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How do antimicrobial resistance genes spread? ​

Abstract ​

Antimicrobial resistance (AMR) poses a critical challenge to global health, characterized by the ability of microorganisms to resist the effects of drugs that once effectively treated them. This review delves into the mechanisms of antimicrobial resistance gene (ARG) dissemination, focusing on horizontal gene transfer (HGT) as a pivotal process. HGT enables bacteria to acquire resistance genes from other organisms through mechanisms such as conjugation, transformation, and transduction, often facilitated by mobile genetic elements (MGEs) like plasmids, transposons, and integrons. The review also examines environmental factors influencing ARG spread, including wastewater and agricultural runoff, which contribute to the proliferation of resistant bacteria. Furthermore, human activities, particularly antibiotic overuse in healthcare and agriculture, play a significant role in the dissemination of resistance genes. The clinical implications of AMR are profound, leading to increased morbidity, mortality, and economic burdens on healthcare systems. This review highlights the urgent need for improved surveillance and monitoring of ARGs, the development of novel antimicrobials, and the implementation of effective public health policies. Understanding the pathways of ARG dissemination is crucial for developing targeted interventions to combat AMR and safeguard global health.

Outline ​

This report will discuss the following questions.

  • 1 引言
  • 2 Mechanisms of Antimicrobial Resistance Gene Dissemination
    • 2.1 Horizontal Gene Transfer
    • 2.2 Mobile Genetic Elements (Plasmids, Transposons, and Integrons)
    • 2.3 Clonal Spread of Resistant Strains
  • 3 Environmental Factors Influencing ARG Spread
    • 3.1 Role of the Environment in Gene Transfer
    • 3.2 Impact of Wastewater and Agricultural Runoff
    • 3.3 Biofilms and Their Role in Resistance
  • 4 Human Activities and Their Contribution to ARG Spread
    • 4.1 Antibiotic Overuse in Healthcare
    • 4.2 Agricultural Practices and Veterinary Use of Antibiotics
    • 4.3 Global Travel and Trade
  • 5 Clinical Implications of Antimicrobial Resistance
    • 5.1 Impact on Treatment Outcomes
    • 5.2 Economic Burden of AMR
    • 5.3 Strategies for Infection Control
  • 6 Future Directions in AMR Research
    • 6.1 Surveillance and Monitoring of ARGs
    • 6.2 Development of Novel Antimicrobials
    • 6.3 Public Health Policies and Interventions
  • 7 总结

1 Introduction ​

Antimicrobial resistance (AMR) represents one of the most significant public health challenges of our time, characterized by the ability of microorganisms to withstand the effects of drugs that once effectively treated them. The World Health Organization has identified AMR as a critical threat to global health, leading to an estimated five million deaths annually, a figure that surpasses the mortality rates of many infectious diseases [1]. This rising tide of resistance not only complicates treatment regimens but also imposes substantial economic burdens on healthcare systems, with costs estimated at approximately $730 billion per year [1]. The urgency to address this crisis is underscored by the need for a comprehensive understanding of how antimicrobial resistance genes (ARGs) spread across bacterial populations.

The dissemination of ARGs occurs through various mechanisms, with horizontal gene transfer (HGT) playing a pivotal role. HGT enables the transfer of genetic material between bacteria, allowing resistant strains to emerge rapidly and adapt to selective pressures, such as antibiotic use [2][3]. Additionally, mobile genetic elements (MGEs), including plasmids, transposons, and integrons, serve as vectors for the transfer of ARGs, facilitating their spread within and between bacterial species [4][5]. Understanding these mechanisms is crucial for developing effective strategies to combat AMR, as the landscape of resistance is continually evolving in response to environmental and anthropogenic factors.

The significance of studying ARG dissemination extends beyond clinical implications; it encompasses agricultural practices and environmental influences as well. The application of antibiotics in livestock and the improper disposal of pharmaceutical waste contribute to the proliferation of resistant bacteria in the environment [6][7]. Furthermore, human activities, such as global travel and trade, exacerbate the spread of ARGs, creating interconnected reservoirs of resistance that transcend geographical boundaries [1][2].

This review aims to provide a detailed overview of the current understanding of how ARGs spread, organized into several key sections. First, we will explore the mechanisms of ARG dissemination, focusing on HGT, the role of MGEs, and the clonal spread of resistant strains. Next, we will examine environmental factors that influence the spread of ARGs, including the impact of wastewater and agricultural runoff, as well as the role of biofilms. The review will also address the contributions of human activities, particularly antibiotic overuse in healthcare and agriculture, to the dissemination of resistance. Following this, we will discuss the clinical implications of AMR, including its impact on treatment outcomes and the economic burden associated with resistant infections. Finally, we will highlight future directions in AMR research, emphasizing the need for improved surveillance and monitoring of ARGs, the development of novel antimicrobials, and the implementation of effective public health policies.

In conclusion, the fight against AMR requires a multifaceted approach that integrates insights from various disciplines, including microbiology, epidemiology, and public health. By understanding the pathways through which ARGs spread, we can develop targeted interventions to mitigate this growing threat and safeguard global health for future generations.

2 Mechanisms of Antimicrobial Resistance Gene Dissemination ​

2.1 Horizontal Gene Transfer ​

Antimicrobial resistance genes (ARGs) spread primarily through horizontal gene transfer (HGT), a process that allows bacteria to acquire new genetic material from other organisms without the need for reproduction. HGT is a significant mechanism for the dissemination of ARGs, contributing to the rapid evolution of bacterial populations and the emergence of multidrug-resistant strains.

There are several key mechanisms of HGT that facilitate the transfer of ARGs among bacteria:

  1. Conjugation: This is the direct transfer of DNA between two bacteria that are in physical contact, typically through a structure known as a pilus. Conjugative plasmids, which are mobile genetic elements capable of mediating their own transfer, play a crucial role in this process. They can carry ARGs and facilitate their spread across different bacterial species (Shen et al. 2022) [8]. The ability of these plasmids to circumvent host defense systems and compete with other plasmids enhances their transmission potential.

  2. Transformation: This process involves the uptake of free DNA from the environment by a bacterial cell. Bacteria can acquire ARGs that are released into the environment from lysed cells, allowing for the integration of new resistance traits into their genome (Liu et al. 2020) [7].

  3. Transduction: This mechanism is mediated by bacteriophages, which are viruses that infect bacteria. Bacteriophages can inadvertently transfer ARGs from one bacterium to another during the infection process. Recent studies have highlighted the significant role of phage-mediated transduction in the dissemination of ARGs, particularly among foodborne pathogens (Colavecchio et al. 2017) [9]. Phages can carry resistance genes and facilitate their introduction into susceptible bacterial populations, thus enhancing the spread of resistance.

  4. Integrons: These are genetic elements that can capture and express genes, including those conferring antibiotic resistance. Integrons often exist on plasmids or within the bacterial chromosome and can facilitate the co-transfer of multiple resistance genes, thereby contributing to the rapid spread of multidrug resistance (Carattoli 2001) [10].

  5. Environmental Factors: The spread of ARGs can be influenced by various environmental factors, including the presence of antibiotics and non-antibiotic substances that promote HGT. For instance, sub-inhibitory concentrations of antibiotics have been shown to enhance the transfer of resistance genes (Zhu et al. 2023) [11]. Additionally, other non-antibiotic compounds may also facilitate the horizontal transfer of ARGs, although their roles are often underestimated (Zhu et al. 2023) [11].

Overall, the interplay between these mechanisms underlines the complexity of ARG dissemination and highlights the challenges in combating antimicrobial resistance. Understanding these processes is essential for developing effective strategies to mitigate the spread of resistance genes in bacterial populations.

2.2 Mobile Genetic Elements (Plasmids, Transposons, and Integrons) ​

Antimicrobial resistance genes spread primarily through mobile genetic elements (MGEs), which include plasmids, transposons, and integrons. These elements facilitate horizontal gene transfer (HGT) among bacteria, allowing for rapid dissemination of resistance traits across diverse bacterial populations.

Plasmids are key players in the spread of antimicrobial resistance. They are extrachromosomal DNA molecules that can replicate independently and often carry resistance genes. Plasmids can be exchanged between bacteria of the same species and even between different species and genera through mechanisms such as conjugation, transformation, and transduction. For instance, plasmids harboring resistance genes can mobilize other genetic elements, including transposons and integrons, enhancing the spread of resistance traits [4].

Transposons, or "jumping genes," are sequences of DNA that can move from one location to another within the genome, including between plasmids and chromosomal DNA. They can carry resistance genes and facilitate their integration into plasmids or chromosomal locations, thus promoting their dissemination. The movement of transposons is often influenced by environmental factors, such as antibiotic selection pressure, which can enhance the transfer of resistance genes from chromosomes to plasmids, making them more readily transferable [12].

Integrons are another crucial component of the MGE landscape. They are genetic elements that can capture and express gene cassettes, which often contain antibiotic resistance genes. Integrons can exist on plasmids or be associated with other MGEs, enabling them to spread resistance genes through recombination events. The flexibility of integrons allows for the shuffling of resistance gene cassettes, which can lead to the rapid evolution of resistance [13]. Integrons also facilitate the clustering of resistance genes, making it easier for bacteria to acquire multiple resistance traits simultaneously [10].

The mobilome, which encompasses all mobile genetic elements within a microbial population, plays a critical role in the dynamics of antimicrobial resistance. Studies have shown that resistance genes are often located on a variety of plasmid types, with many MGEs being shared across different plasmids, further promoting the dissemination of resistance [14]. The diversity of plasmids and their ability to recombine and integrate with chromosomal DNA or other plasmids contribute significantly to the adaptability of bacteria in the face of antibiotic pressure [15].

In summary, the spread of antimicrobial resistance genes is a multifaceted process driven by mobile genetic elements such as plasmids, transposons, and integrons. These elements enable bacteria to acquire, exchange, and express resistance genes, thereby enhancing their survival and adaptability in various environments, particularly in the presence of antibiotics. Understanding these mechanisms is essential for developing strategies to combat the growing threat of antibiotic resistance in clinical and environmental settings.

2.3 Clonal Spread of Resistant Strains ​

The dissemination of antimicrobial resistance (AMR) genes occurs through various mechanisms, prominently including clonal spread of resistant strains. This process involves the propagation of bacteria that carry resistance genes, which can occur through several modes of transmission.

One of the most significant pathways for the clonal spread of antimicrobial resistance is through the clonal expansion of specific bacterial strains. For instance, the carbapenem-hydrolyzing enzyme Klebsiella pneumoniae carbapenemase (KPC) has spread globally primarily via a single clone, sequence type 258. This clonal spread is facilitated by the ability of the bla(KPC) gene to transfer through multiple mechanisms, including plasmid transfer and clonal dissemination (Adler and Carmeli 2011). The persistence and adaptability of such clones in healthcare settings present a substantial challenge for infection control and treatment.

Moreover, the dynamics of resistance dissemination are closely linked to the selective pressure exerted by antibiotic usage. When antibiotics are prescribed, they create an environment that favors the survival and proliferation of resistant strains, thus accelerating the clonal spread of resistance. This phenomenon is described as a dual evolutionary pathway, where the emergence of resistance through genetic mutations or horizontal gene transfer is followed by the dissemination of these resistant strains (Courvalin 2008). The clonal epidemics, along with the spread of replicons (plasmid epidemics) and resistance determinants (gene epidemics), contribute to an exponential increase in the prevalence of resistant bacteria.

In addition to clonal spread, the mobility of genetic elements such as plasmids plays a crucial role in the dissemination of AMR genes. Conjugative plasmids, which can transfer DNA between bacteria through direct contact, are significant vectors for the horizontal gene transfer that underlies the spread of antimicrobial resistance. The evolutionary mechanisms of these plasmids allow them to evade host defenses and compete effectively within bacterial populations, further enhancing their role in the dissemination of resistance (Shen et al. 2022).

Overall, the interplay between clonal spread and horizontal gene transfer through plasmids underpins the complexity of antimicrobial resistance dissemination. The global nature of this issue necessitates comprehensive monitoring and control strategies to mitigate the impact of resistant strains on public health (O'Brien 1997).

3 Environmental Factors Influencing ARG Spread ​

3.1 Role of the Environment in Gene Transfer ​

Antimicrobial resistance genes (ARGs) spread through various mechanisms, predominantly facilitated by environmental factors that influence horizontal gene transfer (HGT) among bacterial populations. The dissemination of ARGs is a complex process influenced by multiple ecological and anthropogenic factors, as evidenced by recent studies.

One of the primary mechanisms for the spread of ARGs is horizontal gene transfer, which allows for the transfer of genetic material between bacteria, often through mobile genetic elements such as plasmids and transposons. This process is particularly prevalent in environments where bacteria coexist, such as in soil, water, and clinical settings. Environmental factors, including temperature, salinity, and the presence of certain contaminants, significantly affect the efficiency of HGT.

For instance, a systematic review identified that the conjugation efficiency (ce) of antibiotic resistance genes is highly dependent on incubation conditions. Specific antibiotics and metallic compounds, such as nitrofurantoin and mercury (II) chloride, enhance the conjugation process, indicating that the chemical composition of the environment plays a critical role in the transfer of ARGs among bacterial species (Dadeh Amirfard et al., 2024) [16]. Additionally, salinity has been identified as a predominant factor modulating the distribution patterns of ARGs in marine and freshwater ecosystems, suggesting that abiotic factors significantly influence the spread of resistance (Zhang et al., 2019) [17].

The environment also serves as a reservoir for antimicrobial-resistant bacteria and their genes. The presence of resistant microorganisms in natural settings, exacerbated by human activities such as agricultural runoff and improper waste management, facilitates the migration and accumulation of ARGs in various environmental compartments. For example, antibiotic residues from agricultural practices and wastewater can lead to the proliferation of resistant bacteria, which in turn contributes to the dissemination of ARGs into the soil and water systems (Wang et al., 2023) [18].

Furthermore, environmental hotspots, such as wastewater treatment plants and agricultural fields, have been recognized as critical areas for the accumulation and spread of ARGs. These hotspots create conditions that favor the exchange of resistance genes among diverse bacterial populations, leading to the emergence of multidrug-resistant pathogens (Kunhikannan et al., 2021) [19].

The interplay between various environmental factors and the dynamics of microbial communities further complicates the spread of ARGs. Factors such as pollution, nutrient availability, and microbial diversity contribute to the selection pressures that promote the survival and proliferation of resistant strains (Bengtsson-Palme et al., 2018) [20]. For example, environmental contaminants like bisphenols have been shown to enhance the conjugative transfer of ARGs among bacteria, indicating that chemical exposure can facilitate genetic exchange even in the presence of sub-lethal concentrations (Xiong et al., 2024) [21].

In summary, the spread of antimicrobial resistance genes is significantly influenced by environmental factors that facilitate horizontal gene transfer and create conducive conditions for the proliferation of resistant bacteria. Understanding these dynamics is crucial for developing effective strategies to combat the growing threat of antimicrobial resistance.

3.2 Impact of Wastewater and Agricultural Runoff ​

Antimicrobial resistance genes (ARGs) spread through various environmental factors, particularly influenced by wastewater and agricultural runoff. The environment serves as a critical reservoir and transmission pathway for ARGs, significantly contributing to the global public health crisis associated with antimicrobial resistance (AMR).

Wastewater treatment plants (WWTPs) have been identified as significant sources of ARGs. They act as hotspots for the dissemination of resistance genes into aquatic environments. For instance, a study demonstrated that untreated wastewater influents contained a high diversity and abundance of ARGs, which were subsequently reduced by approximately 87% in the treated effluent. However, even after treatment, the effluents significantly increased the ARG abundance in the receiving rivers, with an average increase of 543% from upstream to downstream sediments [22]. This indicates that while WWTPs can reduce the levels of ARGs, they still play a role in spreading these genes into the environment.

Agricultural practices also contribute substantially to the spread of ARGs. The application of manure from livestock treated with antibiotics introduces sub-therapeutic levels of antibiotics and resistant bacteria into soil and water systems. This practice fosters the selection and horizontal transfer of resistance genes among microbial communities. Specifically, studies have shown that agricultural runoff from areas using antibiotics can lead to increased abundance and diversity of ARGs in nearby water bodies [23][24]. For example, a study in the Lake Tai Basin revealed that orchard runoffs contained a more diverse array of ARGs compared to traditional cropland runoffs, highlighting the impact of different agricultural practices on the environmental resistome [25].

The mechanisms facilitating the spread of ARGs in the environment include horizontal gene transfer (HGT), which occurs through various means such as plasmids, integrons, and transposons. Bacteriophages also play a role in mediating the transfer of resistance genes among bacteria in environmental settings [26]. This horizontal transfer is particularly effective in environments like soils and sediments, where microbial communities can interact and exchange genetic material.

Furthermore, environmental factors such as salinity, pollution, and the presence of co-selective agents like heavy metals and microplastics can exacerbate the spread of ARGs. These factors create conditions that favor the persistence and dissemination of resistance genes across ecological and geographical boundaries [27].

In summary, the spread of antimicrobial resistance genes is significantly influenced by environmental factors, particularly through the mechanisms of wastewater discharge and agricultural runoff. The interactions between resistant bacteria and their environments, coupled with anthropogenic activities, underscore the urgent need for integrated surveillance and mitigation strategies to combat the rise of AMR in both human and environmental health contexts.

3.3 Biofilms and Their Role in Resistance ​

Antimicrobial resistance genes (ARGs) spread through various mechanisms, with biofilms playing a significant role in this process. Biofilms are structured communities of microorganisms embedded in a self-produced extracellular matrix, which can serve as reservoirs for ARGs and facilitate their dissemination.

Biofilms enhance the spread of ARGs through several key mechanisms. Firstly, they provide a protective environment that allows bacteria to survive in the presence of antibiotics, thereby promoting the persistence of resistant strains. The dense cellular structure of biofilms increases the likelihood of horizontal gene transfer (HGT), which is the primary mode of ARG dissemination. Studies indicate that HGT occurs more frequently in biofilms than in planktonic cultures, with mechanisms such as transformation, transduction, and conjugation being particularly effective in these communities[28].

Moreover, biofilms are often hotspots for the transfer of ARGs due to the high population density and proximity of bacterial cells. This close association facilitates genetic exchange among different bacterial species, enabling the rapid spread of resistance traits. Environmental factors, such as the presence of pollutants and nutrients, can influence biofilm formation and stability, further affecting the dynamics of ARG dissemination[29].

The ecological context of biofilms is crucial; they can develop in various environments, including wastewater systems, which are often rich in nutrients and pollutants. For instance, biofilms formed in wastewater can harbor a diverse array of ARGs, posing significant risks for public health, especially in vulnerable communities with limited access to healthcare[30]. Additionally, biofilms can interact with mobile genetic elements (MGEs), which can carry ARGs and facilitate their transfer between bacteria[28].

Furthermore, the role of environmental stressors cannot be overlooked. Factors such as antibiotic exposure, heavy metals, and biocides can induce stress responses in bacteria, which may enhance their capacity to acquire and transfer ARGs. For example, exposure to biocides like polyhexamethylene biguanide (PHMB) has been shown to promote adaptive cross-resistance to antibiotics in biofilms, indicating that biocides may inadvertently select for resistant phenotypes[31].

In conclusion, biofilms are critical in the spread of antimicrobial resistance genes due to their structural properties, the high likelihood of horizontal gene transfer, and the influence of environmental factors. Addressing the challenges posed by biofilms in the context of antimicrobial resistance requires a multifaceted approach, including improved monitoring of biofilm-associated ARGs in various environments and the development of strategies to mitigate their impact on public health[1][29].

4 Human Activities and Their Contribution to ARG Spread ​

4.1 Antibiotic Overuse in Healthcare ​

Antimicrobial resistance genes (ARGs) spread through various mechanisms, significantly influenced by human activities, particularly the overuse of antibiotics in healthcare settings. The dissemination of ARGs can occur via vertical gene transfer, which involves the transmission of genetic material from parent to offspring, and horizontal gene transfer (HGT), which encompasses transformation, transduction, and conjugation. These processes enable bacteria to acquire resistance genes from other bacterial strains, thereby contributing to the emergence of multidrug-resistant organisms (MDROs) (Nadeem et al., 2020; Dzidic & Bedeković, 2003).

The selective pressure exerted by the extensive use of antibiotics in clinical environments, such as hospitals, is a primary driver of this phenomenon. In intensive care units (ICUs) and among immunocompromised patients, the frequent administration of antimicrobials leads to the selection of MDROs, including methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococci (VRE) (Dzidic & Bedeković, 2003). The misuse of antibiotics, such as prescribing them for viral infections or inappropriate dosages, further exacerbates this issue, allowing susceptible bacteria to be outcompeted by resistant strains.

Environmental factors also play a critical role in the spread of ARGs. The gut microbiota, which harbors a diverse array of bacteria, serves as a reservoir for resistance genes. Horizontal gene transfer is frequent in the gut, allowing for the mobilization of ARGs among commensal and pathogenic bacteria (van Schaik, 2015). Furthermore, the discharge of antibiotic residues from healthcare facilities into the environment creates hotspots for ARGs, where high bacterial densities facilitate genetic exchange (Mann et al., 2021; Ahmad et al., 2021).

In addition to direct healthcare practices, the agricultural sector contributes to the spread of ARGs through the use of antibiotics in livestock and crop production. The runoff from agricultural practices and wastewater treatment plants introduces resistant bacteria and their genes into the environment, which can then be transferred to human pathogens (Iwu et al., 2020; Kunhikannan et al., 2021). This interconnectedness between human health, agriculture, and the environment underscores the complexity of combating antimicrobial resistance.

In summary, the spread of antimicrobial resistance genes is a multifaceted issue driven by the overuse of antibiotics in healthcare, environmental factors, and the interconnectedness of various ecosystems. The continuous emergence of MDROs necessitates stringent measures to regulate antibiotic use and implement effective infection control practices to mitigate the transmission of ARGs (Cheng et al., 2015; Pillay et al., 2022).

4.2 Agricultural Practices and Veterinary Use of Antibiotics ​

Antimicrobial resistance genes (ARGs) spread through a variety of mechanisms, significantly influenced by human activities, particularly in the agricultural and veterinary sectors. The misuse and overuse of antibiotics in these fields create selective pressures that promote the proliferation of antibiotic-resistant bacteria (ARB) and their associated resistance genes.

One of the primary contributors to the spread of ARGs is the extensive use of antibiotics in livestock. According to research, a substantial portion of antibiotics used globally is for veterinary purposes, where they are administered not only for therapeutic reasons but also as growth promoters in food animals. This practice creates a conducive environment for the selection of antibiotic-resistant bacteria within the gut microbiome of these animals. When these bacteria are excreted, they can contaminate the environment through manure application on agricultural land, leading to the dissemination of ARGs into the soil and water systems (Teuber 2001; Khachatourians 1998; Vidovic 2020) [32][33][34].

The application of manure, which may contain high concentrations of ARB and ARGs, serves as a significant route for the transmission of resistance from livestock to crops and subsequently to humans. Continuous manure application has been shown to affect the environmental microbiome and resistome, thereby enhancing the potential for ARG enrichment and persistence in agricultural ecosystems (Tyrrell et al. 2019; Checcucci et al. 2020) [6][35].

In addition to direct contamination through manure, horizontal gene transfer (HGT) plays a crucial role in the dissemination of ARGs. Bacteria can acquire resistance genes from other bacteria through mechanisms such as transformation, transduction, and conjugation. The agricultural environment, especially where antibiotics are used, provides numerous opportunities for these gene transfer events to occur. The presence of mobile genetic elements (MGEs) facilitates the horizontal transfer of ARGs among diverse bacterial populations, including pathogens and commensal bacteria (Baker et al. 2016; Zhang et al. 2023) [36][37].

Furthermore, the environmental impact of antibiotics and their residues contributes to the persistence and spread of resistance genes. Antibiotic residues can enter soil, water, and sediments through various routes, including agricultural runoff and wastewater discharge from medical and veterinary practices. These residues not only promote the selection of resistant strains but also can directly contribute to the environmental reservoir of ARGs (Samreen et al. 2021) [24].

The interconnectedness of human, animal, and environmental health emphasizes the importance of a One Health approach in combating the spread of antimicrobial resistance. This strategy advocates for interdisciplinary collaboration to monitor and manage antibiotic use and resistance across all sectors (Horodyska et al. 2025) [38].

In conclusion, the spread of antimicrobial resistance genes is a multifaceted issue driven by agricultural practices, veterinary antibiotic use, and the environmental conditions that facilitate gene transfer. Addressing this challenge requires targeted surveillance, responsible antibiotic usage, and a comprehensive understanding of the mechanisms underlying ARG dissemination to mitigate its impact on public health.

4.3 Global Travel and Trade ​

Antimicrobial resistance genes (ARGs) spread through various mechanisms influenced significantly by human activities, particularly in the contexts of global travel and trade. The dissemination of ARGs is primarily facilitated by horizontal gene transfer (HGT), where genetic material is transferred between bacteria, enabling the rapid spread of resistance traits. This process is exacerbated by the inappropriate and excessive use of antibiotics in healthcare, agriculture, and veterinary practices, which creates selective pressures that favor the survival and proliferation of resistant strains [24].

Travel and migration play critical roles in the international spread of antimicrobial resistance. When individuals travel, they can carry resistant bacteria or ARGs back to their home countries, contributing to local resistance patterns. A study indicated that international travelers experienced an increase in antimicrobial resistance genes, particularly Escherichia species, within their gut microbiota without significantly affecting microbial diversity [39]. This suggests that the act of traveling can facilitate the introduction of ARGs into new environments, where they may persist and spread.

Trade, especially the international exchange of food products and animals, also contributes to the transmission of resistant pathogens. Bacteria with ARGs can be transmitted through food products, and resistant genes can spread from commensal bacteria to pathogens, complicating the quantification of transmission routes [40]. The global food supply chain, characterized by intensive use of antibiotics in livestock, is a significant driver of resistance emergence and spread. The review highlights that the main transmission route from food animals to humans is via food products, but direct contact and environmental pathways also contribute [40].

Moreover, socioeconomic factors and environmental conditions, such as sanitation infrastructure and population density, can influence the dynamics of ARG dissemination. In low to middle-income countries (LMICs), where sanitation may be poor and antibiotic use is increasing, the risk of ARG spread is heightened [41]. The environmental context plays a crucial role in how ARGs are retained and transmitted, as resistant bacteria and genes can persist in various environmental reservoirs, including soil, water, and sediments [24].

In summary, the spread of antimicrobial resistance genes is a multifaceted issue driven by human activities, including global travel and trade. The combination of HGT, environmental factors, and the selective pressures imposed by antibiotic use creates a complex landscape for the dissemination of ARGs, necessitating comprehensive surveillance and intervention strategies to mitigate their impact on public health.

5 Clinical Implications of Antimicrobial Resistance ​

5.1 Impact on Treatment Outcomes ​

The spread of antimicrobial resistance genes (ARGs) is a complex process influenced by various mechanisms, with significant implications for clinical treatment outcomes. The dissemination of ARGs occurs primarily through horizontal gene transfer (HGT), which includes several mechanisms such as conjugation, transformation, and transduction.

Conjugation is widely recognized as a major mechanism for the transfer of resistance genes among bacteria. It involves direct cell-to-cell contact, allowing the transfer of plasmids that often carry multiple resistance genes. This method is particularly concerning because it enables the rapid spread of resistance traits within bacterial populations, including between pathogenic and commensal bacteria [42].

Transformation and transduction also contribute to the spread of ARGs. Transformation involves the uptake of free DNA from the environment by a bacterial cell, while transduction is mediated by bacteriophages that can introduce resistance genes into bacterial genomes. Although these mechanisms have been deemed less significant compared to conjugation, recent studies suggest that their roles may be more substantial than previously understood [42].

Environmental factors play a critical role in the dissemination of ARGs. The use of antibiotics in agriculture, for instance, creates selective pressure that promotes the survival and proliferation of resistant strains. Additionally, wastewater treatment plants, soil, and manure are identified as significant reservoirs for ARGs, facilitating their transfer to human pathogens [43]. The presence of mobile genetic elements (MGEs) further enhances the ability of bacteria to acquire and disseminate resistance genes, creating a loop of transmission between the environment, animals, and humans [43].

The clinical implications of the spread of ARGs are profound. The emergence of multidrug-resistant bacteria leads to increased morbidity and mortality rates, as well as clinical challenges in treating infections. The development of new antimicrobial agents has slowed, and the existing antibiotics are becoming less effective due to the rapid evolution of resistance [2]. This situation necessitates urgent strategies to combat the spread of resistance, including improved stewardship of antibiotic use, surveillance of resistance patterns, and the development of novel therapeutic approaches [2].

Understanding the mechanisms behind the dissemination of ARGs is crucial for informing clinical practice. Clinicians must be aware of the genetic and biochemical pathways that contribute to antimicrobial resistance to make informed treatment decisions. This knowledge can lead to the implementation of strategies such as de-escalation of broad-spectrum antibiotics, targeted therapies, and combination treatments that may improve patient outcomes and reduce the risk of resistance [44].

In summary, the spread of antimicrobial resistance genes through horizontal gene transfer and environmental reservoirs poses significant challenges to public health and clinical outcomes. Addressing this issue requires a multifaceted approach that combines scientific research, clinical awareness, and responsible antibiotic use to mitigate the impact of antimicrobial resistance on treatment outcomes.

5.2 Economic Burden of AMR ​

Antimicrobial resistance (AMR) genes spread primarily through horizontal gene transfer (HGT) mechanisms, which facilitate the exchange of genetic material between bacteria, thereby promoting the dissemination of resistance traits. This phenomenon is particularly significant in the context of the interconnected microbiomes and resistomes present in various environments, including human, animal, and ecological systems.

The mechanisms underlying the spread of AMR genes include:

  1. Horizontal Gene Transfer: HGT is the predominant mode through which antimicrobial resistance genes (ARGs) are disseminated among bacterial populations. This process can occur via several mechanisms, including transformation, transduction, and conjugation. For instance, plasmids, which are mobile genetic elements, play a crucial role in carrying and transferring resistance genes across different bacterial species and genera. These plasmids can exchange genetic material not only within the same species but also between diverse bacterial groups, thus amplifying the spread of resistance traits (Schwarz et al., 2014)[4].

  2. Environmental Reservoirs: The environmental reservoirs, such as soil and water systems, serve as significant sources for the acquisition of ARGs by pathogenic bacteria. Studies have shown that the presence of antibiotic residues in these environments can enhance the selective pressure on bacteria, facilitating the transfer of resistance genes. For example, the application of livestock manure, which often contains ARB and ARGs, to agricultural fields is a recognized pathway for the dissemination of resistance genes into the soil-water system (Checcucci et al., 2020)[6].

  3. Conjugative Plasmids as Dissemination Vectors: Research indicates that conjugative plasmids are the primary vectors for the dissemination of ARGs. These plasmids can carry multiple resistance genes and facilitate their spread from one bacterium to another through direct cell-to-cell contact (Sánchez-Osuna et al., 2023)[2]. The degree of dissemination often correlates with the resistance mechanism involved, suggesting that certain mechanisms may be more prone to spread than others.

  4. Role of Mobile Genetic Elements: Mobile genetic elements (MGEs), such as transposons and integrons, are integral to the mobility of ARGs. They can facilitate the incorporation of resistance genes into plasmids or chromosomal DNA, thus enhancing their stability and persistence within bacterial populations (Cross et al., 2025)[5]. The interplay between MGEs and ARGs is crucial for understanding the dynamics of resistance dissemination.

  5. Impact of Antibiotic Use: The patterns of antibiotic use, particularly in agricultural and clinical settings, significantly influence the dissemination of AMR genes. Increased antibiotic usage creates selective pressures that favor the survival of resistant strains, which can then spread their resistance traits through HGT (Vikesland et al., 2019)[41]. In low- and middle-income countries (LMICs), the rising use of antibiotics, often coupled with inadequate sanitation practices, exacerbates the problem of AMR dissemination (Pehrsson et al., 2016)[45].

In conclusion, the spread of antimicrobial resistance genes is a multifaceted process influenced by various biological, environmental, and socioeconomic factors. Understanding these dynamics is critical for developing effective surveillance and control strategies to mitigate the impact of AMR on public health and the economy. The economic burden of AMR is substantial, as it leads to increased healthcare costs, prolonged hospital stays, and a higher incidence of morbidity and mortality associated with resistant infections (Despotovic et al., 2023)[3]. Thus, addressing the spread of AMR genes is essential for both clinical and economic considerations in public health.

5.3 Strategies for Infection Control ​

Antimicrobial resistance (AMR) genes spread primarily through horizontal gene transfer (HGT), which allows bacteria to acquire resistance genes from other bacteria. This process can occur via several mechanisms, including conjugation, transformation, and transduction. Conjugation is particularly significant, as it involves the direct transfer of DNA between bacteria through physical contact, often mediated by plasmids, which are mobile genetic elements that can carry multiple resistance genes [8].

The dissemination of AMR genes is facilitated by various environmental factors. For instance, areas with strong anthropogenic pressures, such as hospitals, pharmaceutical industries, and agricultural practices, are hotspots for the accumulation and spread of antibiotic resistance genes (ARGs) [46]. The selective pressure exerted by the use of antibiotics in these environments accelerates the evolution of resistant strains, making them more likely to survive and proliferate [3].

In addition to anthropogenic influences, natural reservoirs such as animal guts, wastewater treatment plants, and agricultural runoff also play a critical role in the spread of AMR genes. These environments often harbor a high density of bacteria, phages, and plasmids, which facilitate significant genetic exchange and recombination [46]. The presence of mobile genetic elements (MGEs) further enhances the spread of resistance genes, as they can easily transfer between different bacterial species [5].

The consequences of AMR are profound, contributing to nearly five million deaths annually and imposing a significant economic burden, estimated at approximately $730 billion per year [1]. To mitigate the spread of AMR, a multifaceted approach is required. This includes the implementation of robust infection control measures, such as antimicrobial stewardship programs that promote the rational use of antibiotics, as well as education initiatives aimed at healthcare providers and the general public [1].

Furthermore, innovative technologies such as genomic surveillance and predictive modeling can provide valuable insights into the dynamics of AMR dissemination, enabling more effective tracking and management of resistance patterns [1]. By understanding the complex interplay between human, animal, and environmental health within the One Health framework, strategies can be developed to address the challenges posed by antimicrobial resistance more effectively [3].

In conclusion, the spread of antimicrobial resistance genes is a multifactorial issue driven by horizontal gene transfer, environmental pressures, and human activities. Effective infection control strategies must encompass a broad range of interventions, including improved antibiotic use, public education, and advanced monitoring techniques to curb the ongoing threat of AMR.

6 Future Directions in AMR Research ​

6.1 Surveillance and Monitoring of ARGs ​

Antimicrobial resistance genes (ARGs) spread through various mechanisms, with horizontal gene transfer (HGT) being a primary driver. HGT allows for the rapid dissemination of ARGs among bacterial populations, facilitated by mobile genetic elements (MGEs) such as plasmids, transposons, and integrons. These MGEs enable the transfer of genetic material not only within the same species but also across different species and genera, significantly enhancing the genetic diversity of resistance traits within microbial communities[3][5][47].

The movement of ARGs can occur via several mechanisms of HGT, including conjugation, transformation, and transduction. Conjugation involves direct cell-to-cell contact, often mediated by plasmids that carry ARGs. Transformation refers to the uptake of free DNA from the environment by competent bacteria, while transduction involves the transfer of DNA through bacteriophages. The ecological implications of these processes are profound, as they can lead to the emergence of multidrug-resistant pathogens, complicating treatment options for infections[3][38].

Surveillance and monitoring of ARGs are crucial for understanding their spread and for developing strategies to combat antimicrobial resistance (AMR). Effective surveillance systems can help identify hotspots of resistance, track the movement of ARGs in various environments, and assess the impact of different reservoirs, including human, animal, and environmental sources. The One Health approach, which integrates human, animal, and environmental health, is vital in mapping the resistome and understanding the complex interactions that contribute to the dissemination of ARGs[3][5].

Recent studies emphasize the importance of characterizing the genetic contexts surrounding ARGs to understand their transmission dynamics better. By combining genomic information with knowledge of biological processes, researchers can draw more accurate conclusions about the pathways through which ARGs spread. This includes the analysis of bacterial genome sequences to extract information about MGE associations, which is crucial for elucidating the mechanisms of ARG dissemination[5][47].

Moreover, targeted surveillance strategies are necessary to monitor the presence and abundance of ARGs in various environments, such as agricultural settings, wastewater treatment plants, and clinical settings. This monitoring can inform public health interventions and guide antibiotic stewardship efforts aimed at reducing the selection pressure that drives the spread of resistance[24][48].

In summary, the spread of antimicrobial resistance genes is a multifaceted issue that requires comprehensive surveillance and monitoring strategies to mitigate its impact on public health. Understanding the mechanisms of HGT and the role of different reservoirs in the dissemination of ARGs will be critical for developing effective interventions to combat AMR in the future[3][5][47].

6.2 Development of Novel Antimicrobials ​

Antimicrobial resistance genes (ARGs) spread through several mechanisms, primarily via horizontal gene transfer (HGT) and vertical gene transfer (VGT). HGT involves the transfer of genetic material between organisms, allowing for the rapid dissemination of resistance traits across different bacterial species. This process is facilitated by mobile genetic elements (MGEs), such as plasmids, transposons, and bacteriophages, which can carry ARGs and facilitate their movement between bacteria, including both pathogenic and non-pathogenic strains.

In particular, plasmids have been identified as significant vectors for the dissemination of ARGs. They can replicate independently of the bacterial chromosome and can be transferred between bacteria through processes such as conjugation, transformation, and transduction. The prevalence of ARGs on plasmids enhances the likelihood of multiple resistance traits being co-transferred, leading to the emergence of multi-drug resistant strains [2].

The dynamics of ARG dissemination are influenced by various factors, including environmental conditions, anthropogenic activities, and the genetic characteristics of the bacteria involved. For instance, antibiotic use in clinical settings and agriculture creates selective pressure that promotes the survival and proliferation of resistant strains. Areas with high concentrations of antibiotics, such as hospitals and farms, are recognized as hotspots for the emergence and spread of resistance genes [49].

In addition to the mechanisms of transfer, the genetic context of ARGs is crucial for understanding their spread. The association of ARGs with specific MGEs can affect their expression and stability within bacterial populations. Characterizing these associations through genomic approaches can provide insights into the pathways of resistance dissemination and inform strategies for monitoring and controlling ARG spread [5].

Future directions in antimicrobial resistance research should focus on developing novel antimicrobials that can effectively combat resistant strains. This includes exploring alternative therapeutic strategies, understanding the interactions between bacteria and their resistomes in various environments, and improving surveillance systems to track the emergence and spread of ARGs. By integrating knowledge from genomic studies and ecological perspectives, researchers can devise more effective interventions to mitigate the impact of antimicrobial resistance on public health [6].

6.3 Public Health Policies and Interventions ​

Antimicrobial resistance (AMR) genes spread through various mechanisms, primarily through horizontal gene transfer (HGT) and vertical gene transfer (VGT). HGT allows for the direct transfer of resistance genes between bacteria, which can occur via several mobile genetic elements (MGEs) such as plasmids, transposons, and integrons. These MGEs facilitate the movement of resistance genes across different bacterial species, significantly contributing to the dissemination of antimicrobial resistance across diverse environments.

Research has shown that the dissemination of antimicrobial resistance genes is influenced by environmental factors, including the presence of antibiotics and the physical and socio-economic conditions of specific regions. For instance, in low-income countries (LMICs), high population densities, inadequate sanitation infrastructure, and poor waste disposal practices create conditions that favor the spread of antibiotic-resistant bacteria (ARB) and antibiotic resistance genes (ARGs) [41]. The interconnectedness of human, animal, and environmental reservoirs in the One Health framework underscores the complexity of AMR dynamics and highlights the need for comprehensive surveillance and intervention strategies [3].

Recent studies have identified that certain habitats, such as human feces, serve as significant reservoirs for the global resistome, with around 85% of resistance genes being transmitted from external environments to humans [50]. This transmission occurs through various routes, including contact with contaminated water, air, and soil. The effectiveness of resistance gene transfer can also vary depending on the specific characteristics of the resistance genes and the bacteria involved, as well as the environmental conditions that facilitate or hinder gene transfer [2].

In terms of public health policies and interventions, it is crucial to adopt a One Health approach that integrates efforts across human health, animal health, and environmental sectors. This approach can help in mapping the resistome and understanding the epidemiology of AMR [3]. Effective monitoring systems are necessary to track the spread of AMR, particularly in environments where resistance genes are likely to proliferate, such as agricultural settings where livestock manure is used [6]. Additionally, implementing robust sanitation practices and antibiotic stewardship programs can significantly reduce the selection pressure that drives the emergence and spread of AMR [51].

Overall, future directions in AMR research should focus on elucidating the mechanisms of gene transfer, understanding the ecological and environmental factors that influence the spread of resistance, and developing targeted public health interventions that can mitigate the impact of AMR on global health. Enhanced surveillance and localized strategies will be essential in addressing the complexities of AMR dissemination in diverse settings.

7 Conclusion ​

The findings presented in this review underscore the multifaceted nature of antimicrobial resistance (AMR) gene dissemination, highlighting the complex interplay between horizontal gene transfer (HGT), mobile genetic elements (MGEs), and environmental factors. The significant role of HGT mechanisms such as conjugation, transformation, and transduction illustrates how rapidly ARGs can spread among bacterial populations, leading to the emergence of multidrug-resistant organisms. Furthermore, the impact of human activities, particularly antibiotic overuse in healthcare and agriculture, along with environmental reservoirs, exacerbates the challenge of AMR. The review emphasizes the urgent need for comprehensive surveillance and monitoring strategies to track the movement of ARGs and develop targeted interventions to mitigate their spread. Future research should focus on understanding the genetic contexts of ARGs, improving antibiotic stewardship, and implementing effective public health policies that address the interconnectedness of human, animal, and environmental health. By adopting a One Health approach, we can enhance our ability to combat the growing threat of AMR and protect global health for future generations.

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