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Changes in the Prevalence of Nasal Colonization with Staphylococcus aureus in the United States, 2001–2004

  1. Rachel J Gorwitz1,
  2. Deanna Kruszon-Moran2,
  3. Sigrid K McAllister1,
  4. Geraldine McQuillan2,
  5. Linda K McDougal1,
  6. Gregory E Fosheim1,
  7. Bette J Jensen1,
  8. George Killgore1,
  9. Fred C Tenover1 and
  10. Matthew J Kuehnert1
  1. 1National Center for Preparedness, Detection, and Control of Infectious Diseases
  2. 2National Center for Health Statistics, Centers for Disease Control and PreventionAtlanta, Georgia
  1. Reprints or correspondence: Rachel Gorwitz, MD, MPH, Centers for Disease Control and Prevention, 1600 Clifton Rd. NE, MS A35, Atlanta, GA 30333 (rgorwitz{at}cdc.gov)
 
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Abstract

BackgroundStaphylococcus aureus is a common cause of infection, particularly in persons colonized by this organism. Virulent strains of methicillin-resistant S. aureus (MRSA) have emerged in the general community

MethodsA 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 subgroups. Cofactors independently associated with colonization were determined with backward stepwise logistic modeling

ResultsThe prevalence of colonization with S. aureus decreased from 32.4% in 2001–2002 to 28.6% in 2003–2004 (P<.01), whereas the prevalence of colonization with MRSA increased from 0.8% to 1.5% (P<.05). Colonization 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 2003–2004, a total of 19.7% (95% confidence interval, 12.4%–28.8%) of MRSA-colonized persons carried a PFGE type associated with community transmission

ConclusionsNasal 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. aureus (MRSA) isolates are resistant to all currently available β-lactam antimicrobial agents, including β-lactamase–stable penicillins and cephalosporins, and have been recognized as a source of healthcare-associated infections since the 1960s [2]. More recently, 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 initially characterized by a lack of association with a healthcare setting, resistance to a limited number of non-β-lactam agents, presence of genes for the Panton-Valentine leukocidin (PVL) toxin, presence of staphylococcal cassette chromosome mec (SCCmec) 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 emerging resistance to non–β-lactam agents [10]

S. aureus may colonize the anterior nares and other body sites [11]. Colonization is a strong risk factor for subsequent infection, although most persons colonized with the organism do not develop clinical disease [12]. Colonization with MRSA, in particular with PFGE type USA300, may be associated with an increased risk of subsequent infection, compared with colonization 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 colonization with S. aureus and with MRSA specifically and to describe the evolving epidemiology of nasal colonization with S. aureus

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Methods

Survey design and collection of dataThe National Health and Nutrition Examination Survey (NHANES) is administered to a nationally representative sample of the civilian, noninstitutionalized US population selected on the basis of a stratified, multistage, probability cluster design. NHANES has been conducted 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 representative sample is selected each year, but data are released in 2-year cycles to protect confidentiality and to increase statistical reliability. NHANES is reviewed and approved annually by an institutional review board. Informed consent is obtained from subjects 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 oversamples low-income persons, adolescents aged 12 through 19 years, persons aged 60 years and older, non-Hispanic black persons, 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 Bureau 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. Persons who were not classified in one of these groups were included in the category “other” and were only included in analyses when all racial ethnic groups were combined. The poverty 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 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 (1–5 years, 6–11 years, 12–19 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, 18.5–24.9; overweight, 25–29.9; 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 complex sample design [19]. Estimates with relative SE >30% or <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 confidence intervals were calculated by multiplying weighted prevalence estimates by the noninstitutionalized US population at the midpoint of each survey cycle (2001–2002 and 2003–2004), as determined by the US Census Bureau Current Population Survey [21]

Data from 2001 through 2004 were combined to provide more reliable estimates of the prevalence of colonization and to increase the study’s power to detect statistically significant differences. 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 colonization and the prevalence of MRSA colonization were compared across population subgroups, estimates were standardized by the direct method to the age distribution of the 2000 US population 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 2001–2002, compared with 2003–2004, P values <.05 were considered significant. To adjust for multiple subgroup comparisons, P values <.01 were considered significant 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 Satterthwaite 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 colonization with S. aureus and MRSA were initially created separately 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 significantly 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 methodsNasal swab samples were collected from both anterior nares using a Culturette swab (BBL Microbiology Systems; Becton Dickinson). Culturette swabs were plated on mannitol salt agar (BBL Microbiology Systems). Each distinctive morphotype of mannitol-fermenting colony was selected from a mannitol salt agar plate and subcultured on a trypticase soy agar plate containing 5% sheep blood (BBL Microbiology Systems). Plates were incubated at 35°C. 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 suspended in Mueller-Hinton broth to the turbidity of a 0.5 McFarland standard and plated on Mueller-Hinton agar, and a 1-μg oxacillin disk was placed in the inoculum. Inhibition zone diameters were measured and recorded after 24 h of incubation at 35°C (zones were interpreted as follows: susceptible, ⩾13 mm; intermediate, 11–12 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 susceptible 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]

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Results

In NHANES 2003–2004, a total of 9645 persons aged ⩾1 year were selected and interviewed; of these, 9179 (95.2%) were examined, and 9004 (98.1%) of the persons examined had nasal cultures performed. Similarly, in NHANES 2001–2002, 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 examined had cultures performed

In NHANES 2003–2004, 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 persons (95% CI, 75.0–82.9 million persons) colonized with S. aureus in the US population. The prevalence of nasal colonization with S. aureus decreased, compared to 2001–2002, when the prevalence was 32.4% (95% CI, 30.8%–34.0%) or 89.4 million persons (95% CI, 85.2–93.8 million persons) (P<.01)

Age-standardized and age-specific estimates of colonization with S. aureus from NHANES 2001–2002 and 2003–2004 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 2003–2004 only, Mexican Americans were significantly more likely to be colonized than non-Hispanic blacks (P<.001). In 2001–2002 only, males were significantly more likely to be colonized than females (P<.001). When prevalence was compared across surveys, significant 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)

Table 1
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Table 1

Prevalence of nasal colonization with Staphylococcus aureus and methicillin-resistant S. aureus (MRSA), by demographic characteristics—National Health and Nutrition Examination Survey, 2001–2002 and 2003–2004

Age-specific and age-standardized estimates of S. aureus colonization for all 4 years combined (2001–2004) are displayed in table 2. Colonization with S. aureus was significantly more common 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)

Table 2
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Table 2

Prevalence of nasal colonization with Staphylococcus aureus and methicillin-resistant S. aureus (MRSA), by demographic and clinical characteristics—National Health and Nutrition Examination Survey, 2001–2004

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, foreign birth was negatively associated with colonization by S. aureus (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 ethnicity, compared with non-Hispanic black ethnicity and race (P<.05). Colonization with S. aureus among men also decreased from NHANES 2001–2002 to 2003–2004 (P<.01)

Table 3
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Table 3

Multivariable models for nasal colonization with Staphylococcus aureus and methicillin-resistant S. aureus (MRSA)—National Health and Nutrition Examination Survey, 2001–2004

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 children, those aged 6–11 years and 12–19 years were significantly more likely to be colonized than those aged 1–5 years. Non-Hispanic white and Mexican American race and ethnicity, compared with non-Hispanic black race and ethnicity, were associated with S. aureus colonization for male children only (P<.001 and P<.01, respectively)

The prevalence of colonization with MRSA in 2003–2004 was 1.5% (95% CI, 1.2%–1.8%), or 4.1 million persons (95% CI, 3.3–5.1 million persons) in the US population. This represented 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, 1.3–3.8 million persons) in 2001–2002 (P<.05). The prevalence 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 2003–2004

When data from all 4 years were combined (table 2), colonization with MRSA was significantly more common among persons aged ⩾60 years, compared with those aged 1–19 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 adults—was significantly associated with colonization. Subsequent models therefore did not include these variables and were not stratified by age. Factors significantly 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 2003–2004, compared with 2001–2002 (P<.05), even after controlling for other possible cofactors. For females, colonization with MRSA was significantly associated with age ⩾60 years, compared with 1–19 years (P<.01), as well as diabetes (P<.05) and household 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, recovered from 15.8% (95% CI, 9.4%–24.4%) of persons colonized with MRSA. The prevalence and distribution of strains associated 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 isolates 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)

Table 4
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Table 4

Prevalence of particular traits among methicillin-resistant Staphylococcus aureus (MRSA) isolates recovered from MRSA-colonized persons, by study variable—National Health and Nutrition Examination Survey, 2001–2004

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Discussion

Between 2001–2002 and 2003–2004, the overall prevalence of nasal colonization with S. aureus decreased, whereas the prevalence 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 anticipated, due to the recent emergence of new strains of MRSA that 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 unexpected. 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 increased risk that MRSA but not MSSA would be recovered from inpatients [25] and outpatients [26], and the prescription of fluoroquinolones in US ambulatory care settings increased significantly from 1993–1994 through 2003–2004 [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 general, cardiothoracic, or neurologic surgery [28]. The reasons for this association are unclear, but may include physical, biochemical, 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 healthcare setting (such as recent healthcare exposure for males and diabetes and older age for females) [29, 30] and factors that have been associated with community transmission (poverty for females). Previous reports have also described a high prevalence of MRSA colonization and infection among persons of low socioeconomic status in the general community [31]; this may be associated with crowding, limited access to healthcare, or barriers 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 [32–35]

USA100, a frequent cause of healthcare-associated MRSA infections 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 2003–2004, compared with 8.1% (95% CI, 1.1%–25.3%) in 2001–2002. 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 becoming more prevalent. If so, the implications for morbidity and mortality due to staphylococcal infection are uncertain. However, the apparent increase in the virulence and transmissibility 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 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 community [4, 44], the prevalence of colonization with MRSA remained fairly low in this representative sample of the noninstitutionalized US population. The small proportion of persons carrying MRSA PFGE types USA300 or USA400 among all persons colonized 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 hypothesis that certain strains of MRSA are more likely to colonize sites other than the nares, culture samples of colonizing organisms 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 identified a mobile genetic element, called the arginine catabolic mobile element, which was not detected in other S. aureus strains but was prevalent among S. epidermidis which commonly colonizes 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 control and clinical management strategies that are impacted by the prevalence of colonization with MRSA. The increasing prevalence of MRSA as a cause of community-associated skin infection [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 against infection with a patient’s endogenous flora. It is important to monitor the population-specific prevalence of colonization and infection with MRSA on a local level to best inform both infection control strategies and selection of antimicrobial prophylaxis. 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 intermittent or prolonged colonization, the frequency of colonization with organisms possessing these characteristics would thus have been underestimated. Some variables of interest, 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 2001–2002 and 2003–2004. 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 unclear, and additional data will be required to determine whether these changes represent ongoing trends. The epidemiology 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 settings suggests that MRSA acquisition in the healthcare environment 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. Although the prevalence of colonization with MRSA is increasing, 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

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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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Footnotes

  • Presented in part: National Foundation for Infectious Diseases 2007 Annual Conference on Antimicrobial Resistance, Bethesda, Maryland 25–27 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

  • Received May 25, 2007.
  • Accepted September 28, 2007.
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  1. J Infect Dis. (2008) 197 (9): 1226-1234. doi: 10.1086/533494
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