Genotypic characterization and antimicrobial susceptibility of human Campylobacter jejuni isolates in Southern Spain

Abstract

Campylobacter jejuni is the main cause of bacterial gastroenteritis and a public health problem worldwide. Little information is available on the genotypic characteristics of human C. jejuni in Spain. This study is based on an analysis of the resistome, virulome, and phylogenetic relationship, antibiogram prediction, and antimicrobial susceptibility of 114 human isolates of C. jejuni from a tertiary hospital in southern Spain from October 2020 to June 2023. The isolates were sequenced using Illumina technology, and a bioinformatic analysis was subsequently performed. The susceptibility of C. jejuni isolates to ciprofloxacin, tetracycline, and erythromycin was also tested. The resistance rates for each antibiotic were 90.3% for ciprofloxacin, 66.7% for tetracycline, and 0.88% for erythromycin. The fluoroquinolone resistance rate obtained is well above the European average (69.1%). CC-21 (n = 23), ST-572 (n = 13), and ST-6532 (n = 13) were the most prevalent clonal complexes (CCs) and sequence types (STs). In the virulome, the cadF, ciaB, and cdtABC genes were detected in all the isolates. A prevalence of 20.1% was obtained for the genes wlaN and cstIII, which are related to the pathogenesis of Guillain-Barré syndrome (GBS). The prevalence of the main antimicrobial resistance markers detected were CmeABC (92.1%), RE-cmeABC (7.9%), the T86I substitution in gyrA (88.9%), bla_OXA-61 (72.6%), tet(O) (65.8%), and ant (6)-Ia (17.1%). High antibiogram prediction rates (>97%) were obtained, except for in the case of the erythromycin-resistant phenotype. This study contributes significantly to the knowledge of C. jejuni genomics for the prevention, treatment, and control of infections caused by this pathogen.IMPORTANCEDespite being the pathogen with the greatest number of gastroenteritis cases worldwide, Campylobacter jejuni remains a poorly studied microorganism. A sustained increase in fluoroquinolone resistance in human isolates is a problem when treating Campylobacter infections. The development of whole genome sequencing (WGS) techniques has allowed us to better understand the genotypic characteristics of this pathogen and relate them to antibiotic resistance phenotypes. These techniques complement the data obtained from the phenotypic analysis of C. jejuni isolates. The zoonotic transmission of C. jejuni through the consumption of contaminated poultry supports approaching the study of this pathogen through "One Health" approach. In addition, due to the limited information on the genomic characteristics of C. jejuni in Spain, this study provides important data and allows us to compare the results with those obtained in other countries.

Keywords: Campylobacter jejuni; antimicrobial resistance; epidemiology; virulome; whole-genome sequencing.

Fig 1

Phylogenetic analysis of 114 isolates of C. jejuni. A neighbor-joining phylogenetic tree was constructed to establish the phylogenetic relationships among the isolates based on allelic distances from the cgMLST scheme. The clades are denoted by the numbers 1, 2, 3, 4, and 5. Clade 5 is divided into subclades 5.1, 5.2, and 5.3. Clonal complexes (CCs), sequence types (STs), and core genome sequence types (cgSTs) are listed on the labels of each isolate. The presence of antimicrobial resistance at markers and virulence factors is visualized by circles in colors for each gene. Location (Cadiz and San Fernando) and year of isolation (from 2021 to 2023) are represented in colors. The isolates that could not be assigned a single cgST are labeled “na” (not assigned). The presence of the RE-cmeABC operon is indicated by a small red circle. (*) 23S rRNA mutations.