Skip directly to search Skip directly to A to Z list Skip directly to page options Skip directly to site content

Volume 20, Number 5—May 2014


Extended-Spectrum β-Lactamases in Escherichia coli and Klebsiella pneumoniae in Gulls, Alaska, USA

On This Page


Technical Appendices


Cite This Article


Highlight and copy the desired format.

EID Bonnedahl J, Hernandez J, Stedt J, Waldenström J, Olsen B, Drobni M, et al. Extended-Spectrum β-Lactamases in Escherichia coli and Klebsiella pneumoniae in Gulls, Alaska, USA. Emerg Infect Dis. 2014;20(5):899.
AMA Bonnedahl J, Hernandez J, Stedt J, et al. Extended-Spectrum β-Lactamases in Escherichia coli and Klebsiella pneumoniae in Gulls, Alaska, USA. Emerging Infectious Diseases. 2014;20(5):899. doi:10.3201/eid2005.130325.
APA Bonnedahl, J., Hernandez, J., Stedt, J., Waldenström, J., Olsen, B., & Drobni, M. (2014). Extended-Spectrum β-Lactamases in Escherichia coli and Klebsiella pneumoniae in Gulls, Alaska, USA. Emerging Infectious Diseases, 20(5), 899.

To the Editor: Resistance to β-lactam antibacterial drugs has spread rapidly, particularly through the CTX-M β-lactamase enzymes (CTX-M) (1). Although CTX-Ms are geographically widely distributed, reports of extended-spectrum β-lactamase (ESBL) dissemination are few from remote regions. In 2008, we reported phenotypic resistance traits in Escherichia coli isolates in 8.2% of wild birds sampled in the Arctic (2). We sampled approximately 260 wild birds, mainly gulls and geese, but found no ESBL-harboring isolates (J. Bonnedahl et al., unpub. data). Here we report results of our 2010 study at Barrow, Alaska, USA, a follow up to our 2005 study in which we found vancomycin-resistant enterococci (VRE) with clear traits of human origin in glaucous gulls (3). Our findings show a remarkable change, not in VRE dissemination, which is fairly unchanged, but in the emergence of ESBLs and general resistance of E. coli isolates.

We collected 150 fecal samples from a population of adult gulls residing close to a landfill site. For a description of general resistance levels (4,5), susceptibility of 1 randomly selected E. coli isolate per sample (137 isolated from 150 samples) was tested to a set of 10 antibacterial agents. Nearly half (48%) of the 137 E. coli isolates were resistant to at least 1 of the drugs tested. Resistance to 1 or 2 antimicrobial agents was found in 32% and 13% of the tested isolates, respectively, and resistance to >3 was found in 3% of isolates (Technical Appendix [PDF - 32 KB - 1 page] Table).

We analyzed samples for presence of VRE (3). Seven (4.7%) E. faecium isolates were found, all of which harbored both the vanA and the esp genes (found in isolates of the CC17 lineage) (3). No other VRE were found.

To investigate the presence of ESBL-producing bacteria, we conducted a selective screen as described (6). ESBL-producing bacteria were found (E. coli and K. pneumoniae), and ESBL genes (blaCTX-M, blaSHV, and blaTEM) in ESBL-positive isolates were analyzed (6). We found 33 E. coli and 35 K. pneumoniae ESBL-producing isolates in 55 samples (12 samples had >1 unique isolate), a total of 37% of ESBL-harboring samples (Table).

We performed multi-locus sequence typing (MLST) on ESBL-producing E. coli isolates (4). Isolates were of described sequence types (STs) (ST131 [12 isolates], ST38 [10], ST405 [3], and ST10 [1]), and of previously undescribed STs (designated ST2253 [1 isolate] and ST2967 [6 isolates]) (Table).

In our 2005 study in Barrow, general resistance was relatively low, and no ESBL was found; surprisingly, however, 2 VRE isolates of a human clonal lineage were found (3; M. Drobni et al., unpub. data). Since then, resistance dissemination, particularly that of ESBLs, has exploded globally (1). In 2010, we found a high level of general resistance; 48% of randomly selected E. coli isolates displayed resistance toward >1 antibacterial drugs. This level is similar to the level we found in gulls in France in 2008, an area with high current and historical clinical antibacterial drug use and where birds have close contact with human activities (4).

We screened samples for VRE and ESBL-producing bacteria. The prevalence of VRE decreased from 6% in 2005 to 4.7% in the current study (3), indicating a slow decline or stability in VRE. ESBL, on the other hand, was not found in the 2005 study (M. Drobni et al., unpub. data) but emerged in 37% of samples carrying E. coli and/or K. pneumoniae harboring ESBLs. In the study from France, only 9.4% of birds carried ESBLs (4), although a study of gulls in Portugal during 2007–2008 reported an ESBL carriage of 32% (7), more similar to results of our current study but in contrast also because they investigated gulls from a highly populated area.

E. coli isolates mainly carried blaCTX-M-14 or blaTEM-19, whereas K. pneumoniae isolates mainly carried blaCTX-M-15, blaSHV-12, or blaSHV-102. To our knowledge, ESBLs in E. coli and K. pneumoniae have not been reported from Alaska, but in two 10-year perspective reports from Canada (8,9), similar patterns and genotypes are reported in E. coli and K. pneumoniae in clinical isolates (mainly from samples of persons with urinary tract infections and urosepsis). Our MLST of E. coli indicated 4 known STs; ST10, ST38, ST131, and ST405, all very common in the material from Canada (8), and major STs responsible for CTX-M dissemination worldwide (1). Two novel STs were found; several isolates were designated to 1 of them. We conclude that the relatively limited variation in clonal variants (STs) and ESBL genotypes is a consequence of recent introduction from connecting areas, such as Canada, possibly directly by bird migration or human activities, of a few resistant clones, followed by a local clonal expansion. This conclusion is supported by our 2005 study showing no ESBLs and by studies showing where different clones might have been introduced continuously for long periods, such as our study in France (4), which display a much larger diversity.

The dissemination of ESBLs to Barrow is part of this global pattern, and it is safe to say that humans and wildlife share resistant E. coli flora. When areas such as remote parts of Alaska are affected, global coverage is imminent.


This work was supported financially by the Swedish Research Council (2008-6892); the Health Research Council of Southeast Sweden; and the Department of Medical Sciences, Uppsala University.

Jonas Bonnedahl, Jorge Hernandez, Johan Stedt, Jonas Waldenström, Björn Olsen, and Mirva DrobniComments to Author 

Author affiliations: Linnaeus University, Kalmar, Sweden (J. Bonnedahl, J. Hernandez, J. Stedt, J. Waldenström); Kalmar County Hospital, Kalmar (J Bonnedahl, J. Hernandez); Uppsala University, Uppsala, Sweden (J. Hernandez, B. Olsen, M. Drobni)


  1. Naseer U, Sundsfjord A. The CTX-M conundrum: dissemination of plasmids and Escherichia coli clones. Microb Drug Resist. 2011;17:8397. DOIPubMed
  2. Sjölund M, Bonnedahl J, Hernandez J, Bengtsson S, Cederbrant G, Pinhassi J, Dissemination of multidrug-resistant bacteria into the Arctic. Emerg Infect Dis. 2008;14:702. DOIPubMed
  3. Drobni M, Bonnedahl J, Hernandez J, Haemig P, Olsen B. Vancomycin-resistant enterococci, Point Barrow, Alaska, USA. Emerg Infect Dis. 2009;15:8389. DOIPubMed
  4. Bonnedahl J, Drobni M, Gauthier-Clerc M, Hernandez J, Granholm S, Kayser Y, Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellow-legged gulls in the south of France. PLoS ONE. 2009;4:e5958. DOIPubMed
  5. Gordon DM. Geographical structure and host specificity in bacteria and the implications for tracing the source of coliform contamination. Microbiology. 2001;147:107985 .PubMed
  6. Bonnedahl J, Drobni P, Johansson A, Hernandez J, Melhus Å, Stedt J, Characterization, and comparison, of human clinical and black-headed gull (Larus ridibundus) extended-spectrum beta-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden. J Antimicrob Chemother. 2010;65:193944. DOIPubMed
  7. Simões RR1. Poirel L, Da Costa PM, Nordmann P. Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli. Emerg Infect Dis. 2010;16:1102.PubMed
  8. Peirano G, van der Bij AK, Gregson DB, Pitout JD. Molecular epidemiology over an 11-year period (2000 to 2010) of extended-spectrum β-lactamase–producing Escherichia coli causing bacteremia in a centralized Canadian region. J Clin Microbiol. 2012;50:2949. DOIPubMed
  9. Peirano G, Sang JH, Pitondo-Silva A, Laupland KB, Pitout JD. Molecular epidemiology of extended-spectrum-β–lactamase-producing Klebsiella pneumoniae over a 10 year period in Calgary, Canada. J Antimicrob Chemother. 2012;67:111420. DOIPubMed


Technical Appendix

Cite This Article

DOI: 10.3201/eid2005.130325

Related Links

Table of Contents – Volume 20, Number 5—May 2014


Please use the form below to submit correspondence to the authors or contact them at the following address:

Mirva Drobni, Department of Medical Sciences/Section of Clinical Microbiology and Infectious Diseases, Uppsala University Hospital, SE-751 85 Uppsala, SwedenMirva Drobni, Department of Medical Sciences/Section of Clinical Microbiology and Infectious Diseases, Uppsala University Hospital, SE-751 85 Uppsala, Sweden

character(s) remaining.

Comment submitted successfully, thank you for your feedback.