Citation classics: the 50 most cited articles in surgery in Asia
Department of Surgical Disciplines, All India Institute of Medical Sciences (AIIMS), New Delhi, India
Objective: The term ‘citation classics’ is used for highly cited papers in the scientific literature. It was aimed to understand the current landscape of academic surgery and the quality of the scientific contribution of authors belonging to Asia using citation classics.
Material and Methods: We searched the WoS core collection database under the category ‘surgery’ to include the 50 most cited articles whose lead author was affiliated to an Asian country during the research period. We noted the following characteristics for each article: total citations, average cita- tions per year, year of publication, publishing journal, institution and country, journal quartile and impact factor, authorship, field of surgical research. Results were analyzed using IBM SPSS Statistics v26.
Results: The number of citations ranged from 447 to 1170 (mean +/- SD is 616.9 +/- 150.16) and citations per year ranged from 10.04 to 98.17 (mean +/- SD is 30.87 +/- 17.27). Most productive decade was 1991-2000 (n= 19 articles). Majority of the articles were published in ‘Annals of Surgery’ (28%). Four authors contributed two or more articles as lead author with ‘Poon RTP’ taking the lead. Japan’s contribution was highest (60%) followed by China and its dependents’ (26%). University of Hong Kong was the leading institution (n= 7). Observational study was the most commonly used design (n= 24). Most papers belonged to gastrointestinal surgery (n= 28) and surgical oncology (n= 26). 66% articles originated from a single institution, 22% had inter-institutional collaboration and 12% had national collaboration from countries outside Asia.
Conclusion: The study identified the most influential papers in surgery from Asia. This should provoke interest in academic surgery and research col- laboration with other nations in Asia and the rest of the world.
Keywords: Citation classics, citations, bibliometrics, surgery, Asia
Asia harbors 60% of the world’s population and carries a substantial burden for surgically treatable disorders (1). Moreover, the distribution of currently available surgical services is inequitable. A good way to approach this problem is to understand the current situation of academic surgery in Asia.
The term ‘citation classics’ was coined by Garfield who used the term for highly cited papers in the Web of Science (WoS) database (2). Bibliometric study using citation counts is an important tool to measure scientific impact and/or significance of the published literature from an individual or a region (3,4). Citation classics help in understanding the current research status and serve as a guide for future direction in a field. They can also estimate the quality of research output from a region, which can influence decisions regarding the allocation of funds and research priorities (5).
Previous reviews have looked at citation classics in different surgical specialties such as general surgery (6), plastic surgery (7,8), gastrointestinal surgery (9), neurosurgery (5), orthopedic surgery (4) et cetera. However, there has been no previous report of citation classics in surgery originating from Asia. It was aimed to understand the current landscape of academic surgery and the quality of the scientific contribution of authors belonging to Asia using citation classics determined through the Web of Science core collection database.
Material and Methods
Our study was based on the Science Citation Index Expanded (SCI-EXPANDED) database of the Clarivate Analytics (formerly known as the Thomson Reuters and the Institute for Scientific Information) Web of Science (WOS) Core Collection database. According to the Journal Citation Reports (JCR) of 2019 (InCites Journal Citation Reports dataset updated June 20th, 2019), it indexes 11,877 journals with citation references across 236 disciplines. Search conducted in May, 2020 revealed a total of 1,911,690 documents in the WOS category of ‘surgery’. This search was further refined by countries to include at least one author from Asian countries and their dependencies: Afghanistan, Armenia, Azerbaijan, Bahrain, Bangladesh, Bhutan, Brunei, Cambodia, China, Cyprus, Georgia, India, Indonesia, Iran, Iraq, Israel, Japan, Jordan, Kazakhstan, Kuwait, Kyrgyzstan, Laos, Lebanon, Malaysia, Maldives, Mongolia, Myanmar, Nepal, North Korea, Oman, Pakistan, Philippines, Qatar, Saudi Arabia, Singapore, South Korea, Sri Lanka, State of Palestine, Syria, Tajikistan, Thailand, Timor-Leste, Turkey, Turkmenistan, United Arab Emirates, Uzbekistan, Vietnam, Yemen, Taiwan, Hong Kong, Macao revealing a total of 349,326 documents. Search results were then arranged in descending order of the total number of citations received from WOS core collection.
These results were manually searched by the author to include only those publications whose lead author was affiliated to one of these Asian countries during the period of research. Results related to dental surgery were excluded. We selected the top 50 most cited papers which satisfied the above criteria. We searched the PubMed or Google Scholar database to obtain the full texts/abstracts of these articles. For each article, we extracted the following characteristics: article title, total number of citations in WoS core collection, average citations per year, year of publication, publishing journal, publishing institution, publishing country, journal quartile, journal impact factor (IF), authorship, area of surgical research and type of research. We inserted all data for each included article into a spreadsheet software and used descriptive statistics to quantitatively describe the features of the sample using IBM SPSS Statistics v26.
Our analysis of the citation classics of surgical research originating from Asia revealed the following findings.
Citation and Timeline Characteristics
The list of top 50 articles is provided in Table 1. The number of citations ranged from 447 to 1170 (mean +/- SD was 616.9 +/- 150.16). Eight papers were cited more than 800 times. The average number of citations per year ranged from 10.04 to 98.17 (mean +/- SD was 30.87 +/- 17.27). The paper published by Shigeyuki et al. (10) received the highest number of total citations (1170 times). It was entitled, “Mesenchymal Cell-based Repair of Large, Full-thickness Defects of Articular-cartilage.” published in 1994. This basic science study attempted to repair articular cartilage defects using osteochondral progenitor cells in rabbits. This is the only paper in the list which has been cited >1000 times. The paper ranked lowest in this list (cited 447 times) was, “Intrahepatic recurrence after curative resection of hepatocellular carcinoma – Long-term results of treatment and prognostic factors” published in 1999 (11).
All papers in the list were published between 1976 to 2015. Figure 1 depicts this timeline trend. Highest number of articles were published in 1991-2000 decade (n= 19 articles) followed by the 2001-2010 decade (n= 15 articles). The most productive decade for citation classics has been variable in medical literature (1980s in Hand surgery (12), 1990s in Aesthetic surgery, Neurosurgery and Otolaryngology (5,7,13), 2000s in Ophthalmology and GI surgery (9,14) et cetera. In the list of 35 most cited articles in surgery published by Long et al., the most productive decade was 1970 (15). Since citations take time to accumulate, it is expected that even the ‘landmark’ papers recently published will not be able to make it into this list. According to Garfield et al. even older papers are cited less often as they become ‘common concept’ over time. This is termed as Obliteration by incorporation (2). Thus, when we looked at the number of citations per year, it produced significant shifts in rank when compared to the rank based on the total number of citations (mean absolute rank change 14.44 ± 10.07; range -33 to +32). The paper with the highest number of average annual citations among the top 50 list was produced by Wakabayashi et al. (16) This was a consensus statement on laparoscopic liver resection.
Journals and Authors
Journals publishing top 50 cited papers are listed in Table 2. These include a total of 25 journals. Largest number of top-cited papers were published by ‘Annals of Surgery’ (n= 14 articles) followed by ‘Journal of Bone and Joint Surgery-American Volume’ (n= 4 articles). Impact factors of these journals varied from 1.29 to 10.13 according to JCR 2019. Most of these journals belong to the 1. quartile in surgery and related sub-specialties. Six journals belong to the 2. quartile and two journals ‘ActaNeurochirurgica’ and ‘Aesthetic Plastic Surgery’ belong to the 3. quartile. Top cited articles are more likely to be published in journals of high impact. This in turn increases the impact factor of these journals (17). On the other hand, landmark papers, even if published in journals with low impact, could be highly cited if they are considered important in the field. Most of the journals in our list have an origin in the US or UK. There is a reluctance of highly cited authors to publish papers in native journals as many of them are not included in major bibliographic databases.
Four authors contributed two or more articles as a lead author. The list was led by Poon RTP who contributed to four articles as a lead author. This was followed by Makuuchi T (n= 3 articles), Naruke, T and Kitano S (n= 2 articles each).
Countries and Institutions
A total of six countries in Asia contributed these top 50 papers (Figure 2). Japan’s contribution was the highest (60% of total papers) followed by China and its dependent’s Taiwan and Hong Kong (26% of total papers). Next in line were Singapore and South Korea (4% each) and India, Israel and Lebanon (2% each). The institutions producing three or more papers are enlisted in Table 3. University of Hong Kong produced the highest number of articles (n= 7) followed by National Cancer Center Hospital in Japan (n= 6) and University of Tokyo in Japan (n= 3). The remaining institutions produced one article each. These findings are similar to citation classics in other specialties where the top-cited papers are concentrated in a few institutions and countries (5,7,8,12,14). The US predominates in the world’s quality research output (18,19). The reason for this has been attributed to large research funding and diverse scientific community and also in part due to bias of American authors and reviewers towards the articles published locally which falsely amplifies citation counts (20,21). It has also been found that even among top journals, papers published by high-income countries are more frequently cited than low and middle-income countries (22).
Japan and China are the main contributors to classical surgical research output from Asia. This is also observed for other medical disciplines such as Ophthalmology (14), Orthopaedics (23,24) and Transplantation (25). This could be largely attributed to their better research and development expenditure compared to other Asian countries and their focus on basic science research lately. Favorable national policies in Japan for healthcare research and high productivity of human resources have contributed to its success in academic surgery across the globe (26). However, none of the papers in the list were able to make it to the list of the top 35 cited papers in surgery by Long et al. (15). This could be due to a few reasons. First, studies have shown a strong positive correlation between GDP and number of publications (25,27). While the US spends 17% of its GDP on healthcare, Japan and China spend 11 and 5% respectively according to the World Bank (28). This amounted to 120 billion dollars spent on biomedical research by the US alone compared to only 62 billion dollars spent in Asia in 2012 (29). However, the amount of GDP spent on healthcare research has grown significantly in the last two decades in some of the Asian countries (29,30). The effect of this measure is beginning to be seen. Second, English is being used for the majority of scientific publications and bibliometric search engines. This becomes a problem particularly for Asian non-native English-speaking countries such as China where most of the papers are published in Chinese. Besides, papers written in English from these countries take more time to publish and incur higher costs due to language editing services. This could deter young academic surgeons from publishing in these journals. Third, lack of comprehensive national healthcare databases in many low and middle-income countries in Asia(1) do not encourage research for endemic surgically treatable diseases in Asia.
Type of Research and Surgical Field
A total of seven different study designs/research types were included in the top 50 list (Figure 3). Observational study was the most commonly used design (n= 24). Three papers reported interventional studies (randomized trials). The predominance of observational studies have been observed in other surgical disciplines’ classics as well including aesthetic surgery (7), Urogynaecology (31) and eye surgery (14). The reason for such observation could be due to their role in hypothesis testing (14) and ethical concerns with interventional studies. Of note, only 4 review articles were present in our list contrary to the expectation since reviews are more likely to be cited by authors (32).
The most common studied topics was gastrointestinal (GI) surgery (n= 28) and surgical oncology (n= 26) (Figure 4). GI surgery and GI cancer remain the most studied topics even among top cited surgical and gastroenterology literature in the world respectively (6,33). This is not surprising, since the incidence of gastrointestinal cancer is highest in Asia (34) and it is the fifth most frequently diagnosed cancer worldwide (35). Japan has been a pioneer in the development of GI surgery. The concept of Billroth gastrectomy, extended lymphadenectomy and lymph node metastasis in gastric cancer and right hepatectomy for hepatocellular carcinoma were all developed in Japan (36).
Thirty-three articles (66%) in this list originated from a single institution, 11 (22%) had inter-institutional collaboration and 6 (12%) had national collaboration from countries outside Asia. None of the articles in this list had solely intra continental collaboration. These numbers are similar when compared to citation classics from surgery and its subspecialties around the world (6,8,15). It is widely accepted that international collaboration in surgical research can facilitate the conduction of research studies and improve the generalizability and applicability of the results (37). Asian countries should look at strengthening international research cooperation particularly with low and middle-income Asian countries to establish global standards for surgically treatable diseases.
There are limitations to this research. First, we used the WoS database to determine citation classics but excluded PubMed and Scopus, where the results may vary. Second, we did not correct for self-citations. However, self-citations have been shown to account for only <1% of total citations among top-cited papers (38). In addition, biases such as journal bias and omission bias exist in this type of study which may exclude deserving articles. Third, citation classics exclude recently published landmark papers as accumulation of citations takes time, so the results may vary over time. Despite these limitations, we believe this analysis gives a fair idea about the history and landscape of Academic surgery in Asia.
Citation classics remain the best way of looking at the most influential papers in the field of surgery. This paper highlights some of the most important contributions from the academic surgeons of Asia to the world. It offers an insight into the development of surgical specialty in Asia over time. This list should help early career surgeons for classical reading and experts in the field for having working knowledge of seminal contributions. In addition, this list should provoke interest in academic surgery and research collaboration with other nations in Asia and the rest of the world.
Ethics committee approval is not required for this study.
Concept - V.A.; Design - V.A.; Supervision - V.A.; Materials - V.A.; Data Collection and/or Processing - V.A.; Analysis and/or Interpratation - V.A.; Literature Review - V.A.; Writing Manuscript - V.A.; Critical Reviews - V.A.
The authors declare that they have no conflict of interest.
The authors declared that this study has received no financial support.
- Nagral S, Hussain M, Nayeem SA, Dias R, Enam SA, Nundy S. Unmet need for surgery in South Asia. BMJ 2017; 357: j1423.
- Garfield E. 100 citation classics from the Journal of the American Medical Association. JAMA 1987; 257(1): 52-9.
- Loonen MPJ, Hage JJ, Kon M. Value of citation numbers and impact factors for analysis of plastic surgery research. Plast Reconstr Surg 2007; 120(7): 2082-91; discussion 2092-4.
- Li Y, Xu G, Long X, Ho YS. A bibliometric analysis of classic publications in web of science category of orthopedics. J Orthop Surg Res 2019; 14(1): 227.
- Lipsman N, Lozano AM. Measuring impact in stereotactic and functional neurosurgery: an analysis of the top 100 most highly cited works and the citation classics in the field. Stereotact Funct Neurosurg 2012; 90(3): 201-9.
- Paladugu R, Schein M, Gardezi S, Wise L. One hundred citation classics in general surgical journals. World J Surg 2002; 26(9): 1099-105.
- Joyce CW, Joyce KM, Kelly JC, Kelly JL, Carroll SM, Sugrue C. An analysis of the “classic” papers in aesthetic surgery. Aesthetic Plast Surg 2015; 39(1): 8-16.
- Loonen MPJ, Hage JJ, Kon M. Plastic Surgery classics: characteristics of 50 top-cited articles in four plastic surgery journals since 1946: Plast Reconstr Surg 2008; 121(5): 320e-7e.
- Ahmad Suhaib JS, Ahmed A, Exadaktylos A, McWhinnie D, Nickel F, Hakky S, et al. Systematic review on citation classics in minimally invasive gastrointestinal surgery. J Minimal Access Surg 2018; 14(4): 265.
- Wakitani S, Goto T, Pineda S, Young R, Mansour J, Caplan A, et al. Mesenchymal cell-based repair of large, full-thickness defects of articular-cartilage. J Bone Joint Surg Am 1994; 76(4): 579-92.
- Poon RTP, Fan ST, Lo CM, Liu CL, Wong J. Intrahepatic recurrence after curative resection of hepatocellular carcinoma-long-term results of treatment and prognostic factors. Ann Surg 1999; 229(2): 216-22.
- Joyce CW, Kelly JC, Carroll SM. The 100 top-cited classic papers in hand surgery. J Plast Surg Hand Surg 2014; 48(4): 227-33.
- Coelho DH, Edelmayer LW, Fenton JE. A century of citation classics in otolaryngology-head and neck surgery journals revisited. Laryngoscope 2014; 124(6): 1358-62.
- Koh BMQR, Banu R, Sabanayagam C. The 100 most cited articles in ophthalmology in Asia. Asia Pac J Ophthalmol (Phila) 2020; 9(5): 379-97.
- Long X, Huang J-Z, Ho Y-S. A historical review of classic articles in surgery field. Am J Surg 2014; 208(5): 841-9.
- Wakabayashi G, Cherqui D, Geller DA, Buell JE, Kaneko H, Han HS, et al. Recommendations for laparoscopic liver resection a report from the Second International Consensus Conference held in Morioka. Ann Surg 2015; 261(4): 619-29.
- Schein M, Fingerhut A. Where can surgeons publish? Br J Surg 2000; 87(3): 261-4.
- Soteriades ES, Falagas ME. Comparison of amount of biomedical research originating from the European Union and the United States. BMJ 2005; 331(7510): 192-4.
- Soteriades ES, Rosmarakis ES, Paraschakis K, Falagas ME. Research contribution of different world regions in the top 50 biomedical journals (1995-2002). FASEB J 2006; 20(1): 29-34.
- Campbell FM. National bias: a comparison of citation practices by health professionals. Bull Med Libr Assoc 1990; 78(4): 376-82.
- Link AM. US and non-US submissions: an analysis of reviewer bias. JAMA 1998; 280(3): 246-7.
- Akre O, Barone-Adesi F, Pettersson A, Pearce N, Merletti F, Richiardi L. Differences in citation rates by country of origin for papers published in top-ranked medical journals: do they reflect inequalities in access to publication? J Epidemiol Community Health 2011; 65(2): 119-23.
- Lao L, Daubs MD, Phan KH, Wang JC. Comparative study of scientific publications in orthopedics journals originating from USA, Japan and China (2000-2012). Acta Cir Bras 2013; 28(11): 800-6.
- Xie Y, Wang J, Wang L, Zhu Y, Lei L, Wan T, et al. Research trends in osteoporosis in Asian countries and regions in the last 20 years. Arch Osteoporos 2020; 15(1): 130.
- Pu QH, Lyu QJ, Su HY. Bibliometric analysis of scientific publications in transplantation journals from Mainland China, Japan, South Korea and Taiwan between 2006 and 2015. BMJ Open 2016; 6(8): e011623.
- Bean JR. National healthcare spending in the U.S. and Japan: national economic policy and implications for neurosurgery. Neurol Med Chir (Tokyo) 2005; 45(1): 18-24.
- Oelrich B, Peters R, Jung K. A bibliometric evaluation of publications in urological journals among European Union countries between 2000-2005. Eur Urol 2007; 52(4): 1238-48.
- The World Bank. Current health expenditure (% of GDP) | Data. Available from: https://data.worldbank.org/indicator/SH.XPD.CHEX.GD.ZS?most_recent_value_desc=false (Accessed date: 05.11.2020).
- Chakma J, Sun GH, Steinberg JD, Sammut SM, Jagsi R. Asia’s Ascent — Global trends in biomedical R&D expenditures. N Engl J Med 2014; 370(1): 3-6.
- Fu H-Z, Ho Y-S. Independent research of China in Science Citation Index Expanded during 1980-2011. J Informetr 2013; 7(1): 210-22.
- Gupta A, Kennedy B, Meriwether KV, Francis SL, Cardenas-Trowers O, Stewart JR. Citation classics: the 100 most cited articles in Urogynecology. Int Urogynecology J 2020; 31(2): 249-66.
- Seglen PO. Why the impact factor of journals should not be used for evaluating research. BMJ 1997; 314(7079): 498-502.
- Yuan F, Cai J, Liu B, Tang X. Bibliometric analysis of 100 top-cited articles in gastric disease. Bio Med Res Int 2020; 2020: 1-8.
- Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68(6): 394-424.
- Zhang CD, Yamashita H, Seto Y. Gastric cancer surgery: historical background and perspective in Western countries versus Japan. Ann Transl Med 2019; 7(18): 493.
- Colvin H, Mizushima T, Eguchi H, Takiguchi S, Doki Y, Mori M. Gastroenterological surgery in Japan: the past, the present and the future. Ann Gastroenterol Surg 2017; 1(1): 5-10.
- Søreide K, Alderson D, Bergenfelz A, Beynon J, Connor S, Deckelbaum DL, et al. Strategies to improve clinical research in surgery through international collaboration. Lancet 2013; 382(9898): 1140–51.
- Luo P, Xu D, Wu J, Chen YH, Pfeifer R, Pape HC. The top 100 cited of injury-international journal of the care of the injured: a bibliometric analysis. Injury 2017; 48(12): 2625-33.