Phenotypic and genotypic characterization of antimicrobial resistance profiles in Salmonella isolated from waterfowl in 2002-2005 and 2018-2020 in Sichuan, China

Ying Guan; Yanwan Li; Jin Li; Zhishuang Yang; Dekang Zhu; Renyong Jia; Mafeng Liu; Mingshu Wang; Shun Chen; Qiao Yang; Ying Wu; Shaqiu Zhang; Qun Gao; Xumin Ou; Sai Mao; Juan Huang; Di Sun; Bin Tian; Anchun Cheng; Xinxin Zhao

doi:10.3389/fmicb.2022.987613

Phenotypic and genotypic characterization of antimicrobial resistance profiles in Salmonella isolated from waterfowl in 2002-2005 and 2018-2020 in Sichuan, China

Front Microbiol. 2022 Oct 6:13:987613. doi: 10.3389/fmicb.2022.987613. eCollection 2022.

Authors

Ying Guan¹, Yanwan Li¹, Jin Li¹, Zhishuang Yang¹, Dekang Zhu^{1

2

3}, Renyong Jia^{1

2

3}, Mafeng Liu^{1

2

3}, Mingshu Wang^{1

2

3}, Shun Chen^{1

2

3}, Qiao Yang^{1

2

3}, Ying Wu^{1

2

3}, Shaqiu Zhang^{1

2

3}, Qun Gao¹, Xumin Ou¹, Sai Mao¹, Juan Huang¹, Di Sun¹, Bin Tian¹, Anchun Cheng^{1

1

1}, Xinxin Zhao^{1

1

1}

Affiliations

¹ Institute of Preventive Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China.
² Research Center of Avian Diseases, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu, Sichuan, China.
³ Key Laboratory of Animal Disease and Human Health of Sichuan Province, Chengdu, Sichuan, China.

Abstract

Salmonella enterica is a widespread foodborne pathogen with concerning antimicrobial resistance (AMR). Waterfowl are a major source of Salmonella transmission, but there are few systematic studies on Salmonella prevalence in waterfowl species. In this study, 126 Salmonella isolates (65 collected in 2018-2020 and 61 collected in 2002-2005) were obtained from waterfowl samples in Sichuan, China. Their serotypes, pulsed-field gel electrophoresis (PFGE) types, and phenotypic and genotypic AMR profiles were systematically examined. The isolates were distributed in 7 serotypes, including serovars Enteritidis (46.0%), Potsdam (27.8%), Montevideo (7.9%), Cerro (6.3%), Typhimurium (4.8%), Kottbus (4.0%) and Apeyeme (3.2%). Their PFGE characteristics were diverse; all isolates were distributed in four groups (cutoff value: 60.0%) and 20 clusters (cutoff value: 80.0%). Moreover, all isolates were multidrug resistant, and high rates of AMR to lincomycin (100.0%), rifampicin (100.0%), sulfadiazine (93.7%), erythromycin (89.7%), ciprofloxacin (81.0%), and gentamicin (75.4%) were observed. Finally, 49 isolates were subjected to whole-genome sequencing, and a wide variety of AMR genes were found, including multiple efflux pump genes and specific resistance genes. Interestingly, the tet(A)/tet(B) and catII resistance genes were detected in only isolates obtained in the first collection period, while the gyrA (S83F, D87N and D87G) and gyrB (E466D) mutations were detected at higher frequencies in the isolates obtained in the second collection period, supporting the findings that isolates from different periods exhibited different patterns of resistance to tetracycline, chloramphenicol and nalidixic acid. In addition, various incompatible plasmid replicon fragments were detected, including Col440I, Col440II, IncFIB, IncFII, IncX1, IncX9, IncI1-I and IncI2, which may contribute to the horizontal transmission of AMR genes and provide competitive advantages. In summary, we demonstrated that the Salmonella isolates prevalent in Sichuan waterfowl farms exhibited diverse serotypes, multiple AMR phenotypes and genotypes, and AMR changes over time, indicating their potential risks to public health.

Keywords: Salmonella; antimicrobial resistance; prevalence; pulsed-field gel electrophoresis; serotypes; waterfowl.