MAJOR ARTICLE

Changes in the Prevalence of Nasal Colonization

with Staphylococcus aureus in the United States,
20012004
Rachel J. Gorwitz,1 Deanna Kruszon-Moran,2 Sigrid K. McAllister,1 Geraldine McQuillan,2 Linda K. McDougal,1
Gregory E. Fosheim,1 Bette J. Jensen,1 George Killgore,1 Fred C. Tenover,1 and Matthew J. Kuehnert1
1
National Center for Preparedness, Detection, and Control of Infectious Diseases and 2National Center for Health Statistics, Centers for Disease
Control and Prevention, Atlanta, Georgia

(See the article by David et al., on pages 1235 43; the article by Emonts et al., on pages 1244 53; and the editorial
commentary by Flynn and Cohen, on pages 12179.)
Background. Staphylococcus aureus is a common cause of infection, particularly in persons colonized by this

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organism. Virulent strains of methicillin-resistant S. aureus (MRSA) have emerged in the general community.
Methods. A nationally representative survey of nasal colonization with S. aureus was conducted from 2001
through 2004 as part of the National Health and Nutrition Examination Survey. MRSA isolates were identified by the
oxacillin disk-diffusion method. The pulsed-field gel electrophoresis (PFGE) type was determined for all MRSA
isolates. A t statistic was used to compare the prevalence of colonization across biennia and across population sub-
groups. Cofactors independently associated with colonization were determined with backward stepwise logistic
modeling.
Results. The prevalence of colonization with S. aureus decreased from 32.4% in 20012002 to 28.6% in 2003
2004 (P .01), whereas the prevalence of colonization with MRSA increased from 0.8% to 1.5% (P .05). Colo-
nization with MRSA was independently associated with healthcare exposure in males and with having been born in the
United States, age 60 years, diabetes, and poverty in females. In 20032004, a total of 19.7% (95% confidence
interval, 12.4%28.8%) of MRSA-colonized persons carried a PFGE type associated with community transmission.
Conclusions. Nasal colonization with MRSA has increased in the United States, despite an overall decrease in
nasal colonization with S. aureus. PFGE types associated with community transmission only partially account for the
increase in MRSA colonization.

Staphylococcus aureus is an important cause of skin
infections and invasive diseases, such as endocarditis,
pneumonia, and osteomyelitis, in healthcare and
community settings [1]. Methicillin-resistant S. au-
reus (MRSA) isolates are resistant to all currently
Received 25 May 2007; accepted 28 September 2007; electronically published
28 March 2008.
Presented in part: National Foundation for Infectious Diseases 2007 Annual
Conference on Antimicrobial Resistance, Bethesda, Maryland 2527 June 2007
(abstract S1).
Potential conflicts of interest: None reported.
Financial support: Office of Antimicrobial Resistance, Division of Healthcare
Quality Promotion, Centers for Disease Control and Prevention.
The findings and conclusions in this report are those of the authors and do not
necessarily represent the views of the Centers for Disease Control and Prevention.
Reprints or correspondence: Rachel Gorwitz, MD, MPH, Centers for Disease
Control and Prevention, 1600 Clifton Rd. NE, MS A35, Atlanta, GA 30333
(rgorwitz@cdc.gov).
The Journal of Infectious Diseases 2008; 197:1226 34
This article is in the public domain, and no copyright is claimed.
0022-1899/2008/19708-0004
DOI: 10.1086/533494
available -lactam antimicrobial agents, including
-lactamasestable penicillins and cephalosporins,
and have been recognized as a source of healthcare-
associated infections since the 1960s [2]. More re-
cently, distinct strains of MRSA have emerged as a
cause of skin abscesses and invasive, life-threatening
infections among previously healthy persons in the
community [3, 4]. These epidemic strains were ini-
tially characterized by a lack of association with a
healthcare setting, resistance to a limited number of
non--lactam agents, presence of genes for the
Panton-Valentine leukocidin (PVL) toxin, presence
of staphylococcal cassette chromosome mec (SCC-
mec) type IV and, in the United States, pulsed-field gel
electrophoresis (PFGE) types USA300 and USA400
[5]. However, these strains are now also transmitted
in healthcare settings [6 9] and demonstrate emerg-
ing resistance to non-lactam agents [10].

1226 JID 2008:197 (1 May) Gorwitz et al.

 S. aureus may colonize the anterior nares and other body sites
[11]. Colonization is a strong risk factor for subsequent infec-
tion, although most persons colonized with the organism do not
develop clinical disease [12]. Colonization with MRSA, in par-
ticular with PFGE type USA300, may be associated with an in-
creased risk of subsequent infection, compared with coloniza-
tion with methicillin-susceptible S. aureus (MSSA) [13, 14].
The first national population-based prevalence survey of nasal
colonization with S. aureus was conducted in 2001 and 2002, and
it showed a measurable prevalence of colonization with MRSA
in the community [15]. The objectives of the current study were
to assess national changes in the overall prevalence of nasal col-
onization with S. aureus and with MRSA specifically and to de-
scribe the evolving epidemiology of nasal colonization with S.
aureus.
METHODS
Survey design and collection of data. The National Health
and Nutrition Examination Survey (NHANES) is administered
to a nationally representative sample of the civilian, noninstitu-
tionalized US population selected on the basis of a stratified,
multistage, probability cluster design. NHANES has been con-
ducted continuously since 1999 and was conducted periodically
before then. Data are collected through household interviews,
standardized physical exams, and the collection of biological
samples at mobile examination centers. A nationally representa-
tive sample is selected each year, but data are released in 2-year
cycles to protect confidentiality and to increase statistical reli-
ability. NHANES is reviewed and approved annually by an insti-
tutional review board. Informed consent is obtained from sub-
jects or their parents or guardians. Descriptions of the survey
design and sampling methods have been published elsewhere
[16].
To ensure adequate sample size, the current NHANES over-
samples low-income persons, adolescents aged 12 through 19
years, persons aged 60 years and older, non-Hispanic black per-
sons, and Mexican Americans. Weights were calculated for the
NHANES sample to account for the unequal probabilities of
selection, to adjust for nonresponse to the survey interview or
examination, and to post-stratify on the basis of the Census Bu-
reau estimates of the US population [17, 18].
Testing for nasal carriage of S. aureus was completed for all
participants aged 1 year for the years 2001 through 2004. Race
and ethnicity were defined by self report and classified as non-
Hispanic white, non-Hispanic black, or Mexican American. Per-
sons who were not classified in one of these groups were in-
cluded in the category other and were only included in
analyses when all racial ethnic groups were combined. The pov-
erty index was calculated by dividing the total family income by
the US poverty threshold, adjusted for family size. Healthcare
exposure was defined as an overnight stay in either an acute care
Changes in Prevalence of S. aureus Nasal Colonization
or a long-term healthcare facility during the 12 months before
participation in the survey. Other cofactors examined for their
association with nasal carriage included sex, age (15 years, 6 11
years, 1219 years, 20 39 years, 40 59 years, or 60 years),
place of birth (inside or outside the United States), educational
level (high school diploma or less than high school education),
history of diabetes diagnosed by a health professional, and body
mass index ([BMI] normal, 18.524.9; overweight, 2529.9;
obese 30). Educational level and BMI were analyzed only for
participants older than 19 years.
All statistical procedures were conducted using SUDAAN
(version 9.0.1; Research Triangle Institute), a family of statistical
procedures for analysis of data from complex sample surveys
[19]. Estimates of the prevalence of colonization with S. aureus
and MRSA were weighted to represent the US population; 95%
confidence intervals (CIs) were calculated by use of an exact
binomial method [20]. Standard errors were calculated by use of
the Taylor series linearization method to account for the com-
plex sample design [19]. Estimates with relative SE 30% or
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12 degrees of freedom did not meet standards of reliability or
precision and are indicated in the tables. The estimated total
numbers of persons colonized and the corresponding confi-
dence intervals were calculated by multiplying weighted preva-
lence estimates by the noninstitutionalized US population at the
midpoint of each survey cycle (20012002 and 20032004), as
determined by the US Census Bureau Current Population Sur-
vey [21].
Data from 2001 through 2004 were combined to provide
more reliable estimates of the prevalence of colonization and to
increase the studys power to detect statistically significant dif-
ferences. The prevalence of colonization was also determined for
each survey cycle separately, to compare prevalence between the
2 time periods. A t statistic from a linear contrast procedure was
used to compare prevalence between survey cycles and between
levels of a given cofactor. When the prevalence of S. aureus col-
onization and the prevalence of MRSA colonization were com-
pared across population subgroups, estimates were standardized
by the direct method to the age distribution of the 2000 US pop-
ulation for the 6 age groups used in the analyses. For the primary
outcome of overall prevalence of colonization with S. aureus and
MRSA in NHANES 20012002, compared with 20032004, P
values .05 were considered significant. To adjust for multiple
subgroup comparisons, P values .01 were considered signifi-
cant for all other comparisons.
A backward stepwise logistic modeling procedure in SUDAAN
was used to identify cofactors that were independently associated
with colonization with S. aureus or MRSA . Cofactors with a Satter-
thwaite adjusted F statistic P .05 were considered significant.
For all multivariable models, data from 2001 through 2004 were
included and survey cycle was included as a variable. Because
some cofactors were measured only for adults, models for colo-
nization with S. aureus and MRSA were initially created sepa-
JID 2008:197 (1 May) 1227
rately for children and adults and subsequently combined if
none of the adult-specific variables were significantly associated
with colonization. Interactions between each cofactor and age,
sex, race and ethnicity, and survey cycle were examined. Because
the associations between a number of cofactors and colonization
varied by sex, models were stratified by sex to control for these
interactions. Final models included race and ethnicity, age
group, and survey cycle, along with all other cofactors signifi-
cantly associated with colonization in either males or females in
the relevant age cohort (20 years or 20 years for S. aureus; all
ages 1 year for MRSA).
Laboratory methods. Nasal swab samples were collected
from both anterior nares using a Culturette swab (BBL Micro-
biology Systems; Becton Dickinson). Culturette swabs were
plated on mannitol salt agar (BBL Microbiology Systems). Each
distinctive morphotype of mannitol-fermenting colony was se-
lected from a mannitol salt agar plate and subcultured on a tryp-
ticase soy agar plate containing 5% sheep blood (BBL Microbi-
ology Systems). Plates were incubated at 35C. Isolates were
identified as S. aureus by morphology, latex agglutination test
(Remel), and tube coagulase test (Becton Dickinson).
S. aureus isolates were screened for oxacillin resistance by use
of the disk-diffusion method [22]. Cultures grown overnight on
trypticase soy agar plates containing 5% sheep blood were sus-
pended in Mueller-Hinton broth to the turbidity of a 0.5 McFar-
land standard and plated on Mueller-Hinton agar, and a 1-g
oxacillin disk was placed in the inoculum. Inhibition zone diam-
eters were measured and recorded after 24 h of incubation at
35C (zones were interpreted as follows: susceptible, 13 mm;
intermediate, 1112 mm; and resistant, 10 mm).
Isolates that were shown by disk diffusion to be resistant to
oxacillin (i.e., MRSA) and every tenth isolate shown to be sus-
ceptible to oxacillin (i.e., MSSA) were selected and saved for
additional testing, including polymerase chain reaction (PCR)
assays for the genes that encode PVL and SCCmec types I-IV [23,
24]. Strain typing was performed using PFGE with SmaI. The
PFGE patterns were analyzed with Bionumerics (Applied
Maths), and isolates were grouped into PFGE types by use of
Dice coefficients and 80% relatedness [5].
RESULTS
In NHANES 20032004, a total of 9645 persons aged 1 year
were selected and interviewed; of these, 9179 (95.2%) were ex-
amined, and 9004 (98.1%) of the persons examined had nasal
cultures performed. Similarly, in NHANES 20012002, a total of
10,470 persons aged 1 year were selected and interviewed, 9929
(94.8%) of these were examined, and 9622 (96.9%) of those ex-
amined had cultures performed.
In NHANES 20032004, a total of 2442 of the 9004 samples
were culture-positive for S. aureus, corresponding to a weighted
prevalence of 28.6% (95% CI, 27.2%30.0%) or 78.9 million
1228 JID 2008:197 (1 May) Gorwitz et al.
persons (95% CI, 75.0 82.9 million persons) colonized with S.
aureus in the US population. The prevalence of nasal coloniza-
tion with S. aureus decreased, compared to 20012002, when the
prevalence was 32.4% (95% CI, 30.8%34.0%) or 89.4 million
persons (95% CI, 85.293.8 million persons) (P .01).
Age-standardized and age-specific estimates of colonization
with S. aureus from NHANES 20012002 and 20032004 are
displayed in table 1. In both surveys, colonization with S. aureus
was most common in persons aged 20 years and non-Hispanic
white persons, compared with other age groups and other racial
and ethnic groups (P .001). In 20032004 only, Mexican
Americans were significantly more likely to be colonized than
non-Hispanic blacks (P .001). In 20012002 only, males were
significantly more likely to be colonized than females
(P .001). When prevalence was compared across surveys, sig-
nificant decreases in nasal colonization with S. aureus occurred
in males (P .01) and in adults aged 60 years (P .01), as
well as in the population overall (P .01).
Age-specific and age-standardized estimates of S. aureus col-
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onization for all 4 years combined (20012004) are displayed in
table 2. Colonization with S. aureus was significantly more com-
mon among males, compared with females (P .001), among
non-Hispanic whites and Mexican Americans, compared with
non-Hispanic blacks (P .001 and P .01, respectively), and
among persons aged 20 years, compared with older persons
(P .001).
Independent risk factors for S. aureus carriage among adults
were different for men and women (table 3). For both men and
women, S. aureus carriage was associated with non-Hispanic
white ethnicity and race, compared with non-Hispanic black
ethnicity and race (P .001, men; P .01, women), and with
obesity, compared with normal and overweight body mass index
combined (P .01, men; P .05, women). For women, for-
eign birth was negatively associated with colonization by S. au-
reus (P .05). For men, colonization with S. aureus was also
associated with younger age (P .001, for comparison of ages
20 39 years and ages 60 years) and Mexican American ethnic-
ity, compared with non-Hispanic black ethnicity and race
(P .05). Colonization with S. aureus among men also de-
creased from NHANES 20012002 to 20032004 (P .01).
Independent risk factors for colonization with S. aureus in
children (i.e., aged 20 years) were also analyzed separately for
males and females (table 3). Among both male and female chil-
dren, those aged 6 11 years and 1219 years were significantly
more likely to be colonized than those aged 15 years. Non-
Hispanic white and Mexican American race and ethnicity, com-
pared with non-Hispanic black race and ethnicity, were associ-
ated with S. aureus colonization for male children only
(P .001 and P .01, respectively).
The prevalence of colonization with MRSA in 20032004 was
1.5% (95% CI, 1.2%1.8%), or 4.1 million persons (95% CI,
3.35.1 million persons) in the US population. This represented
 Table 1. Prevalence of nasal colonization with Staphylococcus aureus and methicillin-resistant S. aureus (MRSA),
by demographic characteristicsNational Health and Nutrition Examination Survey, 20012002 and 20032004.

Prevalence of nasal colonization, % (95% CI)

Subjects tested, no. S. aureus MRSA

Characteristic 20012002 20032004 20012002 20032004 20012002 20032004

a b
All participants 9622 9004 32.3 (30.833.8) 28.7 (27.330.1) 0.9 (0.51.4) 1.5 (1.21.8)c
Sexa
Male 4685 4413 36.6 (34.039.3)d 30.6 (28.632.7)b 0.5 (0.30.9)e 1.4 (1.11.9)b
Female 4937 4591 28.1 (26.529.8) 26.7 (24.728.7) 1.1 (0.61.9) 1.6 (1.12.1)
Ethnicity and racea
Non-Hispanic white 3990 3659 33.3 (31.734.9)d 30.7 (28.632.8)d 0.9 (0.51.5) 1.6 (1.32.1)
Non-Hispanic blackf 2395 2424 25.8 (23.428.4) 22.0 (19.724.4) 1.1 (0.61.9) 1.6 (1.22.1)
Mexican American 2417 2237 29.0 (26.631.6) 26.0 (23.728.4)d 0.5 (0.30.9) 1.1 (0.42.2)g
Age
119 yearsf 4772 4338 36.9 (34.839.1) 34.6 (31.937.3) 0.6 (0.11.5)g 1.3 (0.81.9)
2059 years 3290 2945 31.4 (29.533.4)d 27.4 (25.229.7)d 0.6 (0.31.2)g 1.1 (0.71.7)
60 years 1560 1721 27.7 (25.030.6)d 22.7 (20.824.7)b,d 2.2 (1.23.6) 3.1 (2.14.4)
a
Estimates standardized to the age distribution of the 2000 US population.

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b
P .01 across surveys (20012002 vs. 20032004; this cutoff is reported for all comparisons).
c
P .05 across surveys (20012002 vs. 20032004; this cutoff is reported only when analyzing all participants not stratified by sex, race, or
age).
d
P .001, for comparison with reference group within survey (20012002 or 20032004).
e
P .01, for comparison with reference group within survey (20012002 or 20032004).
f
Reference group.
g
Estimate unstable because relative SE 30.

an increase in the prevalence of colonization with MRSA from
0.8% (95% CI, 0.5%1.4%) or 2.3 million persons (95% CI,
1.33.8 million persons) in 20012002 (P .05). The preva-
lence of colonization with MRSA increased among males
(P .01) but not among females (table 1). Colonization with
MRSA was significantly more prevalent among females in 2001
2002, compared with males (P .01), but this difference was
not evident in 20032004.
When data from all 4 years were combined (table 2), coloni-
zation with MRSA was significantly more common among per-
sons aged 60 years, compared with those aged 119 years
(P .001). The prevalence of colonization with MRSA did not
vary significantly by sex, ethnicity and race, or other cofactors in
univariate analysis.
In a multivariable model of colonization with MRSA in adults
(i.e., 20 years of age), neither BMI nor educational level
variables evaluated only for adultswas significantly associated
with colonization. Subsequent models therefore did not include
these variables and were not stratified by age. Factors signifi-
cantly associated with colonization by MRSA were different for
males and females (table 3). Among males, colonization with
MRSA was independently associated with healthcare exposure
(P .05) and was more prevalent during NHANES 20032004,
compared with 20012002 (P .05), even after controlling for
other possible cofactors. For females, colonization with MRSA
was significantly associated with age 60 years, compared with
119 years (P .01), as well as diabetes (P .05) and house-
hold income below poverty level (P .05), although foreign
birth (vs birth in the United States) was negatively associated
with colonization by MRSA (P .001).
Among the 208 persons colonized with MRSA, the largest
proportion, 50.1% (95% CI, 36.8% 63.4%), carried PFGE type
USA100. USA800 was the next most prevalent PFGE type, recov-
ered from 15.8% (95% CI, 9.4%24.4%) of persons colonized
with MRSA. The prevalence and distribution of strains associ-
ated with community transmission among persons colonized
with MRSA are presented in table 4. Although these data were
based on a small subsample of the original NHANES population
(N 101), USA800 accounted for the largest proportion of iso-
lates recovered from persons colonized with MRSA of SCCmec
type IV (33.9% of isolates [95% CI, 18.9%51.7%]) (data not
shown in table).
DISCUSSION
Between 20012002 and 20032004, the overall prevalence of
nasal colonization with S. aureus decreased, whereas the preva-
lence of colonization with MRSA increased. However, without
additional data points, it is impossible to determine whether
these changes represent trends in the prevalence of colonization
or simply short-term modulations due to sampling variability or
fluctuations in unmeasured variables, such as temperature or
humidity. An increase in colonization with MRSA was antici-
pated, due to the recent emergence of new strains of MRSA that

Changes in Prevalence of S. aureus Nasal Colonization JID 2008:197 (1 May) 1229

 Table 2. Prevalence of nasal colonization with Staphylococcus aureus and
methicillin-resistant S. aureus (MRSA), by demographic and clinical charac-
teristicsNational Health and Nutrition Examination Survey, 20012004.

Prevalence of
colonization, % (95% CI)
Subjects
Characteristic tested, no. S. aureus MRSA
a
All participants 18,626 30.4 (29.431.5) 1.2 (0.91.5)
Sexa
Male 9098 33.5 (31.835.2)b 1.0 (0.71.3)
Female 9528 27.4 (26.128.7) 1.4 (1.01.8)
Ethnicity and racea
Non-Hispanic white 7649 31.9 (30.633.3)b 1.3 (1.01.6)
Non-Hispanic blackc 4819 23.8 (22.225.5) 1.4 (1.01.8)
Mexican American 4654 27.4 (25.529.3)d 0.8 (0.41.4)
Age group
119 yearsc 9110 35.7 (34.037.5) 0.9 (0.61.4)
2059 years 6235 29.4 (27.930.9)b 0.9 (0.61.2)
60 years 3281 25.0 (23.426.8)b 2.7 (1.93.6)b
Household incomea

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Below poverty level 4571 29.5 (27.731.3) 1.7 (1.12.4)
At or above poverty level 12,992 30.5 (29.231.8) 1.1 (0.81.4)
Healthcare exposurea
Any hospitalization 1679 30.6 (26.734.6) 2.5 (1.44.1)
No hospitalization 16,942 30.4 (29.331.5) 1.1 (0.81.4)
Birthplacea
Foreign born 2811 29.6 (27.032.3) 0.8 (0.31.9)e
US born 15,799 30.6 (29.531.8) 1.3 (1.01.6)
Diabetesa
Yes 1125 32.4 (23.842.0) 1.6 (0.63.6)e
No 17,494 30.2 (29.231.2) 1.1 (0.91.5)
Body mass indexa,f
Normalc 2877 27.1 (25.029.4) 1.4 (0.92.2)
Overweight 3322 27.5 (25.629.4) 1.0 (0.61.5)
Obese 2961 31.0 (28.733.3) 1.5 (1.02.2)
Educational levela,f
Less than high school 2817 25.3 (23.127.6) 1.5 (1.12.1)
High school diploma 6684 29.0 (27.730.4) 1.2 (0.91.7)
a
Estimates standardized to the age distribution of the 2000 US population.
b
P .001.
c
Reference group.
d
P .01.
e
Estimate unstable because relative SE 30.
f
Cofactor analyzed in adults 20 years only.

have been causing an increasing proportion of S. aureus infections
among otherwise healthy persons in the community [4]. However,
a decrease in overall nasal colonization with S. aureus was unex-
pected. If this represents a true trend, one potential explanation is an
increase in population-level exposure to antimicrobial agents that
may suppress MSSA and promote colonization with MRSA. For
example, fluoroquinolone exposure has been associated with an in-
creased risk that MRSA but not MSSA would be recovered from
inpatients [25] and outpatients [26], and the prescription of fluo-
roquinolones in US ambulatory care settings increased significantly
from 19931994 through 20032004 [27].
We identified a significant association between obesity and
colonization with S. aureus in adults. This association has been
described elsewhere among adult patients who underwent gen-
eral, cardiothoracic, or neurologic surgery [28]. The reasons for
this association are unclear, but may include physical, biochem-
ical, or hormonal factors that predispose these individuals to
colonization with S. aureus.
Factors associated with colonization with MRSA included
both characteristics suggesting acquisition of MRSA in a health-
care setting (such as recent healthcare exposure for males and
diabetes and older age for females) [29, 30] and factors that have

1230 JID 2008:197 (1 May) Gorwitz et al.

 Table 3. Multivariable models for nasal colonization with Staphylococcus aureus and methicillin-resistant S. aureus
(MRSA)National Health and Nutrition Examination Survey, 20012004.

Colonization with S. aureus, Colonization with MRSA,

odds ratio (95% CI) odds ratio (95% CI)

Children (20 years) Adults (20 years) All ages (1 year)

Male Female Male Female Male Female

Variable (n 4155) (n 4162) (n 4066) (n 4412) (n 7892) (n 8232)
Age , children
15 yearsa 1.0 1.0
611 years 2.6 (2.03.5)b 2.5 (2.03.2)b
1219 years 2.0 (1.42.7)b 1.5 (1.11.9)c
Age, adults
2039 yearsa 1.0 1.0
4059 years 0.8 (0.70.9)d 1.0 (0.81.2)
60 years 0.6 (0.40.7)b 0.9 (0.81.1)
Age, all participants
119 yearsa 1.0 1.0
2059 years 0.6 (0.21.5) 1.4 (0.82.7)
60 years

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1.4 (0.63.0) 3.3 (1.47.4)d
Ethnicity and race
Non-Hispanic blacka 1.0 1.0 1.0 1.0 1.0 1.0
Non-Hispanic white 1.6 (1.42.0)b 1.2 (1.01.5) 1.8 (1.52.3)b 1.4 (1.11.7)d 1.0 (0.61.7) 0.9 (0.51.6)
Mexican American 1.3 (1.11.6)d 1.0 (0.81.2) 1.4 (1.11.8)c 1.2 (1.01.6) 0.9 (0.42.4) 0.5 (0.21.2)
Household income below
poverty level 0.9 (0.51.7) 2.0 (1.23.4)c
Foreign born 1.1 (0.91.5) 0.7 (0.51.0)c 1.2 (0.43.1) 0.1 (0.00.4)b
Hospitalization in past year 0.6 (0.31.3) 1.3 (0.82.1) 3.5 (1.29.9)c 1.3 (0.62.6)
Diabetes 0.6 (0.21.6) 2.1 (1.04.1)c
Obesee 1.3 (1.11.5)d 1.2 (1.01.5)c
Survey cycle 200304 1.0 (0.81.2) 1.0 (0.81.2) 0.7 (0.60.9)d 0.9 (0.81.1) 2.3 (1.24.4)c 1.3 (0.72.3)

NOTE. Bold type indicates statistical significance. CI, confidence interval.

a
Reference group.
b
P .001.
c
P .05.
d
P .01.
e
Reference group is non-obese (i.e., body mass index indicating the subject was normal or overweight).

been associated with community transmission (poverty for fe-
males). Previous reports have also described a high prevalence of
MRSA colonization and infection among persons of low socio-
economic status in the general community [31]; this may be
associated with crowding, limited access to healthcare, or barri-
ers to maintaining adequate hygiene. It is not clear why foreign
birth was associated with a decreased risk of colonization with
MRSA among females, but this may relate to differences in the
amount and type of antimicrobial exposure between immigrant
and nonimmigrant populations [3235].
USA100, a frequent cause of healthcare-associated MRSA in-
fections in the United States [5], and USA800, most commonly
described as a source of infection among hospitalized children
[36], were the most prevalent PFGE types identified in isolates
from persons colonized with MRSA. This suggests that most of
these colonized persons in the United States acquired MRSA in a
healthcare setting. Although SCCmec type IV is a commonly
described characteristic of community-associated MRSA strains
such as USA300 and USA400, it is not exclusive to these PFGE
types [5]. For example, MRSA of PFGE type USA800 accounted
for a large proportion of SCCmec type IV isolates in this study.
The proportion of persons colonized with MRSA who
carried PFGE type USA300 or USA400 was 19.7% (95% CI,
12.4%28.8%) in 20032004, compared with 8.1% (95% CI,
1.1%25.3%) in 20012002. However, this difference was not
statistically significant, and the prevalence estimate for 2001
2002 was unstable. Further surveillance will be required to
determine whether colonization with these strains is becom-
ing more prevalent. If so, the implications for morbidity and
mortality due to staphylococcal infection are uncertain.
However, the apparent increase in the virulence and trans-
missibility of MRSA strains USA300 and USA400 is cause for
concern [4, 37 40]. Not surprisingly, PFGE types USA300
and USA400 and the presence of PVL genes were negatively

Changes in Prevalence of S. aureus Nasal Colonization JID 2008:197 (1 May) 1231

 Table 4. Prevalence of particular traits among methicillin-resistant Staphylococcus aureus (MRSA) isolates recovered
from MRSA-colonized persons, by study variableNational Health and Nutrition Examination Survey, 20012004.

Isolates, no. (% [95% CI])

Subjects colonized
Variable with MRSA, no. PVL genes present SCCmec IV present USA300 or USA400
All participants 208 31 (14.4 [8.821.7]) 101 (44.7 [32.257.6]) 37 (15.6 [9.922.9])
Sex
Male 93 14 (13.9 [6.524.9)a) 50 (46.2 [28.165.0]) 15 (14.1 [6.725.1)a)
Femaleb 115 17 (14.7 [7.325.5]) 51 (43.7 [30.757.3]) 22 (16.6 [9.027.1])
Ethnicity and racec
Non-Hispanic white 102 15 (14.5 [8.223.1]) 36 (39.8 [25.555.5)d) 17 (15.3 [8.624.2])
NonHispanic blackb 64 11 (15.8 [5.831.7)a,e) 49 (74.7 [60.386.0)e) 14 (19.9 [8.436.9)a,e)
Age group
119 yearsb 79 14 (15.2 [6.727.9)a,e) 55 (65.3 [37.587.0)e) 17 (16.5 [7.829.0)a,e)
2059 years 51 14 (23.5 [12.338.3)e) 35 (63.4 [45.179.3)e) 15 (24.4 [13.338.8)e)
60 years 78 3 (3.0 [0.212.6)a) 11 (9.7 [3.520.4)a,f) 5 (4.6 [0.714.1)a)
Healthcare exposure
Any hospitalization 51 3 (4.6 [0.714.6)a,d,e) 16 (28.8 [13.948.0)e) 4 (4.9 [0.814.7)a,d,e)
No hospitalizationb 157 28 (16.7 [9.925.6]) 85 (48.4 [34.962.2]) 33 (18.2 [11.227.2])
Survey

Downloaded from http://jid.oxfordjournals.org/ by guest on January 4, 2015

20012002b 75 6 (7.9 [1.125.2)a,e) 37 (47.2 [22.872.6)e) 7 (8.1 [1.125.3)a,e)
20032004 133 25 (17.9 [10.926.9]) 64 (43.3 [30.257.2]) 30 (19.7 [12.428.8])

NOTE. Weighted estimates and 95% confidence intervals (CIs) are presented along with the actual numbers of subjects so that the reliability
of the estimates can be evaluated and interpreted appropriately. Estimates are based on small sample sizes and small numbers of subjects with
a given characteristic. CI, confidence interval; MRSA, methicillin-resistant Staphylococcus aureus; PVL, Panton-Valentine leukocidin; SCCmec,
staphylococcal cassette chromosome mec.
a
Relative SE 30.
b
Reference group.
c
Categories for Mexican American and Other ethnicity are not provided because of small sample sizes but are included in totals.
d
P .01.
e
Degrees of freedom 12.
f
P .001.

associated with recent hospitalization. This may change as
these PFGE types become more established in healthcare
facilities.
Unlike some other recent reports of colonization with MRSA
[41 43], and in contrast to reports of increasing incidence of
MRSA infection in healthcare settings and the general commu-
nity [4, 44], the prevalence of colonization with MRSA remained
fairly low in this representative sample of the noninstitutional-
ized US population. The small proportion of persons carrying
MRSA PFGE types USA300 or USA400 among all persons colo-
nized with S. aureus, in contrast to the large proportion of
community-associated S. aureus infections caused by MRSA
PFGE type USA300 in some reports [4], suggests that strains of
this PFGE type are more virulent than other S. aureus strains and
therefore more likely to cause infection in those persons who do
become colonized [13]. It is also possible, although unproven,
that the new epidemic MRSA strains preferentially colonize sites
other than the nares. Although the anterior nares are considered
the primary site of S. aureus colonization, based on historical
data, colonization can occur at other sites, such as the skin,
throat, vagina, or gastrointestinal tract [45 47]. To test the hy-
pothesis that certain strains of MRSA are more likely to colonize
sites other than the nares, culture samples of colonizing organ-
isms must be obtained from multiple body sites on colonized
persons. Few data are available to test this hypothesis directly
[48]. However, recent sequencing of the USA300 genome iden-
tified a mobile genetic element, called the arginine catabolic mo-
bile element, which was not detected in other S. aureus strains
but was prevalent among S. epidermidis, which commonly colo-
nizes the skin [49]. The authors hypothesized that the arginine
catabolic mobile element enhances the capacity of USA300 to
survive on human skin by maintaining pH homeostasis in an
acidic environment.
The results of our study have implications for infection con-
trol and clinical management strategies that are impacted by the
prevalence of colonization with MRSA. The increasing preva-
lence of MRSA as a cause of community-associated skin infec-
tion [4] has led to the assumption that colonization with MRSA
must be widespread in the general community. This could make
it impractical to maintain special infection control measures for
hospitalized patients with MRSA infection. In addition, it would
indicate a need to modify prophylaxis for surgical site infections
and other wound infections to provide MRSA coverage, because
such prophylaxis is primarily selected to provide coverage

1232 JID 2008:197 (1 May) Gorwitz et al.

against infection with a patients endogenous flora. It is impor-
tant to monitor the population-specific prevalence of coloniza-
tion and infection with MRSA on a local level to best inform both
infection control strategies and selection of antimicrobial pro-
phylaxis. However, our data suggest that modification of current
measures is not universally warranted at this time.
This analysis was subject to limitations. First, the survey
design was cross-sectional. Therefore, persons who were only
intermittently colonized may not have been detected. To the
extent that some organism characteristics correlate with in-
termittent or prolonged colonization, the frequency of colo-
nization with organisms possessing these characteristics
would thus have been underestimated. Some variables of in-
terest, such as recent exposure to antimicrobial agents, were
not available for analysis. In addition, because the NHANES
sample is not selected to be nationally representative on a
monthly or quarterly basis, seasonal variation in S. aureus
colonization could not be explored. Finally, many estimates
did not meet standards of reliability or precision when the
prevalence of colonization with particular MRSA isolate types
was examined. These results should, therefore, be interpreted
with caution.
In conclusion, the prevalence of nasal colonization with
MRSA increased in the United States between 20012002 and
20032004. Although the prevalence of colonization with
MRSA remains low, this increase is remarkable, given that the
overall prevalence of colonization with S. aureus decreased
over the same time period. Reasons for these changes are un-
clear, and additional data will be required to determine
whether these changes represent ongoing trends. The epide-
miology of S. aureus infection has continued to evolve, due in
part to the emergence and epidemic spread of certain MRSA
PFGE types, such as USA300 [4]. The spread of these PFGE
types in community and healthcare settings may account for
some of the increase in colonization with MRSA [9, 42, 43].
However, the relative prevalence of other MRSA PFGE types
linked almost exclusively to transmission in healthcare set-
tings suggests that MRSA acquisition in the healthcare envi-
ronment remains an important source of colonization with
MRSA in the community. Additional studies are needed to
determine whether available intervention strategies, such as
decolonization, are warranted under certain circumstances;
to determine whether these interventions will have an impact
on the risk of subsequent infection; to explore the role of
antimicrobial exposure in colonization with S. aureus and/or
MRSA; and to determine whether PFGE types USA300 and
USA400 preferentially colonize sites other than the nares. Al-
though the prevalence of colonization with MRSA is increas-
ing, our data suggest that surveillance cultures not directed at
any specific high-risk population in the community setting
are unlikely to identify a substantial proportion of persons
colonized with MRSA at this time.
Changes in Prevalence of S. aureus Nasal Colonization
Acknowledgments
We would like to thank Roberta Carey, PhD; Brandi Limbago, PhD; David
Lonsway, MMS; L. Clifford McDonald, MD; and Jean Patel, PhD, at the
Centers for Disease Control and Prevention, Atlanta, Georgia, for their input
on the analysis and interpretation of these data.
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