Characteristics of Methicillin Resistant Staphylococcus aureus Strains Isolated from Hospital Wastewater in Tehran, Iran

Document Type : Original Research

Authors
Department of Microbiology, Faculty of Biological Science and Technology, University of Isfahan, Isfahan, Iran
Abstract
Backgrounds: Hospital sewage is known as an important source of human pathogenic bacteria such as methicillin resistant Staphylococcus aureus (MRSA) strains disseminated from hospital to the environment. This study aimed to investigate the presence of MRSA in the treated outgoing wastewater collected from a referral hospital in Tehran, Iran.

Materials & Methods: During 2015, sampling was carried out at two stages from a hospital wastewater. All black colonies with halos on HiCrome aureus agar medium supplemented with oxacillin were collected and identified as MRSA using specific primers for nucA and mecA genes. Isolates susceptibility to 18 antibiotics was determined according to the recommendations of the Clinical and Laboratory Standards Institute (CLSI). Bacterial typing was performed for the isolates using a combination of Phene plate (PhP) typing, prophage typing, staphylococcal cassette chromosome mec (SCCmec) and ccr typing methods.

Findings: A total of 79 MRSA isolates were confirmed using specific primers and showed susceptibility to quinupristin-dalfopristin, vancomycin, chloramphenicol, and linezolid. High resistance to penicillin, ciprofloxacin, kanamycin, tobramycin, and erythromycin was reported. Sixteen PhP types consisting of eight common types (CTs) and eight single types (STs) were identified among the strains, among which CT1 was the dominant type. Also, two prophage patterns and four prophage types were identified, and all the strains were positive for SCCmec type III and ccr type 3.

Conclusion: The results of this study revealed that sewage-treatment process was able to remove community-acquired MRSA (CA-MRSA) strains; however, hospital-acquired MRSA (HA-MRSA) strains were able to survive during the treatment process in this hospital.

Keywords

Subjects


1. Hanssen AM, Ericson Sollid JU. SCCmec in staphylococci: genes on the move. FEMS Immunology & Medical Microbiology. 2006;46(1):8-20.
2. Rahimi F, Katouli M, Karimi S. Biofilm production among methicillin resistant Staphylococcus aureus strains isolated from catheterized patients with urinary tract infection. Microbial Pathogenesis. 2016;98:69-76.
3. Rahimi F, Katouli M, Pourshafie MR. Characteristics of hospital-and community-acquired meticillin-resistant Staphylococcus aureus in Tehran, Iran. Journal of Medical Microbiology. 2014;63(6):796-804.
4. Fatholahzadeh B, Emaneini M, Gilbert G, Udo E, Aligholi M, Modarressi MH, et al. Staphylococcal cassette chromosome mec (SCCmec) analysis and antimicrobial susceptibility patterns of methicillin-resistant Staphylococcus aureus (MRSA) isolates in Tehran, Iran. Microbial Drug Resistance. 2008;14(3):217-20.
5. Rahimi F, Katouli M, Pourshafie MR. Characterization of methicillin-resistant Staphylococcus aureus strains in sewage treatment plants in Tehran, Iran. Journal of Water and Health 2021;19(2):216-28.
6. Börjesson S, Dienues O, Jarnheimer P-Å, Olsen B, Matussek A, Lindgren P-E. Quantification of genes encoding resistance to aminoglycosides, β-lactams and tetracyclines in wastewater environments by real-time PCR. International Journal of Environmental Health Research. 2009;19(3):219-30.
7. Börjesson S, Matussek A, Melin S, Löfgren S, Lindgren P-E. Methicillin‐resistant Staphylococcus aureus (MRSA) in municipal wastewater: an uncharted threat? Journal of Applied Microbiology. 2010;108(4):1244-51.
8. Börjesson S, Melin S, Matussek A, Lindgren P-E. A seasonal study of the mecA gene and Staphylococcus aureus including methicillin-resistant S. aureus in a municipal wastewater treatment plant. Water Research. 2009;43(4):925-32.
9. Goldstein RER, Micallef SA, Gibbs SG, Davis JA, He X, George A, et al. Methicillin-resistant Staphylococcus aureus (MRSA) detected at four US wastewater treatment plants. Environmental Health Perspectives. 2012;120(11):1551.
10. Rahimi F, Bouzari M. Biochemical fingerprinting of methicillin-resistant Staphylococcus aureus isolated from sewage and hospital in Iran. Jundishapur Journal of Microbiology. 2015;8(7):e19760.
11. Thompson J, Gündoğdu A, Stratton H, Katouli M. Antibiotic resistant Staphylococcus aureus in hospital wastewaters and sewage treatment plants with special reference to methicillin‐resistant Staphylococcus aureus (MRSA). Journal of Applied Microbiology. 2013;114(1):44-54.
12. Rahimi F, Shokoohizadeh L. Characterization of methicillin resistant Staphylococcus aureus strains among inpatients and outpatients in a referral hospital in Tehran, Iran. Microbial Pathogenesis. 2016;97:89-93.
13. Pantůček R, Doškař J, Růžičková V, Kašpárek P, Oráčová E, Kvardová V, et al. Identification of bacteriophage types and their carriage in Staphylococcus aureus. Archives of Virology. 2004;149(9):1689-703.
14. Rahimi F, Bouzari M, Katouli M, Pourshafie MR. Prophage and antibiotic resistance profiles of methicillin-resistant Staphylococcus aureus strains in Iran. Archives of Virology. 2012;157(9):1807-11.
15. Clinical and Laboratory Standard Institute C. Performance standards for antimicrobial susceptibility testing, 26th informational supplement. Clinical and Laboratory Standard Institute, Wayne, Pa. 2016.
16. Zhang K, McClure J-A, Elsayed S, Louie T, Conly JM. 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. 2005;43(10):5026-33.
17. Rahimi F, Karimi S. Characteristics of methicillin resistant Staphylococcus aureus strains isolated from poultry in iran. Archives of Clinical Infectious Diseases. 2015;10(4):e30885.
18. Rahimi F, Karimi S. Isolation of methicillin-resistant Staphylococcus aureus strains producing enterotoxins A, K and Q From chicken meat in Isfahan, Iran, 2014. Archives of Clinical Infectious Diseases. 2016;11(4):e35601.
19. Rahimi F, Qasemi A. Epidemiological link between methicillin-resistant Staphylococcus aureus strains isolated from 2 different cities in Iran. Infectious Diseases in Clinical Practice. 2019;27(3):163-9.
20. Rahimi F, Shafiei R. Characteristics of enterotoxin-producing methicillin-resistant Staphylococcus aureus strains isolated from meat in Tehran, Iran. Journal of Consumer Protection and Food Safety. 2019;14(4): 389-98.
21. Rahimi F, Shokoohizadeh L. Characterization of virulence factors and prophage profiles of methicillin-resistant Staphylococcus aureus strains isolated from a referral hospital in Tehran, Iran. Archives of Clinical Infectious Diseases. 2018;13(5):e59385.
22. Schwartz T, Kohnen W, Jansen B, Obst U. Detection of antibiotic-resistant bacteria and their resistance genes in wastewater, surface water, and drinking water biofilms. FEMS Microbiology Ecology. 2003;43(3):325-35.
23. Goudarzi M, Goudarzi H, Figueiredo AMS, Udo EE, Fazeli M, Asadzadeh M, et al. Molecular characterization of methicillin resistant Staphylococcus aureus strains isolated from intensive care units in Iran: ST22-SCCmec IV/t790 emerges as the major clone. PloS One. 2016;11(5):e0155529.
24. Rahimi F, Bouzari M, Katouli M, Pourshafie MR. Antibiotic resistance pattern of methicillin resistant and methicillin sensitive Staphylococcus aureus isolates in Tehran, Iran. Jundishapur Journal of Microbiology. 2013;6(2):144-9.
25. Rahimi F, Bouzari M, Maleki Z, Rahimi F. Antibiotic susceptibility pattern among Staphylococcus spp. with emphasis on detection of mecA gene in methicillin resistant Staphylococcus aureus isolates. Iranian Journal of Clinical Infectious Diseases. 2009;4(3):143-50.
26. Rahimi F, Bouzari M, Katouli M, Pourshafie M. Prophage typing of methicillin resistant Staphylococcus aureus isolated from a tertiary care hospital in Tehran, Iran. Jundishapur Journal of Microbiology. 2013;6(1):80-5.
27. Rahimi F, Karimi S. Characteristics of virulence factors in methicillin-resistant Staphylococcus aureus strains isolated from a referral hospital in Tehran, Iran. Archives of Clinical Infectious Diseases. 2016;11(1):e33220.