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Antibiotic Resistant Escherichia coli Isolates from Barn Swallow Droppings in Ishaka Town, Uganda

Tonny Okullu, Albert Nyanchoka Onchweri, Conrad Ondieki Miruka*, Emmanuel Eilu, Justus B. Abimana, Maniga Josephat Nyabayo

Department of Biochemistry, Faculty of Biomedical Sciences, Kampala International University-Western Campus, Bushenyi, Uganda

Abstract: Considerable concern has been raised over the problem of antibiotic resistance in bacteria from humans and farm animals. However, in spite of this concern, the spread of resistance into wider ecosystems has not received the desired attention. The transfer of antibiotic resistance to wildlife is an important risk for environmental health. Detection of resistance to antibiotics in populations of wild animals usually entails examination of isolates of the common intestinal bacterium Escherichia coli. Bird populations sympatric to areas with human settlements and areas that have high density of livestock are colonised with antibiotic resistant E. coli strains. Data regarding occurrence of antibiotic-resistant bacteria in African domestic and wild mammals is very limited. There is therefore a need to carry out studies in other parts of the African continent to find out if sympatric animals represent a possible reservoir for antibiotic resistant microbes. This study was therefore carried out to analyze faecal samples from barn swallow (Hirundo rustica) droppings in Ishaka Town, Uganda, for the presence of antibiotic resistant E. coli strains. Results of the study showed that, out of the one hundred and sixteen (116) fecal samples of Barn Swallow droppings collected, twenty seven isolates of Escherichia coli were obtained. All the 27 isolates (100%) were resistant to one or more of the tested antibiotics. Out of the 27 isolates, 20 (74.1%) were multi-drug resistant isolates (resistant to three or more classes of antimicrobials). Such birds can act as reservoirs for antibiotic resistant microbes if enough attention is not given to the problem. Further research is recommended to determine the prevalence of antibiotic resistant Escherichia coli from barn swallows residing in other parts of the country and even on the continent and the whole world at large.

Keywords: drug resistance, wild birds, Escherichia coli, barn swallow, reservoirs

Citation: Tonny Okullu, Albert Nyanchoka Onchweri, Conrad Ondieki Miruka, Emmanuel Eilu, Justus B. Abimana, Maniga Josephat Nyabayo, Antibiotic Resistant Escherichia coli Isolates from Barn Swallow Droppings in Ishaka Town, Uganda. Journal of Applied & Environmental Microbiology, 4 (2). 34-38. January 2016. doi:10.12691/jaem-4-2-2

1. Introduction

Bacteria have a very unique ability to adapt to changes in their environment, and to develop mechanisms to protect themselves against toxic compounds. Their ability to develop resistance mechanisms to antimicrobial drugs has reached catastrophic proportions, rendering increasingly more infections difficult or impossible to treat [1]. Majority of reports indicate that the main force behind emergence of drug resistance is the use and misuse of antimicrobial drugs during the past few decades, but there is also evidence for the epidemic spread of drug-resistant bacteria as a contributing factor [2]. There is evidence that resistance genes can be found even in a region where no selection pressure for resistance development exists, thus implying that dissemination of drug-resistant bacteria is worldwide [3]. Although wild bird populations are not influenced directly by antibiotic practice, it has been demonstrated that antibiotic resistant strains of E. coli are found in faeces of wild birds. This includes strains with various antibiotic resistance genes [4]. The problem of antibiotic resistance in bacteria from humans and farm animals has raised considerable concern. In spite of this, the spread of resistance into wider ecosystems has not received the desired attention [5]. Detection of antibiotic resistance in populations of wild animals usually entails examination of isolates of the common intestinal bacterium Escherichia coli [6]. The transmission of antibiotic resistance from livestock and humans remains a poorly understood mechanism, with wild animals acting as reservoirs of the resistance that may be eventually amplified and spread to the environment. It should be considered that the transfer of antibiotic resistance to wildlife is an important risk for environmental health [7]. In a study conducted in the inland Hamilton Harbour on Lake Ontario, Canada, it was found out that faeces of wild geese, ducks and gulls could have been a more prominent contributor of antibiotic resistant E. coli to a beach near Hamilton than municipal wastewater sources [8]. Various strains of E. coli colonise wild bird populations, including the E.coliO157 strain that is pathogenic to humans [6]. Faecal sample isolate strains of E. coli resistant to antibiotics have been found at varying prevalence in wild bird populations. Most notably, bird populations sympatric to areas with human settlements and areas that have high density of livestock are colonised with antibiotic resistant E. coli strains [9,10,11,12]. This poses a potential risk to public health. House sparrows living with cattle and coming into contact with cattle waste on farms in the Czech Republic were found to be infected by resistant E. coli strains with different characteristics from those found in cattle [13]. There is reported occurrence of E. coli strains that are pathogenic to humans and animals in the eggs and nestlings of house sparrows [14]. Corvids and gulls that feed on garbage dumps and in areas with urbanization are frequently colonised with resistant strains of E. coli and salmonella spp. Such birds are considered to form important reservoirs and vectors of these resistant strains in the environment [15,16]. Seagulls of diverse species colonised with resistant E. coli strains producing extended-spectrum beta-lactamase have been reported in Portugal [17]. Resistant strains carrying class 1 and 2 integrons have been isolated in Canada geese (Branta canadensis) in the United States and black-headed gulls in the Czech Republic [18,19]. Strains that are resistant to fluoroquinolones have also been reported in gulls living in Greenland [3]. Resistance to penicillin G, ampicillin, cephalothin, and sulfathiazole has been reported in a high frequency of E. coli isolates from migratory Canada geese sampled on the eastern shore of Maryland in the United States [20]. Bacteria displaying commensalism in humans and animals constitute hidden reservoirs of antimicrobial drug resistance [21]. There are reported cases of antimicrobial drug–resistant bacteria in wild animals with little or no contact with human settings [22,23]. There is limited data regarding occurrence of antibiotic-resistant bacteria in African domestic and wild mammals [24]. Studies conducted in Senegal and Kenya showed that rats represent a possibly important reservoir for antibiotic-resistant Enterobacteriaceae including extended-spectrum beta-lactamase producing strains [24,25]. Therefore, a great impact on human health can be brought about by antibiotic resistance in animals. This can occur especially in an environment where humans and animals share the same ecosystem [25]. In order to determine the extent of the spread of extended-spectrum beta-lactamases, it is necessary to characterize antibiotic-resistant bacteria in each geographical area and environments including wildlife, especially in areas where resources are limited and antibiotics are unregulated [26]. In view of this, there is therefore a need to carry out studies in other parts of the African continent to find out if sympatric animals represent a possible reservoir for antibiotic resistant microbes. In this study, we were particularly interested in analysing faecal samples from barn swallow (Hirundo rustica) droppings in Ishaka Town, Uganda, for the presence of antibiotic resistant E. coli strains. This bird’s habit of nesting in buildings associated with human habitation has led it to be one of the most familiar bird species in the world [27]. Because this species of birds come into close contact with human habitats [28,29], one recent study(the first of its kind) has implicated them as a potential source of Clostridium difficile in animals and humans [30]. Ishaka Town area of Uganda is fairly densely populated with this species of birds.

2. Materials and Methods

2.1. Bird Faecal Samples

The faecal samples were collected from twenty residential areas and ten educational institutions housing nests of Barn swallows in Ishaka town, Uganda. Individual faecal samples were transported to the Microbiology laboratory of Kampala International University-Western Campus, Ishaka. They were then placed overnight in buffered peptone water at 37°C.

2.2. Culturing and Isolation of Antibiotic Resistant E. coli Strains

The samples were cultivated for E. coli on selective chromogenic media for E. coli and coliform bacteria (CM0956; Oxoid, United Kingdom). A single colony of each plate was tested for susceptibilities to antimicrobial agents by the disk diffusion method in accordance with the Clinical and Laboratory Standards Institute (31). Susceptibilities to the following antibacterial substances were tested: ampicillin (10 μg), ceftazidime (30 μg), chloramphenicol (30 μg), ciprofloxacin (5 μg), nalidixic acid (30 μg), streptomycin (10 μg), Sulfamethoxazole (25 μg) and Cotrimoxazole (25μg).

2.3. Isolation of Extended-Spectrum Beta-lactamase and Quinolone-resistant Strains

This was done according to the method described by Literak et al. [32]. By this method, samples from peptone buffered water were enriched in MacConkey broth and subcultivated on MacConkey agar (MCA) containing ceftazidime (2 mg liter⁻¹) to detect the presence of E. coli strains with extended-spectrum beta-lactamase. These were then subcultivated on MacConkey agar containing ciprofloxacin (0.05 mg liter⁻¹) to isolate E. coli strains resistant to fluoroquinolone. To detect E. coli strains resistant to nalidixic acid and other quinolones, samples from the buffered peptone water were also enriched in MacConkey broth and subcultivated on MacConkey agar containing nalidixic acid (20 mg liter⁻¹).

2.4. Data Interpretation

Diameter of zones of inhibition was measured to the nearest millimeter using a transparent ruler. This was indicative of the susceptibility of E coli to the different antibiotic discs used. It was then compared with the standard zone of inhibition of E coli by the respective antibiotic disc.

3. Results

Out of the one hundred and sixteen (116) fecal samples of Barn Swallow droppings collected, twenty seven (23.3%) isolates of E. coli were obtained. The 27 E. coli isolates were therefore subjected to further analysis to identify isolates that are resistant to the antibiotics used in the study. All the 27 isolates (100%) were resistant to one or more of the tested antibiotics. Out of the 27 isolates, 20 (74.1%) were multi-drug resistant (resistant to three or more classes of antimicrobials) isolates. As shown in Table 1, susceptibility to Ciprofloxacin was noted to be highest, while resistance to Ampicillin was highest. None of the isolates was resistant to ciprofloxacin, whereas two isolates (7.4%) were intermediately susceptible and twenty five isolates (92.6%) were highly susceptible to the antibiotic. This meant that the microbes had not developed resistance against the antibiotic. All the 27 isolates (100%) were resistant to Ampicillin as evidenced by no zone of inhibition. Resistance of more than 50% was observed towards two other antibiotics, namely ceftazidime and streptomycin at 55.6% and 51.9% respectively. The 15 isolates that were resistant to ceftazidime were hence regarded as being extended-spectrum beta-lactamase (ESBL) producing strains. Nine (9) of the isolates were resistant to the quinolone nalidixic acid, which represented 33.3% of all the isolates. Out of these nine quinolone resistant isolates, three of them (33.3%) were highly resistant, as evidenced by completely no zone of inhibition. Figure 1 below shows the numbers of susceptible and resistant isolates.

Table 1. Resistance pattern of E. coli isolated from Barn Swallow droppings

Figure 1. Distribution of resistant and susceptible isolates to the various antibiotics

4. Discussion

The prevalence of E. coli in Barn Swallow droppings was low according to the findings of this study. Generally, the carriage of antibiotic resistance was observed to be high. Resistance to Ciprofloxacin was observed to be the least occurring. This suggests that the antibiotic is still effective against the isolated microbes. However, this finding seems to be opposite to the findings of another study which indicated that E. coli isolated from the Asian Open Bill Stork (Anastomus oscitans) were resistant to the antibiotic [33]. Findings of this study indicated the presence of a high number of multi-drug resistant E. coli in the samples obtained. This is in agreement with another recent study done in Taif Province of Saudi Arabia [34] that found multidrug resistance in E. coli isolated from both migratory and non-migratory birds (Hirrundo rustica included). However, it is worth noting that the Saudi Arabian study only used two birds of Hirrundo rustica species because the analysis was performed on a heterogeneous sample of birds. In our study, fifteen E. coli isolates were found to be ESBL producing strains. Although these ESBL producing strains were first isolated in 2006 from wild birds, more reports of their prevalence have been published in recent years, especially from European countries [35-44]. A recent comparative study on ESBL-producing E. coli carriage in raptors from Germany and Mongolia [45] found higher carriage rates in German than Mongolia (13.8% and 10.8% respectively). There are several factors which have been postulated to contribute to the prevalence of antibiotic resistance among wild birds in any given geographic area. Notably, the various characteristics of an area are more likely to contribute to antibiotic resistance than its actual location in the world. Natural preservation state, livestock and human densities, and the remoteness of an area have been put forward as important factors. In this study, the bird faecal samples were obtained from residential areas and schools which are located around two major hospitals, namely Kampala International University Teaching Hospital and Ishaka Adventist Hospitals. There are several other smaller clinics which serve the population in and around Ishaka. It is probable that since antibiotics are highly prescribed in these health institutions, microbes could have evolved mechanisms of becoming resistance to them. Another important thing to note is that Hirrundo rustica living in this area are frequently seen flying in and around these hospitals, where they could be easily picking the antibiotic resistant microbes from. There are other studies which have shown that the level of resistance in microbes seem to correlate with the degree of association to human activities [46,47]. Hospital waste water has been shown to be a reservoir of antibiotic resistant microbes in Nigeria [48]. This can significantly be a source from which wild birds pick-up antibiotic resistant E. coli. Studies done elsewhere have shown that aquatic associated species are seemingly more prone to pick up antibiotic resistance including ESBL-producing strains [49]. The fact that migrating birds travel long distances in short time frames and the large number of reports from many places concerning carriage of antibiotic resistant bacteria by wild birds leads to the genuine concern that spread of antibiotic resistance can be facilitated by wild birds. It is important to note that the bird species used in this study is a migratory bird. It will therefore not be surprising that the antibiotic resistant microbes isolated from this bird’s droppings could be found elsewhere in the continent or even in another continent. In a study conducted in Chile in recent years, the prevalence of ESBL-producing E. coli among Franklin’s gulls (Leucophaeus pipixcan) was found to be more than twice as high as in humans within the same geographical area [44].

5. Conclusion

In conclusion, our study and other studies done elsewhere have shown the carriage of antibiotic-resistant E. coli in wild birds. Such birds can act as reservoirs for antibiotic resistant microbes if enough attention is not given to the problem. Further research is recommended to determine the prevalence of antibiotic resistant E. coli from barn swallows residing in other parts of the country and even on the continent at large.

Acknowledgements

The authors would like to acknowledge the immense support received from Mr. Jackson, the lab technologist in Microbiology department.

Competing Interests

The authors have no competing interests

References

[1]   | Cohen ML “Epidemiology of drug resistance: implications for a post-antimicrobial era”. Science 257:1050-5.10.1126. 1992.
[2]   | Livermore DM. “Bacterial resistance: origins, epidemiology, and impact”. Clin Infect Dis; 36(Suppl 1):S11-23.10.1086 . 2003.
[3]   | Sjolund, M., J. Bonnedahl, J. Hernandez, S. Bengtsson, G. Cederbrant, J. Pinhassi, G. Kahlmeter, and B. Olsen. “Dissemination of multidrug-resistant bacteria into the Arctic”. Emerg. Infect. Dis. 14:70-72. 2008.

[4]  
Literak I, Dolejska M, Janoszowska D, Hrusakova J, Meissner W, Rzyska H, Bzoma S and Cizek A. “Antibiotic-Resistant Escherichia coli Bacteria, Including Strains with Genes Encoding the Extended-Spectrum Beta-Lactamase and QnrS, in Waterbirds on the Baltic Sea Coast of Poland”. Appl. Environ. Microbiol. 24 (76) 8126-8134. 2010.

[5]   | Livermore D. M., M. Warner L. M. C. Hall V. I. Enne S. J. Projan P. M. Dunman S. L. Wooster, and G. Harrison. “Antibiotic resistance in bacteria from magpies (Pica pica) and rabbits (Oryctolagus cuniculus) from west Wales”. Environ. Microbiol. 3:658-661. 2001.
[6]   | Wallace J. S, T. Cheasty, and K. Jones. “Isolation of Vero cytotoxin-producing Escherichia coli O157 from wild birds”. J. Appl. Microbiol. 82:399-404. 1997
[7]   | Blanco G., J. A. Lemus, and J. Grande. “Microbial pollution in wildlife: linking agricultural manuring and bacterial antibiotic resistance in red-billed choughs”. Environ. Res. 109: 405-412. 2009.
[8]   | Edge T. A., and. Hill S. “Occurrence of antibiotic resistance in Escherichia coli from surface waters and fecal pollution sources near Hamilton, Ontario”. Can. J. Microbiol. 51:501-505. 2005.
[9]   | Literak, I, R. Vanko, Dolejska M, Cizek A., and Karpiskova R. “Antibiotic resistant Escherichia coli and Salmonella in Russian rooks (Corvus frugilegus) wintering in the Czech Republic”. Lett. Appl. Microbiol. 45:616-621. 2007.
[10]   | Rose JM, Gast RJ, Bogomolni A, Ellis JC, Lentell BJ, Touhey K, et al. Occurrence and patterns of antibiotic resistance in vertebrates off the Northeastern United States coast. FEMS Microbiol Ecol.67:421-31. 2009.
[11]   | Nakamura M, Yoshimura H., and Koeda T. “Drug resistance and R plasmids of Escherichia coli strains isolated from six species of wild birds”. Jpn. J. Vet. Sci. 44:465-471. 1982.
[12]   | Sato, G., C. Oka, M. Asagi, and N. Ishiguro. “Detection of conjugative R plasmids conferring chloramphenicol resistance in Escherichia coli isolated from domestic and feral pigeons and crows”. Zentralbl. Bakteriol. Orig. A 241:407-417. 1978.
[13]   | Dolejska, M., Senk D, Cizek A, Rybarikova J, Sychra O, and Literak I.“Antimicrobial resistant Escherichia coli isolates in cattle and house sparrows on two Czech dairy farms”. Res. Vet. Sci. 85:491-494. 2008.

[14]  
Pawiak, R., Mazurkiewicz M, Molenda J, Pinowski J, and Wieliczko A.. The occurrence of Escherichia coli strains pathogenic to humans and animals in the eggs and nestlings of Passer spp., p. 139-151. In J. Pinowski, B. P. Kavanagh, and W. Górski (ed.), Nestling mortality of granivorous birds due to microorganisms and toxic substances. Proceedings of the International Symposium of the Working Group on Granivorous Birds, INTECOL. Polish Scientific Publishers, Warsaw, Poland. 1989.

[15]   | Dolejska M, Bierosova B, Kohoutova L, Literak I, and 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. 106: 1941-1950. 2009.
[16]   | Janecko N, Čížek A, Halová D, Karpíšková R, Myšková P, andLiterák I. “Prevalence, Characterization and Antibiotic Resistance of Salmonella Isolates in Large Corvid Species of Europe and North America Between 2010 and 2013”. Zoonoses and Public Health 62 (4): 292-300. 2015.

[17]  
Poeta P, Radhouani H, Igrejas G, Goncalves A, Carvalho C, Rodrigues J, Vinue L, Somalo S, and Torres C. “Seagulls of the Berlengas natural reserve of Portugal as carriers of fecal Escherichia coli harboring CTX-M and TEM extended-spectrum beta-lactamases”. Appl. Environ. Microbiol. 74:7439-7441. 2008.

[18]   | Cole D, Drum D. J. V, Stallknecht D. E, White D. G, Lee M. D, Ayers S, Sobsey M, and Maurer J. J. “Free-living Canada geese and antimicrobial resistance”. Emerg. Infect. Dis. 11:935-938. 2005.
[19]   | Dolejska M, Cizek A., and Literak I. “High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from black-headed gulls in the Czech Republic”. J. Appl. Microbiol. 103:11-19. 2007.
[20]   | Middleton J. H and Ambrose A. “Enumeration and antibiotic resistance patterns of fecal indicator organisms isolated from migratory Canada geese (Branta canadensis)”. J Wildl Dis; 41: 334-41. 2005.
[21]   | Andremont, A. “Commensal flora may play key role in spreading antibiotic resistance”. American Society for Microbiology News; 69:601-7. 2003.
[22]   | Gilliver MA, Bennett M, Begon M, Hazel SM and Hart CA “Antibiotic resistance found in wild rodents”. Nature;401:233-4. 1999.
[23]   | Lillehaug A, Bergsjo B, Schau J, Bruheim T, Vikoren T, Handeland K “Campylobacter spp., Salmonella spp., verocytotoxic Escherichia coli, and antibiotic resistance in indicator organisms in wild cervids”. Acta Vet Scand;46:23-32. 2005.
[24]   | Literak I, Dolejska M, Cizek A, Djigo C. A. T, Konecny A, and Koubek P. “Reservoirs of antibiotic-resistant Enterobacteriaceae among animals sympatric to humans in Senegal: extended-spectrum beta-lactamases in bacteria in a black rat (Rattus rattus)” Afr. J. Microbiol. Res. 3, 751-754. 2009.
[25]   | Gakuya FM, Kyule MN, Gathura PB, Kariuki S. “Antimicrobial susceptibility and plasmids from Escherichia coli isolated from rats” .East Afr. Med. J. 78: 518-522. 2001
[26]   | Okeke IN, Lamikanra A, Edelman R. “Socioeconomic and behavioral factors leading to acquired bacterial resistance to antibiotics in developing countries”. Emerg. Infect. Dis. 5: 18-27. 1999.
[27]   | Brown C.R,Bomberger Brown M (1999)Barn Swallow(Hirundo rustica). In The Birds on North America Online. Edited by Poole A. Ithaka: Cornell lab of Ornithology. http://bna.birds.cornell.edu/bna/species/452/articles/introduction accessed on (01/12/2015).
[28]   | Cramps S (1998) the Birds of western Palaearctic, Volume V. Oxford University Press, UK.
[29]   | MØller A.P. “The effect of dairy farming on Barn swallow Hirundo rustica abundance, distribution and reproduction”. J Appl Ecol. 38(2):378-389. 2001.
[30]   | Bandelj P, Trilar T, Blagus R, Ocepek M, Rousseau J, Weese JS, Vengust M. “Prevalence and molecular characterization of Clostridium difficile isolated from European Barn swallows (Hirundo rustica)during migration”. Veterinary Research 10:40. 2014.
[31]   | CLSI. 2008. Performance standards for antimicrobial susceptibility testing, 8th informational supplement. CLSI, Wayne, PA.

[32]  
Literak I, Dolejska M, Radimersky T, Klimes J, Friedman M, Aarestrup F. M, Hasman H, and Cizek A. “Antimicrobial resistant faecal Escherichia coli in wild mammals in central Europe: multiresistant Escherichia coli producing extended-spectrum beta-lactamases in wild boars”. J. Appl. Microbiol. 108:1702-1711. 2010.

[33]   | Rashid M, Rakib M.M and Hasan B. “Antimicrobial-resistant and ESBL-producing Escherichia coli in different ecological niches in Bangladesh”. Infection Ecology and Epidemiology 5: 26712. 2015.
[34]   | Shobrak MY and Abo-Amer AE. “Role of wild birds as carriers of multi-drug resistant Escherichia coli and Escherichia vulneris”. Brazilian Journal of Microbiology 45 (4) 1199-1209. 2014.
[35]   | Costa D, Poeta P, Saenz Y, Vinue L, Rojo-Bezares B, Jouini A, et al. “Detection of Escherichia coli harbouring extended-spectrum beta-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal”. J Antimicrob Chemother. 58:1311-12. 2006.
[36]   | Costa D, Poeta P, Saenz Y, Vinue L, Coelho AC, Matos M, et al. “Mechanisms of antibiotic resistance in Escherichia coli isolates recovered from wild animals”. Microb Drug Resist. 14:71-7. 2008.
[37]   | 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.106:1941-50. 2009.
[38]   | Poeta P, Radhouani H, Igrejas G, Goncalves A, Carvalho C, Rodrigues J, et al. “Seagulls of the Berlengas natural reserve of Portugal as carriers of fecal Escherichia coli harboring CTXM and TEM extended-spectrum beta-lactamases”. Appl Environ Microbiol.74:7439-41. 2008.
[39]   | Bonnedahl J, Drobni M, Gauthier-Clerc M, Hernandez J, Granholm S, Kayser Y, et al. “Dissemination of Escherichia coli with CTX-M type ESBL between humans and yellowlegged gulls in the south of France”. PLoS One.4:e5958. 2009.

[40]  
Bonnedahl J, Drobni P, Johansson A, Hernandez J, Melhus A, Stedt J, et al. “Characterization, and comparison, of human clinical and black-headed gull (Larus ridibundus) extendedspectrum beta-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden”. J Antimicrob Chemother. 65:1939-44. 2010.

[41]   | Literak I, Dolejska M, Rybarikova J, Cizek A, Strejckova P, Vyskocilova M, et al. “Highly variable patterns of antimicrobial resistance in commensal Escherichia coli isolates from pigs, sympatric rodents, and flies”. Microb Drug Resist.15: 229-37. 2009.
[42]   | Simoes RR, Poirel L, Da Costa PM, Nordmann P. “Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli”. Emerg Infect Dis.16:110-12. 2010.
[43]   | Wallensten A, Hernandez J, Ardiles K, Gonzalez-Acuna D, Drobni M, Olsen B. “Extended spectrum beta-lactamases detected in Escherichia coli from gulls in Stockholm, Sweden”. Infect Ecol Epidemiol.1:7030. 2011.

[44]  
Hernandez J, Johansson A, Stedt J, Bengtsson S, Porczak A, Granholm S, et al. “Characterization and comparison of extended-spectrum beta-lactamase (ESBL) resistance genotypes and population structure of Escherichia coli isolated from Franklin’s gulls (Leucophaeus pipixcan) and humans in Chile”. PLoS One.8:e76150. 2013.

[45]   | Guenther S, Aschenbrenner K, Stamm I, Bethe A, Semmler T, et al. “Comparable High Rates of Extended-Spectrum-Beta-Lactamase-Producing Escherichia coli in Birds of Prey from Germany and Mongolia”. PLoS ONE 7(12): e53039. 2012.
[46]   | 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.8:251-9. 2010.
[47]   | Skurnik D, Ruimy R, Andremont A, Amorin C, Rouquet P, Picard B, et al. “Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli”. J Antimicrob Chemother. 57:1215-19. 2006.
[48]   | Bolaji A.S, Akande I.O, Iromini F.A, Adewoye S.O and Opasola O.A. “Antibiotic resistance pattern of bacteria spp isolated from hospital waste water in Ede South Western, Nigeria”. European Journal of Experimental Biology. 1 (4):66-71. 2011.
[49]   | Veldman K, van Tulden P, Kant A, Testerink J, Mevius D. “Characteristics of cefotaxime-resistant Escherichia coli from wild birds in The Netherlands”. Appl Environ Microbiol. 79:7556-61. 2013.