Citation Analysis of the Most Influential Publications in Travel Medicine

Since its origins in the early 1980s, travel medicine has matured into a multidisciplinary specialism which serves the health needs of growing numbers of international travelers. The body of knowledge of the International Society of Travel Medicine has become increasingly complex, and specialty postgraduate training pathways in this discipline have started to emerge.1 Travel medicine is also being incorporated into undergraduate medical curricula in the British Isles.2 Multiple international conferences on travel medicine, including the Conference of the International Society of Travel Medicine and the Northern European Conference on Travel Medicine, enable researchers to showcase their original works in the field. The Journal of Travel Medicine came into existence as the first specialist travel medicine journal in 1994 and is now ranked as 48th of 151 peer-reviewed journals in the category of General Medicine. Travel medicine has embraced the concept of evidence-based clinical practice, and research priorities have been proposed3 which will stimulate further original studies in domains where gaps in the evidence have been identified. Citation analysis is a bibliometric technique which calculates the number of times a published article has been cited as evidence in another publication.4 It has already been used in a variety of specialties, including plastic and reconstructive surgery,5 cardiac surgery,6 emergency medicine,7 and critical care medicine.8 Articles reporting data which is likely to influence the direction of future research in travel medicine may be expected to yield higher citation numbers. Tabulating the citation metrics of articles published in travel medicine http://ijtmgh.com Int J Travel Med Glob Health. 2016 Dec;4(4):122-131 doi 10.21859/ijtmgh-040407 TMGH IInternational Journal of Travel Medicine and Global Health J


Introduction
Since its origins in the early 1980s, travel medicine has matured into a multidisciplinary specialism which serves the health needs of growing numbers of international travelers.The body of knowledge of the International Society of Travel Medicine has become increasingly complex, and specialty postgraduate training pathways in this discipline have started to emerge. 1 Travel medicine is also being incorporated into undergraduate medical curricula in the British Isles. 2 Multiple international conferences on travel medicine, including the Conference of the International Society of Travel Medicine and the Northern European Conference on Travel Medicine, enable researchers to showcase their original works in the field.The Journal of Travel Medicine came into existence as the first specialist travel medicine journal in 1994 and is now ranked as 48th of 151 peer-reviewed journals in the category of General Medicine.Travel medicine has embraced the concept of evidence-based clinical practice, and research priorities have been proposed 3 which will stimulate further original studies in domains where gaps in the evidence have been identified.
Citation analysis is a bibliometric technique which calculates the number of times a published article has been cited as evidence in another publication. 4It has already been used in a variety of specialties, including plastic and reconstructive surgery, 5 cardiac surgery, 6 emergency medicine, 7 and critical care medicine. 8Articles reporting data which is likely to influence the direction of future research in travel medicine may be expected to yield higher citation numbers.Tabulating the citation metrics of articles published in travel medicine for an original research article published in 2013 by Bhatt et al which examined the global distribution and burden of dengue infection using cartographic modeling.The next most cited paper, published in 2006, had just over half as many citations (632) and reported the results from the GeoSentinel Surveillance Network of an analysis of 17 353 ill returned travellers presenting to GeoSentinel sites around the world.Temporal analysis of the top 174 papers showed that the most productive decade for the most cited articles was 2000-2009, and 2006 was the year of publication with the greatest number (17) of top-cited papers.Figure 1    blind randomized controlled clinical trial of 245 patients and concluded that the Lactobacillus GG species may be effective in preventing travelers' diarrhea.Of the 9 leading journals publishing 5 or more of the most cited papers, 2 were devoted exclusively or substantially to travel medicine, 2 to tropical medicine, 3 to general internal medicine and other specialties, 1 to infectious diseases, and 1 to sports and exercise medicine.The journal with the highest impact factor in the current analysis was the New England Journal of Medicine.Categorical analysis demonstrated that 122 of the 174 leading articles were original research articles, 47 were review articles, and 5 belonged to other article categories (1 letter to the editor on the H1N1 influenza virus, 2 conference papers, 1 short survey, and 1 editorial on logarithmic risk scales).Twenty-three papers were related largely to the basic sciences while 152 were principally of a clinical nature.The levels of evidence of the clinical articles mostly belonged to levels 2-5 of the Oxford Centre for Evidence-Based Medicine Levels of Evidence.Randomized controlled clinical trials comprised 5 of the most influential papers and investigated the efficacy of low molecular weight heparin for prevention of travel-related venous thrombosis, rifaximin for prevention of travelers' diarrhea, melatonin for alleviation of jet lag symptoms, acetazolamide for prevention of acute mountain sickness, and a virosomal malaria vaccine.Of the 47 review articles represented in the top 174 papers, 6 were systematic reviews and meta-analyses and addressed travelers' diarrhea (in 3 systematic reviews), hepatitis E, venous thromboembolism in air travel, and rapid diagnostic tests for malaria diagnosis.
By using citation counts as a proxy measure of researcher influence in the field of travel medicine, the top-ranked author was R. Steffen with 15 articles among the most cited (Table 3).The highest ranked author to appear on the list of most cited articles based on the cumulative citation count was J. S. Keystone with 1825 citations (Table 4).Fourteen authors, all highly active in travel medicine practice and research, had at least 5 articles in the top 174 most referenced papers.The United States had 85 of the most cited papers, followed by the United Kingdom with 40 and Switzerland with 32.Sixteen countries produced at least 5 of the most cited  7 presents a thematic analysis of the most cited publications in travel medicine.Nine broad themes characterized the group with at least 5 articles on the most cited publication list; air travel (29), malaria (26), post-travel assessment (16), travelers' diarrhea (14), and high altitude illness (13) were the most prominent subjects.Studies of the knowledge, attitudes, and practices of travelers comprised 6 of the most frequently cited papers.Three airport surveys conducted in 9 major European airports, 2 airports in Zimbabwe, and Johannesburg international airport received a combined total of 373 citations.

Discussion
Citation analysis is a widely endorsed measure of the influence of peer-reviewed articles published in medical literature.This method of evaluating the most influential output at a specialty level has been reported in other areas of medical practice, including pediatrics, 11 orthopedic surgery, 12 plastic surgery, 5 and cardiac surgery. 6This study sought to identify the travel medicine publications that have exerted the greatest academic influence on the discipline by ranking its most cited works.Bibliometric advice established that 50 citations would be a reasonable, though arbitrary, benchmark of influence for travel medicine, given that the first specialized travel medicine journal only came into being 22 years ago.Since then, travel medicine has come of age and its research output has expanded greatly.Faculty of Travel Medicine recommendations for the practice of travel medicine 13 and an extensive body of knowledge 14 guiding continuing medical education in the field have been published.While the Zika virus infection has been the subject of a recent bibliometric analysis, 15 this is the first overall citation analysis regarding travel medicine.
Citation analysis has limitations in evaluating the academic importance of an article. 16There is a temporal lag between publication and citation, with the most recent article being at a disadvantage in this regard.However, it is believed that citation analysis should be performed at reasonable intervals, e.g., 5 years, to provide the most up-to-date view of publication trends.Self-cited articles were not excluded, and citations in textbooks or conference proceedings were not considered to avoid possibly introducing selection bias into the methodology.The recognized tendency for authors to preferentially cite articles in their target journal may also potentially inflate citation numbers for some papers, although the rigor of the external peer review process and editorial oversight exercised by the high quality academic journals featured in this study's citation table provide reassurance about the accuracy of the citation report.A further source of bias in relation to citations in general is the so-called snowball effect' which means that authors are more likely to cite a work because it has been cited in previous publications rather than purely for its scientific content and academic quality.Furthermore, there is an obvious bias toward articles published in English, but the leading journals in the field and in related specialties are all English language publications.Citation analysis also ignores whether a citation is positive or negative.It is widely accepted that, with the passage of time, truly 'classic' papers are gradually cited with less frequency, because they have been consumed by current knowledge in a process of "obliteration by incorporation." 17 The researchers acknowledge that the detailed bibliometric analysis in this study may have excluded a small number of relevant papers which had been incorrectly indexed or the keywords of which were not comprehensive.Since travel medicine has a far reach and overlaps other disciplines, an even wider search strategy may have disclosed additional highly cited articles.This limitation is inherent in every citation analysis.This is the first citation analysis to be conducted in travel medicine, and it highlights the most influential topics in the field.Air travel-related publications featured most prominently among the most cited papers, followed closely by malaria.Both topics affect a large number of international travelers and are fertile fields of research activity.This finding aligns closely with the observation that air travel-related venous thrombosis, jet lag, and prevention and treatment of travelers' diarrhea were among the topics represented by the highest level of scientific evidence in the form of systematic reviews and randomized controlled clinical trials.Analysis of the time course of travel medicine articles with the greatest

What Is Already Known?
Travel medicine has flourished since its origins in the early 1980s into a multidisciplinary discipline which serves the health needs of international travelers.No comprehensive citation analysis of travel medicine-related articles has been published to date.

What This Study Adds?
A total of 174 travel medicine-related articles with at least 50 citations each was found.The most productive decade for these most cited articles was 2000-2010.One hundred twenty-two of the articles were original research articles, and 47 were review articles.The top-ranked author published 15 articles among the most cited.Nine broad themes emerged from the most cited article list, including air travel, malaria, post-travel assessment, travelers' diarrhea, and high altitude illness.
Research Highlights academic impact identified the decade 2000-2009 as the most prolific decade in travel medicine research to date.It is likely that, as travel medicine research output increases over time, the decade of greatest influence will shift to a later time period, making follow-up citation analyses essential.The ease of modern online literature database searches and the migration to a web-based continuous publication platform for leading journals have removed barriers to accessing the most recently published articles in medical literature, a factor which may diminish this long observed time lag in citation metrics.
While the majority of classic travel medicine papers were published in specialized travel medicine and tropical medicine journals, a reasonable proportion of the most cited articles appeared in high impact factor general internal medicine and infectious disease journals.Travel medicine interdigitates with a large number of other specialties, including general practice, internal medicine, public health medicine, infectious diseases, and occupational medicine.While this citation analysis did not specifically examine the citing journals, it does suggest that the discipline of travel medicine is exerting a wide sphere of influence across clinical practice.The high proportion of review articles among the most cited papers is reassuring as it demonstrates the maturity of travel medicine as a field of academic enquiry.These review articles were mostly narrative literature reviews rather than systematic reviews; however, the latter represents a higher form of scientific evidence that takes account of bias in research.That an editorial appeared in the top 174 papers speaks to the capacity of well-written editorial articles to influence academic research.
The geographic distribution of classic papers in travel medicine was weighted towards the United States, United Kingdom, Switzerland, and Germany, where many of the leading institutions and most prolific researchers were also located.Only two Asian countries and not a single Latin American or African country were found in the most cited article list.There may be a less skewed distribution of publications in future citation analyses of travel medicine as regional travel medicine societies such as the Asia Pacific Travel Health Society, 18 South African Society of Travel Medicine, and Latin American Society of Travel Medicine 19 raise the profile of travel medicine research among their members and as research funding becomes available to support such activity.

Conclusion
Using citation analysis as a proxy marker of influence in academic travel medicine, this study offers a perspective on the key publications in this relatively young area of practice.Despite its limitations, citation analysis highlights the countries and institutions of origin of the most seminal travel medicine research output.Furthermore, it provides insights into the direction in which travel medicine has progressed since its origins some 40 years ago.A follow-up bibliometric analysis of travel medicine literature will focus on identifying areas of unmet research need within the field and will confirm future research priorities.
illustrates the total citation number per decade of publication in travel medicine, indicating that the current decade has witnessed the greatest level of citations to date.The most influential articles were published between 1952 and 2013.The oldest article was written by Dick et al and published in 1952 in Transactions of the Royal Society of Tropical Medicine and Hygiene; it described the isolation and serological diagnosis of the Zika virus.The most recently published papers to appear on the most cited list were published in 2013 by Leder et al in the Annals of Internal Medicine and Bhatt et al in Nature and described the findings of a GeoSentinel surveillance of 42 173 ill returned travelers between 2007 and 2011 and the global distribution of dengue infection, respectively.

Figure 1 .
Figure 1.Temporal Trends in the Publication of Most Cited Articles.

Table 2
lists the journals in which the greatest number of influential papers were published.The Journal of Travel Medicine published 41 of the top 174 most cited articles (23.4%).The article with the highest number of citations (235) was published in the Journal of Travel Medicine by Hilton et al in 1997 at the Albert Einstein College of Medicine in New York City, USA.It reported the findings of a double-

Table 2 .
Impact Factor (IF) of Journals Publishing the Most Cited Travel Medicine Papers

Table 3 .
Authors With Five or More Publications in the Top-Cited Articles

Table 4 .
Authors With Largest Cumulative Citation Records in the Top-Cited Articles

Table 5 )
. A total of 160 different institutions were represented in the analysis.The most prolific institution in the most cited article collection was the Ludwig-Maximilians-Universität based in Munich, Germany with 15 contributions (Table6).Nine of the institutions with at least 5 articles among the top 174 papers were affiliated with European academic and clinical institutions.The Centers for Disease Control and Prevention in the United States was the source of 11 of the top-cited papers.Table

Table 5 .
Countries of Origin of the Most Cited Articles

Table 6 .
Institutions Publishing in the Most Cited Articles in Travel Medicine

Table 7 .
Thematic Analysis of Most Frequently Cited Articles