animals
Article
Prevalence and Antimicrobial Resistance of Enteropathogenic
Bacteria in Yellow-Legged Gulls (Larus michahellis) in
Southern Italy
Tamara Pasqualina Russo
1,
* , Antonino Pace
1,2
, Lorena Varriale
1
, Luca Borrelli
1
, Antonio Gargiulo
1
,
Marina Pompameo
3
, Alessandro Fioretti
1
and Ludovico Dipineto
1
Citation: Russo, T.P.; Pace, A.;
Varriale, L.; Borrelli, L.; Gargiulo, A.;
Pompameo, M.; Fioretti, A.; Dipineto,
L. Prevalence and Antimicrobial
Resistance of Enteropathogenic
Bacteria in Yellow-Legged Gulls
(Larus michahellis) in Southern Italy.
Animals 2021, 11, 275. https://
doi.org/10.3390/ani11020275
Received: 17 December 2020
Accepted: 19 January 2021
Published: 22 January 2021
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1
Department of Veterinary Medicine and Animal Productions, Università degli Studi di Napoli Federico II,
via Delpino 1,80137 Naples, Italy; antonino.pace@szn.it (A.P.); lorena.varriale@unina.it (L.V.);
luca.borrelli@unina.it (L.B.); angargiulo@libero.it (A.G.); fioretti@unina.it (A.F.);
ludovico.dipineto@unina.it (L.D.)
2
Marine Turtle Research Centre, Stazione Zoologica Anton Dohrn, via Nuovo Macello 16, 80055 Portici, Italy
3
Veterinary Hospital, ASL Napoli 1 Centro, via M. Rocco di Torrepadula 13, 80145 Naples, Italy;
marina.pompameo@aslnapoli1centro.it
* Correspondence: russo.tamara@gmail.com
Simple Summary: Several Mediterranean countries have suffered from a significant increase in the
populations of gulls. These birds are agile fliers and are able to adapt easily to different habitats
and to profit from food discarded by humans. In addition, gulls may be considered by some as
pests, given their interactions with human activities, and have been described as carriers, but actually
function as environmental sentinels of enteropathogenic bacteria and antibiotic-resistant strains.
Therefore, the aim of this study was to examine the role of gulls as vectors of zoonotic agents of high
importance for human health and as potential reservoirs of antimicrobial-resistant strains.
Abstract: Wild birds may host and spread pathogens, integrating the epidemiology of infectious
diseases. Particularly, Larus spp. have been described as responsible for the spread of many enteric
diseases, primarily because of their large populations at landfill sites. The aim of this study was to
examine the role of yellow-legged gulls as a source of enteropathogenic bacteria such as Campylobacter
spp., Salmonella spp., Shiga toxin-producing Escherichia coli and Yersinia spp., with particular attention
to antibiotic-resistant strains. Enteropathogenic bacteria were isolated from 93/225 yellow-legged
gulls examined from April to July, during a four-year period (2016–2019). Specifically, Campylobacter
spp. was isolated from 60/225 samples (26.7%), and identified as C. coli (36/60) and as C. jejuni
(24/60). Salmonella spp. was isolated from 3/225 samples (1.3%), and identified as Salmonella arizonae.
Shiga toxin-producing E. coli were isolated from 30/225 samples (13.3%) samples, and serotyped
as E. coli O128 (12/30) O26 (9/30), O157 (6/30) and O11 (3/30); Yersinia spp. was never detected.
Isolated strains exhibited multidrug resistance, including vitally important antibiotics for human
medicine (i.e., fluoroquinolones, tetracyclines). Our study emphasizes the importance of yellow-
legged gulls as potential reservoirs of pathogenic and resistant strains and their involvement in the
dissemination of these bacteria across different environments, with resulting public health concerns.
Keywords: yellow-legged gull; Salmonella; Campylobacter; Shiga toxin-producing E. coli; zoonosis;
antimicrobial resistance; public health
1. Introduction
The yellow-legged gull (Larus michahellis) (Laridae) inhabits different kinds of habi-
tats, from seashores, lakes, and rivers to farmlands and urban surroundings. Indeed, the
yellow-legged gull is considered an opportunistic species, given its adaptability to differ-
ent environments. The Italian yellow-legged gull population, as in most Mediterranean
Animals 2021, 11, 275. https://doi.org/10.3390/ani11020275 https://www.mdpi.com/journal/animals