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1.  Geographic Distribution of Staphylococcus aureus Causing Invasive Infections in Europe: A Molecular-Epidemiological Analysis 
PLoS Medicine  2010;7(1):e1000215.
Hajo Grundmann and colleagues describe the development of a new interactive mapping tool for analyzing the spatial distribution of invasive Staphylococcus aureus clones.
Staphylococcus aureus is one of the most important human pathogens and methicillin-resistant variants (MRSAs) are a major cause of hospital and community-acquired infection. We aimed to map the geographic distribution of the dominant clones that cause invasive infections in Europe.
Methods and Findings
In each country, staphylococcal reference laboratories secured the participation of a sufficient number of hospital laboratories to achieve national geo-demographic representation. Participating laboratories collected successive methicillin-susceptible (MSSA) and MRSA isolates from patients with invasive S. aureus infection using an agreed protocol. All isolates were sent to the respective national reference laboratories and characterised by quality-controlled sequence typing of the variable region of the staphylococcal spa gene (spa typing), and data were uploaded to a central database. Relevant genetic and phenotypic information was assembled for interactive interrogation by a purpose-built Web-based mapping application. Between September 2006 and February 2007, 357 laboratories serving 450 hospitals in 26 countries collected 2,890 MSSA and MRSA isolates from patients with invasive S. aureus infection. A wide geographical distribution of spa types was found with some prevalent in all European countries. MSSA were more diverse than MRSA. Genetic diversity of MRSA differed considerably between countries with dominant MRSA spa types forming distinctive geographical clusters. We provide evidence that a network approach consisting of decentralised typing and visualisation of aggregated data using an interactive mapping tool can provide important information on the dynamics of MRSA populations such as early signalling of emerging strains, cross border spread, and importation by travel.
In contrast to MSSA, MRSA spa types have a predominantly regional distribution in Europe. This finding is indicative of the selection and spread of a limited number of clones within health care networks, suggesting that control efforts aimed at interrupting the spread within and between health care institutions may not only be feasible but ultimately successful and should therefore be strongly encouraged.
Please see later in the article for the Editors' Summary
Editors' Summary
The bacterium Staphylococcus aureus lives on the skin and in the nose of about a third of healthy people. Although S. aureus usually coexists peacefully with its human carriers, it is also an important disease-causing organism or pathogen. If it enters the body through a cut or during a surgical procedure, S. aureus can cause minor infections such as pimples and boils or more serious, life-threatening infections such as blood poisoning and pneumonia. Minor S. aureus infections can be treated without antibiotics—by draining a boil, for example. Invasive infections are usually treated with antibiotics. Unfortunately, many of the S. aureus clones (groups of bacteria that are all genetically related and descended from a single, common ancestor) that are now circulating are resistant to methicillin and several other antibiotics. Invasive methicillin-resistant S. aureus (MRSA) infections are a particular problem in hospitals and other health care facilities (so-called hospital-acquired MRSA infections), but they can also occur in otherwise healthy people who have not been admitted to a hospital (community-acquired MRSA infections).
Why Was This Study Done?
The severity and outcome of an S. aureus infection in an individual depends in part on the ability of the bacterial clone with which the individual is infected to cause disease—the clone's “virulence.” Public-health officials and infectious disease experts would like to know the geographic distribution of the virulent S. aureus clones that cause invasive infections, because this information should help them understand how these pathogens spread and thus how to control them. Different clones of S. aureus can be distinguished by “molecular typing,” the determination of clone-specific sequences of nucleotides in variable regions of the bacterial genome (the bacterium's blueprint; genomes consist of DNA, long chains of nucleotides). In this study, the researchers use molecular typing to map the geographic distribution of MRSA and methicillin-sensitive S. aureus (MSSA) clones causing invasive infections in Europe; a MRSA clone emerges when an MSSA clone acquires antibiotic resistance from another type of bacteria so it is useful to understand the geographic distribution of both MRSA and MSSA.
What Did the Researchers Do and Find?
Between September 2006 and February 2007, 357 laboratories serving 450 hospitals in 26 European countries collected almost 3,000 MRSA and MSSA isolates from patients with invasive S. aureus infections. The isolates were sent to the relevant national staphylococcal reference laboratory (SRL) where they were characterized by quality-controlled sequence typing of the variable region of a staphylococcal gene called spa (spa typing). The spa typing data were entered into a central database and then analyzed by a public, purpose-built Web-based mapping tool (SRL-Maps), which provides interactive access and easy-to-understand illustrations of the geographical distribution of S. aureus clones. Using this mapping tool, the researchers found that there was a wide geographical distribution of spa types across Europe with some types being common in all European countries. MSSA isolates were more diverse than MRSA isolates and the genetic diversity (variability) of MRSA differed considerably between countries. Most importantly, major MRSA spa types occurred in distinct geographical clusters.
What Do These Findings Mean?
These findings provide the first representative snapshot of the genetic population structure of S. aureus across Europe. Because the researchers used spa typing, which analyzes only a small region of one gene, and characterized only 3,000 isolates, analysis of other parts of the S. aureus genome in more isolates is now needed to build a complete portrait of the geographical abundance of the S. aureus clones that cause invasive infections in Europe. However, the finding that MRSA spa types occur mainly in geographical clusters has important implications for the control of MRSA, because it indicates that a limited number of clones are spreading within health care networks, which means that MRSA is mainly spread by patients who are repeatedly admitted to different hospitals. Control efforts aimed at interrupting this spread within and between health care institutions may be feasible and ultimately successful, suggest the researchers, and should be strongly encouraged. In addition, this study shows how, by sharing typing results on a Web-based platform, an international surveillance network can provide clinicians and infection control teams with crucial information about the dynamics of pathogens such as S. aureus, including early warnings about emerging virulent clones.
Additional Information
Please access these Web sites via the online version of this summary at
This study is further discussed in a PLoS Medicine Perspective by Franklin D. Lowy
The UK Health Protection Agency provides information about Staphylococcus aureus
The UK National Health Service Choices Web site has pages on staphylococcal infections and on MRSA
The US National Institute of Allergy and Infectious Disease has information about MRSA
The US Centers for Disease Control and Infection provides information about MRSA for the public and professionals
MedlinePlus provides links to further resources on staphylococcal infections and on MRSA (in English and Spanish)
SRL-Maps can be freely accessed
PMCID: PMC2796391  PMID: 20084094
2.  Spread of Epidemic MRSA-ST5-IV Clone Encoding PVL as a Major Cause of Community Onset Staphylococcal Infections in Argentinean Children 
PLoS ONE  2012;7(1):e30487.
Community-associated methicillin-resistant Staphylococcus aureus-(CA-MRSA) strains have emerged in Argentina. We investigated the clinical and molecular evolution of community-onset MRSA infections (CO-MRSA) in children of Córdoba, Argentina, 2005–2008. Additionally, data from 2007 were compared with the epidemiology of these infections in other regions of the country.
Methodology/Principal Findings
Two datasets were used: i) lab-based prospective surveillance of CA-MRSA isolates from 3 Córdoba pediatric hospitals-(CBAH1-H3) in 2007–2008 (compared to previously published data of 2005) and ii) a sampling of CO-MRSA from a study involving both, healthcare-associated community-onset-(HACO) infections in children with risk-factors for healthcare-associated infections-(HRFs), and CA-MRSA infections in patients without HRFs detected in multiple centers of Argentina in 2007. Molecular typing was performed on the CA-MRSA-(n: 99) isolates from the CBAH1-H3-dataset and on the HACO-MRSA-(n: 51) and CA-MRSA-(n: 213) isolates from other regions. Between 2005–2008, the annual proportion of CA-MRSA/CA-S. aureus in Córdoba hospitals increased from 25% to 49%, P<0.01. Total CA-MRSA infections increased 3.6 fold-(5.1 to 18.6 cases/100,000 annual-visits, P<0.0001), associated with an important increase of invasive CA-MRSA infections-(8.5 fold). In all regions analyzed, a single genotype prevailed in both CA-MRSA (82%) and HACO-MRSA(57%), which showed pulsed-field-gel electrophoresis-(PFGE)-type-“I”, sequence-type-5-(ST5), SCCmec-type-IVa, spa-t311, and was positive for PVL. The second clone, pulsotype-N/ST30/CC30/SCCmecIVc/t019/PVL+, accounted for 11.5% of total CA-MRSA infections. Importantly, the first 4 isolates of Argentina belonging to South American-USA300 clone-(USA300/ST8/CC8/SCCmecIVc/t008/PVL+/ACME−) were detected. We also demonstrated that a HA-MRSA clone-(pulsotype-C/ST100/CC5) caused 2% and 10% of CA-MRSA and HACO-MRSA infections respectively and was associated with a SCCmec type closely related to SCCmecIV(2B&5).
The dissemination of epidemic MRSA clone, ST5-IV-PVL+ was the main cause of increasing staphylococcal community-onset infections in Argentinean children (2003–2008), conversely to other countries. The predominance of this clone, which has capacity to express the h-VISA phenotype, in healthcare-associated community-onset cases suggests that it has infiltrated into hospital-settings.
PMCID: PMC3264586  PMID: 22291965
3.  The molecular epidemiology of incident methicillin-resistant Staphylococcus aureus cases among hospitalized patients in Alberta, Canada: a retrospective cohort study 
Infection Prevention and Control (IPC) surveillance for incident methicillin-resistant Staphylococcus aureus (MRSA) in hospitalized patients is performed in a complete provincial surveillance network of all acute care facilities in Alberta, Canada. IPC surveillance is centralized using a web-based data entry platform so that each patient is counted only once. All diagnostic laboratories submit the first clinical MRSA isolate associated with a patient without previous MRSA positive clinical cultures in the preceding year to the Provincial Laboratory for Public Health (ProvLab) for molecular typing. This study will investigate the relationship between the IPC epidemiological classification based on time of detection following admission to hospital (Hospital Acquired and Community Associated) and the matched laboratory MRSA surveillance data using a retrospective cohort study design.
Incident IPC MRSA cases were classified according to IPC epidemiologic definitions. DNA sequencing of the Staphylococcus protein A (spa) gene and pulsed-field gel electrophoresis (PFGE) typing was performed. IPC MRSA surveillance data were matched to the ProvLab molecular surveillance data. Univariate comparisons of proportions were performed for categorical variables and the Student’s t test for continuous variables.
MRSA molecular typing data were available for matching for 46.7 % (2248/4818) of incident IPC cases. There was agreement in definitions for traditional nosocomial clones (USA100/CMRSA2) with Hospital Acquired (HA)-MRSA (65.1 % of all IPC HA-MRSA) and traditional community clones (USA400/CMRSA7 and USA300/CMRSA10) with Community Acquired (CA)-MRSA (62.4 % of CA-MRSA). However, we observed discordance for both traditional nosocomial/CA-MRSA (30.4 % of CA-MRSA) and for traditional community/HA-MRSA (26.9 % of HA-MRSA).
We note agreement between traditional nosocomial clones and HA-MRSA, and traditional community clones and CA-MRSA. However, approximately one-quarter of HA-MRSA are those of traditional community clones while approximately one-third of CA-MRSA are those of traditional nosocomial clones. Collaborative provincial MRSA surveillance is important as the distinction between IPC case attribution in acute care settings and the historical definitions of MRSA clones as community- or healthcare-associated have blurred.
PMCID: PMC4570609  PMID: 26380079
MRSA epidemiology; Infection prevention and control; Community-associated MRSA; Healthcare-associated MRSA
4.  Molecular Typing and Virulence Characteristic of Methicillin-Resistant Staphylococcus Aureus Isolates from Pediatric Patients in Bucaramanga, Colombia 
PLoS ONE  2013;8(8):e73434.
Staphylococcus aureus is among the most common global nosocomial pathogens. The emergence and spread of methicillin-resistant Staphylococcus aureus (MRSA) is a public health problem worldwide that causes nosocomial and community infections. The goals of this study were to establish the clonal complexes (CC) of the isolates of MRSA obtained from pediatric patients in a university hospital in Colombia and to investigate its molecular characteristics based on the virulence genes and the genes of staphylococcal toxins and adhesins.
A total of 53 MRSA isolates from pediatric patients with local or systemic infections were collected. The MRSA isolates were typed based on the SCCmec, MLST, spa and agr genes. The molecular characterization included the detection of Panton-Valentine Leukocidin, superantigenic and exfoliative toxins, and adhesin genes. The correlation between the molecular types identified and the profile of virulence factors was determined for all isolates.
Four CC were identified, including CC8, CC5, CC80 and CC78. The ST8-MRSA-IVc-agrI was the predominant clone among the isolates, followed by the ST5-MRSA-I-agrII and ST5-MRSA-IVc-agrII clones. Twelve spa types were identified, of which t10796 and t10799 were new repeat sequences. The isolates were carriers of toxin genes, and hlg (100%), sek (92%) and pvl (88%) were the most frequent. Ten toxin gene profiles were observed, and the most frequent were seq-sek-hlg (22.6%), sek-hlg (22.6%), seb-seq-sek-hlg (18.9%) and seb-sek-hlg (15.1%). The adhesion genes were present in most of the MRSA isolates, including the following: clf-A (89%), clf-B (87%), fnb-A (83%) and ica (83%). The majority of the strains carried SCCmec-IVc and were identified as causing nosocomial infection. No significant association between a molecular type and the virulence factors was found.
Four major MRSA clone complexes were identified among the isolates. ST8-MRSA-IVc-agrI pvl+ (USA300-LV) was the most frequent, confirming the presence of community-associated MRSA in Colombian hospitals.
PMCID: PMC3751954  PMID: 24058415
5.  Transmission and Microevolution of USA300 MRSA in U.S. Households: Evidence from Whole-Genome Sequencing 
mBio  2015;6(2):e00054-15.
Methicillin-resistant Staphylococcus aureus (MRSA) USA300 is a successful S. aureus clone in the United States and a common cause of skin and soft tissue infections (SSTIs). We performed whole-genome sequencing (WGS) of 146 USA300 MRSA isolates from SSTIs and colonization cultures obtained from an investigation conducted from 2008 to 2010 in Chicago and Los Angeles households that included an index case with an S. aureus SSTI. Identifying unique single nucleotide polymorphisms (SNPs) and analyzing whole-genome phylogeny, we characterized isolates to understand transmission dynamics, genetic relatedness, and microevolution of USA300 MRSA within the households. We also compared the 146 USA300 MRSA isolates from our study with the previously published genome sequences of the USA300 MRSA isolates from San Diego (n = 35) and New York City (n = 277). We found little genetic variation within the USA300 MRSA household isolates from Los Angeles (mean number of SNPs ± standard deviation, 17.6 ± 35; π nucleotide diversity, 3.1 × 10−5) or from Chicago (mean number of SNPs ± standard deviation, 12 ± 19; π nucleotide diversity, 3.1 × 10−5). The isolates within a household clustered into closely related monophyletic groups, suggesting the introduction into and transmission within each household of a single common USA300 ancestral strain. From a Bayesian evolutionary reconstruction, we inferred that USA300 persisted within households for 2.33 to 8.35 years prior to sampling. We also noted that fluoroquinolone-resistant USA300 clones emerged around 1995 and were more widespread in Los Angeles and New York City than in Chicago. Our findings strongly suggest that unique USA300 MRSA isolates are transmitted within households that contain an individual with an SSTI. Decolonization of household members may be a critical component of prevention programs to control USA300 MRSA spread in the United States.
USA300, a virulent and easily transmissible strain of methicillin-resistant Staphylococcus aureus (MRSA), is the predominant community-associated MRSA clone in the United States. It most commonly causes skin infections but also causes necrotizing pneumonia and endocarditis. Strategies to limit the spread of MRSA in the community can only be effective if we understand the most common sources of transmission and the microevolutionary processes that provide a fitness advantage to MRSA. We performed a whole-genome sequence comparison of 146 USA300 MRSA isolates from Chicago and Los Angeles. We show that households represent a frequent site of transmission and a long-term reservoir of USA300 strains; individuals within households transmit the same USA300 strain among themselves. Our study also reveals that a large proportion of the USA300 isolates sequenced are resistant to fluoroquinolone antibiotics. The significance of this study is that if households serve as long-term reservoirs of USA300, household MRSA eradication programs may result in a uniquely effective control method.
PMCID: PMC4453535  PMID: 25759497
6.  Retrospective study of necrotizing fasciitis and characterization of its associated Methicillin-resistant Staphylococcus aureus in Taiwan 
BMC Infectious Diseases  2011;11:297.
Methicillin-resistant Staphylococcus aureus (MRSA) has emerged as a prevalent pathogen of necrotizing fasciitis (NF) in Taiwan. A four-year NF cases and clinical and genetic differences between hospital acquired (HA)- and community-acquired (CA)-MRSA infection and isolates were investigated.
A retrospective study of 247 NF cases in 2004-2008 and antimicrobial susceptibilities, staphylococcal chromosomal cassette mec (SCCmec) types, pulsed field gel electrophoresis (PFGE) patterns, virulence factors, and multilocus sequence typing (MLST) of 16 NF-associated MRSA in 2008 were also evaluated.
In 247 cases, 42 microbial species were identified. S. aureus was the major prevalent pathogen and MRSA accounted for 19.8% of NF cases. Most patients had many coexisting medical conditions, including diabetes mellitus, followed by hypertension, chronic azotemia and chronic hepatic disease in order of decreasing prevalence. Patients with MRSA infection tended to have more severe clinical outcomes in terms of amputation rate (p < 0.05) and reconstruction rate (p = 0.001) than those with methicillin-sensitive S. aureus or non-S. aureus infection. NF patients infected by HA-MRSA had a significantly higher amputation rate, comorbidity, C-reactive protein level, and involvement of lower extremity than those infected by CA-MRSA. In addition to over 90% of MRSA resistant to erythromycin and clindamycin, HA-MRSA was more resistant than CA-MRSA to trimethoprim-sulfamethoxazole (45.8% vs. 4%). ST59/pulsotype C/SCCmec IV and ST239/pulsotype A/SCCmec III isolates were the most prevalent CA- and HA-MRSA, respectively in 16 isolates obtained in 2008. In contrast to the gene for γ-hemolysin found in all MRSA, the gene for Panton-Valentine leukocidin was only identified in ST59 MRSA isolates. Other three virulence factors TSST-1, ETA, and ETB were occasionally identified in MRSA isolates tested.
NF patients with MRSA infection, especially HA-MRSA infection, had more severe clinical outcomes than those infected by other microbial. The prevalent NF-associated MRSA clones in Taiwan differed distinctly from the most predominant NF-associated USA300 CA-MRSA clone in the USA. Initial empiric antimicrobials with a broad coverage for MRSA should be considered in the treatment of NF patients in an endemic area.
PMCID: PMC3221646  PMID: 22040231
7.  High Genetic Diversity among Community-Associated Staphylococcus aureus in Europe: Results from a Multicenter Study 
PLoS ONE  2012;7(4):e34768.
Several studies have addressed the epidemiology of community-associated Staphylococcus aureus (CA-SA) in Europe; nonetheless, a comprehensive perspective remains unclear. In this study, we aimed to describe the population structure of CA-SA and to shed light on the origin of methicillin-resistant S. aureus (MRSA) in this continent.
Methods and Findings
A total of 568 colonization and infection isolates, comprising both MRSA and methicillin-susceptible S. aureus (MSSA), were recovered in 16 European countries, from community and community-onset infections. The genetic background of isolates was characterized by molecular typing techniques (spa typing, pulsed-field gel electrophoresis and multilocus sequence typing) and the presence of PVL and ACME was tested by PCR. MRSA were further characterized by SCCmec typing. We found that 59% of all isolates were associated with community-associated clones. Most MRSA were related with USA300 (ST8-IVa and variants) (40%), followed by the European clone (ST80-IVc and derivatives) (28%) and the Taiwan clone (ST59-IVa and related clonal types) (15%). A total of 83% of MRSA carried Panton-Valentine leukocidin (PVL) and 14% carried the arginine catabolic mobile element (ACME). Surprisingly, we found a high genetic diversity among MRSA clonal types (ST-SCCmec), Simpson’s index of diversity = 0.852 (0.788–0.916). Specifically, about half of the isolates carried novel associations between genetic background and SCCmec. Analysis by BURP showed that some CA-MSSA and CA-MRSA isolates were highly related, suggesting a probable local acquisition/loss of SCCmec.
Our results imply that CA-MRSA origin, epidemiology and population structure in Europe is very dissimilar from that of USA.
PMCID: PMC3338755  PMID: 22558099
8.  Characterization of Methicillin-Resistant Staphylococcus aureus Strains Recovered from a Phase IV Clinical Trial for Linezolid versus Vancomycin for Treatment of Nosocomial Pneumonia 
Journal of Clinical Microbiology  2012;50(11):3694-3702.
A total of 434 methicillin-resistant Staphylococcus aureus (MRSA) baseline isolates were collected from subjects enrolled in a prospective, double-blind randomized trial comparing linezolid versus vancomycin for the treatment of nosocomial pneumonia. Isolates were susceptibility tested by broth microdilution, examined for inducible clindamycin resistance by D-test, and screened for heterogeneous resistance to vancomycin (hVISA) by the Etest macromethod. All strains were subjected to Panton-Valentine leukocidin (PVL) screening, and SCCmec, pulsed-field gel electrophoresis (PFGE), and spa typing. Selected strains were evaluated by multilocus sequence typing (MLST). Clonal complexes (CCs) were assigned based on the spa and/or MLST results. Most strains were CC5 (56.0%), which originated from North America (United States) (CC5-MRSA-SCCmec II/IV; 70.0%), Asia (CC5-MRSA-II; 14.0%) and Latin America (CC5-MRSA-I/II; 12.3%). The second- and third-most-prevalent clones were CC8-MRSA-IV (23.3%) and CC239-MRSA-III (11.3%), respectively. Furthermore, the CC5-MRSA-I/II clone predominated in Asia (50.7% within this region) and Latin America (66.7%), followed by CC239-MRSA-III (32.8% and 28.9%, respectively). The European strains were CC8-MRSA-IV (34.5%), CC22-MRSA-IV (18.2%), or CC5-MRSA-I/II/IV (16.4%), while the U.S. MRSA isolates were CC5-MRSA-II/IV (64.4%) or CC8-MRSA-IV (28.8%). Among the U.S. CC8-MRSA-II/IV strains, 73.7% (56/76 [21.2% of all U.S. MRSA strains]) clustered within USA300. One strain from the United States (USA800) was intermediate to vancomycin (MIC, 4 μg/ml). All remaining strains were susceptible to linezolid, daptomycin, vancomycin, and teicoplanin. hVISA strains (14.5%) were predominantly CC5-MRSA-II, from South Korea, and belonged to a single PFGE type. Overall, each region had two predominant clones. The USA300 rate corroborates previous reports describing increased prevalence of USA300 strains causing invasive infections. The prevalence of hVISA was elevated in Asia, and these strains were associated with CC5.
PMCID: PMC3486224  PMID: 22972817
9.  CC8 MRSA Strains Harboring SCCmec Type IVc are Predominant in Colombian Hospitals 
PLoS ONE  2012;7(6):e38576.
Recent reports highlight the incursion of community-associated MRSA within healthcare settings. However, knowledge of this phenomenon remains limited in Latin America. The aim of this study was to evaluate the molecular epidemiology of MRSA in three tertiary-care hospitals in Medellín, Colombia.
An observational cross-sectional study was conducted from 2008–2010. MRSA infections were classified as either community-associated (CA-MRSA) or healthcare-associated (HA-MRSA), with HA-MRSA further classified as hospital-onset (HAHO-MRSA) or community-onset (HACO-MRSA) according to standard epidemiological definitions established by the U.S. Centers for Disease Control and Prevention (CDC). Genotypic analysis included SCCmec typing, spa typing, PFGE and MLST.
Out of 538 total MRSA isolates, 68 (12.6%) were defined as CA-MRSA, 243 (45.2%) as HACO-MRSA and 227 (42.2%) as HAHO-MRSA. The majority harbored SCCmec type IVc (306, 58.7%), followed by SCCmec type I (174, 33.4%). The prevalence of type IVc among CA-, HACO- and HAHO-MRSA isolates was 92.4%, 65.1% and 43.6%, respectively. From 2008 to 2010, the prevalence of type IVc-bearing strains increased significantly, from 50.0% to 68.2% (p = 0.004). Strains harboring SCCmec IVc were mainly associated with spa types t1610, t008 and t024 (MLST clonal complex 8), while PFGE confirmed that the t008 and t1610 strains were closely related to the USA300-0114 CA-MRSA clone. Notably, strains belonging to these three spa types exhibited high levels of tetracycline resistance (45.9%).
CC8 MRSA strains harboring SCCmec type IVc are becoming predominant in Medellín hospitals, displacing previously reported CC5 HA-MRSA clones. Based on shared characteristics including SCCmec IVc, absence of the ACME element and tetracycline resistance, the USA300-related isolates in this study are most likely related to USA300-LV, the recently-described ‘Latin American variant’ of USA300.
PMCID: PMC3380008  PMID: 22745670
10.  Community-Acquired Methicillin-Resistant Staphylococcus aureus: Prevalence and Risk Factors  
Journal of Athletic Training  2006;41(3):337-340.
Reference/Citation: Salgado CD, Farr BM, Calfee DP. Community-acquired methicillin-resistant Staphylococcus aureus: a meta-analysis of prevalence and risk factors. Clin Infect Dis.20033613113912522744.
Clinical Question: What are the prevalence rates and risk factors associated with community-acquired methicillin-resistant Staphylococcus aureus (MRSA)?
Data Sources: Studies were identified by searching MEDLINE (January 1966–February 2002) and abstracts from scientific meetings (1996–2001). Reviews of citations and reference lists were performed to identify additional eligible studies. The search terms included Staphylococcus aureus , infection, colonization, methicillin resistance, community-acquired, community-onset, prevalence, frequency, and risk factors.
Study Selection: The search was limited to English-language investigations identified from the electronic and manual searches. Studies were divided into 2 groups, as follows: group 1, retrospective or prospective studies that reported the prevalence of community-acquired MRSA (CA-MRSA) among hospital patients who were colonized (presence of bacteria without infection) or infected with MRSA; and group 2, studies that reported the prevalence of MRSA colonization in the community. The studies were evaluated independently by 2 authors, and case reports were excluded.
Data Extraction: Data extraction and study quality assessment procedures were not fully explained. The outcome measures for hospital patients were definitions of CA-MRSA used in the study, prevalence of CA-MRSA, sample size, number and type of risk factors assessed, and number of patients with ≥1 health care–associated risk factor. The studies were grouped based on type, retrospective or prospective. The pooled prevalence of CA-MRSA was calculated for each group (retrospective or prospective) and was limited to the prevalence among patients with MRSA. The proportion of patients who reported ≥1 health care–associated risk factor was also calculated. The outcome measures among community members were prevalence of MRSA, sample size, number and type of risk factors assessed, number of members with ≥1 risk factor, and MRSA strain type, when available. The studies were grouped based on the population surveyed (surveillance cultures, contacts with MRSA-colonized individuals, or sport team members or day care contacts). The pooled prevalence of MRSA colonization and the proportion of members with ≥1 reported risk factor were calculated for each of the study populations listed above. The proportion of CA-MRSA strains that represented typical nosocomial (infection that develops in the hospital) strains was also determined. Chi-square analysis was performed to compare proportions and to determine heterogeneity among the studies.
Main Results: Specific search criteria identified 104 studies for review, of which 57 met inclusion and exclusion criteria. Thirty-nine studies focused on CA-MRSA among hospital patients who were colonized or infected with MRSA. Of these, 32 groups (27 retrospective, 5 prospective) reported the prevalence of CA-MRSA using clinical specimens. Seven groups identified risk factors of CA-MRSA among patients previously diagnosed with MRSA. Thirteen different definitions of CA-MRSA were used in 31 of these studies, and 8 groups did not report the definitions used. The isolation of MRSA within 48 hours of hospital admission, with or without recent admission to a hospital or long-term care facility, or previous history of MRSA colonization were the most common definitions in the studies.
The risk factors included recent hospitalization (range, 1–24 months before identification of MRSA infection or colonization), recent outpatient visit (usually within 12 months), recent nursing home admission (usually within 12 months), recent antibiotic exposure (range, 1–12 months), chronic illness (eg, end-stage renal disease, diabetes, or malignancy), injection drug use, and close contact with a person who had risk factor(s) for MRSA acquisition. The presence of health care–associated risk factors was examined in 17 of the retrospective studies, and the median number of factors studied was 2 (range, 1–6). Among 4121 patients in these studies, 86.1% were found to have ≥1 health care–associated risk factor. All authors of prospective studies (5) examined health care–associated risk factors, and the median number of factors studied was 4 (range, 2–4). Among the 636 patients, 86.9% had ≥1 health care–associated risk factor. In the 7 studies with 515 patients previously diagnosed with MRSA, 84.7% had ≥1 health care–associated risk factor. The most common risk factors assessed in the 17 retrospective studies were recent hospitalization and chronic illness requiring health care visits.
The pooled CA-MRSA prevalence was 30.2% (range, 1.9%– 96%) among 5932 patients from the 27 retrospective studies and 37.3% (range, 18.2%–51.2%) among 636 patients from the 5 prospective studies. Eighteen groups reported the prevalence of MRSA colonization in the community. Ten of these reported MRSA prevalence using surveillance cultures, 4 examined colonization status of household contacts with discharged hospital patients with nosocomial MRSA colonization, and 4 reported colonization status of sports team members or day care contacts of persons colonized with MRSA. In the 10 surveillance studies, the pooled MRSA colonization prevalence was 1.3% (95% confidence interval [CI], 1.04%–1.53%; range, 0.2%– 7.4%) among 8350 community members. Nine of these studies were stratified based on culture samples taken before the assessment of risk factors, and among 4825 people, the pooled MRSA colonization prevalence was 2.1%. When examining health care–associated risk factors, the median number of factors studied was 5 (range, 1–10), and 47.5% with MRSA had ≥1 health care–associated risk factor. The risk factors included those previously identified. In the remaining surveillance study, the MRSA colonization prevalence was 0.20% among 3525 people without prior health care contact. Compared with subjects in the 9 stratified studies with a health care contact, subjects in this study were 90% less likely to have MRSA (relative risk, 0.10; 95% CI, 0.05–0.21). Cultures for 3898 subjects in 7 of the 10 surveillance studies were obtained at the time of a hospital admission, an outpatient clinic visit, or an emergency department visit, and the pooled prevalence of MRSA colonization was 1.8%. In 3 studies in which cultures were obtained outside of a health care facility (schools, day care centers, homeless shelters, or military bases), the pooled MRSA colonization prevalence among 4452 subjects was reported to be 0.76%. Therefore, subjects in a health care facility were 2.35 times more likely to carry MRSA than were subjects outside of a health care facility (95% CI, 1.56–3.53). In one study examining 94 subjects in a semiclosed community, the prevalence of MRSA colonization was 7.4%. These subjects were 36 times more likely to carry MRSA than were subjects who were not in a semiclosed community (95% CI, 13.7–94.7).
The studies also identified 70 MRSA isolates (pure form of an organism in a microbial culture) from subjects who reported no health care–associated risk factors. Strain typing was performed with 32 isolates, and 29 (91%) isolates were similar to strains identified in hospitals. The colonization status of 191 household contacts of 93 patients with nosocomial MRSA colonization discharged from the hospital was examined in 4 studies. The results demonstrated that 17.8% of the contact subjects were colonized with a strain of MRSA having the same antibiogram (record of the susceptibility of bacteria to antibiotics) as the index case (initial individual with the strain). The authors reported that subjects who had household contacts with MRSA-colonized patients were 14 times more likely to be colonized than were community subjects without a known MRSA contact (95% CI, 9.8–20.1). In 4 studies examining 517 sports team members or day care contacts of persons known to be colonized with MRSA, 5.4% demonstrated colonization of MRSA with the same strain as the index case.
Conclusions: Based on the available data, the prevalence of MRSA among community members without health care–associated risk factors was relatively low. However, 85% of hospital patients diagnosed with CA-MRSA and 47.5% of healthy community members colonized with MRSA were found to have ≥1 health care–associated risk factor. The risk factors identified were recent hospitalization, outpatient visit, nursing home admission, antibiotic exposure, chronic illness, injection drug use, and close contact with a person with risk factor(s). Most MRSA colonization occurred among community members who had health care–associated risk factors or contact with persons with risk factors. The evidence indicated that control of MRSA in the community may require control of MRSA in the health care setting (hospital, health care office, and nursing home). The absence of a standardized definition for CA-MRSA and questions regarding the actual site of colonization versus acquisition should be considered in the interpretation of these findings.
PMCID: PMC1569547  PMID: 17043704
infectious diseases
11.  Subtle genetic changes enhance virulence of methicillin resistant and sensitive Staphylococcus aureus 
BMC Microbiology  2007;7:99.
Community acquired (CA) methicillin-resistant Staphylococcus aureus (MRSA) increasingly causes disease worldwide. USA300 has emerged as the predominant clone causing superficial and invasive infections in children and adults in the USA. Epidemiological studies suggest that USA300 is more virulent than other CA-MRSA. The genetic determinants that render virulence and dominance to USA300 remain unclear.
We sequenced the genomes of two pediatric USA300 isolates: one CA-MRSA and one CA-methicillin susceptible (MSSA), isolated at Texas Children's Hospital in Houston. DNA sequencing was performed by Sanger dideoxy whole genome shotgun (WGS) and 454 Life Sciences pyrosequencing strategies. The sequence of the USA300 MRSA strain was rigorously annotated. In USA300-MRSA 2658 chromosomal open reading frames were predicted and 3.1 and 27 kilobase (kb) plasmids were identified. USA300-MSSA contained a 20 kb plasmid with some homology to the 27 kb plasmid found in USA300-MRSA. Two regions found in US300-MRSA were absent in USA300-MSSA. One of these carried the arginine deiminase operon that appears to have been acquired from S. epidermidis. The USA300 sequence was aligned with other sequenced S. aureus genomes and regions unique to USA300 MRSA were identified.
USA300-MRSA is highly similar to other MRSA strains based on whole genome alignments and gene content, indicating that the differences in pathogenesis are due to subtle changes rather than to large-scale acquisition of virulence factor genes. The USA300 Houston isolate differs from another sequenced USA300 strain isolate, derived from a patient in San Francisco, in plasmid content and a number of sequence polymorphisms. Such differences will provide new insights into the evolution of pathogens.
PMCID: PMC2222628  PMID: 17986343
12.  Population Structure of Staphylococcus aureus from Remote African Babongo Pygmies 
Pandemic community-acquired methicillin-resistant Staphylococcus aureus isolates (CA-MRSA) predominantly encode the Panton-Valentine leukocidin (PVL), which can be associated with severe infections. Reports from non-indigenous Sub-Saharan African populations revealed a high prevalence of PVL-positive isolates. The objective of our study was to investigate the S. aureus carriage among a remote indigenous African population and to determine the molecular characteristics of the isolates, particularly those that were PVL-positive.
Methodology/Principal Findings
Nasal S. aureus carriage and risk factors of colonization were systematically assessed in remote Gabonese Babongo Pygmies. Susceptibility to antibiotics, possession of toxin-encoding genes (i.e., PVL, enterotoxins, and exfoliative toxins), S. aureus protein A (spa) types and multi-locus sequence types (MLST) were determined for each isolate. The carriage rate was 33%. No MRSA was detected, 61.8% of the isolates were susceptible to penicillin. Genes encoding PVL (55.9%), enterotoxin B (20.6%), exfoliative toxin D (11.7%) and the epidermal cell differentiation inhibitor B (11.7%) were highly prevalent. Thirteen spa types were detected and were associated with 10 STs predominated by ST15, ST30, ST72, ST80, and ST88.
The high prevalence of PVL-positive isolates among Babongo Pygmies demands our attention as PVL can be associated with necrotinzing infection and may increase the risk of severe infections in remote Pygmy populations. Many S. aureus isolates from Babongo Pygmies and pandemic CA-MRSA-clones have a common genetic background. Surveillance is needed to control the development of resistance to antibiotic drugs and to assess the impact of the high prevalence of PVL in indigenous populations.
Author Summary
Staphylococcus aureus is a bacterium that colonizes humans worldwide. The anterior nares are its main ecological niche. Carriers of S. aureus are at a higher risk of developing invasive infections. Few reports indicated a different clonal structure and profile of virulence factors in S. aureus isolates from Sub-Saharan Africa. As there are no data about isolates from remote indigenous African populations, we conducted a cross-sectional survey of S. aureus nasal carriage in Gabonese Babongo Pygmies. The isolates were characterized regarding their susceptibility to antibiotic agents, possession of virulence factors and clonal lineage. While similar carriage rates were found in populations of industrialized countries, isolates that encode the genes for the Panton-Valentine leukocidin (PVL) were clearly more prevalent than in European countries. Of interest, many methicillin-susceptible S. aureus isolates from Babongo Pygmies showed the same genetic background as pandemic methicillin-resistant S. aureus (MRSA) clones. We advocate a surveillance of S. aureus in neglected African populations to control the development of resistance to antibiotic drugs with particular respect to MRSA and to assess the impact of the high prevalence of PVL-positive isolates.
PMCID: PMC3091839  PMID: 21572985
13.  Molecular Evidence for Spread of Two Major Methicillin-Resistant Staphylococcus aureus Clones with a Unique Geographic Distribution in Chinese Hospitals▿  
Methicillin (meticillin)-resistant Staphylococcus aureus (MRSA) is a serious problem worldwide. To investigate the molecular epidemiology of MRSA isolates in China, a total of 702 MRSA isolates collected from 18 teaching hospitals in 14 cities between 2005 and 2006 were characterized by antibiogram analysis, pulsed-field gel electrophoresis (PFGE), staphylococcal cassette chromosome mec (SCCmec) typing, and spa typing; and 102 isolates were selected for multilocus sequence typing (MLST). Overall, SCCmec type III was the most popular type and was found in 541 isolates (77.1%), followed by SCCmec type II (109/702; 15.5%). Twenty-four PFGE types were obtained among 395 isolates collected in 2005, and 18 spa types were obtained among 702 isolates. spa type t030, which corresponded to PFEG types A to E, constituted 52.0% (365/702) of all isolates, and isolates of this type were present in all 14 cities; spa type t037, which corresponded to PFGE types F and G, accounted for 25.5% (179/702) of all isolates, and isolates of this type were identified in 12 cities. The two spa genotypes belonged to sequence type 239 (ST239) and carried SCCmec type III. spa type t002, which included isolates of PFGE types L to T, made up 16.0% (112/702) of the isolates that belonged to ST5 and SCCmec type II, and isolates of this type were distributed in 12 cities. The distribution of spa types varied among the regions. spa type t002 was the most common in Dalian (53.4%) and Shenyang (44.4%); spa type t037 was predominant in Shanghai (74.8%), whereas spa type t030 was the most common in the other cities. Two isolates from Guangzhou that harbored SCCmec type IVa with ST59 and ST88 were identified as community-associated MRSA. The prevalence of the Panton-Valentine leukocidin gene was 2.3%. The data documented two major epidemic MRSA clones, ST239-MRSA-SCCmec type III and ST5-MRSA-SCCmec type II, with unique geographic distributions across China.
PMCID: PMC2630620  PMID: 19029328
14.  Molecular characterization of Staphylococcus aureus from outpatients in the Caribbean reveals the presence of pandemic clones 
Staphylococcus aureus infections continue to pose a global public health problem. Frequently, this epidemic is driven by the successful spread of single S. aureus clones within a geographic region, but international travel has been recognized as a potential risk factor for S. aureus infections. To study the molecular epidemiology of S. aureus infections in the Caribbean, a major international tourist destination, we collected methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA) isolates from community-onset infections in the Dominican Republic (n=112) and Martinique (n=143). Isolates were characterized by a combination of pulsed-field gel electrophoresis (PFGE), spa typing, and multilocus sequence typing (MLST) typing. In Martinique, MRSA infections (n=56) were mainly caused by t304-ST8 strains (n=44), whereas MSSA isolates were derived from genetically diverse backgrounds. Among MRSA strains (n=22) from the Dominican Republic, ST5, ST30, and ST72 predominated, while ST30 t665-PVL+ (30/90) accounted for a substantial number of MSSA infections. Despite epidemiological differences in sample collections from both countries, a considerable number of MSSA infections (~10%) were caused by ST5 and ST398 isolates at each site. Further phylogenetic analysis suggests the presence of lineages shared by the two countries, followed by recent genetic diversification unique to each site. Our findings also imply the frequent import and exchange of international S. aureus strains in the Caribbean.
PMCID: PMC3226914  PMID: 21789605
15.  Emergence of New CMRSA7/USA400 Methicillin-Resistant Staphylococcus aureus spa Types in Alberta, Canada, from 2005 to 2012 
Journal of Clinical Microbiology  2014;52(7):2439-2446.
Methicillin-resistant Staphylococcus aureus (MRSA) has become one of the most significant pathogens affecting global public health and health care systems. In Canada and the United States, the spread of MRSA is primarily attributed to a single dominant epidemic clone: CMRSA10/USA300. Despite this, the CMRSA7/USA400 epidemic clone has been reported to be the predominate epidemic clone in several Canadian provinces and some parts of the United States. This study examined the epidemiology of CMRSA7/USA400 MRSA in Alberta, Canada, from June 2005 to December 2012. Molecular characterization of CMRSA7/USA400 isolates was done using spa, SCCmec, PVL, and PFGE typing and identified two predominant spa types in Alberta: t128 and t1787. Although closely related, these spa types have distinct geographic distributions. From 2010 to 2012, the number of t128 infections has remained stable while there has been a nearly 3-fold increase in the number of provincial t1787 infections, accompanied by 10-fold increases in t1787 infection rates in some communities. Most t128 and t1787 patients were First Nations or Inuit people, and isolates were usually from skin and soft tissue infections in outpatients. t128 patients were significantly older than t1787 patients. Antimicrobial susceptibility testing showed higher mupirocin resistance in t1787 than in t128 MRSA. Improved strategies to reduce or stabilize t1787 infections in Alberta are needed.
PMCID: PMC4097756  PMID: 24789179
16.  USA300 and USA500 Clonal Lineages of Staphylococcus aureus Do Not Produce a Capsular Polysaccharide Due to Conserved Mutations in the cap5 Locus 
mBio  2015;6(2):e02585-14.
The surface capsular polysaccharide (CP) is a virulence factor that has been used as an antigen in several successful vaccines against bacterial pathogens. A vaccine has not yet been licensed against Staphylococcus aureus, although two multicomponent vaccines that contain CP antigens are in clinical trials. In this study, we evaluated CP production in USA300 methicillin-resistant S. aureus (MRSA) isolates that have become the predominant community-associated MRSA clones in the United States. We found that all 167 USA300 MRSA and 50 USA300 methicillin-susceptible S. aureus (MSSA) isolates were CP negative (CP−). Moreover, all 16 USA500 isolates, which have been postulated to be the progenitor lineage of USA300, were also CP−. Whole-genome sequence analysis of 146 CP− USA300 MRSA isolates revealed they all carry a cap5 locus with 4 conserved mutations compared with strain Newman. Genetic complementation experiments revealed that three of these mutations (in the cap5 promoter, cap5D nucleotide 994, and cap5E nucleotide 223) ablated CP production in USA300 and that Cap5E75 Asp, located in the coenzyme-binding domain, is essential for capsule production. All but three USA300 MSSA isolates had the same four cap5 mutations found in USA300 MRSA isolates. Most isolates with a USA500 pulsotype carried three of these four USA300-specific mutations, suggesting the fourth mutation occurred in the USA300 lineage. Phylogenetic analysis of the cap loci of our USA300 isolates as well as publicly available genomes from 41 other sequence types revealed that the USA300-specific cap5 mutations arose sequentially in S. aureus in a common ancestor of USA300 and USA500 isolates.
The USA300 MRSA clone emerged as a community-associated pathogen in the United States nearly 20 years ago. Since then, it has rapidly disseminated and now causes health care-associated infections. This study shows that the CP-negative (CP−) phenotype has persisted among USA300 isolates and is a universal and characteristic trait of this highly successful MRSA lineage. It is important to note that a vaccine consisting solely of CP antigens would not likely demonstrate high efficacy in the U.S. population, where about half of MRSA isolates comprise USA300. Moreover, conversion of a USA300 strain to a CP-positive (CP+) phenotype is unlikely in vivo or in vitro since it would require the reversion of 3 mutations. We have also established that USA300 MSSA isolates and USA500 isolates are CP− and provide new insight into the evolution of the USA300 and USA500 lineages.
PMCID: PMC4453534  PMID: 25852165
17.  Rapid Change of Methicillin-Resistant Staphylococcus aureus Clones in a Chinese Tertiary Care Hospital over a 15-Year Period▿  
The incidence of methicillin-resistant Staphylococcus aureus (MRSA) has been increasing yearly at Peking Union Medical College Hospital (PUMCH). In order to understand the molecular evolution of MRSA at PUMCH, a total of 466 nonduplicate S. aureus isolates, including 302 MRSA and 164 methicillin-susceptible (MSSA) isolates recovered from 1994 to 2008 were characterized by staphylococcal cassette chromosome mec (SCCmec) typing, spa typing, pulsed-field gel electrophoresis (PFGE), and multilocus sequence typing (MLST). The 302 MRSA isolates were classified into 12 spa types and 9 sequence types (STs). During the years from 1994 to 2000, the most predominant MRSA clone was ST239-MRSA-III-spa t037. Since 2000, ST239-MRSA-III-spa t030 has rapidly replaced t037 and become the major clone. Another clone, ST5-MRSA-II-spa t002 emerged in 2002 and constantly existed at a low prevalence rate. The 164 MSSA isolates were classified into 62 spa types and 40 STs. ST398 was the most common MLST type for MSSA, followed by ST59, ST7, ST15, and ST1. Several MSSA genotypes, including ST398, ST1, ST121, and ST59, were identical to well-known epidemic community-acquired MRSA (CA-MRSA) isolates. MLST eBURST analysis revealed that the ST5, ST59, and ST965 clones coexisted in both MRSA and MSSA, which suggested that these MRSA clones might have evolved from MSSA by the acquisition of SCCmec. Two pvl-positive ST59-MRSA-IV isolates were identified as CA-MRSA according to the clinical data. Overall, our data showed that the ST239-MRSA-III-spa t037 clone was replaced by the emerging ST239-MRSA-III-spa t030 clone, indicating a rapid change of MRSA at a tertiary care hospital in China over a 15-year period.
PMCID: PMC2863666  PMID: 20176895
18.  An uncommon presentation for a severe invasive infection due to methicillin-resistant Staphylococcus aureus clone USA300 in Italy: a case report 
Methicillin resistant Staphylococcus aureus (MRSA) has been considered for many years a typical nosocomial pathogen. Recently MRSA has emerged as a frequent cause of infections in the community. More commonly, community-acquired (CA)-MRSA is a cause of infections of the skin and soft-tissues, but life-threatening infections such as necrotizing pneumonia and sepsis can occasionally occur.
Case presentation
This report describes an uncommon presentation of invasive CA-MRSA infection in an adolescent without known risk factors. The presentation was typical for bacterial meningitis, but the clinical findings also revealed necrotizing pneumonia. Following the development of deep venous thrombosis, the presence of an inherited trombophilic defect (factor V Leiden) was detected. The patient was successfully treated with an antibiotic combination including linezolid and with anticoagulant therapy. CA-MRSA was isolated from both cerebrospinal fluid and blood. The isolates were resistant to oxacillin and other beta-lactam antibiotics and susceptible to the other antibiotics tested including erythromycin. Molecular typing revealed that the strains contained the Panton-Valentine leukocidin genes and type IV SCCmec, and were ST8, spa type t008, and agr type 1. This genetic background is identical to that of the USA300 clone.
This report highlights that meningitis can be a new serious presentation of CA-MRSA infection. CA-MRSA strains with the genetic background of the USA300 clone are circulating in Italy and are able to cause severe infections.
PMCID: PMC2390582  PMID: 18447939
19.  Molecular Epidemiology of Methicillin-Resistant Staphylococcus aureus (MRSA) among Patients Admitted to Adult Intensive Care Units: the STAR*ICU Trial 
The multi-center cluster-randomized Strategies to Reduce Transmission of Antimicrobial Resistant Bacteria in Intensive Care Units (STAR*ICU) trial was carried out in 18 U.S. adult intensive care units (ICUs) and evaluated the effectiveness of infection control strategies in reducing transmission of methicillin-resistant Staphylococcus aureus (MRSA) colonization and/or infection. Our study objective was to examine the molecular epidemiology of MRSA and assess the prevalence and risk factors for community acquired (CA)-MRSA genotype nasal carriage at the time of ICU admission.
Selected MRSA isolates were subjected to molecular typing using pulsed-field gel electrophoresis.
Among 5,512 ICU patient-admissions in the STAR*ICU trial during the intervention period, 626 (11%) had a positive nares culture for MRSA. 210/626 (34%) available isolates were selected by weighted random sampling for molecular typing. Of 210 patients, 123 (59%) were male; mean age was 63 years. Molecular typing revealed that 147 isolates (70%) were the USA100 clone; 26 (12%) USA300; 12 (6%) USA500; 8 (4%) USA800; 17 (8%) other. In multivariate analysis, patients with CA-MRSA genotype (USA300, USA400, or USA1000) colonization were less likely to have been hospitalized during the previous 12 months (PR=0.39; 95% C.I. 0.21–0.73) and less likely to have an older age (PR=0.97 per year; 0.95–0.98) compared to patients with a HA-MRSA genotype.
CA-MRSA genotypes have emerged as a cause of MRSA nares colonization among patients admitted to adult ICUs in the U.S. During the study period (2006), the predominant site of CA-MRSA genotype acquisition appeared to be in the community.
PMCID: PMC4149749  PMID: 22011531
MRSA; community-associated; healthcare-associated; ICU
20.  Diversity of Methicillin-Resistant Staphylococcus aureus Strains Isolated from Residents of 26 Nursing Homes in Orange County, California 
Journal of Clinical Microbiology  2013;51(11):3788-3795.
Nursing homes represent a unique and important methicillin-resistant Staphylococcus aureus (MRSA) reservoir. Not only are strains imported from hospitals and the community, strains can be transported back into these settings from nursing homes. Since MRSA bacteria are prevalent in nursing homes and yet relatively poorly studied in this setting, a multicenter, regional assessment of the frequency and diversity of MRSA in the nursing home reservoir was carried out and compared to that of the MRSA from hospitals in the same region. The prospective study collected MRSA from nasal swabbing of residents of 26 nursing homes in Orange County, California, and characterized each isolate by spa typing. A total of 837 MRSA isolates were collected from the nursing homes. Estimates of admission prevalence and point prevalence of MRSA were 16% and 26%, respectively. The spa type genetic diversity was heterogeneous between nursing homes and significantly higher overall (77%) than the diversity in Orange County hospitals (72%). MRSA burden in nursing homes appears largely due to importation from hospitals. As seen in Orange County hospitals, USA300 (sequence type 8 [ST8]/t008), USA100 (ST5/t002), and a USA100 variant (ST5/t242) were the dominant MRSA clones in Orange County nursing homes, representing 83% of all isolates, although the USA100 variant was predominant in nursing homes, whereas USA300 was predominant in hospitals. Control strategies tailored to the complex problem of MRSA transmission and infection in nursing homes are needed in order to minimize the impact of this unique reservoir on the overall regional MRSA burden.
PMCID: PMC3889768  PMID: 24025901
21.  Prevalence and Characterization of Staphylococcus aureus, Including Methicillin-Resistant Staphylococcus aureus, Isolated from Bulk Tank Milk from Minnesota Dairy Farms 
Journal of Clinical Microbiology  2012;50(3):688-695.
Staphylococcus aureus is a common causative agent of bovine mastitis in dairy herds. The emergence of methicillin-resistant Staphylococcus aureus (MRSA) in hospitals as well as the community is a significant and costly public health concern. S. aureus-related bovine mastitis is a common reason for therapeutic and/or prophylactic use of antibiotics on dairy farms. In this study, herd prevalence of S. aureus, including MRSA, was estimated from bulk tank milk (BTM) from Minnesota farms. A total of 150 pooled BTM samples from 50 farms, collected over 3 seasons (spring, summer, and fall of 2009), were assessed. Herd prevalence of methicillin-susceptible S. aureus (MSSA) was 84%, while MRSA herd prevalence was 4%. A total of 93 MSSA isolates and 2 MRSA isolates were recovered from 150 BTM samples. Antibiotic susceptibility testing of S. aureus isolates showed pansusceptibility in 54 isolates, resistance to a single antibiotic class in 21 isolates, resistance to two antibiotic classes in 13 isolates, and resistance to ≥3 antibiotics classes and thus multidrug resistance in 5 isolates. The two MRSA isolates displayed resistance to β-lactams, cephalosporins, and lincosamides and were multiresistant. Staphylococcal protein A gene (spa) typing identified spa types t529 and t034 most frequently among methicillin-susceptible isolates, while t121 was observed in MRSA isolates. Seven isolates, including the two MRSA isolates, produced staphylococcal enterotoxins B, C, D, and E on overnight culture. MRSA isolates were further genotyped using multilocus sequence typing (MLST) and pulsed-field gel electrophoresis (PFGE). Of the 2 MRSA isolates, one had a composite genotype profile of MLST ST 5-PFGE USA100-unknown spa type, which has been reported among hospital-associated MRSA isolates, while the second isolate carried the MLST ST 8-PFGE USA300-spa type t121 genotype, commonly identified among community-associated MRSA isolates. These results suggest that MRSA genotypes associated with hospitals and community can be isolated from milk at very low rates.
PMCID: PMC3295154  PMID: 22170937
22.  Comparing Pulsed-Field Gel Electrophoresis with Multilocus Sequence Typing, spa Typing, Staphylococcal Cassette Chromosome mec (SCCmec) Typing, and PCR for Panton-Valentine Leukocidin, arcA, and opp3 in Methicillin-Resistant Staphylococcus aureus Isolates at a U.S. Medical Center 
Journal of Clinical Microbiology  2013;51(3):814-819.
Methicillin-resistant Staphylococcus aureus (MRSA) has become a common cause of skin infections and invasive infections in community dwellers in the United States since the late 1990s. Isolates characterized as USA300 by pulsed-field gel electrophoresis (PFGE) are the predominant strain type in these infections. USA100 and USA500 strains commonly cause health care-associated infections. We compared PFGE with a number of other methods of genotyping in a sample of 149 clinical MRSA isolates from the University of Chicago Medical Center. The 5 USA500 isolates yielded 3 spa types and 2 multilocus sequence types (MLSTs). Among the 24 USA100 isolates, 21 (88%) were of spa type t002, 19 (79%) were of ST5, 2 carried arcA and opp3, and 1 was Panton-Valentine leukocidin positive (PVL+). Among the 102 USA300 isolates, 96 (94%) were of ST8 and 94 (92%) were of spa type t008. The combination of traits that provided the best sensitivity (98%), specificity (97%), positive predictive value (PPV) (99%), and negative predictive value (NPV) (95%) for identifying USA300 isolates were the presence of the arcA gene and the presence of the PVL genes (area under the curve, 0.980; 95% confidence interval [CI], 0.955 to 1.0). PFGE did not delineate a homogeneous group of MRSA genetic backgrounds, as documented for other typing methods, particularly for USA500 and USA100 pulsotypes. Documenting the presence of arcA and PVL genes by PCR was an efficient and accurate means of identifying USA300 in a collection of MRSA isolates in which USA300 is common. None of the tested genotyping methods provided an accurate means of identifying the next most common PFGE-based backgrounds, USA100 and USA500.
PMCID: PMC3592068  PMID: 23269731
23.  Predominance of Community-Associated Methicillin-Resistant Staphylococcus aureus Strains Carrying Staphylococcal Chromosome Cassette mec Type IVA in South Korea▿  
Journal of Clinical Microbiology  2007;45(12):4021-4026.
Studies on the molecular epidemiologic characteristics of methicillin-resistant Staphylococcus aureus (MRSA) strains have demonstrated their genetic and geographical diversity. In addition, it has been reported that there are genetic differences between community-associated (CA) and health care-associated (HA) MRSA strains. Therefore, we investigated the major epidemiologic characteristics of CA MRSA isolates in South Korea and compared them with those of HA MRSA strains. Distributions of staphylococcal chromosome cassette mec (SCCmec) types and other molecular features, including the Panton-Valentine leukocidin (PVL) gene, were studied in 138 invasive MRSA isolates. Multiplex type IVA SCCmec was identified as the major CA MRSA infection type (53.1%), with a significantly higher prevalence than in HA MRSA (P < 0.001). One major group of type IVA strains carried a larger atypical class B mec element and new subtypes of ccrA2 (96% amino acid homology). The PVL gene was detected in one USA300-like isolate only. Seven major clone types determined by combinational grouping (genetic background SCCmec typing) showed representative patterns of antimicrobial susceptibilities. We concluded that less multi-drug-resistant strains of clone types B-I and D-1 (genetic background, B and D complexes; type IVA SCCmec) predominate in CA MRSA and that international PVL-positive strains have not spread in South Korea as yet.
PMCID: PMC2168574  PMID: 17942660
24.  Trends in Methicillin-Resistant Staphylococcus aureus Anovaginal Colonization in Pregnant Women in 2005 versus 2009▿  
Journal of Clinical Microbiology  2010;48(10):3675-3680.
In 2005, the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) anovaginal colonization in pregnant women at our center (Columbia University Medical Center) was 0.5%, and MRSA-colonized women were less likely to carry group B streptococcus (GBS). In this study, our objectives were to identify changing trends in the prevalence of MRSA and methicillin-susceptible S. aureus (MSSA) anovaginal colonization in pregnant women, to assess the association between MRSA and GBS colonization, and to characterize the MRSA strains. From February to July 2009, Lim broths from GBS surveillance samples were cultured for S. aureus. MRSA strains were identified by resistance to cefoxitin and characterized by MicroScan, staphylococcal cassette chromosome mec (SCCmec) typing, pulsed-field gel electrophoresis (PFGE), spa typing, and Panton-Valentine leukocidin PCR. A total of 2,921 specimens from different patients were analyzed. The prevalences of MSSA, MRSA, and GBS colonization were 11.8%, 0.6% and 23.3%, respectively. GBS colonization was associated with S. aureus colonization (odds ratio [OR], 1.9; 95% confidence interval [95% CI], 1.5 to 2.4). The frequencies of GBS colonization were similar in MRSA-positive (34.2%) versus MRSA-negative patients (21.8%) (P = 0.4). All MRSA isolates from 2009 and 13/14 isolates from 2005 were SCCmec type IV or V, consistent with community-associated MRSA; 12/18 (2009) and 0/14 (2005) isolates were the USA300 clone. Levofloxacin resistance increased from 14.3% (2005) to 55.6% (2009) (P = 0.028). In conclusion, the prevalence of MRSA anovaginal colonization in pregnant women in New York City, NY, remained stable from 2005 to 2009, and USA300 emerged as the predominant clone with a significant increase in levofloxacin-resistant isolates.
PMCID: PMC2953117  PMID: 20686089
25.  Epidemiology of European Community-Associated Methicillin-Resistant Staphylococcus aureus Clonal Complex 80 Type IV Strains Isolated in Denmark from 1993 to 2004▿  
In Europe, community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections have been caused predominantly by isolates belonging to the “European CA-MRSA” clone (sequence type 80, staphylococcal cassette chromosome mec type IV). In this study, the epidemiology of European CA-MRSA was investigated on a nationwide scale, covering the period from 1993 to 2004. Denmark has been a low-prevalence country regarding MRSA since the mid-1970s but has experienced an increase in the number of new MRSA cases in recent years. Our results show that European CA-MRSA contributed to this increase. The isolates primarily caused skin and soft tissue infections (SSTIs) in patients outside hospitals, and transmission between household members was the predominant mode of spread. Although some of the isolates were found in hospitalized patients, nosocomial transmission seemed likely in only one instance, pointing to endogenous infections as an important factor. Compared to the CA-MRSA clone most common in the United States (USA300), the European CA-MRSA clone seems less well adapted to persist in hospital environments. Patients with a recent history of travel or family relation to the Mediterranean or Middle East were highly overrepresented. The epidemiological data indicated that the European CA-MRSA isolates were introduced into Denmark on multiple occasions, paralleled by an increasing level of genetic diversity of the isolates found during the study period. European CA-MRSA has previously been described as a rather uniform clone. However, we found pronounced, diverse pulsed-field gel electrophoresis subtypes, staphylococcal protein A gene (spa) types, and susceptibility patterns.
PMCID: PMC2224276  PMID: 17989197

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