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
Authors: Abukhattab Said , Hosch Salome , Abu-Rmeileh Niveen M. E. , Hasan Shadi , Vonaesch Pascale , Crump Lisa , Hattendorf Jan , Daubenberger Claudia , Zinsstag Jakob , Schindler Tobias 
Published: September 2023

ABSTRACT

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.