Abbreviations
MAP: Mycobacterium avium subsp. paratuberculosis
WOS: Web of Science
SCIE: Science Citation Index Expanded
ESCI: Emerging Sources Citation Index
Hirsch index: h-index
Introduction
Mycobacterium avium subsp. paratuberculosis (MAP) is a Gram-positive bacterium with a size of 0.5×1.5 microns as short thick rods. MAP is acid-fast, immobile, non-spore-forming, aerobic, non-encapsulated, and an obligate intracellular bacterium. It grows very slowly in media and forms a visible colony in 8-24 weeks [ 1 ]. Due to its lipid-rich cell wall, MAP can survive for over a year in cattle feces and soil, approximately 160 days in river waters, 9 months in pool waters, and at least one year at -14°C [ 2 ]. MAP is the etiological agent of paratuberculosis (Johne's disease), an infectious disease characterized by chronic gastroenteritis, diarrhea, and emaciation in domestic and wild ruminants [ 3 , 4 ]. Animals usually contract MAP through the consumption of contaminated feed, water, and colostrum. In infected animals, it progresses with diverse symptoms, such as severe diarrhea, cachexia, rough fur, dry skin, severe anemia, submandibular edema, and a decrease in milk yield [ 5 ]. Paratuberculosis has been reported in many countries with a high prevalence [ 6 - 8 ]. There is a hypothesis that MAP, the causative agent of paratuberculosis, may also be involved in Crohn's disease in humans [ 9 ]. Crohn's disease is a chronic inflammatory condition affecting the human gastrointestinal tract from the mouth to the anus, and its exact cause remains undetermined [ 3 ]. The similarity of the clinical and pathological findings between paratuberculosis in animals and Crohn's disease in humans supports the idea that MAP might be involved in Crohn's disease [ 10 , 11 ]. Studies have shown the presence of MAP DNA in the intestines of individuals with Crohn's disease, strengthening the notion that MAP could play a role in this disease [ 12 , 13 ].
It has been suggested that the transmission of MAP from infected animals to humans may occur through the consumption of contaminated meat, meat products, dairy products, and water [ 14 ]. Both milk and feces from dairy cows with clinical and subclinical paratuberculosis can lead to foodborne contamination [ 15 ]. Studies have reported the presence of MAP in milk, dairy products, meat, meat products, baby foods, and river waters [ 16 - 20 ]. The fact that MAP causes great economic losses in the ruminant/livestock industry worldwide, harming animal welfare, and its role in Chron’s disease in humans reveals the importance and seriousness of this bacterium. Recently, there have been increasing reports on the role and importance of MAP in public health [ 21 ].
The aim of this study was to investigate the importance of publications in this field and to perform a bibliometric analysis to review relevant trends and clusters. This analysis will provide a better understanding of the direction for future scientific and clinical research.
Result
Document Analysis
In our bibliometric analysis of MAP studies conducted during 2001-2021, we identified 1755 articles, 96.467% of which were published in SCIE-indexed journals, and 3.533% were published in ESCI-indexed journals. English was the predominant language, accounting for 95.448% of the papers (Table 1).
| Languages | Record Count | % of 1.755 |
|---|---|---|
| English | 1722 | 98.120 |
| Spanish | 13 | 0.741 |
| German | 10 | 0.570 |
| Portuguese | 5 | 0.285 |
| Indonesian | 2 | 0.114 |
| Polish | 2 | 0.114 |
| Italian | 1 | 0.057 |
Citation Distribution by Year
The analyzed articles amassed a total of 36 237 citations, resulting in an average h-index of 72. Notably, 2013 had the highest number of papers, while 2021 had the highest number of citations (Figure 1). The United States was the most cited country (Figure 2).
Figure 1. Publication and citation frequency of Mycobacterium avium subsp. paratuberculosis by year.
Figure 2. Countries most cited in Mycobacterium avium subsp. paratuberculosis studies
Distribution of Publications by Country
The leading countries in terms of MAP-related publications were the USA (n = 536), Canada (n = 167), and Australia (n = 141). MAP-related publications emanated from 75 different countries across the globe (Table 2 and Figure 3).
| Countries/Regions | Record Count | % of 1.755 |
|---|---|---|
| USA | 536 | 30.541 |
| Canada | 167 | 9.516 |
| Australia | 141 | 8.034 |
| Germany | 133 | 7.578 |
| India | 127 | 7.236 |
| Italy | 116 | 6.610 |
| Spain | 84 | 4.786 |
| Netherlands | 79 | 4.501 |
| England | 67 | 3.818 |
| New Zealand | 55 | 3.134 |
| Czech Republic | 53 | 3.020 |
| North Ireland | 51 | 2.906 |
| Scotland | 45 | 2.564 |
| France | 44 | 2.507 |
| Ireland | 39 | 2.222 |
| South Korea | 39 | 2.222 |
| Egypt | 37 | 2.108 |
| Iran | 37 | 2.108 |
| Chile | 35 | 1.994 |
| Argentina | 34 | 1.937 |
| Brazil | 31 | 1.766 |
| Japan | 31 | 1.766 |
| Denmark | 29 | 1.652 |
| Norway | 23 | 1.311 |
| Greece | 22 | 1.254 |
| *Showing 25 out of 53 entries, 4 record(s) (0.228%) do not contain data in the field being analyzed | ||
Figure 3. Global article map of Mycobacterium avium subsp. paratuberculosis *4 record(s) (0.228%) do not contain data in the field being analyzed
Most Active Research Areas
The articles were primarily related to the research fields of Veterinary Sciences (n = 730), Microbiology (n = 519), and Immunology (n = 287) (Table 3).
| Research Areas | Record Count | % of 1.755 |
|---|---|---|
| Veterinary Sciences | 730 | 41.595 |
| Microbiology | 519 | 29.573 |
| Immunology | 287 | 16.353 |
| Agriculture | 226 | 12.877 |
| Food Science Technology | 169 | 9.630 |
| Biotechnology Applied Microbiology | 158 | 9.003 |
| Infectious Diseases | 134 | 7.635 |
| Science Technology Other Topics | 81 | 4.615 |
| Biochemistry Molecular Biology | 79 | 4.501 |
| Gastroenterology Hepatology | 55 | 3.134 |
| Research Experimental Medicine | 38 | 2.165 |
| Genetics Heredity | 28 | 1.595 |
| Cell Biology | 22 | 1.254 |
| Public Environmental Occupational Health | 15 | 0.855 |
| Zoology | 15 | 0.855 |
| Neurosciences Neurology | 14 | 0.798 |
| Pathology | 14 | 0.798 |
| Life Sciences Biomedicine Other Topics | 12 | 0.684 |
| Chemistry | 10 | 0.570 |
| Reproductive Biology | 8 | 0.456 |
| General Internal Medicine | 6 | 0.342 |
| Engineering | 5 | 0.285 |
| Environmental Sciences Ecology | 4 | 0.228 |
| Mathematical Computational Biology | 4 | 0.228 |
| Pharmacology Pharmacy | 4 | 0.228 |
| *Showing 25 out of 53 entries, 5 record(s) (0.285%) do not contain data in the field being analyzed. | ||
Most Prolific Affiliations
The organization with the most extensive research output on MAP, contributing 168 articles, was the United States Department of Agriculture (USDA) (Table 4).
| Affiliations | Record Count | % of 1.755 |
|---|---|---|
| United States Department of Agriculture USDA | 168 | 9.573 |
| University of Wisconsin System | 88 | 5.014 |
| University of Wisconsin Madison | 87 | 4.957 |
| University of Sydney | 84 | 4.786 |
| Indian Council of Agricultural Research Icar | 81 | 4.615 |
| University of Minnesota System | 76 | 4.330 |
| University of Minnesota Twin Cities | 76 | 4.330 |
| University of Sassari | 58 | 3.305 |
| Cornell University | 53 | 3.020 |
| Czech Veterinary Research Institute | 53 | 3.020 |
| Iowa State University | 53 | 3.020 |
| Icar Central Institute for Research on Goats | 51 | 2.906 |
| University of Guelph | 48 | 2.735 |
| University of Pennsylvania | 48 | 2.735 |
| University of Calgary | 46 | 2.621 |
| Queens University Belfast | 45 | 2.564 |
| Icar Indian Veterinary Research Institute | 39 | 2.222 |
| Utrecht University | 39 | 2.222 |
| Egyptian Knowledge Bank Ekb | 37 | 2.108 |
| University of Veterinary Medicine Hannover Foundation | 36 | 2.051 |
| Justus Liebig University Giessen | 35 | 1.994 |
| Universidad Austral De Chile | 35 | 1.994 |
| Agresearch New Zealand | 34 | 1.937 |
| Inrae | 33 | 1.880 |
| Friedrich Loeffler Institute | 31 | 1.766 |
| *Showing 25 out of 1.201 entries, 753 record(s) (42.906%) do not contain data in the field being analyzed. | ||
Most Prolific Journals
The Journal of Dairy Science stood out as the journal with the highest number of MAP-related papers, with a total of 102 publications on this subject (Table 5).
| Journals | Record Count | % of 1.755 |
|---|---|---|
| Journal of Dairy Science | 102 | 5.812 |
| Veterinary Microbiology | 94 | 5.356 |
| Veterinary Immunology and Immunopathology | 74 | 4.217 |
| Plos One | 58 | 3.305 |
| Applied and Environmental Microbiology | 57 | 3.248 |
| Preventive Veterinary Medicine | 52 | 2.963 |
| Journal of Clinical Microbiology | 42 | 2.393 |
| Journal of Veterinary Diagnostic Investigation | 38 | 2.165 |
| Infection and Immunity | 37 | 2.108 |
| Clinical and Vaccine Immunology | 32 | 1.823 |
| Veterinary Research | 26 | 1.481 |
| Journal of Microbiological Methods | 22 | 1.254 |
| Vaccine | 22 | 1.254 |
| Small Ruminant Research | 21 | 1.197 |
| Tropical Animal Health and Production | 21 | 1.197 |
| Journal of Wildlife Diseases | 19 | 1.083 |
| American Journal of Veterinary Research | 18 | 1.026 |
| Canadian Veterinary Journal Revue Veterinaire Canadienne | 18 | 1.026 |
| International Journal of Food Microbiology | 18 | 1.026 |
| Veterinary Record | 18 | 1.026 |
| BMC Microbiology | 17 | 0.969 |
| BMC Veterinary Research | 17 | 0.969 |
| Gut Pathogens | 17 | 0.969 |
| Journal of Applied Microbiology | 17 | 0.969 |
| Research in Veterinary Science | 17 | 0.969 |
| *Showing 25 out of 329 entries | ||
Keyword Occurrence
Our bibliometric analysis highlighted the most frequently used keywords depicted in Figure 4. Keywords are integral to bibliometric analysis, aiding in the identification of primary topics and themes within a specific research area. Search engine algorithms rely on keywords to detect relevant literature. In our keyword visualization analysis, colors indicate preferred keywords, with red representing particularly popular ones. Keywords displayed in larger font sizes had a higher frequency of occurrence in the articles (Figure 2).
Figure 4. Keyword visualization map of articles containing Mycobacterium avium subsp. paratuberculosis at least 5 times *** Colors demonstrate preferred keywords, especially red show popular keywords.. Keywords represented with larger circle size or font size had a relatively higher occurrence in the articles.
Bibliographic Coupling Between Countries
In the network visualization of bibliographic coupling between countries, the size of the bubbles was directly proportional to the volume of research conducted by each country. The width of the lines connecting countries indicates the strength of their coupling, while the line colors signify the cluster to which each country has been assigned. For this research, we considered a minimum of 5 documents and 0 citations for each country's documents (Figure 5).
Figure 5. Countries with at least 5 publications and 5 citations are shown on the map. *Collaboration is shown with lines linking nations. Stronger cooperation is indicated by thicker lines. Countries with a bigger circle or text size had a higher level of international cooperation.
Using Vosviewer for Mapping
In the network map of overlay visualization for the co-authorship analysis of countries, the size of the bubbles was directly linked to the number of articles published by each country. The diameters of the lines connecting authors represent the extent of their collaboration, and the colors of these lines indicate the clusters to which the authors belong. Authors within the same cluster tend to work closely together. The co-authorship analysis employs a color gradient, transitioning from red to yellow, to depict the level of collaboration among authors. We used a minimum of five documents for co-authorship analysis (Figure 6).
Figure 6. Authors with at least 10 publications and 100 citations are shown on the map. **Citations are shown by lines linking authors. Authors with a greater circle size or font size had a higher number of citations.
Bibliographic Coupling between Country, Keywords, and Cited Journals
A three-field Graph (Sankey diagram) consisting of country, keywords, and cited journals for the ten most researched topics is given in Supplementary Figure 1. Trend topics by years in MAP investigations are shown in Supplementary Figure 2.
Discussion
The results of bibliometric analysis in the field of diseases have increasingly captured the attention of scientists in recent years [ 22 , 23 ]. Bibliometric analysis provides a scientific map of various diseases. In the realm of health sciences, it evaluates how a particular disease has evolved over the years and how the inclination to research that disease has shifted, employing a variety of indicators. Bibliometric analysis serves as an analytical method unveiling the broader intellectual landscape surrounding the disease while helping to identify particularly influential articles [ 23 , 24 ].
In our bibliometric analysis of MAP studies spanning from 2001 to 2021, we discovered 1775 articles, 96.467% and 3.533% of which were published in SCIE-indexed and ESCI-indexed journals, respectively. These papers collectively received 36 237 citations, resulting in an average h-index of 72. While the year 2013 had the highest number of articles, 2021 saw the highest number of citations. A steady increase in the number of citations persisted until 2017; however, in recent years (2018-2020), the average number of citations has decreased. This phenomenon might be attributed to older publications being cited more frequently than newly published articles within that year [ 25 ].
Our findings revealed that a substantial portion of MAP publications originated from the United States, accounting for 30.541 articles. This is hardly surprising, as the USA, similar to the case of tuberculosis, allocates more resources to research and development related to paratuberculosis than most other countries [ 26 ]. In terms of the sheer number of publications, Canada ranks second with 9516 articles, while Australia secures the third position with 8349 articles. The presence of these countries in the top three may signify the widespread prevalence of this factor within their regions. Germany, as the fourth most productive country, with 7578 publications, can be linked to its substantial research funding initiatives. India, an Asian nation, also occupies a prominent position in the top five for productivity in MAP research. An overarching examination of the worldwide distribution of publications by country underscores the necessity for the development and implementation of global strategies to combat paratuberculosis.
Reviewing the leading journals based on the number of published articles, we find that the Journal of Dairy Science, ranked first, with an impact factor of 4.225. It is worth noting that the official publication of the American Dairy Science Association is not only indexed in WOS but is also included in various databases, such as Agricola, Biological Abstracts, Biological and Agriculture Index, BIOSIS Database, CABI Abstracts, Current Contents, Elsevier Bibliographic Databases, PubMed, and Scopus. When examining the most cited publications, the article titled 'The Complete Genome Sequence of MAP' by Li L. et al. published in 2005, has garnered 353 citations.
In our co-citation analysis among countries, an interesting trend emerges; the countries ranking in the top ten for article publication, including the USA, Australia, Germany, India, Netherlands, Italy, and Spain, are also prominent in joint citation analysis for MAP.
The keywords "paratuberculosis" and "Johne's disease" were the most frequently encountered in our bibliometric analysis of the number of publications, which aligns with previous research confirming these data [ 27 ]. The fact that the agent is pathogenic for both animals and humans makes these keywords the most commonly used.
The varying budgets between countries and universities influence the number of research projects funded. The role of financial institutions in advancing science and research is crucial [ 28 ]. The results of the present research showed that the USA ranks in the top three financial institutions contributing to MAP research, which is consistent with other studies [ 29 ].
Analyzing the institutions where research published during 2001-2021 was conducted, the United States Department of Agriculture, the University of Wisconsin System, and the University of Wisconsin Madison emerged as the top three funders of paratuberculosis research. The significance of these data is expected to increase over time, encouraging funders to be more diligent in using official fund names [ 30 ]. In line with the mentioned argument, a book by Kazda et al. (2009) documented the prevalence of mycobacteria and their impact on the health of animals and humans, highlighting financial losses in ruminants due to MAP, food, and environmental contamination [ 31 ].
The majority of publications were in English (98.12%), and other languages included Spanish (0.74%), German (0.57%), Portuguese (0.28%), Indonesian (0.11%), Polish (0.11%), and Italian (0.05%). These findings in our bibliometric analysis align with a previous study [ 27 ]. The prevalence of English in publications can be attributed to the widespread acceptance of English in the scientific community and the fact that many publishers primarily accept articles in English, increasing the international accessibility of research findings.
The current study, conducted by veterinarians, physicians, and food researchers, aims to define MAP. It presents up-to-date data and sheds light on the boundaries and trends in paratuberculosis research from the past to the present. The continuous increase in the number of publications addressing paratuberculosis signifies that this factor remains a topic of active research worldwide. Given the importance of determining effective control strategies for paratuberculosis in both the food industry and public health, it is crucial to foster research collaborations between countries. This bibliometric analysis provides a substantial period within the scientific literature for assessing paratuberculosis, offering diverse data for future research endeavors.
In conclusion, this study provides up-to-date data on MAP, providing important information about the frontiers and trends in MAP research from past to present were presented. The steady rise in the number of publications on paratuberculosis reflects the continued global interest in this factor. Establishing effective control strategies for paratuberculosis is vital for the food industry and veterinary medicine as well as public health, highlighting the need for international research collaborations. This bibliometric analysis provides an important timeframe in the scientific literature for evaluating paratuberculosis and provides diverse data for future research in veterinary and human medicine.
Limitations
In this study, we examined the current status and prospects of MAP research through bibliometric analysis. However, there are several limitations to this analysis. Firstly, the scope of this bibliometric analysis was limited to publications published and indexed in the WOS database, potentially overlooking reports from other databases. Despite these limitations, the study provided valuable insights into MAP trends and identified areas with information gaps.
Secondly, considering that some authors may have multiple names or variations in name spellings, standardizing author names and terms based on VOSviewer results may not be entirely accurate. This could potentially lead to inaccurate results for certain authors. Despite these drawbacks, this article offers a foundational overview of MAP research.
Materials and Methods
Data Collection
Ethics approval was not required for this study as no human or animal participants were included. To retrieve Mycobacterium avium subsp. paratuberculosis publications, the WOS database (Clarivate PA, USA) was used. To evaluate the impact of scientific research effectively, the h-index was introduced as an alternative to traditional bibliometric indicators. Data for this research were sourced from the WOS database as of November 28, 2022. Information from WOS, including publication titles, authors' names, publication years, research countries, affiliated organizations, journal names, keywords, abstracts, and citation data for each record, was saved as TXT files and imported into Microsoft Office Excel 2019 (Los Angeles, USA). The research materials were accessed through Çanakkale Onsekiz Mart University's online library and digital resources.
Comprehensive Overview of the WOS Database
The WOS database was used to determine the research location or country, the type of study, authorship, and the number of citations. Only studies published during 2001-2021 were considered within the designated time frame. As the publication process for 2023 investigations has not been completed yet, those belonging to 2022 and 2023 were not included in the study. English was the selected search language, and h-index was employed as an indicator of publication impact.
Search Strategy
The search terms (keywords) for this study were "Mycobacterium avium paratuberculosis" (Title) OR "Mycobacterium avium subspecies paratuberculosis" (Title) and Article (Document Types) OR Science Citation Index Expanded (SCI-EXPANDED) OR Emerging Sources Citation Index (ESCI) (WOS Index) and 2001-2021 (Publication Years). The selected timeframe was 2001-2021, allowing us to observe bibliometric developments over the last two decades. This research exclusively included research articles, while letters, reviews, editorials, and other types of articles were excluded. The WOS publications saved as TXT files were imported into Microsoft Office Excel 2019 alongside document categories, publication years, author names, journals, affiliations, keywords, group authors, and citations.
Network Analysis
In this bibliometric study, VOSviewer (version 1.6.10, Leiden University, The Netherlands) was employed for data importation and also to reveal future trends, collaboration networks, and significant findings. In addition, authorship, links, keywords, citations, and thematic words were collected and reviewed using this software. This tool allowed for the analysis of keywords, co-occurrences, citations, co-authorships, and co-citations.
Authors' Contributions
M.E.A. and S.K.A. conceived and planned the experiments. S.A. carried out the analysis. M.E.A., S.K.A. and S.A. contributed to the interpretation of the results. M.E.A. took the lead in writing the manuscript. All authors provided critical feedback for nalysis and manuscript.
Acknowledgements
Thanks to everyone who helped us in the current study.
Competing Interests
The authors declare that there is no conflict of interest.
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