Genomic Investigation of Antimicrobial-Resistant Salmonella enterica Isolates From Dead Chick Embryos in China

Mohammed Elbediwi; Yanting Tang; Dawei Shi; Hazem Ramadan; Yaohui Xu; Sihong Xu; Yan Li; Min Yue

doi:10.3389/fmicb.2021.684400

Genomic Investigation of Antimicrobial-Resistant Salmonella enterica Isolates From Dead Chick Embryos in China

Front Microbiol. 2021 Aug 23:12:684400. doi: 10.3389/fmicb.2021.684400. eCollection 2021.

Authors

Mohammed Elbediwi¹, Yanting Tang¹, Dawei Shi², Hazem Ramadan^{3

4}, Yaohui Xu⁵, Sihong Xu², Yan Li^{1

6

7}, Min Yue^{1

6

7

8}

Affiliations

¹ Department of Veterinary Medicine, Institute of Preventive Veterinary Sciences, Zhejiang University College of Animal Sciences, Hangzhou, China.
² National Institutes for Food and Drug Control, Beijing, China.
³ Hygiene and Zoonoses Department, Faculty of Veterinary Medicine, Mansoura University, Mansoura, Egypt.
⁴ Bacterial Epidemiology and Antimicrobial Resistance Research Unit, United States National Poultry Research Center, United States Department of Agriculture, Agricultural Research Service (USDA-ARS), Athens, GA, United States.
⁵ College of Veterinary Medicine, Henan University of Animal Husbandry and Economy, Zhengzhou, China.
⁶ Hainan Institute of Zhejiang University, Sanya, China.
⁷ Zhejiang Provincial Key Laboratory of Preventive Veterinary Medicine, Hangzhou, China.
⁸ State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, National Clinical Research Center for Infectious Diseases, National Medical Center for Infectious Diseases, The First Affiliated Hospital, College of Medicine, Zhejiang University, Hangzhou, China.

Abstract

Salmonella spp. is recognized as an important zoonotic pathogen. The emergence of antimicrobial resistance in Salmonella enterica poses a great public health concern worldwide. While the knowledge on the incidence and the characterization of different S. enterica serovars causing chick embryo death remains obscure in China. In this study, we obtained 45 S. enterica isolates from 2,139 dead chick embryo samples collected from 28 breeding chicken hatcheries in Henan province. The antimicrobial susceptibility assay was performed by the broth microdilution method and the results showed that 31/45 (68.8%) isolates were multidrug-resistant (≥3 antimicrobial classes). Besides the highest resistance rate was observed in the aminoglycoside class, all the isolates were susceptible to chloramphenicol, azithromycin, and imipenem. Furthermore, genomic characterization revealed that S. Enteritidis (33.33%; 15/45) was a frequent serovar that harbored a higher number of virulence factors compared to other serovars. Importantly, genes encoding β-lactamases were identified in three serovars (Thompson, Enteritidis, and Kottbus), whereas plasmid-mediated quinolone resistance genes (qnrB4) were detected in certain isolates of S. Thompson and the two S. Kottbus isolates. All the examined isolates harbored the typical virulence factors from Salmonella pathogenicity islands 1 and 2 (SPI-1 and SPI-2). Additionally, a correlation analysis between the antimicrobial resistance genes, phenotype, and plasmids was conducted among Salmonella isolates. It showed strong positive correlations (r < 0.6) between the different antimicrobial-resistant genes belonging to certain antimicrobial classes. Besides, IncF plasmid showed a strong negative correlation (r > -0.6) with IncHI2 and IncHI2A plasmids. Together, our study demonstrated antimicrobial-resistant S. enterica circulating in breeding chicken hatcheries in Henan province, highlighting the advanced approach, by using genomic characterization and statistical analysis, in conducting the routine monitoring of the emerging antimicrobial-resistant pathogens. Our findings also proposed that the day-old breeder chicks trading could be one of the potential pathways for the dissemination of multidrug-resistant S. enterica serovars.

Keywords: Salmonella; antimicrobial resistance; chicken embryo; correlation; genomic characterization; virulence factor.