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  Table of Contents  
MINI SYMPOSIUM: LUNG
Year : 2012  |  Volume : 49  |  Issue : 1  |  Page : 82-88
 

The relevance of "Nonsmoking-associated lung cancer" in India: A single-centre experience


1 Division of Surgical Oncology, Cancer Institute (WIA), Adyar, Chennai, Tamilnadu, India
2 Department of Molecular Oncology, Cancer Institute (WIA), Adyar, Chennai, Tamilnadu, India
3 Department of Epidemiology, Cancer Institute (WIA), Adyar, Chennai, Tamilnadu, India
4 Division of Medical Oncology, Cancer Institute (WIA), Adyar, Chennai, Tamilnadu, India

Date of Web Publication25-Jul-2012

Correspondence Address:
A Krishnamurthy
Division of Surgical Oncology, Cancer Institute (WIA), Adyar, Chennai, Tamilnadu
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0019-509X.98928

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 » Abstract 

Background: Lung cancer remains a major cause of morbidity and mortality worldwide, accounting for more deaths than any other cancer cause. Aim: The aim of this study was to analyze the clinical profile and the epidemiological trends in lung cancer patients from a single centre with an emphasis on the smoking practices. Materials and Methods: This is a retrospective analysis of prospectively collected data of 258 consecutive hospital in-patients with a proven diagnosis of lung cancer at a tertiary care oncology centre between 2003 and 2007. Results: The median age of patients in our study was 56 years; the male to female ratio was approximately 3.5:1. Non-small-cell lung cancer (NSCLC) was the predominant histology in 224 patients; the histology in the remaining 34 patients was small-cell carcinoma. Within NSCLC, the most common histology was adenocarcinoma followed by squamous cell carcinoma. One hundred and two patients were never-smokers as compared to 156 patients who were ever-smokers. Among the smokers, the majority of them were found to be cigarette smokers compared to 28.2% bidi smokers. There was a very significant correlation found with adenocarcinoma among nonsmokers, and with squamous cell carcinoma among the smokers compared to non-smokers. Conclusions: Our study suggests that the epidemiology of lung cancer in India is possibly changing, with close to 40% of our lung cancer patients being nonsmokers. More importantly, our study reflects the global trend of rise in adenocarcinoma histology. These observations need to be substantiated in similar studies of larger magnitude, preferably population-based.


Keywords: Histology, lung cancer, never-smokers, overall survival


How to cite this article:
Krishnamurthy A, Vijayalakshmi R, Gadigi V, Ranganathan R, Sagar T G. The relevance of "Nonsmoking-associated lung cancer" in India: A single-centre experience. Indian J Cancer 2012;49:82-8

How to cite this URL:
Krishnamurthy A, Vijayalakshmi R, Gadigi V, Ranganathan R, Sagar T G. The relevance of "Nonsmoking-associated lung cancer" in India: A single-centre experience. Indian J Cancer [serial online] 2012 [cited 2019 Sep 21];49:82-8. Available from: http://www.indianjcancer.com/text.asp?2012/49/1/82/98928



 » Introduction Top


Lung cancer remains a major cause of morbidity and mortality worldwide, accounting for more deaths than any other cancer cause. Lung cancer has been the most common cancer in the world for several decades, and by 2008, there were an estimated 1.61 million new cases, representing 12.7% of all new cancers. It was also the most common cause of death from cancer, with 1.38 million deaths.(18.2% of the total). [1] While there has been a substantial decline in lung cancer rates in developed countries, [2] incidence rates are reportedly rising in newly industrialized and developing countries like China and India. [3]

According to the recent GLOBOCAN 2008 report, [1] India showed 47,010 new lung cancer cases among males and 11,557 new lung cancer cases among females. The age standardized incidence /100,000 is reported to be 10.9 for males and 2.5 for females in 2008 in India. [4] Lung cancer has also been the leading cause of disability-adjusted life year (DALY) with 549,000 in males and 127,000 in females in 2004. At a rate of 85 age-adjusted DALYs/100,000 population lung cancer accounts for 7% of total DALYs in India. [5]

Lung cancer (80-90%) is most commonly attributed to smoking; a smaller proportion (10-20%) is attributed to occupational exposure to agents. The observed patterns in lung cancer rates reflect the historical prevalence and variation in the trends of smoking among men and women. Robust data on the similar epidemiological trends in lung cancers from the Indian subcontinent is, however, lacking. The aim of this study was to analyze the clinical profile and the epidemiological trends in lung cancer patients with an emphasis on the smoking practices from a single tertiary care center.


 » Materials and Methods Top


This is a retrospective analysis of prospectively collected data of consecutive hospital in-patients with a proven diagnosis of lung cancer at a tertiary care oncology centre in Chennai India, during a five-year period (2003-2007). All patients underwent the routine evaluation for lung cancer, which apart from the comprehensive history and clinical examination included a bronchoscopy, an imaging study (chest X-ray and computed tomography (CT) scan of the thorax and upper abdomen) and a pathologic confirmation of cancer. Positron emission tomography-computed tomography (PET-CT) scans have been incorporated into the staging algorithm for lung cancers ever since. The clinico-pathological details were then reviewed by the multidisciplinary group and a final decision on therapy was arrived. Data was entered and analyzed using SPSS software (SPSS for Windows, Version 18).


 » Results Top


Overall, data was extracted from a total of 258 patients with lung cancer between January 2003 and December 2007. A summary of the patient data is provided in [Table 1].
Table 1: Patient details

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Age

The median age of patients in our study was 56 years (SD=10.08) with a range from 26 to 77 years. The median age among men was 57 years while among women, it was 52.5 years. More than half of the patients (55%) were in the age group 40-60 years, 9.3% of patients were in the < 40 age group, while 35.7% patients were above 60 years of age. We found a significant association of early age of presentation (<40 years) among nonsmokers and presentation at advanced age (>60 years) among smokers (P=0.01)

Sex

The male: female ratio was approximately 3.5:1; there were 200 (77.5%) males and 58 (22.5%) females.

Clinical presentation

The symptoms at presentation included cough (54.7%), dyspnea (41.1%), chest pain (29.5%), and hemoptysis (25.2%). Loss of weight was reported in 16.3% of patients at presentation; 86% of our patients presented to us within six months of onset of symptoms. We found a significant correlation with chest pain and dyspnea as presenting symptoms of lung cancer among smokers compared to nonsmokers (P=0.0424).

Histology

Non-small-cell lung cancer (NSCLC) was the predominant histology in 224 patients (86.8%); the histology in the remaining 34 patients (13.2%) was small-cell carcinoma. Within NSCLC, the most common histology was adenocarcinoma (42.6%) followed by squamous cell carcinoma, (15.6%), large cell carcinoma (2.3%) and others (7%). Subclassification was not possible in 49 patients (19%) largely in view of the diagnosis being cytological. There was a very significant correlation found with adenocarcinoma among non-smokers compared to smokers, and with squamous cell carcinoma among the smokers compared to non-smokers (P=0.0002).

Clinical stage

All our patients were restaged based on the latest 7th edition of american joint committee on cancer (AJCC) TNM staging. Majority of the patients presented at advanced stages of the disease with 137 patients belonging to Stage IV (53%) and 87 (33.7%) patients belonged to Stage III. Though the majority of the patients presented at advanced stages, we found a very significant correlation comparing Stage III and Stage IV between the smokers and nonsmokers (P=0.0001). Presentation at very advanced Stage IV seemed to have a similar trend both among smokers and nonsmokers unlike Stage III.

Tobacco use

Of the 258 patients, 102 patients (39.5%) were never-smokers as compared to 156 patients (60.5%) who were ever-smokers. Among the smokers, the majority of them (71.8%; 112/156) were found to be cigarette smokers compared to 28.2% (44/156) who were bidi smokers [Figure 1]. The pack year distribution among smokers is shown in [Figure 2].
Figure 1: Smoker/Nonsmoker distribution

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Figure 2: Pack year distribution among the smokers of bidi and cigarette

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The median age of nonsmokers (53 years) was found to be significantly lower than that of smokers (56 years). There was a significant correlation with early age at presentation (<40 years) among nonsmokers compared to advanced age at presentation (>60 years) among smokers (P=0.01).

Among the nonsmokers, 58.3% (14/24) were <40 years of age as compared to 31.5% (29/92) who were > 60 years of age. A significant proportion of females (91%) were nonsmokers as compared to only 32.4% of males who were nonsmokers.

Smoking habits, histology and gender correlations

Although adenocarcinoma was the most common histology seen among both smokers and nonsmokers, it was found to occur more among nonsmokers (52.7%; 58/110), and squamous cell carcinoma histology was found to occur among smokers (80.4%; 33/41) (P= 0.001).

We found 36% (28/78) male nonsmokers presenting with adenocarcinoma histology compared to 15.38% (6/39) presenting with squamous histology (P=0.0299). Among the females, we found 93.75% (30/34) presenting with adenocarcinoma. Within the lung cancers with squamous histology, majority of the cases were male smokers (33/39; 84.6%) whereas females presenting with this histology were nonsmokers (P=0.0341).

We found a significant correlation of smokers presenting at advanced age (>60 years) with squamous histology compared to adenocarcinoma histology (P=0.0028).

Survival

There was no significant difference in the overall survival as shown by Kaplan Meier Curves between smokers and nonsmokers [Figure 3].
Figure 3: Kaplan Meier overall survival curves among smokers and nonsmokers

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 » Discussion Top


The incidence of lung cancer is fast increasing, particularly in developing countries like India and China.

Lung cancer in India: Population-based studies

Currently, lung cancer in India is one of the most lethal cancers, accountable as the fourth largest cause of cancer mortality. Among males, it is a leading cause of mortality accounting for 13% of all cancer deaths [5] and its incidence is rising among women.

Viswanathan et al., in their data collected from different hospitals of the country found that the incidence of lung cancer in the hospital population was 27.4 per million in 1950 and in 78.6 per million in 1959. [6]

In the data of the National Cancer Registry Program, collected from six different parts of the country, cancer of the trachea, bronchus and lungs was the most common form of malignancy in males in 1989 from Bombay (Mumbai), Delhi, and Bhopal, it was the second most common in Madras (Chennai) and third in Bangalore, and was reported the most unusual in the rural belt of Barshi. [7]

According to the recent GLOBOCAN 2008, India showed 41,865 deaths due to lung cancer among males and 10,404 deaths due to lung cancer among females. [1] The age-standardized incidence of deaths/100,000 was reported to be 9.8 for males and 2.3 for females in 2008 for the Indian population.

As per the national cancer control program (NCRP), Chennai has a crude incidence rate of 9.9/100,000 and age-adjusted incidence rate of 11.3/100,000. Evidences of trends in cancer incidence in Chennai city and predictions of the future burden of cancer in Tamil Nadu state by 2016, indicate that lung cancer would be the most common cancer surpassing cancer cervix in the state. [8]

Lung Cancer in India-Hospital-based studies

Viswanathan et al., found an increase in the incidence of bronchogenic carcinoma (16.1 in 1950 to 26.9 in 1961 per 1000 malignancies), following analysis of the records of 15 teaching institutions in India over a period of 10 years. [6]

Behera et al.. [9] analyzed the pattern of malignancy in patients admitted to PGIMER, Chandigarh from 1973 to 1982 and found that lung cancer was the fifth common cancer accounting for 0.38% of the 223,930 hospital admissions. They also noted that the total number of lung cancer admissions steadily rose from 1973. Behera et al.. [10] further showed tabulations of the published data on lung cancers from different parts of the country.

In the Hospital-based Cancer Registry (HBCR) Chennai, lung cancer was consistently ranked among the top five cancers among men, constituting about 7.5% of all cancers (HBCR 2005-2006). It, however, did not find a mention in the list of the top ten cancers among women (<2%) although its incidence is reportedly increasing over the years.

There appears to be a marginal increase in the mean age of diagnosis of lung cancers in India over the years, it was 52.16 years in 1958-1985, [10] and 54.6 years during 1985-2001. [10]

Our study showed the mean age to be 56 years. The mean and peak ages of lung cancers in India are lower when compared to the studies from the West. [11] In our study, although adenocarcinoma was found to be the common histology among all age groups, we found a significant correlation between advanced age at presentation (>60 years) with a smoking history to squamous histology.

Lung cancer has remained predominantly a disease of male smokers across the world with a male to female ratio ranging from 5.76:1 to 6.67:1 in the previously published data from Indian studies. [10] The sex ratio in our study also showed a male preponderance at 3.5:1 concordant to the earlier reports. However, the slight changes in the sex ratio over the years suggest that the incidence of lung cancers in women is increasing, a majority (91%) of whom are never-smokers. There is strong evidence of involuntary smoking and lung cancer risk in never-smokers, especially spouses of smokers.

The overwhelming cause of lung cancer across the world is cigarette smoking, with risk increasing with early age at initiation, intensity and duration. In our study 60% of lung cancer patients were found to be smokers, and more than 70% of them were cigarette smokers. Previous studies from India have shown that the risk of lung cancer varies according to the type of tobacco consumption. [10] Bidi smoking is another popular form of tobacco use across India conferring a high risk of lung cancer. Several studies have reported a higher odds ratio of bidi smoking in comparison with cigarette smoking. [12],[13],[14],[15],[16] Our study showed 28% of lung cancer patients to be bidi smokers.

Renewed cessation and prevention efforts are therefore mandatory to curb the prevalence of cigarette as well as bidi smoking. Tobacco control programs have been associated with declines in smoking rates and subsequent lung cancer incidence and mortality rates. Less than 2% of our nonsmokers were using smokeless tobacco. There is, however, no strong evidence of correlation between smokeless tobacco and lung cancer in the literature. [16],[17]

The variations and trends in histology have been a matter of interest in many studies. The strength of the association between smoking and lung cancer varies by histology, with the odds ratios historically higher for squamous and small cell carcinomas and somewhat lower for adenocarcinoma.

We, however, have found adenocarcinomas accounting for 42.6% of NSCLC, while only 15.6% were squamous cell carcinomas in our series of patients. These results possibly suggest a shift in histology from squamous cell carcinoma to adenocarcinoma in India as well. Our study showed a significant association of squamous cell carcinoma among smokers and adenocarcinoma among nonsmokers. The never-smoking cohort is also characterized by an increased incidence in females, and a higher occurrence of adenocarcinoma in comparison to the smokers' group.

Devesa et al., had first pointed to the trend of a shift from squamous cell carcinoma to adenocarcinoma which was subsequently confirmed in many other studies. Two possible hypotheses to explain the trend were cited: [18],[19],[20] the first pertains to the changing patterns in smoking-with the switch from unfiltered to filtered cigarettes, where the depth of inhalation may have been altered. Smoke from unfiltered cigarettes may be shallowly inhaled, resulting in chemical carcinogen deposition centrally in the bronchial area and giving rise to squamous cell carcinomas. Smoke from filtered milder cigarettes may be more deeply inhaled, resulting in carcinogen deposition more peripherally and giving rise to adenocarcinomas. The second plausible explanation pertains to the nature of carcinogens in tobacco-reduction in the yield of carcinogenic polycyclic aromatic hydrocarbons (PAHs) which are inducers of squamous cell carcinomas, while an increase in the yields of carcinogenic tobacco-specific N-nitrosamines (TSNAs) which are inducers of adenocarcinomas.

The majority of the Indian studies showed that squamous cell carcinoma was the most common histological subtype followed by adenocarcinoma and small cell carcinoma. [10] Large cell carcinoma is a less commonly seen variety. However, our study and other recent studies [21],[22],[23],[24],[25],[26],[27] suggest that the increase in adenocarcinoma is not solely due to a change in the pattern of cigarette smoking alone, but must be due to non-smoking related factors also, since the increase is demonstrated in nonsmokers as well.

Tokuhata and Lilienfeld [28] provided the first epidemiological evidence suggesting the interaction of genes, shared environment and common lifestyle factors in the etiology of lung cancer. Studies conducted earlier in a north Indian population have shown association of genetic polymorphism in gene CYP1A1 (homozygous variant to CYP1A1 gene) and GSTT1 null phenotype to be linked to lung cancer. [29] Lung cancer in nonsmokers probably involves complex interplay of genetic and environmental mechanisms that lead to progressive accumulation of genetic lesions. [27],[30],[31] Primary factors closely tied to lung cancer in never-smokers include exposure to known and suspected carcinogens including secondhand smoke exposure, [32],[33] and other indoor air pollutants. [34] Several other occupational exposures, pre-existing lung diseases, diet, estrogen exposure, etc. have been implicated. [35],[36] However, a large fraction of lung cancers occurring in never-smokers cannot be definitively associated with established environmental risk factors.

Recently recognized novel gene mutations in EGFR (epidermal growth factor receptor) and EML4 (echinoderm microtubule-associated protein-like 4)-ALK (anaplastic lymphoma kinase) fusion gene in lung cancer patients are largely limited to never smokers or light smokers. It has been extensively documented that abnormalities in these genes are responsible for clinical efficacy of the targeted agents. These trends therefore deserve the attention of researchers in epidemiology, experimental carcinogenesis, and molecular biology as well as among physicians and public health authorities who need to coordinate their expertise towards reducing the burden of future lung cancers.

We had the nonsmokers and smokers, both diagnosed at an advanced stage of the disease unlike the Japanese studies where more nonsmoker patients were diagnosed at an earlier stage with both smaller tumor size and less vascular permeation of the primary tumor than was found in the smokers. [37]

The symptoms such as cough, dyspnea, chest pain, hemoptysis and weight loss are common to both tuberculosis and lung cancer irrespective of their smoking status. It is not uncommon to find a lung cancer patient in India being treated for tuberculosis initially. [10],[38],[39] The delays in diagnosis in developing countries like India can be attributed to many factors-patients' ignorance in reporting to general practitioners, misinterpretation of chest radiograph findings and starting anti-tuberculosis therapy for suspicious opacities on the chest radiograph without proper evaluation. [38],[39]

The intent of treatment was palliative in close to 82% of our patients, considering the fact that a similar percentage of patients presented in advanced stages. One would assume that smokers would have a higher occurrence of co-morbidities, mainly cardiac and respiratory and that this could possibly reflect on the performance status. We however found no difference in the performance status between the smokers and nonsmokers both among males and females and this was further supported by the finding that the intention and type of treatment offered to the two groups was not different.

There have been conflicting reports on the effect of smoking on overall survivals. Several studies [37],[40],[41] have reported superior survival in NSCLC patients who had not smoked, compared to smoking-related NSCLCs in various stages, with an Hazard ratio (HR) of around 0.8. Toh et al.,[30] found that overall survival for never-smokers was significantly better than smokers in mainly advanced non-resectable NSCLC. There was however no significant survival difference between never-smokers and ever-smokers in the study by Subramanian et al., [42] which largely included advanced stage lung cancers. Our reports on survival seem to be similar to the above mentioned study which includes a wide majority of our cases presenting at advanced stages.

A major limitation of our study was the fact that it was entirely conducted at a single tertiary care facility. The inherent referral bias of such hospital-based studies is that it may not be representative of the general population. There is therefore a need to expand this study to incorporate data from multiple centers as well as from all the cancer registries.


 » Conclusion Top


Our study suggests that the epidemiology of lung cancer in India is possibly changing, with close to 40% of our lung cancer patients being non-smokers. More importantly our study reflects the global trend of rise in adenocarcinoma histology; this trend is in contrast to the earlier reported Indian studies of squamous carcinoma being the most common histology. These observations need to be substantiated in similar studies of larger magnitude, preferably population-based. Such studies will help clinicians better understand the direction of the lung cancer epidemic and also aid policymakers in better channelizing the resources for effective public health interventions.

 
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