Molecular Epidemiology and Recycling of Staphylococcus aureus Resistant
to Methicillin Among the Staff, Patients, and Surfaces in University Hospital
in West Iran, Ilam

Fatemeh      Ghanbari; Heshmatollah      Nourmoradi; Ali      Nazari; Nourkhoda      Sadeghifard; Iraj      Pakzad; Setareh      Soroush; Behnam      Ashrafi; Morovat      Taherikalani

Abstract

Background: Staphylococcus aureus is a human pathogen causing nosocomial infections and increased hospitalization and mortality among human communities. Methicillin-resistant S. aureus strains are considered a severe threat in nosocomial infections and cause complications in the remedy process of bacterial infections. In this study, 137 samples were collected from different departments, staff, and patients in Ilam hospital.

Methods: Eighty-eight samples of these strains were examined to test antibiotic resistance and diffusion. MIC (minimum inhibitory concentration) and PCR (polymerase chain reaction) were performed on the samples resistant to oxacillin. 36 (40.9%) strains were MRSA, and 52 (59.1%) isolates were MSSA. 44.4% of MRSA strains with IV SCCmec type.

Results: Fourteen different spa types were found using spa typing, of which the most abundant types were t037, t030, and t701, and three new types, including t15471, t15474, and t17470, were identified among the strains. The molecular analysis by MLST showed that the strains are classified into 11 different sequence types. Sequence type 239 and clonal complexes of 329 and 22 were dominant. ST239- spat037-SCCmec III was also identified as the most frequent clone of MRSA. The most identified clones were MRSA ST239-spa t037-SCCmec III.

Conclusion: The results show the spa-type distribution between samples of patients, personnel, and surfaces, demonstrating MRSA circulation between patients and the environment. The results show the need to control environmental health.

Keywords: SCCmec MLST typing, spa typing, MRSA, S. aureus, nosocomial infections, MSSA.

Graphical Abstract

[1]
Hamilton SM, Alexander JAN, Choo EJ, et al. High-level resistance of Staphylococcus aureus to β-lactam antibiotics mediated by Penicillin-Binding Protein 4 (PBP4). Antimicrob Agents Chemother  2017; 61(6): e02727-16.
 [http://dx.doi.org/10.1128/AAC.02727-16] [PMID:  28373193]

[2]
Chambers HF, DeLeo FR. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol  2009; 7(9): 629-41.
 [http://dx.doi.org/10.1038/nrmicro2200] [PMID:  19680247]

[3]
Wang JT, Chen YC, Yang TL, Chang SC. Molecular epidemiology and antimicrobial susceptibility of methicillin-resistant Staphylococcus aureus in Taiwan. Diagn Microbiol Infect Dis  2002; 42(3): 199-203.
 [http://dx.doi.org/10.1016/S0732-8893(01)00351-0] [PMID:  11929692]

[4]
Aires de Sousa M. Crisóstomo MI, Santos Sanches I, et al. Frequent recovery of a single clonal type of multidrug-resistant Staphylococcus aureus from patients in two hospitals in Taiwan and China. J Clin Microbiol  2003; 41(1): 159-63.
 [http://dx.doi.org/10.1128/JCM.41.1.159-163.2003] [PMID:  12517842]

[5]
Rahbar M, Yaghoobi M, Fattahi A. Comparison of different laboratory methods for detection of methicillin resistant Staphylococcus aureus. Pak J Med Sci  2006; 22: 442-5.

[6]
Sabath LD, Wallace SJ. The problems of drug-resistant pathogenic bacteria. Factors influencing methicillin resistance in Staphylococci. Ann N Y Acad Sci  1971; 182(1 The Problems): 258-66.
 [http://dx.doi.org/10.1111/j.1749-6632.1971.tb30662.x] [PMID: 5285290]

[7]
Hartman BJ, Tomasz A. Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus. J Bacteriol  1984; 158(2): 513-6.
 [http://dx.doi.org/10.1128/jb.158.2.513-516.1984] [PMID:  6563036]

[8]
Ito T, Katayama Y, Hiramatsu K. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother  1999; 43(6): 1449-58.
 [http://dx.doi.org/10.1128/AAC.43.6.1449] [PMID:  10348769]

[9]
Chang FY, MacDonald BB, Peacock JE Jr, et al. A prospective multicenter study of Staphylococcus aureus bacteremia: incidence of endocarditis, risk factors for mortality, and clinical impact of methicillin resistance. Medicine (Baltimore)  2003; 82(5): 322-32.
 [http://dx.doi.org/10.1097/01.md.0000091185.93122.40] [PMID:  14530781]

[10]
Llarrull LI, Fisher JF, Mobashery S. Molecular basis and phenotype of methicillin resistance in Staphylococcus aureus and insights into new β-lactams that meet the challenge. Antimicrob Agents Chemother  2009; 53(10): 4051-63.
 [http://dx.doi.org/10.1128/AAC.00084-09] [PMID:  19470504]

[11]
Pozzi C, Waters EM, Rudkin JK, et al. Methicillin resistance alters the biofilm phenotype and attenuates virulence in Staphylococcus aureus device-associated infections. PLoS Pathog  2012; 8(4): e1002626.
 [http://dx.doi.org/10.1371/journal.ppat.1002626] [PMID:  22496652]

[12]
Rudkin JK, Laabei M, Edwards AM, et al. Oxacillin alters the toxin expression profile of community-associated methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother  2014; 58(2): 1100-7.
 [http://dx.doi.org/10.1128/AAC.01618-13] [PMID:  24295979]

[13]
de Lencastre H, Oliveira D, Tomasz A. Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power. Curr Opin Microbiol  2007; 10(5): 428-35.
 [http://dx.doi.org/10.1016/j.mib.2007.08.003] [PMID:  17921044]

[14]
Oliveira DC, Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother  2002; 46(7): 2155-61.
 [http://dx.doi.org/10.1128/AAC.46.7.2155-2161.2002] [PMID:  12069968]

[15]
Zhang K, McClure JA, 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. J Clin Microbiol  2005; 43(10): 5026-33.
 [http://dx.doi.org/10.1128/JCM.43.10.5026-5033.2005] [PMID:  16207957]

[16]
Chongtrakool P, Ito T, Ma XX, et al. Staphylococcal cassette chromosome mec (SCCmec) typing of methicillin-resistant Staphylococcus aureus strains isolated in 11 Asian countries: a proposal for a new nomenclature for SCCmec elements. Antimicrob Agents Chemother  2006; 50(3): 1001-12.
 [http://dx.doi.org/10.1128/AAC.50.3.1001-1012.2006] [PMID:  16495263]

[17]
Oie S, Suenaga S, Sawa A, Kamiya A. Association between isolation sites of methicillin-resistant Staphylococcus aureus (MRSA) in patients with MRSA-positive body sites and MRSA contamination in their surrounding environmental surfaces. Jpn J Infect Dis  2007; 60(6): 367-9.
 [PMID:  18032836]

[18]
Hoseinzadeh E, Samarghandie MR, Ghiasian SA, Alikhani MY, Roshanaie G. Evaluation of bioaerosols in five educational hospitals wards air in Hamedan, During 2011-2012. Jundishapur J Microbiol  2013; 6(6): 6.
 [http://dx.doi.org/10.5812/jjm.10704]

[19]
Choobineh A, Rostami R, Tabatabaei SH.  Assessment of bioaerosols types and concentration in ambient air of Shiraz University of Medical Sciences Educational Hospitals, 2008. Iran Occupat Health 2009; 6(2).

[20]
Okhuoya J, Okaraedge S. Microflora of road side air and leaf surfaces of selected vegetables. Nigerian J Pure Appl Am Sci  1992; 12: 42-8.

[21]
 CLSI. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. 11th ed. CLSI standard M07. Wayne, PA: Clinical and Laboratory Standards Institute; 2018. Available from: https://clsi.org/media/1928/m07ed11_sample.pdf

[22]
Kateete DP, Namazzi S, Okee M, et al. High prevalence of methicillin resistant Staphylococcus aureus in the surgical units of Mulago hospital in Kampala, Uganda. BMC Res Notes  2011; 4(1): 326.
 [http://dx.doi.org/10.1186/1756-0500-4-326] [PMID:  21899769]

[23]
Okuma K, Iwakawa K, Turnidge JD, et al. Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J Clin Microbiol  2002; 40(11): 4289-94.
 [http://dx.doi.org/10.1128/JCM.40.11.4289-4294.2002] [PMID:  12409412]

[24]
Khalili MB, Sharifi-Yazdi MK, Dargahi H, Sadeghian HA. Nasal colonization rate of Staphylococcus aureus strains among health care service employee’s of teaching university hospitals in Yazd 2009.

[25]
Dumford DM III, Nerandzic MM, Eckstein BC, Donskey CJ. What is on that keyboard? Detecting hidden environmental reservoirs of Clostridium difficile during an outbreak associated with North American pulsed-field gel electrophoresis type 1 strains. Am J Infect Control  2009; 37(1): 15-9.
 [http://dx.doi.org/10.1016/j.ajic.2008.07.009] [PMID:  19171247]

[26]
Hill RLR, Duckworth GJ, Casewell MW. Elimination of nasal carriage of methicillin-resistant Staphylococcus aureus with mupirocin during a hospital outbreak. J Antimicrob Chemother  1988; 22(3): 377-84.
 [http://dx.doi.org/10.1093/jac/22.3.377] [PMID:  3141347]

[27]
Azimian A, Havaei SA, Fazeli H, et al. Genetic characterization of a vancomycin-resistant Staphylococcus aureus isolate from the respiratory tract of a patient in a university hospital in northeastern Iran. J Clin Microbiol  2012; 50(11): 3581-5.
 [http://dx.doi.org/10.1128/JCM.01727-12] [PMID:  22933598]

[28]
Mohammadi S, Sekawi Z, Monjezi A, et al. Emergence of SCCmec type III with variable antimicrobial resistance profiles and spa types among methicillin-resistant Staphylococcus aureus isolated from healthcare- and community-acquired infections in the west of Iran. Int J Infect Dis  2014; 25: 152-8.
 [http://dx.doi.org/10.1016/j.ijid.2014.02.018] [PMID:  24909489]

[29]
Felten A, Grandry B, Lagrange PH, Casin I. Evaluation of three techniques for detection of low-level methicillin-resistant Staphylococcus aureus (MRSA): A disk diffusion method with cefoxitin and moxalactam, the Vitek 2 system, and the MRSA-screen latex agglutination test. J Clin Microbiol  2002; 40(8): 2766-71.
 [http://dx.doi.org/10.1128/JCM.40.8.2766-2771.2002] [PMID:  12149327]

[30]
Kampf G, Adena S, Rüden H, Weist K. Inducibility and potential role of MecA-gene-positive oxacillin-susceptible Staphylococcus aureus from colonized healthcare workers as a source for nosocomial infections. J Hosp Infect  2003; 54(2): 124-9.
 [http://dx.doi.org/10.1016/S0195-6701(03)00119-1] [PMID:  12818586]

[31]
Nikbakht M, Nahaei M, Akhi M, Asgharzadeh M, Nikvash S. Nasal carriage rate of Staphylococcus aureus in hospital personnel and inpatients and antibiotic resistance pattern of isolated strains from nasal and clinical specimens in tabriz 2007.

[32]
Shahsavan S, Jabalameli L, Maleknejad P, et al. Molecular analysis and antimicrobial susceptibility of methicillin resistant Staphylococcus aureus in one of the hospitals of Tehran University of Medical Sciences: High prevalence of sequence type 239 (ST239) clone. Acta Microbiol Immunol Hung  2011; 58(1): 31-9.
 [http://dx.doi.org/10.1556/amicr.58.2011.1.4] [PMID:  21450553]

[33]
Xu BL, Zhang G, Ye HF, et al. Predominance of the Hungarian clone (ST 239-III) among hospital-acquired meticillin-resistant Staphylococcus aureus isolates recovered throughout mainland China. J Hosp Infect  2009; 71(3): 245-55.
 [http://dx.doi.org/10.1016/j.jhin.2008.10.029] [PMID:  19157644]

[34]
Feil EJ, Nickerson EK, Chantratita N, et al. Rapid detection of the pandemic methicillin-resistant Staphylococcus aureus clone ST 239, a dominant strain in Asian hospitals. J Clin Microbiol  2008; 46(4): 1520-2.
 [http://dx.doi.org/10.1128/JCM.02238-07] [PMID:  18234867]

[35]
Song JH, Hsueh PR, Chung DR, et al. Spread of methicillin-resistant Staphylococcus aureus between the community and the hospitals in Asian countries: an ANSORP study. J Antimicrob Chemother  2011; 66(5): 1061-9.
 [http://dx.doi.org/10.1093/jac/dkr024] [PMID:  21393157]

[36]
Shibuya Y, Hara M, Higuchi W, Takano T, Iwao Y, Yamamoto T. Emergence of the community-acquired methicillin-resistant Staphylococcus aureus USA300 clone in Japan. J Infect Chemother  2008; 14(6): 439-41.
 [http://dx.doi.org/10.1007/s10156-008-0640-1] [PMID:  19089559]

[37]
Park C, Lee D-G, Choi S-M, et al. A case of perianal abscess due to Panton-Valentine leukocidin positive community-associated methicillin-resistant Staphylococcus aureus: report in Korea and literature review from the Far East Infect and Chemo  2008; 40: 121-6.

[38]
Hsu LY, Tristan A, Koh TH, et al. Community associated methicillin-resistant Staphylococcus aureus, Singapore. Emerg Infect Dis  2005; 11(2): 341-2.
 [http://dx.doi.org/10.3201/eid1102.040782] [PMID:  15759335]

[39]
Ahmad N, Ruzan IN, Abd Ghani MK, et al. Characteristics of community- and hospital-acquired meticillin-resistant Staphylococcus aureus strains carrying SCCmec type IV isolated in Malaysia. J Med Microbiol  2009; 58(9): 1213-8.
 [http://dx.doi.org/10.1099/jmm.0.011353-0] [PMID:  19528158]

[40]
Kinnevey PM, Shore AC, Brennan GI, et al. Extensive genetic diversity identified among sporadic methicillin-resistant Staphylococcus aureus isolates recovered in Irish hospitals between 2000 and 2012. Antimicrob Agents Chemother  2014; 58(4): 1907-17.
 [http://dx.doi.org/10.1128/AAC.02653-13] [PMID:  24395241]

[41]
Goudarzi M, Fazeli M, Goudarzi H, Azad M, Seyedjavadi SS. Spa typing of Staphylococcus aureus strains isolated from clinical specimens of patients with nosocomial infections in Tehran, Iran. Jundishapur J Microbiol  2016; 9(7): e35685.
 [http://dx.doi.org/10.5812/jjm.35685] [PMID:  27679706]

[42]
Liu Y, Wang H, Du N, et al. Molecular evidence for spread of two major methicillin-resistant Staphylococcus aureus clones with a unique geographic distribution in Chinese hospitals. Antimicrob Agents Chemother  2009; 53(2): 512-8.
 [http://dx.doi.org/10.1128/AAC.00804-08] [PMID:  19029328]

[43]
Mirzaii M, Emaneini M, Jabalameli F, Halimi S, Taherikalani M. Molecular investigation of Staphylococcus aureus isolated from the patients, personnel, air and environment of an ICU in a hospital in Tehran. J Infect Public Health  2015; 8(2): 202-6.
 [http://dx.doi.org/10.1016/j.jiph.2014.09.002] [PMID:  25458916]

[44]
Neela V, Ghasemzadeh Moghaddam H, van Belkum A, Horst-Kreft D, Mariana NS, Ghaznavi Rad E. First report on methicillin-resistant Staphylococcus aureus of Spa type T037, Sequence type 239, SCCmec type III/IIIA in Malaysia. Eur J Clin Microbiol Infect Dis  2010; 29(1): 115-7.
 [http://dx.doi.org/10.1007/s10096-009-0813-6] [PMID:  19779745]

[45]
Song Y, Du X, Li T, Zhu Y, Li M. Phenotypic and molecular characterization of Staphylococcus aureus recovered from different clinical specimens of inpatients at a teaching hospital in Shanghai between 2005 and 2010. J Med Microbiol  2013; 62(2): 274-82.
 [http://dx.doi.org/10.1099/jmm.0.050971-0] [PMID:  23118474]

[46]
Shang W, Hu Q, Yuan W, et al. Comparative fitness and determinants for the characteristic drug resistance of ST239-MRSA-III-t030 and ST239-MRSA-III-t037 strains isolated in China. Microb Drug Resist  2016; 22(3): 185-92.
 [http://dx.doi.org/10.1089/mdr.2015.0226] [PMID:  26565599]

[47]
Faria NA, Oliveira DC, Westh H, et al. Epidemiology of emerging methicillin-resistant Staphylococcus aureus (MRSA) in Denmark: a nationwide study in a country with low prevalence of MRSA infection. J Clin Microbiol  2005; 43(4): 1836-42.
 [http://dx.doi.org/10.1128/JCM.43.4.1836-1842.2005] [PMID:  15815005]

[48]
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(11): e949-54.
 [http://dx.doi.org/10.1016/j.ijid.2013.03.023] [PMID: 23706379]

[49]
Kinnevey PM, Shore AC, Mac Aogáin M, et al. Enhanced tracking of the nosocomial transmission of endemic ST22-MRSA-IV among patients and environmental sites using whole-genome sequencing. J Clin Microbiol  2016; 54(2): 445-8.

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DOI https://dx.doi.org/10.2174/1871526522666220928145550	Print ISSN 1871-5265
Publisher Name Bentham Science Publisher	Online ISSN 2212-3989

Infectious Disorders - Drug Targets

Molecular Epidemiology and Recycling of Staphylococcus aureus Resistant to Methicillin Among the Staff, Patients, and Surfaces in University Hospital in West Iran, Ilam

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