Isolation of Methicillin-Resistant Staphylococcus epidermidis Strains Containing the arcA Gene Producing Enterotoxins A, B, C, D, E, G, H, and I from Hospital Infections in Isfahan, Iran
Subject Areas : microbiology
Parisa Behshod
1
,
Elahe Tajbakhsh
2
1 - Department of Microbiology, Islamic Azad University,Shahrekord, Iran.
2 - گروه زیست شناسی دانشگاه آزاد اسلامی واحد شهرکرد
Keywords: mecA gene, Enterotoxins, Antimicrobial susceptibility patterns,
Abstract :
ABSTRACT Background: Staphylococcus epidermidis produces various types of extracellular protein toxins including staphylococcal enterotoxins that act as superantigens, and can provide conditions to attack host cells. The goal of the current study was to determine antibiotic resistance patterns, and detection of prevalent enterotoxin genes in MRSE strains containing the ACME-arcA gene in Isfahan. Methods: This survey was done, on a total of 150 staphylococcal isolates acquired from different nosocomial infections. MRSE strains isolated by the PCR procedure. The antimicrobial patterns of MRSE isolates were determined by the disk diffusion procedure. Finally, enterotoxin genes in MRSE strains containing the ACME-arcA gene were detected by using the PCR system. Results: Out of 150 clinical infections, 100 Staphylococcus epidermidis strains were isolated. Among 100 Staphylococcus epidermidis strains, 65 (65%) isolates were MRSE. Of these, 33 isolates (50.7%) had both mecA, and ACME-arcA genes. The antimicrobial patterns of MRSE isolates in this study showed that the MRSE isolates exhibited the highest rates of resistance to erythromycin (81.5%), and clindamycin (64.6%), while they showed the lowest resistance to rifampicin (7.6%), and linezolid (1.5%). Moreover, the frequency of enterotoxin genes sea, seb, sec, sed, see, seg, seh, and sei was reported 60.6%, 63.6%, 66.6%, 15.1%, 6%, 72.7%, 0%, and 75.7% respectively, in the isolates containing the mecA, and ACME-arcA genes.Conclusion: The variety of enterotoxin genes types, and resistance index among ACME-arcA encoding MRSE are causes for a public health concern; so rapid and accurate reporting of the presence of enterotoxin genes from hospital infections is essential.
References 1. Gordon RJ, Miragaia M, Weinberg AD, Lee CJ, Rolo J, Giacalone JC, et al. Staphylococcus epidermidis colonization is highly clonal across US cardiac centers.Int J Infect Dis. 2012;205(9):1391-8.doi: 10.1093/infdis/jis218. 2. Aghazadeh M, Ghotaslou R, Rezaee MA, Moshafi MH, Hojabri Z, Saffari F. Determination of antimicrobial resistance profile and inducible clindamycin resistance of coagulase negative staphylococci in pediatric patients: the first report from Iran. World J Pediatr. 2015;11(3):250-4.doi: 10.1007/s12519-014-0524-7.3. Halaji M, Karimi A, Shoaei P, Nahaei M, Khorvash F, Ataei B, et al. Distribution of SCCmec elements and presence of Panton-Valentine Leukocidin in Methicillin-Resistant Staphylococcus epidermidis isolated from clinical samples in a University Hospital of Isfahan City, Iran. J Clin Diagn Res. 2017;11(7):DC27. doi: 10.7860/JCDR/2017/25518.10258. 4. Lindgren J, Thomas VC, Olson M, Chaudhari S, Nuxoll AS, Schaeffer C, et al. Arginine deiminase in Staphylococcus epidermidis functions to augment biofilm maturation through pH homeostasis. J Bacteriol. 2014;196(12):2277-89. doi: 10.1128/JB.00051-14.5. Danesh M, Rahimi F, Arabestani MR. Antibiotic resistance pattern of Staphylococcus epidermidis strains isolated from a referral hospital in Isfahan. J Clin Infect Dis Trop Med. 2016; 20(71): 25-31.6.Wang PJ, Xie CB, Sun FH, Guo LJ, Dai M, Cheng X, Ma YX. Molecular characteristics of methicillin-resistant Staphylococcus epidermidis on the abdominal skin of females before laparotomy. Int J Mol Sci. 2016;17(6):992. doi: 10.3390/ijms17060992.7. Shamansouri S, Zadeh V, Khazaei M. Study on the percent of frequency of ACME-Arca in clinical isolates resistant to methicillin-Staphylococcus epidermidis in Isfahan, Iran. J Fundam Appl Sci. 2016;8(2):1046-57.http://dx.doi.org/10.4314/jfas.v8i2S.1198.Deplano A, Vandendriessche S, Nonhoff C, Dodémont M, Roisin S, Denis O. National surveillance of Staphylococcus epidermidis recovered from bloodstream infections in Belgian hospitals. J. Antimicrob. Chemother.2016;71(7):1815-9. doi: 10.1093/jac/dkw086. 9. Ertas N, Gonulalan Z, Yildirim Y, Kum E. Detection of Staphylococcus aureus enterotoxins in sheep cheese and dairy desserts by multiplex PCR technique.Int J Food Microbiol. 2010;142(1-2):74-7.doi: 10.1016/j.ijfoodmicro.2010.06.002.10. Fisher EL, Otto M, Cheung GY. Basis of virulence in enterotoxin-mediated staphylococcal food poisoning. Front Microbiol. 2018; 9: 436.doi: 10.3389/fmicb.2018.0043611. Karimi M, Esfahani BN, Halaji M, Mobasherizadeh S, Shahin M, Havaei SR, et al. Molecular characteristics and antibiotic resistance pattern of Staphylococcus aureus nasal carriage in tertiary care hospitals of Isfahan, Iran. Infez Med. 2017;25(3):234-40.[PubMed Central:PMID:28956540] 12. Oliveira D, Borges A, Simões M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. TOXINS. 2018;10(6):252. doi: 10.3390/toxins10060252.13. Janik E, Ceremuga M, Saluk-Bijak J, Bijak M. Biological toxins as the potential tools for bioterrorism.Int. J. Mol. Sci. 2019;20(5):1181. doi: 10.3390/ijms20051181.14. Tuffs S, Haeryfar S, McCormick J. Manipulation of innate and adaptive immunity by staphylococcal superantigens. Pathogens. 2018;7(2):53. doi: 10.3390/pathogens702005315. Clinical and Laboratory Standards Institute (CLSI). Performance standards for antimicrobial susceptibility testingTwenty-FourthEdition, M100Ed24E; 2014.16. Hoveida L, Ataei B, Amirmozafari N, Noormohammadi Z. Species Variety, Antibiotic Susceptibility Patterns and Prevalence of Enterotoxin Genes in Staphylococci Isolated from Foodstuff in Central Iran. Iranian Journal of Public Health. 2020 Jan;49(1):96.17. Adwan G, Adwan K, Jarrar N, Salama Y, Barakat A. Prevalence of seg, seh and sei Genes among Clinical and Nasal Staphylococcus aureus Isolates in Palestine. Br Microbiol Res J. 2013;3(2):139-49.doi: 10.9734/BMRJ/2013/291318. Du X, Zhu Y, Song Y, Li T, Luo T, Sun G, et al. Molecular analysis of Staphylococcus epidermidis strains isolated from community and hospital environments in China. PLoS One. 2013;8(5):e62742. doi: 10.1371/journal.pone.0062742.19.Razavi S, Dadashi M, Pormohammad A, Khoramrooz S S, Mirzaii M, et al. Methicillin-Resistant Staphylococcus epidermidisin Iran: A Systematic Review and Meta-Analysis, Arch Clin Infect Dis. 2018 ; 13(4):e58410. doi: 10.5812/archcid.58410.20. Ramazanzadeh R, Salimizand H, Shahbazi B, Narenji H. Prevalence of mecA Gene of Methicillin Resistant Staphylococcus spp. Isolated from Nosocomial Infections and Environmental Specimens in Sanandaj Hospitals, Kurdistan, Iran. Res Mol Med. 2015;3(3):38-42. doi: 10.7508/rmm.2015.03.008.21. Xu Z, Shah HN, Misra R, Chen J, Zhang W, Liu Y, et al. The prevalence, antibiotic resistance and mecA characterization of coagulase negative staphylococci recovered from non-healthcare settings in London, UK.Antimicrob Resist Infect Control. 2018;7(1):73. doi: 10.1186/s13756-018-0367-4.22. Rahimi F, Bouzari M, Katouli M, Pourshafie M R. Antibiotic Resistance Pattern of Methicillin Resistant and Methicillin Sensitive Staphylococcus aureus Isolates in Tehran, Iran, Jundishapur J Microbiol. 2013 ; 6(2):144-149. doi: 10.5812/jjm.4896. 23. Shoja S, Nahaei MR, Nahaei M, Farajnia S, AHANGARZADEH RM, Nikvash S. Study of methicillin-resistance by oxacillin disc diffusion and pcr methods in Staphylococcus epidermidis isalates collected from blood cultures and their antibiotic susceptibility.Med J Tabriz Univ Med Sci. 2009; 31(1):39-44.24. Nourbakhsh, F. H. Momtaz. An investigation of antibiotic resistance pattern in the strains of methicillin-resistant Staphylococcus epidermidis isolated from clinical samples in Iisfahan province, Iran.Qom Univ Med Sci J. 2016;10(6):68-74. 25. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA, et al. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis. 2008;197(11):1523-30. doi: 10.1086/587907.26. Granslo HN, Klingenberg C, Fredheim EG, Rønnestad A, Mollnes TE, Flægstad T. Arginine catabolic mobile element is associated with low antibiotic resistance and low pathogenicity in Staphylococcus epidermidis from neonates.Pediatr Res. 2010;68(3):237. doi: 10.1203/00006450-201011001-00463.27. Miragaia M, de Lencastre H, Perdreau-Remington F, Chambers HF, Higashi J, Sullam PM, et al. Genetic diversity of arginine catabolic mobile element in Staphylococcus epidermidis. PLoS One. 2009;4(11):e7722. doi: 10.1371/journal.pone.000772228. Pereira VC, Pinheiro L, Oliveira A, Martins KB, Riboli DFM, de Souza MdLR. Expression of superantigens and the agr system in Staphylococcus epidermidis. Microb Pathog. 2018;115:19-24. doi: 10.1016/j.micpath.2017.11.008.29. Rosenthal ME, Dever LL, Moucha CS, Chavda KD, Otto M, Kreiswirth BN. Molecular characterization of an early invasive Staphylococcus epidermidis prosthetic joint infection.MICROB DRUG RESIST. 2011;17(3):345-50. doi: 10.1089/mdr.2010.0157. 30. Vasconcelos N, Pereira V, Júnior JA, da Cunha MdL. Molecular detection of enterotoxins E, G, H and I in Staphylococcus aureus and coagulase‐negative staphylococci isolated from clinical samples of newborns in Brazil. J APPL MICROBIOL. 2011;111(3):749-62. doi: 10.1111/j.1365-2672.2011.05076.x31. Pinheiro L, Brito C, de Oliveira A, Martins P, Pereira V, da Cunha M. Staphylococcus epidermidis and Staphylococcus haemolyticus: molecular detection of cytotoxin and enterotoxin genes. TOXINS. 2015;7(9):3688-99. doi: 10.3390/toxins709368832. Alfatemi SM, Motamedifar M, Hadi N, Saraie HS. Analysis of virulence genes among methicillin resistant Staphylococcus aureus (MRSA) strains. Jundishapur journal of microbiology. 2014;7(6).33. Mehrabi F, Asgari A. Resistant Strains of Enterotoxigenic Staphylococcus aureus; Unknown Risk for Multiple Sclerosis Exacerbation. Iranian Red Crescent Medical Journal. 2015;17(9).
