Antimicrobial Resistance of E. coli and Salmonella Isolated from Wild Birds in a Rehabilitation Center in Turkey

1. Introduction

There are more than 10,000 bird species throughout the world, which migrate between countries and continents ( 1 , 2 ). Wild birds carry and transmit more than 40 diseases to humans and animals as a result of this movement, including bacterial, viral, parasitic and mycotic diseases ( 3 ). Furthermore, there may be an alarming relationship between wild birds and serious ongoing novel coronovirus (CoV) pandemic all over the world ( 4 ). Many recent studies have also emphasized that wild birds are the source of pathogens that cause diseases in humans; they can show signs of infection or appear completely healthy as carriers of pathogens ( 5 ). Since wild birds are highly mobile, they can carry pathogens long distances during migration, which introduces a risk of spreading disease beyond local outbreaks.

Wildlife plays a critical role as a reservoir for enteric bacterial pathogens and zoonotic diseases. Many wild bird species gravitate towards untreated sewage, garbage, manure, and other sources of enteric pathogens for their nutritional needs. As a result, Salmonella spp., which belongs to the Enterobacteriaceae family, and Escherichia coli are common enteric bacteria that are present as potential pathogens in these settings ( 6 - 8 ).

The development and spread of antibiotic resistance throughout the world has been increasing since the early 1960s, which is seen as a major threat to the global public health of wild birds due to their ability to freely travel over long distances during annual migrations ( 9 , 10 ). Although potentially pathogenic enteric bacteria have been isolated from many wild bird species, recent studies have highlighted that the role of these birds in human and veterinary diseases has been largely under-researched and further work is needed to determine their role in zoonotic transmission ( 9 ). Thus, the aim of this study was to investigate the presence of E.coli and Salmonella spp. in various wild birds, and characterize it phenotypically regarding serovars, tetracycline resistance genes (Tcrs, tet) and antimicrobial susceptibility.

2. Materials and Methods

2.1. Sample Collection, Bacterial Isolation and Identification

Intestine and fecal samples were obtained from 82 dead wild birds found in Afyon (38° 45' 24.787" N 30° 32' 19.334" E), Denizli (37° 46' 59.9988'' N 29° 5' 40.9740'' E), Uşak (38° 31' 15.59" N 29° 20' 18.60" E) and Eskişehir (39° 45' 58.2948'' N 30° 31' 36.1704'' E) provinces of Turkey (Table 1). The samples were cultured on MacConkey agar (Oxoid, UK) and aerobically incubated at 37°C for 24 h. Lactose positive, pink-to-red colonies were selected and assessed for E. coli precence using several biochemical tests (catalase, oxidase, indole, urease, motility, methyl red, citrate, and Voges-Proskauer) ( 11 ). All strains were maintained at -20°C in Luria-Bertani (LB) medium containing 15% glycerol until tests were performed.

All collected samples were analyzed for Salmonella positivity using ISO 6579:2002/Amd 1:2007. Specifically, samples were inoculated in buffered peptone water (BPW) as pre-enrichment medium and then incubated at 37°C for 18-24 h. After incubation, samples were transferred to Muller-Kauffmann tetrathionate-novobiocin broth (MKTTn) and modified semi-solid Rappaport-Vassiliadis (MSRV) medium and enriched for 18-24 h at 37°C and 24 h at 41.5°C, respectively. The cultures obtained were plated onto xylose lysine deoxycholate (XLD) incubated at 37°C, and then examined after 24 h incubation ( 12 ). All presumptive Salmonella colonies were characterized biochemically (triple sugar iron (TSI), H₂S, gas formation, voges proskauer (VP), urea, lysine decarboxylase, and β-galactosidase tests) by Microgen® GN-ID A sytem (Microgen Bioproducts, UK) ( 12 ).

2.2. Serotyping

The serotyping of microbiologically Salmonella spp. positive samples were conducted by slide agglutination using polyvalent and monovalent Salmonella "O" and "H" antisera according to the Kauffman-White scheme ( 12 ). Assessment was conducted at the Ministry of Health, Directorate General of Public Health, Department of Microbiology Reference Laboratories and Biological Products, National Enteric Pathogens Reference Laboratory in Ankara, Republic of Turkey.

2.3. Antimicrobial Susceptibility Testing

An antimicrobial susceptibility test was carried out using the agar disk diffusion method according to the guidelines from the Clinical and Laboratory Standards Institute on Mueller-Hinton agar (Oxoid Ltd, Hampshire, UK) according to the guidelines from Clinical and Laboratory Standards Institute ( 13 ). The following antibiotics were selected: ampicillin (10μg; AMP) amoxicillin (25μg; AX), cefotaxime (5μg; CTX), ceftriaxone (30μg; CRO), ciprofloxacin (5μg; CIP), enrofloxacin (5μg; ENR), erythromycin (15μg; E), gentamicin (10μg; CN), florfenicol (30μg; FFC), kanamycin (5μg; K), lincomycin (15μg; MY), nalidixic acid (30μg; NA) neomycin (30μg; N), doxycycline (30μg; DO), oxytetracycline (30μg; OT), tetracycline (10 μg; T), penicillin (10units; P), sulphamethoxazole trimethoprim (25μg; SXT). The results were obtained by measuring the diameter of the growth inhibition zone around the antibiotic disc for each isolated bacterial strain and recorded as sensitive, intermediate or resistant. Isolates displaying resistance to three or more antimicrobial agents were defined as exhibiting multi-drug resistance (MDR) ( 13 ).

2.4. Detection of tet Genes

The detailed sequence information of primer sets are listed in table 2 ( 14 - 16 ). DNA extraction were performed according to the instructions of the Gene JET Genomic DNA Purification Kit (Thermo Scientific, USA). DNAs were stored for use as template DNA at -20°C until amplification. Singeleplex PCR assay was carried out for tet(W) gene. The protocol was as follows: 25 µl reaction volumes containing 3 µl MgCl (25 mM), 0.5 µl dNTP (10 mM), 10 pmols of primers and 0.2 µl Taq polymerase (5U/µl). PCR amplifications were performed with the following cycling conditions: 3 min at 94°C, followed by 30 cycles of 1 min at 94°C (denaturation) and 1 min at 54°C (primer annealing), 1 min at 72°C (extension), and 7 min at 72°C (final extension). Multiplex PCR was performed for Tcrs groups, Group I; tet(B), tet(C) and tet(D), Group II; (tet(A), tet(E) and tet(G), Group III; tet(K), tet(L), tet(M), tet(O) and tet(S), Group IV; tetA(P), tet(Q) and tet(X). Each multiplexed group's PCR reaction mix concentration and amplification conditions were carried out following the previous research ( 15 ).

3. Results

3.1. Bacterial Isolation and Identification

A total of 51 E. coli strains were isolated from 22 different wild bird species (Asio otus, Buteo rufinus, Pelecanus onocrotalus, Falco tinnunculus, Ciconia ciconia, Scolopax rusticola, Buteo buteo, Anas platyrhynchos, Crex crex, Tyto alba, Pelecanus onocrotalus, Athene noctua, Ardea cinerea, Accipiter gentilis, Pernis apivorus, Garrulus glandarius, Tadorna ferruginea, Apus apus, Phoenicopterus roseus, Larus michahellis, Columba livia and Phalacrocorax carbo). In contrast, Salmonella spp. isolates were only recovered from intestine and fecal samples of Asio otus (long-eared owl) and Buteo buteo (common buzzard).

3.2. Serotyping

Two isolates were serotyped; one was Salmonella enterica subsp. enterica serovar Bispebjerg (S. Bispebjerg; common buzzard) and the other was exhibited the common serotype Salmonellaenterica subsp. enterica serovar Kentucky (S. Kentucky; long-eared owl).

3.3. Antimicrobial Susceptibility Testing

E. coli isolates had the greatest antimicrobial resistance patterns for lincomysin (100%), penicilline (96.1%), kanamycin (80.4%), tetracycline (68.6%), oxytetracycline (64.7%), and doxycycline (41.2%). Salmonella serotypes were resistant to lincomycin, nalidixic acid and penicilline but S. Bispebjerg was totally susceptible to nalidixic acid (Table 3). The majority (58.82%) of E. coli isolates exhibited phenotypic resistance to at least three or more antimicrobials. The S. Kentucky exhibited MDR to lincomycin, penicilline and nalidixic acid (100%) (Table 4).

3.4. Distribution of Antibiotic Resistance Genes

Of the 51 E.coli isolates, 35 (68.62%) carried Tcrs genes; 19 (54.3%) with tet (A), 10 (28.6%) with tet (B) and 6 (17.2%) with tet (D). The tet (A), tet (B), and tet (D) genes were identified in isolates resistant to tetracycline (8 (22,9%), 5 (14,3%), and 5 (14,3%)), oxytetracycline (6 (18.2%), 3 (9.1%), and 1 (3.3%)) and doxyxcycline (5 (23.8%) and 2 (9.5%)) respectively. Moreover, none of the isolates resistance to doxycycline were found to possess the tet (D) gene.

4. Discussion

In recent years, it has been increasingly interest in wild life and natural hosts for detecting pathogens and antibiotic resistant bacteria. The ability hazard posed by using antibiotic resistant bacterial colonization of wildlife and the following contamination of the surroundings has been strongly recounted ( 9 , 17 , 18 ). It's far been envisioned that the majority of rising infectious diseases in human beings have a flora and fauna reservoir ( 18 ) and the potential switch of antibiotic resistant bacteria from wildlife/surroundings to plants, human beings and domestic animals need to now be noted ( 9 , 18 ). Thus, evidence suggests a positive correlation between the wild life hosts and antibiotic resistant Enterobacteriaceae especially E. coli and Salmonella spp. ( 17 , 19 ) Transfer of antibiotic-resistant bacteria/genetic elements found in the feces of wild birds known as transmits from wildlife to animals or humans are approved ( 20 , 21 ). The role of wild birds as reservoir hosts for some zoonotic pathogens within the Enterobactericeae family has been previously investigated in many studies all over the world, including Norway ( 22 ), Japan ( 7 , 23 ), Malaysia ( 24 ), USA ( 25 ), and Egypt ( 26 ).

These findings were reflected in our bacteriological analysis; overall prevalence of E. coli and Salmonella were 62.2% and 2.44% in examined wild birds. Although E. coli positive birds were higher than other findings in Egypt, USA, Arabia, Italy, Brasil and Switzerland, lower than Canada (62.7%), Brasil (69.38%) and Trinidad and Tobago (83.8%); Salmonella spp. also recovered nearly similar with the previous reports ( 21 , 27 - 31 ). In Contrast to E. coli isolation, Salmonella spp. carriage of migratory or non-migratory wild bird' intestine or fecal shedding is almost 0- <1% ( 27 ). Despite the low recovery of Salmonella spp., is an evidence of circulation of serovars in the population ( 32 ). Interestingly, some studies in which neither E. coli nor Salmonella spp. have not been isolated were reported ( 32 - 34 ). In the last twenty years, studies demonstratean increase in the prevalence of isolation of the Salmonella spp. from wild birds ( 7 , 35 ).

Nevertheless, it was also reported that climate conditions in particular, might play a role on the isolation rates of migratory birds ( 36 , 37 ). E. coli and Salmonella serovars were recovered autumn-winter and summer were expected in this study. The comparable reason of E. coli and Salmonella spp. prevalence rates may be variations in sampling (e.g. storage conditions of samples), laboratory strategies employed individual studies or species of wild bird examined, localities, season and bird' feeding habits.

The most remarkable part of the resistance of E. coli isolates' was lincomysin and penicillin in our study. World Health Organization (WHO) classified tetracyclines, followed by penicillins, and sulfonamides as highly important antimicrobials ( 38 ). In this study, E. coli isolates were possessed high phenotypic resistance to all tetracyclines as like as other reports ( 39 , 40 ). Moreover, 64.7% of the isolates were resistant to ampicilline, this case was significantly differ from various reports ( 41 - 43 ) as there were same studies ( 44 ). Although extended-spectrum b-lactamase resistance had limited data for wild birds, a high rate of cefotaxime resistance were detected in various countries such as Porto, Portugal contrast to our resistance rate (29.4%) ( 40 , 45 ). The results for detection of high antibiotic resistance of E.coli isolates against to lincomisin, penicilline, kanamycin and tetracyclines were detected from long-legged buzzard (Buteo rufinus) following other species as Great white pelican (Pelecanus onocrotalus), White stork (Ciconia ciconia) and Ruddy shelduck (Tadorna ferruginea). It is noteworthy that the highest prevalence of antibiotic-resistant bacteria was found in aquatic birds, therefore Ruddy shelduck and Great white pelican could be good examples ( 17 , 34 ).

Our evaluation of the multidrug resistance patterns of the E. coli to 58.82%, which was contrast with previous studies showing 1.5-47.4% ( 28 , 31 , 39 , 46 , 47 ). Moreover, the most prevelant resistances were to ampiciline, lincomycine, tetracycline, oxytetracycline and sulphamethaxazole trimetoprim. Wild birds are less likely to faced with the antimicrobials than domestic ones. Wild birds can become MDR reservoirs by ingesting contaminated food and water in landfills, livestock farms, wastewater treatment facilities, or sewage systems ( 48 ). In fact, another scenario that reveals today's reality is the expansion of urban areas and loss of wildlife habitats, thus showing wild birds could reach the contaminated enviroment ( 49 , 50 ).

In this study, we found the high frequency of tetracycline resistance (68.62%) due to the tet (A), tet (B), and tet (D) genes. The presence of tet (A) was the most frequent, followed by tet (B) and tet (D). According to the our results, tet (A), tet (B) and tet (D) was confered resistance to three tetracycline preparation is approximately 3-20% and the lower detection of the resistant genes could have been due to indefinite phenotypic resistance, lack of gene expression, or other resistance mechanisms was confirmed ( 51 ). It was notable that tet (A) gene has also been reported to be a common in contrast to other tet genes in E. coli from wild birds as poultry ( 14 , 16 ). In addition, prominent wild birds such as common buzzard, flamingo and owl were recorded in detection of tet (A) and tet (B) genes in consistence with our results ( 29 , 44 , 52 ).

Prevalence studies in different regions of the world (e.g. Argentina, Brasil, United Kingdom, Australia, Spain, Iran, Sweden, United States, Belgium and Italy) over a 40-year period have identified S. Typimurium, S. Bredeney, S. Hadar, S. Agona, S. Panama, S. Virchow, S. Enteritidis, and S. Newport, S. Haifa, S. Chester, S. Heidelberg, S. Infantis, S. Kottbus, S. Livingstone, S. Veneziana, S. Muenster ( 53 , 54 ). S. Typimurium, S. Enteritidis and S. Infantis are remarkable serovars due to zoonotic importance ( 55 ). In contrast, we are the first to detect S. Kentucky and S. Bispebjerg in the long-eared owl and common buzzard from Turkey in this study respectively. Several other studies have investigated the presence of Salmonella spp. in various species such as dove, sparrow, Temminck’s seedeater, chestnut-capped black-bird and common kestrel ( 7 , 22 , 30 , 35 ). We also previously identified S. Hessarek from starlings ( 56 ). These data represent a potential avian host range, especially for the genus Salmonella, which appears limited in Turkey. It is noteworthy, these may be associated to sporadic Salmonella infections and mortalities in particularly young wild birds. Concerning the distribution of many serotypes were not represented a host specific in wild birds than livestock and humans ( 57 ).

In present study, a significant cases were represented by S. Kentucky also referred as MDR from long eared owl was exhibited resistance to lincomycin, penicilline and nalidixic acid (100%) and by S. Bispebjerg was the highest frequency of resistance against lincomycin, penicilline. However, serovars were susceptible or intermediately susceptible to 15 out of 18 tested antimicrobials. In addition, none of the Salmonella isolates possesed tet gene. To our knowledge, in previous studies antimicrobial resistance concerning serovars due to isolation rates were rather limited, compared to E. coli. With respect to the overall, Salmonella resistance against to antimicrobials in wildbirds in various researches reported such as beta-lactam, penicillin, sulphonamides, aminoglycosid, tetracycline and quinolones ( 28 , 32 , 53 ). The present study provides a prevalence rate of E. coli and Salmonella isolates from wild birds in Turkey, which enhances our understanding of the local epidemiology of wild life pathogens and antibiotic resistance profiles. This findings focused on antibiotic resistance, which remains a significant concern for humans and animals interacting directly or indirectly with wild birds. In addition, further researches should be conducted on public health, resistance mechanisms and genetic diversity of pathogens remain regarding the potential for wild birds to act as reservoirs.

Authors' Contribution

O. S. Y., E. H. K. and D. O. planned and designed the study. O. S. Y. and D. O. performed the experiments, and O. S. Y. and D. O. contributed to the analysis and interpretation of data. O. S. Y. drafted the manuscript. All authors read and approved the final manuscript.

Ethics

This study was approved by Republic of Turkey Ministry of Agriculture and Forestry, General Directorate of Nature Conservation and National Parks (Protocol no. E-21264211-288.04-892913), Burdur Directorate of Provincial Agriculture and Forestry (Protocol no. E-39637749-325.04.03-802375) and the institutional ethics committee for the local use of animals in experiments (Protocol no. E-93773921-020-20960).

Conflict of Interest

The authors declare that they have no conflict of interest.

Grant Support

This research has not been funded.

References

1. Barrowclough GF, Cracraft J, Klicka J, Zink RM. How Many Kinds of Birds Are There and Why Does It Matter?. PLoS One. 2016; 11(11):0166307.
2. Benskin CM, Wilson K, Jones K, Hartley IR. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev Camb Philos Soc. 2009; 84(3):349-73.
3. Gaukler SM, Linz GM, Sherwood JS, Dyer NW, Bleier WJ, Wannemuehler YM, et al. Escherichia coli, Salmonella, and Mycobacterium avium subsp. paratuberculosis in wild European starlings at a Kansas cattle feedlot. Avian Dis. 2009; 53(4):544-51.
4. Rahman MM, Talukder A, Chowdhury MMH, Talukder R, Akter R. Coronaviruses in wild birds - A potential and suitable vector for global distribution. Vet Med Sci. 2021; 7(1):264-72.
5. Lagerstrom KM, Hadly EA. The under-investigated wild side of Escherichia coli: genetic diversity, pathogenicity and antimicrobial resistance in wild animals. Proc Biol Sci. 2021; 288(1948):20210399.
6. Fogarty LR, Haack SK, Wolcott MJ, Whitman RL. Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull faeces. J Appl Microbiol. 2003; 94(5):865-78.
7. Kobayashi H, Kanazaki M, Shimizu Y, Nakajima H, Khatun MM, Hata E, et al. Salmonella isolates from cloacal swabs and footpads of wild birds in the immediate environment of Tokyo Bay. J Vet Med Sci. 2007; 69(3):309-11.
8. Moore JE, Gilpin D, Crothers E, Canney A, Kaneko A, Matsuda M. Occurrence of Campylobacter spp. and Cryptosporidium spp. in seagulls (Larus spp.). Vector Borne Zoonotic Dis. 2002; 2(2):111-4.
9. Greig J, Rajic A, Young I, Mascarenhas M, Waddell L, LeJeune J. A scoping review of the role of wildlife in the transmission of bacterial pathogens and antimicrobial resistance to the food Chain. Zoonoses Public Health. 2015; 62(4):269-84.
10. Hernandez J, Bonnedahl J, Eliasson I, Wallensten A, Comstedt P, Johansson A, et al. Globally disseminated human pathogenic Escherichia coli of O25b-ST131 clone, harbouring blaCTX-M-15 , found in Glaucous-winged gull at remote Commander Islands, Russia. Environ Microbiol Rep. 2010; 2(2):329-32.
11. Quinn P, Markey B, Lenonard F, FitzPatrick E, Fanning S, Hartigan P. Enterobactericeae. Veterinary Microbiology and Microbial Disease. 2nd ed. USA: Wiley-Blackwell Publication; 2011.
12. International Organization for Standardization I. Microbiology of the food chain-Horizontal method for the detection, enumeration and serotyping of Salmonella - Part 1: Detection of Salmonella spp Geneva, Switzerland: International Organization for Standardization; 2017.
13. Clinical and Laboratory Standards Institute C. Performance standards for antimicrobial susceptibility testing. CLSI supplement M100. 28th ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2018.
14. Chopra I, Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev. 2001; 65(2):232-60.
15. Ng LK, Martin I, Alfa M, Mulvey M. Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes. 2001; 15(4):209-15.
16. Roberts MC, Schwarz S, Aarts HJ. Erratum: Acquired antibiotic resistance genes: an overview. Front Microbiol. 2012; 3:384.
17. Bonnedahl J, Jarhult JD. Antibiotic resistance in wild birds. Ups J Med Sci. 2014; 119(2):113-6.
18. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, et al. Global trends in emerging infectious diseases. Nature. 2008; 451(7181):990-3.
19. Maysa A, Abdallah M, Rehab E. Prevalence of zoonotic Escherichia coli and Salmonellae in wild birds and humans in Egypt with emphasis on RAPD-PCR fingerprinting of E. coli. Glob Vet J. 2013; 11(6):781-8.
20. Dolejska M, Papagiannitsis CC. Plasmid-mediated resistance is going wild. Plasmid. 2018; 99:99-111.
21. Okullu T, Onchweri A, Miruka C, Eilu E, Abimana J, Nyabayo M. Antibiotic resistant Escherichia coli isolates from barn swallow droppings in Ishaka Town, Uganda. J App Env Microbiol. 2016; 4(2):34-8.
22. Refsum T, Handeland K, Baggesen DL, Holstad G, Kapperud G. Salmonellae in avian wildlife in Norway from 1969 to 2000. Appl Environ Microbiol. 2002; 68(11):5595-9.
23. Aruji Y, Tamura K, Sugita S, Adachi Y. Intestinal microflora in 45 crows in Ueno Zoo and the in vitro susceptibilities of 29 Escherichia coli isolates to 14 antimicrobial agents. J Vet Med Sci. 2004; 66(10):1283-6.
24. Lee HY, Stephen A, Sushela D, Mala M. Detection of protozoan and bacterial pathogens of public health importance in faeces of Corvus spp. (large-billed crow). Trop Biomed. 2008; 25(2):134-9.
25. Phalen DN, Drew ML, Simpson B, Roset K, Dubose K, Mora M. Salmonella enterica subsp. Enterica in Cattle Egret (Bubulcus ibis) chicks from central Texas: prevalence, serotypes, pathogenicity, and epizootic potential. J Wildl Dis. 2010; 46(2):379-89.
26. Awad-Alla ME, Abdien HM, Dessouki AA. Prevalence of bacteria and parasites in White Ibis in Egypt. Vet Ital. 2010; 46(3):277-86.
27. Brittingham MC, Temple SA, Duncan RM. A survey of the prevalence of selected bacteria in wild birds. J Wildl Dis. 1988; 24(2):299-307.
28. Elsohaby I, Samy A, Elmoslemany A, Alorabi M, Alkafafy M, Aldoweriej A, et al. Migratory Wild Birds as a Potential Disseminator of Antimicrobial-Resistant Bacteria around Al-Asfar Lake, Eastern Saudi Arabia. Antibiotics (Basel). 2021; 10(3)
29. Gambino D, Vicari D, Vitale M, Schiro G, Mira F, Giglia M, et al. Study on Bacteria Isolates and Antimicrobial Resistance in Wildlife in Sicily, Southern Italy. Microorganisms. 2021; 9(1)
30. Suphoronski SA, Raso TdF, Weinert NC, Seki MC, Carrasco AdOT. Occurrence of Salmonella sp. and Escherichia coli in free-living and captive wild birds from 2010-2013 in Guarapuava, Paraná, Brazil. Afr J Microbiol Res. 2015; 9(29):1778-82.
31. Zurfluh K, Albini S, Mattmann P, Kindle P, Nuesch-Inderbinen M, Stephan R, et al. Antimicrobial resistant and extended-spectrum beta-lactamase producing Escherichia coli in common wild bird species in Switzerland. Microbiologyopen. 2019; 8(11):e845.
32. Matias CA, Pereira IA, de Araujo Mdos S, Santos AF, Lopes RP, Christakis S, et al. Characteristics of Salmonella spp. Isolated from Wild Birds Confiscated in Illegal Trade Markets, Rio de Janeiro, Brazil. Biomed Res Int. 2016; 2016:3416864.
33. Foti M, Mascetti A, Fisichella V, Fulco E, Orlandella BM, Lo Piccolo F. Antibiotic resistance assessment in bacteria isolated in migratory Passeriformes transiting through the Metaponto territory (Basilicata, Italy). Avian Res. 2017; 8(1):26.
34. Guenther S, Aschenbrenner K, Stamm I, Bethe A, Semmler T, Stubbe A, et al. Comparable high rates of extended-spectrum-beta-lactamase-producing Escherichia coli in birds of prey from Germany and Mongolia. PLoS One. 2012; 7(12):e53039.
35. Vlahović K, Matica B, Bata I, Pavlak M, Pavičić Ž, Popović M, et al. Campylobacter, salmonella and chlamydia in free-living birds of Croatia. Eur J Wildl Res. 2004; 50(3):127-32.
36. Sanches LA, Gomes MDS, Teixeira RHF, Cunha MPV, Oliveira MGX, Vieira MAM, et al. Captive wild birds as reservoirs of enteropathogenic E. coli (EPEC) and Shiga-toxin producing E. coli (STEC). Braz J Microbiol. 2017; 48(4):760-3.
37. Shelton DR, Karns JS, Coppock C, Patel J, Sharma M, Pachepsky YA. Relationship between eae and stx virulence genes and Escherichia coli in an agricultural watershed: implications for irrigation water standards and leafy green commodities. J Food Prot. 2011; 74(1):18-23.
38. Collignon PJ, Conly JM, Andremont A, McEwen SA, Aidara-Kane A, World Health Organization Advisory Group BMoISoAR, et al. World Health Organization Ranking of Antimicrobials According to Their Importance in Human Medicine: A Critical Step for Developing Risk Management Strategies to Control Antimicrobial Resistance From Food Animal Production. Clin Infect Dis. 2016; 63(8):1087-93.
39. Hasan B, Sandegren L, Melhus A, Drobni M, Hernandez J, Waldenstrom J, et al. Antimicrobial drug-resistant Escherichia coli in wild birds and free-range poultry, Bangladesh. Emerg Infect Dis. 2012; 18(12):2055-8.
40. Shobrak MY, Abo-Amer AE. Role of wild birds as carriers of multi-drug resistant Escherichia coli and Escherichia vulneris. Braz J Microbiol. 2014; 45(4):1199-209.
41. Dolejska M, Bierosova B, Kohoutova L, Literak I, Cizek A. Antibiotic-resistant Salmonella and Escherichia coli isolates with integrons and extended-spectrum beta-lactamases in surface water and sympatric black-headed gulls. J Appl Microbiol. 2009; 106(6):1941-50.
42. Sacristan C, Esperon F, Herrera-Leon S, Iglesias I, Neves E, Nogal V, et al. Virulence genes, antibiotic resistance and integrons in Escherichia coli strains isolated from synanthropic birds from Spain. Avian Pathol. 2014; 43(2):172-5.
43. Stedt J, Bonnedahl J, Hernandez J, McMahon BJ, Hasan B, Olsen B, et al. Antibiotic resistance patterns in Escherichia coli from gulls in nine European countries. Infect Ecol Epidemiol. 2014; 4
44. Radhouani H, Poeta P, Goncalves A, Pacheco R, Sargo R, Igrejas G. Wild birds as biological indicators of environmental pollution: antimicrobial resistance patterns of Escherichia coli and enterococci isolated from common buzzards (Buteo buteo). J Med Microbiol. 2012; 61(Pt 6):837-43.
45. Mohsin M, Raza S, Schaufler K, Roschanski N, Sarwar F, Semmler T, et al. High Prevalence of CTX-M-15-Type ESBL-Producing E. coli from Migratory Avian Species in Pakistan. Front Microbiol. 2017; 8:2476.
46. Blyton MD, Pi H, Vangchhia B, Abraham S, Trott DJ, Johnson JR, et al. Genetic Structure and Antimicrobial Resistance of Escherichia coli and Cryptic Clades in Birds with Diverse Human Associations. Appl Environ Microbiol. 2015; 81(15):5123-33.
47. Ong KH, Khor WC, Quek JY, Low ZX, Arivalan S, Humaidi M, et al. Occurrence and Antimicrobial Resistance Traits of Escherichia coli from Wild Birds and Rodents in Singapore. Int J Environ Res Public Health. 2020; 17(15)
48. Allen HK, Donato J, Wang HH, Cloud-Hansen KA, Davies J, Handelsman J. Call of the wild: antibiotic resistance genes in natural environments. Nat Rev Microbiol. 2010; 8(4):251-9.
49. Karkman A, Parnanen K, Larsson DGJ. Fecal pollution can explain antibiotic resistance gene abundances in anthropogenically impacted environments. Nat Commun. 2019; 10(1):80.
50. Smith S, Wang J, Fanning S, McMahon BJ. Antimicrobial resistant bacteria in wild mammals and birds: a coincidence or cause for concern?. Ir Vet J. 2014; 67(1):8.
51. Arabzadeh F, Aeini F, Keshavarzi F, Behrvash S. Resistance to Tetracycline and Vancomycin of Staphylococcus aureus Isolates from Sanandaj Patients by Molecular Genotyping. Ann Clin Lab Res. 2018; 06
52. Santos T, Silva N, Igrejas G, Rodrigues P, Micael J, Rodrigues T, et al. Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipelago. Anaerobe. 2013; 24:25-31.
53. Botti V, Navillod FV, Domenis L, Orusa R, Pepe E, Robetto S, et al. Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet Ital. 2013; 49(2):195-202.
54. Forte Beleza A, Cardoso Maciel W, Souza Lopes E, de Albuquerque Á, Silva Carreira A, Guedes Nogueira C, et al. Evidence of the role of free-living birds as disseminators of Salmonella spp. Arq Inst Biol. 2020; 87
55. Tizard I. Salmonellosis in wild birds. Semin Avian Exot Pet Med. 2004; 13(2):50-66.
56. First Isolation of Salmonella Hessarek from Sturnus vulgaris in Turkey : A Case Report. Kafkas Univ Vet Fak Derg. 2017; 23 (2): 343-346.
57. Daoust P-Y, Prescott JF. Salmonellosis. Infectious Diseases of Wild Birds. 2007;270-88.