View From Above: Bibliometric and Citation Analysis of Global High Altitude Medicine Research

Adequate pre-travel preparation is required for certain travel destinations due in part to challenging physical environments. These include high altitude destinations, access to which is facilitated in the modern era by improved transport infrastructure such as high altitude airports1 and railway systems.2 Traveling to high altitude destinations presents inherent challenges, including a toll on both physical3 and mental health.4 Much of the published literature focuses on preventive5 and treatment strategies6 for high altitude-related medical issues. The expectations and challenges encountered by workers at high altitude have also received attention from researchers in this field.7 High altitude medicine is a well-established discipline with an evolving scholarship and evidence base. It has close ties with travel medicine and is listed under the special itineraries sub-domain of the Body of Knowledge of the International Society of Travel Medicine (www.istm.org). The continued development of high altitude medicine requires that research priorities reflect its expanding knowledge base. This may be achieved by developing a body of knowledge or syllabus which reflects the current scope of high altitude research and practice. This framework may be beneficial for the professional development of high altitude physicians and researchers and for shaping the content of educational programs8 in high altitude medicine. This has proved to be a successful and worthwhile initiative in other disciplines such as travel medicine.9 http://ijtmgh.com Int J Travel Med Glob Health. 2020 Aug;8(3):107-115 doi 10.34172/ijtmgh.2020.19 TMGH IInternational Journal of Travel Medicine and Global Health J


Introduction
Adequate pre-travel preparation is required for certain travel destinations due in part to challenging physical environments. These include high altitude destinations, access to which is facilitated in the modern era by improved transport infrastructure such as high altitude airports 1 and railway systems. 2 Traveling to high altitude destinations presents inherent challenges, including a toll on both physical 3 and mental health. 4 Much of the published literature focuses on preventive 5 and treatment strategies 6 for high altitude-related medical issues. The expectations and challenges encountered by workers at high altitude have also received attention from researchers in this field. 7 High altitude medicine is a well-established discipline with an evolving scholarship and evidence base. It has close ties with travel medicine and is listed under the special itineraries sub-domain of the Body of Knowledge of the International Society of Travel Medicine (www.istm.org). The continued development of high altitude medicine requires that research priorities reflect its expanding knowledge base. This may be achieved by developing a body of knowledge or syllabus which reflects the current scope of high altitude research and practice. This framework may be beneficial for the professional development of high altitude physicians and researchers and for shaping the content of educational programs 8 in high altitude medicine. This has proved to be a successful and worthwhile initiative in other disciplines such as travel medicine. 9 Bibliometric analysis is an established research methodology which involves a quantitative analysis of the academic literature in order to achieve a specific aim. These include evaluating the contribution and collaboration of authors, institutions, and countries, calculating the number of times a published article has been cited, and identifying gaps in the field that are amenable to further research. 10 Specialty and journal-level bibliometric analyses have also been published in the fields of travel medicine, [11][12][13] tropical medicine, 14 cardiovascular medicine, 15 respiratory medicine, 16 infectious diseases, 17 emergency medicine, 18 surgery, 19 and obstetrics and gynecology. 20 High altitude medicine and biology (HAMB), which has been in existence since the turn of the new millennium, is the only journal devoted exclusively to high altitude medicine research. It is affiliated with the International Society for Mountain Medicine (ISMM), which was founded in 1985 by the medical commission of the International Climbing and Mountaineering Federation (UIAA) in Switzerland. To our knowledge, there has been no bibliometric analysis conducted to date for publications in HAMB. This study is the first journal-level bibliometric analysis of high altitude research articles. It has the additional aim of identifying research trends and gaps in a theoretical body of knowledge through the mapping of articles to specific domains. This may inform the setting of research priorities in this evolving area of clinical activity. By analyzing the characteristics of these publications, the qualities which make a high altitude medicine paper important to the specialty may be elucidated.

Curriculum Mapping Exercise
All indexed articles, including original research articles, reviews, editorials, letters, and case reports, appearing in the 81 issues of HAMB through April 2020, were retrieved from the journal website between February and April 2020. These articles were screened from their titles and abstracts. A theoretical framework was constructed, which yielded a body of knowledge in high altitude medicine. This collective effort involved consultation with experts and leading textbooks in the field, as well as the UIAA Diploma in Mountain Medicine. 21 The framework was divided into a series of domains, against which articles were mapped.
The full text versions of articles were interrogated further when their domain identity was not apparent from their title. Where an individual article reflected more than one domain, it was categorized into each domain. Additional information recorded included title, year of publication, article type, country of origin (corresponding author), institutional affiliations, number of countries and authors involved in individual articles, and the gender of authors.
Abstracts of proceedings or conferences, book reviews, and several miscellaneous article categories such as 'high altitude web' , 'poems' , and 'corrections' were not included in the analysis. Both authors followed the same search protocol independently and agreed upon the final list of articles for analysis. Data were entered and stored in a Microsoft Excel 2019 database. A consensus on final designations of domain allocations for each article was reached by the two authors. Publications were analyzed in Microsoft Excel by article type, annual number of publications, geographical location, authorship, international collaboration, and citation analysis. A temporal analysis of publication trends was also performed to track research productivity over time.

Citation Analysis
Citation counts of articles, as well as authors publishing the most articles in HAMB, were obtained from Scopus, the largest citation database of peer-reviewed literature. 22 To enrich the analysis of citation metrics, data on citations made to HAMB by other citing journals, as well as data on the cited half-life of HAMB, were obtained from Web of Science, Journal Citation Reports (JCR). Cited half-life refers to the median age of the citations received by a journal in a given JCR year.

Collaboration Analysis
Collaboration analysis was performed by examining the degree of collaboration (C), which was derived from the formula C = N m /(N m +N s ), where N m is the number of publications by multiple authors and N s is the number of publications by a single author. 23 Collaboration index (CI) was obtained from the formula CI = number of multiple authors/number of publications by multiple authors. 23 VOSviewer version 1.6.15 (Leiden University, Leiden, The Netherlands), a visualizing software tool, was used to generate bibliometric network maps based on co-authorship and citations of retrieved publications. Under visualization mode, network maps represent different parameters using circles of different size, font size, colors, and connecting line thickness. The thickness of connecting lines indicates the strength of collaboration either between countries or between authors, which is summarized numerically as the total link strength. A stronger collaboration reflects a higher total link strength. 24,25 Descriptive analysis for categorical variables was presented as frequencies and percentages. Continuous data were presented as mean, median and interquartile range (Q1-Q3), and range values.

Publication Trends
The mean number of annual publications in HAMB for the study period was 55 publications. There was an increase in published research productivity over time, from 32 in 2000 to 76 in 2014, with recognizable peaks occurring mainly in the last decade. The maximum productivity per year was observed in 2013 and 2014 with 76 (6.6%) publications each, while the minimum productivity per year was recorded in 2000 (2.8%, n = 32). As of April 1, 2020, published articles had attracted a total of 13 324 citations, with a mean of 11.6 citations per article, a median (Q1-Q3) of 4 (0-15) and a range of 237 (0-237). Table 2 shows the total citation count of all articles published in any given year, from 2000 to 2020. The median number of citations per publication reached a peak in 2010 with 14 and was at its lowest level in 2019 with a median of zero and mean of 0.41 citations.

Geographical Distribution of Publications
The geographical distribution of publications in HAMB spanned 48 countries. The United States had 56 of the most cited papers (i.e., 25 or more citations), followed by Switzerland with 12 and the United Kingdom with 10 ( Table 3). Eleven countries produced at least 5 of the most cited publications. Table 4 displays the leading countries in terms of productivity with a minimum of 25 publications each. The USA was the most productive country with 432 publications (37.6%), followed by the UK (9.5%, n = 109) and Switzerland (5.6%, n = 64). A total of 1031 different academic research institutions were represented in the analysis.     (Table 8). Multi-authored publications had an average of 4.4 authors per publication, which was derived from a calculation of the average annual number of authors per multi-author publication during the study period. The total number of articles with international collaboration, defined as articles that involved at least two countries on a given paper, was 329 (28.6%). The average number of international institutions involved in an individual paper was 1.4. International collaboration was further analyzed based on country of origin using VOSviewer. The USA had the strongest collaboration network, indicated by a total link strength of 158, followed by the UK (total link strength 143) and Switzerland (total link strength 132). Figure 2 and Figure 3 depict the strength of collaboration networks in the published high altitude medicine literature.

Citation Analysis
The total citations per year revealed two temporal peaks:  Table 9 illustrates the top twenty journals that cited HAMB to the greatest extent in the JCR year 2018. The journal, Frontiers in Physiology, contributed the highest number of citations (149) to HAMB, followed by HAMB itself (115) and PLoS One (34). Articles published in HAMB from all years were cited by the journals listed in Table 9.
Of the 1150 articles, the most cited publication was entitled 'Consensus statement on chronic and subacute high altitude diseases' with a cumulative citation count of 237. This was an international consensus statement produced by a committee formed by the ISMM at the VI World Congress on Mountain Medicine and High Altitude Physiology in Xining, China (2004). It provided guidelines on the definition, diagnosis, treatment, and prevention of the most common chronic high altitude diseases. Table 10 summarizes the most cited publications in HAMB. Among the top ten cited publications, eight papers were review articles addressing topics such as high altitude illnesses and adaptation to high altitude hypoxia. The highest number of top cited papers (25 or more citations) was in 2003 (n = 17), followed by 2008 (n = 16).
A total of 2508 (87.5%) authors received at least one citation, 1372 authors accumulated at least ten citations (47.8%), and 93 authors had a citation count of at least 100 (3.2%). The most influential author was the Peruvian physiologist, Fabiola León-Velarde, from Cayetano Heredia University in Lima, with the highest cumulative citation count of 618 (1% of total citation counts for all authors). The average number of citations per author for papers published in HAMB was 22.3. Citation analysis revealed that the USA was the most prolific   country (5650 citations), followed by the UK (1807) and Switzerland (1803).

Discussion
We have completed the first bibliometric and citation analysis of papers published in a leading specialist high altitude medicine journal. This included a detailed analysis of publication trends and measures of research collaboration which chart the growth and trajectory of the journal over the past two decades. Bibliometric analysis allows for the identification of trends, patterns, areas of research neglect and imbalances in academic publishing, which may be variously addressed by editorial board strategies, active solicitation of articles and funded external research grant calls. 12 Based on our experience with a similar tool in travel medicine, 9 we designed a body of knowledge comprising 34 domains, based on a triangulation of information from multiple reputable sources in order to map published articles against individual knowledge areas. This body of knowledge may have multiple applications for workers in the field, including the design of educational courses and webinars and the development of journal editorial strategy. The body of knowledge should be a live document that responds to changing priorities in the field and we believe that it should be updated at regular intervals with a more granular sub-categorization of topics in order to maximize its educational value. Our analysis revealed that the leading topics (domains) in high altitude medicine were altitude acclimatization, cardiovascular physiology, high altitude working environments, acute mountain sickness, and high altitude respiratory physiology. The least represented areas related to renal physiology at altitude, aerospace medicine, environmental issues, and lightning injuries.
The most cited papers tended to be review articles or randomized controlled trials. Systematic reviews constituted a very low proportion of the total number of reviews published and, given that they represent the highest level of research evidence, 26 there may be scope for increasing the proportion of systematic reviews published in the journal. The most cited paper to date has been a consensus statement on the theme  of chronic and subacute mountain sickness. Older papers understandably tended to accumulate a larger number of citations and citations to HAMB papers were received from a diverse array of other academic journals, with the top citing journal in 2018 being a prominent physiology journal.
There were relatively few citations to HAMB articles from travel medicine journals, which is surprising given the close interaction between these disciplines. It may be beneficial  to develop closer links between high altitude medicine and travel medicine, for example in the joint hosting of scientific conferences. This is particularly pertinent given the educational needs of travel medicine clinicians, who are often consulted by international travelers for pre-travel health advice and recommendations for altitude illness chemoprophylaxis. 27 There was a clear geographic dominance in both volume of research output and citations generated, with epicenters identified in Europe and Asia. A quarter of the most productive institutions were based in the USA. Despite the global reach of the ISMM, most countries do not appear to be research active in this field or at least have not yet published in the society journal. While there was a strong gender imbalance towards male authorship, with a 3:1 malefemale ratio, the proportion of female authors has increased steadily over time and this should be actively encouraged. Collaboration between authors and international institutions on high altitude medicine articles has also increased over time, reflecting perhaps the work of the ISMM in promoting activity in high altitude medicine globally. We have recently observed a similar collaboration trend in the emerging discipline of preventive cardiology. 15 The most prolific author in HAMB was the renowned respiratory physiologist, John B. West, who served as editorin-chief of the journal for a large part of its existence (2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015). The total number of articles attributed to this leading academic high altitude scientist may have been inflated by the large number of editorials published in his role as journal editor. The most influential author as measured by cumulative citation counts was also a physiologist, Fabiola Léon-Velarde from Peru. This highlights the close connections between the disciplines of high altitude medicine and physiology. It is possible that other influential leaders in the field published their work in non-specialist journals and may thus not be recognized among the top authors in our citation analysis.
While the current bibliometric analysis reflects activity in this journal since it was founded in 2000, we recommend that a similar bibliometric analysis be performed at ten-yearly intervals, to allow for the effect of any editorial interventions in the interim to be discerned. Our analysis, though comprehensive, is limited in its capacity to truly quantify the full influence of individual authors and papers, given the inherent flaws in the process of citation metrics, including bias that results from excessive self-citation. 28 Our analysis cannot identify with any authority the changing editorial board strategies that may have influenced the article profile of the journal since its inception. The body of knowledge, while derived from multiple reputable sources, cannot be considered to be exhaustive and must also be subject to critical review and revision. Despite its modest impact factor which has declined in recent years, HAMB is regarded as a specialist journal in high altitude medicine with a strong affiliation to the ISMM. It would be of interest, however, to extend the bibliometric analysis to the level of the discipline as a whole, to incorporate articles published in other journals. 11 Travel medicine academic journals, including International Journal of Travel Medicine and Global Health, should issue calls for submission of manuscripts under the high altitude medicine theme, with particular emphasis on exploring the relevance of high altitude physiology and illness to recreational travelers.

Conclusion
We have performed the first comprehensive bibliometric analysis in high altitude medicine and mapped articles against a proposed body of knowledge. Our analysis has identified a broad range of topics published by almost 3000 authors from over 1000 institutions, with a particular focus on acclimatization, cardiovascular physiology, and acute mountain sickness. The USA has a dominant position in terms of institutional output, but most of the leading countries in terms of research volume and impact as measured by citations are based in Europe and Asia. There was a discernible longitudinal trend towards enhanced collaboration between authors from different institutions and countries, reflecting the academic maturation of high altitude medicine as a scholarly discipline. Efforts to increase the research activity in neglected topics and to promote greater collaboration between high altitude medicine and neighboring fields of study such as travel medicine may yield reciprocal benefits. Travel medicine journals should proactively solicit manuscripts from high altitude medicine researchers. Academic journals should not feel threatened by bibliometric analysis, but rather recognize it as a legitimate tool which serves the best interests of their contributors and readers and helps to raise the profile of their discipline.

What Is Already Known?
High altitude travel is a popular activity but one that carries attendant health risks, including high altitude illness and traumatic injuries. High altitude medicine is a relatively new scientific discipline but its evidence base is growing.

What This Study Adds?
We have developed the first theoretical body of knowledge in high altitude medicine and performed the first bibliometric analysis in the field. Interesting publication trends have emerged. Efforts to promote greater collaboration between high altitude medicine and related fields of study such as travel medicine should be encouraged. Travel medicine journals should actively solicit manuscripts which relate to high altitude travel risks and their mitigation.