Open-access Global research output on antimicrobial resistance in dairy farming

[Resultado de pesquisa global sobre resistência antimicrobiana na pecuária leiteira]

ABSTRACT

Antimicrobials are pivotal in treating bacterial infections. More often than any other class of antimicrobial, antibiotics are a class of antimicrobials used primarily to treat bacterial infections. Thus, both human health and life longevity, as well as the welfare of animals, have greatly improved with the development of antibiotics as a means of treating infectious diseases. Dairy farming is essential to satisfying the world's demand for dairy products. Nevertheless, improper use of antibiotics in dairy farming contributes greatly to the formation of antimicrobial resistance. Moreover, the resulting antimicrobial resistance can be transferred to humans by consuming contaminated dairy products. Therefore, the scientific community has been intensively studying the relationship between dairy farming and antimicrobial resistance since 1983. And, due to the increasing awareness of antimicrobial resistance worldwide, studies on antimicrobial resistance in dairy farming have rapidly increased 89 times in the last twenty years. Today, the development of antimicrobial resistance in dairy farming is among the trending research topics. For this purpose, this study is the first bibliometric approach that aims to guide future studies by revealing all aspects of the studies on this subject between 1983 and 2023.

Keywords:
antimicrobial; antibiotic; antimicrobial resistance; dairy farming; mastitis; bacterium

RESUMO

Os antimicrobianos são essenciais no tratamento de infecções bacterianas. Mais frequentemente do que qualquer outra classe de antimicrobiano, os antibióticos são uma classe de antimicrobianos usados principalmente para tratar infecções bacterianas. Assim, a saúde humana e a longevidade da vida, bem como o bem-estar dos animais, melhoraram muito com o desenvolvimento de antibióticos como meio de tratamento de doenças infecciosas. A criação de gado leiteiro é essencial para atender à demanda mundial por produtos lácteos. No entanto, o uso inadequado de antibióticos na pecuária leiteira contribui muito para a formação de resistência antimicrobiana. Além disso, a resistência antimicrobiana resultante pode ser transferida para os seres humanos por meio do consumo de produtos lácteos contaminados. Portanto, a comunidade científica tem estudado intensamente a relação entre a pecuária leiteira e a resistência antimicrobiana desde 1983. E, devido à crescente conscientização sobre a resistência antimicrobiana em todo o mundo, os estudos sobre a resistência antimicrobiana na pecuária leiteira aumentaram rapidamente 89 vezes nos últimos vinte anos. Hoje em dia, o desenvolvimento da resistência antimicrobiana na pecuária leiteira está entre os tópicos de pesquisa mais populares. Para esse fim, este estudo é a primeira abordagem bibliométrica que visa orientar estudos futuros, revelando todos os aspectos dos estudos sobre esse assunto entre 1983 e 2023.

Palavras-chave:
antimicrobiano; antibiótico; resistência antimicrobiana; pecuária leiteira; mastite; bactéria

INTRODUCTION

Antimicrobial resistance (AMR) is a global threat that poses significant challenges to effectively preventing and treating infectious diseases (Dadgostar 2019; Ferri et al., 2017). Thus, many studies show that the number of infections due to resistant microorganisms constantly increases (Saga and Yamaguchi 2009; Serwecińska 2020). AMR has a heavy cost to the world economy. AMR causes serious economic harm by prolonging hospital stays and causing more medical expenses (Cosgrove 2006; Maragakis et al., 2008). In a new report titled "Stemming the superbug tide," published on November 7, 2018, the Organization for Economic Co-operation and Development (OECD) estimates that infections with resistant microorganisms will kill 2.4 million people in Europe, North America, and Australia over the next 30 years, with annual costs potentially reaching US$3.5 billion (Hofer 2019; OECD 2018). The worldwide issue of antimicrobial resistance endangers human and animal health. With an emphasis on collaborative action in this area, the "One Health" approach was interpreted more widely to include collaboration between the human and animal sectors and economic, social, and behavioral components (Ferri et al., 2017; Shallcross et al., 2015).

Antimicrobials are pivotal in treating bacterial infections (Kalelkar et al., 2022; Keir and Dickinson 2015). More often than any other class of antimicrobial, antibiotics are a class of antimicrobials used primarily to treat bacterial infections (Salam et al., 2023). Thus, both human health and life longevity, as well as the welfare of animals, have greatly improved with the development of antibiotics as a means of treating infectious diseases. However, the overuse and misuse of antibiotics can cause microorganisms to become resistant to antibiotics, resulting in the spread of antimicrobial resistance (Lieberman 2003; Verraes et al., 2013).

Antibiotics are widely used to treat disease and increase animal performance in farm animals. Thus, the application of antibiotics for treatment (e.g., lameness, mastitis, scours, and respiratory sickness), as well as for preventative health advantages and productivity gains, is the clearest selection pressure for antimicrobial resistance in cattle production systems (Call et al., 2008; Jayarao et al., 2019). Today, there have been increasing concerns about the emergence of antimicrobial resistant diseases and the spread of antimicrobial resistance due to the widespread use of antibiotics in farm animals (Economou and Gousia, 2015; Gebreyes et al., 2017; Vidovic and Vidovic 2020). Given different possible sources of human contact with antimicrobial resistant microorganisms, it is vital to optimize antibiotic use in farm animals to reduce the development of antimicrobial resistance (Krömker and Leimbach, 2017; More, 2020).

By 2050, it is expected to be 9.7 billion people worldwide, a rise from the current estimated 7.6 billion. Consequently, increasing population growth brings with it the demand for dairy products (Jayarao et al., 2019; Lagrange et al., 2015). In addition to making a substantial contribution to the agricultural industry, dairy farming is essential to satisfying the world's demand for dairy products (Douphrate et al., 2013; Maijala, 2000). However, improper use of antibiotics in dairy farming contributes greatly to the formation of antimicrobial resistance (Sharma et al., 2020; Wemette et al., 2020). Moreover, the resulting antimicrobial resistance can be transferred to humans by consuming contaminated dairy products (Brown et al., 2020; Elafify et al., 2020).

Although efforts to limit the use of antibiotics in dairy farming have been made in recent years, the desired success has not yet been achieved. The scientific community is investigating the role of dairy farming in the development of antimicrobial resistance (Hailu et al., 2021; Lam et al., 2020; Saini et al., 2012). However, the relationship between dairy farming and antimicrobial resistance is a comprehensive issue that should be addressed within the “One Health” approach (Garcia et al., 2019; Kayode and Okoh, 2022). In recent years, it has been observed that studies on the relationships between antimicrobial resistance and dairy farming have increased rapidly (Massé et al., 2023; Paschoalini et al., 2023; Wang et al., 2023a; Widodo et al., 2023). Therefore, this study aims to give significant insights and implications for future studies by providing a comprehensive bibliometric literature analysis revealing the relationship between dairy farming and antimicrobial resistance.

MATERIAL AND METHODS

Ethics committee approval was not required for this study because there was no study on animals or humans.

The current study retrieved data from the Web of Science (WoS) database between 1983 and 2023 as of November 4, 2023 (Table 1). This study used a search query that utilized the terms "dairy farming" and "antimicrobial resistance" found in the titles or abstracts of the articles. The Web of Science (WoS) categories “microbiology”, “veterinary science”, “food science technology”, “agriculture”, “dairy animal science”, “pharmacology”, “biotechnology” and “public environmental occupational health” were included in the bibliometric analysis. The journals were carefully chosen as source material to gain access to the target studies related to the topic in the WoS database. The data for the subject was then downloaded in plain text format from the WoS database system. The retrieved data comprised the document types, annual scientific publications, authors, citations, journals, keywords, clusters, institutions, and the most relevant countries. The downloaded data is arranged using R software's "convert2pdf" package. Only the top ten active authors, countries, journals, institutions, and funding agencies were listed in this study. The "bibliometrix" package in R software was used to perform the bibliometric analysis (Aria and Cuccurullo 2017; Team 2020).

RESULTS AND DISCUSSION

The data of this study consists of 3617 documents. The main document type of the data consists of journal articles (3186). Thus, the journal articles constitute 86.3% of 3617 documents. The most common document type after articles is reviews. Reviews constitute 269 of 3617 documents, accounting for 7.4% of all documents. Other document types, such as proceedings papers and book chapters, comprise a small part of all documents. The number of documents and their percentages among all documents are shown in Table 1.

The current study provides the annual growth of publications on antimicrobial resistance in dairy farming between 1983 and 2023. Publication increases were evaluated from 1983 to 1999 and 2000 to 2023. Only 40 articles in total were published between 1983 and 1999. The average number of articles per year in this period is 2.5. However, in 2000, 18 articles were published, with a rapid increase in the number of articles. The highest number of articles between 2000 and 2023 was reached in 2022, with 466 publications. It is seen that the number of articles per year between 2000 and 2023 is 155.3, and the total number of publications in this period is 3574. Scientists have received intense interest in antimicrobial resistance in dairy farming in the last twenty years. Although all data for 2023 is not available, there are currently 337 publications. The annual growth of publications between 1983 to 2023 is given in Figure 1.

Table 1
Types of documents on antimicrobial resistance in dairy farming (1983-2023)

The research results have found that many research organizations or universities from different countries of the world are related to this research field. However, the current study shows the top ten research organizations or universities. As seen in Table 2, there are studies of 2589 research organizations worldwide on antimicrobial resistance in dairy farming. It is seen that these research institutions produced 12051 publications. The Egyptian Knowledge Bank (Egypt) is the most productive research organization with 420 (3.8%) publications, followed by the United States Department of Agriculture (USA) with 179 (1.4%), the Indian Council of Agricultural Research (IN) with 169 (%1.4), the Cornell University (USA) with 168 (1.3%), the University of California Davis (USA) with 130 (1.0%), the University of California System (USA) with 109 (0.9%), the Ohio State University (USA) with 81 (0.6%), the University of Calgary (CA) with 78 (0.6%), the Mansoura University (Egypt) with 70 (0.5%) and the Ghent University (Belgium) with 69 (0.5%) publications. Figure 2 shows the distribution of scientific production on antimicrobial resistance in dairy farming according to their countries. The first three ranks among 104 countries are the United States, China, and Brazil, with 1793, 878, and 749 scientific productions, respectively. Canada followed them with (601), India (464), Egypt (455), Italy (401), United Kingdom (385), Spain (346), and Germany with (340) in scientific production.

Figure 1
The annual growth of publications on antimicrobial resistance in dairy farming (1983-2023)

Table 2
The top ten research organizations on antimicrobial resistance in dairy farming studies

Figure 2
Country scientific production map on antimicrobial resistance in dairy farming (1983-2023). The level of color saturation increases with the number of publications in each country

The top ten worldwide academic journals for publishing articles on antimicrobial resistance in dairy farming are shown in Figure 3. The current study shows that all the worldwide academic journals have 3496 articles on antimicrobial resistance in dairy farming between 1983 and 2023. Among the worldwide academic journals, the top ten academic journals are responsible for (n=1042, 29.8%) the number of articles. The first rank top ten academic journal is the Journal of Dairy Science with 318 articles, followed by the Frontiers in Microbiology with 129, the Foodborne Pathogens and Disease with 88, the Antibiotics with 82, the Veterinary Microbiology with 76, the Animals with 73, the Frontiers in Veterinary Science with 72, the Plus One with 70, the International Journal of Food Microbiology with 69 and Applied and Environmental Microbiology with 65 articles. The most preferred top ten academic journals are in the fields of food, microbiology, and dairy sciences.

Figure 3
The top ten academic journals on antimicrobial resistance in dairy farming (1983-2023)

The present study revealed that the top ten authors with the most publications on antimicrobial resistance in dairy farming are five from the USA, two from Belgium, one from Canada, and one from China, as seen in Figure 4. Berkema (University of Calgary) is the most productive author with 40 publications. Warnick (Cornell University) with 37 publications, and Han (China Agricultural University) are second and third ranked authors. The h index of Berkema, Varnick, and Han is 20, 21, and 13, respectively. These authors have an important role in worldwide disseminating studies on antimicrobial resistance in dairy farming.

Figure 4
Top ten most influential authors on antimicrobial resistance in dairy farming (1983-2023).

In the current study, Figure 5 shows that the USA is the most productive country, with 563 articles on antimicrobial resistance in dairy farming, followed by China and Brazil, with 332 and 252 articles, respectively. The multiple country publications (MCP) Ratios of the USA, China, and Brazil appear to be 0.23, 0.28, and 0.17, respectively. Australia, Canada, and Spain have 60, 161, and 131 publications, respectively. However, Australia has the highest rate of MCP ratio at 0.43, followed by Canada at 0.36 and Spain at 0.36. These countries appear to support collaborative multi country research. It is seen that Turkey is among the top 10 countries with 92 publications. However, most studies (86) conducted in Turkey are single country publications. So, it can be concluded that the studies are generally carried out within the country.

The analysis of the number of keyword occurrences on antimicrobial resistance in dairy farming studies revealed that the most common keyword is antimicrobial resistance, with 789 occurrences, followed by prevalence with 725, antibiotic resistance with 681, identification with 490, strains with 466, resistance with 446, Escherichia coli with 399, susceptibility and milk with 398 and 355, respectively (Figure 6). Analysis showed that these studies have concentrated on identifying milk's antimicrobial and antibiotic resistance properties in terms of bacterial strains.

This study identified five main clusters of keywords related to antimicrobial resistance in dairy farming studies (Figure 7). The first cluster (blue cluster, n=19) discussed the identification of bacteria and virulence factors that cause antimicrobial and antibiotic resistance in dairy products using different molecular methods. The second cluster (red cluster, n=2) discussed the relationships between antimicrobial resistance and health. The third cluster (yellow cluster, n=20) discussed the bacteria that cause mastitis in dairy cattle and the relationships between mastitis and antimicrobial resistance. The fourth cluster (green cluster, n=4) mainly discussed the Listeria monocytogenes bacteria, which causes bacterial contamination in cheese products. The fifth cluster (purple cluster, n=1) is mainly related to laboratory and in vitro conditions.

Figure 5
Collaboration network of productive countries.

Figure 6
The word cloud and number of occurrences of keywords. The left side represents the word cloud created using the most important keywords associated with worldwide studies on antimicrobial resistance in dairy farming. The right side represents the number of occurrences of the most important keywords from 1983 to 2023.

Figure 7
Clustering map of keywords using antimicrobial resistance in dairy farming studies.

Bibliometric analysis is a sociometric analysis method that reveals the relationships between scientific studies in a specific field (Onder and Tirink, 2022). The current study is the first bibliometric study that provides a detailed analysis of antimicrobial resistance in dairy farming, both its research trends and growth over the years. The analysis revealed that there has been a significant increase in research activity about antimicrobial resistance in dairy farming, especially in the last two decades. According to the current study, publications have increased 89-fold in the last two decades. Thus, this significant increase in research activities reveals the high impact of this subject on a global scale.

The current study showed that the USA and China are among the most productive countries on antimicrobial resistance in dairy farming. The USA and China are the leading countries that allocate the most budgets to research in the world (Das and Mukherjee, 2020; Xu and Huang, 2019). Both countries seriously suffer from antimicrobial resistance. The USA spends USD 5 billion annually on health problems related to antimicrobial resistance (Váradi et al., 2022). The Centers for Disease Control and Prevention (CDC) released a 2019 report on AMR infections and deaths in the USA, indicating that over 2.8 million AMR infections occur in the United States each year, leading to over 35,000 deaths (Craig, 2019). Antimicrobial resistance appears to be a crisis that threatens public security in China (Qu et al., 2019; Wang et al., 2023b). In China, antimicrobial resistance caused by gram negative bacteria such as carbapenem resistant Pseudomonas aeruginosa, Klebsiella pneumoniae, and Acinetobacter is quite serious problem (Liu et al., 2020; Wang et al., 2018; Zhang et al., 2020).

This study indicated that the Egyptian Knowledge Bank (Egypt) is the most productive organization with 420 research outputs. Egyptian Knowledge Bank is an online library established in 2016 in line with the digitalization steps of Egypt's 2030 vision (AbdelKader and Sayed, 2022; Saavedra, 2019). The Egyptian government's efforts to combat antimicrobial resistance and the intense interest of Egyptian scientists have been effective in increasing the number of publications on this subject (Edward et al., 2023; Helmy et al., 2023; Mogheith, 2023).

In the current study, the Journal of Dairy Science and the Frontiers in Microbiology are the leading journals in the top ten listed journals. All journals were determined to be high impact factor journals in the Q1 subregion. The countries of the journals in the top ten list are the USA, Switzerland, and the Netherlands. Throughout the study period, one of the most frequently cited articles obtained 785 citations published in the Food Science and Technology. This study discussed the importance of biofilm formation on microbial control in the dairy industry (Simões et al., 2010). The following study received 720 citations and was published in Microbiology. This study argued the role of understanding Enterococcus species' ecology, virulence, and epidemiology in preventing antibiotic resistance development (Fisher and Phillips, 2009). The third most cited study, with 676 citations discusses the effect of antibiotic use in agricultural areas on the spread of antibiotic resistance genes (Heuer et al., 2011).

In this study, the keyword and clustering analysis revealed that Escherichia coli and Listeria-monocytogenes are among the most frequently encountered microorganisms on antimicrobial resistance in dairy studies. In the last twenty years, many studies have shown that these bacteria play an active role in the spread of antimicrobial resistance by causing contamination in dairy products (Asfaw et al., 2023; Obaidat and Stringer, 2019; Praça et al., 2023). Analyzes also showed a significant relationship between mastitis disease and antimicrobial resistance. Mastitis is a disease that causes significant productivity losses in dairy cattle (Azooz et al., 2020; He et al., 2020; Muturi 2020). According to the literature, the most prevalent bacterial pathogens that cause mastitis are Staphylococcus aureus, Streptococcus agalactiae, Escherichia coli, Streptococcus dysgalactiae and Streptococcus uberis (Kudi et al., 2009). Among these bacteria, especially Staphylococcus aureus and Escherichia coli, are multidrug resistant and effective in the global spread of antimicrobial resistance (Bessa et al., 2018; Kenar et al., 2017; Kheiri et al., 2016; Saidi et al., 2015).

CONCLUSION

In conclusion, the subject of this study attracts much attention from scientists because it closely concerns human health and nutrition. Although dairy farming has a critical importance in human nutrition, antibiotics used in care, feeding, and herd health practices are an important source of antimicrobial resistance. Thus, this subject forms an important part of a global problem. In this study, the studies revealing the relationship between dairy farming and antimicrobial resistance were examined using the bibliometric perspective. In this regard, this study provides valuable information about the research activities of world countries, scientists and research institutions to combat this problem. Therefore, this study not only provides a detailed analysis of studies about antimicrobial resistance in dairy farming from 1983 to 2023, but also provides a scientific framework for future studies.

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Publication Dates

  • Publication in this collection
    04 Nov 2024
  • Date of issue
    Nov-Dec 2024

History

  • Received
    26 Apr 2024
  • Accepted
    29 Apr 2024
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Universidade Federal de Minas Gerais, Escola de Veterinária Caixa Postal 567, 30123-970 Belo Horizonte MG - Brazil, Tel.: (55 31) 3409-2041, Tel.: (55 31) 3409-2042 - Belo Horizonte - MG - Brazil
E-mail: abmvz.artigo@gmail.com
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