Hostname: page-component-77c89778f8-5wvtr Total loading time: 0 Render date: 2024-07-19T09:44:16.501Z Has data issue: false hasContentIssue false

The role of gulls (Laridae) in the emergence and spreading of antibiotic resistance in the environment

Published online by Cambridge University Press:  11 October 2016

D. LJUBOJEVIĆ*
Affiliation:
Scientific Veterinary Institute “Novi Sad”, Rumenački put 20, 21000 Novi Sad, Serbia
V. RADOSAVLJEVIĆ
Affiliation:
Institute of Veterinary Medicine of Serbia, Vojvode Toze 14, 11000 Belgrade, Serbia
D. MILANOV
Affiliation:
Scientific Veterinary Institute “Novi Sad”, Rumenački put 20, 21000 Novi Sad, Serbia
Get access

Abstract

The importance of gulls as bioindicators, reservoirs and vectors of Escherichia coli strains resistant to the older generation of antibiotics, broad spectrum cephalosporins and fluoroquinolones is reviewed in the following paper. The aim is to highlight the fact that they could be a hot spot for the development of new resistance types. Even though gulls do not naturally come into contact with antibiotics, they are omnivorous and they often eat food in agricultural, rural and urban areas so they can be infected with resistant strains from livestock or human sources which they can spread again into the environment. They may then come into contact with poultry kept under free range conditions. More intensive investigations of this subject are required, as well as the need to find accurate and reliable preventive measures, are demonstrated in the present paper.

Type
Reviews
Copyright
Copyright © World's Poultry Science Association 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

ALLEN, H.K., DONATO, J., WANG, H.H., CLOUD-HANSEN, K.A., DAVIES, J. and HANDELSMAN, J. (2010) Call of the wild: antibiotic resistance genes in natural environments. Nature Reviews Microbiology 8: 251-259.Google Scholar
BONNEDAHL, J., DROBNI, M., GAUTHIER-CLERC, M., HERNANDEZ, J., GRANHOLM, S., KAYSER, Y., MELHUS, A., KAHLMETER, G., WALDENSTROM, J., JOHANSSON, A. and OLSEN, B. (2009) Dissemination of Escherichia coli with CTX-M type ESBL between humans and Yellow-legged gulls in the south of France. PLoS One 4: e5958.Google Scholar
BONNEDAHL, J., DROBNI, P., JOHANSSON, A., HERNANDEZ, J., MELHUS, Å., STEDT, J., OLSEN, B. and DROBNI, M. (2010) Characterisation, and comparison, of human clinical and black-headed gull (Larus ridibundus) extended-spectrum β-lactamase-producing bacterial isolates from Kalmar, on the southeast coast of Sweden. Journal of Antimicrobial Chemotherapy 65: 1939-1944.Google Scholar
BONNEDAHL, J., HERNANDEZ, J., STEDT, J., WALDENSTRÖM, J., OLSEN, B. and DROBNI, M. (2014) Extended-spectrum β-lactamases in Escherichia coli and Klebsiella pneumoniae in gulls, Alaska, USA. Emerging Infectious Diseases 20: 897-899.Google Scholar
CAMARDA, A., CIRCELLA, E., PENNELLI, D., MADIO, A., BRUNI, G., LAGRASTA, V., MARZANO, G., MALLIA, E. and CAMPAGNARI, E. (2010) Wild Birds as biological indicators of environmental pollution: biotyping and antimicrobial resistance patterns of Escherichia coli isolated from Audouin's gulls (Larus Audouinii) living in the Bay of Gallipoli (Italy). Italian Journal of Animal Science 5: 287-290.Google Scholar
CARATTOLI, A. (2008) Animal reservoirs for extended spectrum β-lactamase producers. Clinical Microbiology and Infection 14 (s1): 117-123.Google Scholar
COSTA, D., POETA, P., SÁENZ, Y., VINUÉ, L., ROJO-BEZARES, B., JOUINI, A., ZARAZAGA, M., RODRIGUES, J. and TORRES, C. (2006) Detection of Escherichia coli harbouring extended-spectrum β-lactamases of the CTX-M, TEM and SHV classes in faecal samples of wild animals in Portugal. Journal of Antimicrobial Chemotherapy 58: 1311-1312.Google Scholar
DOLEJSKA, M., CIZEK, A. and LITERAK, I. (2007) High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from Black-headed Gulls in the Czech Republic. Journal of Applied Microbiology 103: 11-19.Google Scholar
DOLEJSKA, M., BIEROŠOVÁ, B., KOHOUTOVA, L., LITERAK, I. and ČÍŽEK, A. (2009) Antibiotic-resistant Salmonella and Escherichia coli isolates with integrons and extended-spectrum beta-lactamases in surface water and sympatric black-headed gulls. Journal of Applied Microbiology 106: 1941-1950.CrossRefGoogle ScholarPubMed
EDGE, T.A. and HILL, S. (2005) Occurrence of antibiotic resistance in Escherichia coli from surface waters and faecal pollution sources near Hamilton, Ontario. Canadian Journal of Microbiology 51: 501-505.CrossRefGoogle ScholarPubMed
FOGARTY, L.R., HAACK, S.K., WOLCOTT, M.J. and WHITMAN, R.L. (2003) Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull faeces. Journal of Applied Microbiology 94: 865-878.Google Scholar
GALAS, M., DECOUSSER, J.W., BRETON, N., GODARD, T., ALLOUCH, P.Y., PINA, P. and COLLÈGE DE BACTÉRIOLOGIE VIROLOGIE HYGIÈNE (COLBVH) STUDY GROUP (2008) Nationwide study of the prevalence, characteristics, and molecular epidemiology of extended-spectrum-β-lactamase-producing Enterobacteriaceae in France. Antimicrobial Agents and Chemotherapy 52: 786-789.Google Scholar
GIONECHETTI, F., ZUCCA, P., GOMBAC, F., MONTI-BRAGADIN, C., LAGATOLLA, C., TONIN, E., EDALUCCI, E., VITALI, L.A. and DOLZANI, L. (2008) Characterisation of antimicrobial resistance and class 1 integrons in Enterobacteriaceae isolated from Mediterranean herring gulls (Larus cachinnans). Microbial Drug Resistance 14: 93-99.Google Scholar
GORDON, D.M. and COWLING, A. (2003) The distribution and genetic structure of Escherichia coli in Australian vertebrates: host and geographic effects. Microbiology 149: 3575-3586.Google Scholar
GUERRA, B., JUNKER, E., SCHROETER, A., MALORNY, B., LEHMANN, S. and HELMUTH, R. (2003) Phenotypic and genotypic characterisation of antimicrobial resistance in German Escherichia coli isolates from cattle, swine and poultry. Journal of Antimicrobial Chemotherapy 52: 489-492.Google Scholar
HERNANDEZ, J., BONNEDAHL, J., ELIASSON, I., WALLENSTEN, A., COMSTEDT, P., JOHANSSON, A., GRANHOLM, S., MELHUS, Å., OLSEN, B. and DROBNI, M. (2010) Globally disseminated human pathogenic Escherichia coli of O25b-ST131 clone, harbouring blaCTX-M-15, found in Glaucous-winged gull at remote Commander Islands, Russia. Environmental microbiology reports 2: 329-332.Google Scholar
KANG, H.Y., JEONG, Y.S., OH, J.Y., TAE, S.H., CHOI, C.H., MOON, D.C., LEE, W.K., LEE, Y.C., SEOL, S.Y., CHO, D.T. and LEE, J.C. (2005) Characterisation of antimicrobial resistance and class 1 integrons found in Escherichia coli isolates from humans and animals in Korea. Journal of Antimicrobial Chemotherapy 55: 639-644.Google Scholar
LANZ, R., KUHNERT, P. and BOERLIN, P. (2003) Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Veterinary Microbiology 91: 73-84.Google Scholar
LE DEVENDEC, L., BOUDER, A., DHEILLY, A., HELLARD, G. and KEMPF, I. (2011) Persistence and spread of qnr, extended-spectrum beta-lactamase, and ampC resistance genes in the digestive tract of chickens. Microbial Drug Resistance 17: 129-134.Google Scholar
LÉVESQUE, B., BROUSSEAU, P., BERNIER, F., DEWAILLY, É. and JOLY, J. (2000) Study of the bacterial content of ring-billed gull droppings in relation to recreational water quality. Water Research 34: 1089-1096.Google Scholar
LITERAK, I., DOLEJSKA, M., JANOSZOWSKA, D., HRUSAKOVA, J., MEISSNER, W., RZYSKA, H., BZOMA, S. and CIZEK, A. (2010) 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. Applied and Environmental Microbiology 76: 8126-8134.Google Scholar
LJUBOJEVIĆ, D., PUVAČA, N., PELIĆ, M., TODOROVIĆ, D., PAJIĆ, M., MILANOV, D. and VELHNER, M. (2016) Epidemiological significance of poultry litter for spreading the antibiotic-resistant strains of Escherichia coli. World's Poultry Science Journal72: 485-494.Google Scholar
MAKINO, S., KOBORI, H., ASAKURA, H., WATARAI, M., SHIRAHATA, T., IKEDA, T., TAKESHI, K. and TSUKAMOTO, T. (2000) Detection and characterisation of Shiga toxin-producing Escherichia coli from seagulls. Epidemiology and Infection 125: 55-61.Google Scholar
MILANOV, D., PRUNIĆ, B., VELHNER, M., TODOROVIĆ, D. and POLAČEK, V. (2015) Investigation of Biofilm Formation and Phylogenetic Typing of Escherichia Coli Strains Isolated from Milk of Cows with Mastitis. Acta Veterinaria 65: 202-216.Google Scholar
MOULIN-SCHOULEUR, M., RÉPÉRANT, M., LAURENT, S., BRÉE, A., MIGNON-GRASTEAU, S., GERMON, P., RASSCHAERT, D. and SCHOULER, C. (2007) Extraintestinal pathogenic Escherichia coli strains of avian and human origin: link between phylogenetic relationships and common virulence patterns. Journal of Clinical Microbiology 45: 3366-3376.Google Scholar
NABER, K.G., SCHITO, G., BOTTO, H., PALOU, J. and MAZZEI, T. (2008) Surveillance study in Europe and Brazil on clinical aspects and Antimicrobial Resistance Epidemiology in Females with Cystitis (ARESC): implications for empiric therapy. European Urology 54: 1164-1178.Google Scholar
NIELSEN, E.M., SKOV, M.N., MADSEN, J.J., LODAL, J., JESPERSEN, J.B. and BAGGESEN, D.L. (2004) Verocytotoxin-producing Escherichia coli in wild birds and rodents in close proximity to farms. Applied and Environmental Microbiology 70: 6944-6947.Google Scholar
ÖSTERBLAD, M., NORRDAHL, K., KORPIMÄKI, E. and HUOVINEN, P. (2001) Antibiotic resistance: How wild are wild mammals? Nature 409: 37-38.Google Scholar
PATERSON, D.L. and BONOMO, R.A. (2005) Extended-spectrum β-lactamases: a clinical update. Clinical Microbiology Reviews 18: 657-686.Google Scholar
POETA, P., RADHOUANI, H., IGREJAS, G., GONÇALVES, A., CARVALHO, C., RODRIGUES, J., VINUÉ, L., SOMALO, S. and TORRES, C. (2008) Seagulls of the Berlengas natural reserve of Portugal as carriers of faecal Escherichia coli harbouring CTX-M and TEM extended-spectrum beta-lactamases. Applied and Environmental Microbiology 74: 7439-7441.Google Scholar
RADHOUANI, H., POETA, P., IGREJAS, G., GONÇALVES, A., VINUE, L. and TORRES, C. (2009) Antimicrobial resistance and phylogenetic groups in isolates of Escherichia coli from seagulls at the Berlengas nature reserve. The Veterinary record 165: 138.Google Scholar
ROLAIN, J.M., CANTON, R. and CORNAGLIA, G. (2012) Emergence of antibiotic resistance: need for a new paradigm. Clinical Microbiology and Infection 18: 615-616.CrossRefGoogle ScholarPubMed
ROSE, J.M., GAST, R.J., BOGOMOLNI, A., ELLIS, J.C., LENTELL, B.J., TOUHEY, K. and MOORE, M. (2009) Occurrence and patterns of antibiotic resistance in vertebrates off the Northeastern United States coast. FEMS Microbiology Ecology 67: 421-431.Google Scholar
SIMÕES, R.R., POIREL, L., DA COSTA, P.M. and NORDMANN, P. (2010) Seagulls and beaches as reservoirs for multidrug-resistant Escherichia coli . Emerging Infectious Diseases 16: 110-112.Google Scholar
SJÖLUND, M., BONNEDAHL, J., HERNANDEZ, J., BENGTSSON, S., CEDERBRANT, G., PINHASSI, J., KAHLMETER, G. and OLSEN, B. (2008) Dissemination of multidrug-resistant bacteria into the Arctic. Emerging Infectious Diseases 14: 70-72.Google Scholar
SKURNIK, D., RUIMY, R., ANDREMONT, A., AMORIN, C., ROUQUET, P., PICARD, B. and DENAMUR, E. (2006) Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli . Journal of Antimicrobial chemotherapy 57: 1215-1219.Google Scholar
SØRUM, H. and SUNDE, M. (2001) Resistance to antibiotics in the normal flora of animals. Veterinary Research 32: 227-241.Google Scholar
STEDT, J., BONNEDAHL, J., HERNANDEZ, J., MCMAHON, B.J., HASAN, B., OLSEN, B., DROBNI, M. and WALDENSTRÖM, J. (2014) Antibiotic resistance patterns in Escherichia coli from gulls in nine European countries. Infection Ecology & Epidemiology 4: 21565.Google Scholar
STEDT, J., BONNEDAHL, J., HERNANDEZ, J., WALDENSTRÖM, J., MCMAHON, B.J., TOLF, C., OLSEN, B. and DROBNI, M. (2015) Carriage of CTX-M type extended spectrum β-lactamases (ESBLs) in gulls across Europe. Acta Veterinaria Scandinavica 57: 74.Google Scholar
STRAHILEVITZ, J., JACOBY, G.A., HOOPER, D.C. and ROBICSEK, A. (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clinical Microbiology Reviews 22: 664-689.Google Scholar
TODOROVIĆ, D., VELHNER, M., LJUBOJEVIĆ, D., PAJIĆ, M. and MILANOV, D. (2015) Resistance to fluoroquinolones in Escherichia coli from pigs. Archives of Veterinary Medicine 8: 103-112.Google Scholar
VELHNER, M., PETROVIĆ, J., STOJANOV, I., RATAJAC, R. and STOJANOVIĆ, D. (2010) Mehanizmi prenošenja rezistencije kod baktrija. Archives of Veterinary Medicine 3: 85-92.Google Scholar
VELHNER, M. and MILANOV, D. (2015) Resistance to tetracycline in Escherichia coli and Staphylococcus aureus: brief overview on mechanisms of resistance and epidemiology. Archives of Veterinary Medicine 8: 27-36.Google Scholar
WRAY, C. and GNANOU, J.C. (2000) Antibiotic resistance monitoring in bacteria of animal origin: analysis of national monitoring programmes. International Journal of Antimicrobial Agents 14: 291-294.Google Scholar