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Microbiology and Biotechnology Letters


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Environmental Microbiology (EM)  |  Microbial Ecology and Diversity

Microbiol. Biotechnol. Lett. 2021; 49(3): 367-373

Received: February 13, 2021; Revised: April 7, 2021; Accepted: April 8, 2021

Ambient Air Waste Sorting Facilities Could Be a Source of Antibiotic Resistant Bacteria

Ana Calheiros1, Joana Santos1,2, Carla Ramos1, Marta Vasconcelos2,3, and Paulo Fernandes1,2*

1Escola Superior de Tecnologia e Gestão, Instituto Politécnico de Viana do Castelo, Rua Escola Industrial e Comercial de Nun’Álvares, 4900-347, Viana do Castelo, Portugal 2CISAS, Escola Superior de Tecnologia e Gestão, Instituto Politécnico de Viana do Castelo, Rua Escola Industrial e Comercial de Nun’Álvares, 4900-347, Viana do Castelo, Portugal 3Instituto Politécnico de Coimbra, ESTESC–Coimbra Health School, Saúde Ambiental, Coimbra, Portugal

Correspondence to :
Paulo Fernandes,

The antimicrobial resistance of Staphylococcus spp. and Gram negative strains present in air samples from waste sorting facilities was assessed. Phenotypic studies have revealed a high percentage of strains of Staphylococcus spp. resistant to methicillin. Genotypically and by RT-PCR, it was found that the mecA gene usually associated with methicillin resistance was present in 8% of the Staphylococcus strains isolated. About 30% of the Gram negative strains from the same samples also displayed resistance to meropenem and 79% of these were resistant to multiple antibiotics from different classes, namely cephalosporins and β- lactams. The results suggest that in professional activities with high levels of exposure to biological agents, the quantification and identification of the microbial flora in the work environment, with the determination of the presence of potential agents displaying multi-resistances is of relevance to the risk assessment. The personal protection of workers is particularly important relevance in these cases, since many of the strains that exhibit multi-resistance are potential opportunistic agents.

Keywords: Staphylococcus, Enterobacteriaceae, biological risk, antimicrobial resistance

Graphical Abstract

  1. Anderson M, Clift C, Schulze K, Sagan A, Nahrgang S, Alt Ouakrim D, et al. 2019. Averting the AMR Crisis: What are the Avenues for Policy Action for Countries in Europe. In POLICY BRIEF 32, European Observatory on Health Systems and Policies, WHO.
  2. World Health Organization. 2020. Antibiotic Resistance. Available from Accessed Jan. 30, 2020.
  3. Berendonk TU, Manaia CM, Merlin C, Fatta-Kassinos D, Cytryn E, Walsh F, et al. 2015. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13: 310-317.
  4. Brun E. 2007. Expert forecast on emerging biological risks related to occupational safety and health. Luxembourg: EUR-OP.
  5. Pinto MJdV, Veiga JM, Fernandes P, Ramos C, Gonçalves S, Velho MMLV, et al. 2015. Airborne microorganisms associated with packaging glass sorting facilities. J. Toxicol. Environ. Health Part A. 78: 685-696.
  6. Matuschek E, Brown DF, Kahlmeter G. 2014. Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin. Microbiol. Infect. 20: O255-266.
  7. Leclercq R, Cantón R, Brown DFJ, Giske CG, Heisig P, MacGowan AP, et al. 2013. EUCAST expert rules in antimicrobial susceptibility testing. Clin. Microbiol. Infect. 19: 141-160.
  8. CLSI. 2012. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard—11th, Ed. CLSI document M02A11.
  9. The European Comittee on Antimicrobial Susceptibility Testing. 2014. Breakpoint tables for interpretation of MICs and zone diameters. Version 4.0, 2014.
  10. CLSI. 2012. Methods for Dilution Antimicrobial Susceptibility Tests f or Bacteria That Grow Aerobically; Approved St andard— 9th, Ed. CLSI document M07-A9.
  11. Kalia A, Rattan A, Chopra P, Kalia A, Rattan A, Chopra P. 1999. A method for extraction of high-quality and high-quantity genomic DNA generally applicable to pathogenic bacteria. Anal. Biochem. 275: 1-5.
  12. Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S. 1991. Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J. Clin. Microbiol. 29:2240-2244.
    Pubmed KoreaMed
  13. DTU Food NFI, European Union Reference Laboratory-Antibiotic Resistance. 2012. Protocol for PCR Amplification of mecA, mecC (mecALGA251), spa and pvl. Accessed Nov. 16, 2017.
  14. Muyzer G, Dewaal EC, Uitterlinden AG. 1993. Profiling of complex microbial-populations by denaturing gradient gel-electrophoresis analysis of polymerase chain reaction-amplified genes-coding for 16s ribosomal-RNA. Appl. Environ. Microbiol. 59: 695-700.
    Pubmed KoreaMed
  15. Bhargava K, Zhang Y. 2012. Multidrug-resistant coagulase-negative Staphylococci in food animals. J. Appl. Microbiol. 113: 1027-1036.
  16. Fontes CO, Silva VL, de Paiva MRB, de Paiva B, Garcia RA, Resende JA, et al. 2013. Prevalence, antimicrobial resistance, and virulence characteristics of mecA-encoding coagulase-negative Staphylococci isolated from soft cheese in Brazil. J. Food Sci. 78: M594M599.
  17. Nascimento TC, Januzzi WD, Leonel M, da Silva VL, Diniz CG. 2009. Occurrence of clinically relevant bacteria in health service waste in a Brazilian sanitary landfill and antimicrobial susceptibility profile. Rev. Soc. Bras. Med. Trop. 42: 415-419.
  18. Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. 2012. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18: 268-281.
  19. Laurent F, Chardon H, Haenni M, Bes M, Reverdy M-E, Madec J-Y, et al. 2012. MRSA harboring mecA variant gene mecC, France. Emerg. Infect. Dis. 18: 1465-1467.
    Pubmed KoreaMed
  20. Perazzi B, Fermepin MR, Malimovka A, García SD, Orgambide M, Vay CA, et al. 2006. Accuracy of cefoxitin disk testing for characterization of oxacillin resistance mediated by penicillin-binding protein 2a in coagulase-negative Staphylococci. J. Clin. Microbiol. 44: 3634-3639.
    Pubmed KoreaMed
  21. Ghoshal U, Prasad KN, Singh M, Tiwari DP, Ayyagari A. 2004. A comparative evaluation of phenotypic and molecular methods for the detection of oxacillin resistance in coagulase-negative staphylococci. J. Infect. Chemother. 10: 86-89.
  22. Elhassan MM, Ozbak HA, Hemeg HA, Elmekki MA, Ahmed LM. 2015. Absence of the mecA Gene in methicillin resistant Staphylococcus aureus isolated from different clinical specimens in Shendi City, Sudan. BioMed. Res. Int. 2015: 895860-895860.
    Pubmed KoreaMed
  23. Pitout JD, Laupland KB. 2008. Extended-spectrum beta-lactamaseproducing Enterobacteriaceae: an emerging public-health concern. Lancet Infect. Dis. 8: 159-166.
  24. Paterson DL. 2006. Resistance in gram-negative bacteria: enterobacteriaceae. Am. J. Med. 119: S20-S28.
  25. Cohen Stuart J, Leverstein-Van Hall MA. 2010. Guideline for phenotypic screening and confirmation of carbapenemases in Enterobacteriaceae. Int. J. Antimicrob. Agents 36: 205-210.
  26. Douwes J, Thorne P, Pearce N, Heederik D. 2003. Bioaerosol health effects and exposure assessment: progress and prospects. Ann. Occup. Hyg. 47: 187-200.
  27. Brooks JP, Maxwell SL, Rensing C, Gerba CP, Pepper IL. 2007. Occurrence of antibiotic-resistant bacteria and endotoxin associated with the land application of biosolids. Can. J. Microbiol. 53:616-622.

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