0095-1137/11/$12.00
doi:10.1128/JCM.05323-11
Copyright © 2011, American Society for Microbiology. All Rights Reserved.
Evaluation of the Impact of Direct Plating, Broth Enrichment, and
Specimen Source on Recovery and Diversity of
Methicillin-Resistant Staphylococcus aureus
Isolates among HIV-Infected Outpatients
䌤
S. K. McAllister,
1V. S. Albrecht,
1G. E. Fosheim,
1H. K. Lowery,
2P. J. Peters,
1R. Gorwitz,
1J. L. Guest,
2J. Hageman,
1R. Mindley,
2L. K. McDougal, D. Rimland,
2and B. Limbago
1*
Centers for Disease Control and Prevention, Atlanta, Georgia,
1and Veterans Affairs Medical Center, Atlanta, Georgia
2Received 2 August 2011/Returned for modification 29 August 2011/Accepted 28 September 2011
We compared recovery of Staphylococcus aureus and methicillin-resistant S. aureus (MRSA) from nasal and
groin swab specimens of 600 HIV-infected outpatients by selective and nonselective direct plating and broth
enrichment. Swabs were collected at baseline, 6-month, and 12-month visits and cultured by direct plating to
mannitol salt agar (MSA) and CHROMagar MRSA (CM) and overnight broth enrichment with subculture to
MSA (broth). MRSA isolates were characterized by pulsed-field gel electrophoresis (PFGE), staphylococcal
cassette chromosome mec (SCCmec) typing, and PCR for the Panton-Valentine leukocidin. At each visit, 13 to
15% of patients were colonized with MRSA and 30 to 33% were colonized with methicillin-susceptible S. aureus
(MSSA). Broth, CM, and MSA detected 95%, 82%, and 76% of MRSA-positive specimens, respectively. MRSA
recovery was significantly higher from broth than CM (P
< 0.001) or MSA (P < 0.001); there was no significant
difference in recovery between MSA and CM. MSSA recovery also increased significantly when using broth
than when using MSA (P
< 0.001). Among specimens collected from the groin, broth, CM, and MSA detected
88%, 54%, and 49% of the MRSA-positive isolates, respectively. Broth enrichment had a greater impact on
recovery of MRSA from the groin than from the nose compared to both CM (P
< 0.001) and MSA (P < 0.001).
Overall, 19% of MRSA-colonized patients would have been missed with nasal swab specimen culture only.
USA500/Iberian and USA300 were the most common MRSA strains recovered, and USA300 was more likely
than other strain types to be recovered from the groin than from the nose (P
ⴝ 0.05).
Methicillin-resistant Staphylococcus aureus (MRSA) is an
important pathogen in both health care and community
set-tings. According to the National Healthcare Safety Network
(NHSN) annual update, S. aureus accounts for 15% of health
care-acquired infections in the United States; 50 to 60% of
these S. aureus isolates are MRSA (20). S. aureus is known to
colonize the nares of approximately 30 to 35% of healthy
persons, and estimates for MRSA colonization range from 1 to
9%, depending on the study group (11, 12, 18, 26, 27, 42). S.
aureus colonization is associated with an increased risk of
sub-sequent staphylococcal infection in patients in intensive care
units and following hospitalization or surgery (22, 44, 53).
For more than a decade, community-associated MRSA
(CA-MRSA) has been the leading cause of skin and soft tissue
infections among healthy individuals and selected groups,
in-cluding athletes, intravenous drug users, inmates, and men who
have sex with men (1–5, 24, 29, 32, 38). The predominant
pulsed-field gel electrophoresis (PFGE) type associated with
CA-MRSA in the United States is USA300 (35), which
typi-cally contains the Panton-Valentine leukocidin (PVL) toxin
and staphylococcal cassette chromosome mec (SCCmec) type
IVa (SCCmec IVa) (13, 25, 52). MRSA carriage is increasing
among persons in the community (18, 27), and recent reports
have noted an increased isolation of USA300 S. aureus in
health care settings (17, 21, 23, 39, 47).
In 2003, the Society for Healthcare Epidemiology of
Amer-ica (SHEA) recommended the collection of samples for
sur-veillance cultures at hospital admission for patients at high risk
for MRSA carriage (40). Although active surveillance for
MRSA is recommended, there are no standard methods for
the recovery of MRSA from surveillance cultures. The anterior
nares are considered the primary reservoir for S. aureus
colo-nization; however, several studies have suggested that
CA-MRSA may preferentially colonize other body sites, including
throat, tonsils, rectum, and groin; this has been noted in
spe-cific groups, including infants, children, and HIV-infected
in-dividuals (6, 7, 14, 15, 37, 42, 51).
As part of a study of MRSA colonization in HIV-infected
outpatients (45), we compared recovery of MRSA and
meth-icillin-susceptible S. aureus (MSSA) from nasal and groin swab
specimens taken at three different collection times over a
1-year period and cultured with selective and nonselective
di-rect plating methods and a broth enrichment method. MRSA
isolates were characterized by PFGE, SCCmec typing, and
PCR for PVL.
MATERIALS AND METHODS
Specimen collection and culture.Nasal and groin swab specimens for culture of S. aureus were collected from a study population of 600 HIV-infected outpa-tients at the Atlanta, GA, Veterans Affairs Medical Center (VAMC). Swabs
* Corresponding author. Mailing address: Division of Healthcare
Quality Promotion, Centers for Disease Control and Prevention, 1600
Clifton Rd. NE, MS C16, Atlanta, GA 30329. Phone: (404) 639-2162.
Fax: (404) 718-2174. E-mail: [email protected].
䌤
Published ahead of print on 12 October 2011.
4126
on March 14, 2021 by guest
http://jcm.asm.org/
were collected at the enrollment (n⫽ 600), 6-month (n ⫽ 502), and 12-month
(n⫽ 427) visits between September 2007 and June 2009. Sterile rayon swabs with
liquid Stuart’s transport medium (Becton Dickinson, Sparks, MD) were used to swab the anterior nares (collected by clinic personnel) and the groin (self-collected from the skin folds between the thigh and the genital area) and then stored at 4°C for up to 7 days. Swabs were then plated directly to mannitol salt agar (MSA; Becton Dickinson) and CHROMagar MRSA (CM; Becton Dickin-son), before being placed in Trypticase soy broth containing 6.5% sodium chlo-ride (broth; Becton Dickinson); all cultures were incubated overnight at 35°C. Following overnight incubation, broths were subcultured to MSA and incubated as described above.
CM plates were examined at 24 and 48 h for mauve-colored colonies, which were subcultured on Trypticase soy agar with 5% sheep blood (blood agar plates [BAPs]; Becton Dickinson). MSA plates were examined at 48 h for gold or yellow colonies, which were subcultured on BAPs. Presumptive S. aureus isolates from BAPs were examined for morphology consistent with S. aureus; identification was confirmed by a positive Staphaurex latex agglutination test (Remel, Lenexa, KS).
All S. aureus isolates were frozen at⫺70°C until further characterization.
Growth of any staphylococci on direct plating to MSA was used as an indicator of specimen integrity and S. aureus viability. Potential variation in bacterial growth from swabs stored at 4°C for up to 7 days was assessed by comparing the distribution of cultures positive for S. aureus among swabs stored for 1 to 3 days with the distribution of those stored for 4 to 7 days prior to culture as described above.
Isolate characterization.Methicillin resistance was determined using the ce-foxitin disk-diffusion test following Clinical and Laboratory Standards Institute (CLSI) guidelines (9). MRSA isolates were genotyped by PFGE using SmaI (New England BioLabs, Beverly, MA) digestion as described previously (35). PFGE patterns were analyzed with BioNumerics software (version 5.10; Applied Maths, Austin, TX) and were assigned to USA pulsed-field types using Dice coefficients and 80% relatedness. USA500, Iberian, and Archaic PFGE types were grouped together as USA500/Iberian because they are closely related and difficult to separate by PFGE. The SCCmec type and the presence of PVL were determined for all isolates using PCR, as described previously (16, 31). For the purposes of this paper, USA300 was defined as an isolate with a USA300 PFGE pattern that was PVL positive and contained SCCmec IVa.
Statistical analysis.A patient was defined to be colonized for the purpose of prevalence if S. aureus was detected at either body site at each collection or at any collection for the overall colonization prevalence (Table 1). For the deter-mination of overall prevalence, each patient could be counted only once. Sensi-tivity of culture methods was based on aggregate data from all collection periods. The number of positive culture results per body site for the method evaluated was compared to the number of positive results from that body site detected by any method (Table 2). Prevalence of MRSA strain types was determined by counting all unique PFGE types isolated per sample type from each collection period (Table 3). Sampling methods were compared by the dependent Z test for proportion. Distribution of strain types by body site was evaluated using the
chi-square test. The null hypothesis was rejected at P values ofⱕ0.05. The
potential impact of storage of the swabs at 4°C on recovery of S. aureus was examined using a chi-square test comparing swabs stored for 1 to 3 days and those stored for 4 to 7 days prior to culture.
RESULTS
Prevalence of S. aureus among HIV-infected outpatients.
MRSA colonization at any site averaged 13.7% per collection,
for an overall MRSA colonization prevalence of 21.3% of
subjects over the course of the 1-year study (Table 1). MSSA
colonization averaged 31.7% at each collection time, with
46.5% of patients colonized over the course of the study. As
expected, S. aureus carriage was higher in the nose than in the
groin, although inclusion of culture of specimens from the
groin site enhanced detection of both MRSA and MSSA
com-pared to nasal specimen culture alone. The frequency of nasal
and groin carriage did not vary between collections for MRSA
or MSSA. Nasal carriage prevalence of MRSA at each
collec-tion averaged 11.0%, compared to 8.2% groin carriage, and
MSSA nasal carriage prevalence averaged 27.2%, compared to
TABLE 1. Asymptomatic colonization of HIV-infected patients with S. aureus in the nose and groin
Collection period
Total no. of isolates
Nose Groin Any site
MRSA MSSA MRSA MSSA MRSA MSSA
No. of positive patients % No. of positive patients % No. of positive patients % No. of positive patients % No. of positive patients % No. of positive patients %
Primary
600
66
11.0
165
27.5
49
8.2
110
18.3
79
13.2
191
31.8
6-mo visit
502
50
10.0
145
28.9
46
9.2
94
18.7
67
13.3
167
33.3
12-mo visit
427
52
12.2
108
25.3
28
6.6
76
17.8
62
14.5
128
30.0
Avg
a11.1
27.2
8.0
18.3
13.7
31.7
Overall
b600
101
16.8
245
40.8
91
15.2
183
30.5
128
21.3
279
46.5
aAverage prevalence over three collections.
bEach patient was counted only once for the purpose of overall prevalence.
TABLE 2. Comparison of culture methods for recovery of S. aureus from asymptomatically colonized HIV-infected patients
Collection site or parameter
No. (%) of patients Total no. of isolates
CMadirect, MRSA MSA
b
direct Broth⫹ MSAc
MRSA MSSA MRSA MSSA MRSA MSSA
Nose
169
418
148 (87.6)
139 (82.2)
363 (86.8)
160 (94.7)
418 (100)
Groin
127
280
68 (53.5)
62 (48.8)
136 (48.6)
112 (88.2)
280 (100)
Total S. aureus
296
698
216 (73.0)
201 (67.9)
499 (71.5)
272 (91.9)
698 (100)
Positive patients
208
482
170 (81.7)
159 (76.4)
395 (82.0)
198 (95.2)
482 (100)
a CM, CHROMagar MRSA. bMSA, mannitol salt agar.
c
Broth⫹ MSA, 6.5% NaCl–Trypticase soy broth enrichment, followed by plating on mannitol salt agar.
on March 14, 2021 by guest
http://jcm.asm.org/
18.3% groin carriage. Overall, MRSA and MSSA prevalence
rates were 16.8% and 40.8%, respectively, for the nares, and
15.2% and 30.5%, respectively, for the groin. Inclusion of
cul-ture of specimens from the groin site increased the number of
colonized patients detected by 26.7% for MRSA and 13.8% for
MSSA. Seventeen patients (2.8% of patients enrolled; 6.1% of
MRSA-positive patients) were cocolonized with MSSA and
MRSA in the nares, groin, or both.
Culture methods.
A total of 296 MRSA and 698 MSSA
isolates were recovered from among the 1,529 nasal and groin
swab specimen cultures performed (Table 2). The broth
method detected 272 of 296 (91.9%) MRSA-positive
speci-mens, direct MSA detected 201 (67.9%), and CM detected 216
(73.0%) (Table 2). Broth was more sensitive than CM or MSA
for groin swab specimen cultures (P
⬍ 0.0001) and for overall
MRSA recovery (P
⬍ 0.0001). When limited to only nares
swab specimen cultures, there was no significant difference in
MRSA recovery between the three methods. There was also no
significant difference in MRSA recovery between the CM and
MSA direct plating methods; this was true for both culture
sites and overall MRSA recovery. MSSA recovery was
signif-icantly increased when using broth than when using MSA
di-rect plating for both the nares and groin swab specimens and
for overall MSSA recovery (P
⫽ ⬍0.0001).
Storage of swabs at 4°C for up to 7 days prior to culture did
not appear to have a negative impact on the recovery of S.
aureus, as there was no change in recovery among those stored
for 1 to 3 days and those stored for 4 to 7 days when plated
directly to MSA (P
⫽ 0.11) or incubated in broth prior to
plating on MSA (P
⫽ 0.79). Surprisingly, there was a higher
odds of recovery for S. aureus among swabs stored for a longer
period before plating to CM (P
⫽ 0.046).
Diversity of strain types and association with culture site.
Three PFGE types predominated, accounting for
approxi-mately 95% of all MRSA isolates recovered (Table 3); these
included
USA500/Iberian
(53%),
USA300
(34%),
and
USA100 (6.4%). Although the differences at individual
collec-tions were not significantly different, overall, USA300 was
more likely than other MRSA strain types to be recovered
from the groin than from the nose (P
⬍ 0.05). Twelve of 48
(25%) patients colonized with only USA300 in the groin would
have been missed with nares swab specimen culture alone.
Although the difference in recovery between the nose and the
groin was not statistically significant for USA500/Iberian
iso-lates, 10 of 69 (14.5%) patients colonized with only USA500/
Iberian type in the groin would not have been detected with
nares swab specimen culture alone. Six patients were colonized
with more than one MRSA strain; these were detected on the
basis of different colony morphologies on MSA, and the results
were confirmed by PFGE.
DISCUSSION
Although the prevalence of MRSA colonization among
healthy persons in the U.S. population is low (0.8 to 1.5%) (18,
27), some reports suggest that it is increasing (18, 27). The
prevalence of MRSA colonization in our HIV-infected study
population was higher at all three study visits (range, 13 to
15%) than the reported rates in the community; the cumulative
MRSA prevalence was 21%. The reported prevalence of
MRSA colonization in HIV-infected adults varies widely and
has been reported to be as low as 2 to 4% in Boston, MA, and
Nebraska (34, 51) and as high as 17% in Atlanta and New York
City (21, 50). This variation may be due to factors associated
with HIV status or local MRSA colonization pressure, but is
also likely to reflect the number and source of the swab
spec-imens taken and the method used for culture, as well as the
natural dynamics of human carriage of S. aureus (26, 45).
Numerous clinical laboratory studies have compared
chro-mogenic or selective media for the recovery of MRSA, but
most used isolates from culture collections or cultures of
spec-imens taken from clinical infections or from populations with
high MRSA colonization rates (19, 33, 46, 50). It is difficult to
compare the results of these studies to MRSA recovery from
surveillance samples, which are often from populations with
low MRSA prevalence.
We found that broth enrichment was more sensitive than
direct plating to MSA or CM for detection of MRSA and
MSSA colonization. Overall, broth enrichment increased
sen-sitivity 19% compared to the use of CM and 24% compared to
the use of MSA for recovery of MRSA; the MSSA recovery
rate increased 29% with broth enrichment compared to direct
plating on MSA. Safdar et al. evaluated 32 different
microbi-ological techniques, including broth enrichment, for detection
of MRSA nasal carriage in hospitalized patients and also found
an increase of 7 to 14% in sensitivity when broth enrichment
TABLE 3. Prevalence of MRSA strain types among isolates recovered from nose and groin
USA type
No. (%) of isolatesa
T0 T6 T12 Overall
Groin Nose Groin Nose Groin Nose Groin Nose
USA300
25 (48.1)
20 (30.3)
19 (40.4)
17 (33.3)
9 (32.1)
12 (23.1)
53 (41.7)
49 (29.0)
USA500/Iberian
21 (40.4)
39 (59.1)
24 (51.1)
29 (56.9)
16 (57.1)
29 (55.8)
61 (48.0)
97 (57.4)
USA100
3 (5.8)
4 (6.1)
2 (4.3)
3 (5.9)
2 (7.1)
5 (9.6)
7 (5.5)
12 (7.1)
USA800
1 (1.9)
1 (1.5)
0 (0)
1 (2.0)
1 (3.6)
4 (7.6)
2 (1.6)
6 (3.6)
USA1000
2 (3.8)
1 (1.5)
1 (2.1)
0 (0)
0 (0)
0 (0)
3 (2.4)
1 (0.6)
USA700
0 (0)
1 (1.5)
1 (2.1)
1 (2.0)
0 (0)
1 (1.9)
1 (0.8)
3 (1.8)
USA600
0 (0)
0 (0)
0 (0)
0 (0)
0 (0)
1 (1.9)
0 (0)
1 (0.6)
Total
52
66
47
51
28
52
127
169
aT0, T6, and T12, primary, 6-month, and 12-month visits, respectively.
on March 14, 2021 by guest
http://jcm.asm.org/
was compared to direct plating (48). Other studies comparing
broth enrichment to direct plating for MRSA recovery have
reported a wide variation in sensitivity, ranging from a
de-crease of 4% to an inde-crease of 20% (10, 30, 41, 43). The
dramatic differences in recovery from broth enrichment that
we observed may reflect low numbers of MRSA present in
groin swab samples which could be missed by direct plating, as
the increase in sensitivity between direct plating and broth
enrichment was most noticeable from groin swab samples.
Among the 19 MRSA isolates identified with CM but not
detected with broth enrichment in our study, 14 (74%)
oc-curred when patients were cocolonized with MRSA and
MSSA. We hypothesize that in these instances, small amounts
of MRSA could be if missed if abundant MSSA is present in
the original sample.
Although MSA requires up to 48 h of incubation and some
experience for optimal use, it allows one to detect both MSSA
and MRSA, and variations in the color and intensity produced
by different S. aureus strains on the same plate can be
distin-guished. CM is approximately four times the cost of MSA, but
the result is easy to interpret and can be read at 24 h. A
limitation of our study is the lack of specificity data for the
recovery of MRSA from the three methods that we employed.
The primary goal of our study was to identify all S. aureus
carriage. Because of this, we erred on the side of oversampling
by subculturing all suspicious isolates grown on CM and MSA
and using a latex agglutination test to rule out
coagulase-negative staphylococci. We found that the most sensitive
method for recovery of MRSA and MSSA was broth
enrich-ment and then plating to MSA, but broth enrichenrich-ment and
plating to CM or use of MRSA-specific broth enrichment
might be the most sensitive for recovery of MRSA only. Only
one swab did not yield any Staphylococcus species when plated
directly to MSA (data not shown), and we observed no
de-creased S. aureus yield when swabs were stored under
refrig-eration for up to 7 days. Thus, weekly batch culturing of swabs
might be a practical approach for detecting S. aureus
coloni-zation in large-scale or multisite surveillance studies.
The addition of a groin swab specimen culture in our study
dramatically enhanced recovery of both MRSA and MSSA.
Other studies have reported increased sensitivity when
multi-ple body sites were sammulti-pled. Several studies have
demon-strated that culture of samples from additional body sites, such
as the throat, axilla, perineum, or groin, in addition to the
nares, increased the sensitivity of S. aureus detection, with
improvements ranging from 5 to 25% (6, 28, 37). However,
others have found that the addition of a specimen from a
second body site had little impact on the overall sensitivity of
MRSA recovery (8). Although other colonization studies have
demonstrated a dramatic increase in MRSA detection when
throat swabs were cultured in addition to the nasal swabs, we
specifically sought to address the impact of carriage site on
MRSA strain types and thought that strains carried in the nose
and throat were likely to be the same. Inclusion of a groin swab
specimen culture in our population not only increased the
overall recovery of MRSA but also specifically increased
re-covery of PVL-positive USA300 strains. Overall, 41.7% of
MRSA strains recovered from the groin were USA300,
com-pared to 29.0% from the nose. Similar findings have been
reported; Lautenbach et al. found that a larger percentage of
CA-MRSA was isolated from the groin and perineum than the
nares, throat, and axilla (28), and a recent study by Faden and
colleagues found an association between rectal, but not nasal,
MRSA carriage and S. aureus skin and soft tissue infection in
children (15). At 11.5% prevalence, the USA500/Iberian type
was the most frequently isolated strain in our population,
rep-resenting 48.0% of the MRSA isolates recovered from the
groin and 57.4% from the nares. This is higher than the
re-ported prevalence of USA500 among HIV-infected patients in
Dallas, TX, and New York City (range, 4.8 to 5.6%) (8, 49) but
lower than the reported prevalence (19%) among general
pa-tients screened at admission to another Atlanta-area hospital
(21), and both USA300 and USA500 colonization has been
associated with HIV infection (36).
In summary, the rate of MRSA colonization among our
cohort of HIV-infected outpatients was higher than that which
has been reported for the healthy U.S. population and for
other groups of HIV-infected individuals. Broth enrichment
significantly increased detection of MRSA and MSSA
com-pared to direct plating, and we saw no difference in sensitivity
of direct plating to CM or MSA. Inclusion of a groin swab
specimen also increased MRSA detection and specifically
in-creased detection of PVL-positive USA300 strains. Thus, the
impact on both strain diversity and overall sensitivity should be
considered when selecting body sites for MRSA sampling.
ACKNOWLEDGMENT
The findings and conclusions in this report are those of the authors
and do not necessarily represent the official position of the Centers for
Disease Control and Prevention.
REFERENCES
1. Anonymous. 1999. Four pediatric deaths from community-acquired methi-cillin-resistant Staphylococcus aureus—Minnesota and North Dakota, 1997-1999. MMWR Morb. Mortal. Wkly. Rep. 48:707–710.
2. Anonymous. 2003. Methicillin-resistant Staphylococcus aureus infections among competitive sports participants—Colorado, Indiana, Pennsylvania, and Los Angeles County, 2000-2003. MMWR Morb. Mortal. Wkly. Rep.
52:793–795.
3. Anonymous. 2003. Methicillin-resistant Staphylococcus aureus infections in correctional facilities—Georgia, California, and Texas, 2001-2003. MMWR Morb. Mortal. Wkly. Rep. 52:992–996.
4. Anonymous. 2001. Methicillin-resistant Staphylococcus aureus skin or soft tissue infections in a state prison—Mississippi, 2000. MMWR Morb. Mortal. Wkly. Rep. 50:919–922.
5. Anonymous. 2003. Outbreaks of community-associated methicillin-resistant Staphylococcus aureus skin infections—Los Angeles County, California, 2002-2003. MMWR Morb. Mortal. Wkly. Rep. 52:88.
6. Bitterman, Y., A. Laor, S. Itzhaki, and G. Weber. 2010. Characterization of the best anatomical sites in screening for methicillin-resistant Staphylococcus
aureus colonization. Eur. J. Clin. Microbiol. Infect. Dis. 29:391–397.
7. Brook, I., and P. A. Foote. 2006. Isolation of methicillin resistant
Staphylo-coccus aureus from the surface and core of tonsils in children. Int. J. Pediatr.
Otorhinolaryngol. 70:2099–2102.
8. Cenizal, M. J., R. D. Hardy, M. Anderson, K. Katz, and D. J. Skiest. 2008. Prevalence of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) nasal colonization in HIV-infected ambulatory patients. J. Acquir. Immune Defic. Syndr. 48:567–571.
9. CLSI. 2009. M100-S19. Performance standards for antimicrobial susceptibil-ity testing; 17th informational supplement. Clinical and Laboratory Stan-dards Institute, Wayne, PA.
10. Compernolle, V., G. Verschraegen, and G. Claeys. 2007. Combined use of Pastorex Staph-Plus and either of two new chromogenic agars, MRSA ID and CHROMagar MRSA, for detection of methicillin-resistant
Staphylococ-cus aureus. J. Clin. Microbiol. 45:154–158.
11. Creech, C. B., II, D. S. Kernodle, A. Alsentzer, C. Wilson, and K. M.
Edwards. 2005. Increasing rates of nasal carriage of methicillin-resistant
Staphylococcus aureus in healthy children. Pediatr. Infect. Dis. J. 24:617–621.
12. Davis, K. A., J. J. Stewart, H. K. Crouch, C. E. Florez, and D. R. Hospenthal. 2004. Methicillin-resistant Staphylococcus aureus (MRSA) nares
on March 14, 2021 by guest
http://jcm.asm.org/
tion at hospital admission and its effect on subsequent MRSA infection. Clin. Infect. Dis. 39:776–782.
13. Diep, B. A., G. F. Sensabaugh, N. Somboonna, H. A. Carleton, and F.
Perdreau-Remington.2004. Widespread skin and soft-tissue infections due to two methicillin-resistant Staphylococcus aureus strains harboring the genes for Panton-Valentine leucocidin. J. Clin. Microbiol. 42:2080–2084. 14. Eveillard, M., et al. 2006. Evaluation of a strategy of screening multiple
anatomical sites for methicillin-resistant Staphylococcus aureus at admission to a teaching hospital. Infect. Control Hosp. Epidemiol. 27:181–184. 15. Faden, H., et al. 2010. Importance of colonization site in the current
epi-demic of staphylococcal skin abscesses. Pediatrics 125:e618–e624. 16. Fosheim, G. E., A. G. Nicholson, V. Albrechy, and B. M. Limbago. 2011. A
multiplex real-time PCR assay for detection of methicillin-resistant
Staphy-lococcus aureus and associated toxin genes. J. Clin. Microbiol. 49:3071–3073.
17. Freitas, E. A., R. M. Harris, R. K. Blake, and C. D. Salgado. 2010. Preva-lence of USA300 strain type of methicillin-resistant Staphylococcus aureus among patients with nasal colonization identified with active surveillance. Infect. Control Hosp. Epidemiol. 31:469–475.
18. Gorwitz, R. J., et al. 2008. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J. Infect. Dis.
197:1226–1234.
19. Han, Z., E. Lautenbach, N. Fishman, and I. Nachamkin. 2007. Evaluation of mannitol salt agar, CHROMagar Staph aureus and CHROMagar MRSA for detection of meticillin-resistant Staphylococcus aureus from nasal swab spec-imens. J. Med. Microbiol. 56:43–46.
20. Hidron, A. I., et al. 2008. NHSN annual update: antimicrobial-resistant pathogens associated with healthcare-associated infections: annual summary of data reported to the National Healthcare Safety Network at the Centers for Disease Control and Prevention, 2006-2007. Infect. Control Hosp. Epi-demiol. 29:996–1011.
21. Hidron, A. I., et al. 2005. Risk factors for colonization with methicillin-resistant Staphylococcus aureus (MRSA) in patients admitted to an urban hospital: emergence of community-associated MRSA nasal carriage. Clin. Infect. Dis. 41:159–166.
22. Huang, S. S., and R. Platt. 2003. Risk of methicillin-resistant Staphylococcus aureus infection after previous infection or colonization. Clin. Infect. Dis.
36:281–285.
23. Jenkins, T. C., et al. 2009. Epidemiology of healthcare-associated blood-stream infection caused by USA300 strains of methicillin-resistant Staphy-lococcus aureus in 3 affiliated hospitals. Infect. Control Hosp. Epidemiol.
30:233–241.
24. Kazakova, S. V., et al. 2005. A clone of methicillin-resistant Staphylococcus aureus among professional football players. N. Engl. J. Med. 352:468–475. 25. King, M. D., et al. 2006. Emergence of community-acquired
methicillin-resistant Staphylococcus aureus USA 300 clone as the predominant cause of skin and soft-tissue infections. Ann. Intern. Med. 144:309–317.
26. Kluytmans, J., A. van Belkum, and H. Verbrugh. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associ-ated risks. Clin. Microbiol. Rev. 10:505–520.
27. Kuehnert, M. J., et al. 2006. Prevalence of Staphylococcus aureus nasal colonization in the United States, 2001-2002. J. Infect. Dis. 193:172–179. 28. Lautenbach, E., et al. 2009. Surveillance cultures for detection of
methicillin-resistant Staphylococcus aureus: diagnostic yield of anatomic sites and com-parison of provider- and patient-collected samples. Infect. Control Hosp. Epidemiol. 30:380–382.
29. Lee, N. E., et al. 2005. Risk factors for community-associated methicillin-resistant Staphylococcus aureus skin infections among HIV-positive men who have sex with men. Clin. Infect. Dis. 40:1529–1534.
30. Lee, S., et al. 2008. Comparison of culture screening protocols for methicil-lin-resistant Staphylococcus aureus (MRSA) using a chromogenic agar (MRSA-Select). Ann. Clin. Lab. Sci. 38:254–257.
31. Limbago, B., et al. 2009. Characterization of methicillin-resistant Staphylo-coccus aureus isolates collected in 2005 and 2006 from patients with invasive disease: a population-based analysis. J. Clin. Microbiol. 47:1344–1351. 32. Lindenmayer, J. M., S. Schoenfeld, R. O’Grady, and J. K. Carney. 1998.
Methicillin-resistant Staphylococcus aureus in a high school wrestling team and the surrounding community. Arch. Intern. Med. 158:895–899. 33. Louie, L., D. Soares, H. Meaney, M. Vearncombe, and A. E. Simor. 2006.
Evaluation of a new chromogenic medium, MRSA Select, for detection of
methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 44:4561– 4563.
34. Madariaga, M. G., F. Ullrich, and S. Swindells. 2009. Low prevalence of community-acquired methicillin-resistant Staphylococcus aureus coloniza-tion and apparent lack of correlacoloniza-tion with sexual behavior among HIV-infected patients in Nebraska. Clin. Infect. Dis. 48:1485–1487.
35. McDougal, L. K., et al. 2003. Pulsed-field gel electrophoresis typing of oxacillin-resistant Staphylococcus aureus isolates from the United States: establishing a national database. J. Clin. Microbiol. 41:5113–5120. 36. Mermel, L. A., et al. 2010. Quantitative analysis and molecular fingerprinting
of methicillin-resistant Staphylococcus aureus nasal colonization in different patient populations: a prospective, multicenter study. Infect. Control Hosp. Epidemiol. 31:592–597.
37. Mertz, D., et al. 2007. Throat swabs are necessary to reliably detect carriers of Staphylococcus aureus. Clin. Infect. Dis. 45:475–477.
38. Moran, G. J., R. N. Amii, F. M. Abrahamian, and D. A. Talan. 2005. Methicillresistant Staphylococcus aureus in community-acquired skin in-fections. Emerg. Infect. Dis. 11:928–930.
39. Moran, G. J., et al. 2006. Methicillin-resistant S. aureus infections among patients in the emergency department. N. Engl. J. Med. 355:666–674. 40. Muto, C. A., et al. 2003. SHEA guideline for preventing nosocomial
trans-mission of multidrug-resistant strains of Staphylococcus aureus and entero-coccus. Infect. Control Hosp. Epidemiol. 24:362–386.
41. Nahimana, I., P. Francioli, and D. S. Blanc. 2006. Evaluation of three chromogenic media (MRSA-ID, MRSA-Select and CHROMagar MRSA) and ORSAB for surveillance cultures of methicillin-resistant Staphylococcus aureus. Clin. Microbiol. Infect. 12:1168–1174.
42. Nilsson, P., and T. Ripa. 2006. Staphylococcus aureus throat colonization is more frequent than colonization in the anterior nares. J. Clin. Microbiol.
44:3334–3339.
43. Nonhoff, C., et al. 2009. Comparison of three chromogenic media and en-richment broth media for the detection of methicillin-resistant Staphylococ-cus aureus from mucocutaneous screening specimens: comparison of MRSA chromogenic media. Eur. J. Clin. Microbiol. Infect. Dis. 28:363–369. 44. Patel, M., J. D. Weinheimer, K. B. Waites, and J. W. Baddley. 2008. Active
surveillance to determine the impact of methicillin-resistant Staphylococcus aureus colonization on patients in intensive care units of a Veterans Affairs Medical Center. Infect. Control Hosp. Epidemiol. 29:503–509.
45. Peters, P. J., et al. 2011. Methicillin-resistant Staphylococcus aureus coloni-zation in HIV-infected outpatients is common and detection is enhanced by groin culture. Epidemiol. Infect. 139:998–1008.
46. Peterson, J. F., et al. 2010. Spectra MRSA, a new chromogenic agar medium to screen for methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol.
48:215–219.
47. Popovich, K. J., R. A. Weinstein, and B. Hota. 2008. Are community-asso-ciated methicillin-resistant Staphylococcus aureus (MRSA) strains replacing traditional nosocomial MRSA strains? Clin. Infect. Dis. 46:787–794. 48. Safdar, N., L. Narans, B. Gordon, and D. G. Maki. 2003. Comparison of
culture screening methods for detection of nasal carriage of methicillin-resistant Staphylococcus aureus: a prospective study comparing 32 methods. J. Clin. Microbiol. 41:3163–3166.
49. Shet, A., et al. 2009. Colonization and subsequent skin and soft tissue infec-tion due to methicillin-resistant Staphylococcus aureus in a cohort of other-wise healthy adults infected with HIV type 1. J. Infect. Dis. 200:88–93. 50. Stoakes, L., et al. 2006. Prospective comparison of a new chromogenic
medium, MRSASelect, to CHROMagar MRSA and mannitol-salt medium supplemented with oxacillin or cefoxitin for detection of methicillin-resistant Staphylococcus aureus. J. Clin. Microbiol. 44:637–639.
51. Szumowski, J. D., et al. 2009. Methicillin-resistant Staphylococcus aureus colonization, behavioral risk factors, and skin and soft-tissue infection at an ambulatory clinic serving a large population of HIV-infected men who have sex with men. Clin. Infect. Dis. 49:118–121.
52. Vandenesch, F., et al. 2003. Community-acquired methicillin-resistant Staph-ylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg. Infect. Dis. 9:978–984.
53. von Eiff, C., K. Becker, K. Machka, H. Stammer, and G. Peters. 2001. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N. Engl. J. Med. 344:11–16.
