Abstract
Extended-spectrum-cephalosporin-resistant Enterobacteriaceae are a public health concern due to limited treatment options. Here, we report on the occurrence and the molecular characteristics of extended-spectrum-cephalosporin-resistant Enterobacteriaceae recovered from wild birds (kelp gulls). Our results revealed kelp gulls as a reservoir of various extended-spectrum cephalosporinase genes associated with different genetic platforms. In addition, we report for the first time the presence of a known epidemic clone of Salmonella enterica serotype Heidelberg (JF6X01.0326/XbaI.1966) among wild birds.
TEXT
Extended-spectrum-cephalosporinase-producing Enterobacteriaceae have been reported worldwide among isolates obtained from humans and from food-producing and companion animals, as well as from environmental sources (1). In spite of the limited number of studies regarding the occurrence of antibiotic resistance in natural environments, where animals do not naturally come into contact with antibiotics, the occurrence of extended-spectrum-cephalosporin-resistant (ESCr) Enterobacteriaceae has been detected lately in wild birds, especially in populations of gulls (Laridae) (2–7). The kelp gull (Larus dominicanus) is a large gull species distributed in coastal areas through much of the Southern Hemisphere and is the only gull species inhabiting the Antarctic continent. It is known to be a food generalist, regularly feeding on food resulting from human activities (abattoirs, garbage, sewage outfalls, etc.) (8). This behavior makes it an interesting sentinel species for the study of the environmental spread of antibiotic-resistant bacteria. Our aim was to determine the occurrence and the molecular characteristics of ESCr Enterobacteriaceae isolates recovered from kelp gulls, as this species could favor the dissemination of ESCr Enterobacteriaceae in human populations and in the pristine Antarctic environment.
(Preliminary results from this study were presented as an oral presentation at the 26th European Congress of Clinical Microbiology and Infectious Diseases [ECCMID], 9 to 12 April 2016, Amsterdam, the Netherlands.)
During November 2012, fresh fecal specimens (n = 50) were collected from a flock of approximately 500 kelp gulls on a sandy beach where they were roosting in Ushuaia, in Argentina. All samples were enriched either in brain heart infusion broth (Becton-Dickinson, Franklin Lakes, NJ, USA), supplemented with 16 mg/liter vancomycin, or in buffered peptone water (SVA, Uppsala, Sweden) for 18 to 24 h in 37°C and subsequently inoculated on ChromID ESBL (bioMérieux, Solna, Sweden) for the selective isolation of extended-spectrum-β-lactamase (ESBL)-producing Enterobacteriaceae or on modified semisolid Rappaport Vassiliadis agar (SVA, Uppsala, Sweden) for the selective isolation of Salmonella species, respectively. Presumptive extended-spectrum-cephalosporinase-producing isolates were identified using matrix-assisted laser desorption ionization–time of flight (MALDI-TOF) mass spectrometry (Brucker, Coventry, United Kingdom), while Salmonella isolates were further serotyped by the microtitration method. Antibiotic susceptibility of the isolates was assessed by broth microdilution and interpreted according the epidemiologic cutoff values recommended by the European Committee on Antimicrobial Susceptibility Testing (http://mic.eucast.org), whereas ESBL and/or AmpC production was evaluated by a combined disc test, as previously described (9).
Genes conferring the ESCr phenotype were sought and their genetic location on either the chromosome or a plasmid was determined as previously described (9). Standard methods (PCR-based replicon [rep] typing, plasmid multilocus sequence typing [pMLST]/plasmid double-locus sequence typing [pDLST]/replicon sequence typing [RST], and S1 nuclease pulsed-field gel electrophoresis [PFGE]) were applied for further plasmid analysis, while the conjugal transferability of the extended-spectrum cephalosporinase genes and the presence of known insertion sequences (ISs) upstream of them were examined (9). Genetic relatedness among Escherichia coli and Salmonella enterica serotype Heidelberg isolates was assessed by MLST and XbaI-PFGE typing, respectively, as previously described (9, 10).
Overall, we recovered 37 nonduplicate ESCr Enterobacteriaceae isolates from 34 of the fecal samples included in the study. Among them, 91.9% (n = 34) were identified as E. coli and 8.1% (n = 3) as S. Heidelberg. The copresence of ESCr E. coli and S. Heidelberg was documented in three fecal samples. The recovered isolates exhibited non-wild-type MICs mainly for ciprofloxacin (n = 27; 73.0%), nalidixic acid (n = 25; 67.6%), tetracycline (n = 22; 59.5%), sulfamethoxazole (n = 20; 54.0%), and chloramphenicol (n = 15; 40.5%). All isolates were susceptible to meropenem and tigecycline, whereas they exhibited non-wild-type MICs for the remaining tested agents (ranging from 5.4% to 27.0%). All E. coli isolates exhibited an ESBL phenotype and carried blaCTX-M-2 (n = 14; 41.2%), blaCTX-M-14 (n = 11; 32.3%), blaSHV-2 (n = 4; 11.8%), blaSHV-2A (n = 4; 11.8%), and blaCTX-M-15 (n = 1; 2.9%) genes, whereas all S. Heidelberg isolates exhibited an AmpC phenotype and carried the blaCMY-2 gene.
The broad-host-range IncI1 (n = 21; 67.7%) and narrow-host-range IncF (n = 7; 22.6%) plasmids were by far the most common rep types accounted for the ESCr phenotype among the recovered isolates. The blaCTX-M-2 gene was found mainly on the chromosome (n = 6; 42.9%) or on plasmids of different replicon types, including IncF plasmids with fused FIB-FII replicons (n = 5; 35.7%), IncHI2 (n = 1; 7.1%), IncA/C (n = 1; 7.1%), and nontypeable ones (n = 1; 7.14%). The blaCTX-M-14 and blaCTX-M-15 genes were identified exclusively on IncI1/sequence type 80 (ST80) and IncFIA-FIB plasmids, respectively. The blaSHV-2 gene was associated with IncI1/ST12 and blaSHV-2A with IncI1/ST187 and IncFIA-FIB plasmids, whereas the blaCMY-2 gene was located on IncI1/ST12 plasmids. Detailed results regarding the subtyping, the size, and the transferability of the plasmids are summarized in Table 1.
TABLE 1.
Characteristics of ESCr Enterobacteriaceae isolates recovered from kelp gulls (Larus dominicanus) in Ushuaia, Argentina, in 2012a
| Species (no. of isolates) | ST/PFGE type (no. of isolates) | Resistance phenotypes (no. of isolates) | ESBL/AmpC gene (no. of isolates) | Location (no. of isolates) | Plasmid characteristic(s) |
Upstream region | ||
|---|---|---|---|---|---|---|---|---|
| Plasmid type/subtype (no. of isolates) | Size (kb) | Transferability | ||||||
| E. coli (34) | ST744 (6) | AMP, CAZ, CHL, CIP, CST, CTX, NAL, SMX, TET, TMP (1) | blaCTX-M-14 (6) | Plasmid (6) | IncI1/ST80 (6) | 105 | Conjugative | —e |
| AMP, AZM, CAZ, CHL, CIP, CTX, NAL, SMX, TET, TMP (2) | ||||||||
| AMP, CHL, CIP, CST, CTX, NAL, SMX, TET, TMP (3) | ||||||||
| ST617 (5) | AMP, CAZ, CHL, CIP, CTX, NAL, TET (4) | blaSHV-2A (4) | Plasmid (4) | IncI1/ST187 (3) | 125 | Conjugative | IS26 | |
| IncF/F1:A1:B1 (1) | 70 | Conjugative | IS26 | |||||
| AMP, CAZ, CIP, CTX, NAL, TET (1) | blaCTX-M-14 (1) | Plasmid (1) | IncI1/ST80 (1) | 105 | Conjugative | —e | ||
| ST57 (3) | AMP, CAZ, CIP, CTX, GEN, NAL, SMX, TET, TMP (3) | blaCTX-M-2 (3) | Plasmid (3) | IncF/F18:A-:B1 (3) | 208 | Conjugative | ISCR1 | |
| ST93 (3) | AMP, CAZ, CHL, CTX, SMX, TMP (1) | blaCTX-M-2 (3) | Plasmid (1) | IncHI2/ST2 (1) | 202 | Conjugative | ISCR1 | |
| AMP, CAZ, CIP, CTX, GEN, SMX (1) | Chromosome (2) | NA | NA | Nonconjugatived | ISCR1 | |||
| AMP, CAZ, CTX, SMX, TET (1) | ||||||||
| ST4038 (3) | AMP, CAZ, CTX (3) | blaSHV-2 (3) | Plasmid (3) | IncI1/ST12 (3) | 145 | Conjugative | IS26 | |
| ST10 (2) | AMP, CAZ, CTX, TET (1) | blaCTX-M-14 (2) | Plasmid (2) | IncI1/ST80 (2) | 105 | Conjugative | —e | |
| AMP, CHL, CIP, CTX (1) | ||||||||
| STNew1 (2)b | AMP, CAZ, CIP, CTX, NAL (1) | blaCTX-M-14 (1) | Plasmid (1) | IncI1/ST80 (1) | 105 | Conjugative | —e | |
| AMP, CAZ, CHL, CIP, CTX, GEN, NAL, SMX (1) | blaCTX-M-2 (1) | Chromosome (1) | NA | NA | Nonconjugatived | ISCR1 | ||
| ST69 (1) | AMP, CAZ, CTX, SMX, TET (1) | blaCTX-M-2 (1) | Chromosome (1) | NA | NA | Nonconjugatived | ISCR1 | |
| ST88 (1) | AMP, CTX, TET (1) | blaCTX-M-14 (1) | Plasmid (1) | IncI1/ST80 (1) | 105 | Conjugative | —e | |
| ST101 (1) | AMP, CAZ, CIP, CST, CTX, NAL, SMX, TET (1) | blaCTX-M-2 (1) | Plasmid (1) | IncA/C (1) | 100 | Nonconjugatived | ISCR1 | |
| ST117 (1) | AMP, CAZ, CIP, CTX, NAL, SMX (1) | blaCTX-M-2 (1) | Plasmid (1) | NT (1) | 132 | Conjugative | ISCR1 | |
| ST212 (1) | AMP, CAZ, CTX (1) | blaSHV-2 (1) | Plasmid (1) | IncI1/ST12 (1) | 121 | Conjugative | IS26 | |
| ST359 (1) | AMP, CAZ, CHL, CIP, CTX, NAL, SMX, TET (1) | blaCTX-M-2 (1) | Plasmid (1) | IncF/F24:A-:B1 (1) | 170 | Conjugative | ISCR1 | |
| ST1011 (1) | AMP, CAZ, CIP, CTX, GEN, NAL, SMX (1) | blaCTX-M-2 (1) | Chromosome (1) | NA | NA | Nonconjugatived | ISCR1 | |
| ST1193 (1) | AMP, CAZ, CIP, CTX, NAL, TET (1) | blaCTX-M-15 (1) | Plasmid (1) | IncF/F1:A1:B1 (1) | 87 | Nonconjugatived | ISEcp1 | |
| ST2485 (1) | AMP, CAZ, CHL, CTX, SMX, TET (1) | blaCTX-M-2 (1) | Plasmid (1) | IncF/F24:A-:B10 (1) | 205 | Conjugative | ISCR1 | |
| STNew2 (1)b | AMP, CAZ, CIP, CTX, NAL, SMX (1) | blaCTX-M-2 (1) | Chromosome (1) | NA | NA | Nonconjugatived | ISCR1 | |
| S. Heidelberg (3) | JF6X01.0326 (3)c | AMP, CAZ, CIP, CTX, NAL (3) | blaCMY-2 (3) | Plasmid (3) | IncI1/ST12 (3) | 110 | Conjugative | ISEcp1 |
ST, sequence type; AMP, ampicillin; AZM, azithromycin; CAZ, ceftazidime; CIP, ciprofloxacin; CHL, chloramphenicol; CST, colistin; CTX, cefotaxime; GEN, gentamicin; MEM, meropenem; NAL, nalidixic acid; SMX, sulfamethoxazole; TET, tetracycline; TGC, tigecycline; TMP, trimethoprim; NA, not applicable.
Assignment to a specific ST could not be performed, as uploading new sequences and STs based on AB1 files is no longer supported by the MLST database (http://mlst.warwick.ac.uk/mlst/dbs/Ecoli).
PFGE pattern numbers correspond to the PulseNet database.
No transconjugants were obtained after liquid mating experiments, suggesting either the presence of nonconjugative plasmids or conjugation frequencies below the detection limit (≤1 × 10−9).
ISEcp1, ISCR1, or IS26 insertion sequences were not found upstream of the ESBL genes for these STs.
Three insertion sequence elements previously associated with the mobilization and support of extended-spectrum cephalosporinase genes were identified. Briefly, in all isolates carrying blaCTX-M-2, the gene was accompanied upstream by a copy of ISCR1 in the same orientation as the resistance gene, regardless of the plasmid replicon type or whether the gene was chromosomally located (Table 1). Similarly, ISEcp1 was found upstream of the blaCTX-M-15 and blaCMY-2 genes, while IS26 was found upstream of the blaSHV-2 and blaSHV-2A genes. ISEcp1, ISCR1, or IS26 insertion sequences were not found upstream of blaCTX-M-14 gene (Table 1).
High diversity of genotypes was observed among the E. coli isolates, resulting in 17 different STs, each comprised of one to six isolates. The most predominant genotypes were ST744 (n = 6; 17.6%), ST617 (n = 5; 14.7%), ST57 (n = 3; 8.8%), ST93 (n = 3; 8.8%), and ST4038 (n = 3; 8.8%), while isolates belonging to ST10, ST69, ST88, ST101, ST117, ST212, ST359, ST1011, ST1193, ST2485, STNew1, and STNew2 were also identified. All S. Heidelberg isolates belonged to epidemic clone JF6X01.0326/XbaI.1966 (PulseNet database). Different ESBL determinants were found among isolates with the same genotype; conversely, different genotypes carrying the same ESBL determinants were identified (Table 1).
Several studies have documented the occurrence of ESCr Enterobacteriaceae isolates among wild birds at prevalences ranging from 0% to 37% (4, 11–15). 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, 14–19), we documented for the first time the presence of blaSHV-2A and the predominance of blaCTX-M-2 among wild birds. The latter mirrors the situation observed for nosocomial infections in Argentinian hospitals (20, 21), confirming the endemicity of blaCTX-M-2 within this area and its potential transmission from humans to wild birds and/or vice versa. Of note was the association of blaCTX-M-2 gene with ISCR1 on four different plasmid replicon types associated with six different E. coli STs and on the chromosome of five other different E. coli STs, underscoring that ISCR1 has probably played a significant role in the capture of this gene by conjugative plasmids and in its further interreplicon and interclone dissemination. Moreover, our data suggest the horizontal transfer of a conjugative IncI1/ST80 plasmid (105 kb) carrying blaCTX-M-14 among five different E. coli STs, underscoring the dissemination of this gene owing to a successful plasmid-gene combination.
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 ESCr 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). In contrast with the solely ESCr S. Heidelberg isolate carrying blaCMY-2 on a 97-kb IncN plasmid reported previously from an Argentinian adult inpatient (22), here we documented for the first time the presence in wild birds of a known epidemic ESCr S. Heidelberg clone (JF6X01.0326/XbaI.1966), carrying blaCMY-2 on a 110-kb IncI1/ST12 plasmid. This PFGE type, circulating in the United States and recently introduced to Europe (9), has been documented to cause outbreaks and exhibit potency for bloodstream infections (23).
In conclusion, although there are few studies on the presence of resistance genes conferring the ESCr phenotype among Enterobacteriaceae from wild birds, to our knowledge this is the first report presenting a detailed characterization of ESCr Enterobacteriaceae, including the underlying antibiotic resistance gene content and its genetic support (plasmids and IS elements). Our data imply that kelp gulls act as reservoirs of a variety of extended-spectrum cephalosporinase genes associated with different genetic platforms that could facilitate their horizontal transfer. In addition, our findings underscore the potential role of kelp gulls as a bridge species for transfer of ESCr Enterobacteriaceae between humans and wildlife and as a spreader of these isolates among human populations and naturally antibiotic-resistant-bacterium-free environments (Antarctic continent) via their movement and migration.
ACKNOWLEDGMENTS
We gratefully acknowledge Kees Veldman, Joop Testerink, and Marga Japing for the antimicrobial susceptibility testing of the isolates and Quark Expeditions for supporting the field trip.
Funding Statement
This work was supported by the Dutch Ministry of Economic Affairs (BO-22.04-008-001).
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