Presence of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli and Klebsiella pneumoniae Isolated from Avian Species in a Petting Zoological Garden
Abstract
1. Introduction
2. Materials and Methods
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Hrnková, J.; Schneiderová, I.; Golovchenko, M.; Grubhoffer, L.; Rudenko, N.; Černý, J. Role of zoo-housed animals in the ecology of ticks and tick-borne pathogens—A review. Pathogens 2021, 10, 210. [Google Scholar] [CrossRef] [PubMed]
- Göttling, J.; Heckel, J.O.; Hotzel, H.; Fruth, A.; Pfeifer, Y.; Henning, K.; Pfeffer, M. Zoonotic bacteria in clinically healthy goats in petting zoo settings of zoological gardens in Germany. Zoonoses Public Health 2022, 69, 333–343. [Google Scholar] [CrossRef] [PubMed]
- Potter, R.F.; D’Souza, A.W.; Dantas, G. The rapid spread of carbapenem-resistant Enterobacteriaceae. Drug Resist. Updat. 2016, 29, 30–46. [Google Scholar] [CrossRef]
- Salleh, M.Z.; Nik Zuraina, N.M.N.; Hajissa, K.; Ilias, M.I.; Banga Singh, K.K.; Deris, Z.Z. Prevalence of multidrug-resistant and extended-spectrum beta-lactamase-producing Shigella Species in Asia: A systematic review and meta-analysis. Antibiotics 2022, 11, 1653. [Google Scholar] [CrossRef]
- Parmanik, A.; Das, S.; Kar, B.; Bose, A.; Dwivedi, G.R.; Pandey, M.M. Current treatment strategies against multidrug-resistant bacteria: A review. Curr. Microbiol. 2022, 79, 388. [Google Scholar] [CrossRef]
- De Witte, C.; Vereecke, N.; Theuns, S.; De Ruyck, C.; Vercammen, F.; Bouts, T.; Haesebrouck, F. Presence of broad-spectrum beta-lactamase-producing Enterobacteriaceae in zoo mammals. Microorganisms 2021, 9, 834. [Google Scholar] [CrossRef]
- Isler, M.; Wissmann, R.; Morach, M.; Zurfluh, K.; Stephan, R.; Nüesch-Inderbinen, M. Animal petting zoos as sources of Shiga toxin-producing Escherichia coli, Salmonella and extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae. Zoonoses Public Health 2021, 68, 79–87. [Google Scholar] [CrossRef]
- Wang, X.; Zhang, Y.; Li, C.; Li, G.; Wu, D.; Li, T.; Zou, L. Antimicrobial resistance of Escherichia coli, Enterobacter spp., Klebsiella pneumoniae and Enterococcus spp. isolated from the feces of giant panda. BMC Microbiol. 2022, 22, 102. [Google Scholar] [CrossRef] [PubMed]
- Min, J.; Kim, P.; Yun, S.; Hong, M.; Park, W. Zoo animal manure as an overlooked reservoir of antibiotic resistance genes and multidrug-resistant bacteria. Environ. Sci. Pollut. Res. 2023, 30, 710–726. [Google Scholar] [CrossRef] [PubMed]
- Ramos, C.A.; Ferreira, J.C.; Ballaben, A.S.; Penha Filho, R.A.C.; da Costa Darini, A.L. Analysis of antibiotic resistance in Gram-negative bacilli in wild and exotic healthy birds in Brazil: A warning sign. Vet. Microbiol. 2024, 296, 110196. [Google Scholar] [CrossRef]
- Kim, J.; Kwon, Y.; Pai, H.; Kim, J.W.; Cho, D.T. Survey of Klebsiella pneumoniae strains producing extended-spectrum beta-lactamases: Prevalence of SHV-12 and SHV-2a in Korea. J. Clin. Microbiol. 1998, 36, 1446–1449. [Google Scholar] [CrossRef]
- Marques, A.R.; Pascoal-Filho, N.M.; Teixeira, R.S.; Silva, I.N.; Melo, L.S.; Lima, B.P.; Maciel, W.C. Investigation of enterobacteria with zoonotic and multi-resistant potential in exotic parrots kept in a domestic environment. Pesq. Vet. Bras. 2024, 44, e07387. [Google Scholar] [CrossRef]
- Sem, Y.F.; Abu, J.; Abdul-Aziz, S. Occurrence of antibiotic-resistant Escherichia coli and Salmonella spp. in psittacine birds in selected petting zoos in Klang Valley, Malaysia. J. Vet. Malays. 2024, 36, 7–12. [Google Scholar] [CrossRef]
- Šmíd, J. Geographic and taxonomic biases in the vertebrate tree of life. J. Biogeogr. 2022, 49, 2120–2129. [Google Scholar] [CrossRef]
- Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. In CLSI VET01S, 6th ed.; CLSI Supplement VET01S; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2023; ISBN 978–1–68440-167-3. [Google Scholar]
- 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]
- Edelstein, M.; Pimkin, M.; Palagin, I.; Edelstein, I.; Stratchounski, L. Prevalence and molecular epidemiology of CTX-M extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Russian hospitals. Antimicrob. Agents Chemother. 2003, 47, 3724–3732. [Google Scholar] [CrossRef] [PubMed]
- Essack, S.Y.; Hall, L.M.; Pillay, D.G.; McFadyen, M.L.; Livermore, D.M. Complexity and diversity of Klebsiella pneumoniae strains with extended-spectrum beta-lactamases isolated in 1994 and 1996 at a teaching hospital in Durban, South Africa. Antimicrob. Agents Chemother. 2001, 45, 88–95. [Google Scholar] [CrossRef] [PubMed]
- 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]
- Bartoloni, A.; Pallecchi, L.; Riccobono, E.; Mantella, A.; Magnelli, D.; Di Maggio, T.; Villagran, A.L.; Yara, L.; Saavedra, C.; Strohmayer, M.; et al. Relentless increase of resistance to fluoroquinolones and expanded-spectrum cephalosporins in Escherichia coli: 20 years of surveillance in resource-limited settings from Latin America. Clin. Microbiol. Infect. 2013, 19, 356–361. [Google Scholar] [CrossRef]
- Russo, T.P.; Minichino, A.; Gargiulo, A.; Varriale, L.; Borrelli, L.; Pace, A.; Dipineto, L. Prevalence and phenotypic antimicrobial resistance among ESKAPE bacteria and Enterobacterales strains in wild birds. Antibiotics 2022, 11, 1825. [Google Scholar] [CrossRef]
- Saladin, M.; Cao, V.T.; Lambert, T.; Donay, J.L.; Herrmann, J.L.; Ould-Hocine, Z.; Verdet, C.; Delisle, F.; Philippon, A.; Arlet, G. Diversity of CTX-M betalactamases and their promoter regions from Enterobacteriaceae isolated in three Parisian hospitals. FEMS Microbiol. Lett. 2002, 209, 161–168. [Google Scholar] [CrossRef]
- Rehman, M.A.; Hasted, T.L.; Persaud-Lachhman, M.G.; Yin, X.; Carrillo, C.; Diarra, M.S. Genome analysis and multiplex PCR method for the molecular detection of Coresistance to Cephalosporins and Fosfomycin in salmonella enterica Serovar Heidelberg. J. Food Prot. 2019, 82, 1938–1949. [Google Scholar] [CrossRef]
- Judge, A.; Hu, L.; Sankaran, B.; Van Riper, J.; Venkataram Prasad, B.V.; Palzkill, T. Mapping the determinants of catalysis and substrate specificity of the antibiotic resistance enzyme CTX-M β-lactamase. Commun. Biol. 2023, 6, 35. [Google Scholar] [CrossRef]
- Al Noman, Z.; Tasnim, S.; Masud, R.I.; Anika, T.T.; Islam, M.S.; Rahman, M.T. A systematic review on reverse-zoonosis: Global impact and changes in transmission patterns. J. Adv. Vet. 2024, 11, 601. [Google Scholar] [CrossRef]
- Esposito, M.M.; Turku, S.; Lehrfield, L.; Shoman, A. The impact of human activities on zoonotic infection transmissions. Animals 2023, 13, 1646. [Google Scholar] [CrossRef]
- Siegrist, A.A.; Richardson, K.L.; Ghai, R.R.; Pope, B.; Yeadon, J.; Culp, B.; Boyer, L.V. Probable transmission of SARS-CoV-2 from African lion to zoo employees, Indiana, USA, 2021. Emerg. Infect. Dis. 2023, 29, 1102. [Google Scholar] [CrossRef] [PubMed]
- Tuhamize, B.; Bazira, J. Carbapenem-resistant Enterobacteriaceae in the livestock, humans and environmental samples around the globe: A systematic review and meta-analysis. Sci. Rep. 2024, 14, 16333. [Google Scholar] [CrossRef]
- Parker, D.; Sniatynski, M.K.; Mandrusiak, D.; Rubin, J.E. Extended-spectrum β-lactamase producing Escherichia coli isolated from wild birds in Saskatoon, Canada. Lett. Appl. Microbiol. 2016, 63, 11–15. [Google Scholar] [CrossRef]
- Kim, M.; Kim, M.; Yeo, Y.G.; Lee, Y.T.; Han, J.I. Antimicrobial resistance of commensal Escherichia coli and Enterococcus faecalis isolated from clinically healthy captive wild animals in Seoul zoo. Front. Vet. Sci. 2024, 10, 1283487. [Google Scholar] [CrossRef]
- Clemente, L.; Leão, C.; Moura, L.; Albuquerque, T.; Amaro, A. Prevalence and characterization of ESBL/AmpC producing Escherichia coli from fresh meat in Portugal. Antibiotics 2021, 10, 1333. [Google Scholar] [CrossRef] [PubMed]
- Dobiasova, H.; Dolejska, M.; Jamborova, I.; Brhelova, E.; Blazkova, L.; Papousek, I.; Literak, I. Extended spectrum beta-lactamase and fluoroquinolone resistance genes and plasmids among Escherichia coli isolates from zoo animals, Czech Republic. FEMS Microbiol. Ecol. 2013, 85, 604–611. [Google Scholar] [CrossRef]
- Husna, A.; Rahman, M.M.; Badruzzaman, A.T.M.; Sikder, M.H.; Islam, M.R.; Rahman, M.T.; Ashour, H.M. Extended-spectrum β-lactamases (ESBL): Challenges and opportunities. Biomedicines 2023, 11, 2937. [Google Scholar] [CrossRef] [PubMed]
- Martin, R.M.; Bachman, M. AColonization, infection, and the accessory genome of Klebsiella pneumoniae. Front. Cell Infect. Microbiol. 2018, 8, 4. [Google Scholar] [CrossRef] [PubMed]
- Fowler, M.E. An overview of wildlife husbandry and diseases in captivity. Rev. Sci. Tech. 1996, 15, 15–42. [Google Scholar] [CrossRef]
- Donkor, E.S. Cockroaches and food-borne pathogens. Environ. Health Insights 2020, 14, 1178630220913365. [Google Scholar] [CrossRef]
- Li, Y.; Li, D.; Liang, Y.; Cui, J.; He, K.; He, D.; Yuan, L. Characterization of a tigecycline-resistant and bla CTX-M-bearing Klebsiella pneumoniae strain from a peacock in a Chinese Zoo. Appl. Environ. Microbiol. 2023, 89, e01764-22. [Google Scholar] [CrossRef] [PubMed]
Order | Common Name | Scientific Name | Birds Sampled “n” |
---|---|---|---|
Falconiformes | Karakara | Caracara cheriway | 1 |
Galliformes | Peafowl | Pavo cristatus | 5 |
Guineafowl | Numida meleagris | 2 | |
Chachalacas | Ortalis vetula | 4 | |
Psittaciformes | Yellow-headed amazon | Amazona oratrix | 1 |
White-fronted amazon | Amazona albifrons | 5 | |
Red-lored amazon | Amazona autumnalis | 5 | |
Military macaw | Ara militaris | 4 | |
Piciformes | Keel-billed toucan | Ramphastos sulfuratus | 1 |
Anseriformes | Domestic duck | Anas platyrhynchos domesticus | 4 |
Greylag goose | Anser anser | 2 | |
Total | 34 |
Antimicrobials Class | Target Gene | Primer Sequence (5′ → 3′) | Product Size (bp) | Reference |
---|---|---|---|---|
TAGTTGTTTCTGGATTAGAGCCT | ||||
β-Lactams | blaTEM | ATGAGTATTCAACATTTCCGTG | 840 | [16] |
TTACCAATGCTTAATCAGTGAG | ||||
blaSHV | TGGTTATGCGTTATATTCGCC | 1051 | [11] | |
GCTTAGCGTTGCCAGTGCT | ||||
blaCTX-M | TTTGCGATGTGCAGTACCAGTAA | 544 | [17] | |
CGATATCGTTGGTGGTGCCATA | ||||
blaCTX-M-1 | ATGGTTAAAAAATCACTG C | 900 | [18] | |
GGTGACGATTTTAGCCGC | ||||
blaCTX-M-9 | GATTGACCGTATTGGGAGTTT | 831 | [18] | |
CGGCTGGGTAAAATAGGTCA |
Avian Species | Isolate | ESBL Phenotypes | Antibiotic Resistance Patterns Based on MIC Results | bla Gene |
---|---|---|---|---|
Peafowl | E. coli | + | Resistance (R): AMP, AZT, CFZ, FEP, CTX, CRO, CIP, LFX, GEN, TOB, TZP. Intermediate (I): SAM, TET. Sensible: AMK, CFX, CZA, NIT, ETP, IPM, MPM, TGC, TMP-SMX. | blaCTX-M-1, blaTEM |
Peafowl | E. coli | + | Resistance (R): AMP, AZT, CFZ, FEP, CTX, CRO, CIP, LFX, GEN, TOB, TET. Intermediate (I): SAM, NIT. Sensible (S): AMK, CFX, CZA, NIT, ETP, IPM, MPM, TGC, TMP-SMX. | blaCTX-M-1, blaTEM, blaSHV |
Peafowl | E. coli | + | Resistance (R): SAM, AMP, AZT, CFZ, FEP, CTX, CRO, CIP, LFX, GEN, TOB, TMP-SMX. Intermediate (I): TET Sensible (S): AMK, CFX, CZA, ETP, IPM, MPM, TZP, NIT, TGC. | blaCTX-M-1, blaTEM |
Peafowl | E. coli K. pneumoniae | + + | Resistance (R): AMP, AZT, CFZ, FEP, CTX, CIP, LFX, GEN, TOB, NIT. Intermediate (I): SAM, CRO. Sensible (S): AMK, CFX, CZA, ETP, IPM, MPM, TZP, TET, TGC, TMP-SMX. Resistance (R): AMP, AZT, CFZ, FEP, CFX, CTX, CRO. Intermediate (I): TET Sensible (S): AMK, GEN, TOB, SAM, CZA, CIP, LFX, ETP, IPM, MPM, TZP, NIT, TGC, TMP-SMX. | blaCTX-M-1, blaTEM blaCTX-M-1, |
Guineafowl | E. coli | + | Resistance (R): AMP, AZT, CFZ, FEP, CTX, CRO, CIP, LFX, GEN, TOB, TZP. Intermediate (I): SAM. Sensible (S): AMK, CFX, CZA, ETP, IPM, MPM, NIT, TET, TGC, TMP-SMX. | blaCTX-M-1, blaTEM, |
Guineafowl | E. coli | + | Resistance (R): AMP, AZT, CFZ, FEP, CTX, CIP, GEN, TOB. Intermediate (I): LFX. Sensible (S): AMK, SAM, CFX, CZA, CRO, ETP, IPM, MPM, TZP, NIT, TET, TGC, TMP-SMX. | blaCTX-M-1, blaTEM, |
Karakara | E. coli | - | Resistance (R): AMP, SAM, AZT, CZA, TZP, TET, TMP-SMX. Intermediate (I): IPM. Sensible (S): AMK, GEN, TOB, FEP, CTX, CRO, CFZ, CFX, CIP, LFX, ETP, MPM, TGC, NIT. | blaCTX-M-1, |
Chachalacas | E. coli | - | Resistance (R): AZT, CZA, TZP, TET, TMP-SMX. Sensible (S): AMP, SAM, AMK, GEN, TOB, FEP, CTX, CRO, CFZ, CFX, CIP, LFX, ETP, IPM, MPM, TGC, NIT. | blaCTX-M-1, blaTEM, |
Red-lored amazon | E. coli | - | Intermediate (I): AMK, CTX, LFX Sensible (S): GEN, SAM, AMP, AZT, CFZ, FEP, CFX, CIP, CZA, CRO, ETP, IPM, MPM, TZP, TET, TGC, TOB, TMP-SMX, NIT. | blaCTX-M-1, blaTEM, |
Red-lored amazon | E. coli | - | Intermediate (I): AMK, CTX, LFX Sensible (S): GEN, SAM, AMP, AZT, CFZ, FEP, CFX, CIP, CZA, CRO, ETP, IPM, MPM, TZP, TET, TGC, TOB, TMP-SMX, NIT | blaCTX-M-1, blaTEM, |
Red-lored amazon | E. coli | Intermediate (I): AMK, CTX, LFX Sensible (S): GEN, SAM, AMP, AZT, CFZ, FEP, CFX, CIP, CZA, CRO, ETP, IPM, MPM, TZP, TET, TGC, TOB, TMP-SMX, NIT | blaCTX-M-1, blaTEM, | |
Keel-billed toucan | E. coli | - | Resistance (R): AMP, SAM, TET, TMP-SMX. Sensible (S): AMK, CTX, LFX, GEN, AZT, CFZ, FEP, CFX, CIP, CZA, CRO, ETP, IPM, MPM, TZP, TGC, TOB, NIT. | blaCTX-M-1, blaTEM, |
Domestic duck (1) | E. coli | - | Resistance (R): AMK, GEN, TOB, AMP, SAM, AZT, CFZ, FEP, CTX, CZA, CRO, CIP, LFX, TET, NIT, TMP-SMX Sensible (S): CFX, ETP, IPM, MPM, TZP, TGC. | blaCTX-M-1, |
Domestic duck (2) | E. coli | - | Resistance (R): AMK, GEN, CRO, LFX, TET, TMP-SMX. Intermediate (I): CFX, ETP. Sensible: AMP, SAM, AZT, CFZ, FEP, CZA, CIP, IPM, MPM, TZP, TGC, TOB. | blaCTX-M-1 |
Domestic duck (3) | E. coli | - | Resistance (R): AMP, SAM, TET, TMP-SMX. Intermediate (I): LFX, TOB. Sensible (S): AMK, GEN, CFZ, FEP, CFX, CZA, CRO, TZP, ETP, IPM, MPM, CIP, TGC. | blaCTX-M-1, blaTEM, |
Greylag goose (1) | E. coli | - | Resistance (R): AMK, AMP, SAM, AZT, CRO, TET, TMP-SMX Intermediate (I): FEP, CFX. Sensible (S): AMK, GEN. TOB, CFZ, CZA, CRO, ETP, IPM, MPM, TZP, TGC, CIP, LFX. | blaCTX-M-1 |
Greylag goose (2) | E. coli | - | Resistance (R): AMK, TOB, AMP, AZT, CTX, CZA, ETP, TET, TMP-SMX. Intermediate (I): LFX Sensible (S): AMK, GEN, SAM, CFZ, FEP, CFX, CRO, CIP, IPM, MPM, TZP, TGC, CIP. | blaCTX-M-1, blaTEM, |
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Casas-Paul, J.; Bravo-Ramos, J.L.; Sánchez-Otero, M.G.; Sánchez-Montes, S.; Bonilla-Rojas, S.; Ortíz-Carbajal, L.A.; Ballados-González, G.G.; Gamboa-Prieto, J.; Chong-Guzmán, A.; Olivares Muñoz, A. Presence of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli and Klebsiella pneumoniae Isolated from Avian Species in a Petting Zoological Garden. J. Zool. Bot. Gard. 2025, 6, 42. https://doi.org/10.3390/jzbg6030042
Casas-Paul J, Bravo-Ramos JL, Sánchez-Otero MG, Sánchez-Montes S, Bonilla-Rojas S, Ortíz-Carbajal LA, Ballados-González GG, Gamboa-Prieto J, Chong-Guzmán A, Olivares Muñoz A. Presence of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli and Klebsiella pneumoniae Isolated from Avian Species in a Petting Zoological Garden. Journal of Zoological and Botanical Gardens. 2025; 6(3):42. https://doi.org/10.3390/jzbg6030042
Chicago/Turabian StyleCasas-Paul, Juan, José Luis Bravo-Ramos, María Guadalupe Sánchez-Otero, Sokani Sánchez-Montes, Sashenka Bonilla-Rojas, Luis Arturo Ortíz-Carbajal, Gerardo Gabriel Ballados-González, Jannete Gamboa-Prieto, Alejandra Chong-Guzmán, and Angelica Olivares Muñoz. 2025. "Presence of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli and Klebsiella pneumoniae Isolated from Avian Species in a Petting Zoological Garden" Journal of Zoological and Botanical Gardens 6, no. 3: 42. https://doi.org/10.3390/jzbg6030042
APA StyleCasas-Paul, J., Bravo-Ramos, J. L., Sánchez-Otero, M. G., Sánchez-Montes, S., Bonilla-Rojas, S., Ortíz-Carbajal, L. A., Ballados-González, G. G., Gamboa-Prieto, J., Chong-Guzmán, A., & Olivares Muñoz, A. (2025). Presence of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli and Klebsiella pneumoniae Isolated from Avian Species in a Petting Zoological Garden. Journal of Zoological and Botanical Gardens, 6(3), 42. https://doi.org/10.3390/jzbg6030042