Multidrug-resistant non-typhoidal Salmonella of public health significance recovered from migratory birds in Bangladesh

Abstract

Non-typhoidal <i>Salmonella</i> provides an exemplar for the One Health approach as it encompasses public and animal health, food safety, and environmental considerations. The contribution of environmental aspects is currently less well-defined. The purpose of this study was to determine the carriage occurrence of non-typhoidal <i>Salmonella</i> in migratory birds in Bangladesh and assess the potential significance to public and animal health. Cloacal swabs (<i>N</i> = 453) were collected in the years 2018-2020 from Tanguar and Hakaluki Haors, important wetland ecosystems in Northeastern Bangladesh. The prevalence of <i>Salmonella</i> was 13.5% (61 positive swabs). Classical serotyping identified six serovars: <i>Salmonella enterica</i> subsp. <i>enterica</i> serovars Perth, Kentucky, Albany, Infantis, Weltevreden, and Brancaster. Resistance towards 14 antimicrobials was assessed by broth microdilution minimum inhibitory concentration determination and the antimicrobial resistance (AMR) genotype established by whole-genome sequencing. <i>S.</i> Perth and <i>S.</i> Weltevreden isolates were susceptible and harbored no acquired AMR genes. Isolates from the remaining serovars were multidrug resistant, commonly possessing resistance to tetracycline, ampicillin, chloramphenicol, sulfamethoxazole, trimethoprim, and ciprofloxacin. <i>Salmonella</i> resistant to ciprofloxacin meets WHO criteria for priority pathogens. There was excellent concordance between resistance phenotype and the presence of corresponding AMR genes, many of which reside on <i>Salmonella</i> Genomic Islands. High-level ciprofloxacin resistance correlated with the presence of mutations in the chromosomal <i>gyrB</i> and/or <i>parC</i> genes. The <i>S.</i> Kentucky isolates were ST198, a widely distributed multidrug-resistant lineage reported in humans and animals, and constituting an ongoing risk to public health worldwide. We have demonstrated that multidrug-resistant non-typhoidal <i>Salmonella</i> of public health significance can be recovered from migratory birds. A potential for risk can manifest through direct interaction, transmission to food-producing livestock on farms, and dissemination via the long range migratory movements of birds. Risks can be mitigated by measures including continued surveillance and implementation of good farm biosecurity practices.