Prevalence of Extended-Spectrum-β-Lactamase- and/or Carbapenemase-Producing Escherichia coli Isolated from Yellow-Legged Gulls from Barcelona, Spain

Abstract

Seventy-two (54.5%) out of 132 fecal samples from a group of yellowlegged gulls in Barcelona, Spain, were positive for Escherichia coli producing either extended-spectrum ␤-lactamases (ESBL) (51.5%), carbapenemase (1.5%), or cephamycinase (1.5%). The isolation of two carbapenemase-producing E. coli strains is a matter of concern.KEYWORDS carbapenemases, E. coli, ESBL I n the last decade, the number of bacterial pathogens presenting multidrug resistance to antibacterial agents has increased dramatically, becoming an emergent global concern and a major public health problem (1). The main cause behind the increasing rates of resistance can ultimately be found in the abuse and misuse of antibacterial agents, whether used in patients and livestock or released into the environment. Once antimicrobial-resistant bacteria emerge, they can spread locally or globally. The main factors contributing to their spread at a global level comprise migrant birds, globalization of commercial food, and international travel.There have been several studies about the presence of resistant bacteria in gulls (2, 3), to the extent of being considered an indicator of environmental antibiotic resistance occurrence, as they are distributed almost all around the world (4). Meerburg et al. (5) showed that gull feces contain a greater average concentration of E. coli than other wild animals, and according to Stedt et al. (4), Spain is the country in Europe with the highest levels of gull E. coli isolates resistant to Ն1 antibiotic.The objective of this study was to investigate the prevalence of extended-spectrum ␤-lactamase (ESBL)-and/or carbapenemase-producing Enterobacteriaceae from fecal swabs obtained from a group of yellow-legged gulls (Larus michahellis) in Barcelona, Spain.The study was conducted from the beginning of May to late July 2014 in the city of Barcelona, including the breeding period of the yellow-legged gull in the city. The sampling program was part of the sanitary and epidemiological surveillance that is carried out by the Public Health Agency, Barcelona, the institution responsible for the supervision and surveillance of the species. The sampling sites were chosen according to citizens' reports regarding the species nesting on their terraces or high roofs of the city. Every gull chick from each nest found (Fig. 1) was sampled, which amounts to 132 samples in total. All samples were obtained from young specimens born in that same year, and all nests were independent from each other, since the urban structure of cities The samples were plated on ESBL chromogenic agar (bioMérieux, France), and burgundy red colonies were selected, according to the manufacturer's instructions. Colonies were further identified by matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF MS) (Bruker Daltonics, Inc., Bremen, Germany). Susceptibility to ampicillin, amoxicillin-clavulanic acid, cefuroxime, ceftriaxone, cefotaxime, meropenem, gentamicin, amikacin, nalidixic acid, and ciprofloxacin was determined ...

Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review

“…Wildlife acquires CRE for example by contact with sewage, manure, or waste disposal sites [93]. Importantly, we found several reports describing CRE in swallows, black kites, storks, or gulls (with a high prevalence in France and Australia), demonstrating that these birds may act as reservoirs for bla NDM , bla OXA-48 , bla IMP , bla VIM-1 , and bla KPC-2 [25,78,79,82,83,85]. These findings raise concern because they indicate that these carbapenemases are prevalent in the environment in amounts that not only lead to colonization of wildlife, but also because these (migratory) birds may act as vectors facilitating the spread of CRE beyond borders of farms, dwelling zones, countries, or even continents.…”

“…3. As shown in Tables 2 and S3, CRE isolates harbouring bla OXA-48 , bla NDM-1 , bla NDM-5 , bla NDM-9 , or bla-VIM-1 were detected in dogs [25,67,68,70e75], bla OXA-48 , bla IMP-4 , or bla NDM-1 in cats [67e69, 71,74,75], bla OXA-48 in horses [68,71], bla OXA-48 in pet birds [68], bla NDM-1 and bla NDM-5 in swallows [25], bla OXA-48 in wild boars [77], bla OXA-48 in wild storks [78], bla IMP , bla VIM-1 , and bla KPC-2 in silver and yellow-legged gulls [79,82,85] and bla NDM-1 in a black kite [83]. Carbapenemase-encoding genes were found in the following bacterial species isolated from companion animals and wildlife: E. coli (bla OXA-48 , bla NDM-1 , bla NDM-5 , bla NDM-9 , bla IMP-4 , bla VIM-1 , bla KPC-2 ), Klebsiella spp.…”

High Colonization Rate and Heterogeneity of ESBL- and Carbapenemase-Producing Enterobacteriaceae Isolated from Gull Feces in Lisbon, Portugal

“…Our study revealed frequent occurrence of carbapenemase- and ESBL-producing Enterobacteriaceae (16% and 55%, respectively) colonizing gulls from the Lisbon coastline, Portugal. ESBL-producing Enterobacteriaceae among gulls were previously reported in USA [ 6 ], Canada [ 4 ], Chile [ 5 ], and in different countries in Europe [ 8 , 31 , 32 , 33 , 34 ], including Portugal in 2008 [ 12 , 13 ]. The high heterogeneity observed here in terms of bacterial species, ST, and resistance determinants showed that the high resistance rates observed were basically not simply consequences of shared microbiota between bird individuals, that could have biased our observation.…”

“…In recent years, gulls have been reported as carriers of ESBL-producing E. coli in Europe, South America, North America, and Asia [ 2 , 3 , 4 , 5 , 6 ]. More recently, a very limited number of studies documented fecal carriage of carbapenemase-producers in gulls in Spain, France, Australia, and Alaska, being exclusively E. coli [ 7 , 8 , 9 , 10 ].…”

Predictable anthropogenic food subsidies, density‐dependence and socio‐economic factors influence breeding investment in a generalist seabird

“…Large populations of YLGs have been often associated with negative effects on other syntopic bird species via predation, kleptoparasitism and competition for nesting places (Vidal et al , Oro and Martínez‐Abraín , Paracuellos and Nevado ). In addition, gull‐human conflicts associated to their bold behavior and their role as a potential vector for human pathogens, such as Escherichia coli , might arise due to the usual vicinity of breeding sites to human settlements (Vergara et al ). These issues have raised concerns to the point that several countries have undergone management actions to reduce population size (Bosch et al , Steigerwald et al ).…”