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Microarray-based detection of resistance genes in coagulase-negative staphylococci isolated from cattle and buffalo with mastitis in Egypt

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Abstract

The present study aimed to provide a detailed characterization of coagulase-negative staphylococci (CoNS) isolated from cows and buffaloes with mastitis. The study included seventy-five CoNS isolates (60 came from cattle and 15 from buffaloes) originating from 68 individual quarters of 67 dairy cows (53 cattle and 14 buffaloes). The animals belonged to five different small holding dairy herds (n = 140 cows) that show clinical or subclinical mastitis. CoNS isolates were phenotypically characterized using MALDI-TOF-MS and were further genotypically characterized by microarray-based assays. Furthermore, the antimicrobial susceptibility of CoNS strains which carried the mecA gene was examined by broth microdilution. The occurrence of CoNS in the respective five herds was 10.5%, 14.7%, 14.8%, 12.8%, and 9.9%, with an average of 12.4%. Six different CoNS species were identified: S. sciuri (n = 37; 30 from cattle and 7 from buffaloes), S. chromogenes (n = 14; 8 from cattle and 6 from buffaloes), S. haemolyticus (n = 10; nine from cattle and one buffalo), S. xylosus (n = 10; nine from cattle and one buffalo), S. hyicus (n = 2), S. warneri (n = 1), and unidentified CoNS (n = 1). Twenty percent (20%) of CoNS isolates (17.3% of cattle origin) carried at least one antimicrobial resistance gene, while 4% of the isolate including two isolates of S. haemolyticus and one S. warneri of cattle origin carried the mecA gene and were phenotypically identified as methicillin-resistant strains. The genes detected were blaZ (16%), followed by tet(K) (8%), aacA-aphD (4%), aphA3 (2.6%), msr(A) (2.6%), [far1 (2.6%), and fusC (2.6%)], sat (2.6%), and cat (1.3%) conferring resistance to penicillin, tetracycline, gentamicin, neomycin/kanamycin, erythromycin, fusidic acid, streptothricin, and chloramphenicol, respectively. The majority of investigated CoNS strains displayed considerably low prevalence of resistance genes, while resistance to more than three antibiotics was found in S. haemolyticus and S. warneri. Implementing effective preventive measures is, therefore, important for limiting the transmission of CoNS, rather than using antibiotics to control mastitis in bovines.

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References

  • Bhutia, P. S., Bansal, B. K., Gupta, D. K., Singh, R. S., & Uppal, S. K., 2019. Bacterial isolation of milk samples submitted from clinical mastitis buffaloes during 2007 to 2016. Tropical Animal Health and Production, 51, 1551-1557.

    Article  CAS  Google Scholar 

  • Bianchi, R. M., Schwertz, C. I., de Cecco, B. S., Panziera, W., De Lorenzo, C., Heck, L. C., ... & Driemeier, D., 2019. Pathological and microbiological characterization of mastitis in dairy cows. Tropical Animal Health and Production, 51, 2057-2066.

  • Clinical and Laboratory Standards Institute (CLSI), 2018. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that grow Aerobically, 11th Edition.

  • Dolder, C., van den Borne, P., Traversari, J., Thomann, A., Perreten, V., and Bodmer, M., 2017. Quarter-and cow-level risk factors for intramammary infection with coagulase-negative staphylococci species in Swiss dairy cows. Journal of Dairy Science, 100, 5653-5663.

    Article  CAS  Google Scholar 

  • El-Ashker, M., Gwida, M., Tomaso, H., Monecke, S., Ehricht, R., El-Gohary, F., and Hotzel, H., 2015. Staphylococci in cattle and buffaloes with mastitis in Dakahlia Governorate, Egypt. Journal of Dairy Science, 98, 7450–7459. https://doi.org/10.3168/jds.2015-9432.

    Article  CAS  Google Scholar 

  • El-Ashker, M., Gwida, M., Monecke, S., El-Gohary, F., Ehricht, R., Elsayed, M., ... and Maurischat, S., 2020. Antimicrobial resistance pattern and virulence profile of S. aureus isolated from household cattle and buffalo with mastitis in Egypt. Veterinary Microbiology, 108535.

  • El-Jakee, J., Aref, N., Gomaa, A., El-Hariri, M., Galal, H., Omar, S., and Samir, A., 2013. Emerging of coagulase negative staphylococci as a cause of mastitis in dairy animals: An environmental hazard. International Journal of Veterinary Science and Medicine, 1, 74-78.

    Article  Google Scholar 

  • El-Razik, K., Arafa, A., Hedia, R., and Ibrahim, E., 2017. Tetracycline resistance phenotypes and genotypes of coagulase-negative staphylococcal isolates from bubaline mastitis in Egypt. Veterinary World, 10, 702.

    Article  PubMed Central  Google Scholar 

  • Frey, Y., Rodriguez, J. P., Thomann, A., Schwendener, S., and Perreten, V., 2013. Genetic characterization of antimicrobial resistance in coagulase-negative staphylococci from bovine mastitis milk. Journal of Dairy Science, 96, 2247-2257.

    Article  CAS  PubMed Central  Google Scholar 

  • Gindonis, V., Taponen, S., Myllyniemi, A. L., Pyörälä, S., Nykäsenoja, S., Salmenlinna, S., ... and Rantala, M., 2013. Occurrence and characterization of methicillin-resistant staphylococci from bovine mastitis milk samples in Finland. Acta Veterinaria Scandinavica, 55, 61.

    Article  PubMed Central  Google Scholar 

  • Gröhn, Y. T., Wilson, D. J., Gonzalez, R. N., Hertl, J. A., Schulte, H., Bennett, G., and Schukken, Y. H., 2004. Effect of pathogen-specific clinical mastitis on milk yield in dairy cows. Journal of Dairy Science, 87, 3358-3374.

    Article  Google Scholar 

  • Halasa, T., Nielen, M. V., Huirne, R. B. M., and Hogeveen, H., 2009. Stochastic bio-economic model of bovine intramammary infection. Livestock Science, 124, 295-305.

    Article  Google Scholar 

  • Hernández-Castellano, L., Wall, S. K., Stephan, R., Corti, S., & Bruckmaier, R. M., 2017. Milk somatic cell count, lactate dehydrogenase activity, and immunoglobulin G concentration associated with mastitis caused by different pathogens: A field study. Schweizer Archiv für Tierheilkunde, 159, 283-290.

    Article  Google Scholar 

  • Hernández-Castellano, L. E., Nally, J. E., Lindahl, J., Wanapat, M., Alhidary, I. A., Fangueiro, D., Grace, D., Ratto, M., Bambou, J., and de Almeida, A. M., 2019. Dairy science and health in the tropics: challenges and opportunities for the next decades. Tropical Animal Health and Production, 51, 1009–1017.

    Article  Google Scholar 

  • Igbinosa, E.O., and Beshiru, A., 2019. Characterization of antibiotic-resistant and species diversity of staphylococci isolated from apparently healthy farm animals. African Journal of Clinical and Experimental Microbiology, 20, 289-298.

    Article  Google Scholar 

  • Khazandi, M., Al-Farha, A. A. B., Coombs, G. W., O’Dea, M., Pang, S., Trott, D. J., ... and Hoare, A., 2018. Genomic characterization of coagulase-negative staphylococci including methicillin-resistant Staphylococcus sciuri causing bovine mastitis. Veterinary Microbiology 219, 17-22.

    Article  CAS  Google Scholar 

  • Li, L., Zhou, L., Wang, L., Xue, H., and Zhao, X., 2015. Characterization of methicillin-resistant and-susceptible staphylococcal isolates from bovine milk in Northwestern China. PLoS One. 10, e0116699.

    Article  PubMed Central  Google Scholar 

  • Monecke, S., Coombs, G., Shore, A. C., Coleman, D. C., Akpaka, P., Borg, M., ... and Kadlec, K., 2011. A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PloS One. 6, e17936. https://doi.org/10.1371/journal.pone.0017936

    Article  CAS  PubMed Central  Google Scholar 

  • Sender, G., Pawlik, A., and Korwin-Kossakowska, A., 2017. Current concepts on the impact of coagulase-negative staphylococci causing bovine mastitis as a threat to human and animal health–a review. Animal Science Papers and Reports, 35, 123-135

    CAS  Google Scholar 

  • Simões, J., Branco, M., Andrade, J., and Müller, A., 2020. Phenotypic antimicrobial susceptibility of environmental bacteria from mastitic milk of pastured dairy cows of S. Miguel (Azores). Tropical Animal Health and Production, 52, 407-414.

    Article  Google Scholar 

  • Taponen, S., Björkroth, J., and Pyörälä, S., 2008. Coagulase-negative staphylococci isolated from bovine extramammary sites and intramammary infections in a single dairy herd. Journal of Dairy Science, 75, 422-429.

    CAS  Google Scholar 

  • Taponen, S., Nykasenoja, S., Pohjanvirta, T., Pitkala, A., and Pyorala, S., 2016. Species distribution and in vitro antimicrobial susceptibility of coagulase-negative staphylococci isolated from bovine mastitic milk. Acta Veterinaria Scandinavica, 58, 12.

    Article  PubMed Central  Google Scholar 

  • Thorberg, B. M., Danielsson-Tham, M. L., Emanuelson, U., and Waller, K. P., 2009. Bovine subclinical mastitis caused by different types of coagulase-negative staphylococci. Journal of Dairy Science, 92, 4962-4970.

    Article  CAS  Google Scholar 

  • Tomazi, T., Gonçalves, J. L., Barreiro, J. R., Arcari, M. A., and Dos Santos, M. V., 2015. Bovine subclinical intramammary infection caused by coagulase-negative staphylococci increases somatic cell count but has no effect on milk yield or composition. Journal of Dairy Science, 98, 3071-3078.

    Article  CAS  Google Scholar 

  • Vanderhaeghen, W., Piepers, S., Leroy, F., Van Coillie, E., Haesebrouck, F., and De Vliegher, S., 2015. Identification, ty**, ecology and epidemiology of coagulase negative staphylococci associated with ruminants. Veterinary Journal, 203, 44-51

    Article  Google Scholar 

  • Varela-Ortiz, D. F., Barboza-Corona, J. E., González-Marrero, J., León-Galván, M. F., Valencia-Posadas, M., Lechuga-Arana, A. A., and Gutiérrez-Chávez, A. J., 2018. Antibiotic susceptibility of Staphylococcus aureus isolated from subclinical bovine mastitis cases and in vitro efficacy of bacteriophage. Veterinary Research Communications, 42, 243-250

    Article  Google Scholar 

  • Xu, J., Tan, X., Zhang, X., **a, X., and Sun, H., 2015. The diversities of staphylococcal species, virulence and antibiotic resistance genes in the subclinical mastitis milk from a single Chinese cow herd. Microbial Pathogenesis, 88, 29-38.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Katja Drache, Ylanna Kelner-Burgos (BfR, Berlin, Germany), and Darius Gawlik for their kind laboratory assistance.

Funding

This work was funded in part by The Science & Technology Development Fund, Egypt (Short term fellowship, project number 25474). Sincere gratitude is also given to the Abbott (Alere Technologies GmbH), Jena, Germany, and the German Federal Institute for Risk Assessment (BfR), Berlin, Germany, for their kind cooperation.

Author information

Authors and Affiliations

  1. Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Mansoura University, Mansoura, 35516, Egypt

    Maged El-Ashker

  2. Department of Hygiene and Zoonoses, Faculty of Veterinary Medicine, Mansoura University, Mansoura, 35516, Egypt

    Mayada Gwida, Mona Elsayed & Fatma El-Gohary

  3. Department for Optical Molecular Diagnostics and System Technology, Leibniz-Institute of Photonic Technology (IPHT), Jena, Germany

    Stefan Monecke, Ralf Ehricht, Annett Reißig & Elke Müller

  4. InfectoGnostics Research Campus, Centre for Applied Research, Jena, Germany

    Stefan Monecke, Ralf Ehricht, Annett Reißig & Elke Müller

  5. Institute for Medical Microbiology and Hygiene, Medical Faculty “Carl Gustav Carus”, Technische Universität Dresden, Dresden, Germany

    Stefan Monecke

  6. Institute of Physical Chemistry, Friedrich Schiller University, Jena, Germany

    Ralf Ehricht

  7. Microbiology Unit, Department of Biological Sciences, Covenant University, Ota, Nigeria

    Akinduti Paul

  8. Applied Microbial Processes & Environmental Health Research Group, Department of Microbiology, Faculty of Life Sciences, University of Benin, Private Mail Bag 1154, Benin City, 300001, Nigeria

    Etinosa O. Igbinosa

  9. Department of Microbiology, College of Natural and Applied Sciences, Western Delta University, Private Mail Bag 10, Oghara, Delta State, 331101, Nigeria

    Abeni Beshiru

  10. Department of Biological Safety, German Federal Institute for Risk Assessment, Berlin, Germany

    Sven Maurischat

Authors
  1. Maged El-Ashker
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  2. Mayada Gwida
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  3. Stefan Monecke
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  4. Ralf Ehricht
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  5. Mona Elsayed
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  6. Fatma El-Gohary
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  7. Annett Reißig
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  8. Elke Müller
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  9. Akinduti Paul
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  10. Etinosa O. Igbinosa
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  11. Abeni Beshiru
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  12. Sven Maurischat
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Corresponding author

Correspondence to Maged El-Ashker.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The study was conducted during 2017 and 2018, and it was performed in accordance with the Guidelines for the Care and Use of Agricultural Animals in Research and Teaching, 3rd ed. (http://www.fass.org/), and the ethical guidelines of the Mansoura University, Egypt. All persons gave their informed consent prior to inclusion of their livestock in the current study.

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El-Ashker, M., Gwida, M., Monecke, S. et al. Microarray-based detection of resistance genes in coagulase-negative staphylococci isolated from cattle and buffalo with mastitis in Egypt. Trop Anim Health Prod 52, 3855–3862 (2020). https://doi.org/10.1007/s11250-020-02424-1

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