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Journal of Applied Microbiology ISSN 1364-5072


Characterization of Methicillin-resistant Staphylococcus

aureus isolated from public surfaces on a University
Campus, Student Homes and Local Community
M.C. Roberts, O.O. Soge, D. No, S.E. Helgeson and J.S. Meschke
Department of Environmental and Occupational Health Sciences, School of Public Health, University of Washington, Seattle, WA, USA

Keywords Abstract
environmental surfaces, methicillin-resistant
Staphylococcus aureus, student home Aim: Isolation and characterization of methicillin-resistant Staphylococcus aur-
surfaces, university surfaces. eus (MRSA) from frequently touched nonhospital environmental surfaces at a
large university, student homes and community sites.
Correspondence Methods and Results: Twenty-four isolates from 21 (4Æ1%, n = 509) surfaces
Marilyn C. Roberts, Department of
were MRSA positive and included 14 (58%, n = 24) SCCmec type IV, two
Environmental and Occupational Health
Sciences, 357234, School of Public Health,
(8%, n = 24) type I, and eight (33%, n = 24) were not type I-IV (NT). Six
University of Washington, Seattle, WA 98195- different multilocus sequencing types were identified by PCR and sequencing.
7234, USA. PCR assays identified one (4Æ2%, n = 24) Panton-Valentine leukocidin (PVL)
E-mail: marilynr@u.washington.edu positive, 22 (92%, n = 24) arginine catabolic mobile element (ACME) positive
and 23 (96%, n = 24) multidrug-resistant (kanamycin, macrolide, tetracycline)
2011 ⁄ 0157: received 26 January 2011, MRSA isolates. Eleven (46%, n = 24) USA300 isolates were determined by
revised 27 February 2011 and accepted 14
pulsed-field gel electrophoresis.
March 2011
Conclusion: The MRSA-positive environmental surfaces were identified in stu-
doi:10.1111/j.1365-2672.2011.05017.x dent homes (11Æ8%, n = 85), the community (2Æ3%, n = 130) and the univer-
sity (2Æ7%, n = 294). USA300 strains were isolated from the university, student
homes and community samples. This is the first report of the animal clone
ST97 on urban environmental surfaces.
Significance and Impact of the Study: The study highlights the distribution of
USA300 on frequently touched surfaces. Whether contact with these MRSA
contaminated environmental surfaces are associated with increased risk of
transmission of MRSA to people needs further research.

There are less therapeutic options for treatment of MRSA

infections, patients often require longer hospital stays,
Staphylococcus aureus is carried in the nose of 25–35% of and MRSA infections are more likely to recur which
humans, and it is a common cause of serious and life- increases the costs as compared to infections because of
threatening infections. Methicillin-resistant S. aureus S. aureus (Rubin et al. 1999).
[MRSA] was first identified fifty years ago, and today, it Staphylococcus aureus and MRSA are spread from
has become a major nosocomial pathogen. Community- people-to-people and fomite-to-person, although the
acquired MRSA (CA-MRSA) skin and soft tissue infec- potential reservoirs in the community are unknown (Eady
tions, normally associated with USA300 MRSA strains in and Cove, 2003; Miller and Diep 2008). MRSA-contami-
North America, are on the increase in healthy people with nated public transport handrails (Stepanović et al. 2008),
no healthcare exposure or known classical risk factors beauty salon surfaces (Huijsdens et al. 2008), fire stations,
(Eady and Cove 2003; Klevens et al. 2007). Identified risk medic trucks and ambulance surfaces have been identified
factors associated with CA-MRSA outbreaks include (Brown et al. 2010; Roberts et al. 2011b; Roline et al.
sharing of personal care products, frequent skin-to-skin 2007). Scott et al. (2009) found MRSA contaminated
contact, skin abrasions and crowded living conditions. surfaces in nine (26%) of 35 homes with MRSA isolated

ª 2011 The Authors

Journal of Applied Microbiology 110, 1531–1537 ª 2011 The Society for Applied Microbiology 1531
MRSA from environmental nonhospital surfaces M.C. Roberts et al.

from seven of 13 kitchen surfaces and four of 11 bath- housing sites (apartments, houses, parent homes and
room surfaces, and methicillin-susceptible S. aureus dorm rooms) including common areas (couch, bathroom
[MSSA] was isolated from 12 of the kitchen and ten of surfaces, kitchen, microwave touchpad, TV remote, wash-
the bathroom surfaces. One study found that environ- ing machine) using the Scott et al. study (2009) as a
mental survival of MRSA improves in the presence of guide, and students cell phones; 294 surfaces on Univer-
organic material on coins (Tolba et al. 2007). While a sity of Washington (UW) campus (ATM and computer
second study (Desai et al. 2009) showed MRSA may per- keypads, bathroom handles, elevator buttons, locker
sist on contaminated surfaces for >5 weeks, suggesting handles, vending machine keypads, and water fountain
that MRSA may survive for extended time periods. The handles, gym equipment); and 130 community sites
second study also determined that 3 s of skin contact (parking meters, ATM keypads, public library touch
with a MRSA-contaminated surface or object was all that screens) were sampled in 2009–2010 (Table 1). The Uni-
was required to transfer MRSA to the skin under labora- versity has >43 000 students and 22 000 employees.
tory conditions. Two of the indoor UW ATM keypads were sampled nine
Brook et al. (2009) examined 70 frequently used separate times over a 6-month time period for the
environmental surfaces in a university of 25 000 indi- presence of MSSA and MRSA (Table 2). While the other
viduals for contamination of S. aureus and MRSA from sites were sampled once using the SANICULTTM swab
420 samples taken from student desktops, computer (Starplex Scientific Inc., Etobicoke, ON, Canada) or
keyboards, telephone mouthpieces, water fountains, pho- BBLTM RODACTM contact plates (Becton Dickinson Co.,
tocopy keypads, vending machines and elevators buttons Franklin Lakes, NJ, USA) for all surfaces and sterile baby
over a 3-week period in 2007. Staphylococcus aureus was wash clothes in the washing machines as previously
isolated from computer keyboards, telephones and eleva- described (Roberts et al. 2011a). A convenience sampling
tor buttons; however, no MRSA strains were isolated and plan was used.
S. aureus were not further characterized. More recently
we have found 8Æ4% of the 95 environmental surfaces
Sample processing
taken from university dental clinics were MRSA positive.
In that study, three MRSA were SCCmec type IV, three BBLTM RODACTM contact plates (Becton Dickinson Co.)
were Panton-Valentine leukocidin positive (PVL+) and with Bacto Staphylococcus Medium 110 supplemented
none were USA300 (Roberts et al. 2011a). This study sug- with 10 lg ml)1 methicillin and 0Æ01% potassium tellurite
gested that both dental clinic surfaces and dental students were incubated in 5% CO2 at 36Æ5 C. Two millilitres of
may be reservoirs for MRSA, although the dental clinic Bacto m Staphylococcus broth [1Æ5·] (Difco Labora-
services outpatients and thus is more related to a hospital tories, Sparks, MD, USA) supplemented with a final
setting than strictly a university environment. concentration of 75 lg ml)1 polymyxin B and 0Æ1%
In the current study, 24 MRSA isolates were identified potassium tellurite (Sigma Co. St. Louis, MO, USA) was
and characterized from 21 (4Æ1%, n = 509) environmental added to the swabs and 50 ml of media for the wash
surfaces taken from a large university campus, student clothes. All were incubated in 5% CO2 at 36Æ5C until
homes and the local community. Fourteen (58%, n = 24) turbid and black as previously described (Roberts et al.
MRSA were type IV, two (8%, n = 24) type I and eight 2011a,b). Positive samples were diluted and plated onto
(33%, n = 24) NT, and 11 (46%, n = 24) isolates from all Bacto m Staphylococcus Medium 110 supplemented
three sampled areas were USA300. In contrast to earlier with 10 lg ml)1 methicillin and 0Æ01% potassium tellurite
studies, 23 of 24 of the MRSA isolates in this study were and Bacto Mannitol Salts Agar (Difco) as previously
resistant to ‡1 other class of antibiotics which would described (Roberts et al. 2011a,b). All samples were held
reduce therapeutic options if they caused disease (Eady for 7 days before being labelled as negative. Isolates were
and Cove, 2003). MRSA-positive surfaces were identified biochemically verified as S. aureus, and the mecA gene
in all three locations (student homes, community and was verified in the MRSA isolates as previously described
university), suggesting that these contaminated surfaces (Roberts et al. 2011a; Soge et al. 2009).
may be reservoirs for transmission of MRSA to the public.
Detection of mecA, PVL gene, SCCmec typing,
Materials and methods multilocus sequence typing (MLST), and presence of the
arginine catabolic mobile element (ACME)
Surfaces sampled
The PCR assay conditions for the mecA, SCCmec type
A total of 509 frequently touched surfaces including 85 I-V, and presence of the PVL gene used previously
environmental samples from eight undergraduate student described primers and conditions (Roberts et al. 2011a;

ª 2011 The Authors

1532 Journal of Applied Microbiology 110, 1531–1537 ª 2011 The Society for Applied Microbiology
M.C. Roberts et al. MRSA from environmental nonhospital surfaces

Table 1 Molecular typing characteristics of methicillin-resistant Staphylococcus aureus isolated from 21 public surfaces

Isolate Year Location SCCmec type PFGE 300* ACME Resistance genes

Student Homes n = 10 isolates

Student #1
J-5 2010 Dorm water fountain NT 8 M No + None
Student #2
A3-6 2010 Microwave touchpad IV 45 N No + tet(M), msr(A), aadD
A4-3 2010 Couch armrest, fabric IV 45 N No + tet(M), msr(A), aadD
Student #3
S3-23 2010 TV remote IV 5 A Yes + tet(M), tet(K), msr(A), aadD
S9-18 2010 Bathroom floor IV 5 A Yes + tet(M), msr(A), aadD
S5-28 2010 Bathroom light switch NT 5 A Yes + tet(M), tet(K), aadD
Student #4
R501 2010 Couch IV 8 K Yes + tet(M), msr(A), aadD
R502 2010 Toilet Flush Handle IV 931 K Yes + tet(M), tet(K), msr(A), aadD
R509 2010 Bathroom Door Knob IV 931 K Yes + tet(M), tet(K), msr(A), aadD
Student #5
T4-38 2010 Washing Machine IV 5 L No + tet(M), tet(K), msr(A), aadD
University Campus n = 10 isolates
3-22 2009 Bathroom 3rd floor NT 5 E No ) tet(M)
3-36 2009 Bathroom 3rd floor IV 5 A Yes + erm(C), msr(A)
20 2010 Inside ATM Keypad R IV 5 A Yes + tet(M), tet(K), erm(A), erm(C),
msr(A), aadD
36 2010 Inside ATM Keypad R I 45 D No + tet(M), tet(K), erm(A),
erm(C), aadD
26 2010 Inside ATM Keypad T IV 30 C Yes + tet(M), tet(K), erm(A), erm(C),
msr(A), aadD
8-509§ 2009 Locker handle IV 8 B Yes + tet(M), tet(K), msr(A), aadD
3-2– 2009 Elevator button I 8 F No + tet(M), erm(C), msr(A)
3-8– 2009 Elevator button NT 97 H No + tet(M)
3-10 2009 Study lounge floor NT 97 H No + tet(M), erm(C)
3-6 2009 Bathroom 2nd floor NT 97 G No ) tet(M)
Community sites near the University campus n = 4 isolates
40 2009 Outside ATM Keypad A NT 5 A Yes + tet(M), msr(A)
55 2009 Outside ATM Keypad B IV 8 I No + tet(M), erm(C), msr(A), aadD
5-3** 2010 Library computer touch screen NT 30 J No + tet(K), aadD
5-4** 2010 Library computer touch screen IV 30 J No + tet(M), tet(K), msr(A), aadD

*‡ 80% PFGE identity with USA 300 determined by BioNumerics GelCompar II software; ,–,** From the same sample;
Same ATM keypad sampled at two different time periods; #20 was isolated 4 ⁄ 02 ⁄ 10 and #36 was isolated 4 ⁄ 15 ⁄ 10 (see Table 2);
§PVL positive isolate.

Soge et al. 2009). Positive and negative controls were used erm(A), erm(B), erm(C), and msr(A) genes; and tetra-
as previously described in all assays. Those isolates that cycline resistance genes, tet(M) and tet(K), with verifica-
were not type I-V were labelled nontypeable [NT] for the tion by hybridization using internal 32P-labelled probe.
current study. The PCR assay for the ACME encoded Positive and negative controls were used for all PCR
arcA gene used primers and conditions described by Diep assays as previously described (Roberts et al. 2011a; Soge
et al. (2006) with a clinical USA300 as the positive et al. 2009).
control. The MLST PCR assays were performed as previ-
ously described using published primers and conditions
Pulsed-field gel electrophoresis (PFGE)
(Enright et al. 2000; Roberts et al. 2011a; Soge et al. 2009).
Methicillin-resistant S. aureus isolates were PFGE typed
using previously described protocol (McDougal et al.
Detection of antibiotic resistance genes
2003) with SmaI enzyme (Fermentas Inc., Glen Burnie,
PCR assays were used to determine the presence of kana- MD, USA). The different PFGE patterns were labelled A
mycin resistance gene, aadD; macrolide resistance genes, through N (Table 1). The genetic relatedness of the

ª 2011 The Authors

Journal of Applied Microbiology 110, 1531–1537 ª 2011 The Society for Applied Microbiology 1533
MRSA from environmental nonhospital surfaces M.C. Roberts et al.

Table 2 Methicillin-susceptible Staphylococcus aureus [MSSA] and the isolates carried tetracycline resistance genes [11
methicillin-resistant S. aureus [MRSA] from two indoor university ATM tet(M); 10 tet(K) and tet(M); 1 tet(K)]. Eighteen (75%,
n = 24) carried macrolide resistance genes with 12 (50%,
Date MSSA MRSA n = 24) carrying one antibiotic resistance gene and six
(25%, n = 24) carrying ‡2 macrolide resistance genes.
Fifteen isolates carried the msr(A) gene, seven isolates
3 ⁄ 25 ⁄ 10 No No
4 ⁄ 2 ⁄ 10 No Yes
carried the erm(C) gene and three isolates carried the
4 ⁄ 8 ⁄ 10 No No erm(A) gene. Sixteen (67%, n = 24) of the MRSA iso-
4 ⁄ 15 ⁄ 10 No Yes lates carried the aminoglycoside resistance gene, aadD
4 ⁄ 22 ⁄ 10 No No (Table 1).
4 ⁄ 29 ⁄ 10 No No
6 ⁄ 2 ⁄ 10 No No
8 ⁄ 4 ⁄ 10 Yes No Student homes
9 ⁄ 12 ⁄ 10 No No
Five (63%, n = 8) undergraduate student homes had
3 ⁄ 25 ⁄ 10 Yes No MRSA-positive samples (Table 1). The MRSA-positive
4 ⁄ 2 ⁄ 10 No Yes homes included two students who were living in their
4 ⁄ 8 ⁄ 10 No No family home and three living with other students. The
4 ⁄ 15 ⁄ 10 No No three student homes that were negative for MRSA also
4 ⁄ 22 ⁄ 10 No No lived with other students. The number of MRSA-positive
4 ⁄ 29 ⁄ 10 No No
samples ranged from one to three of the 10 surfaces sam-
6 ⁄ 2 ⁄ 10 No No
8 ⁄ 4 ⁄ 10 Yes No
pled per home. Four different ST-types were identified
8 ⁄ 20 ⁄ 10 Yes No with two homes having ST5 or ST8 and two homes
9 ⁄ 12 ⁄ 10 No No (Student #3 and #4) were contaminated with USA300
isolates. Student #5 was the only one to have a MRSA-
positive washing machine. The two MRSA isolated from
Student #2 house surfaces were indistinguishable from
isolates to USA300 was determined by Dice coefficient, each other by all typing methods suggesting they repre-
UPGMA using the GelCompar II software according to sented a single strain. Diversity was found in the SCCmec
the manufacturers’ instructions (Applied Maths, Inc., type, ST type, and number and type of antibiotic resis-
Austin, TX USA). Strains that had ‡80% homology with tance genes carried by the three MRSA isolates recovered
USA300 were classified as USA300 (Table 1). from each of the Student #3 and Student #4 households.
However, the three isolates from each household had
indistinguishable PFGE patterns and were related to
USA300. The USA300 MRSA isolates from Student #3
home had the same ST type, indistinguishable PFGE pat-
Identification and characterization of MRSA-positive
tern, and two of the isolates had the same SCCmec type
IV as the university isolates 3-36 from the bathroom floor
Twenty-four MRSA isolates were identified from 21 and 20 from the ATM keypad, although they differed in
(4Æ1%, n = 509) different environmental surface samples, the number of other antibiotic resistance genes they car-
and included ten (11Æ8%, n = 85) student house samples, ried. All 10 MRSA isolates from the student homes were
eight (2Æ7%, n = 294) university samples and three (2Æ3%, ACME +, nine (90%, n = 10) isolates carried other anti-
n = 130) community samples (Table 1). Fourteen (58%, biotic resistance genes and none were PVL + (Table 1).
n = 24) of the MRSA isolates were SCCmec type IV of
which nine were (‡80% homology) USA300. Two addi-
University surfaces
tional isolates, which were SCCmec NT, were also
USA300. Two (8%, n = 24) isolates were SCCmec type I, Two university ATM keypads were repeatedly sampled
the remaining eight (33%, n = 24) were NT and none of nine times over a 6-month time period (Table 2). During
these were USA300. The 24 MRSA represented six differ- that time period, the ATM #R keypad was positive 3
ent ST types with the most common ST 5 (eight isolates), (33%, n = 9) times for S. aureus including twice for
followed by ST8 (five isolates), ST30, ST40 and ST97 MRSA and MSSA, while ATM #T was positive 4 (44%,
(three isolates each) and ST931 (two isolates). Twenty- n = 9) for S. aureus including once with MRSA and three
three (96%, n = 24) of the MRSA isolates carried other times with MSSA (Table 2). All three of the ATM MRSA
antibiotic resistance genes. Twenty-two (92%, n = 24) of differed in ST type (ST5, ST30, ST45), PFGE patterns and

ª 2011 The Authors

1534 Journal of Applied Microbiology 110, 1531–1537 ª 2011 The Society for Applied Microbiology
M.C. Roberts et al. MRSA from environmental nonhospital surfaces

number of different antibiotic resistance genes carried. All Lozano et al. 2009). This is the first report of the animal
three were ACME positive and isolates 20 and 26 were clone ST97 contaminating urban environmental surfaces.
USA300 (Table 1). Finding three animal associated isolates contaminating an
Five other university samples were MRSA positive and urban University environment was unexpected especially
represented three different ST types (ST5, ST8, ST97). because the ST97 isolates (3-8, 3-10 and 3-6) were taken
Each of these isolates carried ‡1 other antibiotic resis- from three different University Campus Sites. Two of the
tance gene(s). Isolate 8–509 was ST8, PVL+, SCCmec type isolates, 3-8 and 3-10, likely represent a single clone sug-
IV, USA300 and carried aminoglycoside, macrolide and gesting a common source, while the third isolate was
tetracycline resistance genes (Table 1). Two university unrelated. The university is a commuter school with stu-
samples contained two different MRSA strains each [3-22, dents, staff and faculty travelling from surrounding urban
3-36 and 3-2, 3-8]. The isolates 3-22, 3-36 differed from and rural communities. Thus, the possibility that the
each other by SCCmec type (IV vs NT), differed by PFGE three ST97 MRSA isolates originated in animals and ⁄ or
profile, relatedness to USA300, the presence of the ACME food and were transferred to the contaminated surfaces in
element and the number of antibiotic resistance genes the study is an intriguing hypothesis although it would be
carried and likely represent different strains even though difficult to prove.
both were ST5 (Table 1). The second two isolates, 3-2, Early studies on community-acquired USA300 found
3-6, differed by SCCmec type (I vs NT), ST type (ST8 vs that these isolates were usually susceptible to other classes
ST97), PFGE profile and the number of antibiotic resis- of antibiotics (Eady and Cove 2003). However, in a more
tance genes carried and likely represent different strains. recent study in fire stations, environmental USA300 iso-
lates were multidrug resistant as was found in the current
study (Roberts et al. 2011b). Among all the MRSA
Community surfaces
isolates, 23 (96%, n = 24) carried ‡1 other antibiotic
From the 130 community surfaces, 120 of the samples resistance gene(s) with 92%, n = 24 carrying tetracycline,
were taken from ATM keypads sampled in 2009 and 2010 and 79%, n = 24 carrying macrolide resistance genes and
and ten were from other surfaces (Table 1). Two of 120 similar to what has previously been found on other high-
(1Æ7%) ATM keypad samples were MRSA positive and 11 touched environmental surfaces (Roberts et al. 2011b).
of 120 (9Æ2%) were MSSA positive. The two MRSA iso- USA300 MRSA was isolated from university, student
lates differed in SCCmec type (IV vs NT), ST type (ST5 vs homes and the community environmental samples.
ST8), PFGE pattern and antibiotic resistance genes they Five (63%, n = 8) student homes had 1–3 MRSA-
carried. One strain #40 was USA300, while the second positive samples and included both students who lived in
strain #55 was not related to USA300 (Table 1). The two their family homes and students living with multiple stu-
MRSA isolates, 5-3 and 5-4, from the library computer dent roommates. Although this is a very small study, it
touch screen came from the same sample and were was >2-fold higher than what was identified by Scott
SCCmec type IV, ST30, and had the same PFGE pattern, et al. (2009) which identified MRSA in nine (26%) homes
suggesting that they represented a single strain even if samples (Scott et al. 2009). In the current study, three of
though the isolates differed in the number of antibiotic the homes had multiple samples that were MRSA posi-
resistance genes each carried. tive. Of the five homes, two were contaminated with
USA300 strains, and four of five homes had MRSA with
SCCmec type IV. The MRSA isolates from Student #2
home were indistinguishable from each other, suggesting
This is one of the first studies to isolate and molecularly they represented the same strain from two different sam-
characterize MRSA from nonhealthcare environmental ples. The MRSA isolates from Student # 3 and #4 homes
surfaces. SCCmec typeable isolates [I or IV] were found did differ, but overall the data suggest that the isolates
in 66% of the isolates, with 46% of the isolates USA300 from each home were clonally related. The MRSA isolates
and 92% ACME +. The five of the six MLST types (ST5, from Student # 3 home were genetically related to two of
ST8, ST30, ST45, ST931) found in the current study are the university campus MRSA isolates; however, because
associated with humans and include widely disseminated they were all USA300, it is unclear whether the home and
ST types of CA-MRSA found throughout the world university isolates shared a common source. The Scott
(Tavares et al. 2010; te Witt et al. 2009). In contrast, et al.’s (2009) study did not characterize the MRSA
ST97 is closely associated with cattle and more recently isolates recovered, so it is unknown whether the same
described in both healthy and diseased pigs, although it strain was found in multiple locations within the MRSA-
has not been found contaminating food nor associated positive homes, or whether any of the isolates were
with humans as ST398 has (Gomez-Sanz et al. 2010; SCCmec type IV or USA300.

ª 2011 The Authors

Journal of Applied Microbiology 110, 1531–1537 ª 2011 The Society for Applied Microbiology 1535
MRSA from environmental nonhospital surfaces M.C. Roberts et al.

None of the students that sampled their homes had a Brown, R., Minnon, J., Scheider, S. and Vaughn, J. (2010)
MRSA infection although one student (#2) was colonized Prevalence of methicillin-resistant Staphylococcus aureus in
with a MRSA strain that was genetically distinct in all ambulances in southern Maine. Prehosp Emerg Care 14,
characteristics from the home isolates (unpublished data). 176–181.
In the current small study, the undergraduate student Desai, R., Agoplian, J., Pannaraj, P.S., Liu, G.Y. and Miller,
MRSA carriage rate was 12Æ5% which was higher than a L.G. (2009) Survival and transmission of community-
previous study among Texas University students of 7Æ3% associated methicillin-resistant Staphylococcus aureus from
carriage rate (Rohde et al. 2009), but lower than the 21% fomites. # K-1595 from the 49th ICAAC Abstracts.
Diep, B.A., Gill, S.R., Chang, R.F., Phan, T.H., Chen, J.H.,
carriage rate found in dental students (Roberts et al.
Davidson, M.G., Lin, F., Lin, J. et al. (2006) Complete
2011a). A larger study examining more college students
genome sequence of USA300, an epidemic clone of
and student houses is needed to determine whether
community-acquired methicillin-resistant Staphylococcus
college students are at increased risk of MRSA infection.
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ª 2011 The Authors

Journal of Applied Microbiology 110, 1531–1537 ª 2011 The Society for Applied Microbiology 1537