Epidemiology, Virulence Factors and Antimicrobial Resistance in Staphylococcus aureus

A special issue of Antibiotics (ISSN 2079-6382). This special issue belongs to the section "Mechanism and Evolution of Antibiotic Resistance".

Deadline for manuscript submissions: 30 June 2024 | Viewed by 15060

Special Issue Editor

Department of Chemical and Biological Sciences, Institute of Biosciences, São Paulo State University (Unesp), Botucatu, SP, Brazil
Interests: Staphylococcus aureus; coagulase-negative staphylococci; antibiotic resistance; virulence factors; biofilm; molecular epidemiology
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Special Issue Information

Dear Colleagues,

Methicillin-resistant Staphylococcus aureus (MRSA) is a leading cause of healthcare-associated (HA-MRSA) infections, and its prevalence is also increasing in community-associated (CA-MRSA) infections. In addition to resistance to beta-lactams, S. aureus has shown resistance to other classes of antimicrobials, especially the glycopeptide vancomycin, a drug considered as the main alternative in the treatment of infections by MRSA. Currently, newly developed drugs can treat these resistant staphylococci, but there are already reports of reduced sensitivity to them. The variety of S. aureus species causing infections is largely due to the wide variety of virulence factors encoded by these bacteria, including toxins (hemolysins, leukocidins and superantigens), antiphagocytic factors (capsule and protein A) and enzymes associated with obtaining energy and disseminating the microorganism in the host (proteases, nucleases, hyaluronidase, lipases and collagenases), which favors the invasion of different tissues and evasion of the host's immune system. S. aureus infections may also be associated with biofilm formation, which facilitates the adherence of the microorganism to biotic or abiotic surfaces and provides protection against host defense mechanisms and antimicrobial action. Genetically diverse, the epidemiology of MRSA is primarily characterized by the serial emergence of epidemic strains. Although its incidence has recently declined in some regions, MRSA still poses a formidable clinical threat, with persistently high morbidity and mortality. The constant monitoring of these profiles of resistance to antimicrobials and antiseptics, as well as the knowledge of the prevalent and circulating clonal profiles in hospitals, is extremely important for the direction of empirical therapies. In addition to this, the increased use of antimicrobial agents during the COVID-19 pandemic, due to the need to implement mechanical ventilation and the use of invasive medical devices in some patients affected by SARS-COV-2, may intensify the selective pressure on microorganisms present in hospital environments, impacting the emergence of multi-resistant S. aureus. Successful treatment remains challenging and requires the evaluation of both novel antimicrobials and adjunctive aspects of care and source control. This Special Issue seeks manuscript submissions that further our understanding of basic and clinical S. aureus research about epidemiology, transmission, genetic diversity, evolution, virulence factors, surveillance and treatment.

Prof. Dr. Maria de Lourdes R.S. Cunha
Guest Editor

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Keywords

  • MRSA
  • HA-MRSA
  • CA-MRSA
  • VISA
  • Staphylococcus aureus
  • antimicrobial resistance
  • epidemiology
  • surveillance
  • virulence factors
  • genomics

Published Papers (8 papers)

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Research

11 pages, 1140 KiB  
Article
In Vivo-Acquired Resistance to Daptomycin during Methicillin-Resistant Staphylococcus aureus Bacteremia
by Adeline Boutet-Dubois, Chloé Magnan, Alexi Lienard, Cassandra Pouget, Flavien Bouchet, Hélène Marchandin, Romaric Larcher, Jean-Philippe Lavigne and Alix Pantel
Antibiotics 2023, 12(12), 1647; https://doi.org/10.3390/antibiotics12121647 - 22 Nov 2023
Viewed by 1237
Abstract
Daptomycin (DAP) represents an interesting alternative to treat methicillin-resistant Staphylococcus aureus (MRSA) infections. Different mechanisms of DAP resistance have been described; however, in vivo-acquired resistance is uncharacterized. This study described the phenotypic and genotypic evolution of MRSA strains that became resistant to DAP [...] Read more.
Daptomycin (DAP) represents an interesting alternative to treat methicillin-resistant Staphylococcus aureus (MRSA) infections. Different mechanisms of DAP resistance have been described; however, in vivo-acquired resistance is uncharacterized. This study described the phenotypic and genotypic evolution of MRSA strains that became resistant to DAP in two unrelated patients with bacteremia under DAP treatment, in two hospitals in the South of France. DAP MICs were determined using broth microdilution method on the pairs of isogenic (DAP-S/DAP-R) S. aureus isolated from bloodstream cultures. Whole genome sequencing was carried out using Illumina MiSeq Sequencing system. The two cases revealed DAP-R acquisition by MRSA strains within three weeks in patients treated by DAP. The isolates belonged to the widespread ST5 (patient A) and ST8 (patient B) lineages and were of spa-type t777 and t622, respectively. SNP analysis comparing each DAP-S/DAP-R pair confirmed that the isolates were isogenic. The causative mutations were identified in MprF (Multiple peptide resistance Factor) protein: L826F (Patient A) and S295L (Patient B), and in Cls protein: R228H (Patient B). These proteins encoded both proteins of the lipid biosynthetic enzymes. The resistance to DAP is particularly poorly described whereas DAP is highly prescribed to treat MRSA. Our study highlights the non-systematic cross-resistance between DAP and glycopeptides and the importance of monitoring DAP MIC in persistent MRSA bacteremia. Full article
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11 pages, 1735 KiB  
Article
The Diversity and Zoonotic Potential of Staphylococcus pseudintermedius in Humans and Pet Dogs in Trinidad and Tobago
by Sharianne Suepaul, Marc Stegger, Filip Boyen, Karla Georges and Patrick Butaye
Antibiotics 2023, 12(8), 1266; https://doi.org/10.3390/antibiotics12081266 - 31 Jul 2023
Viewed by 879
Abstract
Staphylococcus pseudintermedius is an opportunistic pathogen that is frequently isolated from canines. It is of escalating interest because of its increasing antimicrobial resistance and zoonotic potential. Although many published articles are available that describe isolates obtained from diseased dogs and humans, this study [...] Read more.
Staphylococcus pseudintermedius is an opportunistic pathogen that is frequently isolated from canines. It is of escalating interest because of its increasing antimicrobial resistance and zoonotic potential. Although many published articles are available that describe isolates obtained from diseased dogs and humans, this study focused on isolates obtained from healthy dogs and their owners who presented at clinics for routine veterinary care and utilized whole genome sequencing-based analyses for strain comparisons. A total of 25 humans and 27 canines were sampled at multiple sites, yielding 47 and 45 isolates, respectively. Whole genome sequence analysis was performed. We detected mostly new sequence types (STs) and a high diversity. Strains carried few antimicrobial resistance genes and plasmids, albeit three MRSP strains were found that belonged to two internationally distributed STs. The virulence content did not provide insights toward a tendency to colonization of humans but supported that there may be differences in the surface proteins between carrier strains and those causing pyoderma. We identified 13 cases in which humans were infected with strains from the dog they owned. Full article
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16 pages, 1211 KiB  
Article
Methicillin-Resistant Staphylococcus aureus Strains Isolated from Burned Patients in a Tunisian Hospital: Molecular Typing, Virulence Genes, and Antimicrobial Resistance
by Souhir Kmiha, Ahlem Jouini, Nahawend Zerriaa, Safa Hamrouni, Lamia Thabet and Abderrazak Maaroufi
Antibiotics 2023, 12(6), 1030; https://doi.org/10.3390/antibiotics12061030 - 08 Jun 2023
Cited by 1 | Viewed by 1532
Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) is one of the major causes of a variety of infections in hospitals and the community. Their spread poses a serious public health problem worldwide. Nevertheless, in Tunisia and other African countries, very little molecular typing data on MRSA [...] Read more.
Methicillin-resistant Staphylococcus aureus (MRSA) is one of the major causes of a variety of infections in hospitals and the community. Their spread poses a serious public health problem worldwide. Nevertheless, in Tunisia and other African countries, very little molecular typing data on MRSA strains is currently available. In our study, a total of 64 MRSA isolates were isolated from clinical samples collected from burned patients hospitalized in the Traumatology and Burns Center of Ben Arous in Tunisia. The identification of the collection was based on conventional methods (phenotypic and molecular characterization). The characterization of the genetic support for methicillin resistance was performed by amplification of the mecA gene by polymerase chain reaction (PCR), which revealed that 78.12% of S. aureus harbors the gene. The resistance of all the collection to different antibiotic families was studied. Indeed, the analysis of strain antibiotic susceptibility confirmed their multi-resistant phenotype, with high resistance to ciprofloxacin, gentamicin, penicillin, erythromycin, and tetracycline. The resistance to the last three antibiotics was conferred by the blaZ gene (73.43%), the erm(C) gene (1.56%), the msr(A) gene (6.25%), and tet(M) gene (7.81%), respectively. The clonal diversity of these strains was studied by molecular typing of the accessory gene regulator (agr) system, characterization of the SCCmec type, and spa-typing. The results revealed the prevalence of agr types II and III groups, the SCCmec type III and II cassettes, and the dominance of spa type t233. The characterization of the eight enterotoxins genes, the Panton-Valentine leukocidin and the toxic shock syndrome toxin, was determined by PCR. The percentage of virulence genes detected was for enterotoxins (55%), tst (71.88%), leukocidin E/D (79.69%), and pvl (1.56%) factors. Furthermore, our results revealed that the majority of the strains harbor IEC complex genes (94%) with different types. Our findings highlighted the emergence of MRSA strains with a wide variety of toxins, leukocidin associated with resistance genes, and specific genetic determinants, which could constitute a risk of their spread in hospitals and the environment and complicate infection treatment. Full article
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12 pages, 1999 KiB  
Article
Antimicrobial Resistance of Staphylococcus aureus Isolated between 2017 and 2022 from Infections at a Tertiary Care Hospital in Romania
by Daniela Tălăpan, Andreea-Mihaela Sandu and Alexandru Rafila
Antibiotics 2023, 12(6), 974; https://doi.org/10.3390/antibiotics12060974 - 28 May 2023
Cited by 4 | Viewed by 3124
Abstract
This study aimed to evaluate the frequency of isolation of Staphylococcus aureus from different pathological samples processed in the Microbiology Laboratory of the National Institute of Infectious Diseases “Prof. Dr. Matei Balș”, Romania, between 1 January 2017 and 31 December 2022, aiming to [...] Read more.
This study aimed to evaluate the frequency of isolation of Staphylococcus aureus from different pathological samples processed in the Microbiology Laboratory of the National Institute of Infectious Diseases “Prof. Dr. Matei Balș”, Romania, between 1 January 2017 and 31 December 2022, aiming to establish the ratio of methicillin-resistant to methicillin-susceptible Staphylococcus aureus strains and the antibiotic resistance pattern of isolated microorganisms. The data of isolates originating from routine diagnostic tasks were analyzed retrospectively using laboratory data from the microbiology department. Up to 39.11% of Staphylococcus aureus strains were resistant to oxacillin (MRSA), with 49.97% resistance to erythromycin and 36.06% inducible resistance to clindamycin. Resistance rates to ciprofloxacin, rifampicin, gentamicin, and trimethoprim-sulfamethoxazole were 9.98%, 5.38%, 5.95%, and 0.96%, respectively. There was no resistance to vancomycin. Between 2017 and 2022, the percentage of MRSA strains decreased from 41.71% to 33.63%, sharply increasing to 42.42% in 2021 (the year of the COVID-19 pandemic, when the percentage of strains isolated from lower respiratory tract infections was higher than that of strains isolated from wounds or blood, as in previous years). This study showed a high percentage of MRSA strains (39.11% overall) with a higher proportion of these strains isolated from the blood (42.49%) compared to other clinical specimens. Full article
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14 pages, 1288 KiB  
Article
Staphylococcus aureus and CA-MRSA Carriage among Brazilian Indians Living in Peri-Urban Areas and Remote Communities
by Lígia Maria Abraão, Carlos Magno Castelo Branco Fortaleza, Carlos Henrique Camargo, Thaís Alves Barbosa, Eliane Patrícia Lino Pereira-Franchi, Danilo Flávio Moraes Riboli, Luiza Hubinger, Mariana Fávero Bonesso, Rodrigo Medeiros de Souza and Maria de Lourdes Ribeiro de Souza da Cunha
Antibiotics 2023, 12(5), 862; https://doi.org/10.3390/antibiotics12050862 - 06 May 2023
Viewed by 1228
Abstract
The emergence of Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections among indigenous populations has been reported. Usually, indigenous communities live in extreme poverty and are at risk of acquiring infections. In Brazil, healthcare inequality is observed in this population. To date, there are no [...] Read more.
The emergence of Community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) infections among indigenous populations has been reported. Usually, indigenous communities live in extreme poverty and are at risk of acquiring infections. In Brazil, healthcare inequality is observed in this population. To date, there are no reports of CA-MRSA infections, and no active search for asymptomatic S. aureus carriage has been conducted among Brazilian Indians. The aim of this study was to investigate the prevalence of colonization with S. aureus and CA-MRSA among Brazilian Indians. We screened 400 Indians (from near urban areas and remote hamlets) for S. aureus and CA-MRSA colonization. The isolates were submitted to clonal profiling by pulsed-field gel electrophoresis (PFGE), and selected isolates were submitted to multilocus sequence typing (MLST). Among 931 specimens (nasal and oral) from different indigenous individuals in remote hamlets, S. aureus was cultured in 190 (47.6%). Furthermore, CA-MRSA was found in three isolates (0.7%), all SCCmec type IV. PFGE analysis identified 21 clusters among the S. aureus isolates, and MLST analysis showed a predominance of sequence type 5 among these isolates. Our study revealed a higher prevalence of S. aureus carriage among Shanenawa ethnicity individuals (41.1%). Therefore, ethnicity appears to be associated with the prevalence of S. aureus in these populations. Full article
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14 pages, 640 KiB  
Article
Multi-Drug Resistant Staphylococcus aureus Carriage in Abattoir Workers in Busia, Kenya
by Benear Apollo Obanda, Cheryl L. Gibbons, Eric M. Fèvre, Lilly Bebora, George Gitao, William Ogara, Shu-Hua Wang, Wondwossen Gebreyes, Ronald Ngetich, Beth Blane, Francesc Coll, Ewan M. Harrison, Samuel Kariuki, Sharon J. Peacock and Elizabeth A. J. Cook
Antibiotics 2022, 11(12), 1726; https://doi.org/10.3390/antibiotics11121726 - 01 Dec 2022
Cited by 2 | Viewed by 2595
Abstract
Abattoir workers have been identified as high-risk for livestock-associated Staphylococcus aureus carriage. This study investigated S. aureus carriage in abattoir workers in Western Kenya. Nasal swabs were collected once from participants between February-November 2012. S. aureus was isolated using bacterial culture and antibiotic [...] Read more.
Abattoir workers have been identified as high-risk for livestock-associated Staphylococcus aureus carriage. This study investigated S. aureus carriage in abattoir workers in Western Kenya. Nasal swabs were collected once from participants between February-November 2012. S. aureus was isolated using bacterial culture and antibiotic susceptibility testing performed using the VITEK 2 instrument and disc diffusion methods. Isolates underwent whole genome sequencing and Multi Locus Sequence Types were derived from these data. S. aureus (n = 126) was isolated from 118/737 (16.0%) participants. Carriage was higher in HIV-positive (24/89, 27.0%) than HIV–negative participants (94/648, 14.5%; p = 0.003). There were 23 sequence types (STs) identified, and half of the isolates were ST152 (34.1%) or ST8 (15.1%). Many isolates carried the Panton-Valentine leucocidin toxin gene (42.9%). Only three isolates were methicillin resistant S. aureus (MRSA) (3/126, 2.4%) and the prevalence of MRSA carriage was 0.4% (3/737). All MRSA were ST88. Isolates from HIV-positive participants (37.0%) were more frequently resistant to sulfamethoxazole/trimethoprim compared to isolates from HIV-negative participants (6.1%; p < 0.001). Similarly, trimethoprim resistance genes were more frequently detected in isolates from HIV-positive (81.5%) compared to HIV-negative participants (60.6%; p = 0.044). S. aureus in abattoir workers were representative of major sequence types in Africa, with a high proportion being toxigenic isolates. HIV-positive individuals were more frequently colonized by antimicrobial resistant S. aureus which may be explained by prophylactic antimicrobial use. Full article
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16 pages, 2410 KiB  
Article
Molecular Epidemiology of Staphylococcus aureus and MRSA in Bedridden Patients and Residents of Long-Term Care Facilities
by Lucas Porangaba Silva, Carlos Magno Castelo Branco Fortaleza, Nathalia Bibiana Teixeira, Luís Thadeo Poianas Silva, Carolina Destro de Angelis and Maria de Lourdes Ribeiro de Souza da Cunha
Antibiotics 2022, 11(11), 1526; https://doi.org/10.3390/antibiotics11111526 - 01 Nov 2022
Cited by 3 | Viewed by 1817
Abstract
At present, multidrug-resistant microorganisms are already responsible for community-acquired infections. Methicillin-resistant Staphylococcus aureus (MRSA) poses a serious public health risk worldwide because of the rapid spread and diversification of pandemic clones that are characterized by increasing virulence and antimicrobial resistance. The aim of [...] Read more.
At present, multidrug-resistant microorganisms are already responsible for community-acquired infections. Methicillin-resistant Staphylococcus aureus (MRSA) poses a serious public health risk worldwide because of the rapid spread and diversification of pandemic clones that are characterized by increasing virulence and antimicrobial resistance. The aim of this study was to identify the prevalence and factors associated with nasal, oral and rectal carriage of S. aureus and MRSA in bedridden patients and residents of long-term care facilities for the elderly (LTCFs) in Botucatu, SP, Brazil. Nasal, oral and rectal swab isolates obtained from 226 LTCF residents or home-bedridden patients between 2017 and 2018 were submitted to susceptibility testing, detection of the mecA gene, SCCmec characterization, and molecular typing by pulsed-field gel electrophoresis (PFGE) and multilocus sequence typing (MLST). Logistic regression analysis was used to identify risk factors associated with the presence of S. aureus and MRSA. The prevalence of S. aureus and MRSA was 33.6% (n = 76) and 8% (n = 18), respectively. At the nine LTCFs studied, the prevalence of S. aureus ranged from 16.6% to 85.7% and that of MRSA from 13.3% to 25%. Living in an LTCF, male gender, a history of surgeries, and a high Charlson Comorbidity Index score were risk factors associated with S. aureus carriage, while MRSA carriage was positively associated with male gender. This study showed a high prevalence of S. aureus among elderly residents of small (<15 residents) and medium-sized (15–49 residents) LTCFs and a higher prevalence of MRSA in the oropharynx. Full article
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8 pages, 289 KiB  
Article
Phenotypic and Genotypic Characterization of Macrolide, Lincosamide and Streptogramin B Resistance among Clinical Methicillin-Resistant Staphylococcus aureus Isolates in Chile
by Mario Quezada-Aguiluz, Alejandro Aguayo-Reyes, Cinthia Carrasco, Daniela Mejías, Pamela Saavedra, Sergio Mella-Montecinos, Andrés Opazo-Capurro, Helia Bello-Toledo, José M. Munita, Juan C. Hormazábal and Gerardo González-Rocha
Antibiotics 2022, 11(8), 1000; https://doi.org/10.3390/antibiotics11081000 - 25 Jul 2022
Cited by 4 | Viewed by 1783
Abstract
Macrolides, lincosamides, and type B streptogramins (MLSB) are important therapeutic options to treat methicillin-resistant Staphylococcus aureus (MRSA) infections; however, resistance to these antibiotics has been emerging. In Chile, data on the MLSB resistance phenotypes are scarce in both community-(CA) and [...] Read more.
Macrolides, lincosamides, and type B streptogramins (MLSB) are important therapeutic options to treat methicillin-resistant Staphylococcus aureus (MRSA) infections; however, resistance to these antibiotics has been emerging. In Chile, data on the MLSB resistance phenotypes are scarce in both community-(CA) and hospital-acquired (HA) MRSA isolates. Antimicrobial susceptibility to MLSB was determined for sixty-eight non-repetitive isolates of each HA-(32) and CA-MRSA (36). Detection of SCCmec elements, ermA, ermB, ermC, and msrA genes was performed by PCR. The predominant clones were SCCmec I-ST5 (HA-MRSA) and type IVc-ST8 (CA-MRSA). Most of the HA-MRSA isolates (97%) showed resistance to clindamycin, erythromycin, azithromycin, and clarithromycin. Among CA-MRSA isolates, 28% were resistant to erythromycin, azithromycin, and 25% to clarithromycin. All isolates were susceptible to linezolid, vancomycin, daptomycin and trimethoprim/sulfamethoxazole, and over 97% to rifampicin. The ermA gene was amplified in 88% of HA-MRSA and 17% of CA-MRSA isolates (p < 0.001). The ermC gene was detected in 6% of HA-SARM and none of CA-SARM isolates, whereas the msrA gene was only amplified in 22% of CA-MRSA (p < 0.005). Our results demonstrate the prevalence of the cMLSB resistance phenotype in all HA-MRSA isolates in Chile, with the ermA being the predominant gene identified among these isolates. Full article
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