Scientific Publications in Pharmacology and Pharmacy Journals from Chinese Authors in Various Parts of North Asia: a 10-year Survey of the Literature

The Journal of International Medical Research 2010; 38: 750 759 [first published online as 38(3) 5] Scientific Publications in Pharmacology and Pharmacy Journals from Chinese Authors in Various Parts of North Asia: a 10-year Survey of the Literature G LI 1 *, L-H HU 2 *, Z LIAO 2 *, H-C CUI 3 AND Z-S LI 2 1 Department of General Surgery, 2 Department of Internal Medicine, and 3 Department of Pharmaceutical Sciences, Changhai Hospital, Shanghai, China The amount and quality of pharmacology and pharmacy research by authors from China was investigated by comparing published articles from 136 international journals (1998 2007) by authors from mainland China, Hong Kong and Taiwan. The number of articles, clinical trials, randomized controlled trials, case reports, impact factors, number of citations and number of articles published in top general medicine journals were compared. The total number of articles increased significantly between 1998 and 2007 (from 324 to 2536 per year). In total, there were 12 021 articles: 7576 from mainland China, 3267 from Taiwan and 1178 from Hong Kong. The accumulated impact factor of the articles from mainland China (16 688.94) was much higher than for those from Taiwan (8726.92) and Hong Kong (3161.22) but, among the three regions, Hong Kong had the highest mean impact factor and the most articles published in top general medicine journals. KEY WORDS: PUBLICATION RESEARCH; CHINA; IMPACT FACTOR; SCIENCE CITATION INDEX; JOURNAL CITATION REPORTS; PHARMACY; PHARMACOLOGY Introduction In the scientific community, the productivity of a scientist is usually measured by their scientific output. The productivity of a group, an institution or, on a larger scale, a country can be similarly assessed. 1,2 Although China was ranked sixth out of the top 20 countries in Essential Science Indicators (January 1997 31 August 2007), 3 as measured by publication of articles in all scientific fields, pharmacology and pharmacy publications *Dr Li, Dr Hu and Dr Liao contributed equally to this work. by Chinese authors were not reported. The aim of the present study was to show the contribution of Chinese authors from three major regions of China mainland China, Hong Kong and Taiwan to pharmacology and pharmacy research. Materials and methods JOURNAL SELECTION AND SEARCH STRATEGY A total of 138 journals relating to pharmacology and pharmacy were selected from the pharmacology and pharmacy 750

section of the Institute for Scientific Information (ISI) Science Citation Index (SCI) subject categories. 4 The section covers resources on the discovery and testing of bioactive substances (including animal research), clinical experience, delivery systems and the dispensing of drugs. This category also includes resources on the biochemistry, metabolism and toxic or adverse effects of drugs. The Journal of Drug Delivery Science and Technology and Zeitschrift für Naturforschung, which are not indexed by PubMed, were excluded. A computerized literature search was conducted in the PubMed database on 20 October 2008. 5 Articles from mainland China, Taiwan and Hong Kong published from January 1998 to December 2007 in these journals were sought. The ISSN (print) was used to perform searches in PubMed. The search terms used were: 1671-4083 or 0169-409X or 0741-8329 or 0269-2813 or 1079-2082 or 0002-9459 or 1060-0280 or 0065-7743 or 0362-1642 or 0959-4973 or 0066-4804 or 0166-3542 or 1359-6535 or 0365-6233 or 0004-4172 or 1742-7835 or 0955-8810 or 0006-2952 or 0918-6158 or 1045-1056 or 0269-3879 or 0753-3322 or 0142-2782 or 0306-5251 or 0007-1188 or 0008-4212 or 1084-9785 or 0344-5704 or 0920-3206 or 1755-5914 or 0009-2363 or 0009-2797 or 0009-3157 or 0899-0042 or 1064-1963 or 0305-1870 or 1173-2563 or 0362-5664 or 0312-5963 or 0009-9236 or 0149-2918 or 1172-7047 or 1551-7144 or 0743-4863 or 0929-8673 or 1367-6733 or 1381-6128 or 0011-393X or 0148-0545 or 0363-9045 or 0272-4391 or 1359-6446 or 0090-9556 or 0360-2532 or 0114-5916 or 0012-6667 or 1170-229X or 1382-6689 or 0031-6970 or 0928-0987 or 0939-6411 or 0014-2999 or 0924-977X or 0885-6222 or 0892-3973 or 0268-1315 or 1567-5769 or 0924-8579 or 0946-1965 or 1461-1457 or 0378-5173 or 0167-6997 or 0021-8820 or 0305-7453 or 0160-2446 or 1044-5463 or 0091-2700 or 0269-4727 or 0271-0749 or 0168-3659 or 1061-186X or 0378-8741 or 0300-0605 or 0362-4803 or 0265-2048 or 0163-3864 or 0731-7085 or 0022-3549 or 1567-567X or 1347-8613 or 0022-3565 or 0022-3573 or 0269-8811 or 0140-7783 or 0024-3205 or 0198-6325 or 0379-0355 or 1076-6294 or 0026-895X or 1474-1776 or 0028-1298 or 0028-3908 or 0893-133X or 0161-813X or 0196-9781 or 0724-8741 or 1539-1604 or 1170-7690 or 1053-8569 or 1744-6872 or 1462-2416 or 1043-6618 or 0031-6997 or 0031-7012 or 0163-7258 or 0091-3057 or 0176-3679 or 0277-0008 or 0928-1231 or 0031-7144 or 0951-418X or 0032-0943 or 0278-5846 or 0033-3158 or 1611-020X or 0273-2300 or 0303-4240 or 1660-5527 or 0163-4356 or 0300-483X or 0041-008X or 0041-0101 or 0165-6147 or 1537-1891 or 0049-8254 or 0031-6903 and Hong Kong[ad], Taiwan[ad], and China[ad] not Hong Kong[ad] not Taiwan[ad]. Articles that showed the first author s affiliation (ad) with one of the three regions were considered as research output from that region. The number of articles in the fields of clinical trials, randomized controlled trials (RCTs) and case reports were generated according to the publication types listed by PubMed. COMPARISON OF RESEARCH ARTICLES To compare the quality of the research articles, three methods were used. First, the accumulative impact factor for all articles and the mean impact factor (i.e. the accumulated impact factor for all articles/the number of articles) were generated according to Journal Citation Reports (JCR) 2007 produced by the ISI. 6 Secondly, citation reports of articles having 751

an affiliation with a Chinese institution were collected. Thirdly, articles published in top general medicine journals (N Engl J Med, JAMA, Lancet, BMJ and Ann Intern Med) were collated. Articles related to pharmacology and pharmacy were extracted first independently and, subsequently, by consensus if a disagreement existed between the reviewers (L-H.H. and Z.L.), by reviewing the titles, abstracts and, if necessary, the full text. Articles from China published in the top 10 high impact factor pharmacology and pharmacy journals were also studied. Furthermore, the top 10 most popular pharmacology and pharmacy journals of the three regions were determined according to the number of published articles. STATISTICAL ANALYSIS Statistical analyses were performed using STATA, version 8.0 (StataCorp LP, College Station, TX, USA). A non-parametric test for trends was performed to determine any significant change in the total numbers of papers over the time period. Kruskal Wallis tests were used to detect differences between the three regions, and rank-sum tests were to be carried out between two regions, if necessary. The tests for significance were twotailed and a P-value < 0.05 was considered to be statistically significant. Results TOTAL NUMBER OF ARTICLES AND TRENDS A total of 220 182 pharmacy and pharmacology articles were published worldwide from 1998 to 2007 in the 136 selected journals, of which 5.5% were from China (12 021/220 182). Of the papers from China, 63.0% were from mainland China (7576/12 021), 27.2% from Taiwan (3267/12 021) and 9.8% from Hong Kong (1178/12 021). The numbers of papers published per year increased significantly between 1998 and 2007 in the three regions; from 98 to 1913 in mainland China, from 162 to 467 in Taiwan and from 64 to 156 in Hong Kong (all P < 0.001; Fig. 1). From 2000 onwards, the number of published articles from mainland China exceeded that from Taiwan, and even exceeded the total number of published articles from Taiwan and Hong Kong combined from 2003 onwards. The percentage of articles published in the regions of China each year as a share of the total published articles increased significantly in mainland China (P < 0.001), Taiwan (P = 0.023) and Hong Kong (P = 0.003, Fig. 2). CLINICAL TRIALS, RCTs AND CASE REPORTS Fifteen case reports from mainland China were published (0.2% of total articles published from mainland China) between 1998 and 2007, which was significantly less in percentage terms than for Taiwan (67, 2.1%, P = 0.009) and Hong Kong (12, 1.0%, P = 0.045). The difference between Taiwan and Hong Kong was not statistically significant (Fig. 3). Fifty-nine RCTs from Hong Kong (5.0% of total articles published from Hong Kong) were published between 1998 and 2007, significantly more in percentage terms than for mainland China (122, 1.6%, P = 0.001) or Taiwan (58, 1.8%, P = 0.001); the difference between mainland China and Taiwan was not statistically significant. Since 2004, the number of published RCTs per year from mainland China has exceeded the total number of RCTs published from Taiwan and Hong Kong. The same result was found for clinical trials. Hong Kong published 103 clinical trials (8.7% of total articles published from Hong Kong) between 1998 and 2007; significantly 752

2000 Number of articles 1750 1500 1250 1000 750 500 Mainland China Taiwan Hong Kong 250 0 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 Year FIGURE 1: Trends in publication figures for pharmacology and pharmacy articles from authors from mainland China, Taiwan and Hong Kong from 1998 to 2007, showing a significant increase in the numbers of articles published per year from 1998 to 2007 in the three regions (all P < 0.001) 8 Share of articles (%) 7 6 5 4 3 2 Mainland China Taiwan Hong Kong 1 0 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 Year FIGURE 2: The share of pharmacology and pharmacy articles published each year from authors in mainland China, Taiwan and Hong Kong from 1998 to 2007 as a percentage of the total number of published articles, showing a significant increase in articles from mainland China (P < 0.001), Taiwan (P = 0.023) and Hong Kong (P = 0.003) 753

10 P < 0.001 P < 0.001 Share of different types of article (%) 8 Mainland China Taiwan Hong Kong 6 4 2 P = 0.009 P = 0.045 P = 0.001 P = 0.001 0 Case reports RCT Clinical trials FIGURE 3: The percentage of pharmacology and pharmacy articles from authors from mainland China, Taiwan and Hong Kong reporting clinical trials, randomized controlled trials (RCTs) and case reports, showing that the percentage of published case reports was significantly lower for mainland China versus Taiwan and Hong Kong, and that the percentage of published RCTs and clinical trials was significantly higher for Hong Kong versus Taiwan and mainland China more in percentage terms than mainland China (229, 3.0%, P < 0.001) or Taiwan (139, 4.3%, P < 0.001). When individual years were studied, from 2002 onwards the number of clinical trials published from mainland China exceeded that from Hong Kong and, in 2004, the total published from mainland China exceeded that from Taiwan (data not shown). IMPACT FACTOR As expected, the accumulated impact factor of articles from mainland China (16 688.94) was much higher than for those from Taiwan (8726.92) or Hong Kong (3161.22) (P < 0.001, Kruskal Wallis test). Hong Kong had the highest mean impact factor of 2.68, followed by Taiwan with 2.67 and then mainland China with 2.20 (P < 0.001, Kruskal Wallis test) (Table 1). CITATION REPORTS Currently there is no function within the JCR for searching for citation reports of articles by the department of the first author. 6 So, for the citation reports for articles published in pharmacology and pharmacy journals, the articles included were those affiliated with a Chinese institution, which produced more results than had previous searches in PubMed. Between 1998 and 2007, mainland China had the highest number of total citations, 38 614 for 10 920 articles, followed by Taiwan with 27 772 citations for 4505 articles and Hong Kong with 13 313 citations for 1974 articles. Total citations per year between 1998 and 2007 are shown in Fig. 4. HIGH IMPACT AND TOP-RANKING JOURNALS A total of 88 articles from the three regions 754

TABLE 1: Accumulated and mean impact factor of articles from authors from mainland China, Taiwan and Hong Kong by year, from 1998 to 2007 Accumulated impact factor Mean impact factor Year Mainland China Taiwan Hong Kong Mainland China Taiwan Hong Kong 1998 223.65 416.18 164.18 2.28 2.57 2.57 1999 372.01 523.30 207.20 2.43 2.63 2.69 2000 602.96 592.25 268.76 1.95 2.63 2.56 2001 749.30 710.65 286.08 1.98 2.58 2.67 2002 856.69 766.73 302.20 2.01 2.60 2.80 2003 1233.21 823.96 345.16 2.12 2.64 2.85 2004 1783.59 978.37 335.99 2.10 2.62 2.80 2005 2696.42 1234.32 389.60 2.23 2.67 2.58 2006 3854.42 1376.42 420.94 2.33 2.78 2.49 2007 4316.71 1304.75 441.12 2.26 2.79 2.83 Total 16688.94 8726.92 3161.22 2.20 2.67 2.68 Total accumulated impact factor for mainland China, Taiwan and Hong Kong (P < 0.001, Kruskal Wallis test). Total mean impact factor for mainland China, Taiwan and Hong Kong (P < 0.001, Kruskal Wallis test). were published in the 10 top-ranking pharmacology and pharmacy journals; 77.3% (68/88) were in Neuropsycho - pharmacology, Clin Pharmacol Ther and Trends Pharmacol Sci. Fifty-nine articles from mainland China were published in the high impact top 10 pharmacology and pharmacy journals, compared with 19 and 10 articles from Taiwan and Hong Kong, respectively (Table 2). 14 000 12 000 10 000 Mainland China Taiwan Hong Kong Total citations 8000 6000 4000 2000 0 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 Year FIGURE 4: Total citations for articles by authors from mainland China, Taiwan and Hong Kong in pharmacology and pharmacy journals from 1998 to 2007. There was no statistically significant difference between the three regions 755

A total of 226 articles (mainland China, 41; Taiwan, 58; Hong Kong, 127) were published in the five top general medicine journals, N Engl J Med, Lancet, JAMA, BMJ and Ann Intern Med, of which 54 articles were concerned with pharmacology and pharmacy. Hong Kong, with 40, had the most articles (17 RCTs, six clinical trials, three reviews, five case reports and nine others; 14 in N Engl J Med, three in JAMA, 12 in Lancet, five in BMJ and six in Ann Intern Med); Taiwan had 10 articles (three RCTs, two case reports and five others; six in N Engl J Med, three in Lancet and one in JAMA); and mainland China had only four articles (two RCTs and two others; two in New Engl J Med and two in Lancet). MOST POPULAR JOURNALS The most popular pharmacology and pharmacy journals for authors from these three regions of China to choose for publishing their articles are listed in Table 3. Life Sci was the most popular journal in Taiwan and Hong Kong, while Acta Pharmacol Sin was the most popular in mainland China. Life Sci, Eur J Pharmacol and Planta Med appeared in the 10 top journal lists for each of the three regions. Discussion To the best of the authors knowledge, this is the first report to reveal the contribution of Chinese authors from the major regions of China (mainland China, Hong Kong and Taiwan) to pharmacology and pharmacy research. It is clear from the present study that the volume and quality of research in pharmacology and pharmacy from mainland China, as measured by the number of articles published in international journals, has increased significantly during the past 10 years. From 2000 onwards, the number of articles published from mainland China exceeded that from Taiwan, and has exceeded the total number of combined published articles from Taiwan and Hong Kong since 2003. Hong Kong and Taiwan have been at the forefront of scientific and medical research for many years 7 and investigators from these regions have contributed some of the best scientific papers in pharmacology and pharmacy. When impact factor, citation TABLE 2: Articles published in the 10 top-ranking (by impact factor) pharmacology and pharmacy journals by authors from mainland China, Taiwan and Hong Kong 2007 Mainland impact China Taiwan Hong Kong Rank Journal factor n (%) n (%) n (%) Total 1 Nat Rev Drug Discov 23.31 0 (0) 0 (0) 1 (100) 1 2 Annu Rev Pharmacol Toxicol 21.70 0 (0) 0 (0) 0 (0) 0 3 Pharmacol Rev 18.82 0 (0) 0 (0) 1 (100) 1 4 Trends Pharmacol Sci 9.61 10 (71) 0 (0) 4 (29) 14 5 Adv Drug Deliv Rev 8.22 0 (0) 0 (0) 0 (0) 0 6 Clin Pharmacol Ther 8.03 15 (79) 2 (11) 2 (11) 19 7 Pharmacol Ther 7.97 3 (100) 0 (0) 0 (0) 3 8 Med Res Rev 7.26 7 (64) 2 (18) 2 (18) 11 9 Drug Discov Today 6.76 3 (75) 1 (25) 0 (0) 4 10 Neuropsychopharmacology 6.16 21 (60) 14 (40) 0 (0) 35 Total 59 (67) 19 (22) 10 (11) 88 756

TABLE 3: The 10 most popular pharmacology and pharmacy journals for authors from mainland China, Taiwan and Hong Kong to choose for their publications, 1997 2007 Mainland China Taiwan Hong Kong Impact No. of Impact No. of Impact No. of Rank Journal factor articles Journal factor articles Journal factor articles 1 Acta Pharmacol Sin 1.68 1505 Life Sci 2.26 324 Life Sci 2.26 156 2 J Pharm Biomed Anal 2.76 588 J Nat Prod 2.55 250 Aliment Pharmacol Ther 3.20 107 3 Life Sci 2.26 405 Planta Med 1.85 166 Eur J Pharmacol 2.38 95 4 J Nat Prod 2.55 314 Eur J Pharmacol 2.38 161 Planta Med 1.85 46 5 Planta Med 1.85 265 Biochem Pharmacol 4.01 152 Br J Pharmacol 3.77 42 6 Int J Pharm 2.41 261 Toxicol Appl Pharmacol 3.85 129 J Ethnopharmacol 2.05 42 7 Eur J Pharmacol 2.38 251 Br J Pharmacol 3.77 127 Peptides 2.37 37 8 Chem Pharm Bull 1.22 231 Chem Pharm Bull 1.22 127 J Pharmacol Exp Ther 4.00 31 9 Pharmazie 0.78 226 Mol Pharmacol 3.62 107 Biomed Pharmacother 4.01 29 10 Biomed Chromatogr 1.66 205 J Ethnopharmacol 2.05 104 Clin Exp Pharmacol Physiol 2.04 27 Total 4251 Total 1647 Total 612 757

reports and articles published in top general medicine journals were studied for quality comparisons, the gap between mainland China, Taiwan and Hong Kong still appears to be considerable. Hong Kong had the highest mean impact factor, followed by Taiwan and then mainland China. A major consideration for these results is the fact that publications in the medical and scientific field that reach an international audience are virtually all written in English. This has given a major advantage to English-speaking countries, and has proven a challenge for investigators in non-english speaking countries. In 1978 mainland China decided to reform its economy and, since then, has gradually opened up to the world. The economy has grown rapidly at an average of 9.8% per year from 1978 to 2007 (State Statistical Bureau 2007). 8 Medical expenditure, especially for drugs, has grown even more rapidly. Due to the changing economic system and the higher cost of healthcare, the Chinese government has reformed its healthcare system, including its health and drug policy. The drug policy reform has led to more comprehensive policies on academic research, registration of new drugs, and their subsequent production, distribution, utilization and administration. 9 New policy and rapid economic growth have given an immense boost to the development of pharmacology and pharmacy in mainland China. Although 59 RCTs from Hong Kong were published between 1998 and 2007, and the number of RCTs/total articles published from Hong Kong was much higher than from mainland China or Taiwan, the number of published RCTs per year from mainland China exceeded the total number of published RCTs from Taiwan and Hong Kong in 2004 and in each subsequent year. The same result was found for clinical trials. There are several possible reasons for these results. First, China has a population of 1.3 billion people, and so has a huge number of subjects for prospective enrolment in RCTs. Secondly, Chinese people are more compliant than the Western population. 10,11 Thirdly, trials in China are much cheaper to conduct. 12 The publication of articles concentrating on Chinese ethnicity or traditional Chinese medicine, not only from Chinese authors but also from authors from other parts of the world, has also increased significantly during the past 10 years. 1,7,10,11 The articles in the present study were retrieved using the PubMed computerized search system, which is a comprehensive database run by the National Center for Biotechnology Information at the National Library of Medicine in Bethesda, Maryland, USA, containing articles from high-quality medical journals. The present study also used data from the JCR. The JCR has been published by the ISI since 1975 and represents the most comprehensive citation index to the scientific literature, covering more than 6000 journals in 2007. It should also be mentioned here that, although impact factors are not the optimal parameter for determining the quality of articles since even the main journals may at times publish poor-quality articles, they are at present the best available parameter for determining the quality of studies. 12,13 There are some limitations to the present study. Although the journals were selected from the pharmacology and pharmacy section of the SCI category, some journals related to pharmacology and pharmacy were not included in SCI. The authors addresses were also limited by region (mainland China, Hong Kong or Taiwan), and articles that only addressed particular Chinese cities or provinces were not 758

included. The region of Macau was also originally included in the present analysis, but was excluded when it was found that there were few articles from that region. The study was, therefore, limited to only three regions, which have been used to reflect the state of pharmacology and pharmacy research in the whole of China. In conclusion, the number of published articles from mainland China, Taiwan and Hong Kong has increased significantly during the past 10 years. The numbers of articles published per year from mainland China has exceeded the number published from Taiwan and Hong Kong. Articles from Taiwan and Hong Kong have, however, achieved a higher mean impact factor than published articles from mainland China. Conflicts of interest The authors had no conflicts of interest to declare in relation to this article. Received for publication 1 December 2009 Accepted subject to revision 27 January 2010 Revised accepted 22 March 2010 Copyright 2010 Field House Publishing LLP References 1 Cappell MS, Davis M: A significant decline in the American domination of research in gastroenterology with increasing globalization from 1980 to 2005: an analysis of American authorship among 8,251 articles. Am J Gastoenterol 2008; 103: 1065 1074. 2 Hu LH, Liao Z, Li ZS: Do the two ends reflect the full picture? Am J Gastroenterol 2008; 103: 2941 2942. 3 The Year 2007: Top 20 Country Rankings in All Fields. In-Cites Essential Science Indicators. New York: Thompson Reuters, 2007 (available at: http://www.in-cites.com/countries/2007all fields.html). 4 Journal search. Science Citation Index Expanded Subject Categories. New York: Thompson Reuters (available at: http://science.thomsonreuters. com/mjl/). 5 PubMed. Bethesda: National Center for Biotechnology Information, US National Library of Medicine, National Institutes of Health (available at: http://www.ncbi.nlm. nih.gov/entrez/query.fcgi?db=pubmed). 6 Institute for Scientific Information (ISI): Journal Citation Reports. New York: Thompson Reuters, 2007 (available at: http://www.isiwebof knowledge.com/). 7 Goh KL, Farrell GC: Publications from China: the sleeping giant awakens. J Gastroenterol Hepatol 2008; 23: 341 343. 8 Qin XJ, Shi HZ: Major causes of death during the past 25 years in China. Chin Med J (Engl) 2007; 120: 2317 2320. 9 Dong H, Bogg L, Rehnberg C, et al: Drug policy in China: pharmaceutical distribution in rural areas. Soc Sci Med 1999; 48: 777 786. 10 Cheng TO: Cardiology in contemporary China: An update. Int J Cardiol 2008; 126 147 159. 11 Hu LH, Liao Z, Gao R, et al: Scientific publications in cardiology and cardiovasology journals from Chinese authors in various parts of North Asia: 10-year survey of literature. Int J Cardiol 2010; 140: 304 308. 12 Mervis J: China s unique environment favors large intervention trials. Science 1995; 270: 1149 1151. 13 Hu LH, Liao Z, Gao R, et al: High quality medical journals and impact factors. Int J Cardiol 2010; 140: 362 363. Author s address for correspondence Professor Zhao-Shen Li Department of Internal Medicine, Changhai Hospital, Second Military Medical University, 168 Changhai Road, Shanghai 200433, China. E-mail: zhaoshenli@hotmail.com 759