Fecal Carriage of S. aureus and the mecA Gene in Resident Wild Birds and Its Zoonotic Potential

El-Mahallawy, Heba S.; Hamza, Dalia A.; Ahmed, Zeinab S.

doi:10.21608/javs.2022.132870.1143

Fecal Carriage of S. aureus and the mecA Gene in Resident Wild Birds and Its Zoonotic Potential

Document Type : Original Article

Authors

¹ Department of Animal Hygiene, Zoonoses, and Animal Behaviour and Management - Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt.

² Department of Zoonoses, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt.

10.21608/javs.2022.132870.1143

Abstract

Resistant Staphylococcus (S.) aureus in general and MRSA, in particular, have received great attention in both veterinary and human health sectors. The importance of fecal carriage of staphylococci is rarely encountered. This study aimed to investigate the role of wild birds in Giza governorate, Egypt in spreading resistant S. aureus from winter 2019 to summer 2021. Cloacal swabs and fecal droppings were collected from different species of wild birds (rock pigeons, laughing doves, cattle egrets, and hooded crows). Isolation and identification of Staphylococcus spp. were performed using Columbia agar base with 5% defibrinated sheep blood and mannitol salt agar. Moreover, molecular detection of the coa, nuc, and mecA genes has been investigated via the polymerase chain reaction (PCR) assay. Out of 166 fecal samples examined, staphylococci had been confirmed in 100 samples (60.2%), with S. aureus representing 70% of the obtained staphylococci; however, non-aureus staphylococci represented the remaining 30% of the isolates. The mecA gene carriage was (57.1%) in S. aureus. This study highlighted the zoonotic potential of staphylococci isolated from resident wild birds in Giza, Egypt. Presences of such pathogenic microorganisms with their resistance traits around and in the human habitat add to the microbial community present around human dwellings in the study area. They may play a role in the spreading of various illnesses.

Keywords

Main Subjects

public health and preventive medicine

References

ABDULLAHI, I. N., FERNÁNDEZ-FERNÁNDEZ, R., JUÁREZ-FERNÁNDEZ, G., MARTÍNEZ-ÁLVAREZ, S., EGUIZÁBAL, P., ZARAZAGA, M., LOZANO, C., and TORRES, C., 2021. Wild Animals Are Reservoirs and Sentinels of Staphylococcus aureus and MRSA Clones: A Problem with “One Health” Concern. Antibiotics 10(12):1556.

DOI: https://doi.org/10.3390/antibiotics10121556.

AHMED, Z. S., ELSHAFIEE, E. A., KHALEFA, H. S., KADRY, M., and HAMZA, D. A., 2019. Evidence of colistin resistance genes (mcr-1 and mcr-2) in wild birds and its public health implication in Egypt. Antimicrob Resist Infect Control 8: 197. DOI: https://doi.org/10.1186/s13756-019-0657-5.

AL-AMERY, K., ELHARIRI, M., ELSAYED, A., EL-MOGHAZY, G., ELHELW, R., EL-MAHALLAWY, H., EL HARIRI, M., and HAMZA, D., 2019. Vancomycin-resistant Staphylococcus aureus isolated from camel meat and slaughterhouse workers in Egypt. Antimicrob Resist Infect Control 8: 129. DOI: https://doi.org/10.1186/s13756-019-0585-4.

BECKER, K., HEILMANN, C., and PETERS, G., 2014. Coagulase-negative staphylococci. Clinical Microbiology Reviews 27(4): 870-926. DOI: https://doi.org/10.1128/CMR.00109-13.

BENSKIN, C. M. H., WILSON, K., JONES, K., AND HARTLEY, I. R., 2009. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biological Reviews 84(3): 349-373. DOI: https://doi.org/10.1111/j.1469-185X.2008.00076.x.

CHEN, M. M., BOARDMAN, W. S., and BROWN, M. H., 2016. Methicillin resistance gene diversity in staphylococci isolated from captive and free-ranging wallabies. Infection Ecology & Epidemiology 6(1): 31507. DOI: https://doi.org/10.3402/iee.v6.31507.

CLSI, 2020. performance standards for antimicrobial susceptibility testing. 30th ed. CLSI supplement M100.

CONTRERAS-RODRÍGUEZ, A., AGUILERA-ARREOLA, M. G., OSORIO, A. R., MARTIN, M. D., GUZMÁN, R. L., VELARDE, E., and RUIZ, E. A., 2019. Detection of potential human pathogenic bacteria isolated from feces of two colonial seabirds nesting on Isla Rasa, Gulf of California: Heermann’s gull (Larus heermanni) and elegant tern (Thalasseus elegans). Tropical Conservation Science 12: 1940082919855673.

DOI: https://doi.org/10.1177/1940082919855673.

DWEBA, C. C., ZISHIRI, O. T., and EL ZOWALATY, M. E., 2019. Isolation and molecular identification of virulence, antimicrobial and heavy metal resistance genes in livestock-associated methicillin-resistant Staphylococcus aureus. Pathogens 8(2): 79. DOI: https://doi.org/10.3390/pathogens8020079.

EL TAWEEL, A., KANDEIL, A., BARAKAT, A., ALFAROQ RABIEE, O., KAYALI, G., and ALI, M. A., 2020. Diversity of Astroviruses Circulating in Humans, Bats, and Wild Birds in Egypt. Viruses 12(5): 485. DOI: https://doi.org/10.3390/v12050485.

GAJDÁCS, M., and ZSOLDINÉ URBÁN, E., 2019. Epidemiology and resistance trends of Staphylococcus aureus isolated from vaginal samples: a 10-year retrospective study in Hungary. Acta Dermatovenerologica Alpina, Pannonica et Adriatica 28(4): 143-147.

DOI: https://doi.org/10.15570/actaapa.2019.35.

GONZÁLEZ-MARTÍN, M., CORBERA, J. A., SUÁREZ-BONNET, A., and TEJEDOR-JUNCO, M. T., 2020. Virulence factors in coagulase-positive staphylococci of veterinary interest other than Staphylococcus aureus. Veterinary Quarterly 40(1): 118-131.

DOI: https://doi.org/10.1080/01652176.2020.1748253.

HOOKEY, J. V., RICHARDSON, J. F., and COOKSON, B. D., 1998. Molecular typing of Staphylococcus aureus based on PCR restriction fragment length polymorphism and DNA sequence analysis of the coagulase gene. Journal of Clinical Microbiology 36(4): 1083-1089.

DOI:https://doi.org/10.1128/JCM.36.4.1083-1089.1998.

HUBÁLEK, Z. 2004. An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases 40(4): 639-659. DOI: https://doi.org/10.7589/0090-3558-40.4.639.

KLOOS, W. E., and BANNERMAN, T. L., 1994. Update on clinical significance of coagulase-negative staphylococci. Clinical Microbiology Reviews 7(1): 117-140. DOI: https://doi.org/10.1128/CMR.7.1.117.

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(24): 8126-8134. DOI: https://doi.org/10.1128/AEM.01446-10.

MATIAS, C., PEREIRA, I., RODRIGUES, D. P., and SICILIANO, S., 2018. Staphylococcus spp. isolated from wild birds apprehended in the local illegal trade in Rio de Janeiro, Brazil, and relevance in public health. Letters in Applied Microbiology 67(3): 292-298. DOI: https://doi.org/10.1111/lam.13035.

MONECKE, S., GAVIER-WIDÉN, D., HOTZEL, H., PETERS, M., GUENTHER, S., LAZARIS, A., LONCARIC, I., MÜLLER, E., REISSIG, A., and RUPPELT-LORZ, A., 2016. Diversity of Staphylococcus aureus isolates in European wildlife. PloS One 11(12): e0168433.

DOI: https://doi.org/10.1371/journal.pone.0168433.

NABIL, N. M., ERFAN, A. M., TAWAKOL, M. M., HAGGAG, N. M., NAGUIB, M. M., and SAMY, A., 2020. Wild Birds in Live Birds Markets: Potential Reservoirs of Enzootic Avian Influenza Viruses and Antimicrobial Resistant Enterobacteriaceae in Northern Egypt. Pathogens 9(3). DOI: https://doi.org/10.3390/pathogens9030196.

PETZER, I.-M., KARZIS, J., LESOSKY, M., WATERMEYER, J. C., and BADENHORST, R., 2013. Host adapted intramammary infections in pregnant heifers which were co-housed and reared on fresh milk as calves. BMC Veterinary Research 9(1): 1-6. DOI: https://doi.org/10.1186/1746-6148-9-49.

POURNARAS, S., J SABAT, A., GRUNDMANN, H., HENDRIX, R., TSAKRIS, A., and W FRIEDRICH, A., 2015. Driving forces of mechanisms regulating oxacillin-resistance phenotypes of MRSA: truly oxacillin-susceptible mecA-positive Staphylococcus aureus clinical isolates also exist. Current Pharmaceutical Design 21(16): 2048-2053. DOI: https://doi.org/10.2174/1381612821666150310103754.

QUINN, P. J., MARKEY, B. K., LEONARD, F. C., HARTIGAN, P., FANNING, S., and FITZPATRICK, E., 2011. Veterinary microbiology and microbial disease, John Wiley & Sons.

ROUSHAM, E. K., UNICOMB, L., and ISLAM, M. A., 2018. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioural, epidemiological and One Health approaches. Proceedings of the Royal Society B: Biological Sciences 285(1876): 20180332. DOI: https://doi.org/10.1098/rspb.2018.0332.

SHRESTHA, N. K., TUOHY, M. J., HALL, G. S., ISADA, C. M., and PROCOP, G. W., 2002. Rapid identification of Staphylococcus aureus and the mecA gene from BacT/ALERT blood culture bottles by using the LightCycler system. Journal of Clinical Microbiology 40(7): 2659-2661.

DOI: https://doi.org/10.1128/JCM.40.7.2659-2661.2002.

SILVEIRA, D. R., DE MORAES, T. P., KAEFER, K., BACH, L. G., DE OLIVEIRA BARBOSA, A., MORETTI, V. D., DE MENEZES, P. Q., DE MEDEIROS, U. S., DA SILVA, T. T., and BANDARRA, P. M., 2021. MRSA and enterobacteria of one health concern in wild animals undergoing rehabilitation. Research, Society and Development 10(1): e34810111809-e34810111809. DOI: https://doi.org/10.33448/rsd-v10i1.11809.

VAN HAL, S. J., JENSEN, S. O., VASKA, V. L., ESPEDIDO, B. A., PATERSON, D. L., and GOSBELL, I. B., 2012. Predictors of mortality in Staphylococcus aureus bacteremia. Clinical Microbiology Reviews 25(2): 362-386. DOI: https://doi.org/10.1128/CMR.05022-11.

WANG, J., MA, Z.-B., ZENG, Z.-L., YANG, X.-W., HUANG, Y., and LIU, J.-H., 2017. The role of wildlife (wild birds) in the global transmission of antimicrobial resistance genes. Zoological Research 38(2): 55. DOI: https://doi.org/10.24272/j.issn.2095-8137.2017.024.

WHO, 2020. World Health Organization Antibiotic Resistance. Geneva, Switzerland. Available online: https://www.who.int/news-room/fact-sheets/detail/antibiotic-resistance (accessed on 17 December 2021)

ZHANG, K., MCCLURE, J.-A., ELSAYED, S., LOUIE, T., and CONLY, J. M., 2005. Novel multiplex PCR assay for characterization and concomitant subtyping of staphylococcal cassette chromosome mec types I to V in methicillin-resistant Staphylococcus aureus. Journal of Clinical Microbiology 43(10): 5026-5033. DOI: https://doi.org/10.1128/JCM.43.10.5026-5033.2005.