|MINI SYMPOSIUM: LUNG
|Year : 2012 | Volume
| Issue : 1 | Page : 89-95
Comparison study of clinicoradiological profile of primary lung cancer cases: An Eastern India experience
A Dey1, D Biswas1, SK Saha1, S Kundu2, S Kundu2, A Sengupta3
1 Deptartment of Chest Medicine, Calcutta National Medical College, Kolkata, India
2 Institute of Postgraduate Medical Education and Research, Kolkata, India
3 Nilratan Sarkar Medical College, Kolkata, India
|Date of Web Publication||25-Jul-2012|
Deptartment of Chest Medicine, Calcutta National Medical College, Kolkata
Source of Support: None, Conflict of Interest: None
Context: According to the first population-based cancer registry from eastern part of India, Kolkata and its surrounding areas have the highest prevalence of lung cancer in India. However, there is very limited data from this part of the country. Aims: The aim of this study is to find out the demographic and clinicoradiological profile of primary bronchogenic carcinoma. Settings and Design: This is a retrospective review of lung cancer cases diagnosed in two tertiary institutes of Kolkata over a period of 4 years. Materials and Methods: We have reviewed the cases with proven histological or cytological diagnosis of primary bronchogenic carcinoma and chi-square test is done to calculate statistical significance. Results: Out of 607 patients, male 489 and female 118, 67.7% are from rural area, 67.2% are smoker and only 9.4% are ≤40 years of age. Smoking is the major risk factor for primary lung cancer (P = 0.000) but no significance could be established with the different histological subtypes (P = 0.207). Though squamous cell carcinoma (SCC) is the most predominant variety (35.1%), adenocarcinoma and undifferentiated type are overrepresented in ≤40 years. SCC occurs at a significantly higher age group (60.84 ± 12.16 years) than other subtypes (P = 0.000). At least 55.2% cases of nonsmall cell lung cancer and 54% of small cell lung cancer presented in very advanced stage. Conclusions: SCC is the most common histological subtype of primary bronchogenic carcinoma. The relatively increased frequency of adenocarcinoma in our study as compared to other studies from India is probably due to higher proportion of nonsmokers.
Keywords: Gender-association, histological subtypes, primary bronchogenic carcinoma, smoking
|How to cite this article:|
Dey A, Biswas D, Saha S K, Kundu S, Kundu S, Sengupta A. Comparison study of clinicoradiological profile of primary lung cancer cases: An Eastern India experience. Indian J Cancer 2012;49:89-95
|How to cite this URL:|
Dey A, Biswas D, Saha S K, Kundu S, Kundu S, Sengupta A. Comparison study of clinicoradiological profile of primary lung cancer cases: An Eastern India experience. Indian J Cancer [serial online] 2012 [cited 2019 Aug 19];49:89-95. Available from: http://www.indianjcancer.com/text.asp?2012/49/1/89/98930
| » Introduction|| |
The relative frequency and clinicopathological profile of different histological subtypes of primary lung cancer have been changing in recent years, probably due to changes in the smoking habit, growing popularity of low-tar/filter cigarettes and exposure to other occupational and environmental agents. ,,,,,,, According to the first population-based cancer registry (PBCR) from eastern part of India published in 2002, the highest number of lung cancer cases among male has been documented from Kolkata and suburbs compared to other regions of India. It is the most common site of cancer in male (16.3%) and the fifth leading site in female (3.9%) in Kolkata and suburbs. 
According to the best of our knowledge the only published data from the eastern part of the country was more than a decade earlier.  In this study, we have documented our experience with more than six hundred cases of primary lung cancer diagnosed in two tertiary hospitals in Kolkata and compared it with reports from other parts of India and abroad.
| » Materials and Methods|| |
This study is a retrospective analysis of 607 lung cancer cases diagnosed in the Chest medicine department of two tertiary hospitals of eastern part of India over last four years extending from January 2006 to December 2009. Both the tertiary hospitals provide service to the Kolkata metropolitan area and its suburbs as well as are the referral center for different district hospitals. Only those cases with confirmed histological or cytological diagnosis of primary bronchogenic carcinoma according to WHO classification and complete available data related to demographic profile, smoking status, clinicoradiological and diagnostic details, are included in our database. Patients with secondary lung cancer, lymphoproliferative disease, malignant pleural effusion of unknown primary, or nonpulmonary site, sarcomatoid tumors and other rare varieties were excluded from this study. The age less than or equal to 40 years is accepted as the limit to differentiate younger from older age group based on previous reports. The definition of non-smoker or never-smoker has been adapted from previous literature as a person who had never smoked or had smoked <20 cigarettes in his or her lifetime,  those who stopped smoking for more than ten years as "ex-smoker", and those who have smoked ever in their life more than just occasional smoking as "smoker."
Radiological assessment was done in all patients. The diagnosis of primary bronchogenic carcinoma was established by fiberoptic bronchoscopy (FOB) and/or USG or CT-guided tissue sampling from lung mass, supplemented by pleural fluid analysis and cytological examination of regional lymph nodes and metastatic deposits as appropriate. Postero-anterior and lateral view of chest radiograph was taken in all patients. CT scan of thorax was done in majority of cases. But CT scan of abdomen, brain or other parts of body were done in restricted cases if suggestive symptoms of involvement was there as appropriate due to economic constrains. Hence data related to the exact item smoked (bidi/cigarette/hookah/cigar), family history of cancer and history of cancer in other regions of body are lacking from our database. FOB was performed in 282 (46.5%) cases. Image guided transcutaneous needle aspiration cytology examination of mass was done in 345 (56.8%) cases. Fine needle aspiration cytology from significantly enlarged lymph node and chest wall deposit confirmed metastatic deposits in 87 (14.3%) and 36 (5.8%) cases, respectively. Pleural fluid cytological examination and biopsy contributed to diagnosis in 71 (11.7%) and 28 (4.6%) cases. Contrast enhanced CT thorax was done in 303 (49.9%) patients only and detailed investigation for pathological staging was not possible in majority of cases due to economic constrains.
Chi-square test was done to calculate the significance of different histological subtypes with reference to age, sex, residence, and smoking status.
| » Results|| |
The histopathological subtypes of primary lung carcinoma of all 607 patients are shown in [Figure 1]. There is an overall male predominance with male/female ratio of 4.14:1 (489 male and 118 female) (P = 0.048). Only 15.25% (18/118) of female and 7.9% (39/489) of male are diagnosed at age younger than or equal to 40 years of age. Female presented at a significantly younger age (54.2 ± 13.8 years) as compared to male (58.9 ± 11.5 years) (P = 0.001). Incidence of lung cancer is significantly higher in young female as compared to young male, whereas in older age group more number of male are suffering from lung cancer than female (P = 0.015). The mean age at diagnosis in young and old age group are 34.5 and 60.37 years, respectively. Of the total 607 patients, 67.2% (408/607) are current smoker, 26.8% (163/607) are nonsmoker and rest are exsmoker [Figure 2]a. Smoking status has been found to have a strong correlation with primary lung cancer. Among all the smokers with lung cancer, 93.9% (383/408) are male. In our study, female with lung cancer are more commonly nonsmokers 77.12% (91/118). Overall, male smoker and nonsmoker female are at increased risk of primary lung cancer (P = 0.000).
|Figure 1: Distribution of histopathological subtypes of primary lung cancer (N = 607). SCC, squamous cell carcinoma; AC, adenocarcinoma; Large, large cell carcinoma; Undiff., undifferentiated carcinoma; SCLC, small cell lung carcinoma|
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|Figure 2a: Distribution of histopathological subtypes with respect to smoking status (N = 607). SCC, squamous cell carcinoma, AC, adenocarcinoma; Large, large cell carcinoma; Undiff., undifferentiated carcinoma; SCLC, small cell lung carcinoma|
Figure 2b: Distribution of histopathological types with respect to age (N = 607). SCC, squamous cell carcinoma; AC, adenocarcinoma; Large, large cell carcinoma; Undiff., undifferentiated carcinoma; SCLC, small cell lung carcinoma
Figure 2c: Distribution of histopathological subtypes of primary lung cancer with respect to sex and residence (N = 607). SCC, squamous cell carcinoma; AC, adenocarcinoma; Large, large cell carcinoma; Undiff., undifferentiated carcinoma; SCLC, small cell lung carcinoma
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The most predominant histopathological subtypes of primary bronchogenic carcinoma in our study population are SCC 35.1% (213 out of 607) and adenocarcinoma 30.8% (187 out of 607), followed by SCLC 16.5% (100 out of 607), undifferentiated carcinoma 11.7% (71 out of 607), and large cell carcinoma 5.9% (36 out of 607). There is no significant gender difference in the proportional occurrences of the different histological subtypes (P = 0.112). But the pattern is significantly different in young versus old [Figure 2]b (P = 0.005), i.e., adenocarcinoma and undifferentiated carcinoma are more predominant in young whereas SCC is more common in older age group irrespective of sex. The mean age of incidence of SCC is at significantly higher age group (60.84 ± 12.16) as compared to other types of bronchogenic carcinoma (adenocarcinoma 56.85 ± 11.86, large cell 55.50 ± 12.24, undifferentiated carcinoma 54.32 ± 12.17, and SCLC 57.39 ± 11.14) (P = 0.000). Though SCC is more common among smokers and adenocarcinoma among nonsmokers, no significant association could be established between smoking status and histopathological variety (P = 0.207). SCC is the predominant type in elderly male and undifferentiated type in young male (P = 0.000). Even if adenocarcinoma is the predominant type in female 40.68% (48/118) particularly in nonsmokers, no significance could be established between the age of the patient and the histological subtype (P = 0.101).
Majority of the patients in this study population (67.7%, 411 out of 607) are from rural area. The distribution of different subtypes of primary lung cancer with respect to sex and residence is shown in [Figure 2]c. There is no significant difference in the male female ratio of primary lung cancer among urban versus rural population (P = 0.393). Smoking habit is significantly high among rural population (69.98%) as compared to urban (30.02%) (P = 0.05). Moreover, none of the urban female is observed to be smoker in the present study. Patients from rural area present at relatively later age (58.53 ± 11.024 years) as compared to urban population (56.7 ± 14.015 years) though not significant (P = 0.110). SCC (139/411, 33.8% versus 74/196, 37.7%) and adenocarcinoma (118/411, 28.7% versus 69/196, 35.2%) are the two most common variety of primary bronchogenic carcinoma in both rural and urban population but the proportion is significantly higher in urban population (P = 0.001). However, SCLC is more commonly encountered among rural population.
Cough is the most common presenting complaint (22% approx.) followed by chest pain, shortness of breath, expectoration, constitutional symptoms, hemoptysis and others. Superior venacaval obstruction (SVCO) is present in 44 out of 607 (7.2%) cases, including 2 without any parenchymal lesion, two bilateral lesion and rest 40 with right sided lesion. SCLC was the most common histopathological variety (45%) causing SVCO, followed by SCC. The two cases of SVCO with no parenchymal lesion but mediastinal and cervical lymphadenopathy, FOB showed mucosal erosion and irregularities in right main bronchus. Diagnosis was made from bronchial brushing/biopsy and fine needle aspiration cytology (FNAC) of cervical lymph node. Hoarseness of voice is present in 7.0% (43 out of 607) cases and is mostly associated with left sided lesion. SCC and SCLC being central lesion is the most common type noted causing hoarseness (SCC 34.8% SCLC 25.6% undifferentiated 23.3%, adenocarcinoma 13.9%). Metastatic deposits in liver is present in 47/607, brain in 24/607, adrenal metastasis present in 20/607, osteolytic bone lesion in 27/607, chest wall deposit in 36/607 and opposite lung nodule in 7/607 cases. Malignant pleural effusion is detected in 88/607 cases and pericardial effusion in 14/607.
Radiologically upper zone is the most involved zone (40.19%) followed by midzone (34.9%) and lower zone (22.07%). Mass is the most common lesion of bronchogenic carcinoma (77.3%) followed by pleural effusion (27.8%) and collapse (18.6%). One hundred ten (18.1%) has mediastinal widening, 42 (6.9%) has rib erosion and chest wall deposit, 32 (5.3%) has diaphragm palsy and 29 (4.8%) has cavitating carcinoma.
Only 6 out of 607 (less than one percent) have coexisting sputum positive pulmonary tuberculosis. Three of them have mass lesion and consolidation, one has pleural effusion and two has cavitating lesion. The histological distribution is like three with adenocarcinoma, two with SCC and one poorly differentiated type.
| » Discussion|| |
Though our hospitals are located in Kolkata metropolitan area, we get majority of our patients (about 67.7%) from remote village all over our state and often in very advanced stage. A significant number of patients, who are diagnosed from out-patient department at an advanced stage, opt out any sort of curative or palliative treatment, eventually escape hospital records and are lost. Also, some of the patients get admitted for terminal care in emergency department and are beyond the scope of our data collection process. Moreover, a good number of patients who are diagnosed in private chambers and hospitals in the locality are never enrolled in hospital records.
The distribution of histological subtypes, age-related differences and gender-association in our study are compared with other previous studies in [Table 1], [Table 2] and [Table 3], respectively. Male female ratio is 4.14:1 in our study which is comparable to most of the studies from India and abroad. ,,, The ratio is significantly higher in older population in comparison to younger population (4.5:1 versus 2.17:1, P = 0.015). Female in our study group are relatively younger than male which is very similar to most of the previous reports. ,, However, the comparison is difficult because the previous studies have defined the age limit for young population differently .,,,,,, There is a predominance of female among young population (15.2%, 18/118 female compared to 7.97%, 39/489 male) which is very similar to other previous studies. , The smoking habit is significantly less among young population in our study (45.6% versus 68.5%) which is contributed solely by young male. This emphasizes the presence of some confounding factors other than smoking in young population, particularly in female. Women with lung cancer are more likely to be never-smokers as described in previous literatures. Female smokers are reported to use fewer cigarettes per day and inhale less intensely than male. , Zang and Wynder  estimated that women had a 1.5-fold higher relative risk of lung cancer than men despite all odds. Fu et al. have suggested the possibility of gender-specific increased susceptibility to lung cancer in female. Santos-Martinez  concluded that male sex and smoking are associated with SCC and female sex is associated with adenocarcinoma.
The mean age of incidence of SCC is at significantly higher age group as compared to other types of bronchogenic carcinoma in our study population which is in accordance with other previous studies. , Radzikowaska E et al. showed that adenocarcinoma and SCLC develop at significantly younger age group than SCC in both male and female (SCC 62.18 ± 9.03, SCLC 59.85 ± 9.97, adenocarcinoma 59.96 ± 10.54).There is predominance of adenocarcinoma and undifferentiated type in young and SCC in elder age group in our study which is very similar to various studies outside India. ,,,, Whereas previous studies from India have shown SCC predominance in both young and older age group. ,,
In our study, SCC is the predominant type in male (35.99%) and adenocarcinoma in female (40.68%). Both adenocarcinoma (33.3% versus 20.5%) and SCLC (33.3% versus 10.3%) are found to be more common in young female than young male. Whereas the most common type in elderly female is adenocarcinoma (42%), SCC (37%) is most common in old male. Adenocarcinoma is the predominant histological type in female, especially in young and SCC in male according to most of the previous literatures. ,,,, Kuo et al. have concluded that female sex and adenocarcinoma are predominant in young nonsmall cell lung cancer (NSCLC) patients, when compared with older patients.
Extensive investigation for staging of lung cancer was not possible due to economic constrains and unavailability of certain diagnostic modalities, like PET scan, mediastinoscopy, thoracoscopy, and others in our institution. CT scan of other organs and bone scan was done in symptomatic patients only. Out of 507 cases of non-small cell lung cancer, patients with obvious distant metastasis in the form of deposits in liver, brain, adrenal or bone or chest wall or nodules in opposite lung are detected in 137 (27.02%) and are thus diagnosed as Stage IV. Total number of patients with metastatic deposits in supraclavicular/axillary lymph nodes, with malignant pleural effusion and/or great vessel involvement without obvious distant metastasis are 143 out of 507 (28.2%), i.e., Stage III B disease. However, nodal station involvement could not be assessed accurately in all patients due to several constrains. Hence, the actual number of patients with nonresectable carcinoma stage III B/IV disease may actually be under reported in this study. Among small cell lung cancer 54 out of 100 (54%) are diagnosed with extensive disease. However, the number may be little more.
Tobacco smoking causes approximately 85%-90% of bronchogenic carcinoma.  Smoking is significantly more common among male and rural population in our study. All female from urban areas are nonsmoker which may be because of increased awareness about antismoking campaign and social inhibitions especially among middle class population. Rural female are mostly daily wage earner and share the same work environment as male in agricultural or construction works in road or building and naturally share the same social habit of smoking. In our study, the incidence of adenocarcinoma and SCC among nonsmokers are 38.6% and 34.9%, respectively, whereas in smokers SCC (35.5%) is more common than adenocarcinoma (26.9%), which is not statistically significant (P = 0.207). Radzikowska et al.  concluded that the association of smoking and lung cancer is most strong among SCC and SCLC, whereas it is weaker for adenocarcinoma. The most probable explanation for increased relative frequency of SCC among nonsmokers in our study population may be lack of data related to exposure to passive smoke, nitrogen oxide from traffic fumes, biogas fuel, and exposure to occupational, environmental and other potential carcinogens  in the hospital record. There exists a dose-response relationship between smoking and lung cancer which emphasises the importance of duration and intensity of smoking as well as number of cigarettes smoked.  Compared to never-smokers, smokers have 20-fold increased risk of lung cancer at present.  The risk of lung cancer among smokers increase with duration of smoking and number of cigarettes per day.  The risk for lung cancer in former smoker remains high than never-smoker even after >40 years of abstinence.  Incidences of lung cancer as reported from different parts of India has been nicely compiled by Behera and Balamugsh  and few other studies ,,, which showed mostly SCC predominance in Indian subcontinent. The overall increased proportion of adenocarcinoma over SCC in the western world may be due to use of low-tar or filter cigarettes and decrease in number of smokers.
A noticeable change in the epidemiological pattern of occurrence of primary lung cancer has been observed as reported by Bhattacharya et al. a decade earlier from Kolkata [Table 4]. Smoking is still strongly associated with lung cancer though its percentage has decreased than before (45.6 and 69.4 versus 57.6 and 79.3 in young and old age, respectively). The incidences among female has increased, more so in elderly age group. SCC has still managed to hold its position as leading histological pattern in elderly population. But adenocarcinoma and undifferentiated carcinoma are the more common subtypes among young patients in the present study as compared to SCC in previous published data.
|Table 4: Comparison study of epidemiological trends of lung cancer from Eastern India|
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The actual number of patients diagnosed with primary lung cancer in this part of the country is much higher than reported in this study. The maintenance of a cancer registry is essential to study the temporal trends of the disease. Though SCC is the predominant variety in our study population, adenocarcinoma is being overrepresented in comparison to other reports from India. The relative predominance of adenocarcinoma in our study is not due to shift to low-tar filter cigarettes as described in many of western studies  but probably due to more number of nonsmokers as compared to other studies from India.
| » Acknowledgment|| |
The authors gratefully acknowledge Subrata Rath, Head, SQC and OR Unit, Indian Statistical Institute, Pune for his guidance related to statistical analysis and interpretation of data and continuous encouragement towards completion of the work.
| » References|| |
|1.||Behera D, Balamugsh T. Lung cancer in India. Indian J Chest Dis Allied Sci 2004;46:269-81. |
|2.||Alberg AJ, Samet JM. Epidemiology of lung cancer. Chest 2003;123:21S-49S. |
|3.||Zang EA, Wynder EL. Differences in lung cancer risk between men and women: Examination of the evidence. J Natl Cancer Inst 1996;88:183-92. |
|4.||Quinn D, Gianlupi A, Broste S. The changing radiographic presentation of bronchogenic carcinoma with reference to cell types. Chest 1996;110:1474-9. |
|5.||Lienert T, Serke M, Schonfeld N, Loddenkemper R. Lung cancer in young females. Eur Respir J 2000;16:986-90. |
|6.||Radzikowska E, Glaz P, Roszkowski K. Lung cancer in women: Age, smoking, histology, performance status, stage, initial treatment and survival. Population-based study of 20561 cases. Ann Oncol 2002;13:1087-93. |
|7.||Bhurgri Y, Bhurgri A, Usman A, Sheikh N, Faridi N, Malik J, et al. Patho-epidemiology of lung cancer in Karachi (1995-2002). Asian Pac J Cancer Prev 2006;7:60-4. |
|8.||Janseen-Heijnen ML, Coebergh JW. The changing epidemiology of lung cancer in Europe. Lung Cancer 2003;41:245-58. |
|9.||Sen U, Sankaranarayanan R, Mandal S, Ramanakumar AV, Parkin DM, Siddiqi M. Cancer Patterns In Eastern India: The First Report Of The Kolkata Cancer Registry. Int J Cancer 2002;100:86-91. |
|10.||Bhattacharya K, Deb AR, Dastidar AG, Roy A, Saha S, Sur P. Bronchogenic carcinoma in young adults. J Indian Med Assoc 1996;94:18-20. |
|11.||Bryant A, Cerfolio RJ. Differences in epidemiology, histology, and survival between cigarette smokers and never-smokers who develop non-small cell lung cancer. Chest 2007;132:185-92. |
|12.||Jindal SK, Behera D. Clinical spectrum of primary lung cancer: Review of Chandigarh experience of 10 years. Lung India 1990;8:94-8. |
|13.||Gupta RC, Purohit SD, Sharma MP, Bhardwaj S. Primary bronchogenic carcinoma: Clinical profile of 279 cases from mid-west Rajasthan. Indian J Chest Dis Allied Sci 1998;40:109-16. |
|14.||Prasad R, James P, Kesarwani V, Gupta R, Pant MC, Chaturvedi A, et al. Clinicopathological study of bronchogenic carcinoma. Respirology 2004;9:557-60. |
|15.||Bahader Y, Jazieh AR. Epidemiology of lung cancer. Supplement lung Cancer Guideline. Ann Thorac Med 2008;3(6)S65-7. |
|16.||Santos-Martinez MJ, Curull V, Blanco ML, Macia F, Mojal S, Vila J, et al. Lung cancer at a university hospital: Epidemiological and histological characteristics of a recent and historical series. Arch Bronconeumol 2005;41:307-12. |
|17.||Rawat J, Sindhwani G, Gaur D, Dua R, Saini S. Clinico-pathological profile of lung cancer in Uttarkhand. Lung India 2009;26:74-6. |
|18.||Westphal FL, Lima LC, Andrade EO, Lima Netto JC, Silva AS, Carvalho BC. Characteristics of patients with lung cancer in the city of Manaus, Brazil. J Bras Pneumol 2009;35:157-63. |
|19.||Green LS, Fortoul TI, Ponciano G, Robles C, Rivero O. Bronchogenic cancer in patients under 40 years old. The experience of a Latin American country. Chest 1993;104:1477-81. |
|20.||Kreuzer M, Kreienbrock L, Müller KM, Gerken M, Wichmann E. Histologic types of lung carcinoma and age at onset. Cancer 1999;85:1958-65. |
|21.||Gadgeel SM, Ramalingam S, Cummings G, Kraut MJ, Wozniak AJ. Lung Cancer in Patients <50 Years of Age: The Experience of an Academic Multidisciplinary Program. Chest 1999;115:1232-6. |
|22.||Kuo CW, Chen YM, Chao JY, Tsai CM, Perng RP. Non-small cell lung cancer in very young and very old patients. Chest 2000;117:354-7 |
|23.||Prasad R, Verma SK, Sanjay. Comparison between young and old patients with bronchogenic carcinoma. J Can Res Ther 2009;5:31-5. |
|24.||Ouellette D, Desbiens G, Emond C, Beauchamp G. Lung cancer in women compared with men: Stage, treatment, and survival. Ann Thorac Surg 1998;66:1140-3. |
|25.||Minami H, Yoshimura M, Miyamoto Y, Matsuoka H, Tsubota N. Lung cancer in women: Sex-associated differences in survival of patients undergoing resection for lung cancer. Chest 2000;118:1603-9. |
|26.||Ferguson MK, Wang J, Hoffman PC, Haraf DJ, Olak J, Masters GA, et al. Sex-associated differences in survival of patients undergoing resection for lung cancer.Ann Thorac Surg 2000;69:245-50. |
|27.||Fu JB, Kau TY, Severson RK, Kalemkerian GP. Lung cancer in women: Analysis of the National surveillance, epidemiology, and end results database. Chest 2005;127:768-77. |
|28.||Jindal SK, Malik SK, Dhand R, Gujral JS, Malik AK, Datta BN. Bronchogenic carcinoma in northern India. Thorax 1982;37:343-7. |
|29.||Williams MD, Sandler AB. The epidemiology of lung cancer. Cancer Treat Res 2001;105:31-52. |
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4]
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