Nasal Carriage of Staphylococcus aureus and Methicillin-Resistant S aureus in the United States, 2001–2002
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《家庭医学史册》
ABSTRACT
PURPOSE Staphylococcus aureus is a common cause of invasive infections, yet most assessments of prevalence are based on health care–based samples. We computed population-based estimates of nasal carriage of S aureus and risk factors for carriage, as well as population-based estimates of nasal carriage of methicillin-resistant S aureus (MRSA).
METHODS We used the National Health and Nutrition Examination Survey (NHANES) 2001–2002 to estimate carriage of S aureus and MRSA for the non-institutionalized US population including children and adults.
RESULTS An estimated 86.9 million persons (32.40% of the population) were colonized with S aureus. The prevalence of MRSA among S aureus isolates was 2.58%, for an estimated population carriage of MRSA of 0.84% or 2.2 million persons. Among individuals with S aureus isolates, individuals aged 65 years or older had the highest MRSA prevalence (8.28%). Among all the racial/ethnic groups studied, Hispanics had the highest prevalence of colonization with S aureus but, when colonized, were less likely to have MRSA.
CONCLUSIONS This first nationally representative assessment of carriage of S aureus indicates that nearly one third of the population is currently colonized by this organism. Although the prevalence of MRSA remains low, more than 2.2 million people carry this resistant organism; thus, vigilance in promoting appropriate microbial transmission protocols should remain a priority.
INTRODUCTION
Staphylococcus aureus is one of the most common human pathogens and is capable of causing a wide range of infections. Although primary S aureus infections are not common, a great deal of the virulence from this organism occurs through cross-infection by spread from patient to patient in hospitals and other institutional settings. In contrast, healthy individuals have a small risk of contracting an invasive infection caused by S aureus, but they can be carriers of the organism.1 Because its primary habitat is moist squamous epithelium of the anterior nares,2 most invasive S aureus infections are assumed to arise from nasal carriage.3
The incidence of community-acquired and hospital-acquired S aureus infections has been rising with increasing emergence of drug-resistant strains called methicillin-resistant S aureus (MRSA).4–8 MRSA is an established pathogen in most health care facilities. Previously limited to hospitals, MRSA infections have been increasingly reported in the community.8,9–14 A recent meta-analysis of 27 studies of the prevalence of community-acquired-MRSA among hospital patients that used clinical specimens, as opposed to surveillance cultures conducted at the time of admission, yielded a prevalence of MRSA of 30.2%.15 The strains of MRSA associated with recent community outbreaks have unique microbiologic and genetic properties that may allow them to spread more easily or cause more skin disease than traditional hospital-based strains.16
Because many clinical infections arise from spread from a healthy carrier, an understanding of the risk factors for carriage of S aureus is crucial to understanding the potential for invasive infections and transmission of MRSA; however, most surveillance of S aureus and MRSA has focused on individuals with invasive infections rather than on an entire population.10–12,17,18 Focusing on individuals with invasive infections provides a good indication of severe disease but does not provide an accurate assessment of the reservoir of S aureus and potential for transmission.
A variety of studies have examined community prevalence of nasal carriage of S aureus in diverse sub-populations, such as adult outpatients, health care workers, college students, and injection drug users.19–24 The prevalence of S aureus ranges from 20% to 45%, with an estimate of MRSA colonization from 10 community surveillance studies of 1.3%.15 Few studies, however, have focused on which individuals are most likely to be colonized with S aureus and which are most likely to specifically have MRSA. These are issues that may be very useful to clinicians when trying to decide the likelihood that a given patient has a staphylococcal infection and, if so, whether antibiotic coverage should be provided for resistant strains. We undertook this population-based study to produce population-based estimates of nasal carriage of S aureus and to identify risk factors for carriage and to determine population-based estimates of nasal carriage of MRSA.
METHODS
The data used for the present study come from the National Health and Nutrition Examination Survey (NHANES) 2001–2002. The NHANES 2001–2002 is a nationally representative sample of the noninstitutionalized US population. The NHANES design includes an oversampling of minorities and allows determination of population estimates. More information on the methods of the 2001–2002 survey including laboratory assessment can be found elsewhere.25
Assessment of S aureus was conducted for the entire sample; thus, all participants aged 1 year or older were tested and were included in this study. The number of individuals used in the unweighted sample was 9,622, which represented a weighted population of 268,219,049.
Procedure
Assessment of S aureus The procedure for processing the nasal cultures in the NHANES 2001–2002 began with an inspection of the nasal swabs for proper labeling and integrity. Nasal swabs were refrigerated and shipped weekly to a contract laboratory. Specimens collected from the nares were plated on mannitol salt agar (MSA), a selective medium for the isolation of S aureus. MSA plates were incubated at 37°C for 48 hours. Mannitol-fermenting colonies (ie, those that were yellow or gold) were selected from the MSA plates and subcultured to plates with trypticase soy agar containing 5% sheep blood (ie, blood agar plates [BAPs]) and incubated at 37°C overnight. MSA plates with little or no growth were reincubated at 37°C overnight, and plates with non–mannitol-fermenting growth were held at room temperature. These plates were reexamined the next day, and any yellow or gold colonies were subcultured to BAPs.
Overnight cultures on BAPs were first screened using Staphaurex, a rapid latex kit for the identification of S aureus (Remel, Lenexa, Kan). A tube coagulase test using rabbit plasma with EDTA was then performed on Staphaurex-negative isolates from BAPs with morphology consistent with S aureus and on Staphaurex-positive isolates with morphology inconsistent with S aureus (ie, nonhemolytic). Staphaurex-positive isolates and Staphaurex-negative, tube coagulase–positive isolates were identified as S aureus and saved for further testing. Staphaurex-positive, tube coagulase–negative isolates were discarded.
Assessment of MRSA S aureus isolates were screened for methicillin resistance by the disk diffusion method of the National Clinical and Laboratory Standards Institute. Overnight cultures from BAPs were plated on Mueller-Hinton agar, and a 1-µg oxacillin disk was placed on the inoculated plate. Zone diameters were measured and recorded after a 24-hour incubation at 37°C; the results were classified as sensitive ( 13 mm), intermediate (11–12 mm), or resistant ( 10 mm).
Potential Risk Factors
Several variables were investigated as potential characteristics indicative of carriage of S aureus. These factors included the common demographic variables of age, sex, race/ethnicity, and place of birth. We also examined carriage of S aureus according to self-reported health status, poverty-income ratio, outpatient health care use in the past 12 months, hospitalization in the past, long-term care admission in the past 12 months, use of antibiotics in the past 30 days, self-report of physician diagnosis of diabetes, self-report of physician diagnosis of asthma, self-reported oral health, and current exposure to cigarette smoke (operationalized as either being a current smoker or living in a house with a current smoker). Given the limited population carriage of MRSA, we investigated a limited number of characteristics based on whether the unweighted sample size was large enough to make a reliable population estimate (ie, the standard error was less than one third of the parameter estimate).
Analysis
The selection of variables was based on the ability to use the entire population for our estimates. The NHANES limits some questions to certain age-groups (eg, adults) or other population subsets (eg, Hispanics). Consequently, we investigated variables that were available for the entire sample.
We used SUDAAN software (Research Triangle Institute, Research Triangle Park, NC) to account for the complex sample design used in the NHANES in the analysis. Our analysis incorporated both the stratification and clustering aspects of the sampling design. The proper weighting procedures include adjustments for the basic probability of selection and adjustments for nonresponse. Because minorities were oversampled and the sampling design was complex, we used sampling weights provided by the NHANES to compute population estimates based on weighted parameter estimates and standard errors. Chi-square analyses were used for bivariate comparisons. We also conducted a logistic regression analysis of all variables with a bivariate P value of <.10 and then removed variables that were not significant at this level.
We initially attempted to compute the relationship of several potential risk factors for carriage of S aureus and MRSA but found that for some variables, there were too few unweighted individuals in a cell to make a reliable population estimate. Admission to a long-term care facility was one such variable and is therefore not presented.
RESULTS
Carriage of S aureus
We found that the prevalence of nasal carriage of S aureus in the US population was 32.40% or 86,906,811 persons. Among adults aged 20 and older, nasal carriage of S aureus was present in 30.67%. Table 1 provides an indication of the population prevalence of nasal carriage of S aureus based on demographic characteristics; age, sex, race/ethnicity, and country of birth were associated with carriage in this community surveillance. In particular, it was noteworthy that non-Hispanic blacks were less likely than non-Hispanic whites or Hispanics to be colonized by S aureus.
In addition to looking at demographic characteristics, we also explored the relationship between clinical characteristics and nasal carriage of S aureus (Table 2). Among these characteristics, having asthma was positively related to carriage, whereas exposure to cigarette smoke and recent use of antibiotics were negatively associated with carriage.
To account for potential confounding among the demographic and clinical characteristics, we further analyzed the relationship between the potential predictors with a logistic regression model (Table 3). This model shows that even when controlling for the effect of the other characteristics (eg, age, sex, race/ethnicity), the relationships found in the bivariate analyses remain significant.
Carriage of MRSA
We also looked at carriage of MRSA in the same population. The prevalence of MRSA among S aureus isolates was 2.58%. This value corresponds to a total population carriage of MRSA of 0.84% or 2,239,888 persons and a carriage of methicillin-susceptible S aureus (MSSA) of 31.57% or 84,666,923 persons. Among adults aged 20 years or older, the prevalence of carriage of MRSA was 0.95%. Total population carriage of MRSA was 0.67% for individuals aged 1 to 64 years and 2.16% for individuals aged 65 years or older.
The prevalence of MRSA among S aureus isolates varied by age, race/ethnicity, and sex. Among individuals with S aureus isolates, 2.03% of those aged 1 to 64 years were carriers of MRSA, compared with 8.28% of those aged 65 years or older (P = .01). Also among individuals with S aureus isolates, 2.70% of non-Hispanic whites carried MRSA, compared with 4.14% of non-Hispanic blacks and 0.79% of Hispanics (P = .01). In addition, 4.14% of women with S aureus isolates carried MRSA, compared with only 1.33% of men (P = .01).
DISCUSSION
This study provides the first nationally representative assessment of carriage of S aureus in the total US population. The results suggest that nearly one third of the population is currently colonized by S aureus. Although the community carriage of MRSA is relatively low at less than 1%, this figure translates to more than 2.2 million people in the United States carrying this resistant organism.
Our prevalence results are similar to those of several previous regional studies focusing on different subgroups of the population in the United States.21,24 In regional estimates that were based on patients, however, even though the patients did not have invasive infections, their MRSA prevalence tended to be substantially higher than that in the more generally representative sample of the NHANES 2001–2002.
Our study extends the previous knowledge in this area by identifying several predictors of nasal S aureus carriage. These predictors may help inform clinical decision making when treating community-acquired infections. First, teenagers and male individuals are more likely to be carriers of S aureus. When clinicians encounter infections in these 2 groups, especially in body areas where staphylococcal infections are common, such as the skin, treatment should include an antibiotic that is effective against S aureus. But while carriage is more common in these groups, the prevalence of MRSA remains low; therefore, clinicians should not be highly suspicious of methicillin resistance in these populations unless the infection is atypical, such as one occurring in a body area that is uncommon for staphylococcal infection (eg, the lungs) or one that is rapidly advancing.
Our study also may be useful in that our findings point out that relative to younger individuals, older adults are less likely to be colonized with S aureus but, when colonized, are more likely to have MRSA strains. This finding suggests that older adults with suspected staphylococcal infections may need antibiotic coverage against resistant strains. Because of the higher rates of carriage of resistant organisms in this medically vulnerable population, clinicians may want to initiate vancomycin therapy earlier in the course of a suspected S aureus infection in patients older than 65 years.
Whereas studies looking at the risk of carriage of resistant Streptococcus pneumoniae indicate that recent beta-lactam use increases the rate of carriage of this organism, our data indicate that recent use of antibiotics is associated with a reduced risk of S aureus nasal carriage.26 Unfortunately, because the prevalence of MRSA was low and the number of individuals using antibiotics was small, we were not able to explore whether antibiotic use is related to antibiotic resistance in those who do carry S aureus. Among individuals with an S aureus isolate who had recently used antibiotics, 4.83% were colonized by MRSA, while only 2.45% of those who had not used antibiotics were colonized by MRSA. This estimate, however, does not meet criteria for reliability in this population-based study because only 6 people had used antibiotics recently and carried MRSA.
Finally, these data reflect a national sample. Local rates of carriage and resistance may vary considerably. Additionally, data for this study were collected in 2001–2002. Rapid changes in patterns of carriage and resistance are possible. One recent study of children in Nashville, Tenn, for example, showed an MRSA colonization rate similar to that in our study (0.8%) in 2001, but a considerably higher rate when children of the same age-group were sampled just 3 years later.27 Consequently, when clinicians are making therapeutic decisions, they should monitor bacterial carriage rates and resistance patterns for their own hospital and city, as well as take into account the risk patterns found in our study.
This study has several strengths. It provides the first nationally representative community surveillance estimates of S aureus and MRSA carriage for the United States. By focusing on nasal carriage within an undifferentiated sample ranging from small children to the elderly, the study provides an estimate of the reservoir of S aureus and MRSA that has not been available in studies focusing on individuals in the health care system or small regional samples.
Even with the aforementioned strengths, our study has some limitations. Because of the small number of individuals colonized with MRSA and the corresponding inability to make reliable population estimates, we were limited in our ability to identify risk factors for community carriage of MRSA; thus, although it is encouraging that the community prevalence of MRSA is less than 1%, our ability to identify characteristics of this group beyond age, race/ethnicity, and sex was limited. A second limitation of the study was that it was restricted to the noninstitutionalized population. Although this population provides for the broadest assessment of the entire population, carriage of S aureus and MRSA may differ in other settings.
In conclusion, our study confirms the high prevalence of S aureus nasal colonization in the United States; however, it also shows that the rate of MRSA carriage remains low. Few demographic or clinical characteristics are related to either S aureus carriage or, more specifically, MRSA carriage. Consequently, clinicians and hospital infection control personnel cannot target specific populations who are at highest risk of transmitting S aureus and should remain vigilant in using appropriate protocols for minimizing microbial transmission.
FOOTNOTES
Conflicts of interest: none reported
Funding support: This work was supported in part by grant 1D12HP00023-01 from the Health Resources and Services Administration, grant 1 P30AG021677 from the National Institute on Aging, and a Minority Medical Faculty Development Program grant funded by the Robert Wood Johnson Foundation.
Received for publication July 12, 2005. Revision received September 12, 2005. Accepted for publication September 21, 2005.
REFERENCES
Foster TJ. The Staphylococcus aureus "superbug." J Clin Invest. 2004; 114:1693–1696.
Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol. 2001;9:605–610.
von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med. 2001;344:11–16.
Steinberg JP, Clark CC, Hackman BO. Nosocomial and community-acquired Staphylococcus aureus bacteremias from 1980 to 1993: impact of intravascular devices and methicillin resistance. Clin Infect Dis. 1996;23:255–259.
Emori TG, Gaynes RP. An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev. 1993; 6:428–442.
Deresinski S. Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey. Clin Infect Dis. 2005;40:562–573.
Fluit AC, Wielders CL, Verhoef J, Schmitz FJ. Epidemiology and susceptibility of 3,051 Staphylococcus aureus isolates from 25 university hospitals participating in the European SENTRY study. J Clin Microbiol. 2001;39:3727–3732.
Herold BC, Immergluck LC, Maranan MC, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA. 1998;279:593–598.
Nguyen DM, Mascola L, Brancoft E. Recurring methicillin-resistant Staphylococcus aureus infections in a football team. Emerg Infect Dis. 2005;11:526–532.
Harbarth S, Francois P, Shrenzel J, et al. Community-associated methicillin-resistant Staphylococcus aureus, Switzerland. Emerg Infect Dis. 2005;11:962–965.
Ma XX, Galiana A, Pedreira W, et al. Community-acquired methicillin-resistant Staphylococcus aureus, Uruguay. Emerg Infect Dis. 2005;11:973–976.
Ochoa TJ, Mohr J, Wanger A, Murphy JR, Heresi GP. Community-associated methicillin-resistant Staphylococcus aureus in pediatric patients. Emerg Infect Dis. 2005;11:966–968.
Chambers HF. The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis. 2001;7:178–182.
Naimi TS, LeDell KH, Como-Sabetti K, et al. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA. 2003;290:2976–2984.
Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clin Infect Dis. 2003;36:131–139.
CA-MRSA Information for Clinicians. Web site.
Weber SG, Gold HS, Hooper DC, Karchmer AW, Carmeli Y. Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis. 2003;9:1415–1422.
Kuehnert MJ, Hill HA, Kupronis BA, et al. Methicillin-resistant-Staphylococcus aureus hospitalizations, United States. Emerg Infect Dis. 2005;11:868–872.
Abudu L, Blair I, Fraise A, Cheng KK. Methicillin-resistant Staphylococcus aureus (MRSA): a community-based prevalence survey. Epidemiol Infect. 2001;126:351–356.
Wertheim HF, Vos MC, Boelens HA, et al. Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infect. 2004;56:321–325.
Bischoff WE, Wallis ML, Tucker KB, Reboussin BA, Sherertz RJ. Staphylococcus aureus nasal carriage in a student community: prevalence, clonal relationships, and risk factors. Infect Control Hosp Epidemiol. 2004;25:485–491.
Bassetti S, Wolfisberg L, Jaussi B, et al. Carriage of Staphylococcus aureus among injection drug users: lower prevalence in an injection heroin maintenance program than in an oral methadone program. Infect Control Hosp Epidemiol. 2004;25:133–137.
Eveillard M, Martin Y, Hidri N, Boussougant Y, Joly-Guillou ML. Carriage of methicillin-resistant Staphylococcus aureus among hospital employees: prevalence, duration, and transmission to households. Infect Control Hosp Epidemiol. 2004;25:114–120.
Jernigan JA, Pullen AL, Partin C, Jarvis WR. Prevalence of and risk factors for colonization with methicillin-resistant Staphylococcus aureus in an outpatient clinic population. Infect Control Hosp Epidemiol. 2003;24:445–450.
National Health and Nutrition Examination Survey. Web site.
Brook I, Gober AE. Prophylaxis with amoxicillin or sulfisoxazole for otitis media: effect on the recovery of penicillin-resistant bacteria from children. Clin Infect Dis. 1996;22:143–145.
Creech CB 2nd, Kernodle DS, Alsentzer A, Wilson C, Edwards KM. Increasing rates of nasal carriage of methicillin-resistant Staphylococcus aureus in healthy children. Pediatr Infect Dis J. 2005;24:617–621.(Arch G. Mainous, III, PhD)
PURPOSE Staphylococcus aureus is a common cause of invasive infections, yet most assessments of prevalence are based on health care–based samples. We computed population-based estimates of nasal carriage of S aureus and risk factors for carriage, as well as population-based estimates of nasal carriage of methicillin-resistant S aureus (MRSA).
METHODS We used the National Health and Nutrition Examination Survey (NHANES) 2001–2002 to estimate carriage of S aureus and MRSA for the non-institutionalized US population including children and adults.
RESULTS An estimated 86.9 million persons (32.40% of the population) were colonized with S aureus. The prevalence of MRSA among S aureus isolates was 2.58%, for an estimated population carriage of MRSA of 0.84% or 2.2 million persons. Among individuals with S aureus isolates, individuals aged 65 years or older had the highest MRSA prevalence (8.28%). Among all the racial/ethnic groups studied, Hispanics had the highest prevalence of colonization with S aureus but, when colonized, were less likely to have MRSA.
CONCLUSIONS This first nationally representative assessment of carriage of S aureus indicates that nearly one third of the population is currently colonized by this organism. Although the prevalence of MRSA remains low, more than 2.2 million people carry this resistant organism; thus, vigilance in promoting appropriate microbial transmission protocols should remain a priority.
INTRODUCTION
Staphylococcus aureus is one of the most common human pathogens and is capable of causing a wide range of infections. Although primary S aureus infections are not common, a great deal of the virulence from this organism occurs through cross-infection by spread from patient to patient in hospitals and other institutional settings. In contrast, healthy individuals have a small risk of contracting an invasive infection caused by S aureus, but they can be carriers of the organism.1 Because its primary habitat is moist squamous epithelium of the anterior nares,2 most invasive S aureus infections are assumed to arise from nasal carriage.3
The incidence of community-acquired and hospital-acquired S aureus infections has been rising with increasing emergence of drug-resistant strains called methicillin-resistant S aureus (MRSA).4–8 MRSA is an established pathogen in most health care facilities. Previously limited to hospitals, MRSA infections have been increasingly reported in the community.8,9–14 A recent meta-analysis of 27 studies of the prevalence of community-acquired-MRSA among hospital patients that used clinical specimens, as opposed to surveillance cultures conducted at the time of admission, yielded a prevalence of MRSA of 30.2%.15 The strains of MRSA associated with recent community outbreaks have unique microbiologic and genetic properties that may allow them to spread more easily or cause more skin disease than traditional hospital-based strains.16
Because many clinical infections arise from spread from a healthy carrier, an understanding of the risk factors for carriage of S aureus is crucial to understanding the potential for invasive infections and transmission of MRSA; however, most surveillance of S aureus and MRSA has focused on individuals with invasive infections rather than on an entire population.10–12,17,18 Focusing on individuals with invasive infections provides a good indication of severe disease but does not provide an accurate assessment of the reservoir of S aureus and potential for transmission.
A variety of studies have examined community prevalence of nasal carriage of S aureus in diverse sub-populations, such as adult outpatients, health care workers, college students, and injection drug users.19–24 The prevalence of S aureus ranges from 20% to 45%, with an estimate of MRSA colonization from 10 community surveillance studies of 1.3%.15 Few studies, however, have focused on which individuals are most likely to be colonized with S aureus and which are most likely to specifically have MRSA. These are issues that may be very useful to clinicians when trying to decide the likelihood that a given patient has a staphylococcal infection and, if so, whether antibiotic coverage should be provided for resistant strains. We undertook this population-based study to produce population-based estimates of nasal carriage of S aureus and to identify risk factors for carriage and to determine population-based estimates of nasal carriage of MRSA.
METHODS
The data used for the present study come from the National Health and Nutrition Examination Survey (NHANES) 2001–2002. The NHANES 2001–2002 is a nationally representative sample of the noninstitutionalized US population. The NHANES design includes an oversampling of minorities and allows determination of population estimates. More information on the methods of the 2001–2002 survey including laboratory assessment can be found elsewhere.25
Assessment of S aureus was conducted for the entire sample; thus, all participants aged 1 year or older were tested and were included in this study. The number of individuals used in the unweighted sample was 9,622, which represented a weighted population of 268,219,049.
Procedure
Assessment of S aureus The procedure for processing the nasal cultures in the NHANES 2001–2002 began with an inspection of the nasal swabs for proper labeling and integrity. Nasal swabs were refrigerated and shipped weekly to a contract laboratory. Specimens collected from the nares were plated on mannitol salt agar (MSA), a selective medium for the isolation of S aureus. MSA plates were incubated at 37°C for 48 hours. Mannitol-fermenting colonies (ie, those that were yellow or gold) were selected from the MSA plates and subcultured to plates with trypticase soy agar containing 5% sheep blood (ie, blood agar plates [BAPs]) and incubated at 37°C overnight. MSA plates with little or no growth were reincubated at 37°C overnight, and plates with non–mannitol-fermenting growth were held at room temperature. These plates were reexamined the next day, and any yellow or gold colonies were subcultured to BAPs.
Overnight cultures on BAPs were first screened using Staphaurex, a rapid latex kit for the identification of S aureus (Remel, Lenexa, Kan). A tube coagulase test using rabbit plasma with EDTA was then performed on Staphaurex-negative isolates from BAPs with morphology consistent with S aureus and on Staphaurex-positive isolates with morphology inconsistent with S aureus (ie, nonhemolytic). Staphaurex-positive isolates and Staphaurex-negative, tube coagulase–positive isolates were identified as S aureus and saved for further testing. Staphaurex-positive, tube coagulase–negative isolates were discarded.
Assessment of MRSA S aureus isolates were screened for methicillin resistance by the disk diffusion method of the National Clinical and Laboratory Standards Institute. Overnight cultures from BAPs were plated on Mueller-Hinton agar, and a 1-µg oxacillin disk was placed on the inoculated plate. Zone diameters were measured and recorded after a 24-hour incubation at 37°C; the results were classified as sensitive ( 13 mm), intermediate (11–12 mm), or resistant ( 10 mm).
Potential Risk Factors
Several variables were investigated as potential characteristics indicative of carriage of S aureus. These factors included the common demographic variables of age, sex, race/ethnicity, and place of birth. We also examined carriage of S aureus according to self-reported health status, poverty-income ratio, outpatient health care use in the past 12 months, hospitalization in the past, long-term care admission in the past 12 months, use of antibiotics in the past 30 days, self-report of physician diagnosis of diabetes, self-report of physician diagnosis of asthma, self-reported oral health, and current exposure to cigarette smoke (operationalized as either being a current smoker or living in a house with a current smoker). Given the limited population carriage of MRSA, we investigated a limited number of characteristics based on whether the unweighted sample size was large enough to make a reliable population estimate (ie, the standard error was less than one third of the parameter estimate).
Analysis
The selection of variables was based on the ability to use the entire population for our estimates. The NHANES limits some questions to certain age-groups (eg, adults) or other population subsets (eg, Hispanics). Consequently, we investigated variables that were available for the entire sample.
We used SUDAAN software (Research Triangle Institute, Research Triangle Park, NC) to account for the complex sample design used in the NHANES in the analysis. Our analysis incorporated both the stratification and clustering aspects of the sampling design. The proper weighting procedures include adjustments for the basic probability of selection and adjustments for nonresponse. Because minorities were oversampled and the sampling design was complex, we used sampling weights provided by the NHANES to compute population estimates based on weighted parameter estimates and standard errors. Chi-square analyses were used for bivariate comparisons. We also conducted a logistic regression analysis of all variables with a bivariate P value of <.10 and then removed variables that were not significant at this level.
We initially attempted to compute the relationship of several potential risk factors for carriage of S aureus and MRSA but found that for some variables, there were too few unweighted individuals in a cell to make a reliable population estimate. Admission to a long-term care facility was one such variable and is therefore not presented.
RESULTS
Carriage of S aureus
We found that the prevalence of nasal carriage of S aureus in the US population was 32.40% or 86,906,811 persons. Among adults aged 20 and older, nasal carriage of S aureus was present in 30.67%. Table 1 provides an indication of the population prevalence of nasal carriage of S aureus based on demographic characteristics; age, sex, race/ethnicity, and country of birth were associated with carriage in this community surveillance. In particular, it was noteworthy that non-Hispanic blacks were less likely than non-Hispanic whites or Hispanics to be colonized by S aureus.
In addition to looking at demographic characteristics, we also explored the relationship between clinical characteristics and nasal carriage of S aureus (Table 2). Among these characteristics, having asthma was positively related to carriage, whereas exposure to cigarette smoke and recent use of antibiotics were negatively associated with carriage.
To account for potential confounding among the demographic and clinical characteristics, we further analyzed the relationship between the potential predictors with a logistic regression model (Table 3). This model shows that even when controlling for the effect of the other characteristics (eg, age, sex, race/ethnicity), the relationships found in the bivariate analyses remain significant.
Carriage of MRSA
We also looked at carriage of MRSA in the same population. The prevalence of MRSA among S aureus isolates was 2.58%. This value corresponds to a total population carriage of MRSA of 0.84% or 2,239,888 persons and a carriage of methicillin-susceptible S aureus (MSSA) of 31.57% or 84,666,923 persons. Among adults aged 20 years or older, the prevalence of carriage of MRSA was 0.95%. Total population carriage of MRSA was 0.67% for individuals aged 1 to 64 years and 2.16% for individuals aged 65 years or older.
The prevalence of MRSA among S aureus isolates varied by age, race/ethnicity, and sex. Among individuals with S aureus isolates, 2.03% of those aged 1 to 64 years were carriers of MRSA, compared with 8.28% of those aged 65 years or older (P = .01). Also among individuals with S aureus isolates, 2.70% of non-Hispanic whites carried MRSA, compared with 4.14% of non-Hispanic blacks and 0.79% of Hispanics (P = .01). In addition, 4.14% of women with S aureus isolates carried MRSA, compared with only 1.33% of men (P = .01).
DISCUSSION
This study provides the first nationally representative assessment of carriage of S aureus in the total US population. The results suggest that nearly one third of the population is currently colonized by S aureus. Although the community carriage of MRSA is relatively low at less than 1%, this figure translates to more than 2.2 million people in the United States carrying this resistant organism.
Our prevalence results are similar to those of several previous regional studies focusing on different subgroups of the population in the United States.21,24 In regional estimates that were based on patients, however, even though the patients did not have invasive infections, their MRSA prevalence tended to be substantially higher than that in the more generally representative sample of the NHANES 2001–2002.
Our study extends the previous knowledge in this area by identifying several predictors of nasal S aureus carriage. These predictors may help inform clinical decision making when treating community-acquired infections. First, teenagers and male individuals are more likely to be carriers of S aureus. When clinicians encounter infections in these 2 groups, especially in body areas where staphylococcal infections are common, such as the skin, treatment should include an antibiotic that is effective against S aureus. But while carriage is more common in these groups, the prevalence of MRSA remains low; therefore, clinicians should not be highly suspicious of methicillin resistance in these populations unless the infection is atypical, such as one occurring in a body area that is uncommon for staphylococcal infection (eg, the lungs) or one that is rapidly advancing.
Our study also may be useful in that our findings point out that relative to younger individuals, older adults are less likely to be colonized with S aureus but, when colonized, are more likely to have MRSA strains. This finding suggests that older adults with suspected staphylococcal infections may need antibiotic coverage against resistant strains. Because of the higher rates of carriage of resistant organisms in this medically vulnerable population, clinicians may want to initiate vancomycin therapy earlier in the course of a suspected S aureus infection in patients older than 65 years.
Whereas studies looking at the risk of carriage of resistant Streptococcus pneumoniae indicate that recent beta-lactam use increases the rate of carriage of this organism, our data indicate that recent use of antibiotics is associated with a reduced risk of S aureus nasal carriage.26 Unfortunately, because the prevalence of MRSA was low and the number of individuals using antibiotics was small, we were not able to explore whether antibiotic use is related to antibiotic resistance in those who do carry S aureus. Among individuals with an S aureus isolate who had recently used antibiotics, 4.83% were colonized by MRSA, while only 2.45% of those who had not used antibiotics were colonized by MRSA. This estimate, however, does not meet criteria for reliability in this population-based study because only 6 people had used antibiotics recently and carried MRSA.
Finally, these data reflect a national sample. Local rates of carriage and resistance may vary considerably. Additionally, data for this study were collected in 2001–2002. Rapid changes in patterns of carriage and resistance are possible. One recent study of children in Nashville, Tenn, for example, showed an MRSA colonization rate similar to that in our study (0.8%) in 2001, but a considerably higher rate when children of the same age-group were sampled just 3 years later.27 Consequently, when clinicians are making therapeutic decisions, they should monitor bacterial carriage rates and resistance patterns for their own hospital and city, as well as take into account the risk patterns found in our study.
This study has several strengths. It provides the first nationally representative community surveillance estimates of S aureus and MRSA carriage for the United States. By focusing on nasal carriage within an undifferentiated sample ranging from small children to the elderly, the study provides an estimate of the reservoir of S aureus and MRSA that has not been available in studies focusing on individuals in the health care system or small regional samples.
Even with the aforementioned strengths, our study has some limitations. Because of the small number of individuals colonized with MRSA and the corresponding inability to make reliable population estimates, we were limited in our ability to identify risk factors for community carriage of MRSA; thus, although it is encouraging that the community prevalence of MRSA is less than 1%, our ability to identify characteristics of this group beyond age, race/ethnicity, and sex was limited. A second limitation of the study was that it was restricted to the noninstitutionalized population. Although this population provides for the broadest assessment of the entire population, carriage of S aureus and MRSA may differ in other settings.
In conclusion, our study confirms the high prevalence of S aureus nasal colonization in the United States; however, it also shows that the rate of MRSA carriage remains low. Few demographic or clinical characteristics are related to either S aureus carriage or, more specifically, MRSA carriage. Consequently, clinicians and hospital infection control personnel cannot target specific populations who are at highest risk of transmitting S aureus and should remain vigilant in using appropriate protocols for minimizing microbial transmission.
FOOTNOTES
Conflicts of interest: none reported
Funding support: This work was supported in part by grant 1D12HP00023-01 from the Health Resources and Services Administration, grant 1 P30AG021677 from the National Institute on Aging, and a Minority Medical Faculty Development Program grant funded by the Robert Wood Johnson Foundation.
Received for publication July 12, 2005. Revision received September 12, 2005. Accepted for publication September 21, 2005.
REFERENCES
Foster TJ. The Staphylococcus aureus "superbug." J Clin Invest. 2004; 114:1693–1696.
Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol. 2001;9:605–610.
von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med. 2001;344:11–16.
Steinberg JP, Clark CC, Hackman BO. Nosocomial and community-acquired Staphylococcus aureus bacteremias from 1980 to 1993: impact of intravascular devices and methicillin resistance. Clin Infect Dis. 1996;23:255–259.
Emori TG, Gaynes RP. An overview of nosocomial infections, including the role of the microbiology laboratory. Clin Microbiol Rev. 1993; 6:428–442.
Deresinski S. Methicillin-resistant Staphylococcus aureus: an evolutionary, epidemiologic, and therapeutic odyssey. Clin Infect Dis. 2005;40:562–573.
Fluit AC, Wielders CL, Verhoef J, Schmitz FJ. Epidemiology and susceptibility of 3,051 Staphylococcus aureus isolates from 25 university hospitals participating in the European SENTRY study. J Clin Microbiol. 2001;39:3727–3732.
Herold BC, Immergluck LC, Maranan MC, et al. Community-acquired methicillin-resistant Staphylococcus aureus in children with no identified predisposing risk. JAMA. 1998;279:593–598.
Nguyen DM, Mascola L, Brancoft E. Recurring methicillin-resistant Staphylococcus aureus infections in a football team. Emerg Infect Dis. 2005;11:526–532.
Harbarth S, Francois P, Shrenzel J, et al. Community-associated methicillin-resistant Staphylococcus aureus, Switzerland. Emerg Infect Dis. 2005;11:962–965.
Ma XX, Galiana A, Pedreira W, et al. Community-acquired methicillin-resistant Staphylococcus aureus, Uruguay. Emerg Infect Dis. 2005;11:973–976.
Ochoa TJ, Mohr J, Wanger A, Murphy JR, Heresi GP. Community-associated methicillin-resistant Staphylococcus aureus in pediatric patients. Emerg Infect Dis. 2005;11:966–968.
Chambers HF. The changing epidemiology of Staphylococcus aureus? Emerg Infect Dis. 2001;7:178–182.
Naimi TS, LeDell KH, Como-Sabetti K, et al. Comparison of community- and health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA. 2003;290:2976–2984.
Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clin Infect Dis. 2003;36:131–139.
CA-MRSA Information for Clinicians. Web site.
Weber SG, Gold HS, Hooper DC, Karchmer AW, Carmeli Y. Fluoroquinolones and the risk for methicillin-resistant Staphylococcus aureus in hospitalized patients. Emerg Infect Dis. 2003;9:1415–1422.
Kuehnert MJ, Hill HA, Kupronis BA, et al. Methicillin-resistant-Staphylococcus aureus hospitalizations, United States. Emerg Infect Dis. 2005;11:868–872.
Abudu L, Blair I, Fraise A, Cheng KK. Methicillin-resistant Staphylococcus aureus (MRSA): a community-based prevalence survey. Epidemiol Infect. 2001;126:351–356.
Wertheim HF, Vos MC, Boelens HA, et al. Low prevalence of methicillin-resistant Staphylococcus aureus (MRSA) at hospital admission in the Netherlands: the value of search and destroy and restrictive antibiotic use. J Hosp Infect. 2004;56:321–325.
Bischoff WE, Wallis ML, Tucker KB, Reboussin BA, Sherertz RJ. Staphylococcus aureus nasal carriage in a student community: prevalence, clonal relationships, and risk factors. Infect Control Hosp Epidemiol. 2004;25:485–491.
Bassetti S, Wolfisberg L, Jaussi B, et al. Carriage of Staphylococcus aureus among injection drug users: lower prevalence in an injection heroin maintenance program than in an oral methadone program. Infect Control Hosp Epidemiol. 2004;25:133–137.
Eveillard M, Martin Y, Hidri N, Boussougant Y, Joly-Guillou ML. Carriage of methicillin-resistant Staphylococcus aureus among hospital employees: prevalence, duration, and transmission to households. Infect Control Hosp Epidemiol. 2004;25:114–120.
Jernigan JA, Pullen AL, Partin C, Jarvis WR. Prevalence of and risk factors for colonization with methicillin-resistant Staphylococcus aureus in an outpatient clinic population. Infect Control Hosp Epidemiol. 2003;24:445–450.
National Health and Nutrition Examination Survey. Web site.
Brook I, Gober AE. Prophylaxis with amoxicillin or sulfisoxazole for otitis media: effect on the recovery of penicillin-resistant bacteria from children. Clin Infect Dis. 1996;22:143–145.
Creech CB 2nd, Kernodle DS, Alsentzer A, Wilson C, Edwards KM. Increasing rates of nasal carriage of methicillin-resistant Staphylococcus aureus in healthy children. Pediatr Infect Dis J. 2005;24:617–621.(Arch G. Mainous, III, PhD)