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Original Research: CANCER |

Racial Differences in Cancer Risk Among Relatives of Patients With Early Onset Lung Cancer* FREE TO VIEW

Jessica L. Naff, BS; Michele L. Coté, PhD; Angela S. Wenzlaff, MPH; Ann G. Schwartz, PhD
Author and Funding Information

*From the Department of Epidemiology (Ms. Naff), University of Michigan School of Public Health, Ann Arbor; and Population Studies and Prevention Program (Ms. Wenzlaff), Department of Internal Medicine (Drs. Coté and Schwartz), Karmanos Cancer Institute at Wayne State University School of Medicine, Detroit, MI.

Correspondence to: Michele L. Coté, PhD, 110 E Warren Ave, Detroit, MI 48201; e-mail: cotem@med.wayne.edu



Chest. 2007;131(5):1289-1294. doi:10.1378/chest.06-2687
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Published online

Background: Relatives of patients with early onset lung cancer are at increased risk for lung cancer, and this risk varies by race. This study evaluates whether first-degree relatives of patients with early onset lung cancer are at increased risk for cancer at sites other than lung.

Methods: Family histories were ascertained from 673 lung cancer patients < 50 years of age identified from the Metropolitan Detroit Surveillance, Epidemiology and End Results program, and 773 age-, race-, and sex-matched control subjects were obtained via random-digit dialing. Data were collected for 3,556 case relatives (mothers, fathers, and siblings) and 3,943 control relatives, and unconditional logistic regression models using generalized estimating equations were used to estimate odds ratios (ORs) and 95% confidence intervals (CIs).

Results: Among case relatives, African Americans were 2.44-fold more likely to have head and neck cancers and 1.86-fold more likely to have any tobacco-related cancer compared to white case relatives (95% CI, 1.04 to 5.69% and 95% CI, 1.25 to 2.76, respectively). African-American case relatives were at increased risk for head and neck cancers (OR, 13.42; 95% CI, 1.65 to 109.01), all tobacco-related cancers (OR, 3.77; 95% CI, 2.16 to 6.55), tobacco-related cancers other than lung (OR, 4.10; 95% CI, 1.56 to 10.79), and cancer at any site (OR, 1.45, 95% CI, 1.04 to 2.02) compared to African-American control relatives.

Conclusions: These results can be used to counsel family members of patients with early onset lung cancer, and suggest target populations for preventive strategies, including smoking cessation and appropriate screening.

In 2006, it is estimated that 174,470 new lung cancer diagnoses and 162,460 deaths from lung cancer will occur.1 Lung cancer remains the leading cause of cancer-related death, regardless of gender.1Age-adjusted incidence rates reported in 2003 for lung cancer were higher among African Americans compared to whites (78.5 and 63.6 per 100,000, respectively).2

Familial aggregation of lung cancer has been reported in various populations since 1963.37 Several studies35,89 have shown that relatives of individuals with lung cancer are at an increased risk for the disease even after adjusting for individual risk factors. A metaanalysis10 of 28 case-control studies on family history and lung cancer risk reported an overall pooled estimate of 1.82 (95% confidence interval [CI], 1.58 to 2.10). These studies suggest that familial clustering of lung cancer may not only be influenced by shared environmental factors but also by shared genes.

The present study examines whether parents and siblings of patients with early onset lung cancer are at increased risk for cancers other than lung. This is the first report of risk of other cancers among relatives of patients with early onset lung cancer to include African-American families.

Study Population

Families of patients with lung cancer were identified through population-based lung cancer cases with diagnoses before 50 years of age (case probands) using the Metropolitan Detroit Cancer Surveillance System, a participant in the National Cancer Institute Surveillance, Epidemiology and End Results program. Population-based control subjects < 50 years old (control probands) were identified via random-digit dialing and were frequency matched on age, race, sex, and county of residence. More details regarding case and control ascertainment have been reported elsewhere.11 All analyses were restricted to white and African-American individuals.

Data Collection

This protocol was approved by the local institutional review board, and consent was obtained prior to interview. Risk factor information for first-degree relatives (biological parents, siblings, children) was obtained from probands or their proxies. Only parents and siblings ≥ 18 years old were included in this analysis. Variables including smoking status, number of cigarettes smoked per day, and years of smoking were collected for each family member. Medical history for each relative included asking if a physician had ever diagnosed cancer, the type of cancer, the age at diagnosis for each cancer and, if deceased, the reported cause of death.

Statistical Analysis

Case and control probands are not included in the analysis. Distributions of categorical variables are compared between case and control relatives using χ2 tests, and means for continuous variables are compared using t tests. To determine whether familial risk of cancer is present after adjustment for risk factors among relatives, unconditional logistic regression models using generalized estimating equations, which take into account family correlation structures, are used to estimate odds ratios (ORs), 95% CIs, and p values.12 The final multivariable model used in all regression analyses includes variables found to be significant (α = 0.05) in univariate models: age, race, sex, and pack-years of smoking. To compare racial differences in cancer risk in case families only, we exclude control relatives, and white case families are considered the referent group, compared to African-American case families. Statistical software (SAS version 8.02; SAS Institute; Cary, NC) was used for all analyses.

The following cancers were reported frequently by relatives of cancer patients and control subjects and were analyzed separately: lung, female breast, prostate, bone, all skin cancers (including nonmelanoma skin cancers), and lymphoreticular cancers. Head and neck cancers included primary cancers of the lip, oral cavity, larynx, and pharynx. Cancers of the esophagus, stomach, intestines, liver, pancreas, colon, and rectum were grouped as digestive cancers. Cancers of the female reproductive tract included the endometrium, cervix, and ovaries. Urinary cancers included cancers of the bladder and kidney. Tobacco-related cancers included lung, head and neck, esophagus, pancreas, bladder, kidney, and cervix malignancies. The “other tobacco-related” category excluded lung cancers from the group. Finally, two overall groupings included all cancers except lung, and cancer of any type including lung cancer.

Of the 1,155 early onset cases identified, interviews were completed for 696 patients (60.3%). Due to the rapidly fatal nature of lung cancer, case probands reported family history 54.3% of the time and proxies were responsible for 45.7% of the family history reports. More than 98% of eligible control subjects contacted through random digit dialing agreed to participate in the study (n = 797); however, eligibility was difficult to determine because of refusal to complete the screening questionnaire. After restricting our analysis to African Americans and whites, ORs and 95% CIs were based on family data provided by 673 patients with early onset lung cancer and 773 control subjects. Of the lung cancer cases, 86 cases (12.8%) were diagnosed as squamous cell carcinoma, 89 cases (13.2%) were small cell carcinoma, 308 cases (45.8%) were adenocarcinoma, 64 cases (9.5%) were large cell carcinoma, and 126 cases (18.7%) were with other or unknown lung cancers (data not shown).

This analysis focuses on the relatives of patients with lung cancer and control subjects. Characteristics of these family members are summarized in Table 1 . Family data are reported for 3,556 first-degree relatives (mean, 5.3 per case proband) and 3,943 first-degree relatives (mean, 5.1 per control proband). Approximately one third of the study population is African American. Case relatives are more likely to be eversmokers than control relatives; however, there was no significant difference in mean pack-years smoked among African-American case and control relatives (p = 0.38). Overall, white smokers reported greater pack-years of smoking compared to African-American smokers (p < 0.0001, data not shown).

Cancer of Any Type in Relatives

Risk of lung cancer was 1.94-fold higher in case relatives compared to control relatives (95% CI, 1.37 to 2.76; Table 2 ). Risk of all tobacco-related cancers (including lung) was 1.74-fold higher in case relatives compared to control relatives (95% CI, 1.32 to 2.30) and endometrial cancer was 2.43-fold higher in case relatives compared to control relatives (95% CI, 1.03 to 5.70). Stratification revealed racial differences in familial aggregation.

Cancer Type by Race of Relative

After stratifying by race, increased risk of female reproductive cancers was identified in white case relatives compared to white control relatives after adjusting for age and pack-years of smoking (OR, 1.94; 95% CI, 1.01 to 3.71; Table 2) but not in African-American female relatives. Risk of endometrial cancer was 7.79-fold higher in white female case relatives compared to white female control relatives (95% CI, 1.70 to 35.60). African-American case relatives were at increased risk for lung cancer (OR, 3.30; 95% CI, 1.77 to 6.15), head and neck cancers (OR, 13.42; 95% CI, 1.65 to 109.01), all tobacco-related cancers (OR, 3.72; 95% CI, 2.14 to 6.48), and other tobacco-related cancers (OR, 4.10; 95% CI, 1.56 to 10.79) compared to African-American control relatives, after adjusting for age, sex, and pack-years. These increased risks were not seen in white families. Overall, no increased risk of total cancers other than lung was identified for either race. However, when lung cancers were included, increased risk of all cancers was identified in African American case families compared to African-American control families after adjustment (OR, 1.44; 95% CI, 1.04 to 2.02).

In order to compare the risk of cancer in African-American relatives with white relatives, only case families were considered. African-American case relatives were 2.21-fold more likely to have lung cancer, 2.44-fold more likely to have head and neck cancers, and 1.86-fold more likely to have any tobacco-related cancer compared to white case relatives (95% CI, 1.39 to 3.51; 95% CI, 1.04 to 5.69; and 95% CI, 1.25 to 2.76, respectively; Table 2). No other statistically significant differences in risk were identified between white and African-American case relatives.

This study focuses on a unique population of relatives of early onset lung cancer cases and includes a large number of African Americans so that racial differences in cancer risk can be explored. As reported previously, we identified increased risk of lung cancer in first-degree relatives of patients with early onset lung cancer in this population.11 Not only has lung cancer been shown to aggregate in families, but relatives also appear to be at an increased risk of other cancers.1314 In addition to our prior work, Etzel et al15 reported that 124 of 230 white patients with early onset disease (≤ 50 years old) had a positive family history of cancer. Of those with a family history of cancer, 32 cases (34.7%) were lung cancers, 43 cases (25.8%) were smoking-related cancers, and 21 cases (16.9%) were breast cancers.15However, it should be noted that this study did not compare cancers in relatives of patients with early onset lung cancer with those in relatives of healthy control subjects. An earlier analysis by Etzel et al16 of smoking-related cancer risk in relatives of patients with early onset (< 55 years of age) lung cancer (probands) found no increase in risk. The authors of this hospital-based study16 attributed this to their unique referral patterns, their control population, or sample size limitations.

Although not limited to early onset cases, other studies have reported a link between lung cancer and increased risks of other cancers in first-degree relatives. Sellers et al9 found that first-degree relatives of lung cancer patients had an overall twofold greater risk of cancer at sites other than the lung, as compared to control relatives. Additionally, case families had a 4.6-fold–increased risk of cancer of the nasal cavity/sinus, mid-ear, and larynx, a 2.8-fold–higher risk of skin cancer, and a 2.1-fold–higher risk of cancer of female organs, as compared to families of control subjects.9 A Chinese study by Jin et al4 reported that relatives of patients with lung cancer were more likely to have cancer at any site than relatives of control subjects (OR, 1.82; 95% CI, 1.52 to 2.02) and were more likely to have a greater number of first-degree relatives with cancer.4

Our finding of increased female reproductive tract cancers in white women is similar to a 2.1-fold–increased risk of female cancers in first-degree relatives of lung cancer patients compared to control relatives reported in a white population in Louisiana.9 Aggregation of lung cancer in relatives of individuals with endometrial cancer has also been reported.1718 A report from the Iowa Women’s Health Study18 found that a family history of female reproductive cancer was positively associated with lung cancer risk in postmenopausal women. Fornasarig et al17 also reported familial clustering of endometrial and lung cancers, attributing this to shared environmental exposures. A report from The Cancer and Steroid Hormone Study by Gruber and Thompson,19 however, reported no significant association between endometrial and lung cancers.

The link between lung and endometrial cancer is not well understood. Certain types of cancer of the endometrium have been associated with prolonged estrogen exposure,17 recent research suggests that estrogens may be associated with lung carcinogenesis.2022 In addition, there are enzymes common to both the tobacco and estrogen metabolism pathways. The dual activities of these enzymes and their associated genetic polymorphisms support a common underlying genetic component to lung and endometrial cancers.

We are the first to report a significantly increased risk of tobacco-related cancers among African Americans, but not whites, with a family history of early onset lung cancer even though African Americans report less personal tobacco use than their white counterparts. Other unknown or unmeasured risk factors may account for this increase, but it is also possible that the increased risk is due to inherited susceptibility. Additional evidence of familial aggregation of tobacco-related cancers comes from segregation and linkage analyses. Sellers et al23reported evidence of a Mendelian-dominant pattern of inheritance of smoking-related cancers in white families with early onset lung cancer. A family linkage study24 included relatives with lung, throat, or laryngeal cancers and detected evidence for linkage on chromosome 6q. Although this linkage area contains dozens of potential candidate genes that will require further study, this linkage analysis provides further evidence of a genetic component to these cancers.

There are several strengths to the reported study. First, we examined a large population of relatives of patients with early onset lung cancer and comparable control subjects. Demographic, behavioral, and health information were collected for each relative, allowing for adjustment by sex, age, race, and pack-years of smoking in the analysis. Secondly, unconditional logistic regression models using generalized estimating equations were used in order take into account correlations between relatives. Finally, African Americans comprised approximately one third of the study population. Studying familial clustering of other cancers by race is important because familial aggregation of lung cancer appears to be stronger in African Americans.11 This is the first study to report cancer risk in African-American relatives of patients with early onset lung cancer.

Our study has several limitations. Control response rates were difficult to determine because not everyone completed the screening questionnaire, so eligibility could not be determined. Information about relatives for both case patients and control subjects was reported through the proband or a family member. Although proxy reporting has been found to be reliable for cancers2526 and cigarette consumption,27there is potential for recall bias, since individuals with cancer may be more likely to remember family cancer history than control subjects. Furthermore, proxies were often able to report smoking status; however, the amount of smoking (pack-years) was missing for 540 case relatives (15.2%) and 417 control relatives (10.6%). These individuals were excluded from analyses that required pack-year information, thereby excluding 77 cancers of any type among family members of cases and 44 cancers of any type in control families, making risk estimates conservative. Analyses including these individuals and using ever/never smoked showed similar results. Another limitation is the low number of affected individuals in some categories after stratification by race, so findings should be interpreted with caution. While type of cancer for relatives was not verified by medical records or death certificates, one validation study28 on proxy reporting of family history found that younger probands and proxies were able to provide more accurate family history data than older probands, especially for female breast, colorectal, and prostate cancers. Since the majority of our probands were < 50 years old, the accuracy of cancer reporting is likely high; however, there is always the possibility of misclassification of cancer type in this study population. Also, we did not collect information on other risk factors in relatives, such as alcohol use, nutritional or exercise habits, or use of other tobacco products. Lastly, the findings presented are applicable to first-degree relatives of patients with early onset lung cancer (< 50 years old at diagnosis). Risk estimates may not be applicable for families with disease of later onset.

Findings of familial aggregation of lung cancer identified in case-control studies, along with a chromosomal region of interest identified via linkage analysis support a genetic component to lung cancer development.24 Examining other cancers in families with a history of early onset lung cancer may provide insight into the genetic mechanisms involved in carcinogenesis. It is noteworthy that other than endometrial and tobacco-related cancers, we did not identify an increased risk of other cancers in relatives of patients with early onset lung cancer, but the risks identified did vary by race. Ideally, knowledge that a family history of early onset lung cancer may be a risk factor for both tobacco-related and other types of cancers may encourage individuals to adapt healthier behaviors including smoking cessation and appropriate screening.

Abbreviations: CI = confidence interval; OR = odds ratio

This work was conducted within the Population Studies and Prevention Program, Karmanos Cancer Institute at Wayne State University School of Medicine, Detroit, MI.

This work was supported by National Cancer Institute grant RO1-CA60691 and contract NO1 PC35145 (Dr. Schwartz).

The authors have no conflicts of interest to declare.

Table Graphic Jump Location
Table 1. Characteristics of First-Degree Relatives of Patients With Early Onset Lung Cancer and Control Subjects, by Race*
* 

Data are presented as No. (%) or mean ± SD.

Table Graphic Jump Location
Table 2. Cancer Risk in Relatives of Patients With Early Onset Lung Cancer and Control Subjects, by Race
* 

Data are significant (α = 0.05).

 

Adjusting for age, sex, race, and pack-years.

 

Adjusting for age, sex, and pack-years.

§ 

ORs and CIs could not be calculated.

. American Cancer Society. (2006)Cancer facts and figures 2006. American Cancer Society. Atlanta, GA:
 
Ries, LAG, Harkins, D, Krapcho, M, et al. SEER cancer statistics review, 1975–2003. 2006; National Cancer Institute. Bethesda, MD:.
 
Schwartz, AG, Yang, P, Swanson, GM Familial risk of lung cancer among nonsmokers and their relatives.Am J Epidemiol1996;144,554-562. [PubMed] [CrossRef]
 
Jin, Y, Xu, Y, Xu, M, et al Increased risk of cancer among relatives of patients with lung cancer in China.BMC Cancer2005;5,146. [PubMed]
 
Bromen, K, Pohlabeln, H, Jahn, I, et al Aggregation of lung cancer in families: results from a population-based case-control study in Germany.Am J Epidemiol2000;152,497-505. [PubMed]
 
Hemminki, K, Rawal, R, Chen, B, et al Genetic epidemiology of cancer: from families to heritable genes.Int J Cancer2004;111,944-950. [PubMed]
 
Tokuhata, GK, Lilienfeld, AM Familial aggregation of lung cancer in humans.J Natl Cancer Inst1963;30,289-312. [PubMed]
 
Ooi, WL, Elston, RC, Chen, VW, et al Increased familial risk for lung cancer.J Natl Cancer Inst1986;76,217-222. [PubMed]
 
Sellers, TA, Ooi, WL, Elston, RC, et al Increased familial risk for non-lung cancer among relatives of lung cancer patients.Am J Epidemiol1987;126,237-246. [PubMed]
 
Matakidou, A, Eisen, T, Houlston, RS Systematic review of the relationship between family history and lung cancer risk.Br J Cancer2005;93,825-833. [PubMed]
 
Cote, ML, Kardia, SL, Wenzlaff, AS, et al Risk of lung cancer among white and black relatives of individuals with early-onset lung cancer.JAMA2005;293,3036-3042. [PubMed]
 
Zeger, SL, Liang, KY Longitudinal data analysis for discrete and continuous outcomes.Biometrics1986;42,121-130. [PubMed]
 
Schwartz, AG, Rothrock, M, Yang, P, et al Increased cancer risk among relatives of nonsmoking lung cancer cases.Genet Epidemiol1999;17,1-15. [PubMed]
 
Schwartz, AG, Siegfried, JM, Weiss, L Familial aggregation of breast cancer with early onset lung cancer.Genet Epidemiol1999;17,274-284. [PubMed]
 
Etzel, CJ, Lu, M, Merriman, K, et al An epidemiologic study of early onset lung cancer.Lung Cancer2006;52,129-134. [PubMed]
 
Etzel, CJ, Amos, CI, Spitz, MR Risk for smoking-related cancer among relatives of lung cancer patients.Cancer Res2003;63,8531-8535. [PubMed]
 
Fornasarig, M, Campagnutta, E, Talamini, R, et al Risk factors for endometrial cancer according to familial susceptibility.Int J Cancer1998;77,29-32. [PubMed]
 
Anderson, KE, Woo, C, Olson, JE, et al Association of family history of cervical, ovarian, and uterine cancer with histological categories of lung cancer: the Iowa Women’s Health Study.Cancer Epidemiol Biomarkers Prev1997;6,401-405. [PubMed]
 
Gruber, SB, Thompson, WD A population-based study of endometrial cancer and familial risk in younger women: cancer and Steroid Hormone Study Group.Cancer Epidemiol Biomarkers Prev1996;5,411-417. [PubMed]
 
Schabath, MB, Wu, X, Vassilopoulou-Sellin, R, et al Hormone replacement therapy and lung cancer risk: a case-control analysis.Clin Cancer Res2004;10,113-123. [PubMed]
 
Stabile, LP, Davis, AL, Gubish, CT, et al Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor alpha and beta and show biological responses to estrogen.Cancer Res2002;62,2141-2150. [PubMed]
 
Stabile, LP, Siegfried, JM Estrogen receptor pathways in lung cancer.Curr Oncol Rep2004;6,259-267. [PubMed]
 
Sellers, TA, Chen, PL, Potter, JD, et al Segregation analysis of smoking-associated malignancies: evidence for Mendelian inheritance.Am J Med Genet1994;52,308-314. [PubMed]
 
Bailey-Wilson, JE, Amos, CI, Pinney, SM, et al A major lung cancer susceptibility locus maps to chromosome 6q23–25.Am J Hum Genet2004;75,460-474. [PubMed]
 
Theis, B, Boyd, N, Lockwood, G, et al Accuracy of family cancer history in breast cancer patients.Eur J Cancer Prev1994;3,321-327. [PubMed]
 
Murff, HJ, Spigel, DR, Syngal, S Does this patient have a family history of cancer? an evidence-based analysis of the accuracy of family cancer history.JAMA2004;292,1480-1489. [PubMed]
 
McLaughlin, JK, Mandel, JS, Mehl, ES, et al Comparison of next-of-kin with self-respondents regarding questions on cigarette, coffee, and alcohol consumption.Epidemiology1990;1,408-412. [PubMed]
 
Ziogas, A, Anton-Culver, H Validation of family history data in cancer family registries.Am J Prev Med2003;24,190-198. [PubMed]
 

Figures

Tables

Table Graphic Jump Location
Table 1. Characteristics of First-Degree Relatives of Patients With Early Onset Lung Cancer and Control Subjects, by Race*
* 

Data are presented as No. (%) or mean ± SD.

Table Graphic Jump Location
Table 2. Cancer Risk in Relatives of Patients With Early Onset Lung Cancer and Control Subjects, by Race
* 

Data are significant (α = 0.05).

 

Adjusting for age, sex, race, and pack-years.

 

Adjusting for age, sex, and pack-years.

§ 

ORs and CIs could not be calculated.

References

. American Cancer Society. (2006)Cancer facts and figures 2006. American Cancer Society. Atlanta, GA:
 
Ries, LAG, Harkins, D, Krapcho, M, et al. SEER cancer statistics review, 1975–2003. 2006; National Cancer Institute. Bethesda, MD:.
 
Schwartz, AG, Yang, P, Swanson, GM Familial risk of lung cancer among nonsmokers and their relatives.Am J Epidemiol1996;144,554-562. [PubMed] [CrossRef]
 
Jin, Y, Xu, Y, Xu, M, et al Increased risk of cancer among relatives of patients with lung cancer in China.BMC Cancer2005;5,146. [PubMed]
 
Bromen, K, Pohlabeln, H, Jahn, I, et al Aggregation of lung cancer in families: results from a population-based case-control study in Germany.Am J Epidemiol2000;152,497-505. [PubMed]
 
Hemminki, K, Rawal, R, Chen, B, et al Genetic epidemiology of cancer: from families to heritable genes.Int J Cancer2004;111,944-950. [PubMed]
 
Tokuhata, GK, Lilienfeld, AM Familial aggregation of lung cancer in humans.J Natl Cancer Inst1963;30,289-312. [PubMed]
 
Ooi, WL, Elston, RC, Chen, VW, et al Increased familial risk for lung cancer.J Natl Cancer Inst1986;76,217-222. [PubMed]
 
Sellers, TA, Ooi, WL, Elston, RC, et al Increased familial risk for non-lung cancer among relatives of lung cancer patients.Am J Epidemiol1987;126,237-246. [PubMed]
 
Matakidou, A, Eisen, T, Houlston, RS Systematic review of the relationship between family history and lung cancer risk.Br J Cancer2005;93,825-833. [PubMed]
 
Cote, ML, Kardia, SL, Wenzlaff, AS, et al Risk of lung cancer among white and black relatives of individuals with early-onset lung cancer.JAMA2005;293,3036-3042. [PubMed]
 
Zeger, SL, Liang, KY Longitudinal data analysis for discrete and continuous outcomes.Biometrics1986;42,121-130. [PubMed]
 
Schwartz, AG, Rothrock, M, Yang, P, et al Increased cancer risk among relatives of nonsmoking lung cancer cases.Genet Epidemiol1999;17,1-15. [PubMed]
 
Schwartz, AG, Siegfried, JM, Weiss, L Familial aggregation of breast cancer with early onset lung cancer.Genet Epidemiol1999;17,274-284. [PubMed]
 
Etzel, CJ, Lu, M, Merriman, K, et al An epidemiologic study of early onset lung cancer.Lung Cancer2006;52,129-134. [PubMed]
 
Etzel, CJ, Amos, CI, Spitz, MR Risk for smoking-related cancer among relatives of lung cancer patients.Cancer Res2003;63,8531-8535. [PubMed]
 
Fornasarig, M, Campagnutta, E, Talamini, R, et al Risk factors for endometrial cancer according to familial susceptibility.Int J Cancer1998;77,29-32. [PubMed]
 
Anderson, KE, Woo, C, Olson, JE, et al Association of family history of cervical, ovarian, and uterine cancer with histological categories of lung cancer: the Iowa Women’s Health Study.Cancer Epidemiol Biomarkers Prev1997;6,401-405. [PubMed]
 
Gruber, SB, Thompson, WD A population-based study of endometrial cancer and familial risk in younger women: cancer and Steroid Hormone Study Group.Cancer Epidemiol Biomarkers Prev1996;5,411-417. [PubMed]
 
Schabath, MB, Wu, X, Vassilopoulou-Sellin, R, et al Hormone replacement therapy and lung cancer risk: a case-control analysis.Clin Cancer Res2004;10,113-123. [PubMed]
 
Stabile, LP, Davis, AL, Gubish, CT, et al Human non-small cell lung tumors and cells derived from normal lung express both estrogen receptor alpha and beta and show biological responses to estrogen.Cancer Res2002;62,2141-2150. [PubMed]
 
Stabile, LP, Siegfried, JM Estrogen receptor pathways in lung cancer.Curr Oncol Rep2004;6,259-267. [PubMed]
 
Sellers, TA, Chen, PL, Potter, JD, et al Segregation analysis of smoking-associated malignancies: evidence for Mendelian inheritance.Am J Med Genet1994;52,308-314. [PubMed]
 
Bailey-Wilson, JE, Amos, CI, Pinney, SM, et al A major lung cancer susceptibility locus maps to chromosome 6q23–25.Am J Hum Genet2004;75,460-474. [PubMed]
 
Theis, B, Boyd, N, Lockwood, G, et al Accuracy of family cancer history in breast cancer patients.Eur J Cancer Prev1994;3,321-327. [PubMed]
 
Murff, HJ, Spigel, DR, Syngal, S Does this patient have a family history of cancer? an evidence-based analysis of the accuracy of family cancer history.JAMA2004;292,1480-1489. [PubMed]
 
McLaughlin, JK, Mandel, JS, Mehl, ES, et al Comparison of next-of-kin with self-respondents regarding questions on cigarette, coffee, and alcohol consumption.Epidemiology1990;1,408-412. [PubMed]
 
Ziogas, A, Anton-Culver, H Validation of family history data in cancer family registries.Am J Prev Med2003;24,190-198. [PubMed]
 
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