous cell carcinoma;

Received for publication October 2, 2000. Accepted for publication May 17, 2001.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

  1. Landis, SH, Murray, T, Bolden, S, et al (1999) Cancer statistics. CA Cancer J Clin 49,8-31[Abstract/Free Full Text]
  2. . United States Surgeon General. (1989) Reducing the health consequences of smoking: 25 years of progress. US Government Printing Office Washington, DC.
  3. US Department of Health and Human Services. The health benefit of smoking cessation: a report of the Surgeon General. Rockville, MD: Department of Health and Human Services, 1990; DHHS Publication No. (CDC) 90–8416
  4. Ockene, JK, Kuller, LH, Svendsen, KH, et al (1990) The relationship of smoking cessation to coronary heart disease and lung cancer in the multiple risk factor intervention trial (MRFIT). Am J Public Health 80,954-958[Abstract/Free Full Text]
  5. Khuder, SA, Dayal, HH, Mutgi, AB, et al (1998) Effect of cigarette smoking on major histological types of lung cancer in men. Lung Cancer 22,15-21[CrossRef][ISI][Medline]
  6. Barbone, F, Bovenzi, M, Cavallieri, F, et al (1997) Cigarette smoking and histologic type of lung cancer in men. Chest 112,1474-1479[Abstract/Free Full Text]
  7. Cochran, WG (1954) The combination of estimates from different experiments. Biometrics 8,101-129[CrossRef]
  8. DerSimonian, R, Laird, N (1987) Meta-analysis in clinical trials. Control Clin Trials 7,177-188
  9. Tweedie, RL, Mengersen, KL (1995) Meta-analytic approaches to dose-response relationship, with application in studies of lung cancer and exposure to environmental tobacco smoke. Stat Med 14,545-569[ISI][Medline]
  10. Begg, CB, Mazumdar, M (1994) Operating characteristics of a rank correlation test for publication bias. Biometrics 50,1088-1101[CrossRef][ISI][Medline]
  11. Kreuzer, M, Kreienbrock, L, Muller, KM, et al (1999) Histologic types of lung carcinoma and age at onset. Cancer 85,1958-1965[ISI][Medline]
  12. Hegmann, KT, Fraser, AM, Keaney, RP, et al (1993) The effect of age at smoking initiation on lung cancer risk. Epidemiology 4,444-448[ISI][Medline]
  13. McDuffie, HH, Klaassen, DJ, Dosman, J (1990) Determinants of cell type in patients with cancer of the lung. Chest 98,1187-1193[Abstract/Free Full Text]
  14. Tsugane, S, Watanabe, S, Sugimura, H, et al (1987) Smoking, occupation and family history in lung cancer patients under fifty years of age. Jpn J Clin Oncol 17,309-317[Abstract/Free Full Text]
  15. Auerbach, O, Hammond, EC, Garfinkel, L (1979) Changes in bronchial epithelium in relation to cigarette smoking, 1955–1960 vs 1970–1977. N Engl J Med 300,381-386[Abstract]
  16. Lam, WK, So, SY, Yu, DYC (1983) Clinical features of bronchogenic carcinoma in Hong Kong: review of 480 patients. Cancer 52,369-376[CrossRef][ISI][Medline]
  17. Shimizu, H, Preston-Martin, S, Casagrande, JT, et al (1982) Epidemiological characteristics of adenocarcinoma of the lung in Los Angeles County. Natl Cancer Inst Monogr 62,161-164
  18. Kennedy, A (1973) Relationship between cigarette smoking and histological type of lung cancer in women. Thorax 28,204-208[ISI][Medline]
  19. Weiss, W, Boucot, KR, Seidman, H, et al (1972) Risk of lung cancer according to histologic type and cigarette dosage. JAMA 222,799-801[CrossRef][Medline]
  20. Joly, OJ, Lubin, JH, Caraballoso, M (1983) Dark tobacco and lung cancer in Cuba. J Natl Cancer Inst 70,1033-1039
  21. Doll, R, Peto, R (1978) Cigarette smoking and bronchial carcinoma: dose and time relationships among regular smokers and lifelong non-smokers. J Epidemiol Commun Health 32,303-313[Abstract]
  22. MacLennan, R, Da Costa, J, Day, NE, et al (1977) Risk factors for lung cancer in Singapore Chinese: a population with high female incidence rates. Int J Cancer 20,854-860[ISI][Medline]
  23. Deaner, RM, Trummer, MJ (1970) Carcinoma of the lung in women. Thorac Cardiovasc Surg 59,551-554
  24. Vincent, RG, Pickren, JW, Lane, WW, et al (1977) The changing histopathology of lung cancer: a review of 1682 cases. Cancer 39,1647-1655[CrossRef][ISI][Medline]
  25. Muscat, JE, Wynder, EL (1995) Lung cancer pathology in smokers, ex-smokers and never smokers. Cancer Lett 88,1-5[CrossRef][ISI][Medline]
  26. Chan, WC, Colbourne, MJ, Fung, SC, et al (1979) Bronchial cancer in Hong Kong 1976–1977. Br J Cancer 39,182-192[ISI][Medline]
  27. Osann, KE (1991) Lung cancer in women: the importance of smoking, family history of cancer, and medical history of respiratory disease. Cancer Res 51,4893-4897[Abstract/Free Full Text]
  28. Benhamou, S, Benhamou, E, Tirmarche, M, et al (1985) Lung cancer and use of cigarettes: a French case-control study. J Natl Cancer Inst 74,1169-1175
  29. Harris, RE, Zang, EA, Anderson, JI, et al (1993) Race and sex differences in lung cancer risk associated with cigarette smoking. Int J Epidemiol 22,592-599[Abstract/Free Full Text]
  30. Yu, SZ, Zhao, N (1996) Combined analysis of case-control studies of smoking and lung cancer in China. Lung Cancer 14(suppl),S161-S170
  31. Zang, EA, Wynder, EL (1996) Differences in lung cancer risk between men and women: examination of the evidence. J Natl Cancer Inst 88,183-192
  32. Lubin, JH, Blot, WJ (1984) Assessment of lung cancer factors by histologic category. J Natl Cancer Inst 73,383-389
  33. Vena, JE, Byers, TE, Cookfair, D, et al (1985) Occupation and lung cancer risk: an analysis by histologic subtypes. Cancer 56,910-917[CrossRef][ISI][Medline]
  34. Brownson, RC, Reif, JS, Keefe, TJ, et al (1987) Risk factors for adenocarcinoma of the lung. Am J Epidemiol 125,25-34[Abstract/Free Full Text]
  35. Wu, AH, Henderson, BE, Pike, MC, et al (1985) Smoking and other risk factors for lung cancer in women. J Natl Cancer Inst 74,747-751
  36. Gao, YT, Blot, WJ, Zheng, W, et al (1988) Lung cancer and smoking in Shanghai. Int J Epidemiol 17,277-280[Abstract/Free Full Text]
  37. Shimizu, H, Nagata, C, Tsuchiya, E, et al (1994) Risk of lung cancer among cigarette smokers in relation to tumor location. Jpn Cancer Res 85,1196-1199[ISI][Medline]
  38. Sobue, T, Suzuki, T, Horai, T, et al (1988) Relationship between cigarette smoking and histologic type of lung cancer, with special reference to sex difference. Jpn J Clin Oncol 18,3-13[Abstract/Free Full Text]
  39. Shimizu, H, Hisamichi, S, Motomiya, M, et al (1986) Risk of lung cancer by histologic type among smokers in Miyagi Prefecture. Jpn J Clin Oncol 16,117-121[Abstract/Free Full Text]
  40. Brownson, RC, Chang, JC, Davis, JR (1992) Gender and histologic type variation in smoking-related risk of lung cancer. Epidemiology 3,61-64[ISI][Medline]
  41. Muscat, JE, Stellman, SD, Zhang, Z, et al (1997) Cigarette smoking and large cell carcinoma of the lung. Cancer Epidemiol Biomarkers Prev 6,477-480[Abstract]
  42. Osann, KE, Anton-Culver, H, Kurosaki, T, et al (1993) Sex differences in lung cancer risk associated with cigarette smoking. Int J Cancer 54,44-48[ISI][Medline]
  43. Schoenberg, JB, Wilcox, HB, Mason, TJ, et al (1989) Variation in smoking-related lung cancer risk among New Jersey women. Am J Epidemiol 130,688-695[Abstract/Free Full Text]
  44. Jedrychowski, W, Becher, H, Wahrendorf, J, et al (1992) Effect of tobacco smoking on various histological types of lung cancer. J Cancer Res Clin Oncol 118,276-282[CrossRef][ISI][Medline]
  45. Siemiatycki, J, Krewski, D, Franco, E, et al (1995) Associations between cigarette smoking and each of 21 types of cancer: a multi-site case-control study. Int J Epidemiol 24,504-514[Abstract/Free Full Text]
  46. Morabia, A, Wynder, EL (1991) Cigarette smoking and lung cancer cell type. Cancer 68,2074-2078[CrossRef][ISI][Medline]
  47. Damber, LA, Larsson, LG (1986) Smoking and lung cancer with special regard to type of smoking and type of cancer: a case-control study in north Sweden. Br J Cancer 53,673-681[ISI][Medline]
  48. Risch, HA, Howe, GR, Jain, M, et al (1993) Are female smokers at higher risk for lung cancer than male smokers? A case-control analysis by histologic type. Am J Epidemiol 138,281-293[Abstract/Free Full Text]
  49. Lam, TH, Kung, ITM, Wong, CM, et al (1987) Smoking, passive smoking and histological types in lung cancer in Hong Kong Chinese women. Br J Cancer 56,673-678[ISI][Medline]
  50. Svensson, C, Pershagen, G, Klominek, J (1989) Smoking and passive smoking in relation to lung cancer in women. Acta Oncol 28,623-629[ISI][Medline]
  51. Stayner, LT, Wegman, DH (1983) Smoking, occupation, and histopathology of lung cancer: a case-control study with the use of the Third National Cancer Survey. J Natl Cancer Inst 70,421-426
  52. Ger, LP, Hsu, WL, Chen, KT, et al (1993) Risk factors of lung cancer by histological category in Taiwan. Anticancer Res 13,1491-1500[ISI][Medline]
  53. Pohlabeln, H, Jockel, KH, Muller, KM (1997) The relation between various histological types of lung cancer and the number of years since cessation of smoking. Lung Cancer 18,223-229[ISI][Medline]
  54. Pezzotto, SM, Mahuad, R, Bay, ML, et al (1993) Variation in smoking-related lung cancer risk factors by cell type among men in Argentina: a case-control study. Cancer Causes Control 4,231-237[ISI][Medline]
  55. Sobue, T, Suzuki, T, Fujimoto, I, et al (1994) Case-control study for lung cancer and cigarette smoking in Osaka, Japan: comparison with results from Western Europe. Jpn J Cancer Res 85,464-473[CrossRef][ISI][Medline]
  56. Prescott, E, Osler, M, Hein, HO, et al (1998) Gender and smoking-related risk of lung cancer. Epidemiology 9,79-83[CrossRef][ISI][Medline]
  57. Mollerup, S, Ryberg, D, Hewer, A, et al (1999) Sex differences in lung CYP1A1 expression and DNA adduct levels among lung cancer patients. Cancer Res 59,3317-3320[Abstract/Free Full Text]
  58. Dresler, CM, Fratelli, C, Babb, J, et al (2000) Gender differences in genetic susceptibility for lung cancer. Lung Cancer 30,153-160[CrossRef][ISI][Medline]
  59. Beard, CM, Annegers, JF, Woolner, LB, et al (1985) Bronchogenic carcinoma in Olmsted county, 1935–1979. Cancer 55,2026-2030[CrossRef][ISI][Medline]
  60. Dodds, L, Davis, S, Polissar, L (1986) A population-based study of lung cancer incidence trend by histologic types 1974–1981. J Natl Cancer Inst 77,53-56
  61. Wu, AH, Henderson, BE, Thomas, DC, et al (1986) Secular trends in histologic types of lung cancer. J Natl Cancer Inst 77,53-56
  62. Ries LAG, Hankey BF, Miller BA, et al. Cancer statistics review 1973–88. Bethesda, MD: National Cancer Institute; National Institutes of Health, Publication No. 91–2789
  63. Birrer, MJ, Minna, JD (1988) Molecular genetics of lung cancer. Semin Oncol 15,226-235[ISI][Medline]
  64. Shields, PG (1999) Molecular epidemiology of lung cancer. Ann Oncol 10(suppl),S7-S11



This article has been cited by other articles:


Home page
 ChestHome page
L. Thomas, L. A. Doyle, and M. J. Edelman
Lung Cancer in Women: Emerging Differences in Epidemiology, Biology, and Therapy
Chest, July 1, 2005; 128(1): 370 - 381.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
J.O. Ebbert, P. Yang, C.M. Vachon, R.A. Vierkant, J.R. Cerhan, A.R. Folsom, and T.A. Sellers
Lung Cancer Risk Reduction After Smoking Cessation: Observations From a Prospective Cohort of Women
J. Clin. Oncol., March 1, 2003; 21(5): 921 - 926.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF) Free
Right arrow Submit a response
Right arrow Alert me when this article is cited
Right arrow Alert me when eLetters are posted
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Article Archive
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via ISI Web of Science (17)
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Khuder, S. A.
Right arrow Articles by Mutgi, A. B.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Khuder, S. A.
Right arrow Articles by Mutgi, A. B.

HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS