Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China

Changyan Ju; Yanping Ma; Bi Zhang; Guilan Zhou; Hairui Wang; Muhua Yu; Jiaoming He; Yongxiang Duan; Maojun Zhang

doi:10.3389/fmicb.2023.1152719

Prevalence, genomic characterization and antimicrobial resistance of Campylobacter spp. isolates in pets in Shenzhen, China

Front Microbiol. 2023 Jun 1:14:1152719. doi: 10.3389/fmicb.2023.1152719. eCollection 2023.

Authors

Changyan Ju^#¹, Yanping Ma^#¹, Bi Zhang², Guilan Zhou³, Hairui Wang³, Muhua Yu¹, Jiaoming He¹, Yongxiang Duan¹, Maojun Zhang³

Affiliations

¹ Laboratory, Nanshan Center for Disease Control and Prevention, Shenzhen, China.
² Clinic, IVC Shenzhen Animal Hospital, Shenzhen, China.
³ State Key Laboratory of Infectious Disease Prevention and Control, Chinese Center for Disease Control and Prevention, Beijing, China.

^# Contributed equally.

Abstract

The prevalence of Campylobacter spp.in pets is a potential concern for human health. However, little is known about the pet-related Campylobacter spp. in China. A total of 325 fecal samples were collected from dogs, cats, and pet foxes. Campylobacter spp. were isolated by culture, and MALDI-TOF MS was used to identify 110 Campylobacter spp. isolates in total. C. upsaliensis (30.2%, 98/325), C. helveticus (2.5%, 8/325), and C. jejuni (1.2%, 4/325) were the three found species. In dogs and cats, the prevalence of Campylobacter spp. was 35.0% and 30.1%, respectively. A panel of 11 antimicrobials was used to evaluate the antimicrobial susceptibility by the agar dilution method. Among C. upsaliensis isolates, ciprofloxacin had the highest rate of resistance (94.9%), followed by nalidixic acid (77.6%) and streptomycin (60.2%). Multidrug resistance (MDR) was found in 55.1% (54/98) of the C. upsaliensis isolates. Moreover, 100 isolates, including 88 C. upsaliensis, 8 C. helveticus, and 4 C. jejuni, had their whole genomes sequenced. By blasting the sequence against the VFDB database, virulence factors were identified. In total, 100% of C. upsaliensis isolates carried the cadF, porA, pebA, cdtA, cdtB, and cdtC genes. The flaA gene was present in only 13.6% (12/88) of the isolates, while the flaB gene was absent. By analyzing the sequence against the CARD database, we found that 89.8% (79/88) of C. upsaliensis isolates had antibiotic target alteration in the gyrA gene conferring resistance to fluoroquinolone, 36.4% (32/88) had the aminoglycoside resistance gene, and 19.3% (17/88) had the tetracycline resistance gene. The phylogenetic analysis using the K-mer tree method obtained two major clades among the C. upsaliensis isolates. All eight isolates in subclade 1 possessed the gyrA gene mutation, the aminoglycoside and tetracycline resistance genes, and were phenotypically resistant to six classes of antimicrobials. It has been established that pets are a significant source of Campylobacter spp. strains and a reservoir for them. This study is the first to have documented the presence of Campylobacter spp. in pets in Shenzhen, China. In this study, C. upsaliensis of subclade 1 required additional attention due to its broad MDR phenotype and relatively high flaA gene prevalence.

Keywords: Campylobacter helveticus; Campylobacter jejuni; Campylobacter upsaliensis; antimicrobial resistance; matrix-assisted laser desorption ionization-time of flight mass spectrum; pets; virulence-associated genes; whole-genome sequencing.

Grants and funding

CJ was taking part in the Sanming Project of Medicine (SZSM201803081), the Key Discipline Construction Subsidy of Nanshan District, and the Nanshan District Science and Technology Plan Project (2020049). The study design, data collection, interpretation, and the choice to submit the study for publication were all independent of the funders.