Ten years of ranavirus research (2010–2019): an analysis of global research trends

There are 545 publications in the WOS ranavirus data set published between 2010 and 2019 (average per year = 58.2, SD = 15.2), with a significantly increasing number of publications per year from 41 in 2010 to 86 in 2019 (R = 0.87, p < 0.001; Fig. 1). The greatest number of ranavirus publications between 2010 and 2019 came from the United States (US) and People’s Republic of China (PRC) who had 199 and 153 total publications, respectively, together accounting for more than 60% of ranavirus-related publications in that time period (Table 1). Out of all the countries with more than five publications in the WOS ranavirus data set, the US and PRC are the only countries with a strong increase in publication output (Fig. 2). Publications in the WOS ranaviurs data set between 2010 and 2019 were cited a total of 6830 times with publications from 2010 having the highest collective citation total (1330) compared with any other year (Fig. 3). On average, over the last 10 years, each ranavirus-related publication has been cited 12.5 times (SD = 18.4, median = 7).

The H-index across all publications in the WOS ranavirus data set was 37. Ranavirus-related publications in the WOS ranavirus data set can be divided into top core (Table 2) and auxiliary (Table 3) publications. The top core ranavirus publications are highly cited by other ranavirus-related publications in the WOS data set. The ranavirus publication with the highest number of internal citations (i.e., citations from other publications in the WOS ranavirus data set) is Miller et al. (2011, Table 2). The top 10 core publication list contains several reviews (e.g., Whittington et al. 2010; Chinchar et al. 2011; Miller et al. 2011) that, because of their impact, may be a useful starting resource for those interested in ranavirology. The top auxiliary publications are cited by publications from outside the WOS ranavirus data set. The top auxiliary publication was Hayes et al. (2010) with a total of 176 citations in the WOS core collection.

Interestingly, Fish & Shellfish Immunology was the top journal publishing ranavirus-related research from 2010 to 2019, with over 50 ranavirus publications in the WOS ranavirus data set (Table 4). Diseases of Aquatic Organisms (DAO) had the highest number of citations (572) while the Journal of Virology had the highest average number of citations per ranavirus-related publication (30.0) within the top 10 journals. PLoS ONE and DAO both had an H-index of 14 (i.e., 14 ranavirus publications with at least 14 citations).

There are many common keywords (n = 265) used in publications of the WOS ranavirus data set (Fig. 4). These keywords cluster into five groups that relate to core concepts in the field between 2010 and 2019 (Fig. 4): ecology, emerging disease, amphibians (Group 1); immunology, evolution (group 2); virology, molecular biology (group 3); genetics, ichthyology (group 4); and reptiles (group 5).

It is not surprising that “ranavirus” is the most common key word used by authors in the publications in the WOS ranavirus data set. However, this is not to say the research interest in this field is static (Fig. 5). Areas of research (author keywords) with high median year of publication include biosecurity, antiviral immunity, reptiles, etc. (Fig. 5). Interests in various infectious agents are changing as new species or strains of viruses get discovered. For instance, the median year of publication of publications from 2010 to 2019 that use Epizootic hematopoietic necrosis virus (discovered in the 1980s) as an author keyword was 2011, while the median year of publication for Andrias davidianus ranavirus (discovered in 2011) was mid 2018. From 2010 to 2019 over 50 articles have used keywords relating to Singapore grouper iridovirus (SGIV) indicating that SGIV is an important and stable research topic. Interestingly, Batrachochytrium dendrobatidis (Bd), another important pathogen of amphibians has appeared less frequently as an author keyword in the ranavirus literature in recent years (Fig. 5).

Ranavirus research from 2010 to 2019 has been a global effort with authors in the WOS ranavirus data set hailing from 48 different countries and an increasing number of co-authors every year (average = 5.8; R = 0.90, p < 0.001; Fig. 6). Using co-author analysis, it was possible to visualise the collaborative landscape of the ranavirus field (Fig. 7). Central nodes like the US and England have more international collaborators, whereas peripheral nodes (e.g., Hungary, Thailand, Finland) have a less diverse set of co-authors (Fig. 7A). Interestingly, there are relatively few co-authorships shared between European (green) and Asian countries (red; Fig. 7A). There is a positive correlation between the distance between countries on the co-author map and the actual geographical distance between the countries (R = 0.338, p = 0.005). For the most part, bibliographic coupling (Fig. 7B) is similar to the co-authorship map, suggesting that researchers with similar interests are actively collaborating and refer to the same articles. However, there are a few cases where research interest and co-authorship are less aligned. For example, Germany clusters with the US, PRC, Australia, Canada, etc. (red group) in the bibliographic coupling map (Fig. 7B) but does not cluster with the same group in the co-authorship map (Fig. 7A). This may indicate that researchers from Germany are citing similar publications to those in the red group, and thus working on similar topics, but are not necessarily working with the researchers behind the publications they cite.

Fish & Shellfish Immunology has 51 publications from 2010 to 2019, equating to 9.3% of the total publications in the WOS ranavirus data set. This journal is a specialised immunology journal and its place among the top ranavirus journals indicates the central role of immunology in this field. However, DAO received the most citations (572) during the same period but only represented 8.3% of the total citations for the data set. DAO was originally established in 1985 and focuses on all forms of life—animals, plants, and microorganisms—in marine, limnetic, and brackish habitats making it an excellent fit for ranavirus research that often involves aquatic species. PLoS ONE has the same H-index as DAO (14) for publications in the WOS ranavirus data set, and a total of 26 publications from 2010 to 2019. Although DAO has more publications (44), PLoS ONE has published higher impact papers (in terms of average citations). PLoS ONE is an interdisciplinary, open access journal that was founded in 2015 and despite its relatively recent creation, it is still one of the top journals for ranavirus research. The presence of these three top journals demonstrate the breadth of ranavirus research undertaken. Overall, ranavirus research is published in a range journals, with different specialisations and impacts. There is no clear “ranavirus journal” regardless of the metric used i.e., most citations, most publications, or H-index. The variety of journals publishing ranavirus papers may be a reflection of the variety of research that occurs within the field.

The field of ranavirology is diverse, and there is active research in many areas. Core to ranavirology is the investigation of amphibian population declines and emerging infectious disease; however, other areas of research (molecular biology, genetics, herpetology, ichthyology, etc.) are also well represented. We also observed a cluster of keywords related to reptiles in the keyword map, indicating an increasing interest in viral infections associated with this clade (Wirth et al. 2018). In fact, three of the 10 publications in this special collection of FACETS are related to ranaviral infection in reptiles.

Between 2010 and 2019, topics of interest in the ranavirus field have been evolving. For instance, changes in the interest for particular viral isolates may be an indication of ecological importance of these viruses (i.e., those causing current epizootics) or simply a reflection of what is new. Interest in SGIV appears to be stable and this is likely the result of increased research output of researchers from Asia in the past 10 years, where SGIV is used as a model system for studying iridoviruses and remains a continuing problem for aquaculture in that part of the world (Qin et al. 2001; Ma et al. 2016). Interestingly, Bd has been used less frequently as a keyword in the WOS ranavirus data set in recent years. While often combined in early investigations of amphibian population declines, research on these pathogens is now established and ranaviruses and Bd are recognised as separate issues in their own rights.

Bibliographic maps are useful for understanding a scientific landscape. The US, PRC, England, Canada, and Australia were the top countries in terms of total number publications between 2010 and 2019. The US has been the centre of ranavirology since the field originated there in 1965 with the discovery of Frog virus 3 (FV3) (Granoff et al. 1965) and is thus central in the bibliographic maps for collaboration and shared citations, indicating that researchers from the US are working on and collaborating on a diverse set of ranaviral related questions. The US has also hosted three of the five International Research Symposia (IRS) since 2011. Owing to their central location, researchers from this country should thus play a major role in fostering collaborations between some of the more disparate ranavirus researchers. By contrast, the PRC, despite being the second highest country in terms of research output, has not had the opportunity to host an International Symposium on Ranaviruses (ISR). The PRC is also less central in terms of the collaboration map when compared with the US and may thus benefit from an international symposium in terms of increased collaboration. We also noted a positive correlation between collaborating countries and their geographical distance. Reduced physical distance between collaborators would certainly lower the effort required for collaboration and it is also possible that researchers are working on geographically defined issues (where international collaboration is not required). However, there are cases where geographically close countries are not collaborating as much as they could (i.e., Australia and Asian countries). Since Ranaviruses are global pathogens, we recommend that some topics (e.g., phylogenetics, biosecurity, epidemiology, etc.) can or should ultimately be addressed on a global scale, requiring global collaboration.

This scientometric analysis was based solely on the core collection of the WOS database. Although this feature-rich database is a standard for bibliometrics analysis, it is not exhaustive and some ranavirus-related references have been excluded (nonpeer-reviewed material for example). In addition, only the term “ranavirus” was used as a search term to generate the data set used in this study. We recognise that results may vary when using other databases (e.g., Scopus and Google Scholar) or alternative search terms. However, we chose to limit our search terms to reduce the number of false positives in the data set, and using a single database provided us with a consistent data set. We use citations as a proxy for impact and while this is a useful metric, we acknowledge that there are biases when using citation metrics and newer publications may not be favoured (Seglen 1997). Thus, all the conclusions presented here should be interpreted within the context of the limitations defined above.