Top-cited articles in digestive system disease from 1950 to 2013 Xiaowei Tang, Wei Gong, Fangfang Yuan, Ran Li, Xiaomei Han, Silin Huang, Fachao Zhi and Bo Jiang Department of Gastroenterology, Nanfang Hospital, Southern Medical University, Guangzhou, China

Key words bibliometrics, citation analysis, digestive disease, landmark article, publication. Accepted for publication 25 June 2015. Correspondence Dr. Bo Jiang, Department of Gastroenterology, Nanfang Hospital, Southern Medical University, no. 1838, Guangzhou North Ave, 510515, Guangzhou, China. Email: [email protected] Conflicts of interest: No conflicts of interest exist for all authors.

Abstract Background and Aim: Examination of top-cited articles is a tool that can help to identify and monitor outstanding scientific researches and landmark papers. We aimed to identify the 100 most cited published papers in peer-reviewed biomedical journals in the field of digestive diseases and to examine their characteristics. Methods: The Web of Science (including Science Citation Index) was searched for the most cited papers related to digestive diseases, published from 1955 to the present. The top 100 most cited articles were identified. The number of citations, countries, and institutions of origin, year of publication, study design, topic, and levels of evidence of the articles were noted and analyzed. Results: The most top-cited articles had a mean of 1375 citations. These articles were published between 1978 and 2009 in 29 high-impact journals, with the New England Journal of Medicine (n = 22) topping the list. Of the 100 articles, 34 were clinical studies, 15 were review articles, and 34 were concerned basic science. These articles came from 18 countries, with the USA contributing most of the top-cited articles (n = 53). Eighty-seven institutions produced these 100 top-cited articles, led by the University of Barcelona (n = 4). Seven persons authored two or more of these top-cited articles. The mostly represented specialty was gastrointestinal oncology (n = 49). Conclusions: Our study can give a historical perspective on the scientific progress of digestive diseases, as well as allow for recognition of most important advances in this area and provide useful information to guide future researches.

Introduction The proliferation of journals and the overload of medical papers indexed daily in Internet databases have led to a plethora of information, which makes it difficult for an individual to maintain a general understanding of that body of knowledge. Thus, there is a need to improve the physicians’ ability to quickly find important articles in their area of interest. Articles that are of value to other researches are often cited in subsequent manuscripts. The number of times that one article is cited by other papers is widely used to assess its impact on the scientific community.1,2 Furthermore, frequently cited articles also serve the important role of transferring and exchanging up-to-date knowledge on clinical practice and research methodology within healthcare staff and researchers. In 1977, Eugene Garfield et al. described highly cited articles with the term “citation classics” using the Social Sciences Citation Index.3 Recently, several studies have identified and analyzed highly cited articles in some fields, such as ophthalmology,4 urology,5 emergency care,6 psychiatrics,7 orthopedics,8 and critical care medicine.9 However, to the best of our knowledge, this type of identification has not been conducted in digestive diseases. Thus, the aim of this study was to identify and examine the characteristics of the 100 most

frequently cited articles in the literature and to gain insight into the types of influential publications in this field of gastroenterology and hepatology, both in the present and in the past.

Materials and methods The Institute for Scientific Information (ISI) Web of Knowledge (including Science Citation Index Expanded) was queried on the 25th of September, 2013, for articles relating to digestive and hepatic disease published from 1950 (the earliest year for which data were available) up to and including the date of the search, using the subject term “digestive disease*” or “gastroenterology*” or “hepatology*” (the asterisk was included in the search string as a wild card character), and results were sorted by the category “Times Cited”.10 Our search provided a list of all articles appearing in a given journal ranked by citation count. All electronic searches were conducted on one specific day, September 25, 2013, to avoid changes in citation rate as much as possible. The full texts were mainly obtained by PubMed, Embase, and ScienceDirect. When full text articles were not available online, we used the online abstract. The 100 most frequently cited articles were selected by reading the abstract to estimate whether they were related to digestive

Journal of Gastroenterology and Hepatology 31 (2016) 107–111 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd


X Tang et al.

Top-cited articles in digestive disease

diseases by two researchers (Fangfang Yuan and Ran Li). Data were extracted from each of the articles by researchers (Silin Huang and Fachao Zhi) using a predesigned Microsoft Excel template and then checked by other researchers (Wei Gong and Xiaomei Han). All the data were analyzed by two investigators (Xiaowei Tang and Bo Jiang) with regard to the authorship (only considering the first and the second authors), institution, journal name, date of publication, country of origin, number of citations, the type of study, and the topic. For each article, the type of the article was categorized as follows: (i) review, including literature and systematic review, and meta-analysis; (ii) clinical research, including randomized controlled trials (RCTs), observational (prospective) study, observational (retrospective) study and case report; (iii) guideline and consensus; (iv) basic science, including bench-top laboratory research or research involving animal models; and (v) others, for those not belonging to any of the previous four categories. The topics were divided into gastrointestinal (GI) oncology, hepatology, inflammatory bowel disease, intestinal microbial flora, helicobacter pylori, and others.

ISI Web of Knowledge. The 100 most cited articles were listed in Supporting Information Table S1 in descending order of the number of citations they have. The most cited article received 4895 citations, and the least cited article received 853 citations,11,12 with a mean of 1375 citations per article. Journals and publication years of most cited articles. The top 100 cited articles were published in 29 high-impact journals, led by New England Journal of Medicine (n = 22), followed by Hepatology (n = 12), Nature (n = 10), Lancet (n = 9), Gastroenterology (n = 8), Science (n = 8), Cell (n = 4), Nature Medicine (n = 3), Cancer Research (n = 2), Journal of Biological Chemistry (n = 2), Nature Genetics (n = 2), Alimentary Pharmacology and Therapeutics (1) and others (Table 1). These articles were published between 1978 and 2009. Manning et al.13 had the oldest article in the top 100, and it was published in 1978 in British Medical Journal. The newest article was published in 2009 by Tanaka et al. in Nature Genetics.14 As shown in Figure 1, more than 95% of the 100 most cited articles have been published after the year 2000.

Results During the study period, 8935 articles were cited ≥100 times, and 678 articles were cited ≥400 times related to digestive diseases in Table 1 Rank 1 2 3 4 5a 5b 6 7 8a 8b 8c 9a 9b 9c 9d 9e 9f 9g 9j 9k 9l 9m 9n 9o 9p 9q 9r 9s 9t †

Authors, countries, and institutions. The first author was affiliated with an academic department in most classic articles.

Journals in which the top 100 cited digestive disease articles were published Journals

No. of articles (%)

Average no. of citations per paper

Impact factor† (2012)

New England Journal of Medicine Hepatology Nature Lancet Gastroenterology Science Cell Nature Medicine Cancer Research Journal of Biological Chemistry Nature Genetics Alimentary Pharmacology and Therapeutics Annals of Internal Medicine Annals of Surgery British Medical Journal Gut Human Pathology Infection and Immunity Journal of American Medical Association Journal of Clinical Investigation Journal of Clinical Oncology Journal of Hepatology Journal of the National Cancer Institute Nature Reviews Immunology Nature Reviews Microbiology Nucleic Acids Research Proceedings of the National Academy of Sciences of the United States of America Surgery The Journal of Applied Bacteriology

22 12 10 9 8 8 4 3 2 2 2 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1

1380.030 1279.494 1441.206 1391.742 1038.629 1150.417 1091.985 1353.5 1057.861 982.021 976.025 928 1791 1081 1022 964 1499 1830 1071 1372 1879 2084 982 853 995 2667 979

51.658 12.003 38.597 39.06 12.821 31.027 31.957 22.864 8.65 4.651 35.209 4.548 13.976 6.329 12.827 10.732 2.843 4.074 29.978 12.812 18.038 9.858 14.336 33.129 22.49 8.278 9.737

1 1

1039 1849


Journal impact factor based on Thomson Reuters Web of Knowledge Journal Citation Reports Ranking (2012).


Journal of Gastroenterology and Hepatology 31 (2016) 107–111 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd

X Tang et al.

Top-cited articles in digestive disease

Table 3

Countries of origin of the top-cited articles


Figure 1 year).

Pattern of distribution of top-cited articles (no. of article per

Seven authors published two or more top-cited articles. Table 2 presented a list of these authors, which is obviously led by Llovet JM, who authored four classic papers, and Bruix J, who authored three classic papers. The 100 articles originated from 18 different countries (Table 3): 53 from the USA; 9 from Spain; 8 from France; 5 from Germany; 4 from UK and the Netherlands; 3 from Italy and Japan; 2 from Belgium; and 1 from Australia, Canada, China, Denmark, Finland, Greece, Hong Kong, Switzerland, and Taiwan. Of the total 100 articles, 21 originated from multi-institutional collaboration of which 10 were from multinational collaboration and 53 from individual institutions. Five institutions produced more than one classic article (Table 4). Barcelona-Clínic Liver Cancer Group, Liver Unit, Digestive Disease Institute, IDIBAPS, Hospital, University of Barcelona, Spain, led in this list with four classic articles.

1 2 3 4 5 5 6a 6b 7 8a 8b 8c 8d 8e 8f 8g 8h 8j

Table 4



Research design, topic of study, and level of evidence of most cited articles. In terms of the study design, about half of the articles (n = 44) reported clinical research, including RCTs (n = 24), observational (prospective) study (n = 7), observational (retrospective) study (n = 1), and case report (n = 2); 15 were reviews and 34 were basic science studies, 12 were guidelines and consensus, and the remaining 5 were questionnaires and clarification (Table 5). The most common topic was GI oncology (n = 49), followed by hepatology (n = 25), inflammatory bowel disease (n = 10), intestinal microbial flora (n = 6), helicobacter pylori (n = 3), and others (n = 7). Among the GI oncology, the majority of top-cited articles (n = 24) focused on colorectal cancer, and about half of these Table 2 Rank 1 2 3a 3b 4a 4b 5

Authors with two or more top-cited articles Author

No. of articles


Llovet JM Bruix J Demetri GD Malfertheiner P Strader DB Sherman M Megraud F

4 3 2 2 2 2 2

4 2 2 2 1 1




No. of articles

USA Spain France Germany UK the Netherlands Italy Japan Belgium Australia Canada China Denmark Finland Greece Hong Kong, China Switzerland Taiwan, China

53 9 8 5 4 4 3 3 2 1 1 1 1 1 1 1 1 1

Institutions of origin with two or more top-cited articles

Rank 1



No. of articles

Barcelona-Clínic Liver Cancer Group, Liver Unit, Digestive Disease Institute, IDIBAPS, Hospital, University of Barcelona, Spain Barcelona Clinic Liver Cancer (BCLC) Group, Liver Unit, Hospital Clínic, University of Barcelona, Spain Center for Internal Medicine, Clinic of Gastroenterology, Otto-von-Guericke University of Magdeburg, Germany Division of Gastroenterology and Hepatology, Mayo Clinic and Foundation, USA Division of Gastroenterology, University of Michigan Medical School, USA






studies were RCTs (n = 11). Other subspecialty areas in GI oncology included hepatic cancer (n = 11), GI stromal tumor (n = 6), gastric cancer (n = 4), pancreatic cancer (n = 1), and esophageal cancer (n = 1). For the part of hepatology, hepatitis (n = 15) and nonalcoholic fatty liver disease (n = 6) were mostly discussed. Levels of evidence from Oxford Centre for Evidence-based Medicine (2009 edition) were used to evaluate the clinical studies.15 There were 21 studies at levels 1a, 9, 1, and 1 and two studies at levels 1b, 2a, 2b, and 3a, respectively.


Discussion 1 1 2

With the development of Internet-based search engines, many methods to search for relevant medical literature now exist. While these online databases are easy to use, the results of basic keyword or topic searches are often overwhelming and shed little light on

Journal of Gastroenterology and Hepatology 31 (2016) 107–111 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd


X Tang et al.

Top-cited articles in digestive disease

Table 5

Field of study based on types of studies

Field of study

Gastrointestinal oncology Colorectal cancer Hepatic cancer Gastrointestinal stromal tumor Gastric cancer Pancreatic cancer Esophageal Cancer Others Hepatology Hepatitis Nonalcoholic fatty liver disease Liver fibrosis Others Inflammatory bowel disease Intestinal microbial flora Helicobacter pylori Others Total

Clinical study


49 24 11 6 4 2 1 1 25 15 6 1 3 10 6 3 7 100


Prospective study

Retrospective study

Case report

11 3 2 2 — — — — 3 1 — — 2 — — — 24

1 1 — 1 — — — — 2 2 — — — — — — 7

— — 1 — — — — — — — — — — — — — 1

1 — 1 — — — — — — — — — — — — — 2

Basic science study


Guideline and consensus


8 1 1 1 2 — 1 — 4 — — 3 5 4 — 4 34

— 3 — — — 1 — — 3 1 1 — 3 2 1 — 15

2 2 1 — — — — — 3 1 — — — — 2 1 12

1 1 — — — — — — — 1 — — — — — 2 5

RCT, randomized controlled trial.

the most relevant articles. The number of times that an article is cited by other articles is widely used to measure its impact and to assess its quality by an individual author and can help physicians to quickly find important articles in their area of interest. In this study, we identified and characterized the 100 most frequently cited articles in the field of gastroenterology and hepatology in the past 60 years by using the search tool of ISI Web of Knowledge (including Science Citation Index Expanded). ISI Web of Knowledge, produced by the Institute for Scientific Information, is well known as the world’s leading citation database, which collectively index more than 12 000 academic and scientific journals.10 It can provide academic citation indexing and search service. The 100 most frequently cited articles published in digestive literature from 1950 to 2013 were cited 853–4895 times. This number is considerably higher than citation classics in urology studies, in which studies received from 418–1435 citations,8 or orthopedic surgery,5 counting 353–1748 citations during the time periods covered in those studies. Citation rates differ for each specialty and might depend on the number of researchers working in a specific scientific field.16 As cancer continues to increase largely in the world, research on various cancers draw more and more attention. Based on the GLOBOCAN 2011, there are five kinds of GI cancers in the list of 10 common cancers leading to death.17 In our analysis, 49 most cited articles were related to GI oncology, which demonstrated that more researchers worked in this area in comparison with other subspecialties of digestive diseases. This also explains why the citations of articles in digestive diseases are much higher than the articles of other fields. It is well recognized that different study designs could correspond to different levels of evidence. The goal of rating study designs and levels of evidence is to indicate the best available evidence for use in patient care. Among various study designs,


RCTs are considered to provide the highest quality evidence for most clinical or interventional trials. There were 24 RCTs in the top 100 articles of digestive diseases, the number of which is much higher than the RCTs among other top medical articles, such as urology (14 RCTs),5 rehabilitation (9 RCTs),18 orthodontics (3 RCTs),19 and endodontology (0 RCTs).20 The majority of RCTs focused on the GI oncology (18 RCTs). More high-quality RCTs in other subspecialties of GI diseases, such as hepatology and inflammatory bowel disease, are needed in the future. Our study found that most of the 100 top articles originated from the USA, which is similar to the origin of the top 100 citation classics in the fields of critical care medicine and others.6–9 Also, nine of the 17 top institutions of gastroenterology and hepatology are located in the USA. These findings prove the USA’s overwhelming impact on medical science research because of its large population and the abundant financial resources available to the scientific community. It is also reported that American authors tend to be biased in their citation process toward local articles and that US reviewers prefer US papers.21,22 Articles that are more recently published will have a shorter exposure to the medical community. Arguably, their citations may be less often than older papers that have a longer presence in the literature.23 Surprisingly, our study found that the 100 top-cited articles in digestive diseases were younger articles, only three articles were published before 2000, and more than 95 of the 100 most cited articles have been published after the year 2000. The years with the most publications in our research were 2003 and 2004. This is very unexpected, as it has been reported that the true impact of an article cannot be assessed until 20 years after its publication with an article’s maximum citations per year occurring 3 to 10 years after publication.16 This result is contrary to other study. One of the reasons for that is that the time period

Journal of Gastroenterology and Hepatology 31 (2016) 107–111 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd

X Tang et al.

varies with specialty as different journals and areas have different citation half-lives.24 In addition, this also reflects that the number of researches in digestive diseases increased, and more resources and materials were put into this field in the past 10 years. Another observation is also unexpected. The list of frequent authors on citation classics can give a sampling of some of the world’s best recognized experts in the field of digestive disease research. But some famous experts were missed in our analysis, such as Dr. Marshall BJ and Warren JR, who won the Nobel prize for medicine in 2005 for their discovery of the bacteria Helicobacter pylori and its role in gastritis and peptic ulcer disease.25 This is consistent with an earlier study in other medical specialties.26,27 An explanation for this is that an article will eventually be incorporated into common knowledge and no longer be as frequently cited after its highest number of citations peak in a given year. Its relevance may subsequently wane with new data supplanting or augmenting it. Thus, some important articles are lost to time.28 Our study still has some limitations. First, the selection of articles was confined to English journals, which would have failed to capture landmark articles published in other languages. Language barriers are a known bias to citation rate as authors are more likely to cite articles in their own language, and English articles are more likely to be cited overall.29–31 Then, factors potentially influencing citation rates, such as journal and author selfcitations, incomplete citing, and omission bias, were not considered.22 These biases may interfere with the generation of a representative list of landmark articles based on absolute citation rates. In conclusion, we provide a review of landmark papers in the field of digestive diseases. These 100 most cited articles reflect major advances in gastroenterology and hepatology researches and a number of hot topics during the last 60 years. Our study can provide insights into priorities and trends of digestive diseases and could serve as sources for future academic pursuit.

References 1 Cheek J, Garnham B, Quan J. What’s in a number? Issues in providing evidence of impact and quality of research. Qual. Health Res. 2006; 16: 423–5. 2 Garfield E. Citation analysis as a tool in journal evaluation. Science 1972; 178: 471–9. 3 Garfield E. Introducing citation classics: the human side of scientific reports. Curr Contents 1977; 3: 1–2. 4 Ohba N, Nakao K, Isashiki Y et al. The 100 most frequently cited articles in ophthalmology journals. Arch. Ophthalmol. 2007; 125: 952–60. 5 Hennessey K, Afshar K, Macneily AE. The top 100 cited articles in urology. Can Urol Assoc J 2009; 3: 293–302. 6 Tsai YL, Lee CC, Chen SC et al. Top-cited articles in emergency medicine. Am. J. Emerg. Med. 2006; 24: 647–54. 7 Mazhari S. The 100 top-cited articles published in psychiatric journals. J. Psychiatr. Pract. 2013; 19: 327–38. 8 Lefaivre KA, Shadgan B, O’Brien PJ. 100 most cited articles in orthopaedic surgery. Clin. Orthop. Relat. Res. 2011; 469: 1487–97. 9 Rosenberg AL, Tripathi RS, Blum J. The most influential articles in critical care medicine. J. Crit. Care 2010; 25: 157–70.

Top-cited articles in digestive disease

10 Web of Knowledge. ISI Web of Knowledge. 2011. [Accessed on 25 September 2013.] Available from URL: http://apps.webofknowledge. com/ 11 Hurwitz H, Fehrenbacher L, Novotny W et al. Bevacizumab plus irinotecan, fluorouracil, and leucovorin for metastatic colorectal cancer. N. Engl. J. Med. 2004; 350: 2335–42. 12 Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 2003; 3: 521–33 13 Manning AP, Thompson WG, Heaton KW et al. Towards positive diagnosis of the irritable bowel. Br. Med. J. 1978; 2: 653–4. 14 Tanaka Y, Nishida N, Sugiyama M et al. Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat. Genet. 2009; 41: 1105–9 15 Phillips B, Ball C, Sackett D et al. Levels of evidence. Available from URL: http://www.cebm. net/index.aspx?o=1025. Accessed on 1 October 2013. 16 Garfield E. What is a citation classic? Available from URL: http:// classics.html. Accessed on October 5 2013. 17 Jemal A, Bray F, Center MM et al. Global cancer statistics. CA Cancer J. Clin. 2011; 61: 69–90. 18 Shadgan B, Roig M, Hajghanbari B, Reid WD. Top-cited articles in rehabilitation. Arch. Phys. Med. Rehabil. 2010; 91: 806–15. 19 Hui J, Han Z, Geng G et al. The 100 top-cited articles in orthodontics from 1975 to 2011. Angle Orthod. 2013; 83: 491–9. 20 Fardi A, Kodonas K, Gogos C et al. Top-cited articles in endodontic journals. J. Endod. 2011; 37: 1183–90. 21 Campbell FM. National bias: a comparison of citation practices by health professionals. Bull. Med. Libr. Assoc. 1990; 78: 376–82. 22 Lin AM. US and non-US submissions. JAMA 1998; 280: 246–7. 23 Tripathi RS, Blum JM, Papadimos TJ et al. A bibliometric search of citation classics in anesthesiology. BMC Anesthesiol 2011; 11: 24. 24 Marx W, Schier H, Wanitschek M. Citation analysis using online databases: feasibilities and shortcomings. Scientometrics 2001; 52: 59–82. 25 Talley NJ, Richter J. Nobel prize in medicine awarded to a gastroenterologist in 2005.Am. J. Gastroenterol. 2006; 101: 211. 26 Lipsman N, Lozano AM. The most cited works in major depression: the ‘Citation classics’. J. Affect. Disord. 2011; 134: 39–44. 27 Brandt JS, Downing AC, Howard DL, Kofinas JD, Chasen ST. Citation classics in obstetrics and gynecology: the 100 most frequently cited journal articles in the last 50 years. Am. J. Obstet. Gynecol. 2010; 203 e1–7. 28 Aylward BS, Roberts MC, Colombo J, Steele RG: identifying the classics: an examination of articles published in the journal of pediatric psychology from 1976–2006. J. Pediatr. Psychol. 2008; 33: 576–89. 29 Moed HF, van Leeuwen TN. Impact factors can mislead. Nature 1996; 381: 186. 30 Moed HF. The impact-factors debate: the ISI’s use and limits. Nature 2002; 415: 731–2. 31 Ren S, Zu G, Wang HF. Statistics hide impact of non-English journals. Nature 2002; 415: 732.

Supporting Information Additional Supporting Information may be found in the online version of this article at the publisher’s web-site: Table S1 The 100 most cited papers in digestive system disease.

Journal of Gastroenterology and Hepatology 31 (2016) 107–111 © 2015 Journal of Gastroenterology and Hepatology Foundation and Wiley Publishing Asia Pty Ltd


Top-cited articles in digestive system disease from 1950 to 2013.

Examination of top-cited articles is a tool that can help to identify and monitor outstanding scientific researches and landmark papers. We aimed to i...
269KB Sizes 5 Downloads 11 Views