Emerging Structure of Stem Cell Research in India : An Analysis of Publication Output , 1990-2014

The potential of stem cell to change the face of medical treatment has brought it to the forefront of medical science in recent years. The present study analyzes the stem cell research output of India during 1990-2014 collected from the Scopus database. Some of the parameters used for analysis are publication output, publication share, growth rate, h-index, impact per paper, citation analysis, international collaboration and degree of collaboration, etc. The increasing significance of stem cell research was analyzed by ranking countries, institutions, authors, journals, etc. concerning total publication, their citation, and h-index. It is exciting to note that there has been notable growth in stem cell research publication from India. A total of 3964 papers were contributed by Indian authors during the study period, out of which 71.24% have been cited at least once and has a citation average of 9.27 citations per paper. Given the interdisciplinary and complex nature of the field, most of the research output is multiple authored and out of which more than one-third have internationally collaborated. The United States, which is the top most producing country, also the largest collaborative partner of India in stem cell research. The AIIMS and PlosOne are the most productive institution and journal respectively in this field.


INTRODUCTION
Stem cell research has been ascending to the forefront of medical science and public health in recent years.Stem cells are undifferentiated, totipotent [1] and pluripotent [2] cells that have two fundamental properties:the differena Totipotent cells have total potential, i.e., capacity to form an entire organism.Totipotency is the ability of a single cell to divide and produce all the differentiated cells in an organism, including extra embryonic membranes.b Pluripotent means the potential of a cell to differentiate into any of the three germ layers: endoderm, mesoderm, orectoderm.Pluripotent stem cells can give rise to any foetal or adultcell type.However, they alone cannot develop into a foetal or adult animal because they lack the potential to contribute to extraembryonic tissue such as the placenta.
for medical treatment in the future.Any disease in which there is tissue degeneration may be the potential candidate for stem cell therapy, including the conditions and disabilities as Parkinson's and Alzheimer disease, spinal cord injury, stroke, burns, heart disease, diabetes, arthritis, liver disease, retinal regeneration, limb ischemia, hair cell regeneration, etc. [2] The present study is based on the scientometric analysis of stem cell research output for the year 1990-2014.Publication to exchange research findings is an important aspect of science and is one of the basis of methods to evaluate scientific productivity.The yield of research activities by scholars or organizations are published in journals and being utilized and evaluated by other scholars.This practice makes a collaborative network among researchers.These articles have a unique capacity to discover knowledge patterns in the world.Different approaches have been used to identify knowledge patterns in articles, one of which is scientometric where different scientific areas are mapped using publication outputs as reflected in different databases.Studies have shown that mapped articles can provide a comprehensive representation of a scientific field.The Scientometric analysis is a method for analyzing scientific production and is a tool for evaluating the quality of scientific production.Scientific publications of countries, institutions, or journals in different areas have been evaluated using scientometric methods.The Scientometric analysis includes both quantitative description of research outputs and qualitative analysis using citation analysis.Citation analysis looks at the frequency of citations made to a paper in different sources.The number of citations demonstrates the scientific impact of a paper and quality of that paper using citation indices.However, pint-size research has been done to analyze the trends and quality of global stem cell research and the majority of these studies have been carried out in more developed countries.Therefore, it is imperative to have a clear understanding of the trends of information production in the field of stem cells in India so that researchers and policy makers could plan their future course of action accordingly.
As the study intend to examine qualitative and quantitative status of stem cell research in India in order to analyze its knowledge production patterns, the scientometric indicators used in this study are-

Publication Output:
The global stem cell research output annually and number of publications per country that have at least one author affiliated with an institution in that country.A publication that is co-authored by authors from different countries thus counts toward the publication outputs of both countries.

Global publication share:
The global share of publications for a particular country expressed as a percentage of the total output within the field of stem cells research.Using a global share in addition to absolute publication numbers provides insight by normalizing for increases in world publication growth and expansion of the field in question.

Growth rate:
The compound annual growth rate is the mean annual growth rate over a specific period of time.
Here, V (t o ): start value, V (t n ): finish value, t n -t o : number of years.

H-index:
Is a small number with a big impact, first introduced by J. E. Hirsh in 2005 with the aim to measure the cumulative impact of an author or institutions productivity by analysing the total citation received by their work. [3]Hirsch claims that the h-index is desirable to other single-number criteria, such as the total number of papers, the total number of citations and citations per paper because h-index pools an assessment of both quantity (number of papers) and quality (impact, or citations to these papers). [4]

Impact Per Paper (IPP):
The IPP measures the ratio of citations in a year to scholarly papers published in the three previous years divided by the number of scholarly papers published in those same years.The IPP metric is using a citation window of three years which is considered to be the optimal time period to accurately measure citations in most subject fields.Taking into account the same peerreviewed scholarly papers only in both the numerator and denominator of the equation provides a fair impact measurement of the journal and diminishes the chance of manipulation. [5] Citation analysis: Citation analysis was considered an important indicator since the listing of references in publications is traditionally used by researchers to acknowledge the value of previous work.[6] The study used citation analysis to measure the impact of a publication or author by counting the number of times a paper is cited by other authors in their work.

International collaboration:
In this study collaboration is inferred from publication co-authorship.
A paper is considered an international collaboration if at least one of the authors is affiliated with an institution in a foreign country.

Degree of collaboration:
The study implies the Subramanian's formula to determine the degree of collaboration among authors.His mathematical formula ascertained in calculating author's degree of collaboration in a discipline.The degree of collaboration among authors is the ratio of the number of collaborative publications to the total number of publication published in a discipline during a certain period of time. [7]e degree of collaboration among authors can be measured mathematically as; Where Nm is the number of multi-authored research papers in a discipline published during a period, and Ns is the number of single-author research papers in a discipline published during the same period.

Previous Studies
Scientometrics is a widely used tool to analyze the literature around a research field.However, only a few scientometric studies have been conducted in the past on stem cell research publication.The most of these studies have been carried out in more developed countries and mostly to analyze the global trends in stem cell research.
The earliest scientometric analysis of stem cell research is reported in 2003 on stem cell research productivity globally. [8][11][12][13][14] .Various kinds of methods were used to map the stem cell research publication such as author co-citation analysis [9][10] , co-word analysis [15,16] key-word plus [12,14] etc.The previous studies observed that stem cell field is highly multidisciplinary, with research ranging from biology to therapy, across all organs to a variety of diseases, and from biomedical sciences to social sciences and law.It is extremely fast growing and a sharp increase has been observed since 1991. [17]This field is characterized by its highly collaborative nature and number of scientific disciplines interrelated by stem cell research lends it an exciting yet complicated character. [9,18,13]There are few studies on the intellectual structure of stem cell research in developing countries. [19]and the only scientometric analysis of stem cell research in India has been conducted by Karpagam et al. [20] This study explores the trends in Stem Cell research in India during 1990-2014 using Scopus database.
To analyze Indian's output of stem cell research several parameters like global publication share and rank, average citation per paper, authorship pattern, h-index, impact per paper, Degree of Collaboration, etc. were studied.

OBJECTIVE
The present study intended to explore of Stem Cells literature published during 1990-2014 as per the Scopus database and carry out the quantitative and qualitative assessment by way of analyzing various features of research output.
In particular, the study focuses on the following objective: 1. To analyze the growth of global as well as Indian literature in stem cell research during the period 1990-2014.2. To identify the countries with highest research output and India's collaborative research output with other countries.3. To determine the type of publication, major subject categories and core journals in the field of study.4. To identify the most prolific Indian authors, authorship pattern and degree of collaboration. 5. To evaluate the contribution of top Indian institutions and highly cited papers in stem cell research.6.To analyze the quality and significance of research output using citation and h-index.

METHODOLOGY
For the purpose of the study, the Scopus (Elsevier) database (http://www.scopus.com) was searched to retrieve publications comprising stem cell research and limited the analysis to publications from 1990-2014, i.e., 25 years.
The study selected Scopus for its size as it is the largest international multi disciplinary database of peer-reviewed literature.
The study used 'stem cell' as the search term, limiting this term to the occurrence in 'article titles, abstracts or keywords'.Study solely included papers published from 1990-2014, and the search was conducted within the four broad subject areas offered by Scopus: life sciences; health sciences; physical sciences and social sciences.For this study, all kind of published works was considered that are cited by and include references to other academic publication and are together referred to as 'paper' in this study.
A total of 324,175 publications were received from the Scopus database.The data was download and analyzed by using Microsoft Excel.H-index obtain from the database has been used for evaluating performance measurement.Citation counts received by the papers have been used as a qualitative measure.The performance of institutions, authors, etc. has been judged on four parameters i.e. total publications, total citations, average citation per paper and h-index.

DATA ANALYSIS
This paper examines the stem cell publication landscape from 1990-2014.The study focused on the stem cells because of their clinical relevance and study examined publication data for all kind of stem cells, i.e., embryonic, adult as well as induced pluripotent stem cells.The analysis of data has been done with a view to measuring the growth of literature over the years, global publication share of top ten countries, publication type, research collaboration, authorship pattern, productivity viz.authorwise, institution wise and distribution of articles in journals and the impact factors of such journals.

Annual Publication output of Stem Cell Research
The global pattern shows rapid growth in stem cell research output.Between the year 1990 and 2014, a total of 324175 papers were indexed in Scopus database, with an average output of 12967 papers per year.The literature on stem cell gradually rose from 2718 papers in 1990 to 28834 papers in 2014, showing a gross increase of over 960% in this 25 year with a growth rate of 38.4% annually.This advance reveals activity in a broad range of subject areas, including life sciences, health sciences, physical sciences, social sciences and humanities related to stem cell research.
Analysis of the compound annual growth rate (CAGR), defined as the year-over-year constant growth rate over a specified period of time, shows exceptionally strong growth in stem cell research.Between 1990 and 2014, stem cell research publications grew by 9.91% per year.Thus, data indicates that stem cell research is a rapidly growing field.The Table 1 shows that the doubling time for absolute publications covered by the Scopus, taking 1990 as the base year, is six years.Publications covered by the Scopus increased by 50% in 1994 from that in 1990 whereas it took only two years to increase output by further 50% and from 2000 onwards, it took about four years to increase output by 50%.However, since last five years, from 2010 to 2014, there is only around 21% increase in global publication output.
The publication trends of annual papers in stem cell research from 1990 to 2014, shown in the Figure 1.countries and India, their total publication share and percent increase in published literature is given in the Table 2.

Collaborative research in stem cell area
Stem cell research is becoming increasingly interconnected, and international collaboration has shown many positive attributes such as enhancing the impact of research, bringing together a diversity of skills and solving a complex research problem.
India collaborated with 72 countries for research on stem cell.According to Scopus database, India has total 1539 collaborative research output during the period 1990-2014, which is 38.82% share of total publication output.
Table 3 shows the top 20 collaborative countries on stem cell research.India's highest collaborative research is with United States of America (32.35%), followed by United Kingdom (6.49%), Germany (5.45%), Japan (5.26%), France (4.48%) and Australia (4.48%).India's top collab-  orative partners in the area of stem cell research has been provided in the Figure 3.

Bibliographic forms of stem cell research publication
From this study, 11 types of bibliographic form were found in a total of 3964 publications during the study period.Articles were the dominant document type, comprising 74% of the total production, followed by reviews (15%).Conference papers, letters, books etc. contributes very little to published literature on stem cells.Figure 4 showing the share of different bibliographic forms in stem cell research publication.

Stem cell research output in the context of different subjects
Based on the classification of subject categories of Scopus database, the publication output data of stem cell research is distributed in 27 subject categories during the last 25 years.The top ten productive subject categories are shown in Figure 5.Among these subjects, biochemistry, genetics and molecular biology scored the highest number of total citations as well as h-index whereas, neuroscience scored the highest citation impact (13.82 citations per paper), followed by immunology and microbiology (12.73 citations per paper), Medicine (12.67 CPP), and material science (12.57CPP).Table 4 has provided the details of major subject categories in stem cell research with their total publication, total citation, average citation and h-index.

Most Productive Journals
India's contribution to stem cell research has appeared in 158 national and international journals.The ten most productive journals publishing research papers on stem cell together contributes 402 papers, which accounts for 10.14% share of India's total output during 1990-2014.The analysis shows that there are 23 journals that have published 20 or more papers during the period of study that can be considered as most productive journals.Bradford law claimed that for a given subject area "there are a few very productive periodicals, a larger number of more moderate producers, and a still larger number of constantly diminishing productivity". [21]Bradford's Law of scattering describes a quantitative relationship between journals and the papers they publish.It explains that, only a small number of core journals will supply the nucleus of papers on a given topic which accounts for a substantial percentage (1/3) of the articles, to be followed by a second larger group of journals that accounts for another third, while a much larger group of journals picked up the last third. [22]he Bradford law explains that a few journals publish a relatively high percentage of the papers in a field, and there are many journals that publish only a few papers.The core journals in the field are most prolific, and other journals are with scattered papers.tive journals with their impact per paper and h-index has been provided in the Table 5.

Research profile of most productive Indian Institutions
One hundred and sixty Indian institutions are engaged in stem cell research and produced 3964 documents on stem cell research.Out of these, forty Indian institutions have contributed 25 or more papers.The top 20 most productive institutions in the area of stem cell research account for 34.23% of total publication output of India.
The study found that during the period 1990- A list of most productive Indian institutions, total citation received, average citation per paper and h-index value are given below in Table 6.Using publication data set, the

CONCLUSION
This scientometric investigation of stem cell research papers has revealed some interesting finding of stem cell research in India.There is a rapid growth in stem cell research literature in last 25 years.Public research institutes and hospitals are more productive than private institutions.The study also showed that there is an increasing trend towards collaborative research in this field.The growing tendency of collaboration between researchers from different organizations and decline in single-author publications suggest the inclination of authors toward using capabilities of different institutes.It also seems that progress in the field of stem cells requires collaboration between a wide range of scientists from diverse fields.
The core journals indicate that researchers are selective in publishing their research results in highly specialized and high impact factor journals.However, majority researchers find Indian journals as an easier channel for publication of their research results.India's contribution to global research output is just about 1.22%, which is very low compared to other leading countries.Excellence in stem cell research is still confined to selected few institutions in the country despite wider institutional participation in the research.Given the growing importance of stem cell in regenerative therapy, it is necessary to put more focus on stem cell research.Government and other funding agencies should formulate policies to foster research and development in this area.

Figure 1 :
Figure 1: Growth of Literature in India and the World.Source Scopus.

Figure 2 :
Figure 2: The contribution of top countries in stem cell research.Source: Scopus.

Figure 3 :
Figure 3: India's collaborative publication with major countries in stem cell research.Source: Scopus.

Figure 4 :
Figure 4: The share of different publication types in stem cell research.Source: Scopus.
The subject categories containing atleast 100 papers are Medicine (2156), Biochemistry, genetics and molecular biology (1697), Pharmacology, toxicology and pharmaceutics (611), Agriculture and biological sciences (458), Immunology and Microbiology (230), Neuroscience (228), Chemical Engineering (226), Engineering (212), Material Science (162), and Chemistry (150).The Figure5shows that stem cell research is mainly located in the field of clinical research.The three most productive subject categories, which are mainly related to the clinical research and therapy, accounting for about 68% of the total published literature.With 2156 papers related to medicine, therapeutic research was holding primacy all through the study period.

Figure 5 :
Figure 5: Major subject categories of stem cell research papers.Source: Scopus.

Table 1 : Year wise publication output of stem cell research in India and World Year Number of Publications
As Scopus has indexed 324,175 documents on stem cell research during 1990-2014 published globally, out of these, 3964 documents have been contributed by Indian authors.India's publication output increased from only eight papers in 1990 to 610 papers in 2014, showing a growth rate of above 300% and CAGR of 18.93%.Indian publication data shows a rapid growth in publication output from 2005 onward.From the analysis of above data, study found that India has much more impressive growth rate (above 300%) compare to the world average that is 38.4 percent and compound annual growth rate of India in publication of stem cell literature is also more than double of the world average which shows that in India stem cell research is a fastest growing field.
Source: Scopus.Benchmarking research performance of the countriesThe data analysis shows that the global publication share of top 10 most productive countries in stem cell research varies from 2.56% to 36.18% from 1990-2014.The United States of America is the most productive country.It has contributed the highest number of 117309 (36.18%) papers on stem cell research.The countries other than the USA, which has contributed the most of the papers on stem cell research are Japan 27007 (8.33%), Germany 26698 (8.23%),China 26031 (8.03%),United Kingdom 23612 (7.28%), and Italy 16405 (5.06%).The top productive counties in stem cell research are depicted in the Figure2.India ranks 15 th in stem cell research publication globally with a share of 1.22% of total stem cell publication.However, India shows the second highest growth rate in its publication share on stem cell research during the period studied which is 5277.08%,only behind the China with 19690.85% of increase rate during this period.Spain ranks 3 rd in this growth rate with 2288.69%increase, followed by Italy (976.44%),Germany (961.47%),United Kingdom (666.64%),Netherland (636.59%),United States (622.66%),Japan (587.18%),Canada (571.24%) and France (490.52%).The publication data of top 10

Table 2 : Publication performance of top ten countries and India
Source: Scopus.

Table 3 : India's Collaborative Research Output with Foreign Countries in Stem Cell Research
Source: Scopus.

Table 4 : Subject-wise break up of Indian publications in stem cell research
nd place in terms of the number of publication, rank 2 nd in terms of impact with IPP of 3.345 and 3 rd in h-index (129).Journals that published atleast 20 or more papers related to stem cell research during 1990-2014 with their impact per paper (IPP) and h-index are below.The top most produc-

Table 8 : Authorship pattern and degree of collaboration in Indian stem cell research publication Year Number of Authors Degree of
In total, only 30 papers had more than 100 citations, and 131 papers had 50 or more citations.The top 10 papers that were cited the most since 1990 are shown in Table9.The table shows that multiple authors produce all the most cited papers.

Table 9 : Most cited Indian stem cell research papers
. India ranked 15 th with its 1.22% of world publication share.However, India shows the second highest growth rate in its publication output stands only behind China. 5. International collaborative papers account for 38.82% of India's total output, of which the United States contributed the most, followed by the United Kingdom and Germany.6.Among different bibliographic forms, article is the dominant type (74%), followed by reviews, latter, conference papers, etc. 7. The mainstream of stem cell research is therapy, biochemistry, genetics, molecular biology, pharmaceutics, etc. 8.As a flagship journal of the field, PLoS One published most of the papers, followed by India Journal of Medical Research and Indian Journal of Experimental Biology.9.Among one hundred and sixty Indian institutions are engaged in stem cell research, study obtained All India Institute of Medical Sciences (AIIMS) the most productive institution in the country, whereas, Tata Institute of Fundamental Research has highest citation impact of 42.13 citations per paper and National Centre for Cell Science, Pune has the highest h-index of 26. 10.Most of the publications are multiple authored.Only 8% papers are single authored.11.The study reveals that 71.24% of Indian papers on stem cell research have been cited at least once and has a citation average of 9.27 citations per paper. 4