Abstract
Antimicrobial resistance (AMR) has emerged as a critical public health threat and one of the most complicated global challenges due to its multi-faceted nature. In addition to health burden, AMR also drives up healthcare costs and imposes substantial indirect economic impacts. Despite the ongoing global efforts, the burden of drug-resistant infections is still growing and alarming. Although AMR has been well addressed pertaining to human health, AMR linked to pathogens in other pillars of the food chain has been a hidden menace and a growing public health concern. AMR may arise in the food chain through various pathways, with foodborne drug-resistant pathogens being reported in the literature. Tackling and combatting AMR in the food chain requires a multi-faceted comprehensive approach under the One Health umbrella. This approach is crucial not only to protect public health but also to ensure the sustainability and safety of all components of the food chain.
Keywords: Antimicrobial resistance, Food chain, One Health, Jordan, Eastern Mediterranean Region
1. Introduction
Antimicrobial resisteance (AMR) has emerged as a critical global public health threat and one of the most complicated global challenges due to its multi-faceted nature. In addition to health burden, AMR also drives up healthcare costs and imposes substantial indirect economic burdens. AMR leads to a substantial health burden as revealed by a recent study published in The Lancet [1]. The study estimated that 1.14 million deaths were directly attributed to bacterial AMR globally in 2021, and this burden was forecasted to reach 1.91 million deaths by 2050 [1]. The significance of AMR was officially recognized in 2016 at the UN General Assembly's high-level meeting on AMR, which called on countries to commit to implementing their National Action Plans (NAPs) on AMR [2]. Despite the ongoing efforts, the burden of drug-resistant infections is still alarming.
Rethinking AMR from a One Health perspective emphasizes the interconnectedness of human, animal, and environmental health [3], particularly within the food chain. Although AMR has been well addressed pertaining to human health, AMR linked to pathogens in the other pillars of the food chain has been a hidden menace and a growing public health concern which can result in detrimental impacts. For instance, drug-resistant foodborne bacteria have been previously reported in the literature such as Staphylococcus aureus, Escherichia coli, Salmonella spp., and Listeria spp. [4], nevertheless, there is a lack of knowledge regarding AMR in the food chain and the complex interactions that drive its emergence in limited-resources settings.
In this global context, Jordan represents a critical and underexplored setting for investigating AMR through a One Health lens. Jordan faces multiple pressures that heighten AMR risk, including rapid urbanization, increased food production demands, intensive animal farming practices, and limited regulatory enforcement on antimicrobial use across sectors. Furthermore, Jordan's geopolitical context, characterized by its proximity to neighbouring countries experiencing political instability, armed conflicts, weakened healthcare infrastructures, and large-scale displacement of refugees [[5], [6], [7]], significantly exacerbates the complexity of AMR transmission and management at the national level. Despite national efforts to implement the NAP on AMR, significant challenges persist in achieving coordinated action among human health, veterinary, agricultural, and environmental sectors.
This paper aims to: (1) explore the potential pathways through which AMR emerges and is transmitted within the food chain; (2) critically review the current status of AMR across the food chain in Jordan; (3) propose a conceptual model for AMR mitigation informed by systems thinking approach; (4) examine the roles and responsibilities of key sectors in implementing One Health AMR strategy along with in depth analysis of the current situation; and (5) offer targeted recommendations to strengthen Jordan's national AMR response within a One Health framework, with a particular focus on strategic guidance for policymakers.
2. AMR in the food chain: potential pathways for emergence and transmission
AMR may arise in the food chain through various pathways, particularly involving the use of antimicrobials in agriculture. Antibiotics are often administered to livestock for therapeutic purposes or as growth promoters, which can result in resistant pathogens [8]. These resistant pathogens can then be transmitted to humans through the food chain. Moreover, animal feces containing antimicrobial-resistant pathogens can contaminate soil and water sources used for crop irrigation, leading to the colonization of plant surfaces by these resistant organisms [9]. Consumption of contaminated food is a significant avenue for disseminating antimicrobial-resistant pathogens to humans [9], with animal-derived foods, particularly those from domestic livestock, regarded as one of the main sources of transmission of resistant bacteria [10].
For example, transmission of drug-resistant Salmonella spp. was reported with great alarm in Turkey [11], and drug-resistant genes in ruminants [12,13]. Additionally, several studies hypothesized a significant emergence of drug-resistant bacteria in aquaculture farms due to high rates of genetic exchange [14,15].
Additionally, the scope of AMR in the food chain is not restricted to poultry and livestock pathogens but it also covers contaminated vegetables and grains. Around ten percent of foodborne outbreaks in the last decades were attributed to the transmission of multi-drug resistant (MDR) E. coli through contaminated grains and legumes, as well as MDR Salmonella spp. through contaminated tomatoes, melons, leafy green, and stem vegetables [16]. Moreover, dust from livestock farms and production manufacture is considered an important route for the spread of MDR bacteria such as methicillin-resistant Staphylococcus aureus (MRSA), coliforms, and β-lactamase-Enterobacteriaceae [11]. Also, food handlers may play a role in spreading drug-resistant bacteria through breaching the standards of proper hygienic practices [17]. Concerning water sources, drug-resistant pathogens, mobile genetic elements of drug-resistant bacteria, and antibiotic residues that negatively impact human health, crops, animals, and the environment were also reported in the literature [18].
To better understand the possible pathways of the emergence of AMR in the food chain, Fig. 1 depicts the complex interactions involving the key components, relationships, and pathways through which AMR may emerge.
Fig. 1.
Possible pathways of emergence of antimicrobial resistance (AMR) in the food chain.
3. AMR in the food chain: insights into the situation in Jordan
3.1. National commitment to combat AMR
Jordan is a middle-income country located in the Eastern Mediterranean Region with a population count of 11.7 million [19]. In response to the global call to combat AMR, Jordan took serious actions started in 2017 by forming a multi-sectoral national committee to combat AMR. Afterwards, Jordan's NAP on AMR was developed in accordance with Global Action Plan (GAP) on AMR [20]. Since then, immense multi-sectoral efforts have been invested to tackle and reduce the burden of AMR in the country [21]. Additionally, Jordan established its national AMR surveillance system with eight surveillance sites in 2018. As of 2024, the system had expanded to encompass 42 surveillance sites distributed across all 12 governorates. Notably, 17 surveillance sites are in the capital, Amman. This expansion demonstrates a significant national effort to enhance AMR monitoring capacity. Also, a comprehensive monitoring and evaluation framework was also developed and institutionalized at Jordan Center for Disease Control (JCDC) to systematically assess the progress of national efforts in combating this public health threat [22]. This framework includes clearly defined indicators to track the implementation of interventions across relevant sectors. It enables continuous assessment of both short-term outputs and long-term outcomes, ensuring that NAP strategic goals are being met effectively. Regular evaluations are conducted to identify gaps, inform policy adjustments, and guide resource allocation, with an emphasis on fostering accountability and promoting evidence-based decision-making.
3.2. National AMR surveillance findings
In 2023, a total of 59,535 non-duplicate diagnostic isolates from patients were collected for analysis from the 42 surveillance sites. The most identified organism was E. coli (25,683 isolates), followed by S. aureus (7577 isolates), Klebsiella pneumoniae (6467 isolates), and Pseudomonas aeruginosa (2676 isolates). Altogether, these priority pathogens represented 71.2 % of all isolates reported during the surveillance period [23]. More details are provided in Fig. 2.
Fig. 2.
Antimicrobial resistance (AMR) priority pathogens in Jordan. Raw data were extracted from Jordan's Surveillance of Antimicrobial Resistance Annual Report 2023 which can be accessed at https://www.moh.gov.jo/Default/En.
Approximately 40.0 % of E. coli isolates were identified as MDR, with an additional 15.0 % displaying characteristics suggestive of possible extensive drug resistance (XDR). For K. pneumoniae, 44.0 % of isolates were classified as MDR, and 24.0 % were considered possible XDR. Among P. aeruginosa isolates, 20.0 % were MDR, while 18.0 % with possible XDR. In S. aureus isolates, 41.0 % were MDR, and 5.0 % were categorized as possible XDR [23].
3.3. Drug-resistant pathogens in the food production sector and water sources
At the national level, several cases of drug-resistant bacteria were reported in the food chain including poultry [24], dairy cattle industry [25], as well as drinking and irrigation water [26], as illustrated in Fig. 3.
Fig. 3.
Drug-resistant bacteria in the food chain in Jordan. Created in BioRender https://BioRender.com/xhoj0z0.
In Jordan, multiple studies revealed that E. coli with high rate of drug-resistance was isolated from more than half of broiler chickens with signs and symptoms of infection [24], and dairy cattle with enteritis, metritis, and mastitis [25,27]. MRSA was detected in bulk milk tanks from nationwide cattle, sheep, and goat dairy farms. All MRSA isolates were resistant to cefoxitin, oxacillin, and penicillin [25]. E. coli, S. aureus, coagulase-negative Staphylococci, and Streptococcus non-agalactiae with sulfamethoxazole-trimethoprim and penicillin resistance were the most predominant isolates from bovine mastitis during 2002–2006 [27].
In the poultry production industry, Ibrahim et al. [24] reported the highest resistance rates against amoxicillin, sulfamethoxazole-trimethoprim, spectinomycin, doxycycline, and florfenicol from isolated avian pathogenic E. coli. Also, isolated E. coli from both poultry and dairy production cattle exhibited multi-drug resistance against several antimicrobial classes [28].
Misuse of antibiotics can promote the development of MDR bacteria through the alteration of the animal microbiome, resulting in the emergence of MDR bacteria in cattle guts. E. coli O157:H7, Salmonella enterica, and Listeria monocytogenes with resistance to more than three different antimicrobial classes were isolated from recto-anal swabs, cattle feces, and milk from healthy and asymptomatic dairy cattle in Jordan. Those isolates were significantly resistant to ampicillin, streptomycin, kanamycin, and tetracycline [29].
Extended spectrum β-lactamase and carbapenemase-producing E. coli was isolated from drinking water sources in Jordan. Phenotyping of isolated E. coli revealed the existence of enteroaggregative, enteropathogenic, enteroinvasive, and enterohemorrhagic E. coli with a high resistance rate to ampicillin and sulfamethoxazole-trimethoprim (93.6 % and 41.3 %, respectively) [26]. Also, one-third of the isolates were MDR [26]. Another study in Jordan reported the isolation of MDR Salmonella typhimurium from two of the most important sources of irrigating water in Jordan, the King Abdullah Canal and Wadi Shueib [30]. This study revealed seasonality patterns, where the highest percentage of isolates were in spring and summer seasons. One-fifth of the isolates were MDR, with the highest percentage of resistance to tetracycline.
The evidence outlined in this section underscores the hidden menace of AMR within Jordan's food chain and affirms the urgent need for integrated multi-sectoral mitigation strategies. As revealed by the previous studies in Jordan, the presence of drug-resistant bacteria across poultry, dairy, and environmental samples, emphasizes that the food chain is a critical point of convergence for AMR transmission. Aligning these findings with a nationally coordinated response grounded in the One Health framework enables more precise and effective interventions aimed at disrupting transmission pathways and limiting the spread of drug-resistant pathogens. The detection of antimicrobial-resistant pathogens across both animal production systems and environmental reservoirs in Jordan further emphasizes the necessity of cohesive, cross-sectoral action to address this escalating public health threat.
4. AMR in the food chain: a conceptual model for mitigation under the One Health approach in Jordan
Jordan has been proactively tackling the rising threat of AMR with a comprehensive, multi-sectoral approach, despite existing challenges. The country is actively working on the five pillars of the GAP on AMR, focusing on strengthening AMR surveillance, improving antimicrobial stewardship (AMS) in healthcare and veterinary sectors, optimizing the proper and rationale use of antimicrobials, enhancing awareness and understanding of AMR, as well as fostering scientific research and sustainable economic investment to tackle AMR [31].
Collaboration with international organizations such as the World Health Organization (WHO), Food and Agriculture Organization of the United Nations (FAO), World Organisation for Animal Health (WOAH), and the United Nations Environment Program (UNEP) has been central to Jordan's efforts in tackling AMR. In Jordan, estimates revealed that approximately 2400 deaths were associated with AMR while 625 deaths were attributed to AMR in 2019 [32]. Compared to countries in the Middle East and North Africa (MENA), Jordan has the fifth lowest age-standardized mortality across 21 countries. In the same year, deaths due to AMR (whether associated with or attributable to) surpassed deaths resulted from maternal and neonatal disorders, road traffic accidents, neurological and digestive diseases [32].
AMR poses a significant threat to public health, food security, and environmental sustainability, particularly in limited-resources countries like Jordan. One of the main challenges in combating AMR in the food chain in Jordan lies in the overuse and misuse of antimicrobials in healthcare settings, which can directly contribute to the spread of resistant pathogens. Although progress has been made in regulating antimicrobial prescriptions, the widespread availability of them without proper oversight remains a significant barrier.
Another challenge is the widespread use of antimicrobials in food-producing animals for non-therapeutic purposes. While there is a growing recognition of the risks posed by such practices, enforcement of regulations to limit non-therapeutic antimicrobial use is still not sufficient. In addition, many farmers in Jordan may lack access to alternatives, such as vaccines or probiotics, and may not have the resources or knowledge to adopt more sustainable practices.
From an environmental health perspective, combating AMR in the food chain in Jordan faces several obstacles. The widespread use of antimicrobials in agriculture and animal husbandry often results in the contamination of soil, water, and ecosystems with antimicrobial residues and resistant pathogens. Consequently, addressing these challenges requires a holistic approach that integrates human, animal, and environmental health. We, as shown in Fig. 4, propose a conceptual model, incorporating governance and policy interventions, integrated surveillance, stewardship, research and innovation, and public awareness across all sectors.
Fig. 4.
A Conceptual model to combat antimicrobial resistance in the food chain.
The development of the conceptual model to combat AMR in the food chain was grounded in a systems thinking approach, which was essential for understanding and addressing the multi-faceted and interconnected nature of AMR. Systems thinking enables a comprehensive view of the AMR issue, considering the dynamic interactions and interdependencies that exist between sectors, actors, and processes involved in antimicrobial use and resistance development. Each element of the proposed model—governance and policy frameworks, integrated surveillance and monitoring, AMS across the food chain, public awareness and education, and research and innovation—represents a key area within the broader AMR landscape. Rather than addressing AMR through isolated interventions, the model emphasizes how changes in one domain may trigger effects in others. For instance, data generated from integrated surveillance systems not only inform policy decisions but also support public education efforts and guide AMS interventions. These, in turn, influence antimicrobial usage patterns and the emergence of resistance, which are then captured in subsequent surveillance activities.
The model also accounts for emergence and adaptability. Given that AMR evolves through microbial adaptation, ecological shifts, and human practices, the model places strong emphasis on research and innovation. This ensures that the system remains responsive to emerging resistance patterns, new technological tools, and evolving risk profiles. Through the systems lens, leverage points were identified such as regulatory enforcement, prescriber behavior, and consumer awareness, where targeted interventions can lead to significant improvements across the system. The integration of public education alongside regulatory governance illustrates the importance of both top-down and bottom-up strategies in achieving systemic change.
The proposed areas within the conceptual model are closely aligned with the principles of the One Health approach, which recognizes the interdependence of human, animal, and environmental health. The integrated surveillance system is designed to capture data across sectors, including antimicrobial use and resistance trends in humans, animals, and the environment, allowing for a comprehensive understanding of AMR dynamics and early detection of cross-sector threats. The governance and policy framework promotes collaboration and coordination among ministries of health, agriculture, and environment, facilitating joint decision-making and harmonized regulations. Public awareness and education initiatives are also tailored to reach diverse audiences, including healthcare providers, veterinarians, farmers, and consumers; thus, encouraging responsible antimicrobial use and improved hygiene practices across the food chain. Together, these areas reflect a One Health vision, ensuring that interventions are not developed in isolation but rather in a way that acknowledges and addresses the interconnected nature of AMR risks.
A strong governance and policy framework is essential for controlling antimicrobial use and limiting the emergence of AMR in food systems. Developing and enforcing national AMR action plans that integrate food safety, veterinary, agricultural, and environmental policies can create a unified and effective response. Strengthening regulatory measures to restrict non-therapeutic antimicrobial use in livestock is necessary to prevent misuse. Additionally, providing financial incentives for farmers and food producers to adopt antimicrobial-free practices can encourage sustainable alternatives. Improved coordination between key governmental authorities, including the JCDC, Ministry of Health (MoH), Ministry of Agriculture (MoA), Ministry of Environment (MoEnv), Ministry of Water and Irrigation (MoWI) as well as Jordan Food and Drug Administration (JFDA), will enhance policy implementation and enforcement.
Integrated surveillance and monitoring systems are critical for tracking AMR trends and identifying emerging threats across the food chain. Strengthening the surveillance system by incorporating human, animal, and environmental data will enable early detection of drug-resistant pathogens. Additionally, advanced molecular techniques such as whole genome sequencing and molecular epidemiology can facilitate the identification of AMR genes and transmission pathways. This also can be supported by developing standardized antimicrobial use reporting in livestock, aquaculture, and agriculture, along with strengthened laboratory capacity for detecting AMR in foodborne pathogens; thus, supporting evidence-based decision-making.
Several factors may contribute to AMR in the food chain in Jordan. These include the overuse and misuse of antibiotics in livestock [28] for growth promotion and disease prevention, rather than solely for treating infections, inadequate regulations and enforcement regarding antibiotic use in agriculture, the presence of antimicrobial residues in animal products, and improper disposal of animal waste and antibiotics which may then contaminate the environment, including water sources and soil [33]. Additionally, insufficient public awareness among farmers and consumers about AMR, and the misuse of antimicrobial agents in human population play a pivotal role in AMR [[34], [35], [36], [37]].
Promoting AMS across various sectors involved in the food chain is crucial for reducing unnecessary antimicrobial use while maintaining human health, animal health and food safety. Enforcing prudent antimicrobial guidelines for veterinarians and farmers can minimize the use of antimicrobials to only when necessary. Moreover, improving the knowledge among farmers and dairy herdsmen regarding proper use of antimicrobials through active communication and effective training will decrease the self-prescription of antimicrobials for farm animals [25,28]. Alternatives such as probiotics, vaccines, and phage therapy [38] offer promising solutions. Furthermore, strengthening farm biosecurity measures and supporting good agricultural and husbandry practices can lower infection rates, reducing the need for antimicrobial interventions. This includes better management of waste and manure to prevent contamination of water sources and crops [39].
Public awareness, education, and behavioral change are essential components of a successful AMR mitigation strategy. National AMR awareness campaigns targeting farmers, veterinarians, and consumers can encourage responsible antimicrobial use and demand for antibiotic-free food products. Integrating AMR education into school and university curricula will help build a community and health workforce equipped with the essential knowledge to combat the threat of AMR. Consumer-driven initiatives advocating antibiotic-free food products can also create market incentives for producers to adopt responsible production practices.
Promoting scientific research, and sustainable investment for the development of alternative methods to manage animal health, such as vaccines and probiotics can reduce reliance on antimicrobials [40]. Investing in research, innovation, and alternative solutions is fundamental to developing sustainable AMR mitigation strategies. Funding research on antimicrobial alternatives can provide viable replacements for traditional antimicrobials. Also, precision diagnostic technologies can optimize animal health monitoring, reducing the need for antimicrobials.
5. Cross-sectoral systems thinking, implementation lessons, and future priorities
Strengthening international collaboration between countries and organizations is critical for harmonizing standards, sharing data, and coordinating efforts to tackle AMR in food chain at the global scale. The Jordanian government, including regulatory bodies on antimicrobials, may incentivize the farmers and food producers to comply with the best practices in antimicrobial usage and AMR mitigation through subsidies, grants, and recognition programs [41]. Strengthening food safety protocols across the entire food production chain ensures that drug-resistant pathogens are effectively controlled at each stage.
While the conceptual model offers a theoretical framework, its proposed components are grounded in practical experience, as similar One Health-focused AMR strategies have been successfully implemented in several countries. A recent study revealed critical and in-depth examination of antibiotic prescribing behaviors in hospital facilities in the MENA, drawing on data from 24 antibiotic point prevalence surveys [42]. The findings reveal alarmingly high antibiotic usage rates of exceeding 50.0 % of inpatients across surveyed hospitals, with Jordan reporting an exceptionally high rate of 98.1 %. Broad-spectrum antibiotics like ceftriaxone, metronidazole, and penicillin dominate prescriptions, often inappropriately used, particularly for prolonged surgical prophylaxis [42]. Such practices are identified as major contributors of AMR in the region.
The same study strongly advocates for a structured, multi-faceted approach to reform antimicrobial use, emphasizing the urgent need for institutionalizing antimicrobial stewardship programs (ASPs), aligning clinical practices with national and international treatment guidelines, and implementing evidence-based quality indicators [42]. These reforms require robust policy support, ongoing healthcare provider education, and cross-sectoral engagement under the One Health framework. This underscores the critical need for sustained political will, multi-sectoral collaboration, and regional harmonization to reduce AMR burden and ensure the responsible use of antimicrobials across various sectors in the MENA region.
Also, Sweden represents a leading example of successful AMR control through a holistic One Health approach that integrates governance, education, surveillance, and stewardship across human and animal health sectors [43]. The country's strategy is underpinned by strong policy frameworks and intersectoral collaboration, guided by the national action plan against AMR. Swedish authorities recognized early on that reducing antibiotic use in livestock was essential to preserving antibiotic efficacy. As a result, Sweden banned the use of antibiotics for growth promotion in animals as early as 1986, long before similar measures were adopted across the European Union. This regulatory shift was accompanied by robust support for farmers, including veterinary training, improved biosecurity measures, and preventive animal health strategies, ensuring animal welfare and productivity were not compromised [43].
In the agricultural sector, particularly in dairy farming, Sweden adopted strict animal health protocols and hygiene standards to prevent infections and thus reduce the need for antibiotics. For example, regular herd health visits and surveillance by veterinarians, mandatory reporting of antibiotic use, and selective treatment based on microbiological diagnostics helped maintain one of the lowest antimicrobial usage rates in food-producing animals in Europe. The government-backed Strama network, the Swedish Strategic Programme against AMR, established in 1995, played a crucial role in coordinating AMR strategies across sectors. In hospitals, Strama developed evidence-based prescribing guidelines and promoted rational antibiotic use through ongoing professional education, monitoring, and feedback mechanisms for prescribers. Public awareness campaigns further supported behaviour change, ensuring that both healthcare professionals and the public understood the importance of using antibiotics responsibly.
Sweden also invested in integrated surveillance systems to monitor AMR and antibiotic use across sectors. The annual Swedres-Svarm report, provides a comprehensive overview of resistance trends and consumption patterns in humans and animals [44]. This evidence-based feedback loop allows policymakers to respond rapidly to emerging resistance threats. Additionally, Sweden continues to promote research and innovation in diagnostics, alternative treatments, and infection prevention strategies. These concerted efforts have helped Sweden maintain low levels of AMR and serve as a global model for AMR containment through coordinated One Health action.
These country-level efforts align closely with the proposed components of the conceptual model for Jordan, including governance and coordination, integrated surveillance, AMS across the food chain, and public awareness. They show how One Health-based strategies are not only conceptually sound but also operationally feasible.
AMR in the food chain poses substantial public health risks and economic challenges, including direct healthcare costs and indirect losses due to reduced agricultural productivity. Moreover, AMR can have significant geopolitical implications, particularly in relation to trade regulations and international market access, as countries may impose restrictions on food exports from regions affected by resistant pathogens. Fig. 5 demonstrates the complex interactions among various systems that can be impacted by AMR in the food chain. Also, Table 1 describes the actionable recommendations to combat AMR in the food chain in Jordan, while Table 2 provides in depth analysis of current challenges, proposed actions, stakeholders involved and evidence in the Jordanian context.
Fig. 5.
Complex systems involved in antimicrobial resistance in the food chain.
Table 1.
Cross-sectoral roles and responsibilities to combat antimicrobial resistance (AMR) under One Health umbrella.
| Sector | Roles and responsibilities |
|---|---|
| Human health | Strengthening hospital-based AMR surveillance systems to detect and monitor resistant infections |
| Enforcing antimicrobial stewardship programs to optimize the rationale use of antimicrobials in clinical settings | |
| Raising public awareness through targeted campaigns on the risks of antimicrobial misuse and the importance of completing prescribed courses, and proper disposal of antimicrobials | |
| Enforcing regulations on antimicrobial prescriptions, ensuring that antimicrobials are prescribed only when necessary and appropriate for human health | |
| Animal health | Restricting the use of antimicrobials in food-producing animals for non-therapeutic purposes, such as growth promotion, and regulating their use strictly for disease treatment |
| Promoting the use of vaccines and other preventive measures to reduce the need for antimicrobials in animal husbandry | |
| Establishing regular AMR monitoring programs for livestock, poultry, and aquaculture to track resistance patterns and ensure safe practices in animal health management | |
| Environmental health | Monitoring the presence of antimicrobial-resistant pathogens and genes in wastewater, agricultural runoff, and environmental samples |
| Implementing and enforcing regulations to limit the spread of antibiotics and antimicrobial-resistant microorganisms into the environment, including proper waste disposal practices | |
| Conducting environmental impact assessments to understand how AMR in the food chain affects food safety, biodiversity, and ecosystems, with a focus on sustainable practices |
Table 2.
In-depth analysis of current challenges, proposed actions, stakeholders involved, and evidence based on the proposed conceptual model in Jordan.
| Strategic Pillar | Challenge | Proposed action | Stakeholders involved | Evidence |
|---|---|---|---|---|
| Integrated surveillance and monitoring |
|
|
JCDC, MoH, MoWI, MoEnv, MoA, JFDA, royal Scientific Society, academic and research institutions, private laboratories, food industry sector, veterinary clinics |
|
| Governance and policy |
|
|
Prime Ministry, JCDC, MoH, MoA, JFDA, MoEnv professional associations (medical, pharmacy, veterinary), civil society organizations, private sector representatives, and NGOs | Jordan's updated NAP (2023–2025) incorporates One Health principles. Although multi-sectoral AMR coordination forums are operational, they require formalization under legal frameworks to ensure sustainability |
| Public awareness and capacity building |
|
|
JCDC, MoH, MoHE, MoEnv, MoA, MoWI, universities, professional councils, WHO, FAO, and civil society organizations | Plans are ongoing to extend training to primary healthcare centers and veterinary practices |
| AMS across the food chain |
|
|
JCDC, MoH, JFDA, MoA, hospital administrators, private clinics, community pharmacies, professional councils, veterinary services, and media outlets |
|
| Research and innovation |
|
|
JCDC, MoH, MoA, MoWI, MoEnv, MoHE, HCST, NCRD, universities, international academic partners, private sector, and WHO/FAO/WOAH networks |
|
Abbreviations: AMR, antimicrobial resistance; NAP, National Action Plan; AMS, antimicrobial stewardship; IPC, infection prevention and control; ASPs, antimicrobial stewardship programs; PHCs, primary healthcare centers; MoH, Ministry of Health; MoA, Ministry of Agriculture; MoWI, Ministry of Water and Irrigation; MoEnv, Ministry of Environment; MOHE, Ministry of Higher Education; NCRD, National Center for Research and Development; JCDC, Jordan Center for Disease Control; HCST, Higher Council for Science and Technology; JFDA, Jordan Food and Drug Administration; WHO, World Health Organization; FAO, Food and Agricultural Organization of the United Nations; WOAH, World Organisation for Animal Health; NGO, non-governmental organization; GLASS, Global Antimicrobial Resistance and Use Surveillance; TrACSS, Tracking AMR Country Self-assessment Survey.
While the strategic pillars in the proposed conceptual model provide a clear roadmap for addressing AMR in the food chain in Jordan, it is important to recognize that translating these plans into action will not be without challenges. One of the most pressing obstacles is securing sustainable financing. Many of the proposed initiatives, particularly the expansion of surveillance networks, integration of surveillance systems across various sectors, laboratory upgrades, and workforce training, require significant upfront investment and ongoing support. Without dedicated national funding streams and strategic engagement with international donors, momentum may be difficult to sustain.
Another major hurdle is the need for genuine multi-sectoral collaboration. Although Jordan has made strides in fostering a One Health approach, overcoming deeply rooted divisions between the human health, animal health, and environmental sectors remains a work in progress. Building trust and shared ownership among these diverse actors will be essential for success. Additionally, workforce capacity remains a limiting factor; while recent training programs have made important gains, the shortage of skilled professionals in infection prevention and control (IPC), and AMS especially outside major urban centres could slow down implementation. Importantly, by embedding AMR interventions within existing public health programs, such as disease surveillance, health security, and food safety regulation, the strategy promotes integration rather than creating parallel systems. This not only improves efficiency but also increases the likelihood of long-term sustainability.
Looking beyond Jordan, the approach outlined here offers important lessons for other low- and middle-income countries (LMICs) facing similar AMR challenges. Issues like fragmented governance, gaps in surveillance, inappropriate antimicrobial use, and limited research investment are common across many LMIC settings. Strengthening regional and international collaboration could help scale up successful practices and accelerate collective action against AMR on a global scale.
In conclusion, the successful implementation of this conceptual model across human, animal, and environmental health sectors will enable Jordan to effectively mitigate the impact of AMR in the food chain. This integrated approach is crucial for safeguarding public health by reducing the transmission of resistant pathogens, ensuring food security through sustainable agricultural and veterinary practices, and promoting environmental sustainability by minimizing antimicrobial residues and contamination. A comprehensive national response to AMR requires the establishment of robust policy frameworks to regulate antimicrobial use, the development of an integrated surveillance system to track resistance trends, the promotion of responsible AMS in food production, continuous investment in research and innovation to explore alternative solutions, and widespread public awareness initiatives to encourage behavioural change. Through a coordinated and multi-sectoral effort, Jordan can significantly enhance its ability to mitigate the impacts of AMR, ensuring a more resilient and sustainable response to this growing threat.
CRediT authorship contribution statement
Ala'a B. Al-Tammemi: Writing – review & editing, Writing – original draft, Visualization, Supervision, Software, Project administration, Investigation, Data curation, Conceptualization. Salam Momani: Writing – review & editing, Writing – original draft. Hanan Hasan: Writing – review & editing, Writing – original draft. Amal Obeidat: Writing – review & editing, Writing – original draft. Muna Horabi: Writing – review & editing, Writing – original draft.
Ethical approval
Not required.
Funding
This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
On behalf of the Jordan Center for Disease Control, the authors extend their appreciation to Shanghai Jiao Tong University for covering the open access publication fees of this paper. Also, the authors would like to extend their sincere gratitude to the reviewers for their valuable time, insightful suggestions, and constructive feedback during the peer review process. Their comments greatly contributed to enhancing the clarity, rigor, and overall quality of the paper.
Footnotes
This article is part of a special issue entitled: systems thinking with One Health approach published in Science in One Health.
Contributor Information
Ala'a B. Al-Tammemi, Email: a.altammemi@jcdc.gov.jo.
Salam Momani, Email: s.momani@jcdc.gov.jo.
Hanan Hasan, Email: hananyalu97@gmail.com.
Amal Obeidat, Email: a.obeidat@jcdc.gov.jo.
Muna Horabi, Email: m.horabi@jcdc.gov.jo.
References
- 1.Naghavi M., Vollset S.E., Ikuta K.S., Swetschinski L.R., Gray A.P., Wool E.E., et al. Global burden of bacterial antimicrobial resistance 1990-2021: a systematic analysis with forecasts to 2050. Lancet. 2024;404:1199–1226. doi: 10.1016/S0140-6736(24)01867-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.United Nations, High-Level Meeting on Antimicrobial Resistance . 2016. https://www.un.org/pga/71/2016/09/21/press-release-hl-meeting-on-antimicrobial-resistance/ (accessed 16 December 2024) [Google Scholar]
- 3.Woolhouse M.E.J. One Health approaches to tackling antimicrobial resistance. Sci. One Health. 2024;3:100082. doi: 10.1016/j.soh.2024.100082. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Alsayeqh A.F., Baz A.H.A., Darwish W.S. Antimicrobial-resistant foodborne pathogens in the Middle East: a systematic review. Environ. Sci. Pollut. Control Ser. 2021;28:68111–68133. doi: 10.1007/s11356-021-17070-9. [DOI] [PubMed] [Google Scholar]
- 5.Kanapathipillai R., Malou N., Hopman J., Bowman C., Yousef N., Michel J., et al. Antibiotic resistance in conflict settings: lessons learned in the Middle East. JAC. Antimicrob. Resist. 2019;1:dlz002. doi: 10.1093/jacamr/dlz002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6.Osman M., Rayane R., Mohamad Bachar I., Sarah Al O., Hassan M., Fouad D., et al. Antimicrobial resistance in the protracted Syrian conflict: halting a war in the war. Future Microbiol. 2021;16:825–845. doi: 10.2217/fmb-2021-0040. [DOI] [PubMed] [Google Scholar]
- 7.Abbara A., Rawson T.M., Karah N., El-Amin W., Hatcher J., Tajaldin B., et al. A summary and appraisal of existing evidence of antimicrobial resistance in the Syrian conflict. Int. J. Infect. Dis. 2018;75:26–33. doi: 10.1016/j.ijid.2018.06.010. [DOI] [PubMed] [Google Scholar]
- 8.Asfaw T., Genetu D., Shenkute D., Shenkutie T.T., Amare Y.E., Yitayew B. Foodborne pathogens and antimicrobial resistance in Ethiopia: an urgent call for action on “One Health.”. Infect. Drug Resist. 2022;15:5265–5274. doi: 10.2147/IDR.S375043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Hartinger S.M., Medina-Pizzali M.L., Salmon-Mulanovich G., Larson A.J., Pinedo-Bardales M., Verastegui H., et al. Antimicrobial resistance in humans, animals, water and household environs in rural Andean Peru: exploring dissemination pathways through the One Health lens. Int. J. Environ. Res. Public. Health. 2021;18 doi: 10.3390/ijerph18094604. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.European Food Safety Authority (EFSA) Foodborne antimicrobial resistance as a biological hazard - scientific opinion of the panel on biological hazards. EFSA J. 2008;6:765. doi: 10.2903/j.efsa.2008.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Samtiya M., Matthews K.R., Dhewa T., Puniya A.K. Antimicrobial resistance in the food chain: trends, mechanisms, pathways, and possible regulation strategies. Foods. 2022;11(19):2966. doi: 10.3390/foods11192966. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Liu Y.-Y., Wang Y., Walsh T.R., Yi L.-X., Zhang R., Spencer J., et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect. Dis. 2016;16:161–168. doi: 10.1016/S1473-3099(15)00424-7. [DOI] [PubMed] [Google Scholar]
- 13.Coetzee J., Corcoran C., Prentice E., Moodley M., Mendelson M., Poirel L., et al. Emergence of plasmid-mediated colistin resistance (MCR-1) among Escherichia coli isolated from South African patients. SAMJ (S. Afr. Med. J.): S. Afr. Med. J. 2016;106:449–450. doi: 10.7196/samj.2016.v106i5.10710. [DOI] [PubMed] [Google Scholar]
- 14.Watts J.E.M., Schreier H.J., Lanska L., Hale M.S. The rising tide of antimicrobial resistance in aquaculture: sources, sinks and solutions. Mar. Drugs. 2017;15(6):158. doi: 10.3390/md15060158. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Tate H., Ayers S., Nyirabahizi E., Li C., Borenstein S., Young S., et al. Prevalence of antimicrobial resistance in select bacteria from retail seafood—United States, 2019. Front. Microbiol. 2022;13:928509. doi: 10.3389/fmicb.2022.928509. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.EFSA Panel on Biological Hazards Scientific Opinion on the risk posed by pathogens in food of non-animal origin. Part 1 (outbreak data analysis and risk ranking of food/pathogen combinations) EFSA J. 2013;11:3025. doi: 10.2903/j.efsa.2013.3025. [DOI] [Google Scholar]
- 17.Stein R.A., Chirilã M. In: Foodborne Dis. 3rd ed. Dodd CER, Aldsworth T, Stein RA, Cliver DO, Riemann HP, editors. Academic Press; 2017. Chapter 3 - Routes of Transmission in the Food Chain; pp. 65–103. [DOI] [Google Scholar]
- 18.Shakoor M.B., Nawaz R., Hussain F., Raza M., Ali S., Rizwan M., et al. Human health implications, risk assessment and remediation of As-contaminated water: a critical review. Sci. Total Environ. 2017;601–602:756–769. doi: 10.1016/j.scitotenv.2017.05.223. [DOI] [PubMed] [Google Scholar]
- 19.Department of Statistics Jordan, Population Clock - Jordan . 2023. https://dosweb.dos.gov.jo/ (accessed 10 April 2024) [Google Scholar]
- 20.Hassan S.K., Dahmash E.Z., Madi T., Tarawneh O., Jomhawi T., Alkhob W., et al. Four years after the implementation of antimicrobial stewardship program in Jordan: evaluation of program's core elements. Front. Public Health. 2023;11:1078596. doi: 10.3389/fpubh.2023.1078596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Al-Tammemi A.B., Kanaan D., Omar A., Barakat M. Tackling antimicrobial resistance in Jordan: bridging science, research, and policy for a healthier future. Jordan J. Appl. Sci. 2025;19 doi: 10.35192/jjoas-n.v19i2.2177. [DOI] [Google Scholar]
- 22.Jordan Center for Disease Control . Monitoring & Evaluation of NAP on AMR in Jordan. 2024. https://jcdc.gov.jo/ebv4.0/root_storage/ar/eb_list_page/amr_me_plan_2023-2025_text_24_oct_v8_-_sm-endo-0.pdf (accessed 26 April 2025) [Google Scholar]
- 23.Jordan Ministry of Health . Jordan Surveillance of Antimicrobial Resistance Annual Report 2023, Jordan Ministry of Health. 2024. https://moh.gov.jo/ebv4.0/root_storage/ar/eb_list_page/jordan_national_amr_surveillance_report_2023.pdf [Google Scholar]
- 24.Ibrahim R.A., Cryer T.L., Lafi S.Q., Basha E.-A., Good L., Tarazi Y.H. Identification of Escherichia coli from broiler chickens in Jordan, their antimicrobial resistance, gene characterization and the associated risk factors. BMC Vet. Res. 2019;15:159. doi: 10.1186/s12917-019-1901-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Obaidat M.M., Bani Salman A.E., Roess A.A. High prevalence and antimicrobial resistance of mecA Staphylococcus aureus in dairy cattle, sheep, and goat bulk tank milk in Jordan. Trop. Anim. Health Prod. 2018;50:405–412. doi: 10.1007/s11250-017-1449-7. [DOI] [PubMed] [Google Scholar]
- 26.Swedan S., Abu Alrub H. Antimicrobial resistance, virulence factors, and pathotypes of Escherichia coli isolated from drinking water sources in Jordan. Pathogens. 2019;8(2):86. doi: 10.3390/pathogens8020086. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27.Alekish M.O., Al-Qudah K.M., Al-Saleh A. Prevalence of antimicrobial resistance among bacterial pathogens isolated from bovine mastitis in northern Jordan. Rev. Med. Vet. 2013;164:319–326. [Google Scholar]
- 28.Obaidat M.M., Bani Salman A.E., Davis M.A., Roess A.A. Major diseases, extensive misuse, and high antimicrobial resistance of Escherichia coli in large- and small-scale dairy cattle farms in Jordan. J. Dairy Sci. 2018;101:2324–2334. doi: 10.3168/jds.2017-13665. [DOI] [PubMed] [Google Scholar]
- 29.Obaidat M.M., Stringer A.P. Prevalence, molecular characterization, and antimicrobial resistance profiles of Listeria monocytogenes, Salmonella enterica, and Escherichia coli O157:H7 on dairy cattle farms in Jordan. J. Dairy Sci. 2019;102:8710–8720. doi: 10.3168/jds.2019-16461. [DOI] [PubMed] [Google Scholar]
- 30.Burjaq S.Z., Abu-Romman S.M. Prevalence and antimicrobial resistance of Salmonella spp. from irrigation water in two major sources in Jordan. Curr. Microbiol. 2020;77:3760–3766. doi: 10.1007/s00284-020-02178-x. [DOI] [PubMed] [Google Scholar]
- 31.World Health Organization . Jordan’s National Action Plan on Antimicrobial Resistance Launches under Royal Patronage. 2023. https://www.emro.who.int/jor/jordan-news/jordans-national-action-plan-on-antimicrobial-resistance-launches-under-royal-patronage.html (accessed 21 December 2024) [Google Scholar]
- 32.Global Research on Antimicrobial Resistance (GRAM) The Burden of Antimicrobial Resistance in Jordan. 2023. https://www.healthdata.org/sites/default/files/2023-09/Jordan.pdf (accessed 16 December 2024) [Google Scholar]
- 33.Al-Mashaqbeh O., Alsafadi D., Dalahmeh S., Bartelt-Hunt S., Snow D. Removal of selected pharmaceuticals and personal care products in wastewater treatment plant in Jordan. Water (Basel) 2019;11(10):2004. doi: 10.3390/w11102004. [DOI] [Google Scholar]
- 34.Muflih S.M., Al-Azzam S., Karasneh R.A., Bleidt B.A., Conway B.R., Bond S.E., et al. Public knowledge of antibiotics, self-medication, and household disposal practices in Jordan. Expert Rev. Anti Infect. Ther. 2023;21:477–487. doi: 10.1080/14787210.2023.2182770. [DOI] [PubMed] [Google Scholar]
- 35.Naser A.Y., Amara N., Dagash A., Naddaf A. Medications disposal and medications storage in Jordan: a cross-sectional study. Int. J. Clin. Pract. 2021;75 doi: 10.1111/ijcp.13822. [DOI] [PubMed] [Google Scholar]
- 36.Yusef D., Babaa A.I., Bashaireh A.Z., Al-Bawayeh H.H., Al-Rijjal K., Nedal M., et al. Knowledge, practices & attitude toward antibiotics use and bacterial resistance in Jordan: a cross-sectional study. Infect. Dis. Health. 2018;23:33–40. doi: 10.1016/j.idh.2017.11.001. [DOI] [PubMed] [Google Scholar]
- 37.al-magableh M., Eldos B., Aldughmi S., Bani Hamad L., Abdel Karim R., Damseh R., et al. A systematic review of misuse of antibiotics in Jordan. Jordan Med. J. 2024;58 doi: 10.35516/jmj.v58i3.998. [DOI] [Google Scholar]
- 38.Ferriol-González C., Domingo-Calap P. Phage therapy in livestock and companion animals. Antibiotics (Basel) 2021;10(5):559. doi: 10.3390/antibiotics10050559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Al-Seghayer M.S., Al-Sarraj F.M.B. The outbreak of foodborne disease by pathogenic enterobacteriaceae antimicrobial resistance - a review. Asian Food Sci. J. 2021;20:91–99. doi: 10.9734/afsj/2021/v20i630312. [DOI] [Google Scholar]
- 40.Andrew O., Zhengyao X., Vy T., Blythe D.-J., Zeynep A., Td H., et al. Association of diet and antimicrobial resistance in healthy U.S. Adults. mBio. 2022;13 doi: 10.1128/mbio.00101-22. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Varma J.K., Molbak K., Barrett T.J., Beebe J.L., Jones T.F., Rabatsky-Ehr T., et al. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. J. Infect. Dis. 2005;191:554–561. doi: 10.1086/427263. [DOI] [PubMed] [Google Scholar]
- 42.Haseeb A., Saleem Z., Maqadmi A.F., Allehyani R.A., Mahrous A.J., Elrggal M.E., et al. Ongoing strategies to improve antimicrobial utilization in hospitals across the Middle East and North Africa (MENA): findings and implications. Antibiotics. 2023;12 doi: 10.3390/antibiotics12050827. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43.Food and Agriculture Organization . 1st ed. FAO; Rome, Italy: 2020. Tackling Antimicrobial Use and Resistance in Dairy Cattle: Lessons Learned in Sweden. [DOI] [Google Scholar]
- 44.Public Health Agency of Sweden . Swedres-Svarm Report. 2022. https://www.folkhalsomyndigheten.se/publikationer-och-material/publikationsarkiv/s/swedres-svarm-2022/ (accessed 13 April 2025) [Google Scholar]





