Whole-genome sequencing for One Health surveillance of antimicrobial resistance in conflict zones: a case study of Salmonella spp. and Campylobacter spp. in the West Bank, Palestine.

Antimicrobial resistance (AMR) is a critical global concern driven by the overuse, misuse, and/or usage of inadequate antibiotics on humans, animals' agriculture, and as a result of contaminated environments. This study is the first One Health survey in the Middle East that incorporated whole-genome sequencing (WGS) to examine the spread of AMR in Campylobacter spp. and Salmonella spp. This cross-sectional study was conducted to examine the role of AMR at the human-animal-environmental interface and was performed in Ramallah/Al-Bireh and Jerusalem governorates of the central West Bank, Palestine. In 2021 and 2022, a total of 592 samples were collected and analyzed. From a total of 65 Campylobacter jejuni and 19 Salmonella spp. isolates, DNA was extracted for WGS using Oxford Nanopore Technologies MinION platform. We found that the dominant serotypes of C. jejuni and Salmonella enterica were present in chicken manure, chicken meat sold in markets, and feces of asymptomatic farm workers, with high genetic similarities between the isolates regardless of origin. Additionally, our results showed rapid strain turnover in C. jejuni from the same sites between 2021 and 2022. Most of the positive Salmonella spp. samples were multidrug-resistant (MDR) S. enterica serovar Muenchen carrying the plasmid of emerging S. infantis (pESI) megaplasmid, conferring resistance to multiple antibiotics. Our findings highlight the spread of MDR foodborne pathogens from animals to humans through the food chain, emphasizing the importance of a One Health approach that considers the interconnections between human, animal, and environmental health. IMPORTANCE Prior to this study, there existed hardly an integrated human-animal-environmental study of Salmonellosis and Campylobacteriosis and related AMR in Middle Eastern countries. The few existing studies lack robust epidemiological study designs, adequate for a One Health approach, and did not use WGS to determine the circulating serotypes and their AMR profiles. Civil unrest and war in Middle Eastern countries drive AMR because of the breakdown of public health and food security services. This study samples simultaneously humans, animals, and the environment to comprehensively investigate foodborne pathogens in the broiler chicken production chain in Palestine using WGS. We show that identical serotypes of C. jejuni and S. enterica can be found in samples from chicken farms, chicken meat sold in markets, and asymptomatic broiler chicken production workers. The most striking feature is the rapid dynamic of change in the genetic profile of the detected species in the same sampling locations. The majority of positive Salmonella spp. samples are MDR S. enterica serovar Muenchen isolates carrying the pESI megaplasmid. The results demonstrate a close relationship between the S. enterica serovar Muenchen isolates found in our sample collection and those responsible for 40% of all clinical Salmonella spp. isolates in Israel as previously reported, with a sequence identity of over 99.9%. These findings suggest the transboundary spread of MDR S. enterica serovar Muenchen strains from animals to humans through the food chain. The study underscores the importance of combining integrated One Health studies with WGS for detecting environmental-animal-human transmission of foodborne pathogens that could not be detected otherwise. This study showcases the benefits of integrated environmental-animal-human sampling and WGS for monitoring AMR. Environmental samples, which may be more accessible in conflict-torn places where monitoring systems are limited and regulations are weak, can provide an effective AMR surveillance solution. WGS of bacterial isolates provides causal inference of the distribution and spread of bacterial serotypes and AMR in complex social-ecological systems. Consequently, our results point toward the expected benefits of operationalizing a One Health approach through closer cooperation of public and animal health and food safety authorities.

Systematic Review and Meta-Analysis of Integrated Studies on Salmonella and Campylobacter Prevalence, Serovar, and Phenotyping and Genetic of Antimicrobial Resistance in the Middle East-A One Health Perspective.

Background:Campylobacter and Salmonella are the leading causes of foodborne diseases worldwide. Recently, antimicrobial resistance (AMR) has become one of the most critical challenges for public health and food safety. To investigate and detect infections commonly transmitted from animals, food, and the environment to humans, a surveillance-response system integrating human and animal health, the environment, and food production components (iSRS), called a One Health approach, would be optimal. Objective: We aimed to identify existing integrated One Health studies on foodborne illnesses in the Middle East and to determine the prevalence, serovars, and antimicrobial resistance phenotypes and genotypes of Salmonella and Campylobacter strains among humans and food-producing animals. Methods: The databases Web of Science, Scopus, and PubMed were searched for literature published from January 2010 until September 2021. Studies meeting inclusion criteria were included and assessed for risk of bias. To assess the temporal and spatial relationship between resistant strains from humans and animals, a statistical random-effects model meta-analysis was performed. Results: 41 out of 1610 studies that investigated Campylobacter and non-typhoid Salmonella (NTS) in the Middle East were included. The NTS prevalence rates among human and food-producing animals were 9% and 13%, respectively. The Campylobacter prevalence rates were 22% in humans and 30% in food-producing animals. The most-reported NTS serovars were Salmonella Enteritidis and Salmonella Typhimurium, while Campylobacter jejuni and Campylobacter coli were the most prevalent species of Campylobacter. NTS isolates were highly resistant to erythromycin, amoxicillin, tetracycline, and ampicillin. C. jejuni isolates showed high resistance against amoxicillin, trimethoprim-sulfamethoxazole, nalidixic acid, azithromycin, chloramphenicol, ampicillin, tetracycline, and ciprofloxacin. The most prevalent Antimicrobial Resistance Genes (ARGs) in isolates from humans included tetO (85%), Class 1 Integrons (81%), blaOXA-61 (53%), and cmeB (51%), whereas in food-producing animals, the genes were tetO (77%), Class 1 integrons (69%), blaOXA-61 (35%), and cmeB (35%). The One Health approach was not rigorously applied in the Middle East countries. Furthermore, there was an uneven distribution in the reported data between the countries. Conclusion: More studies using a simultaneous approach targeting human, animal health, the environment, and food production components along with a solid epidemiological study design are needed to better understand the drivers for the emergence and spread of foodborne pathogens and AMR in the Middle East.

Towards a One Health Food Safety Strategy for Palestine: A Mixed-Method Study.

Introduction: Foodborne diseases, together with increasing antimicrobial resistance (AMR), pose a threat to public health in an era of huge challenges with climate change and the risks of zoonotic epidemics. A One Health approach to foster food safety is a key for improvement, particularly in complex socio-ecological systems such as in Palestine, to examine human-animal-environment interfaces and promote intersectoral action. Objectives: This study aimed to assess food safety from farm to public health toward an operational One Health strategy for Palestine. This study evaluates the food production (broiler production) and monitoring system to better understanding the zoonotic foodborne illnesses transmission and their resistance to antimicrobials. Methods: The transdisciplinary approach included multi-stakeholder discussion groups and field visits to broiler farms, slaughterhouses, and meat stores in the Ramallah and Al-Bireh and Jerusalem districts using a semi-structured observational tool. A survey with 337 poultry producers and workers in slaughterhouses and meat stores was conducted to assess hygiene knowledge, attitudes, and practices during broiler meat production. Results: The stakeholders point out various challenges along the food production chain in Palestine, such as a striking scarcity of public slaughterhouses, insufficient coordination between authorities, a gap between public and private sectors, and inconsistent application of the law. From observations, it appears that, unlike traditional broiler production, the public slaughterhouses and meat markets have effective hygiene, while large-scale farms implement biosecurity measures. Overall, surveyed participants reported that they are aware of zoonotic disease transmission routes and value hygiene standards. Semi-structured observations and survey results are contradictory. Observations indicate poor hygiene practices; however, the vast majority of broiler meat production chain workers claim that hygiene standards are met. Discussion and Conclusions: Our study found that the overuse of antimicrobials, system fragmentation, insufficient infrastructure, a lack of regulations and controls, and poor hygiene practices are among the main obstacles to improving food safety in Palestine. Considering the risk of an important human health burden of food-related illnesses, enhancing food safety in Palestine is required using an integrated One Health approach. It is crucial to develop an integrated quality control system for food production along with promoting on-farm biosecurity and antimicrobial stewardship. Infrastructure, especially slaughterhouses and laboratories, must be built, training and education provided, and consumer awareness raised. As an important added value within a One Health strategy for better food safety in Palestine, research should be reinforced and accompany any future development of the food production monitoring system.

The Promotion and Development of One Health at Swiss TPH and Its Greater Potential.

One Health, an integrated health concept, is now an integral part of health research and development. One Health overlaps with other integrated approaches to health such as EcoHealth or Planetary Health, which not only consider the patient or population groups but include them in the social-ecological context. One Health has gained the widest foothold politically, institutionally, and in operational implementation. Increasingly, One Health is becoming part of reporting under the International Health Legislation (IHR 2005). The Swiss Tropical and Public Health Institute (Swiss TPH) has played a part in these developments with one of the first mentions of One Health in the biomedical literature. Here, we summarise the history of ideas and processes that led to the development of One Health research and development at the Swiss TPH, clarify its theoretical and methodological foundations, and explore its larger societal potential as an integrated approach to thinking. The history of ideas and processes leading to the development of One Health research at the Swiss TPH were inspired by far-sighted and open ideas of the directors and heads of departments, without exerting too much influence. They followed the progressing work and supported it with further ideas. These in turn were taken up and further developed by a growing number of individual scientists. These ideas were related to other strands of knowledge from economics, molecular biology, anthropology, sociology, theology, and linguistics. We endeavour to relate Western biomedical forms of knowledge generation with other forms, such as Mayan medicine. One Health, in its present form, has been influenced by African mobile pastoralists' integrated thinking that have been taken up into Western epistemologies. The intercultural nature of global and regional One Health approaches will inevitably undergo further scrutiny of successful ways fostering inter-epistemic interaction. Now theoretically well grounded, the One Health approach of seeking benefits for all through better and more equitable cooperation can clearly be applied to engagement in solving major societal problems such as social inequality, animal protection and welfare, environmental protection, climate change mitigation, biodiversity conservation, and conflict transformation.