Lung Cancer in India: A Scientometric Study of Publications during 2005–14

This paper examines 3,653 Indian publications on lung cancer research, as covered in Scopus database during 2005–14, experiencing an annual average growth rate of 18.81% and citation impact of 4.20. The world lung cancer output (169,352 publications) came from several countries, of which the top 15 most productive countries (United States, China, Germany, Japan, United Kingdom, Italy, France, Canada, and South Korea) accounted for 93.17% share of the global output during 2005–14. India’s global publication share was 2.16% and holds 12th rank in the global output during 2005–14. India’s share of international collaborative publications on lung cancer was 17.79% during 2005–14, which decreased from 19.89 to 17.06% from 2005–09 to 2010–14. Breast cancer in the field of medicine accounted for the largest share (63.62%) of output, followed by biochemistry, genetics and molecular biology (28.77%); pharmacology, toxicology, and pharmaceutics (23.87%); chemistry (9.31%); agricultural and biological sciences (3.26%); and immunology and microbiology (2.23%) during 2005–14. Diagnosis, chemotherapy, surgery, and radiotherapy among treatments methods together accounted for a share of 61.20% publications in Indian lung cancer research during 2005–14. Among the different states, Maharashtra, Delhi, Karnataka, Chandigarh, and Telangana together account for 53.41% share during 2005–14. In India’s cumulative lung cancer publications output during 2005–14, the most productive 14 Indian organizations, 15 authors, and 15 journals together contributed to 33.71, 11.27, and 20.23% share, respectively. The 31 high-cited papers in lung cancer research registered an average citation per paper of 294.74. Of the 31 high-cited papers (19 articles and 12 reviews), 7 were single institution, 3 national collaborative, and 21 international collaborative papers. The 31 high-cited papers have appeared in 23 journals. In light of this, the authors suggest the need to develop a National Cancer Prevention Policy, which should make specific recommendations for national action by governments and non-government organizations, including programs and strategies, to reduce the incidence of specific preventable cancer types.


INTRODUCTION
The lungs are a pair of sponge-like cone-shaped organs in the chest, which are a part of our respiratory system. The left lung is smaller because the heart occupies space on the left side. Furthermore, the lungs are slightly different on each side; the right lung has three lobes, whereas the left lung has two lobes. The lungs are covered by a thin membranous covering called "pleura, " which protects and helps the lungs to move back and forth as they expand and contract during breathing. A thin, dome-shaped muscle below the lungs, called "diaphragm, " separates the chest from the abdomen. The diaphragm moves up and down during breathing forcing air in and out of the lungs. Main function of the lungs is to exchange gases between the air we breathe and the blood. When we breathe in (inhale), oxygen enters into our body through the lungs and when we breathe out (exhale) carbon dioxide is sent out of our body. Air enters the lungs through the nose or mouth via windpipe

Lung Cancer in India: A Scientometric Study of Publications during 2005-14
(trachea), which divides into the right and left lungs. These airways are called "bronchi" (singular, bronchus). Inside each lung, the bronchus divides into smaller tubes, the "secondary bronchi, " which further subdivide into smaller branches called bronchioles. At the end of the bronchioles are tiny air sacs known as "alveoli, " which receives many tiny blood vessels. These tiny alveoli perform the function of exchange of gases. 1 The vast majority (85%) of cases of lung cancer are due to long-term exposure to tobacco smoke. About 10-15% of the cases occur in people who have never smoked. These cases are often caused by a combination of genetic factors and exposure to radon gas, asbestos, or other forms of air pollutants, including second-hand smoke. Lung cancer may be seen on chest radiographs and computed tomography (CT) scans. Its diagnosis can be confirmed by biopsy, which is usually performed by bronchoscopy or CTguidance. 2 Lung cancer appears to arise in the bronchi in response to repetitive carcinogenic stimuli, inflammation, and irritation. Disruption of cell development occurs in the mucosal lining and progresses to elevate or erode the basal membrane. The tumor then spreads throughout the lung and will eventually metastasize to the lymph nodes and other parts of the body. There are four main histologic classifications of lung cancer: squamous cell carcinomas, adenocarcinomas, small cell carcinomas, and large cell carcinoma. Because the behavior and management of squamous cell carcinoma, adenocarcinoma, and large cell carcinomas are very similar, they are often grouped together as non-small cell lung cancer (NSCLC) in contrast to small cell lung cancer (SCLC), which has a distinct natural history and management. Squamous cell carcinoma is most commonly found in men and shows the strongest relationship with smoking. It arises in the larger and more central bronchi and tends to spread locally, later metastasizing to other types but grows rapidly at its site of origin. Adenocarcinoma was previously known as the most common type of lung cancer in women and non-smokers; however, the incidence of adenocarcinoma has increased in the last two decades, and it is now the most common histological subtype in both males and females. The reason for the increasing incidence of adenocarcinoma is not well understood, but may be related to changing patterns of smoking. Cell carcinomas are likely to be undifferentiated squamous cell and adenocarcinoma. They usually consist of large polygonal cells with vesicular nucle. 3 Lung cancer has been the most common cancer in the world for several decades. There are estimated to be 1.8 million new cases in 2012 (12.9% of the total), of which 58% occur in developing countries. Lung cancer remains as the most common cancer in men worldwide (1.2 million, 16.7% of the total), with the highest estimated age-standardized incidence rates in Central and Eastern Europe (53.5 per 100,000) and Eastern Asia (50.4 per 100,000). The low rates are observed in Middle and Western Africa (2.0 and 1.7 per 100,000, respectively). In women, the incidence rates are generally lower, and the geographical pattern is a little different primarily reflecting different historical exposure to tobacco smoking. Thus, the highest estimated rates are in Northern America (33.8%) and Northern Europe (23.7%) with a relatively high rate in Eastern Asia (19.2%) and the lowest rates again in Western and Middle Africa (1.1 and 0.8%, respectively). Lung cancer is the most common cause of death from cancer worldwide, estimated to be responsible for nearly one in five (1.59 million deaths, 19.4% of the total). Furthermore, the overall ratio of mortality to incidence is 0.87. 4 According to GLOBOCAN 2012, there were estimated 70,000 new cases (54,000 in men and 17,000 in women) and estimated mortality of 64,000 in 2012 (49,000 in men and 15,000 in women) in India. In India, lung cancer constitutes 6.9% of all new cancer cases and 9.3% of all cancer related deaths in both sexes; it is the commonest cancer and cause of cancer-related mortality in men, with the highest reported incidences from Mizoram in both males and females (age-adjusted rate: 28.3 and 28.7 per 100,000 population in males and females, respectively). The time trends of lung cancer show a significant rise in Delhi, Chennai, and Bengaluru in both sexes. The incidence and pattern of lung cancer differ as per geographic region and ethnicity and largely reflect the prevalence and pattern of smoking. The overall 5-year survival rate of lung cancer is dismal with approximately 15% in developed countries and 5% in developing countries 3. Screening by low-dose computed tomography (CT) in high-risk population demonstrated a relative risk reduction of 20% in lung cancer mortality but with a false positive rate of 96%. In India, where tuberculosis is prevalent, the applicability of such screening tool is questionable. Development of newer non-invasive methods/biomarkers for early diagnosis and screening of high-risk population is warranted. 5

Literature Review
Ho, Satoh, and Lin 6 explored a bibliometric approach to quantitatively assess research trends in lung cancer in Japan using the Science Citation Index (SCI) database of lung cancer from 1991 to 2008. They analyzed the articles by the scientific output and research performances of individuals, institutions, and collaborative countries with Japan. They applied distribution of words in the article title, author keywords, and Keywords Plus in different periods to evaluate research trends by the frequency of keywords used. Their analysis indicated a strategy to connect molecular biology with clinical practice. Ho, Nakazawa, Sato, Tamura, Kurishma, and Satoh 7 explored a bibliometric approach to quantitatively assess research trends in cisplatincontaining chemotherapy for SCLC using related literature in the SCI expanded database from 1992 to 2011. They analyzed the articles by the scientific output and research performances of countries and institutions. Chitra, Jeyshankar, and Abu 8 examined the research output of lung cancer in the G7 and in Brazil, Russia, India, and China (BRIC countries) using scientometric data by obtaining from Scopus database on lung cancer during 2003-12. They compared the compound annual growth rate (CAGR), collaboration coefficient (CC), and publication activity using transformative activity index (TAI) of both G7 and BRIC countries. They adopted two relative indicators-absolute citation impact (ACI) and relative citation impact (RCI) to compare the quality and impact of the lung cancer research.

Objectives
In this study, our main objectives were to study the performance of Indian research in lung cancer during 2005-14, based on publications covered in Scopus database. In particular, following were the study objectives: (i) to study the growth of world and Indian research output and the citation pattern of the Indian research output; (ii) to study the global publication share of top 15 most productive countries and the place of India in global output; (iii) to study the international collaboration share of Indian publications and the contribution of leading foreign countries in India's collaborative output; (iv) to study the distribution of Indian research output by broad subject areas and study their growth and decline; (v) to study the Indian lung cancer output by treatment methods and their distribution by geographical areas; (vi) to study the publication productivity and citation impact of 15 most productive organizations and authors; (vii) to study the medium of communication; and (vii) to study the characteristics of high-cited papers.

Methodology
We retrieved and downloaded the publication data of the world and of 15 most productive countries in lung cancer from the Scopus database (http://www.scopus.com) for 10 years during 2005-14. We used a number of keywords, such as "lung" and "cancer or neoplasm or carcinoma" were used in "title, abstract, and keyword" tag and restricting it to the period 2005-14 in "date range tag" to search the global publication data, which we term as the main search string. When the main search string was used restricted to 15 most productive countries in "country tag, " as shown below, the publication data on 15 productive countries were obtained. When the main search string was further restricted to "subject area tag, " "country tag, " "source title tag, " "journal title name, " and "affiliation tag, " we obtained information on distribution of publications by subject, collaborating countries, and organization. For citation data, the 3-year, 2-year, and 1-year citation window was used for publications during 2005-12, 2013, and 2014. In addition, citations to publications were also collected from date of publication till the end of April 2015. The data for the study was collected in April 2015. (((TITLE-ABS-KEY (lung) AND TITLE-ABS-KEY(cancer or neoplasm or carcinoma)) AND PUBYEAR > 2004 AND PUBYEAR < 2015) AND by 2.20% in Japan, followed by South Korea (1.72%), United Kingdom (1.30%), and Canada (0.01%) from 2005-09 to 2010-14 (Table 3).

Subject-wise Distribution of Research Output
India's lung cancer research output during 2005-14 has been published in the context of six subfields (as reflected in Scopus database classification), with highest publication share (63.62%) coming from medicine; followed by biochemistry, genetics, and molecular biology (28.77%); pharmacology, toxicology, and pharmaceutics (23.87%); chemistry (9.31%); agricultural and biological sciences (3.26% share); and immunology and microbiology (2.23%). The research activity, as reflected in activity index, has witnessed increase in pharmacology, toxicology, and pharmaceutics (from 68.27 to 111.27); chemistry (from 57.98 to 114.66); and agricultural and biological sciences (from 87.71 to 104.29) in contrast to decrease in medicine (from 111.44 to 96.01); biochemistry, genetics, and molecular biology (from 104.0 to 95.30); and immunology and microbiology (from 104.46% to 98.44) from 2005-09 to 2010-14. Among these six subjects, the largest citation impact per publication (5.15 and 5.09) was registered by chemistry and biochemistry, genetics and molecular biology, followed by pharmacology, toxicology, and pharmaceutics (4.99); agricultural and biological; sciences (4.88); immunology and microbiology (4.87); and medicine (2.77) during 2005-14 ( Table 4).

Profile of Top 14 Most Productive Organizations
The productivity of 14 most productive Indian organizations in lung cancer varied from 35 to 267 publications, which together contributed 33.71% (1201 publications) share in the cumulative publications output of India in lung cancer research during 2005-14.     (

Profile of Top 15 Most Productive Authors
The productivity of 15 most productive Indian authors in lung cancer varied from 21 to 37 publications and together contributed 11.27% (400 publications) share in the cumulative publications output of India in lung cancer research during 2005-14.

Medium of Communication
Of the total publications in lung cancer, 97.18% (3,550) (Table 10).

High-Cited Papers
There were 31 high-cited papers (18 papers in citation range of 100-199; 7 papers in 200-299; 1 paper in 400-499; 2 papers in 500-599; 1 paper each in 600-699, 1000-1099, and 1400-1499) which together received 9,137 citations, accounting for average citation per paper of 294.74. Of the 31 high-cited papers (19 articles and 12 reviews), 7 were single institutional, 3 national collaborative, and 21 international collaborative papers. The 31 high-cited papers have appeared in 23 journals, of which the largest number (7)   citation range of 100-199, 7 papers in 200-299, 1 paper in 400-499, 2 papers in 500-599, 1 paper each in 600-699, 1000-1099 and 1400-1499), which together received 9137 citations, accounting for average citation per paper of 294.74. Of the 31 high-cited papers (19 articles and 12 reviews), 7 were single institution papers, 3 national collaborative and 21 international collaborative. The 31 high-cited papers have appeared in 23 journals, of which the largest number (7) was published in The Lancet, followed by 2 papers in Nanomedicine, The Lancet Oncology, and New England Journal of Medicine and 1 paper each in other journals.