Antimicrobial-Resistant Enterococcus spp. in Wild Avifauna from Central Italy
Abstract
:1. Introduction
2. Results
2.1. Enterococcus spp. Isolation
2.2. Antimicrobial Susceptibility Tests
2.2.1. Agar Disk Diffusion Test
2.2.2. Vancomycin and Ampicillin MIC and HLAR
2.2.3. Classification of Isolates in Relation to Antimicrobial Resistance
2.3. Genotypic Resistance
2.4. Correlation between Phenotypic and Genotypic Resistance
3. Discussion
4. Materials and Methods
4.1. Sampling
4.2. Enterococcus spp. Isolation
4.3. Antimicrobial Susceptibility Tests
4.3.1. Agar Disk Diffusion Test
4.3.2. High-Level Aminoglycoside Resistance (HLAR) and Minimum Inhibitory Concentration (MIC) for Vancomycin and Ampicillin
4.3.3. Classification of Isolates in Relation to Antimicrobial Resistance
4.4. Genotypic Resistance
4.5. Statistical Analyses
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ramos, S.; Silva, V.; Dapkevicius, M.d.L.E.; Igrejas, G.; Poeta, P. Enterococci, from harmless bacteria to a pathogen. Microorganisms 2020, 8, 1118. [Google Scholar] [CrossRef] [PubMed]
- Hegstad, K.; Mikalsen, T.; Coque, T.M.; Werner, G.; Sundsfjord, A. Mobile genetic elements and their contribution to the emergence of antimicrobial resistant Enterococcus faecalis and Enterococcus faecium. Clin. Microbiol. Infect. 2010, 16, 541–554. [Google Scholar] [CrossRef] [PubMed]
- Schwaiger, K.; Schmied, E.M.V.; Bauer, J. Comparative Analysis on Antibiotic Resistance Characteristics of Listeria spp. and Enterococcus spp. Isolated from Laying Hens and Eggs in Conventional and Organic Keeping Systems in Bavaria, Germany. Zoonoses Public Health 2010, 57, 171–180. [Google Scholar] [CrossRef] [PubMed]
- Bertelloni, F.; Salvadori, C.; Moni, A.; Cerri, D.; Mani, P.; Ebani, V.V. Antimicrobial resistance in Enterococcus spp. Isolated from laying hens of backyard poultry flocks. Ann. Agric. Environ. Med. 2015, 22, 665–669. [Google Scholar] [CrossRef] [Green Version]
- Roy, K.; Islam, M.S.; Paul, A.; Ievy, S.; Talukder, M.; Sobur, M.A.; Ballah, F.M.; Khan, M.S.R.; Rahman, M.T. Molecular detection and antibiotyping of multi-drug resistant Enterococcus faecium from healthy broiler chickens in Bangladesh. Vet. Med. Sci. 2022, 8, 200–210. [Google Scholar] [CrossRef]
- EFSA AHAW Panel (EFSA Panel on Animal Health and Welfare); Nielsen, S.S.; Bicout, D.J.; Calistri, P.; Canali, E.; Drewe, J.A.; Garin-Bastuji, B.; Gonzales Rojas, J.L.; Gortázar, C.; Herskin, M.; et al. Assessment of listing and categorisation of animal diseases within the framework of the Animal Health Law (Regulation (EU) No 2016/429): Antimicrobial-resistant Enterococcus faecalis in poultry. EFSA J. 2022, 20, e07127. [Google Scholar] [CrossRef]
- Werner, G.; Coque, T.M.; Franz, C.M.A.P.; Grohmann, E.; Hegstad, K.; Jensen, L.; van Schaik, W.; Weaver, K. Antibiotic resistant enterococci-Tales of a drug resistance gene trafficker. Int. J. Med. Microbiol. 2013, 303, 360–379. [Google Scholar] [CrossRef]
- Maësaar, M.; Tedersoo, T.; Meremaë, K.; Roasto, M. The source attribution analysis revealed the prevalent role of poultry over cattle and wild birds in human campylobacteriosis cases in the Baltic States. PLoS ONE 2020, 15, e0235841. [Google Scholar] [CrossRef]
- Aun, E.; Kisand, V.; Laht, M.; Telling, K.; Kalmus, P.; Väli, Ü.; Brauer, A.; Remm, M.; Tenson, T. Molecular Characterization of Enterococcus Isolates from Different Sources in Estonia Reveals Potential Transmission of Resistance Genes among Different Reservoirs. Front. Microbiol. 2021, 12, 601490. [Google Scholar] [CrossRef]
- Contreras, A.; Gómez-Martín, A.; Paterna, A.; Tatay-Dualde, J.; Prats-Van Der Ham, M.; Corrales, J.C.; De La Fe, C.; Sánchez, A. Epidemiological role of birds in the transmission and maintenance of zoonoses. Rev. Sci. Tech. 2016, 35, 845–862. [Google Scholar] [CrossRef]
- Marrow, J.; Whittington, J.K.; Mitchell, M.; Hoyer, L.L.; Maddox, C. Prevalence and antibiotic-resistance characteristics of Enterococcus spp. Isolated isolated from free-living and captive raptors in central Iillinois. J. Wildl. Dis. 2009, 45, 302–313. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Santos, T.; Silva, N.; Igrejas, G.; Rodrigues, P.; Micael, J.; Rodrigues, T.; Resendes, R.; Gonçalves, A.; Marinho, C.; Gonçalves, D.; et al. Dissemination of antibiotic resistant Enterococcus spp. and Escherichia coli from wild birds of Azores Archipelago. Anaerobe 2013, 24, 25–31. [Google Scholar] [CrossRef] [PubMed]
- Radhouani, H.; Poeta, P.; Gonçalves, 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, 837–843. [Google Scholar] [CrossRef] [PubMed]
- Stępień-Pyśniak, D.; Hauschild, T.; Nowaczek, A.; Marek, A.; Dec, M. Wild birds as a potential source of known and novel multilocus sequence types of antibiotic-resistant Enterococcus faecalis. J. Wildl. Dis. 2018, 54, 219–228. [Google Scholar] [CrossRef]
- Stȩpień-Pyśniak, D.; Hauschild, T.; Dec, M.; Marek, A.; Urban-Chmiel, R. Clonal Structure and Antibiotic Resistance of Enterococcus spp. from Wild Birds in Poland. Microb. Drug Resist. 2019, 25, 1227–1237. [Google Scholar] [CrossRef]
- León-Sampedro, R.; del Campo, R.; Rodriguez-Baños, M.; Lanza, V.F.; Pozuelo, M.J.; Francés-Cuesta, C.; Tedim, A.P.; Freitas, A.R.; Novais, C.; Peixe, L.; et al. Phylogenomics of Enterococcus faecalis from wild birds: New insights into host-associated differences in core and accessory genomes of the species. Environ. Microbiol. 2019, 21, 3046–3062. [Google Scholar] [CrossRef]
- Stogios, P.J.; Savchenko, A. Molecular mechanisms of vancomycin resistance. Protein Sci. 2020, 29, 654. [Google Scholar] [CrossRef]
- Miller, W.R.; Munita, J.M.; Arias, C.A. Mechanisms of antibiotic resistance in enterococci. Expert Rev. Anti Infect. Ther. 2014, 12, 1221–1236. [Google Scholar] [CrossRef]
- Ebani, V.V.; Guardone, L.; Bertelloni, F.; Perrucci, S.; Poli, A.; Mancianti, F. Survey on the Presence of Bacterial and Parasitic Zoonotic Agents in the Feces of Wild Birds. Vet. Sci. 2021, 8, 171. [Google Scholar] [CrossRef]
- Verhagen, J.H.; Fouchier, R.A.M.; Lewis, N. Highly Pathogenic Avian Influenza Viruses at the Wild–Domestic Bird Interface in Europe: Future Directions for Research and Surveillance. Viruses 2021, 13, 212. [Google Scholar] [CrossRef]
- Ahmed, Z.S.; Elshafiee, E.A.; Khalefa, H.S.; Kadry, M.; Hamza, D.A. Evidence of colistin resistance genes (mcr-1 and mcr-2) in wild birds and its public health implication in Egypt. Antimicrob. Resist. Infect. Control 2019, 8, 197. [Google Scholar] [CrossRef] [PubMed]
- Nowaczek, A.; Dec, M.; Stępień-Pyśniak, D.; Urban-Chmiel, R.; Marek, A.; Różański, P. Antibiotic Resistance and Virulence Profiles of Escherichia coli Strains Isolated from Wild Birds in Poland. Pathogens 2021, 10, 1059. [Google Scholar] [CrossRef] [PubMed]
- Ben Yahia, H.; Chairat, S.; Hamdi, N.; Gharsa, H.; Ben Sallem, R.; Ceballos, S.; Torres, C.; Ben Slama, K. Antimicrobial resistance and genetic lineages of faecal enterococci of wild birds: Emergence of vanA and vanB2 harbouring Enterococcus faecalis. Int. J. Antimicrob. Agents 2018, 52, 936–941. [Google Scholar] [CrossRef] [PubMed]
- Stępień-Pyśniak, D.; Hauschild, T.; Różański, P.; Marek, A. MALDI-TOF mass spectrometry as a useful tool for identification of Enterococcus spp. from wild birds and differentiation of closely related species. J. Microbiol. Biotechnol. 2017, 27, 1128–1137. [Google Scholar] [CrossRef] [PubMed]
- Tardón, A.; Bataller, E.; Llobat, L.; Jiménez-Trigos, E. Bacteria and antibiotic resistance detection in fractures of wild birds from wildlife rehabilitation centres in Spain. Comp. Immunol. Microbiol. Infect. Dis. 2021, 74, 101575. [Google Scholar] [CrossRef]
- Hammerum, A.M. Enterococci of animal origin and their significance for public health. Clin. Microbiol. Infect. 2012, 18, 619–625. [Google Scholar] [CrossRef]
- Saengsuwan, P.; Singkhamanan, K.; Madla, S.; Ingviya, N.; Romyasamit, C. Molecular epidemiology of vancomycinresistant Enterococcus faecium clinical isolates in a tertiary care hospital in southern Thailand: A retrospective study. PeerJ 2021, 9, e11478. [Google Scholar] [CrossRef]
- Nocera, F.P.; Ferrara, G.; Scandura, E.; Ambrosio, M.; Fiorito, F.; De Martino, L. A Preliminary Study on Antimicrobial Susceptibility of Staphylococcus spp. and Enterococcus spp. Grown on Mannitol Salt Agar in European Wild Boar (Sus scrofa) Hunted in Campania Region-Italy. Animals 2021, 12, 85. [Google Scholar] [CrossRef]
- Oliveira de Araujo, G.; Huff, R.; Favarini, M.O.; Mann, M.B.; Peters, F.B.; Frazzon, J.; Guedes Frazzon, A.P. Multidrug Resistance in Enterococci Isolated from Wild Pampas Foxes (Lycalopex gymnocercus) and Geoffroy’s Cats (Leopardus geoffroyi) in the Brazilian Pampa Biome. Front. Vet. Sci. 2020, 7, 606377. [Google Scholar] [CrossRef]
- Kristich, C.J.; Rice, L.B.; Arias, C.A. Enterococcal Infection—Treatment and Antibiotic Resistance. In Enterococci: From Commensals to Leading Causes of Drug Resistant Infection; Gilmore, M., Clewell, D., Ike, Y., Shankar, N., Eds.; Massachusetts Eye and Ear Infirmary: Boston, MA, USA, 2014. [Google Scholar]
- Miller, W.R.; Murray, B.E.; Rice, L.B.; Arias, C.A. Resistance in Vancomycin-Resistant Enterococci. Infect. Dis. Clin. N. Am. 2020, 34, 751–771. [Google Scholar] [CrossRef]
- Lozano, C.; Gonzalez-Barrio, D.; Camacho, M.C.; Lima-Barbero, J.F.; de la Puente, J.; Höfle, U.; Torres, C. Characterization of fecal vancomycin-resistant enterococci with acquired and intrinsic resistance mechanisms in wild animals, Spain. Microb. Ecol. 2016, 72, 813–820. [Google Scholar] [CrossRef] [PubMed]
- Dec, M.; Stȩpień-Pyśniak, D.; Gnat, S.; Fratini, F.; Urban-Chmiel, R.; Cerri, D.; Winiarczyk, S.; Turchi, B. Antibiotic Susceptibility and Virulence Genes in Enterococcus Isolates from Wild Mammals Living in Tuscany, Italy. Microb. Drug Resist. 2020, 26, 505–519. [Google Scholar] [CrossRef] [PubMed]
- Bertelloni, F.; Salvadori, C.; Lotti, G.; Cerri, D.; Ebani, V.V. Antimicrobial resistance in Enterococcus strains isolated from healthy domestic dogs. Acta Microbiol. Immunol. Hung. 2017, 64, 301–312. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stępień-Pyśniak, D.; Bertelloni, F.; Dec, M.; Cagnoli, G.; Pietras-Ożga, D.; Urban-Chmiel, R.; Ebani, V.V. Characterization and Comparison of Enterococcus spp. Isolates from Feces of Healthy Dogs and Urine of Dogs with UTIs. Animals 2021, 11, 2845. [Google Scholar] [CrossRef] [PubMed]
- Özdemir, R.; Tuncer, Y. Detection of antibiotic resistance profiles and aminoglycoside-modifying enzyme (AME) genes in high-level aminoglycoside-resistant (HLAR) enterococci isolated from raw milk and traditional cheeses in Turkey. Mol. Biol. Rep. 2020, 47, 1703–1712. [Google Scholar] [CrossRef]
- Shete, V.; Grover, N.; Kumar, M. Analysis of Aminoglycoside Modifying Enzyme Genes Responsible for High-Level Aminoglycoside Resistance among Enterococcal Isolates. J. Pathog. 2017, 2017, 3256952. [Google Scholar] [CrossRef] [Green Version]
- Torres, C.; Alonso, C.A.; Ruiz-Ripa, L.; León-Sampedro, R.; del Campo, R.; Coque, T.M. Antimicrobial Resistance in Enterococcus spp. of animal origin. Antimicrob. Resist. Bact. Livest. Companion Anim. 2018, 6, 185–227. [Google Scholar] [CrossRef]
- Chen, Y.H.; Lin, S.Y.; Lin, Y.T.; Tseng, S.P.; Chang, C.C.; Yu, S.Y.; Hung, W.W.; Jao, Y.T.; Lin, C.Y.; Chen, Y.H.; et al. Emergence of aac(6′)-Ie-aph(2″)-Ia-positive enterococci with non-high-level gentamicin resistance mediated by IS1216V: Adaptation to decreased aminoglycoside usage in Taiwan. J. Antimicrob. Chemother. 2021, 76, 1689–1697. [Google Scholar] [CrossRef]
- European Medicines Agency. Sales of Veterinary Antimicrobial Agents in 31 European Countries in 2017; European Medicines Agency: Amsterdam, The Nederland, 2019. [Google Scholar]
- Yang, Q.; Gao, Y.; Ke, J.; Show, P.L.; Ge, Y.; Liu, Y.; Guo, R.; Chen, J. Antibiotics: An overview on the environmental occurrence, toxicity, degradation, and removal methods. Bioengineered 2021, 12, 7376. [Google Scholar] [CrossRef]
- de Jong, A.; Simjee, S.; El Garch, F.; Moyaert, H.; Rose, M.; Youala, M.; Dry, M. Antimicrobial susceptibility of enterococci recovered from healthy cattle, pigs and chickens in nine EU countries (EASSA Study) to critically important antibiotics. Vet. Microbiol. 2018, 216, 168–175. [Google Scholar] [CrossRef]
- Dadashi, M.; Sharifian, P.; Bostanshirin, N.; Hajikhani, B.; Bostanghadiri, N.; Khosravi-Dehaghi, N.; van Belkum, A.; Darban-Sarokhalil, D. The Global Prevalence of Daptomycin, Tigecycline, and Linezolid-Resistant Enterococcus faecalis and Enterococcus faecium Strains from Human Clinical Samples: A Systematic Review and Meta-Analysis. Front. Med. 2021, 8, 720647. [Google Scholar] [CrossRef] [PubMed]
- Miranda, C.; Silva, V.; Igrejas, G.; Poeta, P. Impact of European pet antibiotic use on enterococci and staphylococci antimicrobial resistance and human health. Future Microbiol. 2021, 16, 185–201. [Google Scholar] [CrossRef]
- Leite-Martins, L.; Mahú, M.I.; Costa, A.L.; Bessa, L.J.; Vaz-Pires, P.; Loureiro, L.; Niza-Ribeiro, J.; De Matos, A.J.F.; Martins Da Costa, P. Prevalence of antimicrobial resistance in faecal enterococci from vet-visiting pets and assessment of risk factors. Vet. Rec. 2015, 176, 674. [Google Scholar] [CrossRef] [PubMed]
- CLSI (Clinical and Laboratory Standards Institute). M02-A12—Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard—Twelfth Edition; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2015; pp. 1–96. [Google Scholar]
- CLSI (Clinical and Laboratory Standards Institute). Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fifth Informational Supplement; CLSI Document M100-S25; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2015. [Google Scholar]
- EUCAST (The European Committee on Antimicrobial Susceptibility Testing). Breakpoint Tables for Interpretation of MICs and Zone Diameters; Version 10.0; The European Committee on Antimicrobial Susceptibility Testing: Basel, Switzerland, 2020. [Google Scholar]
- CLSI (Clinical and Laboratory; Standards Institute). M07-A10 Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard-Tenth Edition; CLSI Document M07-A10; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2015. [Google Scholar]
- Magiorakos, A.P.; Srinivasan, A.; Carey, R.B.; Carmeli, Y.; Falagas, M.E.; Giske, C.G.; Harbarth, S.; Hindler, J.F.; Kahlmeter, G.; Olsson-Liljequist, B.; et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 2012, 18, 268–281. [Google Scholar] [CrossRef] [Green Version]
- Dutka-Malen, S.; Evers, S.; Courvalin, P. Detection of glycopeptide resistance genotypes and identification to the species level of clinically relevant enterococci by PCR. J. Clin. Microbiol. 1995, 33, 24. [Google Scholar] [CrossRef] [Green Version]
- Vakulenko, S.B.; Donabedian, S.M.; Voskresenskiy, A.M.; Zervos, M.J.; Lerner, S.A.; Chow, J.W. Multiplex PCR for Detection of Aminoglycoside Resistance Genes in Enterococci. Antimicrob. Agents Chemother. 2003, 47, 1423. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kobayashi, N.; Mahbub Alam, M.; Nishimoto, Y.; Urasawa, S.; Uehara, N.; Watanabe, N. Distribution of aminoglycoside resistance genes in recent clinical isolates of Enterococcus faecalis, Enterococcus faecium and Enterococcus avium. Epidemiol. Infect. 2001, 126, 197. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Malhotra-Kumar, S.; Lammens, C.; Piessens, J.; Goossens, H. Multiplex PCR for Simultaneous Detection of Macrolide and Tetracycline Resistance Determinants in Streptococci. Antimicrob. Agents Chemother. 2005, 49, 4798. [Google Scholar] [CrossRef] [Green Version]
- Doherty, N.; Trzcinski, K.; Pickerill, P.; Zawadzki, P.; Dowson, C.G. Genetic Diversity of the tet(M) Gene in Tetracycline-Resistant Clonal Lineages of Streptococcus pneumoniae. Antimicrob. Agents Chemother. 2000, 44, 2979. [Google Scholar] [CrossRef] [Green Version]
Antibiotics | Susceptible | Intermediate | Resistant | ||||
---|---|---|---|---|---|---|---|
Class | Molecules | Number of Isolates | % | Number of Isolates | % | Number of Isolates | % |
Ansamycins | RD | 33 | 32.04 | 13 | 12.62 | 57 | 55.34 |
Phenicols | C | 58 | 56.31 | 16 | 15.53 | 29 | 28.16 |
Oxazolidinones | LZD | 43 | 41.75 | 17 | 16.50 | 43 | 41.75 |
Nitrofurantoins | F | 43 | 41.75 | 19 | 18.45 | 41 | 39.81 |
Folate pathway antagonists | W | 2 | 1.94 | 57 | 55.34 | 44 | 42.72 |
Aminoglycoside | N | 0 | 0.00 | 14 | 13.59 | 89 | 86.41 |
CN | 17 | 16.50 | 19 | 18.45 | 67 | 65.05 | |
S | 1 | 0.97 | 11 | 10.68 | 91 | 88.35 | |
Cephems | KF | 9 | 8.74 | 14 | 13.59 | 80 | 77.67 |
Fluoroquinolones | CIP | 15 | 14.56 | 35 | 33.98 | 53 | 51.46 |
ENR | 8 | 7.77 | 22 | 21.36 | 73 | 70.87 | |
Glycopeptides | TEC | 63 | 61.17 | 23 | 22.33 | 17 | 16.50 |
VA | 29 | 28.16 | 36 | 34.95 | 38 | 36.89 | |
Macrolides, Streptogramins, Lincosamides | E | 8 | 7.77 | 44 | 42.72 | 51 | 49.51 |
QD | 11 | 10.68 | 22 | 21.36 | 70 | 67.96 | |
DA | 8 | 7.77 | 4 | 3.88 | 91 | 88.35 | |
Penicillins | OX | 0 | 0.00 | 0 | 0.00 | 103 | 100.00 |
AMC | 80 | 77.67 | 12 | 11.65 | 11 | 10.68 | |
AMP | 78 | 75.73 | 1 | 0.97 | 24 | 23.30 | |
Tetracyclines | TE | 27 | 26.21 | 20 | 19.42 | 56 | 54.37 |
TCG | 36 | 34.95 | 25 | 24.27 | 42 | 40.78 |
Number of Enterococcus Isolates (%) | |||||||||
---|---|---|---|---|---|---|---|---|---|
Examined | Vancomycin Resistant | Ampicillin MIC ≥64 mg/L | HLSR | HLGR | MDR | XDR | PDR | ||
Total | 103 | 5 (4.85) | 6 (5.83) | 34 (33.01) | 15 (14.56) | 79 (76.69) | 20 (19.41) | 3 (2.91) | |
Provenience of birds | Hunting activity | 42 | 1 (2.38) | 0 (0.00) | 3 (7.14) | 2 (4.76) | 26 (61.90) | 15 (35.71) | 1 (2.38) |
Recovery center | 61 | 4 (6.56) | 6 (14.28) | 31 (50.82) | 13 (21.31) | 53 (86.89) | 5 (8.20) | 2 (3.28) | |
Avian category | Synanthropic birds | 18 | 0 (0.00) | 2 (11.11) | 9 (50) | 2 (11.11) | 14 (77.78) | 2 11.11) | 2 (11.11) |
Raptors | 17 | 2 (11.76) | 2 (11.76) | 10 (58.82) | 4 (23.53) | 16 (94.12) | 1 (5.88) | 0 (0.00) | |
Aquatic birds | 68 | 3 (4.41) | 2 (2.94) | 15 (22.06) | 9 (13.24) | 49 (72.06) | 17 (25.00) | 1 (1.47) | |
Bacterial species | E. faecium | 62 | 3 (4.84) | 5 (8.06) | 24 (38.71) | 7 (11.29) | 46 (74.19) | 13 (30.97) | 3 (4.84) |
E. faecalis | 36 | 2 (5.56) | 0 (0.00) | 8 (22.22) | 7 (19.44) | 29 (80.56) | 7 (19.44) | 0 (0.00) | |
E. avium | 3 | 0 (0.00) | 0 (0.00) | 1 (33.33) | 0 (0.00) | 2 (66.67) | 0 (0.00) | 0 (0.00) | |
E. durans | 2 | 0 (0.00) | 1 (50.00) | 1 (50.00) | 1 (50.00) | 2 (100) | 0 | 0 (0.00) |
Provenience of Birds | Avian Category | Bacterial Species | ||||||||
---|---|---|---|---|---|---|---|---|---|---|
Total | Hunting Activity | Recovery Center | Synanthropic Birds | Raptors | Aquatic Birds | E. durans | E. avium | E. faecalis | E. faecium | |
Examined | 103 | 42 | 61 | 18 | 17 | 68 | 2 | 3 | 36 | 62 |
vanA | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) |
vanB | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) |
aac(6′)-Ie-aph(2″)-Ia | 6 (5.82%) | 0 (0.00%) | 6 (9.84%) | 3 (16.67%) | 1 (5.88%) | 2 (2.94%) | 0 (0.00%) | 0 (0.00%) | 2 (5.56%) | 4 (6.45%) |
ant(6)-Ia | 17 (16.50%) | 2 (4.76%) | 15 (24.59%) | 5 (27.78%) | 3 (17.65%) | 9 (13.24%) | 0 (0.00%) | 1 (33.33%) | 5 (13.89%) | 11 (17.74%) |
aac(6′)-li | 55 (53.39%) | 23 (54.76%) | 32 (52.46%) | 10 (55.56%) | 11 (64.71%) | 34 (50.00%) | 0 (0.00%) | 2 (66.67%) | 3 (8.33%) | 50 (80.65%) |
tet(M) | 34 (33.01%) | 8 (19.05%) | 26 (42.62%) | 7 (38.89%) | 7 (41.18%) | 20 (29.41%) | 0 (0.00%) | 1 (33.33%) | 11 (30.56%) | 22 (35.48%) |
tet(L) | 9 (8.74%) | 2 (4.76%) | 7 (11.48%) | 0 (0.00%) | 3 (17.65%) | 6 (8.82%) | 0 (0.00%) | 0 (0.00%) | 4 (11.11%) | 5 (8.06%) |
tet(O) | 2 (1.94%) | 0 (0.00%) | 2 (3.28%) | 0 (0.00%) | 0 (0.00%) | 2 (2.94%) | 0 (0.00%) | 0 (0.00%) | 2 (5.56%) | 0 (0.00%) |
tet(K) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) | 0 (0.00%) |
Int-Tn | 12 (11.65%) | 4 (3.88%) | 8 (7.77%) | 3 (16.67%) | 3 (17.65%) | 6 (8.82%) | 0 (0.00%) | 1 (33.33%) | 2 (5.56%) | 9 (14.52%) |
Provenience of Birds | Avian Category | Common Name | Scientific Name | Number of Tested Animals |
---|---|---|---|---|
Recovery center | Raptors | Little owl | Athene noctua | 5 |
Peregrine falcon | Falco peregrinus | 4 | ||
Common kestrel | Falco tinnunculus | 3 | ||
Eurasian buzzard | Buteo buteo | 3 | ||
Long-eared owl | Asio otus | 1 | ||
Barn owl | Tyto alba | 1 | ||
Synanthropic birds | Common wood pigeon | Columba palumbus | 1 | |
Common starling | Sturnus vulgaris | 1 | ||
European robin | Erithacus rubecula | 1 | ||
Song thrush | Turdus philomelos | 2 | ||
Hooded crow | Corvus cornix | 1 | ||
European turtle dove | Streptopelia turtur | 7 | ||
Domestic pigeon | Columba livia | 5 | ||
Aquatic birds | Yellow-legged gull | Larus michahellis | 26 | |
Hunting activity | Aquatic birds | Eurasian teals | Anas crecca | 29 |
Mallard | Anas platyrhynchos | 3 | ||
Shoveler | Spatula clypeata | 8 | ||
Pintail | Anas acuta | 1 | ||
Mandarin duck | Aix galericulata | 1 |
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Cagnoli, G.; Bertelloni, F.; Interrante, P.; Ceccherelli, R.; Marzoni, M.; Ebani, V.V. Antimicrobial-Resistant Enterococcus spp. in Wild Avifauna from Central Italy. Antibiotics 2022, 11, 852. https://doi.org/10.3390/antibiotics11070852
Cagnoli G, Bertelloni F, Interrante P, Ceccherelli R, Marzoni M, Ebani VV. Antimicrobial-Resistant Enterococcus spp. in Wild Avifauna from Central Italy. Antibiotics. 2022; 11(7):852. https://doi.org/10.3390/antibiotics11070852
Chicago/Turabian StyleCagnoli, Giulia, Fabrizio Bertelloni, Paolo Interrante, Renato Ceccherelli, Margherita Marzoni, and Valentina Virginia Ebani. 2022. "Antimicrobial-Resistant Enterococcus spp. in Wild Avifauna from Central Italy" Antibiotics 11, no. 7: 852. https://doi.org/10.3390/antibiotics11070852