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Published in: Antimicrobial Resistance & Infection Control 1/2017

Open Access 01-12-2017 | Research

Hospital clones of methicillin-resistant Staphylococcus aureus are carried by medical students even before healthcare exposure

Authors: Ido Orlin, Assaf Rokney, Avi Onn, Daniel Glikman, Avi Peretz

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2017

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Abstract

Background

Methicillin-resistant Staphylococcus aureus (MRSA) strains are prevalent in healthcare and the community. Few studies have examined MRSA carriage among medical students.
The aim of this study is to examine Staphylococcus aureus (SA) carriage, and particular MRSA, over time in cohort medical students

Methods

Prospective collection of nasal swabs from medical students in Israel and assessment of SA carriage. Three samples were taken per student in preclinical and clinical parts of studies. Antibiotic susceptibilities were recorded and MRSA typing was performed by staphylococcal cassette chromosome mec (SCCmec) types, Panton Valentine Leukocidin (PVL) encoding genes, and spa types. Clonality was assessed by pulsed-field gel electrophoresis.

Results

Among 58 students, SA carriage rates increased from 33% to 38% to 41% at baseline (preclinical studies), 13 and 19 months (clinical studies), respectively (p = 0.07). Methicillin-susceptible SA (MSSA) carriage increased in the clinical studies period (22 to 41%, p = 0.01). Overall, seven students (12%) carried 13 MRSA isolates. MRSA isolates were PVL negative and were characterized as SCCmecII-t002, SCCmecIV-t032, or t12435 with untypable SCCmec. MRSA carriage during the pre-clinical studies was evident in 4/7 students. Two students carried different MRSA clones at various times and persistent MRSA carriage was noted in one student. Simultaneous carriage of MRSA and MSSA was not detected.

Conclusions

MSSA carriage increased during the clinical part of studies in Israeli medical students. Compared with previous reports, higher rates of MRSA carriage were evident. MRSA strains were genotypically similar to Israeli healthcare-associated clones; however, carriage occurred largely before healthcare exposure, implying community-acquisition of hospital strains.
Literature
1.
go back to reference David M, Daum R. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23(3):616–87.CrossRefPubMedPubMedCentral David M, Daum R. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23(3):616–87.CrossRefPubMedPubMedCentral
2.
go back to reference David M, Glikman D, Crawford S, et al. What is community-associated methicillin-resistant Staphylococcus aureus? J Infect Dis. 2008;197(9):1235–43.CrossRefPubMed David M, Glikman D, Crawford S, et al. What is community-associated methicillin-resistant Staphylococcus aureus? J Infect Dis. 2008;197(9):1235–43.CrossRefPubMed
3.
go back to reference Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10(3):505–20.PubMedPubMedCentral Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10(3):505–20.PubMedPubMedCentral
4.
go back to reference Glick S, Samson D, Huang E, et al. Screening for methicillin-resistant Staphylococcus aureus: A comparative effectiveness review. Am J Infect Control. 2014;42:148–55.CrossRefPubMed Glick S, Samson D, Huang E, et al. Screening for methicillin-resistant Staphylococcus aureus: A comparative effectiveness review. Am J Infect Control. 2014;42:148–55.CrossRefPubMed
5.
go back to reference Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis. 2008;197(9):1226–34.CrossRefPubMed Gorwitz RJ, Kruszon-Moran D, McAllister SK, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis. 2008;197(9):1226–34.CrossRefPubMed
6.
go back to reference Dulon M, Peters C, Schablon A, et al. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect Dis. 2014;14:363.CrossRefPubMedPubMedCentral Dulon M, Peters C, Schablon A, et al. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect Dis. 2014;14:363.CrossRefPubMedPubMedCentral
7.
go back to reference Stubbs E, Pegler M, Vickery A, Harbour C. Nasal carriage of Staphylococcus aureus in Australian (pre-clinical and clinical) medical students. J Hosp Infect. 1994;27(2):127–34.CrossRefPubMed Stubbs E, Pegler M, Vickery A, Harbour C. Nasal carriage of Staphylococcus aureus in Australian (pre-clinical and clinical) medical students. J Hosp Infect. 1994;27(2):127–34.CrossRefPubMed
8.
go back to reference Berthelot P, Grattard F, Fascia P, et al. Is nasal carriage of methicillin-resistant Staphylococcus aureus more prevalent among student healthcare workers? Infect Control Hosp Epidemiol. 2004;25:364–5.CrossRefPubMed Berthelot P, Grattard F, Fascia P, et al. Is nasal carriage of methicillin-resistant Staphylococcus aureus more prevalent among student healthcare workers? Infect Control Hosp Epidemiol. 2004;25:364–5.CrossRefPubMed
9.
go back to reference Güçlü E, Yavuz T, Tokmak A, et al. Nasal carriage of pathogenic bacteria in medical students: effects of clinic exposure on prevalence and antibiotic susceptibility. Eur Arch Otorhinolaryngol. 2007;264:85–8.CrossRefPubMed Güçlü E, Yavuz T, Tokmak A, et al. Nasal carriage of pathogenic bacteria in medical students: effects of clinic exposure on prevalence and antibiotic susceptibility. Eur Arch Otorhinolaryngol. 2007;264:85–8.CrossRefPubMed
10.
go back to reference Higuchi W, Isobe H, Iwao Y, et al. Extensive multidrug resistance of coagulase-negative staphylococci in medical students. J Infect Chemother. 2007;13:63–6.CrossRefPubMed Higuchi W, Isobe H, Iwao Y, et al. Extensive multidrug resistance of coagulase-negative staphylococci in medical students. J Infect Chemother. 2007;13:63–6.CrossRefPubMed
11.
go back to reference Adesida S, Abioye O, Bamiro B, et al. Associated risk factors and pulsed field gel electrophoresis of nasal isolates of Staphylococcus aureus from medical students in a tertiary hospital in Lagos, Nigeria. Braz J Infect Dis. 2007;11:63–9.CrossRefPubMed Adesida S, Abioye O, Bamiro B, et al. Associated risk factors and pulsed field gel electrophoresis of nasal isolates of Staphylococcus aureus from medical students in a tertiary hospital in Lagos, Nigeria. Braz J Infect Dis. 2007;11:63–9.CrossRefPubMed
12.
go back to reference Baliga S, Bansil R, Suchitra U, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus in medical students. J Hosp Infect. 2008;68:91–2.CrossRefPubMed Baliga S, Bansil R, Suchitra U, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus in medical students. J Hosp Infect. 2008;68:91–2.CrossRefPubMed
13.
go back to reference Slifka J, Nettleman M, Dybas L, et al. Is acquisition of methicillin-resistant Staphylococcus aureus an occupational hazard for medical students? Clin Infect Dis. 2009;49:482–3.CrossRefPubMed Slifka J, Nettleman M, Dybas L, et al. Is acquisition of methicillin-resistant Staphylococcus aureus an occupational hazard for medical students? Clin Infect Dis. 2009;49:482–3.CrossRefPubMed
14.
go back to reference Ma X, Sun D, Wang S, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus among preclinical medical students: epidemiologic and molecular characteristics of methicillin-resistant S. aureus clones. Diagn Microbiol Infect Dis. 2011;70:22–30.CrossRefPubMed Ma X, Sun D, Wang S, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus among preclinical medical students: epidemiologic and molecular characteristics of methicillin-resistant S. aureus clones. Diagn Microbiol Infect Dis. 2011;70:22–30.CrossRefPubMed
15.
go back to reference Roberts C, Soge O, Horst A, et al. Methicillin-resistant Staphylococcus aureus from dental school clinic surfaces and students. Am J Infect Control. 2011;39:628–32.CrossRefPubMed Roberts C, Soge O, Horst A, et al. Methicillin-resistant Staphylococcus aureus from dental school clinic surfaces and students. Am J Infect Control. 2011;39:628–32.CrossRefPubMed
16.
go back to reference Chamberlain R, Singh K. Prevalence of methicillin resistant Staphylococcus aureus in nasal samples from preclinical second-year medical students. Mo Med. 2011;108(5):373–6.PubMed Chamberlain R, Singh K. Prevalence of methicillin resistant Staphylococcus aureus in nasal samples from preclinical second-year medical students. Mo Med. 2011;108(5):373–6.PubMed
17.
go back to reference Kitti T, Boonyonying K, Sitthisak S. Prevalence of methicillin-resistant Staphylococcus aureus among university students in Thailand. Southeast Asian J Trop Med Public Health. 2011;42:1498–504.PubMed Kitti T, Boonyonying K, Sitthisak S. Prevalence of methicillin-resistant Staphylococcus aureus among university students in Thailand. Southeast Asian J Trop Med Public Health. 2011;42:1498–504.PubMed
18.
go back to reference Gualdoni A, Lingscheid T, Tobudic S, et al. H. Low nasal carriage of drug-resistant bacteria among medical students in Vienna. GMS Krankenhhyg Interdiszip. 2012;7:Doc04.PubMedPubMedCentral Gualdoni A, Lingscheid T, Tobudic S, et al. H. Low nasal carriage of drug-resistant bacteria among medical students in Vienna. GMS Krankenhhyg Interdiszip. 2012;7:Doc04.PubMedPubMedCentral
19.
go back to reference Bettin A, Causil C, Reyes N. Molecular identification and antimicrobial susceptibility of Staphylococcus aureus nasal isolates from medical students in Cartagena, Colombia. Braz J Infect Dis. 2012;16:329–34.CrossRefPubMed Bettin A, Causil C, Reyes N. Molecular identification and antimicrobial susceptibility of Staphylococcus aureus nasal isolates from medical students in Cartagena, Colombia. Braz J Infect Dis. 2012;16:329–34.CrossRefPubMed
20.
go back to reference Mahmutović Vranić S, Puškar M. Staphylococcus aureus carriage among medical students. Med Glas (Zenica). 2012;9:325–9. Mahmutović Vranić S, Puškar M. Staphylococcus aureus carriage among medical students. Med Glas (Zenica). 2012;9:325–9.
21.
go back to reference Chen C, Chen Y, Huang C. Nasal carriage rate and molecular epidemiology of methicillin-resistant Staphylococcus aureus among medical students at a Taiwanese university. Int J Infect Dis. 2012;16:e799–803.CrossRefPubMed Chen C, Chen Y, Huang C. Nasal carriage rate and molecular epidemiology of methicillin-resistant Staphylococcus aureus among medical students at a Taiwanese university. Int J Infect Dis. 2012;16:e799–803.CrossRefPubMed
22.
go back to reference Syafinaz M, Nur Ain Z, Nadzirahi N, et al. Staphylococcus aureus nasal carriers among medical students in a medical school. Med J Malaysia. 2012;67:636–8.PubMed Syafinaz M, Nur Ain Z, Nadzirahi N, et al. Staphylococcus aureus nasal carriers among medical students in a medical school. Med J Malaysia. 2012;67:636–8.PubMed
23.
go back to reference Bellows C, Smith A, Wheeler J, Morici L. Nasal carriage of methicillin-resistant Staphylococcus aureus among students at a Louisiana medical university. Braz J Infect Dis. 2013;17:118–9.CrossRefPubMed Bellows C, Smith A, Wheeler J, Morici L. Nasal carriage of methicillin-resistant Staphylococcus aureus among students at a Louisiana medical university. Braz J Infect Dis. 2013;17:118–9.CrossRefPubMed
24.
go back to reference Cirković I, Djukić S, Vuković D, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus among medical students of Belgrade University. Srp Arh Celok Lek. 2013;141:349–53.CrossRefPubMed Cirković I, Djukić S, Vuković D, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus among medical students of Belgrade University. Srp Arh Celok Lek. 2013;141:349–53.CrossRefPubMed
25.
go back to reference Trépanier P, Tremblay C, Ruest A. Methicillin-resistant Staphylococcus aureus colonization among medical residents. Can J Infect Dis Med Microbiol. 2013;24:e39–41.PubMedPubMedCentral Trépanier P, Tremblay C, Ruest A. Methicillin-resistant Staphylococcus aureus colonization among medical residents. Can J Infect Dis Med Microbiol. 2013;24:e39–41.PubMedPubMedCentral
26.
go back to reference Treesirichod A, Hantagool S, Prommalikit O. Nasal carriage and antimicrobial susceptibility of Staphylococcus aureus among medical students at the HRH Princess Maha Chakri Sirindhorn Medical Center, Thailand: a follow-up study. J Infect Public Health. 2014;7:205–9.CrossRefPubMed Treesirichod A, Hantagool S, Prommalikit O. Nasal carriage and antimicrobial susceptibility of Staphylococcus aureus among medical students at the HRH Princess Maha Chakri Sirindhorn Medical Center, Thailand: a follow-up study. J Infect Public Health. 2014;7:205–9.CrossRefPubMed
27.
go back to reference Zakai A. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among medical students in Jeddah, Saudi Arabia. Saudi Med J. 2015;36:807–12.CrossRefPubMedPubMedCentral Zakai A. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among medical students in Jeddah, Saudi Arabia. Saudi Med J. 2015;36:807–12.CrossRefPubMedPubMedCentral
28.
go back to reference Collazos Marín F, Estupiñan Arciniegas G, Chavez Vivas M. Characterization of Staphylococcus aureus isolates that colonize medical students in a hospital of the city of Cali, Colombia. Int J Microbiol. 2015;2015:358489.CrossRefPubMedPubMedCentral Collazos Marín F, Estupiñan Arciniegas G, Chavez Vivas M. Characterization of Staphylococcus aureus isolates that colonize medical students in a hospital of the city of Cali, Colombia. Int J Microbiol. 2015;2015:358489.CrossRefPubMedPubMedCentral
29.
go back to reference Ho P-L, Lai EL, Chow K-H. Carriage of methicillin-susceptible and -resistant Staphylococcus aureus by medical students in Hong Kong. J Hosp Infect. 2015;91(2):184–5.CrossRefPubMed Ho P-L, Lai EL, Chow K-H. Carriage of methicillin-susceptible and -resistant Staphylococcus aureus by medical students in Hong Kong. J Hosp Infect. 2015;91(2):184–5.CrossRefPubMed
30.
go back to reference Baek S, Baek H, Yoo J. Higher nasal carriage rate of methicillin-resistant Staphylococcus aureus among dental students who have clinical experience. J Am Dent Assoc. 2015;147:348–53.CrossRef Baek S, Baek H, Yoo J. Higher nasal carriage rate of methicillin-resistant Staphylococcus aureus among dental students who have clinical experience. J Am Dent Assoc. 2015;147:348–53.CrossRef
31.
go back to reference Okamo B, Moremi N, Seni J, et al. Prevalence and antimicrobial susceptibility profiles of Staphylococcus aureus nasal carriage among pre-clinical and clinical medical students in a Tanzanian University. BMC Res Notes. 2016;9:47.CrossRefPubMedPubMedCentral Okamo B, Moremi N, Seni J, et al. Prevalence and antimicrobial susceptibility profiles of Staphylococcus aureus nasal carriage among pre-clinical and clinical medical students in a Tanzanian University. BMC Res Notes. 2016;9:47.CrossRefPubMedPubMedCentral
32.
go back to reference Ansari S, Gautam R, Shrestha S, et al. Risk factors assessment for nasal colonization of Staphylococcus aureus and its methicillin resistant strains among pre-clinical medical students of Nepal. BMC Res Notes. 2016;9:214.CrossRefPubMedPubMedCentral Ansari S, Gautam R, Shrestha S, et al. Risk factors assessment for nasal colonization of Staphylococcus aureus and its methicillin resistant strains among pre-clinical medical students of Nepal. BMC Res Notes. 2016;9:214.CrossRefPubMedPubMedCentral
33.
go back to reference Clinical and Laboratory Standards Institute/NCCLS. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement. Wayne: Clinical and Laboratory Standards Institute; 2014. CLSI/NCCLS Document M100-S24. Clinical and Laboratory Standards Institute/NCCLS. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Fourth Informational Supplement. Wayne: Clinical and Laboratory Standards Institute; 2014. CLSI/NCCLS Document M100-S24.
34.
go back to reference McClure A, Conly M, Lau V, et al. Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from -resistant staphylococci. J Clin Microbiol. 2006;44(3):1141–4.CrossRefPubMedPubMedCentral McClure A, Conly M, Lau V, et al. Novel multiplex PCR assay for detection of the staphylococcal virulence marker Panton-Valentine leukocidin genes and simultaneous discrimination of methicillin-susceptible from -resistant staphylococci. J Clin Microbiol. 2006;44(3):1141–4.CrossRefPubMedPubMedCentral
35.
go back to reference Zhang K, McClure A, Elsayed S, et al. 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.CrossRefPubMedPubMedCentral Zhang K, McClure A, Elsayed S, et al. 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.CrossRefPubMedPubMedCentral
36.
go back to reference Harmsen D, Claus H, Witte W, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41(12):5442–8.CrossRefPubMedPubMedCentral Harmsen D, Claus H, Witte W, et al. Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol. 2003;41(12):5442–8.CrossRefPubMedPubMedCentral
37.
go back to reference Tenover C, Arbeit D, Goering V, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33(9):2233–9.PubMedPubMedCentral Tenover C, Arbeit D, Goering V, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33(9):2233–9.PubMedPubMedCentral
38.
go back to reference Adler A, Chmelnitsky I, Shitrit P, et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Israel: dissemination of global clones and unique features. J Clin Microbiol. 2012;50(1):134–7.CrossRefPubMedPubMedCentral Adler A, Chmelnitsky I, Shitrit P, et al. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Israel: dissemination of global clones and unique features. J Clin Microbiol. 2012;50(1):134–7.CrossRefPubMedPubMedCentral
39.
go back to reference Shitrit P, Openhaim M, Reisfeld S, et al. Characteristics of SCCmec IV and V Methicillin-Resistant Staphylococcus aureus (MRSA) in Israel. Isr Med Assoc J. 2015;17(8):470–5.PubMed Shitrit P, Openhaim M, Reisfeld S, et al. Characteristics of SCCmec IV and V Methicillin-Resistant Staphylococcus aureus (MRSA) in Israel. Isr Med Assoc J. 2015;17(8):470–5.PubMed
40.
go back to reference Biber A, Parizade M, Taran D, et al. Molecular epidemiology of community-onset methicillin-resistant Staphylococcus aureus infections in Israel. Eur J Clin Microbiol Infect Dis. 2015;34(8):1603–13.CrossRefPubMed Biber A, Parizade M, Taran D, et al. Molecular epidemiology of community-onset methicillin-resistant Staphylococcus aureus infections in Israel. Eur J Clin Microbiol Infect Dis. 2015;34(8):1603–13.CrossRefPubMed
41.
go back to reference Grundmann H, Aanensen DM, van den Wijngaard CC, et al. Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: A molecular-epidemiological analysis. PLoS Med. 2010;7:e1000215.CrossRefPubMedPubMedCentral Grundmann H, Aanensen DM, van den Wijngaard CC, et al. Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: A molecular-epidemiological analysis. PLoS Med. 2010;7:e1000215.CrossRefPubMedPubMedCentral
42.
go back to reference Dall’Antonia M, Coen PG, Wilks M, et al. Competition between methicillin-sensitive and -resistant Staphylococcus aureus in the anterior nares. J Hosp Infect. 2005;61:62–7.CrossRefPubMed Dall’Antonia M, Coen PG, Wilks M, et al. Competition between methicillin-sensitive and -resistant Staphylococcus aureus in the anterior nares. J Hosp Infect. 2005;61:62–7.CrossRefPubMed
43.
go back to reference Mongkolrattanothai K, Gray BM, Mankin P, et al. Simultaneous carriage of multiple genotypes of Staphylococcus aureus. J Med Microbiol. 2011;60:317–22.CrossRefPubMed Mongkolrattanothai K, Gray BM, Mankin P, et al. Simultaneous carriage of multiple genotypes of Staphylococcus aureus. J Med Microbiol. 2011;60:317–22.CrossRefPubMed
Metadata
Title
Hospital clones of methicillin-resistant Staphylococcus aureus are carried by medical students even before healthcare exposure
Authors
Ido Orlin
Assaf Rokney
Avi Onn
Daniel Glikman
Avi Peretz
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2017
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-017-0175-2

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