High frequency of exfoliative toxin genes among Staphylococcus aureus isolated from clinical specimens in the north of Iran: Alarm for the health of individuals under risk
AbstractBackground and Objectives: Exfoliative toxins (ETs) of Staphylococcus aureus are the main reason of scalded skin syndrome in infants and young children. The aim of this study was to investigate the prevalence of eta, etb and etd genes in S. aureus. Materials and Methods: A total of 150 S. aureus isolates were collected from clinical specimens during the years 2014 to 2016 in the north of Iran. After confirmation of the species using standard diagnostic procedures, polymerase chain reaction was used for detection of the eta, etb and etd genes among the isolates. Results: Overall, 131 (87.3%) isolates were positive for at least one of the ET genes; 115 (76.7%), 25 (16.7%) and 81 (54%) of the isolates carried the eta, etb and etd genes, respectively. Although eta and etd genes were present in all types of clinical samples, etb was found only in the wound, synovial fluid, sputum and tracheal aspirate. Overall, 7 toxin genotypes were observed, among which the genotypes eta-etd, eta and eta-etb-etd predominated at rates of 35.3%, 26.7% and 9.3%, respectively. Conclusion: Detection of the high rate of prevalence of ET genes in the current study is considered as a serious problem because it is likely to spread and transfer these genes between strains. Furthermore, these isolates circulating in the community, particularly from infants, old people and immunocompromised patients, are important health-wise.
Nishifuji K, Sugai M, Amagai M. Staphylococcal exfoliative toxins: “Molecular scissors” of bacteria that attack the cutaneous defense barrier in mammals. J Dermatol Sci 2008; 49:21-31.
Ladhani S. Recent developments in staphylococcal scalded skin syndrome. Clin Microbiol Infect 2001; 7:301-307.
de Azavedo JCS, Bailey CJ, Arbuthnott JP (1988). Purification of epidermolytic toxin of Staphylococcus aureus. In: Methods in Enzymology. Vol 165, Academic Press, pp. 32-36.
Holochová P, Růzicková V, Pantůcek R, Petrás P, Janisch R, Doskar J. Genomic diversity of two lineages of exfoliative toxin A-converting phages predominating in Staphylococcus aureus strains in the Czech Republic. Res Microbiol 2010; 161:260-267.
Sakurai S, Suzuki H, Machida K. Rapid identification by polymerase chain reaction of Staphylococcal exfoliative toxin serotype A and B genes. Microbiol Immunol 1995; 39:379-386.
Bukowski M, Wladyka B, Dubin G. Exfoliative Toxins of Staphylococcus aureus. Toxins (Basel) 2010; 2:1148-1165.
Yamasaki O, Tristan A, Yamaguchi T, Sugai M, Lina G, Bes M, et al. Distribution of the exfoliative toxin D gene in clinical Staphylococcus aureus isolates in France. Clin Microbiol Infect 2006; 12:585-588.
Ladhani S. Understanding the mechanism of action of the exfoliative toxins of Staphylococcus aureus. FEMS Immunol Med Microbiol 2003; 39:181-189.
Rifai S, Barbancon V, Prevost G, Piemont Y. Synthetic exfoliative toxin A and B DNA probes for detection of toxigenic Staphylococcus aureus strains. J Clin Microbiol 1989; 27:504-506.
Růžičková V, Voller J, Pantůček R, Petráš P, Doškař J. Multiplex PCR for detection of three exfoliative toxin serotype genes in Staphylococcus aureus. Folia Microbiol (Praha) 2005; 50:499-502.
Wang S-J, Chow L-W, Wu M-J. Multiplex PCR for the simultaneous detection of the SEA, SEB, SEC, SED and SEE genes of enterotoxigenic Staphylococcus aureus. J Food Drug Anal 2002; 10:164-169.
Mohseni M, Abbaszadeh J, Nasrollahi Omran A. Radiation resistant of native Deinococcus spp. isolated from the Lout desert of Iran "the hottest place on Earth". Int J Environ Sci Tec 2014; 11:1939-1946.
Koosha RZ, Fooladi AAI, Hosseini HM, Aghdam EM. Prevalence of exfoliative toxin A and B genes in Staphylococcus aureus isolated from clinical specimens. J Infect Public Health 2014; 7:177-185.
Xia G, Wolz C. Phages of Staphylococcus aureus and their impact on host evolution. Infect Genet Evol 2014; 21:593-601.
Jiménez JN, Ocampo AM, Vanegas JM, Rodríguez EA, Garcés CG, Patiño LA, et al. Characterisation of virulence genes in methicillin susceptible and resistant Staphylococcus aureus isolates from a paediatric population in a university hospital of Medellín, Colombia. Mem Inst Oswaldo Cruz 2011; 106:980-985.
Becker K, Friedrich AW, Lubritz G, Weilert M, Peters G, von Eiff C. Prevalence of genes encoding pyrogenic toxin superantigens and exfoliative toxins among strains of Staphylococcus aureus isolated from blood and nasal specimens. J Clin Microbiol 2003; 41:1434-1439.
Kolawole DO, Adeyanju A, Schaumburg F, Akinyoola AL, Lawal OO, Amusa YB, et al. Characterization of colonizing Staphylococcus aureus isolated from surgical wards' patients in a Nigerian university hospital. PLoS One 2013; 8:e68721.
Liu M, Liu J, Guo Y, Zhang Z. Characterization of virulence factors and genetic background of Staphylococcus aureus isolated from Peking University people’s hospital between 2005 and 2009. Curr Microbiol 2010; 61:435-443.
Mehrotra M, Wang G, Johnson WM. Multiplex PCR for detection of genes for Staphylococcus aureus enterotoxins, exfoliative toxins, toxic shock syndrome toxin 1, and methicillin resistance. J Clin Microbiol 2000; 38:1032-1035.
van Trijp MJCA, Melles DC, Snijders SV, Wertheim HFL, Verbrugh HA, van Belkum A, et al. Genotypes, superantigen gene profiles, and presence of exfoliative toxin genes in clinical methicillin-susceptible Staphylococcus aureus isolates. Diagn Microbiol Infect Dis 2010; 66:222-224.
Wu D, Li X, Yang Y, Zheng Y, Wang C, Deng L, et al. Superantigen gene profiles and presence of exfoliative toxin genes in community-acquired meticillin-resistant Staphylococcus aureus isolated from Chinese children. J Med Microbiol 2011; 60:35-45.
Fenner L, Widmer AF, Frei R. Molecular epidemiology of invasive methicillin-susceptible Staphylococcus aureus strains circulating at a Swiss university hospital. Eur J Clin Microbiol Infect Dis 2008; 27:623-626.
Peacock SJ, Moore CE, Justice A, Kantzanou M, Story L, Mackie K, et al. Virulent combinations of adhesin and toxin genes in natural populations of Staphylococcus aureus. Infect Immun 2002; 70:4987-4996.
Demir C, ASLANTAŞ Ö, Duran N, Ocak S, ÖZER B. Investigation of toxin genes in Staphylococcus aureus strains isolated in Mustafa Kemal university hospital. Turk J Med Sci 2011; 41:343-352.
Holtfreter S, Grumann D, Schmudde M, Nguyen HTT, Eichler P, Strommenger B, et al. Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 2007; 45:2669-2680.
Abbasi S, Zamanzad B. Prevalence of virulence genes etA, etB in community acquired methicillin-resistant Staphylococcus aureus in patients referred to teaching hospital by PCR in Shahrekord, 2014. J Arak Uni Med Sci 2015; 18:42-50.
Asadollahi P, Delpisheh A, Hossein Maleki M, Azizi Jalilian F, Alikhani MY, Asadollahi K, et al. Enterotoxin and exfoliative toxin genes among methicillin-resistant Staphylococcus aureus isolates recovered from Ilam, Iran. Avicenna J Clin Microb Infec 2014; 1:e20208.
Hoseini-Alfatemi SM, Motamedifar M, Hadi N, Saraie HSE. Analysis of virulence genes among methicillin resistant Staphylococcus aureus (MRSA) strains. Jundishapur J Microbiol 2014; 7:e10741.
Japoni-Nejad A, Rezazadeh M, Kazemian H, Fardmousavi N, van Belkum A, Ghaznavi-Rad E. Molecular characterization of the first community-acquired methicillin-resistant Staphylococcus aureus strains from central Iran. Int J Infect Dis 2013; 17:e949-954.
Sabouni F, Mahmoudi S, Bahador A, Pourakbari B, Hosseinpour-Sadeghi R, Haghi-Ashtiani M-T, et al. Virulence factors of Staphylococcus aureus isolates in an Iranian referral children's hospital. Osong Public Health Res Perspect 2014; 5:96-100.
Yamaguchi T, Nishifuji K, Sasaki M, Fudaba Y, Aepfelbacher M, Takata T, et al. Identification of the Staphylococcus aureus etd pathogenicity island which encodes a novel exfoliative toxin, ETD, and EDIN-B. Infect Immun 2002; 70:5835-5845.