Comparable High Rates of Extended-Spectrum-Beta-Lactamase-Producing Escherichia coli in Birds of Prey from Germany and Mongolia

Abstract

Frequent contact with human waste and liquid manure from intensive livestock breeding, and the increased loads of antibiotic-resistant bacteria that result, are believed to be responsible for the high carriage rates of ESBL-producing E. coli found in birds of prey (raptors) in Central Europe. To test this hypothesis against the influence of avian migration, we initiated a comparative analysis of faecal samples from wild birds found in Saxony-Anhalt in Germany and the Gobi-Desert in Mongolia, regions of dissimilar human and livestock population characteristics and agricultural practices. We sampled a total of 281 wild birds, mostly raptors with primarily north-to-south migration routes. We determined antimicrobial resistance, focusing on ESBL production, and unravelled the phylogenetic and clonal relatedness of identified ESBL-producing E. coli isolates using multi-locus sequence typing (MLST) and macrorestriction analyses. Surprisingly, the overall carriage rates (approximately 5%) and the proportion of ESBL-producers among E. coli (Germany: 13.8%, Mongolia: 10.8%) were similar in both regions. Whereas bla CTX-M-1 predominated among German isolates (100%), bla CTX-M-9 was the most prevalent in Mongolian isolates (75%). We identified sequence types (STs) that are well known in human and veterinary clinical ESBL-producing E. coli (ST12, ST117, ST167, ST648) and observed clonal relatedness between a Mongolian avian ESBL-E. coli (ST167) and a clinical isolate of the same ST that originated in a hospitalised patient in Europe. Our data suggest the influence of avian migratory species in the transmission of ESBL-producing E. coli and challenge the prevailing assumption that reducing human influence alone invariably leads to lower rates of antimicrobial resistance.

Molecular Characterization of Extended-Spectrum-Cephalosporin-Resistant Enterobacteriaceae from Wild Kelp Gulls in South America

“…However, our study revealed a higher occurrence among kelp gulls in accordance with studies regarding Brown-headed gulls and Franklin's gulls (5). Although the resistance gene families described in this study are similar to those reported previously (2,4,5,12,(14)(15)(16)(17)(18)(19), we documented for the first time the presence of bla SHV-2A and the predominance of bla CTX-M-2 among wild birds. The latter mirrors the situation observed for nosocomial infections in Argentinian hospitals (20,21), confirming the endemicity of bla CTX-M-2 within this area and its potential transmission from humans to wild birds and/or vice versa.…”

“…Several studies have documented the occurrence of ESC r Enterobacteriaceae isolates among wild birds at prevalences ranging from 0% to 37% (4,(11)(12)(13)(14)(15). However, our study revealed a higher occurrence among kelp gulls in accordance with studies regarding Brown-headed gulls and Franklin's gulls (5).…”

“…Among the 17 different STs detected here, we identified several, namely, ST10, ST69, ST101, ST117, ST167, ST617, and ST744, that have been previously reported from ESC r E. coli isolates of human and animal origin (1,5,12,15). Interestingly, some of the identified STs (ST10, ST117, ST157, ST359, ST617, and ST744) have been previously reported among wild birds as well, but they have been found to harbor different extended-spectrum cephalosporinase genes, suggesting that avian commensal E. coli strains play a role in the maintenance and dissemination of these genes (1,5,12,15 (23).…”

Clinical Epidemiology and Molecular Analysis of Extended-Spectrum-β-Lactamase-Producing Escherichia coli in Nepal: Characteristics of Sequence Types 131 and 648

“…Human isolates of CTX-M-producing E. coli ST648 have been reported from various geographical regions, such as Europe, North and South America, Africa, and Asia; the majority of these isolates belong to phylotype D (22)(23)(24)(25). CTX-Mproducing E. coli ST648 strains have also been isolated from wild birds in Mongolia and Germany (24,(26)(27)(28) and from companion and livestock animals in European countries (24,29,30). A recent study on ESBL-producing E. coli isolates (n ϭ 1,152) sampled in Europe, predominantly from dogs, cats, and horses, identified 40 (3.5%) ESBL-producing E. coli strains as ST648 (phylotype D, CTX-M-15 positive; 72.5%), whereas ST131 isolates (phylotype B2, CTX-M-15-positive; 46.9%) occurred less frequently (2.8%) (30).…”

Molecular Typing of CTX-M-Producing Escherichia coli Isolates from Environmental Water, Swine Feces, Specimens from Healthy Humans, and Human Patients

“…Although the ST38 and ST648 groups originated mainly from humans, hospitalized patients accounted for 36.8% (7/19) of isolates in the ST648 group compared with 18.8% (3/16) in the ST38 group. ST648 isolates possessing ␤-lactamases have been identified worldwide (40,42,46), suggesting that ST648 ESBLs may contribute to the spread of the ␤-lactamase gene and that these isolates may be more likely than others to cause extraintestinal infections, ultimately resulting in multidrug resistance.…”