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J Clin Microbiol. Sep 2009; 47(9): 2957–2963.
Published online Jul 22, 2009. doi:  10.1128/JCM.00853-09
PMCID: PMC2738089

Prevalence of and Risk Factors for Colonization by Methicillin-Resistant Staphylococcus aureus among Adults in Community Settings in Taiwan [down-pointing small open triangle]

Abstract

In order to determine the prevalence of methicillin (meticillin)-resistant Staphylococcus aureus (MRSA) colonization among adults in community settings in Taiwan and identify its risk factors, we conducted the present study. For a 3-month period, we enrolled all adults who attended mandatory health examinations at three medical centers and signed the informed consent. Nasal swabs were taken for the isolation of S. aureus. For each MRSA isolate, we performed multilocus sequence typing, identification of the staphylococcal cassette chromosome mec, tests for the presence of the Panton-Valentine leukocidin gene, and tests for drug susceptibilities. Risk factors for MRSA colonization were determined. The results indicated that the MRSA colonization rate among adults in the community settings in Taiwan was 3.8% (119/3,098). Most MRSA isolates belonged to sequence type 59 (84.0%). Independent risk factors for MRSA colonization included the presence of household members less than 7 years old (P < 0.0001) and the use of antibiotics within the past year (P = 0.0031). Smoking appeared to be protective against MRSA colonization (P < 0.0001).

Before the late 1990s, nearly all methicillin (meticillin)-resistant Staphylococcus aureus (MRSA) infections occurred in patients with specific risk factors who were in health care facilities (31). However, the emergence of MRSA infections among previously healthy persons in community settings (without exposure to health care facilities) was noted thereafter (6, 31). Therefore, MRSA infections are now classified as health care-associated MRSA (HA-MRSA) infections and community-associated MRSA (CA-MRSA) infections (38).

Strains responsible for CA-MRSA infections differ from those for HA-MRSA infections in several phenotypic and genetic features (1, 28). CA-MRSA strains carry type IV or V staphylococcal cassette chromosome mec (SCCmec) elements, are usually Panton-Valentine leukocidin (PVL) producing, and are not multidrug resistant; HA-MRSA strains carry type I, II, or III SCCmec elements, are usually not PVL producing, and are multidrug resistant (15, 22, 28).

Initially, CA-MRSA infections were mostly reported in young children (36). However, as CA-MRSA infections became more common, infections were reported among people of all ages and contributed to the increase of community-associated S. aureus infections with significance (25, 29, 36). MRSA colonization is an important risk factor for subsequent MRSA infection (30), so several studies in the United States have characterized the MRSA colonization rate in a community setting (13, 16). These studies demonstrated that the nasal colonization rates among healthy children increased from 0.8% in 2001 to 9.2% in 2004 (13). The colonization rate was 0.84% among people participating in the 2001 to 2002 National Health and Nutrition Examination Survey (NHANES) (16).

In Taiwan, MRSA strains of sequence type 59 (ST59), determined by multilocus sequence typing (MLST) and carrying type IV or V SCCmec elements, were recently found to be the major strains of CA-MRSA (5, 7, 27). Other studies demonstrated that these CA-MRSA strains were responsible for the rapid increase in the number of CA-MRSA infections among children and adults in Taiwan (7, 37). The MRSA colonization rates among Taiwanese children increased from 1.5% from 2001 to 2002 to 7.2% from 2005 to 2006 (18, 19). However, the MRSA colonization rate among adults in community settings in Taiwan is unclear. This study was conducted to determine the prevalence and risk factors for the colonization of MRSA among adults in community settings in Taiwan.

MATERIALS AND METHODS

Study population.

From 1 October 2007 to 31 December 2007, all adults (ages, >18 years) who attended mandatory health examinations (as a part of the workplace health promotion program) at three medical centers located in northern Taiwan and signed the informed consent were enrolled in this study. Three well-trained study assistants took a nasal swab from each enrolled person. The swabs were sent to the central laboratory located at National Taiwan University Hospital (a major teaching hospital in Taiwan with a total capacity of 2,200 beds) and were cultured within 6 h. When an enrolled person was found to be a MRSA carrier, his or her household members were invited to participate in the study. After the informed consent was signed, nasal swabs from these household members were also taken and sent to be cultured. This study has been approved by the institute review boards of the three medical centers.

Bacterial culture and identification of MRSA.

Each swab was plated onto a sheep blood agar plate. All plates were incubated at 35°C ambient air for 48 h. Isolates suspected of being S. aureus from sheep blood agar were first checked by catalase and Gram stain if deemed necessary, and all S. aureus isolates were confirmed by coagulase latex agglutination. S. aureus isolates were spotted onto ChromAgar MRSA to check for methicillin resistance. All isolates were preserved.

Drug susceptibility tests.

The MICs of all MRSA isolates were determined for gentamicin, clindamycin, erythromycin, ciprofloxacin, minocycline, rifampin (rifampicin), trimethoprim-sulfamethoxazole, and vancomycin using the agar dilution method proposed by the Clinical and Laboratory Standards Institute (CLSI) (10). In brief, a Steers' replicator was used to apply 104 CFU of bacteria onto Mueller-Hinton agar containing serial twofold dilutions of each antimicrobial agent (256 to 0.03 mg/liter). The agar plates were incubated at 35°C for 18 h before reading. The MIC was defined as the lowest concentration of antimicrobial agents completely inhibiting the growth of bacteria. S. aureus ATCC 25923 was used as the internal control in each run of the test. The breakpoints used to determine susceptibility were as defined by the CLSI (11).

Molecular typing and detection of the PVL gene.

Chromosomal DNA was prepared as described previously (17). The presence of the PVL gene lukF-lukS was determined by PCR with the use of a primer as described elsewhere (26). Typing of the SCCmec elements (I to V) and the mecA gene was performed by methods described by Ito et al. (22, 23). MLST was performed as described by Enright et al. (14).

Data collection.

A standardized questionnaire was used to collect information on the risk factors for CA-MRSA colonization. The data collected were age; sex; educational degree; marital status; whether the subject was living in a dormitory or not; the number of household members; the presence of any household member who was a health care worker; the presence of any household member who was less than 7 years old; the presence of any household member who was bedridden; the presence of chronic diseases; smoking habits; hospitalizations within the previous year; a history of caring for inpatients within the past year; outpatient clinic visits within the past year; the use of antibiotics within the previous year; tattoos, acupuncture treatments, parenteral drug use, and/or dialysis treatments within the previous year; a history of skin and soft-tissue infection within the previous year; whether the subject takes a shower every day; a history of visiting public places (e.g., hot-spring baths, swimming pools, sauna baths, gymnasiums, and dancing saloons) within the previous year; and economic status.

Statistics.

Continuous variables were given as means ± standard deviations and compared using Student's t test. The categorical variables were compared with a chi-square test or Fisher's exact test if the expected values were below 5. The prevalence of MRSA colonization was determined. To analyze the risk factors for carrying MRSA, we used polytomous logistic regression to compare people with MRSA to those without S. aureus and people with MRSA to those with methicillin-susceptible S. aureus (MSSA). All parameters were initially tested by univariate analysis; those with a P value of <0.05 and those being biologically meaningful were used for the multivariate analysis. However, parameters with colinearity, tested by correlation matrices, were not simultaneously considered in the final model. In the multivariate analysis, stepwise model comparison was used to determine the best model. Statistical analyses were performed using SAS 9.1.3 (SAS Institute, Inc., Cary, NC). All tests were two-tailed, and a P value of <0.05 was considered statistically significant.

RESULTS

During the 3-month study period, there were 3,098 people enrolled. Among them, 686 people were found to carry S. aureus. A total of 119 of these 686 people carried MRSA and 567 had MSSA. The comparisons of demographics and other parameters of the enrolled people are shown in Table Table1.1. There were statistically significant differences between these three groups in the parameters of sex, educational degree, the presence of any household member who was a health care worker, the presence of any household member less than 7 years old, smoking habits, and the use of antibiotics within the past year. Based on a post-hoc analysis, we found that people with MRSA (i) tended to have less education than those with MSSA or without S. aureus colonization (P = 0.0875 and 0.0650, respectively), (ii) were more likely to have household members who were less than 7 years old than the other two groups (both P < 0.0001), (iii) were less likely to be smokers than those without S. aureus colonization (P = 0.0077), and (iv) were more likely to have used antibiotics during the past year than the two other groups (P = 0.0012 and 0.0004, respectively).

TABLE 1.
Characteristics of people with MRSA, MSSA, and no S. aureus colonization (n = 3,098)a

Among the 119 MRSA isolates from the 119 people (henceforth the “index people”), 100 were classified as ST59, 11 as ST508, 5 as ST89, 2 as ST239, and 1 as ST6. Of the 100 isolates of ST59, 65 carried the type IV SCCmec element (ST59-IV) and 35 carried the type V SCCmec element (ST59-V). Of the 65 ST59-IV MRSA isolates, only 10 (15.4%) were positive for the PVL gene. All 35 of the ST59-V isolates were positive for the PVL gene. All isolates of ST6 and ST508 carried the type IV SCCmec element, all isolates of ST89 carried the type II SCCmec element, and both isolates of ST239 carried the type III SCCmec element (Table (Table2).2). All isolates, except two of ST508, that belonged to ST6, ST89, ST239, and ST508 were negative for the PVL gene. The overall prevalence of MRSA was 3.8% (119/3,098; 95% confidence interval, 3.1% to 4.5%). However, when those isolates carrying type IV and V SCCmec elements were taken into consideration as CA-MRSA strains, the prevalence of CA-MRSA carriage among healthy adults in Taiwan was found to be 3.6% (112/3,098; 95% confidence interval, 2.9% to 4.3%).

TABLE 2.
MLST types and SCCmec elements in the 183 MRSA isolates (119 index people and 64 household members)

We also screened household members of 70 of the 119 index people. In total, there were 242 household members screened. Among these 242 people, 64 people (47 adults and 17 children) from 39 families carried MRSA. Of these 64 MRSA isolates, 47 were classified as ST59, 11 as ST508, 2 as ST30, 2 as ST89, 1 as ST182, and 1 as ST342. Of the 47 isolates of ST59, 31 carried the type IV SCCmec element and the other 16 carried the type V SCCmec element. Of the 31 ST59-IV MRSA isolates from household members, 11 (35.5%) were positive for the PVL gene. All 16 ST59-V isolates from household members were positive for the PVL gene. All isolates of ST30, ST182, ST342, and ST508 carried the type IV SCCmec element, and both isolates of ST89 carried the type II SCCmec element (Table (Table2).2). Of the 11 ST508-IV MRSA isolates from household members, one (9.1%) was positive for the PVL gene. All isolates of ST30 and ST182 were positive for the PVL gene. None of the ST89 and ST342 isolates was positive for the PVL gene.

A comparison of genotypes of the MRSA isolates from household members and their associated index people indicated that there were 16 (41.0%) families in which the MRSA isolates from all household members and index people belonged to the same genotypes (same results from MLST typing, same SCCmec element, and identical presence/absence of the PVL gene). There were six (15.4%) families in which MRSA isolates from some (but not all) household members were of the same genotypes as those of the index people. There were five (12.8%) families in which MRSA isolates from household members were of the same MLST type and the same types of SCCmec elements as those of the index people but different in the presence/absence of the PVL gene. There were four (10.3%) families in which MRSA isolates from household members were of the same MLST type as those of the index people but different in the types of SCCmec elements (despite the presence/absence of the PVL gene). And there were eight (20.5%) families in which MRSA isolates from household members differed from those of the index people in MLST type.

We used polytomous logistic regression to identify risk factors for MRSA colonization by comparing people with MRSA to those with MSSA and people with MRSA to those without carriage of S. aureus. Univariate analysis indicated that the female gender, the presence of health care workers in the household, the presence of household members less than 7 years old, being a nonsmoker, and the use of antibiotics during the past year were risk factors for MRSA colonization (Table (Table3).3). Using a multivariate analysis, the presence of household members less than 7 years old, being a nonsmoker, and the use of antibiotics during the past year were independent risk factors for MRSA colonization compared to those without carriage of S. aureus. However, the presence of household members less than 7 years old and the use of antibiotics during the past year were the only two independent risk factors for MRSA colonization compared to those for carriage of MSSA (Table (Table44).

TABLE 3.
Risk factors for people colonized with MRSA compared to those colonized with MSSA and those not colonized with S. aureus by univariate analysis using polytomous logistic regressiona
TABLE 4.
Risk factors for MRSA colonization compared to MSSA colonization and no S. aureus colonization by multivariate analysis using polytomous logistic regression

Table Table55 shows the drug susceptibilities of all 183 MRSA isolates (from the index people and their families) stratified by MLST types. The overall susceptibilities were 25.1% for clindamycin, 16.9% for erythromycin, 99.5% for trimethoprim-sulfamethoxazole, 78.1% for gentamicin, 99.5% for minocycline, 98.9% for ciprofloxacin, 100% for rifampin, and 100% for vancomycin.

TABLE 5.
Drug susceptibilities of the 183 MRSA isolates with stratification by MLST type

DISCUSSION

Several reports from the United States indicated that community-associated S. aureus infections have increased rapidly in recent years and that MRSA (not MSSA) accounts for most of this increase (24, 29). Studies from Taiwan have demonstrated similar findings among children and adults (7, 37). Therefore, it is increasingly important to characterize the MRSA colonization pool among people in communities. The prevalence of MRSA colonization among children in communities has been extensively studied in Taiwan and the United States (5, 13, 18, 19, 21, 32-34), but there are only a few studies of MRSA colonization among adults in communities (16, 39). Our study showed that the MRSA colonization rate among adults in community settings in Taiwan who attended mandatory health examinations as a part of workplace health promotion was 3.8% (95% confidence interval, 3.1% to 4.5%).

A previous population-based study showed that the MRSA colonization rate among people attending the 2001 to 2002 NHANES was 0.84% (16). A study in The Netherlands from 1999 to 2000 indicated that the MRSA colonization rate among the general Dutch population was 0.03% (39). The MRSA colonization rate in this study was about 5- to 10-fold higher than reported in these prior studies. There may be several reasons for this difference. First, the colonization by MRSA among adults in communities may be more prevalent in Taiwan than in the United States and The Netherlands. Second, our study was conducted 5 to 7 years after those studies, so the difference may be due to an overall increase of MRSA during this time. Several previous studies have demonstrated that the MRSA colonization rate of people in communities has increased over time (5, 13). However, we also understand that only adults who attended mandatory health examinations as a part of a workplace health promotion program were enrolled in our study and thus may not be representative of the adult populations in communities. Since these attendees are presumably healthier than average, our results may be biased by the healthy worker effect (2).

Our molecular analysis indicated that most of the MRSA isolates (112/119) from the index people carried the type IV or type V SCCmec element, as is typical for CA-MRSA strains (15, 22, 23, 28). Therefore, the colonization rate of CA-MRSA strains was 3.6% in this study. In this study, ST59 isolates were the most common MLST type of isolates. Previous studies from Taiwan have found that ST59 MRSA isolates were the most common MLST type of MRSA causing CA-MRSA infections in different geographic areas all over Taiwan (8). Studies concerning the MRSA colonization in Taiwanese children also found ST59 is the predominant type among MRSA isolates from child carriers in communities all over Taiwan (7, 18). Our study adds additional information about the MRSA carrier rate and bacterial typing in adults in community settings in Taiwan. However, ST59 MRSA isolates were rarely found in other Asian countries according to the findings from a recent large-scale study (9).

Our molecular analysis that compared MRSA isolates from the index people and their associated households identified numerous instances where the genotypes were different. This strongly suggests that, in addition to household transmission (20), the spread of MRSA in community settings occurred via some other routes, such as sport contact, the use of saunas, exposure to a colonized animal, and so on (3, 4, 12, 40).

We used polytomous logistic regression to identify risk factors for MRSA colonization by comparing people with MRSA colonization to those with MSSA colonization and people with MRSA colonization to those without carriage of S. aureus at the same time. This allowed us to avoid problems associated with multiple intergroup comparisons. Studies that reported the determinants of MRSA colonization in community settings remained limited (16). Our multivariate analysis indicated that the presence of household members less than 7 years old, being a nonsmoker, and the use of antibiotics within the past year were the independent risk factors for MRSA colonization compared to those without S. aureus colonization. The presence of household members less than 7 years old and the use of antibiotics within the past year were the only two independent risk factors for MRSA colonization compared to those for MSSA colonization.

A previous study showed that the MRSA colonization rate of children in community settings in Taiwan was 7.2% from 2005 to 2006 (18), much higher than the adult colonization rate (3.8%) in the present study. In addition, among our 17 pediatric household members who had MRSA, 12 carried MRSA of the same genotype as the associated index person. The hypothesis that transmission from children to their parents through close household contact might play an important role in MRSA colonization among adults is worthy of further study. We also found that the use of antibiotics was associated with the presence of MRSA. This was expected, because antibiotics provide selective pressure and thus facilitated the colonization of drug-resistant pathogens such as MRSA.

Surprisingly, in a comparison of people with MRSA and those without S. aureus colonization, we found that smoking was a protective factor against MRSA colonization. However, a comparison of people with MRSA and those with MSSA found that smoking was not such a factor. In reanalyzing our data, we found that smoking was also an independent protective factor against MSSA and S. aureus (pooling MRSA and MSSA together) colonization compared to those without S. aureus colonization (odds ratio, 0.4612 and 0.4570, respectively; 95% confidence interval, 0.3480 to 0.6111 and 0.3520 to 0.5940, respectively; P < 0.0001 and 0.0001, respectively). Therefore, it seems that smoking is a protective factor against S. aureus, not only specifically against MRSA, colonization. To our best knowledge, only a review article described the similar findings based on the results from a Ph.D. thesis (35). Our study therefore provides the important evidence that smoking might be a protective factor against the nasal colonization of S. aureus. It might be that smoking creates a microenvironment in the nose that protects against the growth of S. aureus. Clearly, the effect of smoking on S. aureus colonization requires further study.

The results of our drug susceptibility tests showed that more than 95% of the isolates were susceptible to trimethoprim-sulfamethoxazole, minocycline, and ciprofloxacin; that all isolates were susceptible to rifampin and vancomycin; and that most isolates were resistant to clindamycin and erythromycin. These results differ from those reported from the United States, where the rate of susceptibility to clindamycin of MRSA isolates causing CA-MRSA infection was as high as 95% (29). This may be due to the predominance of different strains in these different geographic regions.

In conclusion, the present study showed that the rate is 3.8%. Most (94.1%) of these MRSA isolates in the present study had typical characteristics of CA-MRSA. Our study also identifies that the presence of household members less than 7 years old as well as the use of antibiotics within the past year were the independent risk factors for MRSA colonization, and smoking appeared to be a protective factor against MRSA colonization. These findings could be helpful for controlling the spread of MRSA in community settings.

Acknowledgments

This study has been supported by the Center for Disease Control, Taiwan (E9638).

Footnotes

[down-pointing small open triangle]Published ahead of print on 22 July 2009.

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