Making food safer in Palestine: a one health approach to antimicrobial resistance

Background
Foodborne diseases, combined with the growing threat of antimicrobial resistance (AMR), present significant public health challenges, especially in relation to climate change and the risks of zoonotic epidemics. Unsafe food consumption can cause various health issues, ranging from food poisoning to reproductive problems, and can contribute to the emergence of AMR, resulting in severe consequences such as cancer and death. The use of antimicrobials in food production raises safety concerns due to the presence of antibiotic residues, antibiotic-resistant bacteria (ARB), and antibiotic-resistant genes (ARGs) in animals, food products, and the environment.
Foodborne diseases caused by antibiotic-resistant bacteria from animals, such as foodborne urinary tract infections (UTIs), have recently attracted considerable attention. Resistant bacteria from contaminated food can colonize the human gastrointestinal tract, acting as a reservoir for further infections. This hinders infection prevention and control efforts, as well as antimicrobial stewardship programs in communities and hospitals.
The political unrest due to the conflicts and wars, such as in Palestine, have severe consequences for food safety and the spread of AMR. Infrastructure damage, limited resources for food safety programs, increased antibiotic use, hindered access to medical care, and displacement of individuals contribute to compromised food safety and the rise of AMR.
A comprehensive One Health approach is vital to tackle AMR throughout the entire food production process. It considers all relevant factors, from upstream to downstream, and includes an integrated surveillance-response system encompassing human and animal health, the environment, and food production. This holistic approach safeguards antimicrobial efficacy by ensuring food safety, preserving food security, and effectively combating communicable and noncommunicable diseases, benefiting future generations.
Objectives
This PhD thesis utilizes the One Health approach to examine zoonotic bacteria and AMR in the food production chain, particularly in conflict-affected regions. It aims to identify integrated One Health studies on Middle Eastern foodborne illnesses, assess food safety for an operational strategy in Palestine, and evaluate the benefits of implementing an integrated surveillance system for foodborne pathogens and AMR.
Methods
This PhD project tries to find a critical methodology to foster food safety by better understanding the zoonotic foodborne illnesses transmission and their resistance to antimicrobials in socio-ecological systems like in Palestine. The research conducted a systematic review and meta-analysis of scientific literature from 2010 to 2021 to assess the implementation of the One Health approach in the Middle East, with a particular emphasis on Salmonella and Campylobacter strains. Stakeholder perspectives were gathered through multi-stakeholder discussion groups, facilitating communication and identifying diverse viewpoints on the food production monitoring system in Palestine. Additionally, a semi-structured observation design was employed to evaluate hygiene practices in broiler farms, slaughterhouses, and meat stores, pinpointing potential transmission routes and contamination sources. The project also investigated the knowledge, attitudes, and practices of workers in the broiler production industry, to explore the relationship between their attitudes, practices, and hygiene knowledge regarding zoonotic diseases. Furthermore, a One Health integrated surveillance system for Campylobacter and Salmonella, including antimicrobial resistance analysis, was piloted in the central West Bank, Palestine, involving the collection and analysis of samples from various sources. This comprehensive approach provides valuable insights into the complex dynamics of food safety and antimicrobial resistance in Palestine's socio-ecological context.
Results
In the Middle East, a total of 41 studies were analyzed to determine the prevalence rates of non-typhoid Salmonella (NTS) and Campylobacter. The findings revealed that NTS had a prevalence of 9% among humans and 13% among food-producing animals, while Campylobacter had prevalence rates of 22% in humans and 30% in animals. The most common NTS serovars were Salmonella Enteritidis and Salmonella Typhimurium, and the predominant species of Campylobacter were Campylobacter jejuni and Campylobacter coli. Notably, both NTS and Campylobacter showed high resistance to multiple antibiotics, including erythromycin, amoxicillin, tetracycline, and more. However, the implementation of the One Health approach in the Middle East was limited, and data reporting varied across countries.
In Palestine, several challenges were observed in the food production chain, such as the scarcity of public slaughterhouses, inadequate coordination between authorities, and discrepancies in law enforcement. Hygiene practices also varied, with public slaughterhouses and meat markets demonstrating better hygiene compared to large-scale farms. While participants expressed awareness of zoonotic disease transmission and emphasized the importance of hygiene standards, there were conflicting findings between observations and survey results regarding actual hygiene practices.
In a cross-sectional study conducted in Palestine using integrated One Health surveillance, the positivity rate for C. jejuni in chicken manure samples was 24%, while S. enterica had a positivity rate of 6%. The dominant serotypes of both C. jejuni and S. enterica were found in chicken manure, chicken meat sold in markets, and the feces of asymptomatic farm workers, indicating genetic similarities across different sources. Strain turnover was observed in C. jejuni between 2021 and 2022. In 2021, C. jejuni isolates exhibited identical drug resistance gene patterns, including resistance to aminoglycosides, macrolides, quinolones, and tetracycline. In 2022, a different resistance gene pattern emerged, involving beta-lactamase and quinolone resistance genes. Among the Salmonella isolates collected, most belonged to S. enterica serotype Muenchen and showed multidrug resistance, facilitated by the pESI megaplasmid carrying resistance genes to multiple antibiotics, including aminoglycosides, fluoroquinolones, sulfonamides, tetracycline, and trimethoprim.
Conclusion
To effectively implement a One Health strategy in Palestine, the establishment of a technical committee is crucial. This committee would focus on food safety, zoonotic diseases, and AMR, promoting coordination, communication, and partnerships. Proposed measures include developing an integrated quality control system for food production, implementing product certification for broiler meat, and improving slaughterhouse capacity. Veterinary inspections, careful monitoring of antimicrobial use, and sharing of AMR data would further strengthen the food safety system.
Furthermore, implementing an integrated surveillance system and adopting a transdisciplinary approach are key to addressing AMR and enhancing the food safety system in Palestine. Sharing responsibilities and resources among relevant authorities is vital for successful AMR mitigation. The establishment of the Palestinian Integrated Program for Antimicrobial Resistance Surveillance (PIPARS) would lead to financial savings and a comprehensive approach. Employing efficient testing methods like whole genome sequencing enables early identification and timely response to AMR threats, serving as an essential tool for the One Health integrated surveillance system.