year 14, Issue 5 (September - October 2020)                   Iran J Med Microbiol 2020, 14(5): 441-459 | Back to browse issues page

XML Persian Abstract Print

Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Ghaderi H, Shiri Malekabad E, Vahidi M, Dadashi A. Evaluation of Genotypic and Phenotypic Biofilm Formation by Staphylococcus aureus Isolated from Clinical Samples and Their Association with Antimicrobial Resistance. Iran J Med Microbiol. 2020; 14 (5) :441-459
1- Ph.D. Student, Department of Bacteriology, School of Veterinary Science, Shiraz University, Shiraz. Iran
2- Instructor, Department of Biostatistics, Army Medical University (AJA), Tehran, Iran.
3- Assistant Professor, Department of Laboratory Sciences, Army Medical University (AJA), Tehran, Iran.
4- Assistant Professor, Infectious Disease Department, AJA University of Medical Sciences, Tehran, Iran. ,
Abstract:   (1831 Views)
Background:  Staphylococcus aureus is one of the most important bacteria causes nosocomial infections, which by the biofilm formation can be effective in the creation of chronic diseases, and the creation and strengthening of drug resistance. The present study aimed to evaluate the genotypic and phenotypic biofilm formation by S. aureus isolated from clinical samples and their association with antimicrobial resistance.
 Materials & Methods:   In this descriptive cross-sectional study from Dec 2019 to Sep 2019, 200 clinical samples were obtained from AJA hospitals in Tehran. All samples were analyzed using blood agar, Baird-Parker Agar, mannitol salt agar and catalase, OF and coagulase assays. Antimicrobial resistance pattern of isolates was determined by the disc diffusion method. Multiplex PCR method was used to identify biofilm formation genes, includes icaA, icaB, icaC, and icaD genes. Data analyzed using SPSS 20 and the X2 test.
Results:   Out of 200 cultivated samples, 83 (41.5%) cases were confirmed as S. aureus. The highest resistance was observed to Penicillin (94%), Tetracycline (72%), Ampicillin (54%), and Cefoxitin (51%), respectively. Phenotypic biofilm formation ability reported in 65% of isolates. The frequency of presence of icaA, icaB, icaC, and icaD genes was estimated at 67.4%, 60.2%, 61.4%, and 62.6%, respectively. Eighty-seven percent of biofilm producing strains were multidrug-resistant, while all the biofilm negative strains were non- multiple drug resistance (P< 0/05).
Conclusion:   According to the results, Biofilm-positive strains have a very high propensity to demonstrate antimicrobial resistance, multidrug resistance and resistance to methicillin.
Full-Text [PDF 857 kb]   (884 Downloads) |   |   Full-Text (HTML)  (897 Views)  
Type of Study: Original | Subject: Medical Bacteriology
Received: 2020/05/14 | Accepted: 2020/08/31 | ePublished: 2020/10/5

1. Foster TJ, O'Reilly M, Patel AH, Bramley AJ. Genetic studies of Staphylococcus aureus virulence factors. Antonie Van Leeuwenhoek 1988; 54(5): 475-82. [DOI:10.1007/BF00461866] [PMID]
2. Oyama T, Miyazaki M, Yoshimura M, Takata T, Ohjimi H, Jimi S. Biofilm-Forming Methicillin-resistant Staphylococcus aureus Survive in Kupffer Cells and Exhibit High Virulence in Mice. Toxins. 2016 Jul;8(7):198. [DOI:10.3390/toxins8070198] [PMID] [PMCID]
3. 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. [DOI:10.1016/j.micpath.2016.06.031] [PMID]
4. Shahmohammadi MR, Nahaei MR, Akbarzadeh A, Milani M. Clinical test to detect mecA and antibiotic resistance in Staphylococcus aureus, based on novel biotechnological methods. Artificial cells, nanomedicine, and biotechnology. 2016;44(6):1464-8. [DOI:10.3109/21691401.2015.1041639] [PMID]
5. Becker K, Denis O, Roisin S, Mellmann A, Idelevich EA, Knaack D, et al. Detection of mecA- and mecC-Positive Methicillin-Resistant Staphylococcus aureus (MRSA) Isolates by the New Xpert MRSA Gen 3 PCR Assay. J Clin Microbiol. 2016; 54(1): 180-4. [DOI:10.1128/JCM.02081-15] [PMID] [PMCID]
6. Havaei SA, Assadbeigi B, Esfahani BN, Hoseini NS, Rezaei N, Havaei SR. Detection of mecA and enterotoxin genes in Staphylococcus aureus isolates associated with bovine mastitis and characterization of Staphylococcal cassette chromosome mec (SCCmec) in MRSA strains. Iran J Microbiol. 2015; 7(3): 161-7.
7. Federman C, Ma C, Biswas D. Major Components of Orange Oil Inhibit Staphylococcus aureus Growth and Biofilms Formation, and Alter Its Virulence Factors. Journal of Medical Microbiology. 2016; 65(7): 688-695. [DOI:10.1099/jmm.0.000286] [PMID]
8. Thilakavathy P, Priyan RM, Jagatheeswari PA, Charles J, Dhanalakshmi V, Lallitha S, et al. Evaluation of Ica Gene in Comparison with Phenotypic Methods for Detection of Biofilm Production by Coagulase Negative Staphylococci in a Tertiary Care Hospital. J Clin Diagn Res. 2015; 9(8): 16-9. [DOI:10.7860/JCDR/2015/11725.6371] [PMID] [PMCID]
9. Tyner H, Patel R. Propionibacterium acnes biofilm - A sanctuary for Staphylococcus aureus. Anaerobe. 2016; 40: 63-7. [DOI:10.1016/j.anaerobe.2016.05.014] [PMID]
10. Neopane P, Prasad Nepal H, Shrestha R, Uehara O, Abiko Y. In Vitro Biofilm Formation by Staphylococcus aureus Isolated From Wounds of Hospital-admitted Patients and Their Association With Antimicrobial Resistance. International Journal of General Medicine. 2018; 11: 25-32. [DOI:10.2147/IJGM.S153268] [PMID] [PMCID]
11. Costa MO, Beltrame CO, Ferreira FA, Botelho AM, Lima NC, Souza RC, et al. Complete Genome Sequence of a Variant of the Methicillin-Resistant Staphylococcus aureus ST239 Lineage, Strain BMB9393, Displaying Superior Ability to Accumulate ica-Independent Biofilm. Genome announcements. 2013;1(4). [DOI:10.1128/genomeA.00576-13] [PMID] [PMCID]
12. Naicker PR, Karayem K, Hoek KG, Harvey J, Wasserman E. Biofilm Formation in Invasive Staphylococcus aureus Isolates is Associated With the Clonal Lineage. Microb Pathog. 2016; 90: 41-9. [DOI:10.1016/j.micpath.2015.10.023] [PMID]
13. Namvar AE, Asghari B, Ezzatifar F, Azizi G, Lari AR. Detection of the Intercellular Adhesion Gene Cluster (ica) in Clinical Staphylococcus aureus Isolates. GMS Hyg Infect Control. 2013; 8(1): 03.
14. Murray P, Rosenthal K, Kobayashi G, et al. Medical microbiology. 6rd ed. Missouri: Mosby Inc.St.Louis, 2010.
15. Pa W. Clinical and Laboratory Standard Institute C. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically Approved Standard M7-A7 Clinical and Laboratory Standard Institute. 2006.
16. Doebbeling B. The Epidemiology of Methicillin-resistant Staphylococcus aureus Colonisation and Infection. J Chemother. 1995; 7(3): 99-103.
17. Silva G, Kantzanou M, Justice A, Massey RC, Wilkinson AR, Day N, Peacock SJ. The ica Operon and Biofilm Production in Coagulase- Negative Staphylococci Associated with Carriage and Disease in a Neonatal Intensive Care Unit. J Clin Microbiol. 2002; 40(2): 382-8. [DOI:10.1128/JCM.40.02.382-388.2002] [PMID] [PMCID]
18. Christensen GD, Simpon WA, Younger JJ, Baddour LM, Barrett FF, Meleton DM, et al. Adherence of Coagulase-Negative Staphylococci to Plastic Tissue Culture Plates: a Quantitative Model for the Adherence of Staphylococci to Medical Devices. J Clin Microbiol. 1985; 22(6): 996-1006. [DOI:10.1128/JCM.22.6.996-1006.1985] [PMID] [PMCID]
19. Udo R, Hans-Jörg L, Michaela M, Birgit L, Norbert L. Rapid Identification of Methicillin-Resistant Staphylococcus aureus and Simultaneous Species Confirmation Using Real-Time Fluorescence PCR. J. Clin. Microbiol. 2000 38(6): 2429-2433. [DOI:10.1128/.38.6.2429-2433.2000] [PMID] [PMCID]
20. Zhang K, Sparling J, Chow BL, Elsayed S, Hussain Z, Church DL, et al. New Quadriplex PCR Assay for Detection of Methicillin and Mupirocin Resistance and Simultaneous Discrimination of Staphylococcus aureus from Coagulase-negative Staphylococci. Journal of Clinical Microbiology. 2004; 42(11): 4947-55. [DOI:10.1128/JCM.42.11.4947-4955.2004] [PMID] [PMCID]
21. Piechota M, Kot B, Frankowska-Maciejewska A, Grużewska A, Woźniak-Kosek A. Biofilm formation by methicillin-resistant and methicillin-sensitive Staphylococcus aureus strains from hospitalized patients in Poland. BioMed Research International. 2018 Dec 27;2018. [DOI:10.1155/2018/4657396] [PMID] [PMCID]
22. Eftekhar F, Dadaei T. Biofilm Formation and Detection of icaAB Genes in Clinical Isolates of Methicillin Resistant Staphylococcus aureus. Iranian Journal of Basic Medical Sciences. 2011; 14(2):132-6.
23. Manandhar S, Singh A, Varma A, Pandey S, Shrivastava N. Evaluation of methods to detect in vitro biofilm formation by staphylococcal clinical Isolates. BMC Res Notes. 2018; 11: 714. [DOI:10.1186/s13104-018-3820-9] [PMID] [PMCID]
24. Mashaiekhi S, Amini K. Antibiotic resistance pattern and biofilm production in Staphylococcus aureus isolates and Staphylococcus epidermidis isolated from hospital infections Tehran in 2016. Journal of Birjand University of Medical Sciences. 2018; 25(2): 160-166. (Persian).
25. Nourbakhsh F, Momtaz H. Evaluation of Phenotypic and Genotypic Biofilm Formation in Staphylococcus aureus Isolates Isolated from Hospital Infections in Shahrekord, 2015. AMUJ. 2016; 19(109): 69-79.
26. Sadri H, Owlia P, Shahrbanooie R. Vancomycin resistance among clinical isolates of Staphylococcus aureus. Arch Iranian Med. 2005; 8(2): 100-103.
27. Ahmadi Z, Tajbakhsh E, Momtaz H. Detection of the antibiotic resistance pattern in Staphylococcus aureus isolated from clinical samples obtained from patients hospitalised in Imam Reza hospital, Kermanshah. Journal of Microbial World. 2014; 6(4): 299-311.
28. Hauschild T, Sacha P, Wieczorek P, Zalewska M, Kaczyñska K, Tryniszewska E. Aminoglycosides resistance in clinical isolates of Staphylococcus aureus from a University Hospital in Bialystok, Poland. Folia Histochem Cytobiologica. 2008; 46(2): 225-228. [DOI:10.2478/v10042-008-0034-3] [PMID]
29. Mirzaee M, Najar-Peerayeh S, Behmanesh M, Forouzandeh Moghadam M, Ghasemian AM. Biofilm Formation and Presence of ica Genes in Staphylococcus aureus Isolated from Intensive Care Unit. J Mazandaran Univ Med Sci. 2014; 24(115): 43-51.
30. Abdollahi A, Kouhpaye SA, Najafipour S, Mansouri Y, Abdollahi Kherabadi S, Jafari S. Frequency of drug resistance and staphylococcal chromosomal cassette mec (SCCmec). Genotype in Methicillin-Resistant Staphylococcus aureus strains. Scientific and Research Journal of Alborz Medical Sciences. 2012; 1(1): 47-52.
31. Abu-Shady HM, El-Essawy AK, Salama MS, El-Ayesh AM. Detection and molecular characterization of vancomycin resistant Staphylococcus aureus from clinical isolates. African Journal of Biotechnology. 2012; 11(99): 494-503.
32. Tabaei S, Noghondar MK, Mohammadzadeh M, Ataei L, Amel Jamehdar S. Pattern of antibiotic resistance in methicillin-resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens: Imam Reza hospital in Mashhad. Medical Journal of Mashhad University of Medical Sciences. 2016; 59(2): 64-70.
33. Rahimi F, Bouzari M, Katouli M, Pourshafie MR. Antibiotic resistance pattern of methicillin resistant and methicillin sensitive staphylococcus aureus isolates in Tehran, Iran. Jundishapur J Microbiol. 2013; 6:144-149. [DOI:10.5812/jjm.4896]
34. Hassanzadeh S, Pourmand MR, Hadadi A, Nourijeylani K, Yousefi M, Mashhadi R. Frequency and antimicrobial resistance patterns of methicillin resistant staphylococcus aureus in Tehran. J Med Bacteriol. 2013; 2: 41-46.
35. Hatefizade B, Hosseini F, Moradi Bidhendi S. Study of some of antiseptic drugs on Staphylococcal strains biofilm isolated from patients with infectious skin during 2014-2015 in Tehran city. Razi Journal of Medical Sciences. 2016; 23(148): 128-135.
36. Motamedi H, Asghari B, Tahmasebi H, Arabestani MR. Adhesion Factors and Association with Antibiotic Resistance among Clinical Isolates of Staphylococcus aureus. Iran J Med Microbiol. 2017; 11 (3): 27-36
37. Croes S, Deurenberg RH, Boumans ML, Beisser PS, Neef C, Stobberingh EE. Staphylococcus aureus biofilm formation at the physiologic glucose concentration depends on the S. aureus lineage. BMC Microbiol. 2009; 9: 229. [DOI:10.1186/1471-2180-9-229] [PMID] [PMCID]
38. Gad GF, El-Feky MA, El-Rehewy MS, Hassan MA, Abolella H, El-Baky R. M. Detection of icaA, icaD genes and biofilm production by Staphylococcus aureus and Staphylococcus epidermidis isolated from urinary tract catheterized patients. J Infect Dev Ctries. 2009; 3(5): 342-51. [DOI:10.3855/jidc.241] [PMID]

Add your comments about this article : Your username or Email:

Send email to the article author

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

© 2022 CC BY-NC 4.0 | Iranian Journal of Medical Microbiology

Designed & Developed by : Yektaweb | Publisher: Farname Inc