Hospital clones of methicillin-resistant Staphylococcus aureus are carried by medical students even before healthcare exposure
Hospital clones of methicillin-resistant Staphylococcus aureus are carried by medical students even before healthcare exposure
Ido Orlin 0
Assaf Rokney 3
Avi Onn 0 2
Daniel Glikman 0 4
Avi Peretz 0 1
0 The Faculty of Medicine in the Galilee, Bar-Ilan University , Galilee , Israel
1 Clinical Microbiology Laboratory, Padeh Poriya Medical Center , Poriya, Hanna Senesh 818/2, Tiberias , Israel
2 Pediatric Gastrointestinal Unit, Padeh Poriya Medical Center , Poriya, Tiberias , Israel
3 National Staphylococcus aureus Reference Center , Central Laboratories , Israel Ministry of Health , Jerusalem , Israel
4 Pediatric Infectious Diseases Service, Galilee Medical Center , Nahariya , Israel
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.
Methicillin-resistance; Review; Staphylococcus aureus; Carriage; Medical students; Communityassociated; Healthcare-associated
Staphylococcus aureus (SA) is a versatile pathogen
capable of colonizing humans and mammals, and causing
skin and invasive diseases such as endocarditis,
osteomyelitis, and severe sepsis. Methicillin-resistant SA
(MRSA) was reported in 1961, soon after the
introduction of the semisynthetic penicillin, methicillin . Until
the 1990s, MRSA strains were associated mostly with
hospitals and infected patients who had contact with the
healthcare system, hence the name
healthcareassociated MRSA (HA-MRSA). These strains were
typically resistant to multiple antimicrobials
(multidrug resistant – MDR) and carried large
staphylococcal cassette chromosome mec (SCCmec) elements,
mostly types I-III . Beginning in the late 1990s,
community-associated strains of MRSA (CA-MRSA)
were described with increasing incidence, colonizing
and infecting patients who had no recent contact with
the healthcare system. These strains were usually
non-MDR, carried small SCCmec elements, mostly
types IV and V, and also carried the genes encoding the
Panton-Valentine leukocidin (PVL), a pore-forming toxin
rarely found among SA isolates . Nowadays, in many
geographic regions there are no longer lineages, genetic
markers, or susceptibility phenotypes that are indicative
for specific epidemiological origins such as HA-MRSA or
The primary reservoir of SA is the anterior nares, but
the organism can be isolated from multiple sites. The
prevalence and incidence of SA nasal carriage vary
according to the population studied. According to multiple
cross-sectional surveys, the mean carriage rate across
the general population is 37% . Regarding MRSA
carriage in the era of CA-MRSA, the overall MRSA carriage
rate in the United States has increased from 0.8% in
2001–2002 to 1.5% in 2003–2004, and it is particularly
important in the hospital environment because
colonized and infected patients represent the most important
reservoir of MRSA in healthcare facilities [4, 5].
The carriage of MRSA among healthcare workers
(HCW) due to the relation of their exposure to patients
harboring these strains is a well-known phenomenon
. Medical students seem to be no exception, as their
clinical study environment involves various medical
settings such as hospitals and community clinics, which
may contribute to their carriage status. In a
nonsystematic review of the English literature we found
several studies, conducted worldwide, investigating SA
carriage among medical students (Table 1) [7–32]. These
studies reported MRSA carriage rates of 0–5.4% and SA
carriage rates of 14–45% (excluding a small study from
India reporting a higher carriage rate and a study from
Canada of dental students [12, 15]). Only in a minority
of these studies assessed the difference of SA carriage
between pre-clinical and clinical medical students and
most investigations assessed carriage at a single
timepoint only [7, 9, 21–23, 26, 27, 31]. Of these, three
studies demonstrated higher SA carriage rates in the clinical
studies stage [9, 23, 26]. Furthermore, only a single study
from Thailand had prospectively examined the change
in SA carriage in the same group of medical students
over multiple sampling times . Therefore, we
aimed to prospectively examine the change in SA
carriage among medical students transitioning from
pre-clinical to clinical education with a focus on
MRSA. Moreover, we aimed to characterize MRSA
isolates from medical students using SCCmec and spa
typing as well as PFGE.
The study population included medical students at the
Faculty of Medicine in the Galilee of Bar-Ilan University,
in Safed, Israel. The Faculty has two academic classes:
4year and 3-year tracks. The 3-year track students
finished 3 years of pre-clinical medical education in
medical faculties across Europe (such as Hungary, Italy,
and Lithuania). Almost all of these students reported no
patient encounters during their studies, as most of their
education was lecture-based. The 4-year track students
have graduated from various pre-med Israeli academic
institutions. As no dormitories are available, most
students live separately. The study was approved by the
local Ethics Committees of Baruch Padeh Medical
Center, Poriya, and Bar-Ilan University.
Samples were collected three times for each participant
during 2012–2014. Sampling was made by a sterile swab
(COPAN, Italy) from the nostrils, independently by the
participant. First sampling was performed towards the
end of pre-clinical studies, with second and third
samplings collected at 13 and 19 months post-initial
sampling while students were rotating in clinical
clerkships. All samples were kept at room temperature for a
maximum of 24 h before being transferred to the
Staphylococcus aureus identification
Microbiological examinations were performed at the
Baruch Padeh Medical Center Microbiology Laboratory
in Poriya, Israel. Primary culture was performed by
striking technique in order to perform culture and colony
isolation on a selective chromogenic growth medium
(Chromagar MRSA/MSSA, hylabs, Israel). Confirmatory
tests for SA included gram staining, catalase test, and
rapid agglutination test for simultaneous detection of
the fibrinogen affinity antigen (clumping factor), protein
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A, and the capsular polysaccharides (Pastorex™ Staph
Plus, BIO RAD, France).
Antimicrobial susceptibility tests were performed by disc
diffusion method on Muller-Hinton agar (BD Diagnostics,
Sparks, MD) in accordance with the Clinical and
Laboratory Standards Institute (CLSI) guidelines for
rifampicin, vancomycin, erythromycin, gentamicin, cefotaxime,
clindamycin, penicillin, oxacillin, mupirocin, fusidic
acid, tetracycline, trimethoprim-sulfamethoxsazole
(TMPSMX), and cefoxitin . MDR for MRSA was defined as
resistance to at least three antimicrobial agents in addition
Typing of MRSA strains was performed at the National
Staphylococcus aureus Reference Center, Central
Laboratories, Israel Ministry of Health, Jerusalem, Israel.
PCR detection of mecA and PVL genes
PCR reactions in a total volume of 23 mL included
10.5 mL DDW, 12.5 mL PCR mix (ReddyMix, Tamar
Laboratory Supplies, Mevaseret Zion), MecA1 and
MecA2 primers or Luk-PV-1 and Luk-PV-2 primers
(1 mM each). Thermocycling conditions were set at
94 °C for 2 min followed by 30 cycles of 94 °C for
30 s, 55 °C for 30 s, 72 °C for 60 s, followed by a
final step of 72 °C for 2 min [34, 35].
Detection of SCCmec types
SCCmec types were detected using the method of Zhang
et al. . PCR reactions were performed in a total
volume of 20 mL, including 9.5 mL DDW, 9.5 mL PCR mix
(ReddyMix, Tamar Laboratory Supplies, Mevaseret
Zion), and 1 mL primer mix with a final concentration
as recommended . Thermocycling conditions were
set at 95 °C for 5 min, followed by 11 cycles of 94 °C for
45 s, 65 °C for 45 s, 72 °C for 1.5 min, followed by 26
cycles of 94 °C for 45 s, 55 °C for 45 s, 72 °C for 1.5 min,
and a final step of 72 °C for 10 min .
spa typing was performed in a 20 mL reaction including
9.5 mL DDW, 9.5 mL PCR mix (ReddyMix, Tamar
Laboratory Supplies, Mevaseret Zion), and primers 1514R,
1113 F (4pmol each). Thermocycling conditions were set
at 94 °C for 5 min, followed by 35 cycles of 94 °C for
45 s, 60 °C for 45 s, 72 °C for 90 s, followed by a final
extension step of 72 °C for 10 min. Cycle sequencing
was carried out using the BigDye Terminator v1.1
chemistry (Applied Biosystems, Foster City, CA, USA)
according to manufacturer’s protocol. Cycle sequencing
products were purified by gel using Performa DTR
according to the manufacturer’s recommendation.
Electrophoresis was carried out on a 3730 × l Genetic
Analyzer (Applied Biosystems) and the analysis was
done using sequencing Analysis v.5.3.1 software (Applied
Biosystems). spa typing analysis was performed using
BioNumerics 7.5 software .
Agarose-embedded (Lonza, USA) SA DNA was digested
with SmaI (Fermentas, Lithuania) followed by gel
electrophoresis in the CHEF MAPPER (Bio-Rad) system.
Electrophoresis conditions were 14 °C, 0.5 ×
Tris-borateEDTA buffer (Sigma, Switzerland), initial pulse 5 s, final
pulse 50 s, 6 V, 18 h. Salmonella Braenderup H9812
restricted with XbaI (Fermentas, Lithuania) was used
as a marker. PFGE restriction patterns were analyzed
by the BioNumerics software (Applied Maths). The
pulsotypes were compared using the band-based
DICE similarity coefficient with 1% optimization and
tolerance. The un-weighted pair group method with
arithmetic mean (UPGMA) algorithm was used for
cluster analysis .
Statistical analysis was performed using SPSS for
windows version 21 (IBM Analytics). Proportion tests,
Chi-square tests, and Wilcoxon signed ranks test were
used for the univariate analysis using α = 0.05 and 95%
confidence interval (CI). Statistical significance was
based on p ≤ 0.05.
A total of 58/109 students of the 2012 class (53%)
participated in our study: 31 students of the 4-year track and
27 students of the 3-year track. There were 30 females
and 28 males; the age range was 23–35 years. All 58
students participated during the entire study; three samples
were taken from each of these students. Overall, 65 SA
isolates were cultured from 32 students in the entire
study period: 13 MRSA strains from seven students and
52 MSSA strains from 28 students.
First sample (pre-clinical sampling)
Overall, 19 (33%) SA isolates were cultured from 7
(12%) students of the three-year track and 12 (20%)
students of the 4-year track (Figs. 1 and 2). Four (7%)
MRSA isolates were identified: three from students of
the 4-year track (10%) and one from a student of the
3year track (4%). No significant differences in the rates of
MSSA and MRSA isolation between the medical tracks
were noted (p = 0.5; Fig. 2).
Fig. 1 Staphylococcus aureus carriage rates among medical students by sample
Second sample (first clinical sampling)
Thirteen months after the first pre-clinical samples, 22
SA (38%) isolates were cultured from 30% (eight of 27)
of the 3-year track students and 45% (14 of 31) of the
4year track students (Figs. 1 and 2). Further analysis
revealed 16 MSSA (28%) and 6 MRSA isolates (10%)
(Fig. 1). No significant differences were noted in the
rates of MSSA and MRSA isolation between the medical
tracks (p = 0.47) or between the first and second samples
(p = 0.76; Fig. 2).
Third sample (second clinical sampling)
The last sample took place 6 months following the
second sample and included 24 (41%) SA isolates cultured
from 44% (12 of 27) of the 3-year track students and 39%
(12 of 31) of the 4-year track students (Figs. 1 and 2).
Overall, 21 MSSA (36%) and three MRSA isolates
(5%) were identified. No significant differences in the
rates of MSSA and MRSA isolation between the
medical tracks were noted (p = 0.74). Compared with the
second sample, an increase in the carriage rate of
MSSA was noted in students of the 3-year track (p =
0.01; Fig. 2). Non-significant increases in the overall
SA carriage between the pre-clinical sample and the
third sample (p = 0.21) and between the second
sample and the third sample (p = 0.07) were noted.
Phenotypic and genotypic characterization of MRSA
The mecA gene was detected in all MRSA isolates.
According to PFGE analysis, three closely-related clones
of MRSA strains were identified (Fig. 3, Table 2) .
The first clone was isolated exclusively from the 4-year
track students; this clone carried SCCmec IV, was PVL
negative, and typed as spa type t032. The second clone
was isolated from a single student of the 3-year track
and was PVL negative, spa type t12435, with an
untypable SCCmec. The third clone was cultured from
students in both medical tracks and carried SCCmec II,
was PVL negative, and typed as spa type t002.
Fig. 2 Carriage rates of Staphylococcus aureus isolates according to medical track and sampling time
Fig. 3 Pulsed-field gel electrophoresis analysis of methicillin-resistant
Staphylococcus aureus strains found in the study. * The numbers
represent the students with MRSA carriage as mentioned in Fig. 4;
the capital letters represent the sample time. For example: 1C is a
clone cultured from student 1 on the third sample of the study
Overall, 38% of MRSA isolates (5 out of 13) were
resistant to clindamycin whereas only 6% of MSSA isolates
were clindamycin resistant (p = 0.01; Table 3).
Clindamycin resistance rates differed among the various MRSA
clones: half of SCCmec II, t002 isolates were resistant
while none were resistant in the SCCmec IV, t032 clone.
All MRSA isolates were susceptible to TMP-SMX,
tetracycline, rifampicin, fusidic acid, mupirocin, and
vancomycin, and were non-MDR.
Carriage of MRSA over multiple sampling times
Five of the seven (71%) students who were colonized
with MRSA carried the bacterium in more than one
Table 2 Summary of molecular characteristics of carried
methicillin-resistant Staphylococcus aureus strains
SCCmec II, t002
SCCmec IV, t032
All MRSA Isolates were PVL-negative
Staphylococcal Cassette Chromosome mec (SCCmec)
sample (Fig. 4); two students carried different MRSA
clones at various sampling times. Four students (57%) had
MRSA carriage during the pre-clinical studies. None of
the students carried MRSA and MSSA simultaneously.
The carriage of SA increased in medical students along
the sampling time (33, 38, and 41%, respectively). A
non-significant increase (p = 0.07) was noted in the
overall rise of SA carriage. However, a statistically significant
increase in the MSSA carriage among the 3-year track
students was evident when the second sample was
compared with the third; both were taken during the clinical
stages of studies. Thus, it is possible that a larger sample
would also lead to a significant overall rise in SA
carriage between the preclinical and clinical parts of the
studies. This was indeed observed in three of eight
studies comparing preclinical and clinical medical
students [9, 23, 26].
In the multiple samplings we performed, up to 10% of
the students carried MRSA. This rate is higher than
observed in other studies looking at medical students,
where carriage rates of 0–5.4% were noted (Table 1). In
fact, according to a systematic review of MRSA carriage
among healthcare workers in Europe and the United
States, it is close to the reported carriage rates of nursing
staff . Possible explanations for this difference in rates
of MRSA carriage among medical students may be from
various sampling times in the studies, MRSA prevalence
rates in hospitals and communities in different
countries, and the relatively small sample size of studies.
The MRSA strains we isolated are compatible with
HA-MRSA strains. We base this observation on the
molecular characteristics of the strains and epidemiologic
studies from Israel. Both SCCmec II, t002 and SCCmec
IV, t032 are common hospital MRSA strains in Israel
[38, 39]. Indeed, SCCmec II, t002 is reported to be the
second most common clone in Israeli hospitals .
Although mostly described in CA-MRSA strains, up to
30% of HA-MRSA isolates in Israel carry SCCmec types
IV and V [38, 39]. A recent report of community-onset
MRSA in Israel demonstrated SCCmec IV, t032 to
represent nearly 30% of SCCmec IV isolates; thus this strain is
commonly isolated both in Israeli hospitals and in
patients from the community . In contrast, typical
CA-MRSA strains in Israel have different genotypes:
USA300 (SCCmec IV, t008, PVL+) and SCCmec IV, t991,
PVL- . The third strain in our study, t12435, is
relatively rare, being isolated only a few times from
hospitalized patients in northern Israel according to data from
the Israeli National Staphylococcus aureus Reference
Center. Although non-MDR phenotype of MRSA is
commonly described among CA-MRSA strains, this
phenotype was also common among SCCmec IV, t032
Table 3 Antibiotic resistance rates of Staphylococcus aureus isolates
All isolates were susceptible to trimethoprim-sulfamethoxazole (TMP-SMX), fusidic acid, mupirocin, tetracycline, rifampin, and vancomycin
MSSA Methicillin-susceptible Staphylococcus aureus, MRSA Methicillin-resistant Staphylococcus aureus
isolates from Israeli hospitals with relatively low
clindamycin resistance rates [1, 2, 40]. Our findings differ
from other reports of MRSA in medical students:
predominantly CA-MRSA clones (as suggested by the
authors) were isolated from medical students in
China, Serbia, Canada, Colombia and Taiwan,
suggesting these countries have a different MRSA
epidemiology [15, 19, 21, 24, 28, 29].
Two additional observations are worth mentioning: we
did not find new, non-local MRSA clones among the
students, although the 3-year track students arrived
from various countries in Europe. This probably implies
acquisition of MRSA clones in Israel but can also
represent acquisition of global MRSA strains from Europe
. The second observation is that although students
carried MRSA isolates compatible with HA-MRSA
clones, the acquisition of the majority of MRSA isolates,
including two of three clones, took place before the
clinical part of the studies, namely before the exposure
to the healthcare system occurred. Indeed, 80% of
community-onset MRSA isolates among patients insured
by a large health maintenance organization in Israel
were recently shown to be of nosocomial origin .
This can explain the acquisition of HA-MRSA clones by
students before clinical rotations. Another explanation
may be that some students had unrecognized healthcare
exposure early in their studies.
In assessing carriage over time, we observed that in
two students multiple MRSA clones were carried on
different occasions. Compared with MSSA, less is known
about the natural history of MRSA carriage and
therefore comparison to MSSA data may seem tempting.
However, this comparison is problematic as the variety
of genotypes and prevalence in the community is larger
Fig. 4 Time-line of methicillin-resistant S. aureus carriage
for MSSA in most geographic locales [1, 3]. Carrying
multiple genotypes of MRSA over time may imply
acquisition of a new strain from a fellow student or during
healthcare exposure. Furthermore, we noticed that only
one of seven students colonized with MRSA can be
defined as a persistent carrier and even so with multiple
genotypes. Lastly, we observed that there was no
simultaneous carriage of MRSA and MSSA isolates.
Simultaneous carriage of MRSA and MSSA was previously
reported either as a rare occurrence, assuming
competition for colonization space and nutrients, or in contrast,
as a relatively common occurrence [42, 43].
Our study had some limitations. The number of
students participating was relatively small and the sampling
was not done simultaneously in all students. The nose was
the only site tested. Additionally, only one medical school
participated. This may limit the power of the study and
the generalization for all areas of Israel. The strengths of
the study are in the prospective collection of data over
multiple times in preclinical and clinical parts of the
students’ education, the participation of all students during
the whole study, and the genotyping of MRSA strains.
MSSA carriage rates increased during the clinical part of
the studies in medical students in Israel. Higher rates of
MRSA carriage were evident in this study compared with
previous reports of medical students. MRSA strains
carried were genotypically similar to healthcare-associated
clones in Israel; however, MRSA carriage occurred in the
majority of students before healthcare exposure, probably
representing community-acquisition of hospital strains.
Until official recommendations regarding screening and
interventions for MRSA in medical students will be
published, a call for good personal hygiene is in place.
CA-MRSA: Community-associated methicillin-resistant Staphylococcus aureus;
HA-MRSA: Healthcare-associated methicillin-resistant Staphylococcus aureus;
MRSA: Methicillin-resistant Staphylococcus aureus; PVL: Panton-Valentine
Leukocidin; SA: Staphylococcus aureus
Availability of data and materials
Please contact author for data requests.
All authors have read and approved the final version of the manuscript. IO
participated in the design of the study, collected data, helped in drafting the
manuscript, and reviewed the final draft. AR participated in the design of the
study, performed the molecular studies, helped in drafting the manuscript,
and reviewed the final draft. AO participated in the design of the study,
helped in drafting the manuscript, and reviewed the final draft. DG and AP
conceived the study, collected and analyzed data, helped in drafting the
manuscript, and wrote the final draft.
The article was written as part of the requirements of the School of
Medicine in the Galilee, Bar-Ilan University, for an MD degree
The authors declare that they have no competing interests.
Consent for publication
Ethics approval and consent to participate
The study protocol was reviewed and approved by the Poriya-Baruch Padeh
Medical Center Institutional Review Board/Ethics Committee and the Ethics
Committee of Bar-Ilan University. The Ethics Committee approval number is:
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