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1.  Identification of a Highly Transmissible Animal-Independent Staphylococcus aureus ST398 Clone with Distinct Genomic and Cell Adhesion Properties 
mBio  2012;3(2):e00027-12.
ABSTRACT
A methicillin-resistant Staphylococcus aureus (MRSA) clone known as ST398 has emerged as a major cause of acute infections in individuals who have close contact with livestock. More recently, the emergence of an animal-independent ST398 methicillin-sensitive S. aureus (MSSA) clone has been documented in several countries. However, the limited surveillance of MSSA has precluded an accurate assessment of the global spread of ST398 and its clinical relevance. Here we provide evidence that ST398 is a frequent source of MSSA infections in northern Manhattan and is readily transmitted between individuals in households. This contrasts with the limited transmissibility of livestock-associated ST398 (LA-ST398) MRSA strains between humans. Our whole-genome sequence analysis revealed that the chromosome of the human-associated ST398 MSSA clone is smaller than that of the LA-ST398 MRSA reference strain S0385, due mainly to fewer mobile genetic elements (MGEs). In contrast, human ST398 MSSA isolates harbored the prophage φ3 and the human-specific immune evasion cluster (IEC) genes chp and scn. While most of the core genome was conserved between the human ST398 MSSA clone and S0385, these strains differed substantially in their repertoire and composition of intact adhesion genes. These genetic changes were associated with significantly enhanced adhesion of human ST398 MSSA isolates to human skin keratinocytes and keratin. We propose that the human ST398 MSSA clone can spread independent of animal contact using an optimized repertoire of MGEs and adhesion molecules adapted to transmission among humans.
IMPORTANCE
Staphylococcus aureus strains have generally been considered to be species specific. However, cross-species transfers of S. aureus clones, such as ST398 methicillin-resistant S. aureus (MRSA), from swine to humans have been reported. Recently, we observed the emergence of ST398 methicillin-susceptible S. aureus (MSSA) as a colonizing strain of humans in northern Manhattan. Here we report that ST398 is a frequent cause of MSSA infections in this urban setting. The ST398 MSSA clone was readily transmitted within households, independent of animal contact. We discovered that human ST398 MSSA genomes were smaller than that of the LA-ST398 strain S0385 due to fewer mobile genetic elements. Human and LA-ST398 strains also differed in their composition of adhesion genes and their ability to bind to human skin keratinocytes, providing a potential mechanism of S. aureus host adaptation. Our findings illustrate the importance of implementing molecular surveillance of MSSA given the evidence for the rapid and clinically undetected spread of ST398 MSSA.
doi:10.1128/mBio.00027-12
PMCID: PMC3302565  PMID: 22375071
2.  Improved understanding of factors driving methicillin-resistant Staphylococcus aureus epidemic waves 
Clinical Epidemiology  2013;5:205-217.
Methicillin-resistant Staphylococcus aureus (MRSA) remains one of the most important causes of nosocomial infections worldwide. Since the global spread of MRSA in the 1960s, MRSA strains have evolved with increased pathogenic potential. Notably, some strains are now capable of causing persistent infections not only in hospitalized patients but also in healthy individuals in the community. Furthermore, MRSA is increasingly associated with infections among livestock-associated workers, primarily because of transmission from animals to humans. Moreover, many MRSA strains have gained resistance to most available antibiotics. In this review, we will present current knowledge on MRSA epidemiology and discuss new endeavors being undertaken to understand better the molecular and epidemiological underpinnings of MRSA outbreaks.
doi:10.2147/CLEP.S37071
PMCID: PMC3707418  PMID: 23861600
Staphylococcus aureus; MRSA; nosocomial infection; community-associated infection
3.  Suspected Goat-to-Human Transmission of Methicillin-Resistant Staphylococcus aureus Sequence Type 398 
Journal of Clinical Microbiology  2013;51(5):1625-1626.
Transmission of methicillin-resistant Staphylococcus aureus (MRSA) between animals and humans is widely recognized. In this study, we describe the first case of infection of a goat and suspected transmission of MRSA ST398 to a human, which resulted in colonization of animal owners by MRSA sequence type 398.
doi:10.1128/JCM.03052-12
PMCID: PMC3647931  PMID: 23447633
4.  The effect of co-colonization with community-acquired and hospital-acquired methicillin-resistant Staphylococcus aureus strains on competitive exclusion 
Journal of theoretical biology  2010;264(3):645-656.
We investigate the in-hospital transmission dynamics of two methicillin resistant Staphylococcus aureus (MRSA) strains: hospital-acquired methicillin resistant Staphylococcus aureus (HA-MRSA) and community-acquired methicillin resistant Staphylococcus aureus (CA-MRSA). Under the assumption that patients can only be colonized with one strain of MRSA at a time, global results show that competitive exclusion occurs between HA-MRSA and CA-MRSA strains; the strain with the larger basic reproduction ratio will become endemic while the other is extinguished. Because new studies suggest that patients can be concurrently colonized with multiple strains of MRSA, we extend the model to allow patients to be co-colonized with HA-MRSA and CA-MRSA. Using the extended model, we explore the effect of co-colonization on competitive exclusion by determining the invasion reproduction ratios of the boundary equilibria. In contrast to results derived from the assumption that co-colonization does not occur, the extended model rarely exhibits competitive exclusion. More commonly, both strains become endemic in the hospital. When transmission rates are assumed equal and decolonization measures act equally on all strains, competitive exclusion never occurs. Other interesting phenomena are exhibited. For example, solutions can tend toward a co-existence equilibrium, even when the basic reproduction ratio of one of the strains is less than one.
doi:10.1016/j.jtbi.2010.03.036
PMCID: PMC2874575  PMID: 20347850
population model; two-strain model; disease transmission; co-existence; co-infection
5.  Transmission of Methicillin-Resistant Staphylococcus aureus to Household Contacts▿  
Journal of Clinical Microbiology  2009;48(1):202-207.
The frequency of and risk factors for methicillin-resistant Staphylococcus aureus (MRSA) transmission from a MRSA index person to household contacts were assessed in this prospective study. Between January 2005 and December 2007, 62 newly diagnosed MRSA index persons (46 patients and 16 health care workers) and their 160 household contacts were included in the study analysis. Transmission of MRSA from an index person to household contacts occurred in nearly half of the cases (47%; n = 29). These 29 index persons together had 84 household contacts, of which two-thirds (67%; n = 56) became MRSA positive. Prolonged exposure time to MRSA at home was a significant risk factor for MRSA transmission to household contacts. In addition, MRSA colonization at least in the throat, younger age, and eczema in index persons were significantly associated with MRSA transmission; the presence of wounds was negatively associated with MRSA transmission. Furthermore, an increased number of household contacts and being the partner of a MRSA index person were household-related risk factors for MRSA acquisition from the index person. No predominant pulsed-field gel electrophoresis (PFGE) type was observed to be transmitted more frequently than other PFGE types. To date, screening household contacts and providing MRSA eradication therapy to those found positive simultaneously with the index person is not included in the “search-and-destroy” policy. We suggest including both in MRSA prevention guidelines, as this may reduce further spread of MRSA.
doi:10.1128/JCM.01499-09
PMCID: PMC2812253  PMID: 19923490
6.  Methicillin-Resistant Staphylococcus aureus Colonization and Risk of Subsequent Infection in Critically Ill Children: Importance of Preventing Nosocomial Methicillin-Resistant Staphylococcus aureus Transmission 
Methicillin-resistant Staphylococcus aureus (MRSA) colonization is a risk factor for infection in critically ill children. Almost half of children who acquired MRSA colonization in our ICU developed an MRSA infection during their hospitalization or after discharge, highlighting the importance of preventing nosocomial MRSA transmission.
Background. Methicillin-resistant Staphylococcus aureus (MRSA) colonization is a predictor of subsequent infection in hospitalized adults. The risk of subsequent MRSA infections in hospitalized children colonized with MRSA is unknown.
Methods. Children admitted to an academic medical center’s pediatric intensive care unit between March 2007 and March 2010 were included in the study. Anterior naris swabs were cultured to identify children with MRSA colonization at admission. Laboratory databases were queried and National Healthcare Safety Network definitions applied to identify patients with MRSA infections during their hospitalization or after discharge.
Results. The MRSA admission prevalence among 3140 children was 4.9%. Overall, 56 children (1.8%) developed an MRSA infection, including 13 (8.5%) colonized on admission and 43 (1.4%) not colonized on admission (relative risk [RR], 5.9; 95% confidence interval [CI], 3.4–10.1). Of those, 10 children (0.3%) developed an MRSA infection during their hospitalization, including 3 of 153 children (1.9%) colonized on admission and 7 of 2987 children (0.2%) not colonized on admission (RR, 8.4; 95% CI, 2.7–25.8). African-Americans and those with public health insurance were more likely to get a subsequent infection (P < .01 and P = .03, respectively). We found that 15 children acquired MRSA colonization in the pediatric intensive care unit, and 7 (47%) developed a subsequent MRSA infection.
Conclusions. MRSA colonization is a risk factor for subsequent MRSA infection in children. Although MRSA colonized children may have lower risks of subsequent infection than adults, children who acquire MRSA in the hospital have similarly high rates of infection. Preventing transmission of MRSA in hospitalized children should remain a priority.
doi:10.1093/cid/cir547
PMCID: PMC3189167  PMID: 21878424
7.  MRSA Transmission between Cows and Humans 
Emerging Infectious Diseases  2007;13(4):630-632.
We isolated methicillin-resistant Staphylococcus aureus (MRSA) from cows with subclinical mastitis and from a person who worked with these animals. The bovine and human strains were indistinguishable by phenotyping and genotyping methods and were of a low frequency spa type. To our knowledge, this finding indicates the first documented case of direct transmission of MRSA between cows and humans.
doi:10.3201/eid1304.060833
PMCID: PMC2725960  PMID: 17553285
Methicillin-resistant Staphylococcus aureus; cows; mastitis; zoonosis; phage types; PFGE; SCCmec type; spa-typing; MLST; dispatch; Suggested citation for this article: Juhász-Kaszanyitzky E; Jánosi S; Somogyi P; Dán A; van der Graaf-van Bloois L; van Duijkeren E; et al. MRSA transmission between cows and humans. Emerg Infect Dis [serial on the Internet]. 2007 Apr [date cited]. Available from http://www.cdc.gov/eid/content/13/4/630.htm
8.  High Prevalence of EMRSA-15 in Portuguese Public Buses: A Worrisome Finding 
PLoS ONE  2011;6(3):e17630.
Background
The nosocomial prevalence of methicillin resistant Staphylococcus aureus (MRSA) in Portugal remains one of the highest in Europe and is currently around 50%. Transmission of S. aureus, including MRSA, occurs principally by direct human-to-human skin contact. However, S. aureus can survive for long periods on inanimate objects, which may represent an important reservoir for dissemination as well.
Methodology/Principal Findings
Between May 2009 and February 2010, handrails of 85 public urban buses circulating in Oporto, Portugal, were screened for the occurrence of MRSA. Twenty-two (26%) buses showed MRSA contamination. The molecular characterization of a total of 55 MRSA, by pulsed-field gel electrophoresis (PFGE), staphylococcal cassette chromosome (SCC) mec typing, spa typing, and multilocus sequence typing (MLST), clustered the isolates into three clonal types. However, the overwhelming majority (n = 50; 91%) of the isolates belonged to a single clone (PFGE A, spa types t747, t032, t025 or t020, ST22, SCCmec type IVh) that exhibits the characteristics of the pandemic EMRSA-15, currently the major lineage circulating in Portuguese hospitals, namely in the Oporto region. Two additional clones were found but in much lower numbers: (i) PFGE B, ST5, spa type t002, SCCmec IVa (n = 3), and (ii) PFGE C, spa type t008, ST8, SCCmec IVa (n = 2). None of the 55 isolates was PVL positive.
Conclusions/Significance
Public buses in Oporto seem to be an important reservoir of MRSA of nosocomial origin, providing evidence that the major hospital-associated MRSA clone in Portugal is escaping from the primary ecological niche of hospitals to the community environment. Infection control measures are urgently warranted to limit the spread of EMRSA-15 to the general population and future studies are required to assess the eventual increase of MRSA in the Portuguese community, which so far remains low.
doi:10.1371/journal.pone.0017630
PMCID: PMC3047573  PMID: 21407807
9.  Frequency and Possible Infection Control Implications of Gastrointestinal Colonization with Methicillin-Resistant Staphylococcus aureus 
Journal of Clinical Microbiology  2005;43(12):5992-5995.
Methicillin-resistant Staphylococcus aureus (MRSA) is a major cause of health care-associated infections. Multiple factors, including transmission from unrecognized reservoirs of MRSA, are responsible for failure to control the spread of MRSA. We conducted prospective surveillance to determine the frequency of gastrointestinal colonization with MRSA among patients and its possible impact on nosocomial transmission of MRSA. Stool specimens submitted for Clostridium difficile toxin A/B assays were routinely inoculated on colistin-naladixic acid agar plates, and S. aureus was identified by using standard methods. Methicillin resistance was confirmed by growth on oxacillin-salt screening agar. For patients whose stool yielded MRSA, information regarding any previous cultures positive for MRSA or other organisms that would require contact precautions was obtained from the laboratory's computer system. During a 1-year period, 151 (9.8%) of 1,543 patients who had one or more stool specimens screened had MRSA in their stool. Ninety-three (62%) of the 151 patients had no previous history of MRSA colonization or infection. Of these 93, 75 were inpatients. Sixty (80%) of the 75 inpatients with no previous history of MRSA were not under “contact precautions.” The 60 patients would have spent an estimated total of 267 days without being placed under contact precautions if their positive stool cultures had not resulted in their being isolated. Placing patients under contact precautions based on their positive stool cultures prevented an estimated 35 episodes of MRSA transmission. We conclude that gastrointestinal colonization with MRSA may serve as an unrecognized reservoir from which transmission of MRSA may occur in health care facilities.
doi:10.1128/JCM.43.12.5992-5995.2005
PMCID: PMC1317179  PMID: 16333087
10.  Carriage of Methicillin-Resistant Staphylococcus aureus by Wild Urban Norway Rats (Rattus norvegicus) 
PLoS ONE  2014;9(2):e87983.
Methicillin-resistant Staphylococcus aureus (MRSA) is an important cause of multi-drug-resistant infections in people, particularly indigent populations. MRSA can be transmitted between people and domestic animals, but the potential for transmission between people and commensal pests, particularly rodents, had not been investigated. The objective of this study was to identify the presence and characterize the ecology of MRSA in rats (Rattus spp.) from in an impoverished, inner-city neighborhood. Oropharyngeal swabs were collected from rats trapped in 33 city blocks and one location within the adjacent port. Bacterial culture was performed and MRSA isolates were characterized using a variety of methods, including whole-genome sequencing (WGS). The ecology of MRSA in rats was described using phylogenetic analysis, geospatial analysis, and generalized linear mixed models. MRSA was identified 22 of 637 (3.5%) rats tested, although prevalence varied from 0 – 50% among blocks. Isolates belonged to 4 clusters according to WGS, with the largest cluster (n = 10) containing isolates that were genetically indistinguishable from community-acquired USA300 MRSA strains isolated from people within the study area. MRSA strains demonstrated both geographic clustering and dispersion. The odds of an individual rat carrying MRSA increased with increased body fat (OR = 2.53, 95% CI = 1.33 – 4.82), and in the winter (OR = 5.29, 95% CI = 1.04 – 26.85) and spring (OR = 5.50, 95% CI = 1.10 – 27.58) compared to the fall. The results show that urban rats carried the same MRSA lineages occurring in local human and/or animal populations, supporting recent transmission from external sources. MRSA carriage was influenced by season, most likely as a result of temporal variation in rat behavior and rat-human interactions.
doi:10.1371/journal.pone.0087983
PMCID: PMC3912160  PMID: 24498421
11.  Good Performance of the SpectraCellRA System for Typing of Methicillin-Resistant Staphylococcus aureus Isolates 
Journal of Clinical Microbiology  2013;51(5):1434-1438.
Typing of methicillin-resistant Staphylococcus aureus (MRSA) remains necessary in order to assess whether transmission of MRSA occurred and to what extent infection prevention measures need to be taken. Raman spectroscopy (SpectraCellRA [SCRA]; RiverD International, Rotterdam, The Netherlands) is a recently developed tool for bacterial typing. In this study, the performance (typeability, discriminatory power, reproducibility, workflow, and costs) of the SCRA system was evaluated for typing of MRSA strains isolated from patients and patients' household members who were infected with or colonized by MRSA. We analyzed a well-documented collection of 113 MRSA strains collected from 54 households. The epidemiological relationship between the MRSA strains within one household was used as the gold standard. Pulsed-field gel electrophoresis (PFGE) was used for discrepancy analysis. The results of SCRA analysis on the strain level corresponded with epidemiological data for 108 of 113 strains, a concordance of 95.6%. When analyzed at the household level, the results of SCRA were correct for 49 out of 54 households, a concordance of 90.7%. Concordance on the strain level with epidemiological data for PFGE was 93.6% (103/110 isolates typed). Concordance on the household level with epidemiological data for PFGE was 93.5% (49/53 households analyzed). With PFGE regarded as the reference standard, the conclusions reached with Raman spectroscopy were identical to those reached with PFGE in 100 of 105 cases (95.2%). The reproducibility of SCRA was found to be 100%. We conclude that the SpectraCellRA system is a fast, easy-to-use, and highly reproducible typing platform for outbreak analysis that can compete with the currently used typing techniques.
doi:10.1128/JCM.02101-12
PMCID: PMC3647921  PMID: 23426926
12.  MRSA Transmission on a Neonatal Intensive Care Unit: Epidemiological and Genome-Based Phylogenetic Analyses 
PLoS ONE  2013;8(1):e54898.
Background
Methicillin-resistant Staphylococcus aureus (MRSA) may cause prolonged outbreaks of infections in neonatal intensive care units (NICUs). While the specific factors favouring MRSA spread on neonatal wards are not well understood, colonized infants, their relatives, or health-care workers may all be sources for MRSA transmission. Whole-genome sequencing may provide a new tool for elucidating transmission pathways of MRSA at a local scale.
Methods and Findings
We applied whole-genome sequencing to trace MRSA spread in a NICU and performed a case-control study to identify risk factors for MRSA transmission. MRSA genomes had accumulated sequence variation sufficiently fast to reflect epidemiological linkage among individual patients, between infants and their mothers, and between infants and staff members, such that the relevance of individual nurses’ nasal MRSA colonization for prolonged transmission could be evaluated. In addition to confirming previously reported risk factors, we identified an increased risk of transmission from infants with as yet unknown MRSA colonisation, in contrast to known MRSA-positive infants.
Conclusions
The integration of epidemiological (temporal, spatial) and genomic data enabled the phylogenetic testing of several hypotheses on specific MRSA transmission routes within a neonatal intensive-care unit. The pronounced risk of transmission emanating from undetected MRSA carriers suggested that increasing the frequency or speed of microbiological diagnostics could help to reduce transmission of MRSA.
doi:10.1371/journal.pone.0054898
PMCID: PMC3561456  PMID: 23382995
13.  Microfluidic-Chip-Based Multiple-Locus Variable-Number Tandem-Repeat Fingerprinting with New Primer Sets for Methicillin-Resistant Staphylococcus aureus 
Journal of Clinical Microbiology  2012;50(7):2255-2262.
The detection of outbreaks of methicillin-resistant Staphylococcus aureus (MRSA) infections and a rapid and accurate identification of sources and routes of transmission should be conducted in hospital settings as early and swiftly as possible. In this study, we investigated the application potential of a new approach based on multiple-locus variable-number tandem-repeat fingerprinting (MLVF) and microfluidics technology for a rapid discrimination of MRSA lineages in outbreak settings. A total of 206 nonrepetitive MRSA isolates recovered from infected patients at the University Medical Center Groningen between 2000 and 2010 were tested. The results obtained by MLVF using microcapillary electrophoresis with newly designed primers were compared to those obtained by spa typing and multiple-locus variable-number tandem-repeat analysis (MLVA). The discriminatory power was 0.980 (107 patterns), 0.969 (85 allelic profiles), and 0.959 (66 types) for MLVF, MLVA, and spa typing, respectively. All methods tested showed a good concordance of results calculated by the adjusted Rand's coefficient method. Comparisons of data obtained by the three approaches allowed us to propose an 88% cutoff value for the similarity between any two MLVF patterns, which can be used in S. aureus epidemiological studies, including analyses of outbreaks and strain transmission events. Of the three tested methods, MLVF is the cheapest, fastest, and easiest to perform. MLVF applied to microfluidic polymer chips is a rapid, cheap, reproducible, and highly discriminating tool to determine the clonality of MRSA isolates and to trace the spread of MRSA strains over periods of many years. Although spa typing should be used due to its portability of data, MLVF has a high added value because it is more discriminatory.
doi:10.1128/JCM.00056-12
PMCID: PMC3405612  PMID: 22573591
14.  Longitudinal Study of the Molecular Epidemiology of Methicillin-Resistant Staphylococcus aureus at a University Hospital▿  
Journal of Clinical Microbiology  2006;44(12):4297-4302.
Surveillance for methicillin-resistant Staphylococcus aureus (MRSA) at the University Hospital of Heidelberg revealed an increase in the numbers of newly detected MRSA isolates in recent years. We conducted a study to assess the dynamics of the changes in the MRSA population. Pulsed-field gel electrophoresis (PFGE) typing of MRSA isolates from all patients at the University Hospital of Heidelberg collected between 1993 and 2004 was performed. The microbiology database contained 1,807 entries for newly detected MRSA isolates from 1,301 patients. A total of 1,252 isolates were available for PFGE typing. The isolates could be classified into 109 different PFGE types. Most PFGE types (n = 70) were detected less than five times and showed no evidence of transmission (sporadic strains). They accounted for 8.7% of all isolates, with few variations in frequency over the time. Thirty-seven PFGE types were clustered by time of detection, and transmission of the strains was likely (local epidemic strains). A total of 37.3% of the isolates belonged to this group of strains. The remaining 54.0% of the isolates belonged to only two further PFGE types (endemic strains). One endemic strain accounted for 5.0% of all isolates in 1994 and 68.2% in 2004. A second endemic strain was detected in 1.1% of all isolates in 1998 but in 12.4% in 2004. Statistical analysis of the associations between the kind of strain (sporadic, local epidemic, or endemic) and the patients' characteristics revealed a significant association for age and mode of acquisition. The remarkable increase in the rate of MRSA detection at the University Hospital of Heidelberg is mainly due to the dissemination of two different strains. Infection control measures seemed sufficient to prevent further transmission of some but not all of the strains.
doi:10.1128/JCM.01168-06
PMCID: PMC1698402  PMID: 17021064
15.  Transmission Dynamics of Methicillin-Resistant Staphylococcus aureus in Pigs 
From the mid-2000s on, numerous studies have shown that methicillin-resistant Staphylococcus aureus (MRSA), renowned as human pathogen, has a reservoir in pigs and other livestock. In Europe and North America, clonal complex (CC) 398 appears to be the predominant lineage involved. Especially worrisome is its capacity to contaminate humans in close contact with affected animals. Indeed, the typical multi-resistant phenotype of MRSA CC398 and its observed ability of easily acquiring genetic material suggests that MRSA CC398 strains with an increased virulence potential may emerge, for which few therapeutic options would remain. This questions the need to implement interventions to control the presence and spread of MRSA CC398 among pigs. MRSA CC398 shows a high but not fully understood transmission potential in the pig population and is able to persist within that population. Although direct contact is probably the main route for MRSA transmission between pigs, also environmental contamination, the presence of other livestock, the herd size, and farm management are factors that may be involved in the dissemination of MRSA CC398. The current review aims at summarizing the research that has so far been done on the transmission dynamics and risk factors for introduction and persistence of MRSA CC398 in farms.
doi:10.3389/fmicb.2013.00057
PMCID: PMC3602589  PMID: 23518663
MRSA; ST398; pigs; transmission risk factors; transmission routes; transmission pig models
16.  Cloning and Occurrence of czrC, a Gene Conferring Cadmium and Zinc Resistance in Methicillin-Resistant Staphylococcus aureus CC398 Isolates▿  
We recently reported a phenotypic association between reduced susceptibility to zinc and methicillin resistance in Staphylococcus aureus CC398 isolates from Danish swine (F. M. Aarestrup, L. M. Cavaco, and H. Hasman, Vet. Microbiol. 142:455-457, 2009). The aim of this study was to identify the genetic determinant causing zinc resistance in CC398 and examine its prevalence in isolates of animal and human origin. Based on the sequence of the staphylococcal cassette chromosome mec (SCCmec) element from methicillin-resistant S. aureus (MRSA) CC398 strain SO385, a putative metal resistance gene was identified in strain 171 and cloned in S. aureus RN4220. Furthermore, 81 MRSA and 48 methicillin-susceptible S. aureus (MSSA) strains, isolated from pigs (31 and 28) and from humans (50 and 20) in Denmark, were tested for susceptibility to zinc chloride and for the presence of a putative resistance determinant, czrC, by PCR. The cloning of czrC confirmed that the zinc chloride and cadmium acetate MICs for isogenic constructs carrying this gene were increased compared to those for S. aureus RN4220. No difference in susceptibility to sodium arsenate, copper sulfate, or silver nitrate was observed. Seventy-four percent (n = 23) of the animal isolates and 48% (n = 24) of the human MRSA isolates of CC398 were resistant to zinc chloride and positive for czrC. All 48 MSSA strains from both human and pig origins were found to be susceptible to zinc chloride and negative for czrC. Our findings showed that czrC is encoding zinc and cadmium resistance in CC398 MRSA isolates, and that it is widespread both in humans and animals. Thus, resistance to heavy metals such as zinc and cadmium may play a role in the coselection of methicillin resistance in S. aureus.
doi:10.1128/AAC.00058-10
PMCID: PMC2934997  PMID: 20585119
17.  Origin and Molecular Evolution of the Determinant of Methicillin Resistance in Staphylococci ▿  
Antimicrobial Agents and Chemotherapy  2010;54(10):4352-4359.
Methicillin-resistant Staphylococcus aureus (MRSA) is one of the most important multidrug-resistant pathogens around the world. MRSA is generated when methicillin-susceptible S. aureus (MSSA) exogenously acquires a methicillin resistance gene, mecA, carried by a mobile genetic element, staphylococcal cassette chromosome mec (SCCmec), which is speculated to be transmissible across staphylococcal species. However, the origin/reservoir of the mecA gene has remained unclear. Finding the origin/reservoir of the mecA gene is important for understanding the evolution of MRSA. Moreover, it may contribute to more effective control measures for MRSA. Here we report on one of the animal-related Staphylococcus species, S. fleurettii, as the highly probable origin of the mecA gene. The mecA gene of S. fleurettii was found on the chromosome linked with the essential genes for the growth of staphylococci and was not associated with SCCmec. The mecA locus of the S. fleurettii chromosome has a sequence practically identical to that of the mecA-containing region (∼12 kbp long) of SCCmec. Furthermore, by analyzing the corresponding gene loci (over 20 kbp in size) of S. sciuri and S. vitulinus, which evolved from a common ancestor with that of S. fleurettii, the speciation-related mecA gene homologues were identified, indicating that mecA of S. fleurettii descended from its ancestor and was not recently acquired. It is speculated that SCCmec came into form by adopting the S. fleurettii mecA gene and its surrounding chromosomal region. Our finding suggests that SCCmec was generated in Staphylococcus cells living in animals by acquiring the intrinsic mecA region of S. fleurettii, which is a commensal bacterium of animals.
doi:10.1128/AAC.00356-10
PMCID: PMC2944575  PMID: 20679504
18.  Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power 
Current opinion in microbiology  2007;10(5):428-435.
Summary
Nothing documents better the spectacular adaptive capacity of Staphylococcus aureus than the response of this important human and animal pathogen to the introduction of antimicrobial agents into the clinical environment. The effectiveness of penicillin introduced in the early 1940s was virtually annulled within a decade due to the plasmid epidemics that spread the ß-lactamase gene through the entire species of S. aureus. In 1960 within one to two years of the introduction of penicillinase resistant ß-lactams (methicillin), methicillin resistant S. aureus (MRSA) strains were identified in clinical specimens. By the 1980s, epidemic clones of MRSA acquired multidrug resistant traits and spread worldwide to become one of the most important causative agents of hospital acquired infections. In the early 2000s, MRSA strains carrying the Tn1546 transposon-based enterococcal vancomycin resistant mechanism were identified in clinical specimens, bringing the specter of a totally resistant bacterial pathogen closer to reality. Then, in the late 1990s, just as effective hygienic and antibiotic use policies managed to bring down the frequency of MRSA in hospitals of several countries, MRSA strains began to show up in the community.
doi:10.1016/j.mib.2007.08.003
PMCID: PMC2701899  PMID: 17921044
19.  Environmental Methicillin-Resistant Staphylococcus aureus in a Veterinary Teaching Hospital During a Nonoutbreak Period 
Abstract
Concurrent to reports of zoonotic and nosocomial transmission of methicillin-resistant Staphylococcus aureus (MRSA) in veterinary settings, recent evidence indicates that the environment in veterinary hospitals may be a potential source of MRSA. The present report is a cross-sectional study to determine the prevalence of MRSA on specific human and animal contact surfaces at a large veterinary hospital during a nonoutbreak period. A total of 156 samples were collected using Swiffers® or premoistened swabs from the small animal, equine, and food animal sections. MRSA was isolated and identified by pre-enrichment culture and standard microbiology procedures, including growth on Mueller-Hinton agar supplemented with NaCl and oxacillin, and by detection of the mecA gene. Staphylococcal chromosome cassette mec (SCCmec) typing and pulsed-field gel electrophoresis profile were also determined. MRSA was detected in 12% (19/157) of the hospital environments sampled. The prevalence of MRSA in the small animal, equine, and food animal areas were 16%, 4%, and 0%, respectively. Sixteen of the MRSA isolates from the small animal section were classified as USA100, SCCmec type II, two of which had pulsed-field gel electrophoresis pattern that does not conform to any known type. The one isolate obtained from the equine section was classified as USA500, SCCmec type IV. The molecular epidemiological analysis revealed a very diverse population of MRSA isolates circulating in the hospital; however, in some instances, multiple locations/surfaces, not directly associated, had the same MRSA clone. No significant difference was observed between animal and human contact surfaces in regard to prevalence and type of isolates. Surfaces touched by multiple people (doors) and patients (carts) were frequently contaminated with MRSA. The results from this study indicate that MRSA is present in the environment even during nonoutbreak periods. This study also identified specific surfaces in a veterinary environment that need to be targeted when designing and executing infection control programs.
doi:10.1089/vbz.2010.0181
PMCID: PMC3391706  PMID: 21417926
environment; MRSA; nosocomial; veterinary hospital
20.  Community-associated Methicillin-Resistant Staphylococcus aureus in Outpatients, United States, 1999–2006 
Emerging Infectious Diseases  2009;15(12):1925-1930.
These patients likely play a role in transmission of these organisms into hospitals.
Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) has become a major problem in US hospitals already dealing with high levels of hospital-associated MRSA (HA-MRSA). Using antimicrobial drug susceptibility data for 1999–2006 from The Surveillance Network, we characterized the relationship between outpatient and inpatient levels of CA-MRSA nationally. In outpatients, the frequency of CA-MRSA isolates has increased >7× during 1999–2006, which suggests that outpatients have become a major reservoir for CA-MRSA. However, contrary to results in other reports, although CA-MRSA increases are associated with decreases in the frequency of HA-MRSA in hospitals, the decreases are only modest. This finding suggests that instead of replacing HA-MRSA in the hospital, CA-MRSA is adding to the overall presence of MRSA already found within the hospital population.
doi:10.3201/eid1512.081341
PMCID: PMC3044510  PMID: 19961671
Methicillin-resistant Staphylococcus aureus; community-associated MRSA; hospital-associated MRSA; phenotypic susceptibility; outpatients; staphylococci; bacteria; CME; research
21.  Bench-to-bedside review: Understanding the impact of resistance and virulence factors on methicillin-resistant Staphylococcus aureus infections in the intensive care unit 
Critical Care  2009;13(5):222.
Methicillin-resistant Staphylococcus aureus (MRSA) displays a remarkable array of resistance and virulence factors, which have contributed to its prominent role in infections of the critically ill. We are beginning to understand the function and regulation of some of these factors and efforts are ongoing to better characterize the complex interplay between the microorganism and host response. It is important that clinicians recognize the changing resistance patterns and epidemiology of Staphylococcus spp., as these factors may impact patient outcomes. Community-associated MRSA clones have emerged as an increasingly important subset of Staphyloccocus aureus and MRSA can no longer be considered as solely a nosocomial pathogen. When initiating empiric antibiotics, it is of vital importance that this therapy be timely and appropriate, as delays in treatment are associated with adverse outcomes. Although vancomycin has long been considered a first-line therapy for serious MRSA infections, multiple concerns with this agent have opened the door for existing and investigational agents demonstrating efficacy in this role.
doi:10.1186/cc8028
PMCID: PMC2784352  PMID: 19889197
22.  mecA Gene Is Widely Disseminated in Staphylococcus aureus Population 
Journal of Clinical Microbiology  2002;40(11):3970-3975.
Methicillin-resistant Staphylococcus aureus (MRSA) is one of the most important causes of hospital infections worldwide. High-level resistance to methicillin is caused by the mecA gene, which encodes an alternative penicillin-binding protein, PBP 2a. To determine the clonal relationships between methicillin-susceptible S. aureus (MSSA) and MRSA, we typed 1,069 S. aureus isolates (493 MSSA isolates and 576 MRSA isolates), collected mainly in North American and European hospitals between the 1960s and the year 2000, using pulsed-field gel electrophoresis and ribotyping. Of 10 widespread S. aureus lineages recognized, 8 had corresponding mecA-positive strains. Multiresistant MRSA strains are found in hospitals worldwide, while unrelated and more susceptible strains represent less than 1% of the MRSA population. This supports the hypothesis that horizontal transfer plays an important role in the dissemination of the mecA gene in the S. aureus population.
doi:10.1128/JCM.40.11.3970-3975.2002
PMCID: PMC139644  PMID: 12409360
23.  Potential Role of Pet Animals in Household Transmission of Methicillin-Resistant Staphylococcus aureus: A Narrative Review 
Abstract
In this narrative review, we found numerous reports suggesting that dogs and cats may play a role in household methicillin-resistant Staphylococcus aureus (MRSA) transmission and recurrent MRSA infection in human contacts. Future work should emphasize elucidating more clearly the prevalence of MRSA in household pets and characterize transmission dynamics of MRSA humans and pet animals.
doi:10.1089/vbz.2010.0025
PMCID: PMC3115421  PMID: 21142959
Cats; Dogs; Household; MRSA; Pet animals; Transmission
24.  Rapid Emergence of Co-colonization with Community-acquired and Hospital-Acquired Methicillin-Resistant Staphylococcus aureus Strains in the Hospital Setting 
Background
Community-acquired methicillin-resistant Staphylococcus aureus (CA- MRSA), a novel strain of MRSA, has recently emerged and rapidly spread in the community. Invasion into the hospital setting with replacement of the hospital-acquired MRSA (HA-MRSA) has also been documented. Co-colonization with both CA-MRSA and HA-MRSA would have important clinical implications given differences in antimicrobial susceptibility profiles and the potential for exchange of genetic information.
Methods
A deterministic mathematical model was developed to characterize the transmission dynamics of HA-MRSA and CA-MRSA in the hospital setting and to quantify the emergence of co-colonization with both strains
Results
The model analysis shows that the state of co-colonization becomes endemic over time and that typically there is no competitive exclusion of either strain. Increasing the length of stay or rate of hospital entry among patients colonized with CA-MRSA leads to a rapid increase in the co-colonized state. Compared to MRSA decolonization strategy, improving hand hygiene compliance has the greatest impact on decreasing the prevalence of HA-MRSA, CA-MRSA and the co-colonized state.
Conclusions
The model predicts that with the expanding community reservoir of CA-MRSA, the majority of hospitalized patients will become colonized with both CA-MRSA and HA-MRSA.
doi:10.1051/mmnp/20105306
PMCID: PMC2927146  PMID: 20740067
methicillin resistance; Staphylococcus aureus; community; hospital; co-colonization
25.  Community-Associated Methicillin-Resistant Staphylococcus aureus in the Pediatric Population 
PURPOSE
To review the epidemiology and prevalence of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA), define the differences between community-acquired and hospital-acquired strains, highlight the advantages and disadvantages of antibiotics commonly used to treat infections caused by this pathogen, and identify strategies to limit the spread of this organism and prevent future outbreaks.
DATA
Literature was accessed through MEDLINE using the search terms community-acquired methicillin-resistant Staphylococcus aureus, community-associated methicillin-resistant Staphylococcus aureus, CA-MRSA, pediatrics, and children. Articles evaluated were published in the English language and limited to human studies. References of literature identified by initial search techniques were reviewed for additional relevant articles.
DATA SYNTHESIS
Community-associated methicillin-resistant Staphylococcus aureus has become a prominent pathogen in pediatric patients in the last ten years. Its increasing prevalence has been reported throughout the United States, and it is the cause of over one half of all skin and soft tissue infections seen in many hospitals and emergency departments. The risk factors for infection with this pathogen differ from those associated with hospital-acquired strains. Mild to moderate infections can generally be treated with oral antibiotics, while more serious infections may require parenteral therapy. Sulfamethoxazole/trimethoprim and clindamycin are the preferred oral agents due to their efficacy, tolerability, well established side effect profiles, and cost. Vancomycin is the standard of care for parenteral therapy, although clindamycin is an acceptable parenteral alternative. More costly agents such as linezolid, daptomycin, and quinupristin/dalfopristin should be reserved for patients with severe infections, multiple allergies, or in strains with unusual resistance patterns. The best way to prevent and control outbreaks is to maintain standard infection control procedures including excellent hand hygiene.
CONCLUSIONS
CA-MRSA is a serious and frequently seen pathogen. Proper antibiotic selection that takes into account patient factors, disease severity, ease of administration, and cost is necessary to maximize favorable patient outcomes.
doi:10.5863/1551-6776-13.4.212
PMCID: PMC3461986  PMID: 23055880
CA-MRSA; children; community-acquired methicillin-resistant Staphylococcus aureus; community-associated methicillin-resistant Staphylococcus aureus; pediatrics

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