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Prevalence and molecular characterizations of Staphylococcus aureus nasal colonization among patients in pediatric intensive care units in Taiwan



Nasal colonization of Staphylococcus aureus is a risk factor for the pathogen transmission and the development of infections. Limited information is available on the prevalence and molecular characteristics of S. aureus colonization in pediatric intensive care unit (ICU) patients.


A cross-sectional, island-wide study was conducted in 2011. Nasal swabs were collected from pediatric ICU patients at six tertiary hospitals in Taiwan.


Of 114 patients enrolled in total, nasal colonization of S. arueus was detected in 30 (26.3%) of them, among whom 20 (17.5%) with methicillin-resistant S. arueus (MRSA). The ST59/SCCmec IV and V clones were most common and accounted for 45% of MRSA isolates, followed by ST239/SCCmec III (25%) and ST45/SCCmec IV (20%) clones. Three ST59 MRSA isolates carried the Panton-Valentine Leukocidin genes.


The results indicated a high prevalence of S. arueus and MRSA nasal colonization among pediatric ICU patients in Taiwan. Identification of epidemic clones warrants the implement of infection control measures to reduce colonization and prevent the dissemination of MRSA in hospitals.


Staphylococcus aureus is a primary cause for hospital- and community-associated bacterial infections worldwide [1]. It is estimated that over one million S. aureus skin and soft tissue infections occur in the United States every year, potentially leading to around 100,000 bacteremia and 20,000 deaths [2]. Among clinical S. aureus isolates, methicillin-resistant S. aureus (MRSA) has emerged as a widespread pathogen in both the community and hospital settings [1]. In Taiwan, the MRSA has accounted for as much as 50–80% of all S. aureus isolates since 1990s [3, 4]. Moreover, the MRSA bacteremia is associated with an increased risk of mortality compared with the methicillin-susceptible S. aureus (MSSA) bacteremia [5].

Colonization with S. aureus is a risk factor for the development of clinical S. aureus infection [6, 7]. A large-scale prospective study showed that nosocomial S. aureus bacteremia is three times more frequent in nasal S. aureus carrier than in non-carriers, which indicates colonized patients are probably the main source of S. aureus in hospitals [7]. Another study further showed that MRSA-colonized patients are more likely to develop a MRSA invasive infection, compared with MSSA-colonized or non-colonized patients, even after adjusting for patient-specific risk factors such as comorbidities [8]. Over recent years, the continuing increase in the prevalence of nosocomial infections involving multidrug-resistant S. aureus has represented a critical and growing threat to human health [1, 2]. Another concerning issue is the rapid emergence and clonal spread of community-associated strains of MRSA, which often produce virulent exotoxins, i.e. Panton-Valentine leukocidin [9,10,11]. The identification of high-risk groups for carrying S. aureus and MRSA and the delineation of the frequency and molecular epidemiology of colonizing strains will provide valuable information for formulating effective measures in controlling the spread of S. aureus and MRSA in the community and hospital.

The anterior nares are the main reservoir of S. aureus colonization, but S. aureus can also be found in the oral cavity, perineum, axilla and on the skin [12]. In humans, nasal colonization of S. aureus may begin within the first days of life [13, 14]. In the general population, nasal S. aureus and MRSA carriages are more common in children than those in young adults and elders, but the carriage prevalence varies geographically [15,16,17]. In the hospital, the prevalence of S. aureus colonization was investigated among non-surgical patients, patients on hemodialysis or HIV-infected patients [7, 18, 19]. However, limited data is available for the prevalence of S. aureus and MRSA colonization in intensive care unit (ICU) patients [20].

Here, we conducted an island-wide survey to investigate the prevalence of nasal S. aureus colonization among pediatric ICU patients, to delineate molecular characteristics and antimicrobial resistance profiles of MRSA, and to determine the demographic and clinical characteristics associated with the MRSA colonization among six participating tertiary hospitals in Taiwan.


Study design and sample collection

The study is a cross-sectional study involving six tertiary hospitals in Taiwan. Patients who were admitted to the pediatric ICUs of the six hospitals on two designated dates, i.e., October 11 (first survey) and December 12 (second survey), 2011, were eligible for and all were enrolled in this study. The six participating hospitals included Taipei Mackay Memorial Hospital (MM), Linkou Chang Gung Memorial Hospital (LC), National Taiwan University Hospital (T), Kaohsiung Chang Gung Memorial Hospital (KC), National Cheng Kung University Hospital (CK) and Hualien Tzu-Chi General Hospital (TC). All six participating hospitals are tertiary medical centers, of which MM, LC and T are located in northern Taiwan, KC and CK are located in southern Taiwan and TC is located in eastern Taiwan. In total, there were 85 pediatric ICU beds (12 beds in MM, 20 beds in LC, 20 beds in T, 20 beds in KC, 8 beds in CK and 5 beds in TC). The pediatric ICU bed occupancy rate for each participating hospital varies with the number of visited patients and the season.

One nasal swab was obtained from each patient and sent to the central laboratory at National Health Research Institutes for the detection of S. aureus by standard methods [21]. Briefly, the swab sample was inoculated onto trypticase soy agar with 5% sheep blood plates by the streak-plating method. After incubation at 37 °C overnight, the colony of suspected S. aureus based on the hemolysis pattern and other macroscopic appearances, if any, was further inoculated on another 5% sheep blood plates. A coagulase test was performed to ensure the identification of S. aureus. A cefoxitin disk diffusion test was used to distinguish MRSA from MSSA in accordance with the recommendations of the CLSI document M100-S20 [22]. All the S. aureus isolates were stored for further molecular characterization.

Molecular characterization

Pulsed-field gel electrophoresis (PFGE) with SmaI digestion was performed as previously described [23]. The genotypes which were designated were in line with a previous survey and were listed in alphabetical order and we designated the newly identified genotype consecutively [23]. Four or more band differences between two isolates defined different genotypes. Multilocus sequence typing (MLST) was performed by analyzing the DNA sequences of seven housekeeping genes with known alleles at each locus through the MLST website ( [24].

The staphylococcal cassette chromosome mec (SCCmec) typing was performed by multiplex polymerase chain reaction as previously described [25]. The presence of virulence genes, including enterotoxin A, B, C, Panton-Valentine leukocidin (PVL), toxic shock syndrome toxin-1 (TSST-1), exfoliative toxin A (Eta), and fibronectin-binding protein A (FnbA), was examined by polymerase chain reaction analysis.

Antimicrobial susceptibility test

Susceptibility to the antibiotics, including clindamycin, erythromycin, doxycycline, tetracycline, gentamicin, levofloxacin, trimethoprim/sulfamethoxazole, rifampin and vancomycin, was performed on Mueller-Hinton agar plates by modified Kirby-Bauer disc diffusion method. The disc diffusion technique and zone interpretation of each antimicrobial agent were performed in accordance with the CLSI guideline [22]. Staphylococcus aureus ATCC-25923 was used as a standard control strain.


The statistical analysis was performed with the SPSS software (SPSS, Chicago, USA) and SAS 9.3 software (SAS Institute, Cary, USA). We calculated the colonization rates in all patients enrolled, by hospitals and by 2 surveys, and by age, sex, and clinical characteristics, including diagnosis of skin and soft tissue infections at admission, use of nasogastric or nasoduodenal tube, prolonged stay in the PICU (> 3 weeks), history of hospitalization in the past year, history of MRSA colonization or infection in the past year, and antibiotics use during the current hospitalization. Chi-squared tests or Fisher’s exact tests, where appropriate, were used to compare differences in colonization rates among subgroups by characteristics. A P value < 0.05 was considered significant in these comparisons. Study quality was assessed using the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) checklist for cross-sectional studies (Additional file 1).


The prevalence of S. aureus colonization

A total of 114 patients were admitted to pediatric ICUs at two time points (56 in October 10th and 58 in December 12th, 2011, respectively) and all were enrolled in the study. Table 1 showed the number of samples across six hospitals. Of the 114 patients, 30 (26.3%) harbored S. aureus and MSSA and MRSA were identified from 11 (9.6%) and 20 (17.5%) patients, respectively. We noted that one patient carried both MSSA and MRSA. Another patient provided samples at two time points and the MRSA was identified from both samples.

Table 1 Numbers of patients with nasal colonization of methicillin-sensitive S. aureus (MSSA) and of methicillin-resistant S. aureus (MRSA) in pediatric intensive care units by six tertiary hospitals

The MRSA colonization rate ranged from 0 to 27.3% in the six hospitals (P for between-hospital difference = 0.44, Chi-square test). The colonization rate of MRSA was 12.1% (7/58) in October and 23.2% (13/56) in December, 2011 (P for between-survey difference = 0.14, Fisher’s exact test).

Table 2 showed that the MRSA colonization in subgroups by age, sex and clinical characteristics. The numbers in subgroups were small and therefore most statistical tests were underpowered. Nevertheless, with weak statistical significance the colonization rates were found to vary with age (P for rate difference by age = 0.02, Chi-Square test), where the rate among the youngest children (< 1 year old) was found lower than children of older age groups (3.0, 28.9, and 25.0% for < 1 years, 1–6 years, and 7–12 years old, respectively). Despite some rate differences by other characteristics, these differences were not statistically significant by sex, diagnosis of skin and soft tissue infections at admission, use of nasogastric or nasoduodenal tube, prolonged length of stay, history of hospitalization in the past one year, history of MRSA colonization or infection in the past one year, and the antibiotics usage during the hospitalization (P for difference > 0.05 in all comparisons).

Table 2 MRSA nasal colonization rates among subgroups by age, sex, and clinical characteristics

Molecular characteristics and antimicrobial susceptibility profiles of MRSA isolates

The 20 MRSA isolates were classified into five distinct clonal lineages by MLST, of which ST59 (9/20, 45%) being most common, followed by ST239 (5/20, 25%) and ST45 (4/20, 20%) clones (Table 3 and Fig. 1).

Table 3 Molecular characteristics and antimicrobial susceptibility rates (%) among the 20 MRSA colonizing isolates by staphylococcal cassette chromosome mec (SCCmec) types
Fig. 1
figure 1

The molecular characteristics of MRSA isolates. For the antimicrobial susceptibility test (AST), the black and grey bars represent resistance and susceptibility to the antibiotic, respectively. Abbreviations: PFGE, pulsed-field gel electrophoresis; CC, clindamycin; E, erythromycin; LV, levofloxacin; TMP/SMX, trimethoprim/sulfamethoxazole; PVL, Panton-Valentine leucocidin; LC, Linkou Chang Gung Memorial Hospital in northern Taiwan; T, National Taiwan University Hospital in northern Taiwan; KC, Kaohsiung Chang Gung Memorial Hospital in southern Taiwan; MM, Taipei Mackay Memorial Hospital in northern Taiwan; CK, National Cheng Kung University Hospital in southern Taiwan; MLST, multilocus sequence typing

As shown in Table 3 and Fig. 1, PFGE was able to divide the most prevalent ST59 isolates into two major pulsotypes (type C and D), the majority of type D isolates carried SCCmec V and all type C isolates carried SCCmec IV. The ST45 isolates shared similar PFGE pattern, designated as type AK, and all carried SCCmec IV. ST239 isolates were shared by two pulsotypes, namely type A and B, but all ST239 isolates carried SCCmec III. While ST59 and ST239 clones were detected from pediatric ICU patients at various hospitals, the ST45 clone was predominantly found from patients of KC hospital located in southern Taiwan.

Three of 20 MRSA isolates were PVL-positive, of which two were ST59/SCCmec V and the other was ST59/SCCmec IV isolate (Fig. 1). As shown in Table 4, the PVL genes and enterotoxin B genes were only detected in MRSA isolates, while none of MSSA isolates carried these genes.

Table 4 Virulence genes in S. aureus isolates

The 20 MRSA isolates showed variable rates of resistance to antibiotics (Table 3). The rates of resistance to doxycycline, tetracycline, gentamicin, clindamycin, erythromycin, levofloxacin and trimethoprim-sulphamethoxazole were 5, 50, 40, 75, 90, 30 and 25%, respectively. None of the isolates were resistant to rifampin and vancomycin.

Isolates of different clonal complexes exhibited distinct patterns of antibiotic susceptibilities (Table 3 and Fig. 1). The ST239 isolates were resistant to multiple antibiotics, including clindamycin, erythromycin, levofloxacin and trimethoprim-sulphamethoxazole. By contrast, ST59 and ST45 isolates were less resistant and both were susceptible to levofloxacin and trimethoprim-sulphamethoxazole. Besides, all ST45 isolates were susceptible to clindamycin and 50% of isolates were susceptible to erythromycin.


The island-wide survey of S. aureus colonization among patients in pediatric ICUs showed that the S. aureus and MRSA nasal colonization rates were 26.3 and 17.5% in Taiwan, respectively. The MRSA nasal colonization rate in this study was relatively higher than that in pediatric ICU patients in the USA (4.5–6.0%) [26, 27], Saudi Arabia (2.7%), or United Kingdom (1.6–2.9%) [28]. Firstly, the high colonization rate may be associated with the local MRSA epidemiology. In community-level studies, the rates of S. aureus and MRSA nasal colonization were as high as 22.0–30.1% and 7.8–17.6%, respectively, among healthy Taiwanese children in the 2000s [23, 29]. Recently, longitudinal surveys showed that around 40% of healthy Taiwanese children ever carried MRSA during the first 2 years of life [14, 30]. Secondly, although the transmission of S. aureus between healthcare workers, the environment, and patients is an infrequent occurrence, health-care workers are possible sources of MRSA transmission to patients [31]. Previous investigation has showed around 6% of healthcare workers carry MRSA in Taiwan [32]. Taken together, our data suggested that MRSA nasal colonization was common among pediatric patients in the hospital setting in Taiwan. Although the information about the development of subsequent S. aureus and MRSA infections among colonized patients is lacking in the study, previous study found that the relative risk for MRSA infections among pediatric patients who are colonized with MRSA on admission to ICUs are 24.2 compared with those who are not colonized [28]. Continuing surveillance in the MRSA carriage among pediatric ICU patients and a follow-up study to determine related clinical burden are warranted in Taiwan.

The clonal analysis in the study showed that 45% of MRSA nasal isolates belonged to a local community-associated MRSA linage, ST59, and carried either SCCmec IV or SCCmec V. The ST59/SCCmec V is the most prevalent clone in community-associated MRSA isolates in Taiwan and referred as Taiwan clone [4]. The ST59/SCCmec V clone often carries PVL genes, but the other clone, the ST59/SCCmec IV clone, is mostly PVL-negative (Fig. 1) [4, 33]. The emergence and clonal spread of ST59/SCCmec IV isolates in both the community and hospital have been reported in Taiwan and other regions since the early 2000s [10, 11, 33]. Recently, it was found that the ST59/SCCmec IV accounts for 50–60% of colonizing MRSA isolates in the community in Taiwan [23, 32]. Increasing evidence shows that the spread of community associated-MRSA would affect the colonization trends in the hospital and long-term care settings [26, 34, 35], which is further supported by the high detection of community associated-MRSA carriage among inpatients in the present study.

The ST239/SCCmec III clone was the second common MRSA clone in this survey. This clone is a worldwide-disseminated lineage of hospital-associated MRSA [36]. In Taiwan, the ST239 lineage appeared in the 1990s, and remained one of the dominant hospital-associated MRSA clones in 2010 [4]. A recent study demonstrated that the virulence factor sasX/sesI in the ST239 MRSA plays a key role in nasal colonization and the pathogenesis of severe infections [37]. It is suggested that hospital-associated MRSA may continuously colonize and contribute to a reservoir of MRSA infection in the hospital [38]. Similar to the findings of previous studies, this survey revealed that the ST239 clonal lineage contributes to one of major MRSA colonizing clones in hospitals and is resistant to multiple antibiotics such as erythromycin, gentamicin, sulfamethoxazole/trimethoprim, levofloxacin and tetracycline [32, 39].

A subset of MRSA colonizing isolates, characterized as the ST45/SCCmec IV clone, was identified from one hospital in southern Taiwan. In Taiwan, the ST45 clone was firstly identified in an MRSA outbreak in the respiratory ward in 2006 [40] and accounted for 50% of the MRSA colonizing isolates among nursing home residents and staffs in a recent study [41], indicating the transmission and spread of this MRSA clone in healthcare facilities. The ST45 clone was rarely reported in Asia before. However, in the past decade, the ST45 emerged and became prevalent in healthcare settings in Hong Kong and China [42]. The recent study found that the ST45 clone has replaced ST239 as the second leading MRSA nasal colonization strain among patients and healthcare workers in central Taiwan [32] and further molecular characterization and epidemiology should be conducted in the near future.

Several clinical factors may contribute to the MRSA colonization. Previous antimicrobial use has been associated with the MRSA colonization in hospitalized patients, particularly those in ICUs [43]. Other factors included the contact with a health-care facility (the length of stay, history of hospitalization) and personal medical background (diagnosis of skin and soft tissue infections, placement of nasal gastric tube) [43, 44]. Although we found no statistical evidence suggesting different rates of MRSA nasal colonization by these factors other than age, the case number was small and the statistical tests were underpowered. We noted that a majority of young pediatric patients (62% of patients aged 1–6 years) was colonized with the ST59 community-associated MRSA. Although it remains debatable whether frequent person-to-person contacts in the day care center lead to an increased risk of MRSA transmission in young children [45, 46], the spread of MRSA in the community among susceptible individuals may play a role and continues to be a serious issue.

Our results showed that nearly one of six patients in pediatric ICUs in Taiwan carries MRSA, among which local community and hospital clones are identified. These findings have implications for infection control of MRSA. Strict hand hygiene before and after patient contact is the primary measure in preventing and controlling the spread of MRSA [31, 47]. Environmental hygiene is also important to reduce the MRSA reservoirs and the transmission of MRSA in the clinical setting [31]. MRSA decolonization has been proposed as a potential strategy to reduce nosocomial spread of MRSA colonization and the subsequent risk of infection [31, 48]. A study of adult ICU patients supports universal decolonization for prevention of MRSA infections [49]. Evidence also shows targeted decolonization might reduce the risk of subsequent MRSA infection in colonized neonates [50, 51]. However, the study about the efficacy of MRSA decolonization in pediatric ICUs is limited and the optimal protocol for such patients is undetermined [52]. A study in the pediatric ICU showed a significant association between 2% chlorhexidine bathing and a decrease in Gram-positive bacteremia compared with standard bathing [53]. It is generally accepted that decolonization may be considered if a patient develops a recurrent MRSA infection despite the implementation of standard infection control measures; nevertheless, the establishment of decolonization policy with favorable outcomes among pediatric ICU patients would be the necessary next step in this effort. Active surveillance has been considered to detect asymptomatic carriers who could be a possible source of nosocomial MRSA transmission and thus infection control measures can be implemented early on [31, 52], but the routine screening for MRSA would be time-consuming and costly and may have practical considerations. At last, we suggest that pediatric patients and their caregivers should be informed of the MRSA-carriage status and further education about the significance of MRSA and the method to reduce transmission should be provided to the patient and their caregivers as well when the patient is discharged.

There are limitations of this study. Firstly, the study was conducted in 2011 and a new survey to update the prevalence and molecular characteristics of S. aureus nasal carriage in pediatric ICUs is important and should be conducted in the near future. Since the early 2010s, an estimated proportion from 28% to over 70% among clinical S. aureus isolates has been MRSA in hospitals in Asia [4]. In Taiwan, the S. aureus and MRSA continue to be the leading cause of skin and soft tissue infections and invasive bacterial infections in children [38, 54]. Recent reports show that ST59, ST239 and ST45 clones remain prevalent in clinical and colonizing MRSA isolates [32, 35], which is compatible with the findings in the present island-wide survey and indicates that our data is still relevant for the local epidemiology of MRSA in Taiwan today. Secondly, only one patient was admitted to the pediatric ICU and enrolled at the TC (Hualien Tzu Chi Hospital). The TC is the one and only medical center on the east of Taiwan where is a sparsely populated area compared to other areas of Taiwan. The low occupancy rate of the pediatric ICU may partially explain a small number of enrolled patients at the TC. Thirdly, nasal swab was used in the study for active surveillance of S. aureus colonization. Although nasal swab is the most common method, a combination of sampling from two and more sites, such as throat, groin or axilla, may improve the detection of MRSA colonization [55]. Fourthly, the MRSA carriage could be persistent or intermittent, where persons are colonized for a short time period. Nevertheless, the duration of MRSA nasal colonization among our pediatric ICU patients was unclear in this cross-sectional study.


A high prevalence of MRSA and S. aureus colonization was observed in pediatric ICU patients. Identification of dominant MRSA clones in hospitals island-wide warrants an effective infection control measure to reduce nasal colonization and to prevent NRSA dissemination in the hospital setting.

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.



National Cheng Kung University Hospital


Exfoliative toxin A


Fibronectin-binding protein A


Intensive care unit


Kaohsiung Chang Gung Memorial Hospital


Linkou Chang Gung Memorial Hospital


Multilocus sequence typing


Taipei Mackay Memorial Hospital


Methicillin-resistant S. aureus


Methicillin-susceptible S. aureus


Pulsed-field gel electrophoresis


Panton-Valentine leucocidin

SCCmec :

Staphylococcal cassette chromosome mec


National Taiwan University Hospital


Hualien Tzu-Chi Hospital


Toxic shock syndrome toxin-1


  1. Tong SY, Davis JS, Eichenberger E, Holland TL, Fowler VG Jr. Staphylococcus aureus infections: epidemiology, pathophysiology, clinical manifestations, and management. Clin Microbiol Rev. 2015;28(3):603–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kourtis AP, Hatfield K, Baggs J, Mu Y, See I, Epson E, et al. Vital signs: epidemiology and recent trends in methicillin-resistant and in methicillin-susceptible Staphylococcus aureus bloodstream infections – United States. MMWR Morb Mortal Wkly Rep. 2019;68(9):214–9.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ho M, McDonald LC, Lauderdale TL, Yeh LL, Chen PC, Shiau YR. Surveillance of antibiotic resistance in Taiwan, 1998. J Microbiol Immunol Infect. 1999;32(4):239–49.

    CAS  PubMed  Google Scholar 

  4. Chen CJ, Huang YC. New epidemiology of Staphylococcus aureus infection in Asia. Clin Microbiol Infect. 2014;20(7):605–23.

    Article  CAS  PubMed  Google Scholar 

  5. Köck R, Becker K, Cookson B, van Gemert-Pijnen JE, Harbarth S, Kluytmans J, et al. Methicillin-resistant Staphylococcus aureus (MRSA): burden of disease and control challenges in Europe. Euro Surveill. 2010;15(41):19688.

    Article  PubMed  Google Scholar 

  6. 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(1):11–6.

    Article  Google Scholar 

  7. Wertheim HF, Vos MC, Ott A, van Belkum A, Voss A, Kluytmans JA, et al. Risk and outcome of nosocomial Staphylococcus aureus bacteraemia in nasal carriers versus non-carriers. Lancet. 2004;364(9435):703–5.

    Article  PubMed  Google Scholar 

  8. Honda H, Krauss MJ, Coopersmith CM, Kollef MH, Richmond AM, Fraser VJ, et al. Staphylococcus aureus nasal colonization and subsequent infection in intensive care unit patients: does methicillin resistance matter? Infect Control Hosp Epidemiol. 2010;31(6):584–91.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, et al. Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-valentine leukocidin genes: worldwide emergence. Emerg Infect Dis. 2003;9(8):978–84.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Wang CC, Lo WT, Chu ML, Siu LK. Epidemiological typing of community-acquired methicillin-resistant Staphylococcus aureus isolates from children in Taiwan. Clin Infect Dis. 2004;39(4):481–7.

    Article  CAS  PubMed  Google Scholar 

  11. Huang YH, Tseng SP, Hu JM, Tsai JC, Hsueh PR, Teng LJ. Clonal spread of SCCmec type IV methicillin-resistant Staphylococcus aureus between community and hospital. Clin Microbiol Infect. 2007;13(7):717–24.

    Article  CAS  PubMed  Google Scholar 

  12. Mermel LA, Cartony JM, Covington P, Maxey G, Morse D. Methicillin-resistant Staphylococcus aureus colonization at different body sites: a prospective, quantitative analysis. J Clin Microbiol. 2011;49(3):1119–21.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Maayan-Metzger A, Strauss T, Rubin C, Jaber H, Dulitzky M, Reiss-Mandel A, et al. Clinical evaluation of early acquisition of Staphylococcus aureus carriage by newborns. Int J Infect Dis. 2017;64:9–14.

    Article  PubMed  Google Scholar 

  14. Tsai MH, Chiu CY, Shih HJ, Liao SL, Hua MC, Huang SH, et al. Longitudinal investigation of nasopharyngeal methicillin-resistant Staphylococcus aureus colonization in early infancy: The PATCH birth cohort study. Clin Microbiol Infect. 2017;23(2):121.e1–121.e7.

    Article  PubMed  Google Scholar 

  15. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, et al. Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis. 2008;197(9):1226–34.

    Article  PubMed  Google Scholar 

  16. Hamdan-Partida A, Sainz-Espuñes T, Bustos-Martínez J. Characterization and persistence of Staphylococcus aureus strains isolated from the anterior nares and throats of healthy carriers in a Mexican community. J Clin Microbiol. 2010;48(5):1701–5.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Anwar MS, Jaffery G, Rehman Bhatti KU, Tayyib M, Bokhari SR. Staphylococcus aureus and MRSA nasal carriage in general population. J Coll Physicians Surg Pak. 2004;14(11):661–4.

    PubMed  Google Scholar 

  18. Luzar MA, Coles GA, Faller B, Slingeneyer A, Dah GD, Briat C, et al. Staphylococcus aureus nasal carriage and infection in patients on continuous ambulatory peritoneal dialysis. N Engl J Med. 1990;322(8):505–9.

    Article  CAS  PubMed  Google Scholar 

  19. Sissolak D, Geusau A, Heinze G, Witte W, Rotter ML. Risk factors for nasal carriage of Staphylococcus aureus in infectious disease patients, including patients infected with HIV, and molecular typing of colonizing strains. Eur J Clin Microbiol Infect Dis. 2002;21(2):88–96.

    Article  CAS  PubMed  Google Scholar 

  20. Paling FP, Wolkewitz M, Bode LGM, Klein Klouwenberg PMC, Ong DSY, Depuydt P, et al. Staphylococcus aureus colonization at ICU admission as a risk factor for developing S. aureus ICU pneumonia. Clin Microbiol Infect. 2017;23(1):49.e9–49.e14.

    Article  PubMed  Google Scholar 

  21. Murray PR, Bron EJO, Pfaller MA, Tenover FC, Yolken RH. Manual of clinical microbiology. 6th ed Washington DC: American Society of Microbiology; 1980.

  22. Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing, 20st informational supplement; CLSI document M100-S20. Wayne, PA: CLSI, 2010.

  23. Chen CJ, Hsu KH, Lin TY, Hwang KP, Chen PY, Huang YC. Factors associated with nasal colonization of methicillin-resistant Staphylococcus aureus among healthy children in Taiwan. J Clin Microbiol. 2011;49(1):131–7.

    Article  CAS  PubMed  Google Scholar 

  24. Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG. Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000;38(3):1008–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Oliveira DC, de Lencastre H. Multiplex PCR strategy for rapid identification of structural types and variants of the mec element in methicillin-resistant staphylococcus aureus. Antimicrob Agents Chemother. 2002;46(7):2155–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Milstone AM, Carroll KC, Ross T, Shangraw KA, Perl TM. Community-associated methicillin-resistant Staphylococcus aureus strains in pediatric intensive care unit. Emerg Infect Dis. 2010;16(4):647–55.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Horowitz IN, Baorto E, Cirillo T, Davis J. Methicillin-resistant Staphylococcus aureus colonization in a pediatric intensive care unit: risk factors. Am J Infect Control. 2012;40(2):118–22.

    Article  PubMed  Google Scholar 

  28. Zervou FN, Zacharioudakis IM, Ziakas PD, Mylonakis E. MRSA colonization and risk of infection in the neonatal and pediatric ICU: a meta-analysis. Pediatrics. 2014;133(4):e1015–23.

    Article  PubMed  Google Scholar 

  29. Lo WT, Wang CC, Lin WJ, Wang SR, Teng CS, Huang CF, et al. Changes in the nasal colonization with methicillin-resistant Staphylococcus aureus in children: 2004-2009. PLoS One. 2010;5(12):e15791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Huang YC, Chen CJ. Nasal carriage of methicillin-resistant Staphylococcus aureus during the first 2 years of life in children in northern Taiwan. Pediatr Infect Dis J. 2015;34(2):131–5.

    Article  PubMed  Google Scholar 

  31. Price JR, Cole K, Bexley A, Kostiou V, Eyre DW, Golubchik T, et al. Transmission of Staphylococcus aureus between health-care workers, the environment, and patients in an intensive care unit: a longitudinal cohort study based on whole-genome sequencing. Lancet Infect Dis. 2017;17(2):207–14.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Wu TH, Lee CY, Yang HJ, Fang YP, Chang YF, Tzeng SL, et al. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus among nasal carriage strains isolated from emergency department patients and healthcare workers in Central Taiwan. J Microbiol Immunol Infect. 2019;52(2):248–54.

    Article  CAS  PubMed  Google Scholar 

  33. Huang YC, Su LH, Wu TL, Lin TY. Changing molecular epidemiology of methicillin-resistant Staphylococcus aureus bloodstream isolates from a teaching hospital in northern Taiwan. J Clin Microbiol. 2006;44(6):2268–70.

    Article  PubMed  PubMed Central  Google Scholar 

  34. David MZ, Daum RS. Community-associated methicillin-resistant Staphylococcus aureus: epidemiology and clinical consequences of an emerging epidemic. Clin Microbiol Rev. 2010;23(3):616–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Liu CY, Lai CC, Chiang HT, Lu MC, Wang LF, Tsai TL, et al. Predominance of methicillin-resistant Staphylococcus aureus in the residents and environments of long-term care facilities in Taiwan. J Microbiol Immunol Infect. 2019;52(1):62–74.

    Article  CAS  PubMed  Google Scholar 

  36. Harris SR, Feil EJ, Holden MT, Quail MA, Nickerson EK, Chantratita N, et al. Evolution of MRSA during hospital transmission and intercontinental spread. Science. 2010;327(5964):469–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Li M, Du X, Villaruz AE, Diep BA, Wang D, Song Y, et al. MRSA epidemic linked to a quickly spreading colonization and virulence determinant. Nat Med. 2012;18(5):816–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lee CY, Fang YP, Chang YF, Wu TH, Yang YY, Huang YC. Comparison of molecular epidemiology of bloodstream methicillin-resistant Staphylococcus aureus isolates between a new and an old hospital in Central Taiwan. Int J Infect Dis. 2019;79:162–8.

    Article  PubMed  Google Scholar 

  39. Htun HL, Kyaw WM, de Sessions PF, Low L, Hibberd ML, Chow A, et al. Methicillin-resistant Staphylococcus aureus colonisation: epidemiological and molecular characteristics in an acute-care tertiary hospital in Singapore. Epidemiol Infect. 2018;146(14):1785–92.

    Article  CAS  PubMed  Google Scholar 

  40. Lee YT, Lin DB, Wang WY, Tsao SM, Yu SF, Wei MJ, et al. First identification of methicillin-resistant Staphylococcus aureus MLST types ST5 and ST45 and SCCmec types IV and Vt by multiplex PCR during an outbreak in a respiratory care ward in Central Taiwan. Diagn Microbiol Infect Dis. 2011;70(2):175–82.

    Article  CAS  PubMed  Google Scholar 

  41. Tsao FY, Kou HW, Huang YC. Dissemination of methicillin-resistant Staphylococcus aureus sequence type 45 among nursing home residents and staff in Taiwan. Clin Microbiol Infect. 2015;21(5):451–8.

    Article  PubMed  Google Scholar 

  42. Luk S, Ho AY, Ng TK, Tsang IH, Chan EH, Choi KW, et al. Prevalence, prediction, and clonality of methicillin-resistant Staphylococcus aureus carriage at admission to medical units in Hong Kong. China Infect Control Hosp Epidemiol. 2014;35(1):42–8.

    Article  PubMed  Google Scholar 

  43. Graffunder EM, Venezia RA. Risk factors associated with nosocomial methicillin-resistant Staphylococcus aureus (MRSA) infection including previous use of antimicrobials. J Antimicrob Chemother. 2002;49(6):999–1005.

    Article  CAS  PubMed  Google Scholar 

  44. Gesualdo F, Bongiorno D, Rizzo C, Bella A, Menichella D, Stefani S, et al. MRSA nasal colonization in children: prevalence meta-analysis, review of risk factors and molecular genetics. Pediatr Infect Dis J. 2013;32(5):479–85.

    Article  PubMed  Google Scholar 

  45. Adcock PM, Pastor P, Medley F, Patterson JE, Murphy TV. Methicillin-resistant Staphylococcus aureus in two child care centers. J Infect Dis. 1998;178(2):577–80.

    Article  CAS  PubMed  Google Scholar 

  46. 7Hewlett AL, Falk PS, Hughes KS, Mayhall CG. Epidemiology of methicillin-resistant Staphylococcus aureus in a university medical center day care facility. Infect Control Hosp Epidemiol. 2009;30(10):985–92.

  47. Marimuthu K, Pittet D, Harbarth S. The effect of improved hand hygiene on nosocomial MRSA control. Antimicrob Resist Infect Control. 2014;3:34.

    Article  PubMed  PubMed Central  Google Scholar 

  48. Boyce JM, Jackson MM, Pugliese G, Batt MD, Fleming D, Garner JS, et al. Methicillin-resistant Staphylococcus aureus (MRSA): a briefing for acute care hospitals and nursing facilities. The AHA technical panel on infections within hospitals. Infect Control Hosp Epidemiol. 1994;15:105–15.

    Article  CAS  PubMed  Google Scholar 

  49. Huang SS, Septimus E, Kleinman K, Moody J, Hickok J, Avery TR, et al. Targeted versus universal decolonization to prevent ICU infection. N Engl J Med. 2013;368:2255–65.

    Article  CAS  PubMed  Google Scholar 

  50. Popoola VO, Milstone AM. Decolonization to prevent Staphylococcus aureus transmission and infections in the neonatal intensive care unit. J Perinatol. 2014;34:805–10.

    Article  CAS  PubMed  Google Scholar 

  51. Huang YC, Lien RI, Lin TY. Effect of mupirocin decolonization on subsequent methicillin-resistant Staphylococcus aureus infection in infants in neonatal intensive care units. Pediatr Infect Dis J. 2015;34:241–5.

    Article  PubMed  Google Scholar 

  52. Septimus EJ, Schweizer ML. Decolonization in prevention of health care-associated infections. Clin Microbiol Rev. 2016;29:201–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Milstone AM, Elward A, Song X, Zerr DM, Orscheln R, Speck K, et al. Daily chlorhexidine bathing to reduce bacteraemia in critically ill children: a multicentre, cluster-randomised, crossover trial. Lancet. 2013;381:1099–106.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Chen YJ, Chen PA, Chen CJ, Huang YC. Molecular characteristics and clinical features of pediatric methicillin-susceptible Staphylococcus aureus infection in a medical center in northern Taiwan. BMC Infect Dis. 2019;19:402.

    Article  PubMed  PubMed Central  Google Scholar 

  55. Senn L, Basset P, Nahimana I, Zanetti G, Blanc DS. Which anatomical sites should be sampled for screening of methicillin-resistant Staphylococcus aureus carriage by culture or by rapid PCR test? Clin Microbiol Infect. 2012;18(2):E31–3.

    Article  CAS  PubMed  Google Scholar 

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Ethical approval and consent to participate

This study was approved by the Institutional Review Board and Ethics Committee of Taipei Mackay Memorial Hospital, Linkou Chang Gung Memorial Hospital, National Taiwan University Hospital, Kaohsiung Chang Gung Memorial Hospital, National Cheng Kung University Hospital and Hualien Tzu-Chi General Hospital. The need for informed consents was waived owing to the infection control nature of this study.


This research was supported by a grant from National Health Research Institutes of Taiwan (PD-102-SP-01). The funding body had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

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YHC and KYAH analyzed and interpreted the data and drafted the manuscript. YCH (Yi-Chuan Huang), HC, CYL, LYC, YHH and CCL designed the study, collected the sample and analyze the data. LMH designed the study and analyzed the data. CYC and YCH (Yhu-Chering Huang) designed the study, coordinated the data preparation, supervised the data analysis and revised the manuscript. TOY analyzed and interpreted the data and revised the manuscript. The author(s) read and approved the final manuscript.

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Correspondence to Chia-Yu Chi or Yhu-Chering Huang.

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Additional file 1.

STROBE Statement—Checklist of items that should be included in reports of cross-sectional studies

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Chen, YH., Huang, KY.A., Huang, YC. et al. Prevalence and molecular characterizations of Staphylococcus aureus nasal colonization among patients in pediatric intensive care units in Taiwan. Antimicrob Resist Infect Control 9, 41 (2020).

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