Hematology research output from Chinese authors and other countries: a 10-year survey of the literature

Background Hematologic disease affects people of all ages worldwide. In the past decade, researchers have made great progress in the field of hematology. In the present study we compared the hematology research output from China and other countries (USA, Germany, UK, Japan and South Korea) over the past 10 years and 5 years. Methods The related articles were extracted based on the PubMed database. We recorded the number of publications, clinical trials, randomized controlled trials, meta-analyses, case reports, reviews, citations, impact factors, articles in the top 10 journals and most published journals to assess the quantity and quality of research output in each region. Results A total of 120,641 hematology-related articles were published from 2004 to 2013. The USA accounted for 27.13% (32,732/120,641) of the publications, followed by Germany (7,479/120,641; 6.20%), Japan (6,347/120,641; 5.26%), the UK (5,453/120,641; 4.52%), China (2,924/120,641; 2.42%) and South Korea (1,413/120,641; 1.17%). The ranking for cumulative impact factors was as follows: USA; Germany; UK; Japan; China and South Korea. The median impact factors in the UK, USA, and Germany were higher than Japan, South Korea, and China. Interestingly, the median impact factors in the three Asia countries were similar both in 2004–2013 and 2009–2013. The UK had the highest percentage of publications in the top 25% of journals, while China lagged behind and ranked last. When comparing the number of articles in the top 10 journals, the results were similar to the IF findings. Germany had the highest number of average citations, while China had the lowest number of average citation. The status of hematology research output from the 6 countries in 2009–2013 had little difference from 2004–2013. Conclusions Thus, the USA has had a dominant role in hematologic research in the past 10 years. Overall, the quality of publications in European countries was better than Asia countries. Although China has made considerable progress in hematology research, the quality of research needs improvement. Electronic supplementary material The online version of this article (doi:10.1186/s13045-014-0103-3) contains supplementary material, which is available to authorized users.

involving scientific publications by Chinese scholars in the field of hematology. In the present study we determined the contributions made by Chinese authors in the field of hematology between 2004 and 2013. Due to the different systems and funding mechanisms which exist in mainland China, Hong Kong, and Taiwan, articles from Hong Kong and Taiwan were not analyzed. Use of "China" herein referred to mainland China. The comparison of hematology research output among China, the USA, UK, Germany, Japan, and South Korea was not limited to 2004-2013, but also included 2009-2013.

Results
Total number and share of articles A total of 120,641 articles were published between 2004 and 2013 in the 68 hematology-related journals. The USA accounted for the largest proportion (32,732/ 120,641 [27.13%]), followed by Germany (7, [1.17%]). The changes in the annual number and share of articles from each country are shown in Figure 1. As shown in Figure 1, the number of papers published from China surpassed the number of papers published from UK in 2013 for the first time, and approached the number of papers published from Japan.
Clinical trials, randomized controlled trials, case reports, meta-analyses, and reviews The number of different types of articles from the six countries is shown in Figure 2. USA ranked first in the number of each type of article. Interestingly, the number of meta-analyses published by China ranked second, followed closely by the USA; other types of publications from China just exceeded the number published from South Korea.

Impact factor
Based on JCR 2014, we calculated the cumulative and median IFs for each geographic region, which are shown in Table 1. The ranking of the cumulative IFs in six countries was the USA, Germany, the UK, Japan, China and South Korea. The UK, USA, and Germany ranked in the top three of median IFs, and the median IFs were equal in the three Asia countries; these rankings did not change in the past 5 or 10 years.
Furthermore, according to the IF, we divided the 68 journals into 4 levels. The number and percentage of publications from each region in the four levels is shown in Tables 2 and 3. From 2004 to 2013 [Table 2], The UK ranked first, while China ranked last with respect to the number of publications in the top 25% of journals (highest level). The same result was demonstrated in the period between 2009 and 2013 [ Table 3]. The distribution of publications from each country in the four grades differed little between 2004-2013 and 2009-2013.

Citation reports
The rank of total citations-to-published articles between 2004 and 2013 was as follows: USA (921,553 citations and 93,548 articles); Germany (260,570 citations and 23,970 articles); UK (158,171 citations and 19,393 articles); Japan (120,431 citations and 13,984 articles); China (37,712 citations and 6,666 articles) and South Korea (24,134 citations and 3,694 articles) [ Figure 3]. Germany had the highest average citations, meanwhile China had the lowest average citations. It is noteworthy that the average number of citations in Japan surpassed UK and was much higher than South Korea and China [ Table 4].     Table 6], the percentage of articles in the top 10 journals from UK, Germany, and Japan decreased slightly, while the percentage of articles in the top 10 journals from China, USA, and South Korea had a small rise; all of these changes were no more than 2 percentage points.

Most published journals
The journals in which articles from the six countries were published most frequently are listed in Tables 7 and 8. It is worth noting that the same journal (Blood) was the most frequent target journal in the USA and Germany; Blood is one of the most influential journals in the field of hematology.
Articles from China were most often published in Leukemia Research, while the International Journal of hematology and annals of hematology were the most published journals in Japan and South Korea, respectively. These three journals were not amongst the top 10 journals [Tables 7 and 8

Discussion
This is the first study that compared the quantity and quality of publications in hematology-related journals from China and the USA, UK, Germany, Japan, and South Korea. Publications from the six countries were extracted based on the PubMed database, a free search engine primarily accessing the MEDLINE database of references and abstracts pertaining to the life sciences and biomedical topics. The PubMed database was created by the United States National Library of Medicine (NLM) at the National Institutes of Health. The IF of each journal was calculated using the JCR 2014, which helps to quantify the influence of research and impact on the journal or category levels; the IF also indicates the relationship between citing and cited journals.
As shown in Figure 1, only China and South Korea exhibited a sustained trend in growth between 2004 and 2013 with respect to the number of publications in hematology-related journals. The USA had an upward trend in the number of hematology articles published between 2004 and 2011, but the trend was reversed in the last 3 years. The number of articles from the other three countries (the UK, Japan, and Germany) remained relatively stable. In 2013, China surpassed the UK and approached Japan with respect to the number of hematology articles published. There is no doubt that the USA is the leader in this area of research and has a much stronger research effort than the other five countries. The same pattern was demonstrated when the publication of different types of articles was analyzed. The USA was the leader in publishing each type of article, especially reviews and RCTs. A review is an attempt to summarize the current state of understanding on a specific topic and make comments, and is usually written by a leading expert in the area [5]. A RCT is the gold standard for a clinical trial, and is often used to determine the effectiveness of  With respect to the number of articles, China has made tremendous progress. The GDP of China ranks second in the world behind the USA. Between 2000 and 2012, the amount of research spent in China increased from $10.8 billion to $168 billion. According to an OECD estimation, the Chinese government invested 1.98% of the GDP in research in 2012 [6], and the amount announced by the government may reach 2.5% in 2020 [7]. Various types of medical research-funded projects also increased considerably in the past decade. For example, the Department of Health Sciences affiliated with the National Natural Science Foundation of China was founded in 2009 and there is a special office dedicated to funding respiratory, hematology, and circulatory system research. In fact, funds from this office increased significantly from 228.81 million yuan in 2010 to 591.09 million yuan in 2013. Furthermore over the past decade, the number of Chinese scientific and technical personnel experienced the same rapid growth. All of those factors have greatly promoted Chinese research in the field of hematology.
The IF of an academic journal is a measure reflecting the average number of citations to recent articles published in the journal. The IF is frequently used as a proxy for the relative importance of a journal within its field; journals with higher IFs are deemed to be more important than journals with lower IFs. Despite considerable criticism regarding the IF, the IF is universally accepted as the most convincing index for quality evaluation of journals [8,9]. In the past 10 years, the cumulative IFs of articles published in the USA were several times higher than the other countries. With respect to the median IF of published articles, the UK led the countries surveyed, while the articles published from Japan, China, and South Korea were significantly lower than articles published from Europe and USA; these findings did not change significantly in 2009-2013. When comparing the distribution of publications related to the IF, articles published from Europe and USA were shown to be mostly published in the top 25% of journals; however, China lagged behind and ranked last with respect to publications in the top 25% of journals. This is an important method regarding the evaluation of  publication quality, and the result may alert Chinese scientists in this regard. This phenomenon, at least in part, may be a reflection of China, Japan, and South Korea being non-English speaking countries. Indeed, European and USA researchers may not pay close attention to scientific findings published in languages other than English.
Despite the rapid growth in the number of articles from China, the quality was not satisfactory. This may be associated with the current imperfect evaluation system on research performance that exists in mainland China [10,11], which enforced researchers to pay more attention to quantity rather than quality. The citation reports and the number of publications in the top 10 journals further support the above conclusions.
There were several limitations in the present study. Even though the journal list was generated based on the hematology category in SCIE subject categories, there may be excellent hematology journals that were not included by SCIE. Second, the publication of some international collaborative studies may have only listed one address for all authors. Therefore, when included in this study, the contributions of other countries were ignored. Third, there are some hematology-related articles published in general medical journals, which likely affected our results.

Conclusions
In conclusion, there is no doubt that the USA has played the most important role in the field of hematology research in the past decade. Overall, the quality of publications in European countries is better than Asian countries. We are delighted to see that China is closing the gap with

Search strategy
Sixty-eight hematology journals were selected from the Hematology category of the Science Citation Index Expanded (SCIE) subject categories, as designated by Thomson Reuters. The 68 journals, which are all indexed by PubMed, cover resources that involve blood and blood-forming tissues, as well as the function, diseases, and treatments of the hematologic system. The topics included hemophilia, neoplastic disorders of the blood or lymphoid tissues, and mechanisms and disorders of thrombosis. A computerized literature search was conducted in the PubMed database on 2 October 2014, and the articles published in the 68 journals from China, the USA, the UK, Germany, Japan, and South