The prevalence of exotoxins, adhesion, and biofilm-related genes in Staphylococcus aureus isolates from the main burn center of Tehran, Iran

Document Type : Original Article

Authors

1 Microbial Biotechnology Research Center, Department of Microbiology, School of Medicine, Iran University of Medical Sciences, Tehran, Iran

2 Burn Research Center, Shahid Motahari Hospital, Iran University of Medical Sciences, Tehran, Iran

3 School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

4 School of Medicine, Shahroud University of Medical Sciences, Shahroud, Iran

5 Cellular and Molecular Research Center, Yasuj University of Medical Sciences, Yasuj, Iran

Abstract

Objective(s): The present study investigated the prevalence of genes encoding for exotoxins, adhesion and biofilm factors in Staphylococcus aureus isolates obtained from samples in a referral burn hospital in Tehran, Iran.
Materials and Methods: S. aureus isolates obtained from patients, personnel and surfaces in the wards of a burn hospital were identified and confirmed by biochemical and molecular tests, respectively. The susceptibility of isolates was determined using the disk diffusion method. Virulence factors were detected by multiplex PCR.
Results: The frequency of hla, hlb, hld, hlg, tst and pvl genes was 92.8%, 34.7%, 89.8%, 11.9%, 10.7%, and 0.5% respectively. The results revealed that the hla gene had the highest frequency among isolates (94.4% for methicillin-resistant S. aureus (MRSA) and 89.8% for methicillin-susceptible S. aureus (MSSA)). The most prevalent adhesion and biofilm-related gene was eno (85.6%). The prevalence of the remaining genes was as follows:  fib (71.8%), clfB (70%), cna (59.2 %), fnbB (17.9%), icaA (72.4%), and icaD (85.6%). The incidence of fib, hlb, hlg, and tst genes was significantly higher in MRSA isolates compare to the MSSA isolates. Moreover, the resistance rates for all antibiotics were higher is MRSA isolates except for nitrofurantoin and chloramphenicol antibiotics.
Conclusion: Data indicate the high prevalence rates of virulence factors among S. aureus isolates, especially MRSA strains in the burn hospital. This should to be taken into account in the development of an effective infection control policy and continuous monitoring of drug resistance in hospitals.

Keywords

Main Subjects

References

1. Boers SA, van Ess I, Euser SM, Jansen R, Tempelman FR, Diederen BM. An outbreak of a multiresistant methicillin-susceptible Staphylococcus aureus (MR-MSSA) strain in a burn centre: the importance of routine molecular typing. Burns: Burns 2011;37:808-813.
2. Chen X, Yang HH, Huangfu YC, Wang WK, Liu Y, Ni YX, et al. Molecular epidemiologic analysis of Staphylococcus aureus isolated from four burn centers. Burns : Burns 2012;38:738-742.
3. Sina H, Ahoyo TA, Moussaoui W, Keller D, Bankole HS, Barogui Y, et al. Variability of antibiotic susceptibility and toxin production of Staphylococcus aureus strains isolated from skin, soft tissue, and bone related infections. BMC Microbiol 2013;13:188-196.
4. Otto M. Staphylococcus aureus toxins. Curr Opin Microbiol 2014;17:32-37.
5. Teare L, Shelley OP, Millership S, Kearns A. Outbreak of Panton-Valentine leucocidin-positive meticillin-resistant Staphylococcus aureus in a regional burns unit. J Hosp Infect 2010;76:220-224.
6. Foster TJ, Hook M. Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 1998;6:484-488.
7. Tristan A, Ying L, Bes M, Etienne J, Vandenesch F, Lina G. Use of multiplex PCR to identify Staphylococcus aureus adhesins involved in human hematogenous infections. J Clin Microbiol 2003;41:4465-4467.
8. den Reijer PM, Haisma EM, Lemmens-den Toom NA, Willemse J, Koning RI, Demmers JA, et al. Detection of alpha-toxin and other virulence factors in biofilms of Staphylococcus aureus on polystyrene and a human epidermal model. PLoS One 2016;11:e0145722.
9. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence 2011;2:445-459.
10. Rodrigues MVP, Fortaleza CMCB, Riboli DFM, Rocha RS, Rocha C, de Souza MdLR. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in a burn unit from Brazil. Burns 2013;39:1242-1249.
11. Darban-Sarokhalil D, Khoramrooz SS, Marashifard M, Hosseini SAAM, Parhizgari N, Yazdanpanah M, et al. Molecular characterization of Staphylococcus aureus isolates from southwest of Iran using spa and SCCmec typing methods. Microb Pathog 2016;98:88-92.
12. Bar-Gal GK, Blum SE, Hadas L, Ehricht R, Monecke S, Leitner G. Host-specificity of Staphylococcus aureus causing intramammary infections in dairy animals assessed by genotyping and virulence genes. Vet Microbiol 2015;176:143-154.
13. Japoni A, Jamalidoust M, Farshad S, Ziyaeyan M, Alborzi A, Japoni S, et al. Characterization of SCCmec types and antibacterial susceptibility patterns of methicillin-resistant Staphylococcus aureus in Southern Iran. Jpn J Infect Dis 2011;64:28-33.
14. Vasudevan P, Nair MKM, Annamalai T, Venkitanarayanan KS. Phenotypic and genotypic characterization of bovine mastitis isolates of Staphylococcus aureus for biofilm formation. Vet Microbiol 2003;92:179-185.
15. Jarraud S, Mougel C, Thioulouse J, Lina G, Meugnier H, Forey F, et al. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect Immun 2002;70:631-641.
16. Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes forStaphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000;38:1032-1035.
17. Abbasi-Montazeri E, Khosravi AD, Feizabadi MM, Goodarzi H, Khoramrooz SS, Mirzaii M, et al. The prevalence of methicillin resistant Staphylococcus aureus (MRSA) isolates with high-level mupirocin resistance from patients and personnel in a burn center. Burns 2013;39:650-654.
18. Dibah S, Arzanlou M, Jannati E, Shapouri R. Prevalence and antimicrobial resistance pattern of methicillin resistant Staphylococcus aureus (MRSA) strains isolated from clinical specimens in Ardabil, Iran. Iran J Microbiol. 2014;6:163.
19. Kooistra-Smid M, van Dijk S, Beerthuizen G, Vogels W, van Zwet T, van Belkum A, et al. Molecular epidemiology of Staphylococcus aureus colonization in a burn center. Burns 2004;30:27-33.
20. Parhizgari N, Khoramrooz SS, Hosseini M, Asghar SA, Marashifard M, Yazdanpanah M, et al. High frequency of multidrug‐resistant Staphylococcus aureus with SCCmec type III and Spa types t037 and t631 isolated from burn patients in Southwest of Iran. APMIS 2016;124:221-228.
21. Kateete DP, Namazzi S, Okee M, Okeng A, Baluku H, Musisi NL, et al. High prevalence of methicillin resistant Staphylococcus aureus in the surgical units of Mulago hospital in Kampala, Uganda. BMC Res Notes 2011;4:326-330.
22. Song W, Lee KM, Kang HJ, Shin DH, Kim DK. Microbiologic aspects of predominant bacteria isolated from the burn patients in Korea. Burns 2001;27:136-139.
23. Alebachew T, Yismaw G, Derabe A, Sisay Z. Staphylococcus aureus burn wound infection among patients attending yekatit 12 hospital burn unit, addis ababa, ethiopia. Ethiop J Health Sci 2012;22:209-213.
24. Khoramrooz SS, Dolatabad SA, Dolatabad FM, Marashifard M, Mirzaii M, Dabiri H, et al. Detection of tetracycline resistance genes, aminoglycoside modifying enzymes, and coagulase gene typing of clinical isolates of Staphylococcus aureus in the Southwest of Iran. Iran J Basic Med Sci 2017;20:912-919.
25. Davies J, Davies D. Origins and evolution of antibiotic resistance. Microbiol Mol Biol Rev 2010;74:417-433.
26. Bayat B, Zade MH, Mansouri S, Kalantar E, Kabir K, Zahmatkesh E, et al. High frequency of methicillin-resistant Staphylococcus aureus (MRSA) with SCCmec type III and spa type t030 in Karaj’s teaching hospitals, Iran. Acta Microbiol Immunol Hung 2017;64:331-341.
27. Hetem DJ, Bonten MJ. Clinical relevance of mupirocin resistance in Staphylococcus aureus. J Hosp Infect 2013;85:249-256.
28. Patel JB, Gorwitz RJ, Jernigan JA. Mupirocin resistance. Clin Infect Dis. 2009;49:935-941.
29. Khoramrooz SS, Mansouri F, Marashifard M, Hosseini SAAM, Chenarestane-Olia FA, Ganavehei B, et al. Detection of biofilm related genes, classical enterotoxin genes and agr typing among Staphylococcus aureus isolated from bovine with subclinical mastitis in southwest of Iran. Microb Pathog 2016;97:45-51.
30. Motallebi M, Jabalameli F, Asadollahi K, Taherikalani M, Emaneini M. Spreading of genes encoding enterotoxins, haemolysins, adhesin and biofilm among methicillin resistant Staphylococcus aureus strains with staphylococcal cassette chromosome mec type IIIA isolated from burn patients. Microb Pathog 2016;97:34-37.
31. Satorres SE, Alcaraz LE. Prevalence of icaA and icaD genes in Staphylococcus aureus and Staphylococcus epidermidis strains isolated from patients and hospital staff. Cent Eur J Public Health 2007;15:87-90.
32. Haveri M, Hovinen M, Roslof A, Pyorala S. Molecular types and genetic profiles of Staphylococcus aureus strains isolated from bovine intramammary infections and extramammary sites. J Clin Microbiol 2008;46:3728-3735.
33. Gharsa H, Dziri R, Klibi N, Chairat S, Lozano C, Torres C, et al. Environmental Staphylococcus aureus contamination in a Tunisian hospital. J Chemother 2016;28:506-509.
34. Karmakar A, Dua P, Ghosh C. Biochemical and molecular analysis of Staphylococcus aureus clinical isolates from hospitalized patients. Can J Infect Dis Med Microbiol 2016;2016:9041636.
35. Liu C, Chen ZJ, Sun Z, Feng X, Zou M, Cao W, et al. Molecular characteristics and virulence factors in methicillin-susceptible, resistant, and heterogeneous vancomycin-intermediate Staphylococcus aureus from central-southern China. J Microbiol Immunol Infec 2015;48:490-496.
36. Emaneini M, Khoramrooz SS, Shahsavan S, Dabiri H, Jabalameli F. Prevalence of Panton-Valentine leucocidin and phenotypic and genotypic characterization of biofilm formation among Staphylococcus aureus strains isolated from children with adenoid hypertrophy. Microb Pathog 2015;89:150-153.
37. Mkrtchyan HV, Xu Z, Yacoub M, Ter-Stepanyan MM, Karapetyan HD, Kearns AM, et al. Detection of diverse genotypes of methicillin-resistant Staphylococcus aureus from hospital personnel and the environment in Armenia. Antimicrob Resist Infect Control 2017;6:19-23.
38. Murray CK, Holmes RL, Ellis MW, Mende K, Wolf SE, McDougal LK, et al. Twenty-five year epidemiology of invasive methicillin-resistant Staphylococcus aureus (MRSA) isolates recovered at a burn center. Burns 2009;35:1112-1127.
39. Becker K, Roth R, Peters G. Rapid and specific detection of toxigenic Staphylococcus aureus: use of two multiplex PCR enzyme immunoassays for amplification and hybridization of staphylococcal enterotoxin genes, exfoliative toxin genes, and toxic shock syndrome toxin 1 gene. J Clin Microbiol 1998;36:2548-2553.
40. Norouzi J, Goudarzi G, Pakzad P, Razavipour R. The isolation and detection of Staphylococcus aureus enterotoxins AE and TSST-1 genes from different sources by PCR method. Qom Univ Med Sci J 2012;6:78-85.
41. Peck KR, Baek JY, Song JH, Ko KS. Comparison of genotypes and enterotoxin genes between Staphylococcus aureus isolates from blood and nasal colonizers in a Korean hospital. J Korean Med Sci 2009;24:585-591.
42. De Boeck H, Vandendriessche S, Hallin M, Batoko B, Alworonga JP, Mapendo B, et al. Staphylococcus aureus nasal carriage among healthcare workers in Kisangani, the Democratic Republic of the Congo. Eur J Clin Microbiol Infect Dis 2015;34:1567-1572.
43. Jaspers M, Breederveld R, Tuinebreijer W, Diederen B. The evaluation of nasal mupirocin to prevent Staphylococcus aureus burn wound colonization in routine clinical practice. Burns 2014;40:1570-1574.
44. Asadollahi P, Farahani NN, Mirzaii M, Khoramrooz SS, Van Belkum A, Asadollahi K, et al. Distribution of the most prevalent spa types among clinical isolates of methicillin-resistant and-susceptible Staphylococcus aureus around the world: A review. Front Microbiol 2018;9:163-178.
Iranian Journal of Basic Medical Sciences
Volume 22, Issue 11
November 2019
Pages 1267-1274

Files

Share

How to cite

Statistics