Abstract
Campylobacter spp. are the most frequent agent of human gastroenteritis worldwide, and the spread of multidrug-resistant strains makes the clinical treatment difficult. The current study presents the resistome analysis of 39,798 Campylobacter jejuni and 11,920 Campylobacter coli genomes available in public repositories. Determinants of resistance to β-lactams (Be) and tetracyclines (Te) were the most frequent for both species, with resistance to quinolones (Qu) as the third most important on C. jejuni and to aminoglycosides (Am) on C. coli. Moreover, resistance to Te, Qu, and Am was frequently found in co-occurrence with resistance to other antibiotic families. Geographical differences on clonal complexes distribution were found for C. jejuni and on resistome genotypes for both C. jejuni and C. coli species. Attending to the resistome patterns by isolation source, three main clusters of genomes were found on C. jejuni genomes at antimicrobial resistance gene level. The first cluster was formed by genomes from human, food production animals (e.g., sheep, cow, and chicken), and food (e.g., dairy products) isolates. The higher incidence of tet(O), associated with tetracycline resistance, and the gyrA (T86I) single-nucleotide polymorphism (SNP), associated with quinolone resistance, among genomes from this cluster could be due to the intense use of these antibiotics in veterinary and human clinical settings. Similarly, a high incidence of tet(O) genes of C. coli genomes from pig, cow, and turkey was found. Moreover, the cluster based on resistome patterns formed by C. jejuni and C. coli genomes of human, turkey, and chicken origin is in agreement with previous observations reporting chicken or poultry-related environments as the main source of human campylobacteriosis infections. Most clonal complexes (CCs) associated with chicken host specialization (e.g., ST-354, ST-573, ST-464, and ST-446) were the CCs with the highest prevalence of determinants of resistance to Be, Qu, and Te. Finally, a clear trend toward an increase in the occurrence of Te and Qu resistance determinants on C. jejuni, linked to the spread of the co-occurrence of the blaOXA–61 and tet(O)-tet(O/W/O) genes and the gyrA (T86I) SNP, was found from 2001 to date in Europe.
Highlights
Thermophilic Campylobacter species, and specially Campylobacter jejuni and Campylobacter coli, are the most frequent agents of human gastroenteritis both in industrialized countries (Kaakoush et al, 2015; European Food Safety Authority, 2018) and in low- and middle-income countries (Fischer Walker et al, 2013; Liu et al, 2015), with C. jejuni accounting for up to 80% of all human Campylobacter gastroenteritis cases (Bronnec et al, 2016), with estimations of over 800,000 cases per year between 2000 and 2008 (Scallan et al, 2011)
Campylobacter jejuni and C. coli are present in the digestive tract of different animals, including birds, cattle, sheep, pigs, and pets (Thépault et al, 2017), chicken is recognized as the main source of human infection in most countries (Domingues et al, 2012; Newell et al, 2017; Cody et al, 2019)
The C. jejuni genomes belonged to 41 clonal complexes (CCs), with ST21 CC being the most abundant (23.8% of the analyzed genomes) followed by sequence types (ST)-353 and ST-45 CCs (8.9 and 7.8% of the analyzed genomes, respectively), while C. coli genomes belonged to 21 CCs, with ST-828 CC as the main CC (84.8% of analyzed genomes)
Summary
Thermophilic Campylobacter species, and specially Campylobacter jejuni and Campylobacter coli, are the most frequent agents of human gastroenteritis both in industrialized countries (Kaakoush et al, 2015; European Food Safety Authority, 2018) and in low- and middle-income countries (Fischer Walker et al, 2013; Liu et al, 2015), with C. jejuni accounting for up to 80% of all human Campylobacter gastroenteritis cases (Bronnec et al, 2016), with estimations of over 800,000 cases per year between 2000 and 2008 (Scallan et al, 2011). Campylobacter jejuni and C. coli are present in the digestive tract of different animals, including birds, cattle, sheep, pigs, and pets (Thépault et al, 2017), chicken is recognized as the main source of human infection in most countries (Domingues et al, 2012; Newell et al, 2017; Cody et al, 2019). Macrolides (mainly erythromycin), fluoroquinolones (mainly ciprofloxacin), and tetracyclines are the most commonly used and effective antibiotics (Aarestrup et al, 2008; Silva et al, 2011). These antimicrobial agents have analogs widely employed in veterinary settings, and their overuse or misuse have favored the emergence and spread of resistant Campylobacter isolates (Van Boeckel et al, 2015; Asuming-Bediako et al, 2019). The continuous increase in resistance to certain antimicrobial classes has been accompanied by a rise in the occurrence of multidrug-resistant (MDR) C. jejuni and C. coli from farm to fork (Mourkas et al, 2019)
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