Microbial Ecology

, Volume 72, Issue 4, pp 861–869 | Cite as

Wild Birds, Frequent Carriers of Extended-Spectrum β-Lactamase (ESBL) Producing Escherichia coli of CTX-M and SHV-12 Types

  • Leticia Alcalá
  • Carla Andrea Alonso
  • Carmen Simón
  • Chabier González-Esteban
  • Jesús Orós
  • Antonio Rezusta
  • Carmelo Ortega
  • Carmen TorresEmail author
Environmental Microbiology


To get a better insight into the role of birds as reservoirs of extended-spectrum β-lactamase (ESBL) and plasmidic AmpC β-lactamase (pAmpC) Escherichia coli producers, 100 fecal samples belonging to 15 different wild avian species from Northern Spain were analyzed. Cefotaxime-resistant (CTXR) E. coli isolates were identified in 16 of the 100 tested birds, which corresponded to 9 animal species (Gyps fulvus—griffon vulture, Larus michahellis—yellow-legged gull, Milvus migrans—black kite, Milvus milvus—red kite, Ciconia ciconia—white stork, Sturnus unicolor—spotless starling, Aquila chrysaetos—golden eagle, Cuculus canorus—common cuckoo, Tyto alba—barn owl). Fifteen isolates harbored ESBL or pAmpC-encoding genes (number of isolates): bla SHV-12 (9), bla CTX-M-1 (3), bla CTX-M-14 (2), and bla CMY-2 (1). The last CTXR isolate presented a −42-point-mutation in the chromosomal ampC promoter. Eleven out of 15 ESBL/pAmpC E. coli isolates were multiresistant (most common resistance phenotype: β-lactams-quinolones-tetracycline-sulfamethoxazole/trimethoprim). A plasmid-mediated quinolone resistance determinant (qnrS1) was identified in one E. coli from a barn owl. High genetic diversity was observed among ESBL/pAmpC E. coli isolates, with 12 different sequence types (STs), including several strains of STs frequently detected among human clinical isolates (ST38/D, ST131/B2, ST155/B1, ST10/A). The ST131 isolate belonged to the emergent ciprofloxacin-resistant H30R subclone. This study reveals a high percentage of bird as carriers of ESBL/pAmpC E. coli isolates in Spain, highlighting the elevated rate among storks, kites, and vultures. Wild birds can contribute to the global spread of ESBL/pAmpC-producing E. coli in natural ecosystems.


ESBL CMY-2 PMQR Escherichia coli Wild birds Spain 



This work was supported in part by Project SAF2012-35474 from the Ministerio de Economía y Competitividad (MINECO) of Spain and the Fondo Europeo de Desarrollo Regional (FEDER). C. A. A. has a predoctoral fellowship from the MINECO (Spain).

We thank the center for wild animal recovering (CRFS) for its kind collaboration in collecting samples and to the Aragón Government that gave permission to work with the wild birds.


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Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Leticia Alcalá
    • 1
  • Carla Andrea Alonso
    • 2
  • Carmen Simón
    • 1
  • Chabier González-Esteban
    • 3
  • Jesús Orós
    • 1
  • Antonio Rezusta
    • 4
  • Carmelo Ortega
    • 1
  • Carmen Torres
    • 2
    Email author return OK on get
  1. 1.Facultad de VeterinariaUniversidad de ZaragozaZaragozaSpain
  2. 2.Área de Bioquímica y Biología MolecularUniversidad de La RiojaLogroñoSpain
  3. 3.Centro de Recuperación de Fauna Silvestre de La Alfranca, Departamento de AgriculturaGanadería y Medio AmbienteGobierno de AragónSpain
  4. 4.Servicio de MicrobiologíaHospital Universitario Miguel Servet, Zaragoza, Universidad de ZaragozaIIS AragónSpain

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