Veterinary Research Forum
Vet Res Forum

Occurrence, characteristics, and antibiotic sensitivity of Staphylococcus aureus isolated from wild birds in the Kasur district of Punjab, Pakistan

Document Type : Original Article

Authors

Tooba Latif 1
Shahzad Ali 1
Arshad Javid 2
Ali Ahmad Shaikh 3

1 Wildlife Epidemiology and Molecular Microbiology Laboratory (One Health Research Group), Discipline of Zoology, Department of Wildlife and Ecology, Faculty of Fisheries and Wildlife, University of Veterinary and Animal Sciences, Ravi Campus Pattoki, Lahore, Pakistan

2 Department of Wildlife and Ecology, Faculty of Fisheries and Wildlife, University of Veterinary and Animal Sciences, Ravi Campus Pattoki, Lahore, Pakistan

3 Institute of Microbiology, Faculty of Veterinary Sciences, University of Veterinary and Animal Sciences, Lahore, Pakistan

https://doi.org/10.30466/vrf.2024.2009978.3990
Abstract
Staphylococcus aureus is gaining worldwide attention because of its substantial impact on public health. The current study aimed to characterize S. aureus strains isolated from wild birds in the Kasur district of Punjab, Pakistan from 2021 to 2022. A total of one hundred samples were collected from five wild bird species. The samples were enriched, inoculated on selective agars and cultured for 24 hr at 37.00 ˚C. All isolates were verified by matrix-assisted laser desorption ionization–time-of-flight mass spectrometry (MALDI-TOF MS) and polymerase chain reaction (PCR) after Gram staining. Positive isolates were screened for phenotypic (Kirby-Bauer disk diffusion and minimum inhibitory concentration s), genotypic antibiotic resistance, and virulence genes. These samples yielded 30 (30.00%) S. aureus isolates, confirmed by polymerase chain reaction utilizing the 16S rRNA gene. Staphylococcus aureus was more prevalent in cloacal samples (16.00%) than oral samples (14.00%). Various S. aureus isolates showed varying degrees of resistance to three different antibiotics. Oxacillin (56.66%; n = 17) and tetracycline (33.33%; n = 10) showed the highest resistance rates with the lowest susceptibility (43.33%; n = 13). In contrast, vancomycin, rifampicin, linezolid, and daptomycin were 100% susceptible. Further disc diffusion study revealed resistance to tetracycline (33.33%), erythromycin (16.66%), and gentamicin (10.00%). The tetK gene was found in 33.33% of wild bird samples, while the ermA gene was found in 16.66% of samples. The aacA-D gene was only found in three (10.00%) isolates. None of the isolates tested positive for virulence genes. In conclusion, S. aureus is carried by wild birds in this area, posing a potentail threat to both humans and animals.

Keywords

accA-D
Antibiotic resistance
ermA
Staphylococcus aureus
tetK

Subjects

  1. Whelan CJ, Şekercioğlu ÇH, Wenny DG. Why birds matter: from economic ornithology to ecosystem services. J Ornithol 2015; 156(Suppl 1): 227-238.
  2. Robinson RA, Lawson B, Toms MP, et al. Emerging infectious disease leads to rapid population declines of common British birds. PLoS One 2010; 5(8): e12215. doi: 10.1371/journal.pone.0012215.
  3. Amin MAM, Ali MNM, Awadallah MAI, et al. Prevalence of Enterobacteriaceae in wild birds and humans at Sharkia province; with special reference to the genetic relationship between coli and Salmonella isolates determined by protein profile analysis. J Am Sci 2013; 9(4): 173-183.
  4. Badouei MA, Blackall PJ, Koochakzadeh A, et al. Prevalence and clonal distribution of avian Escherichia coli isolates harboring increased serum survival (iss) gene. J Appl Poult Res 2016; 25(1): 67-73.
  5. Altizer S, Bartel R, Han BA. Animal migration and infectious disease risk.Science 2011; 331(6015): 296-302.
  6. Blyton MD, Pi H, Vangchhia B, 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): 5123-5133.
  7. Gaukler SM, Linz GM, Sherwood JS, et al. Escherichia coli, Salmonella, and Mycobacterium avium subsp. paratuberculosis in wild European starlings at a Kansas cattle feedlot. Avian dis 2009; 53(4): 544-551.
  8. Fogarty LR, Haack SK, Wolcott MJ, et al. Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull feces. J Appl Microbiol 2003; 94(5): 865-878.
  9. Kuroki T, Ishihara T, Furukawa I, et al. Prevalence of Salmonella in wild snakes in Japan. Jpn J Infect Dis 2013; 66(4): 295-298.
  10. Suphoronski SA, de Freitas Raso T, Weinert NC, et al. 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): 1778-1782.
  11. Brugman VA, Horton DL, Phipps LP, et al. Epidemiological perspectives on West Nile virus surveillance in wild birds in Great Britain. Epidemiol Infect 2013; 141(6): 1134-1142.
  12. Foti M, Mascetti A, Fisichella V, et al. Antibiotic resistance assessment in bacteria isolated in migratory Passeriformes transiting through the Metaponto territory (Basilicata, Italy). Avian Res 2017; 8: 26. doi: 10.1186/s40657-017-0085-2.
  13. Gómez P, Lozano C, Camacho MC, et al. Detection of MRSA ST3061-t843-mecC and ST398-to11-mecA in white stork nestlings exposed to human residues. J Antimicrob Chemother 2016; 71(1): 53-57.
  14. França A, Gaio V, Lopes N, et al. Virulence factors in coagulase-negative Staphylococci. Pathogens 2021; 10(2), 170. doi: 10.3390/pathogens10020170.
  15. Chin D, Goncheva MI, Flannagan RS, et al. Coagulase-negative staphylococci release a purine analog that inhibits Staphylococcus aureusNat Commun 2021; 12(1): 1887. doi: 10.1038/s41467-021-22175-3.
  16. Rossi CC, Pereira MF, Giambiagi-deMarval M. Underrated Staphylococcus species and their role in antimicrobial resistance spreading. Genet Mol Biol 2020; 43 (1 suppl 2):e20190065. doi: 10.1590/ 1678-4685-GMB-2019-0065.
  17. Van Boeckel TP, Brower C, Gilbert M, et al. Global trends in antimicrobial use in food animals. Proc Natl Acad Sci USA 2015; 112(18): 5649-5654.
  18. Carroll D, Wang J, Fanning S, et al. Antimicrobial resistance in wildlife: implications for public health. Zoonoses Public Health 2015; 62(7): 534-542.
  19. Atyah MA, Zamri-Saad M, Siti-Zahrah A. First report of methicillin-resistant Staphylococcus aureus from cage-cultured tilapia (Oreochromis niloticus). Vet Microbiol 2010; 144(3-4): 502-504.
  20. Strommenger B, Kettlitz C, Werner G, et al. Multiplex PCR assay for simultaneous detection of nine clinically relevant antibiotic resistance genes in Staphylococcus aureus. J Clin Microbiol 2003; 41(9): 4089-4094.
  21. Johnson WM, Tyler SD, Ewan EP, et al. Detection of genes for enterotoxins, exfoliative toxins, and toxic shock syndrome toxin 1 in Staphylococcus aureus by the polymerase chain reaction. J Clin Microbiol 1991; 29(3): 426-430.
  22. Chaudhary S, Batoo AS, Hussain K, et al. Prevalence of pododermatitis caused by Staphylococcus aureus in poultry birds of Jammu. Int J Livest Res 2018; 8(3): 192-195.
  23. Habib F, Malhi KK, Kamboh AA, et al. Antimicrobial susceptibility profile of Staphylococcus aureus isolates recovered from various animal species. J Anim Health Prod 2015; 3(4): 99-103.
  24. Persoons D, Van Hoorebeke S, Hermans K, et al. Methicillin-resistant Staphylococcus aureus in poultry. Emerg Infect Dis 2009; 15(3): 452-453.
  25. Otalu Jr O, Kabir JJ, Okolocha EC, et al. Detection of methicillin-resistant Staphylococcus aureus in chicken carcasses and live birds in Zaria, Nigeria. FUTA J Res Sci 2015; 11(1): 132-138.
  26. Onaolapo JA, Igwe JC, Bolaji RO, et al. Antibiotics susceptibility profile of Staphylococcus aureus isolated from poultry birds in Kaduna, Nigeria. J Clin Microbiol Antimicrob 2017; 1(1): 1-6.
  27. Bakheet AA, Amen O, Habaty SHAL, et al. Prevalence of Staphylococcus aureus in broiler chickens with special reference to beta-lactam resistance genes in the isolated strains. Alex J Vet Sci 2018; 57(2): 25-33.
  28. Ahmed HA, Awad NFS, Abd El-Hamid MI, et al. Pet birds as potential reservoirs of virulent and antibiotic-resistant zoonotic bacteria. Comp Immunol Microbiol Infect Dis 2021; 75, 101606. doi: 10.1016/ j.cimid.2020.101606.
  29. Szczuka E, Wesołowska M, Krawiec A, et al. Staphylococcal species composition in the skin microbiota of domestic pigeons (Columba livia domestica). PLoS One 2023; 18(7): e0287261. doi:10.1371/journal.pone.0287261.
  30. Silva V, Lopes AF, Soeiro V, et al. Nocturnal birds of prey as carriers of Staphylococcus aureus and other Staphylococci: diversity, antimicrobial resistance and clonal lineages. Antibiotics. 2022; 11(2): 240. doi: 10.3390/antibiotics11020240.
  31. El-Mahallawy HS, Hamza DA, Ahmed ZS. Fecal carriage of aureus and the mecA gene in resident wild birds and its zoonotic potential. J Appl Vet Sci 2022; 7(3): 35-40.
  32. Matias CAR, Pereira IA, Rodrigues DP, et al. Staphylococcus isolated from wild birds apprehended in the local illegal trade in Rio de Janeiro, Brazil, and relevance in public health. Lett Appl Microbiol 2018; 67(3): 292-298.
  33. Hubálek Z. An annotated checklist of pathogenic microorganisms associated with migratory birds. J Wildl Dis 2004; 40(4): 639-659.
  34. Dipineto L, Bossa LM, Pace A, et al. Microbiological survey of birds of prey pellets. Comp Immunol Microbiol Infect Dis. 2015; 41: 49-53.
  35. Ruiz-Ripa L, Gómez P, Alonso CA, et al. Frequency and characterization of antimicrobial resistance and virulence genes of coagulase-negative staphylococci from wild birds in Spain. Detection of tst-carrying sciuri isolates. Microorganisms 2020; 8(9): 1317. doi: 10.3390/microorganisms8091317.
  36. Russo TP, Minichino A, Gargiulo A, et al. Prevalence and phenotypic antimicrobial resistance among ESKAPE bacteria and enterobacterales strains in wild birds. Antibiotics (Basel) 2022; 11(12): 1825. doi: 10.3390/antibiotics11121825.
  37. Ali Y, Islam MA, Muzahid NH, et al. Characterization, prevalence and antibiogram study of Staphylococcus aureus in poultry. Asian Pac J Trop Biomed 2017; 7(3): 253-256.
  38. Bagheri SS, Peighambari SM, Soltani M, et al. RAPD-PCR and drug resistance pattern of Staphylococcus aureus isolates recovered from companion and wild birds. Iran J Appl Anim Sci 2019; 13(4): 356-364.
  39. Thapaliya D, Dalman M, Kadariya J, et al. Characterization of Staphylococcus aureus in goose feces from state Parks in Northeast Ohio. EcoHealth. 2017; 14(2): 303-309.
  40. Marshall B, Ochieng J. Levy S. Commensals: an underappreciated reservoir of antibiotic resistance. Probing the role of commensals in propagating antibiotic resistance should help preserve the efficacy of these critical drugs. Microbe 2009; 4: 231-238.
  41. Ramey AM, Ahlstrom CA. Antibiotic-resistant bacteria in wildlife: perspectives on trends, acquisition and dissemination, data gaps, and future directions. J Wildl Dis 2020; 56(1): 1-15.
  42. Carter DL, Docherty KM, Gill SA, et al. Antibiotic-resistant bacteria are widespread in songbirds across rural and urban environments. Sci Total Environ 2018; 627: 1234-1241.
  43. Wu J, Huang Y, Rao D, et al. Evidence for environmental dissemination of antibiotic resistance mediated by wild birds. Front. Microbiol 2018; 9: Article 745. doi: 10.3389/fmicb.2018.00745.
Veterinary Research Forum
Volume 15, Issue 6
June 2024
Pages 283-290

  • Receive Date 25 August 2023
  • Revise Date 16 December 2023
  • Accept Date 08 January 2024

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