Methicillin-Resistant Staphylococci and Macrococci at the Interface of Human and Animal Health

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Bacterial Toxins".

Deadline for manuscript submissions: closed (30 September 2020) | Viewed by 31764

Special Issue Editor


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Guest Editor
Friedrich Loeffler-Institute of Medical Microbiology, University Medicine Greifswald, 17475 Greifswald, Germany
Interests: staphylococci; pathogens; microbiota; epidemiology; multi-drug resistance; one health aspects
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Special Issue Information

Dear Colleagues,

The global importance of methicillin-resistant Staphylococcus aureus (MRSA) strains on human and animal health continues, even considering decreasing MRSA rates in some parts of the world. Subsequent to the emergence of hospital- and community-associated MRSA, livestock-associated MRSA and MSSA of different clonal lineages became an additional threat for human and animal health contributing significantly to morbidity, mortality and socio-economic costs.

However, many aspects of their genetic basis, origin, distribution, transmission, virulence profile and introduction into the health care systems are still poorly understood. The enormous diversity of the SCCmec as mobile genetic element harboring the methicillin resistance-encoding genes and other genes mediating resistances towards antibiotics, heavy metals and metalloids reflects the flexibility of staphylococci and their relatives, the macrococci, to resist the selection pressures occurring in their environment. The recent expansion of the mec “alphabet” by the detection of the mecC, mecB and mecD genes as well as the identification of plasmid-borne methicillin resistance in macrococci and staphylococci is additionally challenging the routine diagnostics as well as epidemiological studies. Moreover, the impact of coagulase-negative staphylococci and coagulase-positive non-S. aureus species as well as the role of macrococci as source for methicillin resistance-encoding genetic elements in S. aureus are only scantily investigated. Also widely unknown is the impact of virulence factors, in particular toxins, on the adaptation of Staphylococcaceae members to novel hosts and/or ecosystems.

Focusing on toxins and methicillin resistance in staphylococci and macrococci, this special issue aims to characterize basic, epidemiological, ecological and medical aspects on the interface between animal keeping, wildlife and putative other niches on one hand and the human and animal health on the other. In particular, submissions, which specifically address the One World – One Health concept in this field, are welcome.

Prof. Dr. Karsten Becker
Guest Editor

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Keywords

  • Toxins
  • Methicillin resistance
  • Oxacillin resistance
  • Betalactam resistance
  • Staphylococcus
  • Macrococcus
  • One Health
  • Husbandry
  • Livestock
  • Health
  • Epidemiology

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Published Papers (8 papers)

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Editorial

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5 pages, 242 KiB  
Editorial
Methicillin-Resistant Staphylococci and Macrococci at the Interface of Human and Animal Health
by Karsten Becker
Toxins 2021, 13(1), 61; https://doi.org/10.3390/toxins13010061 - 14 Jan 2021
Cited by 11 | Viewed by 2340
Abstract
The global impact of methicillin-resistant Staphylococcus aureus (MRSA) clonal lineages on human and animal health continues, even considering the decreasing MRSA rates in some parts of the world [...] Full article

Research

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10 pages, 680 KiB  
Article
Occurrence of Methicillin-Resistant Staphylococcus spp. on Brazilian Dairy Farms that Produce Unpasteurized Cheese
by Laryssa Freitas Ribeiro, Rafael Akira Sato, Andressa de Souza Pollo, Gabriel Augusto Marques Rossi and Luiz Augusto do Amaral
Toxins 2020, 12(12), 779; https://doi.org/10.3390/toxins12120779 - 8 Dec 2020
Cited by 8 | Viewed by 2694
Abstract
Methicillin-resistant Staphylococcus spp. (MRS) have been identified in several foods, including dairy products. Studies are needed about their occurrence and genetic diversity in the dairy production chain in order to gain a better understanding of their epidemiology and control. This study therefore focuses [...] Read more.
Methicillin-resistant Staphylococcus spp. (MRS) have been identified in several foods, including dairy products. Studies are needed about their occurrence and genetic diversity in the dairy production chain in order to gain a better understanding of their epidemiology and control. This study therefore focuses on isolating and characterizing MRS strains detected in milk used in the production of Brazilian artisanal unpasteurized cheeses. To this end, samples were collected from bovine feces, the hands of milkmen, milking buckets, sieves, unpasteurized milk, whey, water, artisanal unpasteurized cheeses, cheese processing surfaces, cheese handlers, cheese trays, cheese molds, and skimmers at five dairy farms located in the state of São Paulo, Brazil. Colonies suggestive of Staphylococcus spp. were subjected to multiplex PCR to confirm the presence of Staphylococcus aureus and to detect the mecA gene. Sixteen isolates containing mecA gene were detected in samples from unpasteurized cheese and from cheese handlers. None of these isolates were positive to enterotoxin genes. These 16 isolates were subjected to antimicrobial susceptibility tests, which revealed they were resistant to oxacillin, penicillin, and cefepime. Using gene sequencing, the MRS isolates were identified as S. haemolyticus, S. hominis, and S. epidermidis. Furthermore, isolates from cheese handlers’ hands and artisanal unpasteurized cheese presented high genetic similarity by random amplified polymorphic DNA (RAPD-PCR) analysis, which indicates cross contamination during cheese production. Thus, we found that people directly involved in milking and cheese processing activities at small dairy farms are a potential source of contamination of MRS strains in unpasteurized milk and cheese, representing a risk to public health. Full article
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19 pages, 1885 KiB  
Article
The Virulence Potential of Livestock-Associated Methicillin-Resistant Staphylococcus aureus Cultured from the Airways of Cystic Fibrosis Patients
by Janina Treffon, Sarah Ann Fotiadis, Sarah van Alen, Karsten Becker and Barbara C. Kahl
Toxins 2020, 12(6), 360; https://doi.org/10.3390/toxins12060360 - 30 May 2020
Cited by 8 | Viewed by 2856
Abstract
Staphylococcus aureus is one of the most common pathogens that infects the airways of patients with cystic fibrosis (CF) and contributes to respiratory failure. Recently, livestock-associated methicillin-resistant S. aureus (LA-MRSA), usually cultured in farm animals, were detected in CF airways. Although some of [...] Read more.
Staphylococcus aureus is one of the most common pathogens that infects the airways of patients with cystic fibrosis (CF) and contributes to respiratory failure. Recently, livestock-associated methicillin-resistant S. aureus (LA-MRSA), usually cultured in farm animals, were detected in CF airways. Although some of these strains are able to establish severe infections in humans, there is limited knowledge about the role of LA-MRSA virulence in CF lung disease. To address this issue, we analyzed LA-MRSA, hospital-associated (HA-) MRSA and methicillin-susceptible S. aureus (MSSA) clinical isolates recovered early in the course of airway infection and several years after persistence in this hostile environment from pulmonary specimens of nine CF patients regarding important virulence traits such as their hemolytic activity, biofilm formation, invasion in airway epithelial cells, cytotoxicity, and antibiotic susceptibility. We detected that CF LA-MRSA isolates were resistant to tetracycline, more hemolytic and cytotoxic than HA-MRSA, and more invasive than MSSA. Despite the residence in the animal host, LA-MRSA still represent a serious threat to humans, as such clones possess a virulence potential similar or even higher than that of HA-MRSA. Furthermore, we confirmed that S. aureus individually adapts to the airways of CF patients, which eventually impedes the success of antistaphylococcal therapy of airway infections in CF. Full article
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22 pages, 1204 KiB  
Article
Molecular Epidemiology of Methicillin-Susceptible and Methicillin-Resistant Staphylococcus aureus in Wild, Captive and Laboratory Rats: Effect of Habitat on the Nasal S. aureus Population
by Dina Raafat, Daniel M. Mrochen, Fawaz Al’Sholui, Elisa Heuser, René Ryll, Kathleen R. Pritchett-Corning, Jens Jacob, Bernd Walther, Franz-Rainer Matuschka, Dania Richter, Uta Westerhüs, Jiri Pikula, Jens van den Brandt, Werner Nicklas, Stefan Monecke, Birgit Strommenger, Sarah van Alen, Karsten Becker, Rainer G. Ulrich and Silva Holtfreter
Toxins 2020, 12(2), 80; https://doi.org/10.3390/toxins12020080 - 24 Jan 2020
Cited by 20 | Viewed by 5681
Abstract
Rats are a reservoir of human- and livestock-associated methicillin-resistant Staphylococcus aureus (MRSA). However, the composition of the natural S. aureus population in wild and laboratory rats is largely unknown. Here, 144 nasal S. aureus isolates from free-living wild rats, captive wild rats and [...] Read more.
Rats are a reservoir of human- and livestock-associated methicillin-resistant Staphylococcus aureus (MRSA). However, the composition of the natural S. aureus population in wild and laboratory rats is largely unknown. Here, 144 nasal S. aureus isolates from free-living wild rats, captive wild rats and laboratory rats were genotyped and profiled for antibiotic resistances and human-specific virulence genes. The nasal S. aureus carriage rate was higher among wild rats (23.4%) than laboratory rats (12.3%). Free-living wild rats were primarily colonized with isolates of clonal complex (CC) 49 and CC130 and maintained these strains even in husbandry. Moreover, upon livestock contact, CC398 isolates were acquired. In contrast, laboratory rats were colonized with many different S. aureus lineages—many of which are commonly found in humans. Five captive wild rats were colonized with CC398-MRSA. Moreover, a single CC30-MRSA and two CC130-MRSA were detected in free-living or captive wild rats. Rat-derived S. aureus isolates rarely harbored the phage-carried immune evasion gene cluster or superantigen genes, suggesting long-term adaptation to their host. Taken together, our study revealed a natural S. aureus population in wild rats, as well as a colonization pressure on wild and laboratory rats by exposure to livestock- and human-associated S. aureus, respectively. Full article
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20 pages, 2446 KiB  
Article
Molecular Characterization of Equine Staphylococcus aureus Isolates Exhibiting Reduced Oxacillin Susceptibility
by Anissa D. Scholtzek, Dennis Hanke, Birgit Walther, Inga Eichhorn, Sabita D. Stöckle, Katja-Sophia Klein, Heidrun Gehlen, Antina Lübke-Becker, Stefan Schwarz and Andrea T. Feßler
Toxins 2019, 11(9), 535; https://doi.org/10.3390/toxins11090535 - 13 Sep 2019
Cited by 25 | Viewed by 4574
Abstract
The detection of borderline oxacillin-resistant Staphylococcus aureus (BORSA) represents a challenge to both, veterinary and human laboratories. Between 2015 and 2017, 19 equine S. aureus with elevated minimal inhibitory concentrations for oxacillin were detected in routine diagnostics. The aim of this study was [...] Read more.
The detection of borderline oxacillin-resistant Staphylococcus aureus (BORSA) represents a challenge to both, veterinary and human laboratories. Between 2015 and 2017, 19 equine S. aureus with elevated minimal inhibitory concentrations for oxacillin were detected in routine diagnostics. The aim of this study was to characterize these isolates to identify factors possibly associated with the BORSA phenotype. All S. aureus were subjected to antimicrobial susceptibility testing and whole genome sequencing (WGS). A quantifiable β-lactamase activity assay was performed for a representative subset of 13 isolates. The WGS data analysis of the 19 BORSA isolates identified two different genomic lineages, sequence type (ST) 1 and ST1660. The core genome multilocus sequence typing (cgMLST) revealed a close relatedness of all isolates belonging to either ST1 or ST1660. The WGS analysis identified the resistance genes aadD, dfrG, tet(L), and/or blaZ and aacA-aphD. Phenotypic resistance to penicillins, aminoglycosides, tetracyclines, fluoroquinolones and sulfamethoxazole/trimethoprim was observed in the respective isolates. For the penicillin-binding proteins 1–4, amino acid substitutions were predicted using WGS data. Since neither transglycosylase nor transpeptidase domains were affected, these alterations might not explain the BORSA phenotype. Moreover, β-lactamase activity was found to be associated with an inducible blaZ gene. Lineage-specific differences regarding the expression profiles were noted. Full article
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14 pages, 1443 KiB  
Article
Distribution of Toxinogenic Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus from Different Ecological Niches in Algeria
by Assia Mairi, Abdelaziz Touati, Alix Pantel, Karima Zenati, Alex Yahiaoui Martinez, Catherine Dunyach-Remy, Albert Sotto and Jean-Philippe Lavigne
Toxins 2019, 11(9), 500; https://doi.org/10.3390/toxins11090500 - 28 Aug 2019
Cited by 22 | Viewed by 4081
Abstract
The diffusion of Panton–Valentine leukocidin (PVL)–positive methicillin-resistant S. aureus (MRSA) is a health problem in Algeria. The objectives of the study were to investigate the global distribution of methicillin-susceptible S. aureus (MSSA) and MRSA isolates in different ecological niches in this country. In [...] Read more.
The diffusion of Panton–Valentine leukocidin (PVL)–positive methicillin-resistant S. aureus (MRSA) is a health problem in Algeria. The objectives of the study were to investigate the global distribution of methicillin-susceptible S. aureus (MSSA) and MRSA isolates in different ecological niches in this country. In total, 2246 samples were collected from humans, livestock, wild animals, pets, food products and the aquatic environment, from 12 Algerian provinces. A total of 312 S. aureus were detected from 2446 samples (12.7%) in the screened niches. We observed the emergence of toxinogenic S. aureus representing 41% of the isolates. Among them, we noted the diffusion of ST80-IV CA-MRSA PVL + strains isolated in human, animals, and food and genetic diversity of MSSA PVL + isolates. This study suggests an alarming dissemination of MRSA-ST80 PVL + in both human and extra-human sources in Algeria. Moreover, MSSA may become a permanent reservoir of the PVL genes necessary for human infections. Full article
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10 pages, 261 KiB  
Article
Nasal Colonization of Humans with Occupational Exposure to Raw Meat and to Raw Meat Products with Methicillin-Susceptible and Methicillin-Resistant Staphylococcus aureus
by Christiane Cuny, Franziska Layer, Sonja Hansen, Guido Werner and Wolfgang Witte
Toxins 2019, 11(4), 190; https://doi.org/10.3390/toxins11040190 - 30 Mar 2019
Cited by 30 | Viewed by 3590
Abstract
Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) is widely disseminated as a nasal colonizer of conventionally raised livestock and of humans subjected to occupational exposure. Reports on contamination of raw meat raise the question as to whether occupationally exposed food handlers are at particular risk [...] Read more.
Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) is widely disseminated as a nasal colonizer of conventionally raised livestock and of humans subjected to occupational exposure. Reports on contamination of raw meat raise the question as to whether occupationally exposed food handlers are at particular risk of nasal colonization by LA-MRSA. Here, we report the results from a cross-sectional study on nasal S. aureus/MRSA colonization of butchers, meat sellers, and cooks in Germany. We sampled 286 butchers and meat sellers in 26 butcheries and 319 cooks handling meat in 16 professional canteen kitchens. Swabs were processed on both blood agar plates and MRSA-selective plates. MRSA were confirmed by PCR for mec genes and by broth microdilution. All isolates were subjected to molecular typing. PCR for markers useful to differentiate human-adapted and animal-adapted subpopulations was performed due to the presence of clonal complexes known to occur in both livestock and humans (CC5, CC7, CC8, CC9, and CC398). Only two participants (0.33%) were colonized by MRSA (Hospital-associated MRSA ST22). Nasal colonization by methicillin-susceptible S. aureus (MSSA) was detected in 16.6% of cooks and in 26.2% of butchers and meat sellers. Among 16 of the isolates attributed to CC7, three were negative for the immune evasion gene cluster, suggesting an animal origin. Isolates attributed to CC5, CC8, and CC398 were negative for markers typical of animal-adapted subpopulations. The occupational handling of raw meat and raw meat products was not associated with nasal colonization by LA-MRSA. Full article

Review

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21 pages, 2018 KiB  
Review
Methicillin-Resistant Staphylococcus aureus ST80 Clone: A Systematic Review
by Assia Mairi, Abdelaziz Touati and Jean-Philippe Lavigne
Toxins 2020, 12(2), 119; https://doi.org/10.3390/toxins12020119 - 14 Feb 2020
Cited by 30 | Viewed by 5180
Abstract
This review assessed the molecular characterization of the methicillin-resistant Staphylococcus aureus (MRSA)-ST80 clone with an emphasis on its proportion of total MRSA strains isolated, PVL production, spa-typing, antibiotic resistance, and virulence. A systematic review of the literature was conducted on MRSA-ST80 clone [...] Read more.
This review assessed the molecular characterization of the methicillin-resistant Staphylococcus aureus (MRSA)-ST80 clone with an emphasis on its proportion of total MRSA strains isolated, PVL production, spa-typing, antibiotic resistance, and virulence. A systematic review of the literature was conducted on MRSA-ST80 clone published between 1 January 2000 and 31 August 2019. Citations were chosen for a review of the full text if we found evidence that MRSA-ST80 clone was reported in the study. For each isolate, the country of isolation, the sampling period, the source of isolation (the type of infection, nasal swabs, or extra-human), the total number of MRSA strains isolated, number of MRSA-ST80 strains, antibiotic resistance patterns, PVL production, virulence genes, and spa type were recorded. The data from 103 articles were abstracted into an Excel database. Analysis of the data showed that the overall proportion of MRSA-ST80 has been decreasing in many countries in recent years. The majority of MRSA-ST80 were PVL positive with spa-type t044. Only six reports of MRSA-ST80 in extra-human niches were found. This review summarizes the rise of MRSA-ST80 and the evidence that suggests that it could be in decline in many countries. Full article
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