Benzylpenicillin-producing Trichophyton erinacei and methicillin resistant Staphylococcus aureus carrying the mecC gene on European hedgehogs – A pilot-study

Dube, Faruk; Söderlund, Robert; Salomonsson, Matilda Lampinen; Troell, Karin; Börjesson, Stefan

doi:10.1186/s12866-021-02260-9

Cited by 13 publications

(14 citation statements)

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“…The SCC mec are considered mobile genetic elements that could harbour AMR genes other than the mec [ 7 ]. The mecA gene (encoding PBP2a) has been detected in most MRSA isolates of animals, humans and the environment [ 8 ]. However, the origin and reservoir host of the mecC gene (which encodes the PBP2c) in MRSA has not been fully determined.…”

Section: Introductionmentioning

confidence: 99%

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Wild Animals Are Reservoirs and Sentinels of Staphylococcus aureus and MRSA Clones: A Problem with “One Health” Concern

et al. 2021

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Background: The availability of comprehensive data on the ecology and molecular epidemiology of Staphylococcus aureus/MRSA in wild animals is necessary to understand their relevance in the “One Health” domain. Objective: In this study, we determined the pooled prevalence of nasal, tracheal and/or oral (NTO) Staphylococcus aureus (S. aureus) and methicillin-resistant S. aureus (MRSA) carriage in wild animals, with a special focus on mecA and mecC genes as well as the frequency of MRSA and methicillin susceptible S. aureus (MSSA) of the lineages CC398 and CC130 in wild animals. Methodology: This systematic review was executed on cross-sectional studies that reported S. aureus and MRSA in the NTO cavities of wild animals distributed in four groups: non-human primates (NHP), wild mammals (WM, excluding rodents and NHP), wild birds (WB) and wild rodents (WR). Appropriate and eligible articles published (in English) between 1 January 2011 to 30 August 2021 were searched for from PubMed, Scopus, Google Scholar, SciElo and Web of Science. Results: Of the 33 eligible and analysed studies, the pooled prevalence of NTO S. aureus and MRSA carriage was 18.5% (range: 0–100%) and 2.1% (range: 0.0–63.9%), respectively. The pooled prevalence of S. aureus/MRSA in WM, NHP, WB and WR groups was 15.8/1.6, 32.9/2.0, 10.3/3.4 and 24.2/3.4%, respectively. The prevalence of mecC-MRSA among WM/NHP/WB/WR was 1.64/0.0/2.1/0.59%, respectively, representing 89.9/0.0/59.1/25.0% of total MRSA detected in these groups of animals.The MRSA-CC398 and MRSA-CC130 lineages were most prevalent in wild birds (0.64 and 2.07%, respectively); none of these lineages were reported in NHP studies. The MRSA-CC398 (mainly of spa-type t011, 53%), MRSA-CC130 (mainly of spa types t843 and t1535, 73%), MSSA-CC398 (spa-types t571, t1451, t6606 and t034) and MSSA-CC130 (spa types t843, t1535, t3625 and t3256) lineages were mostly reported. Conclusion: Although the global prevalence of MRSA is low in wild animals, mecC-mediated resistance was particularly prevalent among MRSA isolates, especially among WM and WB. Considering the genetic diversity of MRSA in wild animals, they need to be monitored for effective control of the spread of antimicrobial resistance.

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Section: Introductionmentioning

confidence: 99%

“…Initially, mecC was related with livestock associated (LA)-MRSA; however, it's continued and increased detection in wild animals indicates that mecC -MRSA is primarily associated with wildlife [ 9 ]. This suggests that mecC -MRSA could be considered as wildlife-associated MRSA (WA-MRSA) [ 8 , 9 ].…”

Section: Introductionmentioning

confidence: 99%

Wild Animals Are Reservoirs and Sentinels of Staphylococcus aureus and MRSA Clones: A Problem with “One Health” Concern

et al. 2021

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“…Our hypothesis that the evolution of mecC -MRSA was driven by natural selection is supported by studies from northwestern Europe and New Zealand that showed that hedgehogs are frequently colonized with the dermatophyte T. erinacei , which produces a penicillinase-labile penicillin-like substance that was recently identified as penicillin G 12 – 19 . To test our hypothesis, we examined the distribution of mecC -MRSA and other S .…”

Section: Mainmentioning

confidence: 62%

“…erinacei is widespread among hedgehogs in New Zealand and northwestern Europe and that isolates from both continents produce a penicillinase-labile penicillin-like substance 12 – 19 , and a recent study characterized penicillin G from T . erinacei in Sweden (the presence of other β-lactams was not investigated) 19 . This suggests that penicillin-producing T .…”

Section: Discussionmentioning

confidence: 99%

Emergence of methicillin resistance predates the clinical use of antibiotics

Larsen

Raisen

et al. 2022

Nature

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186

102

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The discovery of antibiotics more than 80 years ago has led to considerable improvements in human and animal health. Although antibiotic resistance in environmental bacteria is ancient, resistance in human pathogens is thought to be a modern phenomenon that is driven by the clinical use of antibiotics1. Here we show that particular lineages of methicillin-resistant Staphylococcus aureus—a notorious human pathogen—appeared in European hedgehogs in the pre-antibiotic era. Subsequently, these lineages spread within the local hedgehog populations and between hedgehogs and secondary hosts, including livestock and humans. We also demonstrate that the hedgehog dermatophyte Trichophyton erinacei produces two β-lactam antibiotics that provide a natural selective environment in which methicillin-resistant S. aureus isolates have an advantage over susceptible isolates. Together, these results suggest that methicillin resistance emerged in the pre-antibiotic era as a co-evolutionary adaptation of S. aureus to the colonization of dermatophyte-infected hedgehogs. The evolution of clinically relevant antibiotic-resistance genes in wild animals and the connectivity of natural, agricultural and human ecosystems demonstrate that the use of a One Health approach is critical for our understanding and management of antibiotic resistance, which is one of the biggest threats to global health, food security and development.

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“…The occurrence of MRSA in wildlife without exposure to antibiotics has been recently reviewed (Heaton et al, 2020: Silva et al, 2020, showing that most MRSA isolated from wild animals are mecC positive. The dissemination of this mechanism of resistance (García-Álvarez et al et al, 2011;Shore et al, 2011) in freeliving animals and river waters (Porrero et al, 2014a) suggests that the natural environment may be a reservoir of mecC gene, and indeed, a cocolonisation of hedgehogs with S. aureus and dermatophytes that produce penicillin provides a selective pressure favouring mecC in the wild (Dube et al, 2021;Larsen et al, 2022;Smith & Marples, 1965).…”

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confidence: 99%

Survey ofStaphylococcus aureuscarriage by free‐living red deer (Cervus elaphus): Evidence of human and domestic animal lineages

Luzzago

Lauzi

Ehricht

et al. 2022

Transbounding Emerging Dis

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Staphylococcus aureus is a pathogen that can affect multiple host species. Evidence of transmission between humans and animals and among different animal species has been reported in recent years. In this study, we investigated 284 free-living red deer (Cervus elaphus) in the Central Italian Alps to assess the prevalence and molecular characteristics of S. aureus in nasal and intestinal samples in relation to host features and environmental factors. A prevalence of 90%, 26.2% and 10.7% of S. aureus was detected in nasal rectal swabs and faeces, respectively. Calves had a higher probability of being S. aureus intestinal carriers than adults, especially in females when considering faecal samples. Clonal complex (CC) 425 was the most prevalent lineage (61.5%). This is a lineage known to be widespread in both domestic and free-living animals. It was followed by CC2671 (15.4%) and CC350 (6.4%). A high rate of the phage-borne virulence factor lukM/lukF-P83 was detected in CC425 and CC350. Further lineages, which are known to occur in both humans and animals, were detected sporadically in red deer faeces only, that is, CC7, CC9, CC121 and CC707, harbouring the genes of the penicillinase operon and a gene for macrolide resistance (CC9 and CC121). Methicillin resistance genes mecA and mecC were not found. Our results suggest that free-living red deer may be reservoir for S. aureus in Alpine habitats. K E Y W O R D Scervidae, DNA microarray analysis, multi-host pathogen, red deer, Staphylococcus aureus, wildlife INTRODUCTIONStaphylococcus aureus is a generalist bacterial species that inhabits mucosae and skin in humans and animals (Haag et al., 2019;Tong et al., 2015), and whose primary ecological niche is found in the nares.

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Benzylpenicillin-producing Trichophyton erinacei and methicillin resistant Staphylococcus aureus carrying the mecC gene on European hedgehogs – A pilot-study

Cited by 13 publications

References 40 publications

Wild Animals Are Reservoirs and Sentinels of Staphylococcus aureus and MRSA Clones: A Problem with “One Health” Concern

Wild Animals Are Reservoirs and Sentinels of Staphylococcus aureus and MRSA Clones: A Problem with “One Health” Concern

Emergence of methicillin resistance predates the clinical use of antibiotics

Survey ofStaphylococcus aureuscarriage by free‐living red deer (Cervus elaphus): Evidence of human and domestic animal lineages

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