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Research Note
Revised

Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite

[version 2; peer review: 2 approved, 1 not approved]
PUBLISHED 18 Jul 2019
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This article is included in the Emerging Diseases and Outbreaks gateway.

Abstract

Given the emergence and reemergence of tick-borne diseases, here we assessed the publishing patterns of research focused on Babesia. We also discuss the implications for the articles published in the last decade, and how more clinical and epidemiological information concerning Babesia is still required. The findings of this article would be useful to define research priorities about Babesia and diagnose the important of scientific production on this pathogen.

Keywords

Babesia, tick-borne disease, epidemiology, public health, bibliometric

Revised Amendments from Version 1

In this new version, we have significantly increased the results and discussion about it. We added more analyses and figures in order to answer the suggestions of the reviewers. From this, it is revealed that in places where babesiosis is under surveillance, research has been increasing.

See the authors' detailed response to the review by Jeremy S. Gray
See the authors' detailed response to the review by Cristina Casalone
See the authors' detailed response to the review by Stalin Vilcarromero

Introduction

Babesiosis is a zoonotic disease with a global distribution; it is mainly transmitted by ticks from different genera (e.g. Rhipicephalus spp., Dermacentor spp., and Ixodes spp.) and diverse species1. It is caused by infection of the erythrocytes of mammals by Babesia species, which are Apicomplexa protozoa of the suborder Piroplasmmiidea and the family Babesiidae2. The vector role of ticks for these parasites was discovered by Smith and Kilbourne in 1893, who were the first to demonstrate its transmission3. The first human case was described by Skaraballo and occurred in 1957 in Zagreb, Croatia4. As a zoonotic disease, animal reservoirs and their distribution contribute, as the presence of vectors, in the maintenance of the transmission cycle and the risk of transmission to humans.

Human babesiosis is not under surveillance and notification in most countries, including those with autochthonous incidence vector-borne diseases. However, studies show that their vectors are widely distributed in tropical and subtropical areas3. Research is fundamental to better understanding this disease. The relevance of bibliometric evaluations on emerging and reemerging disease has been previously described57 as they can contribute in the understanding on how the global scientific and health communities respond to outbreaks8. Herein, our objective was to use bibliometric approaches to analyze Babesia research.

Methods

A bibliometric evaluation was performed focusing on Babesia scientific bibliography. Six main databases were used for retrieving information: Science Citation Index Expanded (SCI-E – Web of Knowledge), Scopus, Medline, LILACS, SciELO and Google Scholar.

For the search pipeline we used the following combination of keywords (MeSH, Medical Subject Headings): “Babesia” AND “Latin America”, “Babesia” AND “Argentina”, “ Babesia” AND “Colombia”, and this strategy was maintained including the name of each country as a keyword. We searched for the 233 countries of the UN list. Also, “Babesiosis” was used as a substitute of Babesia to increase the number of results. Regarding the type of publications, we decided to include original papers, review articles, case reports and editorials, which were further stratified according to publication year and the name and institution to which the main author was affiliated at the time of publishing. This analysis included results obtained up to December 1, 2018.

Data summaries for quantitative variables (number of articles, articles per country, articles per year or periods, citations and H index) were expressed as means and interquartile ranges (IQRs), and for qualitative variables, proportions are reported.

Results

Overall, 78,137 Babesia-associated items resulted from the initial screening of publications. From Google Scholar 62,100 articles (25% USA, 24.9% South Africa, 18.5% Japan) were recovered, followed by Scopus, with 6,272 articles (25.4% from USA, 8.5% Japan, 7.2% UK), and Medline with 5.045 articles (13.7% USA, 10.1% Japan and 5.2% China) (Table 1). From Web of Science, 4,330 publications were retrieved (28.06% from USA, 11.4% Japan and 7.37% Brazil), followed by LILACS with 202 articles (29.2% Brazil, 2.4% Mexico, 1.9% USA) and SciELO with 188 articles (26.6% Brazil, 3.1% Mexico) (Table 1). Considering the Medline database, the number of research articles on Babesia increased above 100 publications per year only after 2004 (Figure 1).

Table 1. The 20 countries with the highest number of scientific articles on Babesia research that are available in Web of Science, Scopus and Medline.

RankCountryNumber
of articles
Database with highest
number of articles
Population in 2018Number of articles per
10 million inhabitants
1United States of America1594Scopus327,096,2654.87
2Japan536Scopus127,202,1924.21
3United Kingdom456Scopus67,141,6846.79
4Australia424Scopus24,898,15217.03
5Germany324Scopus83,124,4183.90
6Brazil319Web of Science209,469,3231.52
7China 284Web of Science1,427,647,7860.20
8France256Scopus64,990,5113.94
9South Africa254Web of Science57,792,5184.40
10India 195Scopus1,352,642,2800.14
11Poland189Web of Science37,921,5924.98
11Spain178Scopus46,692,8583.81
12Argentina178Medline44,361,1504.01
13Italy172Scopus60,627,2912.84
14Netherlands136Scopus17,059,5607.97
15Turkey119Web of Science82,340,0881.45
16Mexico116Medline126,190,7880.92
17Switzerland101Scopus8,525,61111.85
18Kenya98Scopus51,392,5651.91
19Israel93Scopus8,381,51611.10
20Egypt82Web of Science98,423,5980.83
528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure1.gif

Figure 1. Research trends quantified by the number of published articles on Babesia from 1931 to 2018, Medline.

In the case of Scopus, the median number of articles published each year as of 1970 was only one (IQR: 0-3), from 1970 until 1995 this number increased to 64 (IQR: 56-73) and from 1996 until 2018 was 188 (IQR: 115–271) (Figure 2). At Scopus, 134 countries contributed a minimum of one paper over the study period. For SCI-E, the annual median number of articles reported from 1996 until 2018 was of 99 (IQR: 96-103) (Figure 3), with at least one article published from 129 countries during the study period.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure2.gif

Figure 2. Research trends on Babesia from 1931 to 2018, Scopus.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure3.gif

Figure 3. Research trends on Babesia from 1996 to 2018, Web of Science.

“Obihiro University” in Hokkaido, Japan, was the institution with the most productive research in Scopus, and “Igarashi, I” was the author with the largest record in Babesia research, with 210 articles (Figure 4 and Figure 5). At Web of Science, the H index for the topic is 88, with 70,950 citations, reaching 7,734 citations in 2017 (Figure 6).

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure4.gif

Figure 4. Top research institutions that published scientific literature on Babesia, Scopus.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure5.gif

Figure 5. Top research authors that published scientific literature on Babesia, Scopus.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure6.gif

Figure 6. Citation trends on Babesia from 1931 to 2018, Web of Science.

Analyzing by areas of research according to Scopus, we found that most of the studies belong to the area of immunology and microbiology (28.7%), followed by medicine (26.4%) and veterinary (21.8%) (Figure 7). Also in Scopus, by revising the funding sponsors for the published research on Babesia (Figure 8), we found that the Ministry of Education, Culture, Sports, Science, and Technology from Japan, is the main funder (127, 23.7% of Japanese studies), followed by the Japan Society for the Promotion of Science (113, 21.1%) and the National Institutes of Health (108, 6.8%), amongst other funding institutions (Figure 8).

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure7.gif

Figure 7. Documents by subject area in Scopus.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure8.gif

Figure 8. Documents by funding sponsor in Scopus.

At Web of Science, we found that the areas with more importance for research in Babesia were parasitology (39.2%), veterinary sciences (37.7%), and infectious diseases (13.8%), among others (Figure 9). Consistent with Scopus, at Web of Science, the National Institutes of Health of USA (138, 8.7%), and the Ministry of Education, Culture, Sports, Science, and Technology of Japan (54, 10.1% of Japanese studies), were the main funders (Figure 10).

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure9.gif

Figure 9. Documents by subject area in Web of Science.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure10.gif

Figure 10. Documents by funding sponsor in Web of Science.

The scientific production in USA during 2011-2015 was apparently not influenced significantly by the increasing number of babebiosis cases that were reported by surveillance (Figure 11). However, in Wisconsin, probably the sustained increased observed by the surveillance since 2001, led to an increase in babesiosis research after 2010 (Figure 12).

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure11.gif

Figure 11. Trends in the number of cases of human babesiosis reported in USA and the number of published articles on babesiosis at Scopus, Web of Science (Wos) and PubMed, 2011–2015.

528f522a-e99c-4d3f-b64c-cbd020e02e0a_figure12.gif

Figure 12. Trends in the number of cases of human babesiosis reported in Wisconsin, USA, and the number of published articles on babesiosis at Scopus, Web of Science (Wos) and PubMed, 2001–2015 from Wisconsin, USA.

The raw data generated in this study is available on OSF9.

Discussion

The results presented here show that the USA and Japan have primary roles in Babesia research, with USA leading the scientific production with nearly quarter of the published articles, followed by Japan and the UK (Table 1). However, when we calculated the number of articles per million of inhabitants, we found that Australia publish 3.49 more times than USA (and 4.04 times than Japan), followed by Switzerland, Israel, Netherlands, UK and Poland. Certainly, in USA, tickborne disease occurrence is frequent especially in certain areas and months over the year. Tickborne diseases such as babesiosis are commonly reported in Northeastern states as well in the upper Midwest, often with higher incidence in summer. In addition, blood transfusions is still a matter of concern, even in the USA1013. In countries in Asia, such as Japan, human babesiosis was not reported until fairly recently (1999), when a symptomatic case was describe in Kobe City, Hyogo Prefecture, Japan14,15; however, since then research has significantly increased in this country. Authors from UK have collaborated with research with others from endemic countries. However, in 2006 and 2016, two cases of autochthonous canine babesiosis were reported in the UK. Since November 2015, there have been at least three more cases of canine babesiosis in untraveled dogs from Essex, all were confirmed B. canis infections by PCR. Dermacentor reticulatus ticks were found on the dogs16. The number of articles published by USA and Japan comes as a result from the considerable funding, reflected in the publications supported by their respective agencies. In addition, in USA, babesiosis is a notifiable disease since 2011 (CDC) and most human cases have been reported. Of interest the strong research activity of institutions and countries as Japan and UK, in which Babesia represents a new emerging problem in both animals and humans. The findings highlight the increased research activity on this neglected zoonosis, considered of growing importance in several countries and the need of further studies addressed to preventive and therapeutic aspects.

One of the relevant aspects surrounding babesiosis is that there are not yet licensed human prophylactic vaccines, and treatment alternatives remain limited. Two commonly used antimicrobial regimes are highly effective: the combination of atovaquone and azithromycin and the combination of clindamycin and quinine17. Thus, more preventive measures are needed to reduce the risk of infection from ticks and wild and domestic reservoirs (e.g. rats).

The vision of zoonoses should be one. All integrated. Then, having separated human and animal babesiosis, to us, is not rationale today. Babesiosis is one zoonotic disease, no matter the host. The work on babesiosis, including research, should be together between veterinarians and human physicians, working in the interphase that zoonosis, such as babesiosis, provide. One World, One Health. However, as reflected from this bibliometric study, there is a predominance of studies from human medicine compared to veterinary medicine. There is a need for increase of integration with veterinary sciences, given the relevance of babesiosis as a zoonosis.

Bibliometric analyses contribute an objective vision of the scientific activity of a country or a region, in an investigative area. In the particular case of infectious diseases, there are different reports about its utility58, especially in emerging infectious diseases1820, being possible to establish and to compare the amount of scientific production in journals, institutions, and authors publishing about a certain issue; this would allow establishment of a plan in terms of scientific policy as well in other matters21. No previous bibliometric studies about babesiosis or Babesia have been found in the consulted scientific databases.

It would be ideal to have epidemiological data, such as incidence by active surveillance, but unfortunately such data is not available in most countries, in order to correlate the level of research with the epidemiological relevance of babesiosis. Again, babesiosis is a neglected disease, of importance in several countries, the topic, certainly deserves still more research. Even, in USA, where human babesiosis is now notifiable, only available data is from 2011 to 201522, and we retrieved that in order to see if there was a relationship between the number of cases and the number of articles, but this was not apparently influenced, given that during that period, the number of articles from USA did not increased at Scopus, Web of Science and PubMed. However, in Wisconsin, its Department of Health Services, Division of Public Health, in 2001 defines a confirmed case of babesiosis as the occurrence of fever, anemia, or thrombocytopenia in a patient with confirmatory laboratory findings, and its surveillance begun23. Analyzing the number of reported cases from Wisconsin and the number of articles of babesiosis from 2001 to 2015, especially after 2010, epidemiology appears to have influenced an increase in the publications in Scopus.

In conclusion, it is time to translate research findings into effective control of babesiosis. As occurs with other emerging diseases, research leading to vaccinal or effective therapeutic options are of utmost importance. Tick-borne pathogens such as Babesia and others with even clearer epidemic potential need to be researched more and to be prioritized with effective interventions to reduce their negative impact.

Data availability

Raw bibliometric data generated in this study are available on OSF. DOI: https://doi.org/10.17605/OSF.IO/ER9UP9.

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Rodriguez-Morales AJ, Bonilla-Aldana DK, Escalera-Antezana JP and Alvarado-Arnez LE. Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite [version 2; peer review: 2 approved, 1 not approved]. F1000Research 2019, 7:1987 (https://doi.org/10.12688/f1000research.17581.2)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 2
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PUBLISHED 18 Jul 2019
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Reviewer Report 25 Jul 2019
Stalin Vilcarromero, Division of Infectious Disease, Department of Medicine, Stony Brook University, New York, NY, USA;  Sociedad Científica de Estudiantes de Medicina de la Amazonía Peruana (SOCIEMAP), Facultad de Medicina, Universidad Nacional de la Amazonía Peruana, Iquitos, Peru 
Approved
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In the manuscript entitled "Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite", the authors have included the recommendations made by the reviewers and their quality has improved. This bibliometric review is of interest to future researchers in ... Continue reading
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Vilcarromero S. Reviewer Report For: Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite [version 2; peer review: 2 approved, 1 not approved]. F1000Research 2019, 7:1987 (https://doi.org/10.5256/f1000research.21848.r51373)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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PUBLISHED 30 Dec 2018
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Reviewer Report 28 Feb 2019
Cristina Casalone, Experimental Institute for Zooprophylaxis in Piedmont, Liguria and Valle D’Aosta, Turin, Italy 
Approved
VIEWS 19
The manuscript submitted by Rodríguez Morales et al. represents a bibliometric evaluation on Babesia, in order to contribute to understanding this neglected zoonosis and addressing future research and control strategies. Bibliometric evaluation is an excellent tool to obtain objective information ... Continue reading
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HOW TO CITE THIS REPORT
Casalone C. Reviewer Report For: Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite [version 2; peer review: 2 approved, 1 not approved]. F1000Research 2019, 7:1987 (https://doi.org/10.5256/f1000research.19225.r43816)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 18 Jul 2019
    Alfonso Rodriguez-Morales, Fundación Universitaria Autónoma de las Américas, Colombia
    18 Jul 2019
    Author Response
    Dear Dr. Casalone
     
    Thanks for your valuable comments. Regards them, we would like to comment and discuss, in the context of the submission a new revised version (version 2).
     
    The manuscript submitted ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 18 Jul 2019
    Alfonso Rodriguez-Morales, Fundación Universitaria Autónoma de las Américas, Colombia
    18 Jul 2019
    Author Response
    Dear Dr. Casalone
     
    Thanks for your valuable comments. Regards them, we would like to comment and discuss, in the context of the submission a new revised version (version 2).
     
    The manuscript submitted ... Continue reading
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33
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Reviewer Report 26 Feb 2019
Jeremy S. Gray, UCD School of Biology & Environmental Science, University College Dublin, Dublin, Ireland 
Not Approved
VIEWS 33
This article attempts to assess the bibliographic status of Babesia parasites with the declared objective of identifying research priorities in order to achieve effective prevention and control of babesiosis. The authors have produced publication data from various sources showing trends ... Continue reading
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HOW TO CITE THIS REPORT
Gray JS. Reviewer Report For: Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite [version 2; peer review: 2 approved, 1 not approved]. F1000Research 2019, 7:1987 (https://doi.org/10.5256/f1000research.19225.r44953)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 18 Jul 2019
    Alfonso Rodriguez-Morales, Fundación Universitaria Autónoma de las Américas, Colombia
    18 Jul 2019
    Author Response
    Dear Dr. Gray
     
    Thanks for your comments. We have revised and improved the manuscript. In regard to your observations, we would like to comment and discuss, in the context of the ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 18 Jul 2019
    Alfonso Rodriguez-Morales, Fundación Universitaria Autónoma de las Américas, Colombia
    18 Jul 2019
    Author Response
    Dear Dr. Gray
     
    Thanks for your comments. We have revised and improved the manuscript. In regard to your observations, we would like to comment and discuss, in the context of the ... Continue reading
Views
26
Cite
Reviewer Report 08 Feb 2019
Stalin Vilcarromero, Division of Infectious Disease, Department of Medicine, Stony Brook University, New York, NY, USA;  Sociedad Científica de Estudiantes de Medicina de la Amazonía Peruana (SOCIEMAP), Facultad de Medicina, Universidad Nacional de la Amazonía Peruana, Iquitos, Peru 
Approved with Reservations
VIEWS 26
In the manuscript entitled “Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite” the authors try to evaluate the previous bibliometric research regarding babesiosis in the world. It has recognized the value of this type of study because ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Vilcarromero S. Reviewer Report For: Research on Babesia: A bibliometric assessment of a neglected tick-borne parasite [version 2; peer review: 2 approved, 1 not approved]. F1000Research 2019, 7:1987 (https://doi.org/10.5256/f1000research.19225.r42304)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 18 Jul 2019
    Alfonso Rodriguez-Morales, Fundación Universitaria Autónoma de las Américas, Colombia
    18 Jul 2019
    Author Response
    Dear Dr. Vilcarromero
     
    Thanks for your valuable comments. Regards them, we would like to comment and discuss, in the context of the submission a new revised version (version 2).
     
    In the manuscript ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 18 Jul 2019
    Alfonso Rodriguez-Morales, Fundación Universitaria Autónoma de las Américas, Colombia
    18 Jul 2019
    Author Response
    Dear Dr. Vilcarromero
     
    Thanks for your valuable comments. Regards them, we would like to comment and discuss, in the context of the submission a new revised version (version 2).
     
    In the manuscript ... Continue reading

Comments on this article Comments (0)

Version 2
VERSION 2 PUBLISHED 30 Dec 2018
Comment
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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