Study on the factors affecting the resistance and transmission of Staphylococcus aureus in the 'animal-environment-worker' of the broiler feeding cycle

Fangyuan Hu ¹ Yaopeng Liu ¹ Wang Lin ² Juan Wang ^2* Na Liu ² Yan Li ^3* Xiaoxiao Duan ^3* Junwei Wang ^2* Mingzhe Lu ^2* Keguang Han ^1* Zhina Qu ^2* Junhui Liu ^2*

• ¹ College of Veterinary Medicine, Shanxi Agricultural University, Jinzhong, China
• ² China Animal Health and Epidemiology Center, Qingdao, Shandong Province, China
• ³ Qingdao Center for Animal Disease Control and Prevention, Qingdao, Shandong Province, China

Multidrug-resistant Staphylococcus aureus (S.aureus) poses an increasingly serious threat to agricultural safety and public health. Based on the concept of "One Health", this study analysed the multidrug resistance and transmission factors of S. aureus isolated from the "animal-environment-human" interface during one feeding cycle of commercial broilers in China by using antimicrobial susceptibility testing and whole genome sequencing (WGS) technologies. The results showed that in stage 1, the isolation rate of S. aureus was 1.32% (6/453), that of workers was 25.0% (4/16), and that of environment samples was 0.69% (2/287), the multidrug-resistance rate was 83.33%. After one feeding cycle, the isolation rate of S. aureus (221/772, 28.63%) increased significantly (P < 0.01) during stage 2, and the multi-resistance rate was as high as 97%.The resistance rate to eight drugs including erythromycin, clindamycin, enrofloxacin, oxfloxacin, doxycycline, fosfenicol, tylosin, and tamagliflozin were elevated, but the differences were not significant (P > 0.05). The dominant strain in both stages was ST398 (79.13%), which was prevalent in 11 types of samples from three sources and clustered in the same sub-branch of the SNP evolutionary tree, and the loci of difference between strains ranged from 1-541, and with SNPs of less than 10 between the human strains of stage1 and three sources in stage 2. The 42 representative strains carried mobile elements mainly plasmid replicons (10 types), transposons (3 types) and 20 antibiotic resistance genes in 9 classes. 10 ST398 strains found the fosB gene for fosfomycin resistance, and 6 ST9 strains from stage 2 found the mecA resistance gene, the SNP evolutionary analysis showed that the fosB resistance gene might have been brought in by workers during stage 1. This study reveals the critical impact of environmental residual and worker-carried S. aureus, as well as the transmission of antibiotic resistance in stage 1. It highlighted the importance of the "One Health" approach and biosecurity measures and provided recommendations for the prevention of the spread of pathogens and resistance.