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      High toxinogenic potential of Staphylococcus aureus from wild ungulates in Brandenburg, Germany with a low level of antibiotic resistance

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          Abstract

          Introduction

          Data regarding the occurrence and virulence of Staphylococcus ( S.) aureus in wild living animals is rare. However, S. aureus may carry a multitude of virulence factors and express resistance to several antimicrobial substances. Handling game meat may thus lead to serious infections or food poisoning. The aim of this study was to provide insights into the occurrence and characteristics of S. aureus in wild ungulates from Brandenburg, Germany.

          Methods

          Nasal swabs of externally healthy-looking wild boars, roe, fallow and red deer were collected in hunts during season 2021/2022 and analyzed for S. aureus by selective enrichment. Species were determined using matrix assisted laser desorption ionization mass spectrometry and tested for phenotypic antimicrobial resistance. Whole-genome sequencing was conducted for genotyping, determination of virulence associated genes and analysis of phylogenetic relationships.

          Results

          S. aureus were recovered from approximately 8% of nasal swabs. However, the strains were only obtained from the sampled wild ruminants. S. aureus isolates were associated with sequence types (ST) 1, ST30, ST133, ST425, ST582 and ST6238. Isolates of ST1 clustered closely together in the phylogenetic analysis. Genes encoding staphylococcal enterotoxin (SE) or SE-like (SEl) were found in 14/17 isolates. In particular, a seh gene was present in 12/17 isolates. Moreover, two isolates harbored a multiplicity of genes encoding SE or SEl. In addition, the toxic shock syndrome toxin encoding tst gene was detected in one isolate. This isolate was resistant to penicillin and cefoxitin and accordingly harbored the blaZ gene.

          Discussion

          Wild ungulates intended for human consumption may carry potentially virulent S. aureus. In one case, the close phylogenetic relationship of S. aureus isolates indicates a possible intraspecific spread within a common territory. However, for others, the origin or the spread pattern can only be inferred. Handling of animals or their carcasses might contribute to staphylococcal infections in humans. Moreover, food poisoning due to SE producing strains may occur, if recommended hygiene practices are not applied during processing of game meat.

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          Most cited references63

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          Global mortality associated with 33 bacterial pathogens in 2019: a systematic analysis for the Global Burden of Disease Study 2019

          Background Reducing the burden of death due to infection is an urgent global public health priority. Previous studies have estimated the number of deaths associated with drug-resistant infections and sepsis and found that infections remain a leading cause of death globally. Understanding the global burden of common bacterial pathogens (both susceptible and resistant to antimicrobials) is essential to identify the greatest threats to public health. To our knowledge, this is the first study to present global comprehensive estimates of deaths associated with 33 bacterial pathogens across 11 major infectious syndromes. Methods We estimated deaths associated with 33 bacterial genera or species across 11 infectious syndromes in 2019 using methods from the Global Burden of Diseases, Injuries, and Risk Factors Study (GBD) 2019, in addition to a subset of the input data described in the Global Burden of Antimicrobial Resistance 2019 study. This study included 343 million individual records or isolates covering 11 361 study-location-years. We used three modelling steps to estimate the number of deaths associated with each pathogen: deaths in which infection had a role, the fraction of deaths due to infection that are attributable to a given infectious syndrome, and the fraction of deaths due to an infectious syndrome that are attributable to a given pathogen. Estimates were produced for all ages and for males and females across 204 countries and territories in 2019. 95% uncertainty intervals (UIs) were calculated for final estimates of deaths and infections associated with the 33 bacterial pathogens following standard GBD methods by taking the 2·5th and 97·5th percentiles across 1000 posterior draws for each quantity of interest. Findings From an estimated 13·7 million (95% UI 10·9–17·1) infection-related deaths in 2019, there were 7·7 million deaths (5·7–10·2) associated with the 33 bacterial pathogens (both resistant and susceptible to antimicrobials) across the 11 infectious syndromes estimated in this study. We estimated deaths associated with the 33 bacterial pathogens to comprise 13·6% (10·2–18·1) of all global deaths and 56·2% (52·1–60·1) of all sepsis-related deaths in 2019. Five leading pathogens— Staphylococcus aureus, Escherichia coli, Streptococcus pneumoniae, Klebsiella pneumoniae , and Pseudomonas aeruginosa —were responsible for 54·9% (52·9–56·9) of deaths among the investigated bacteria. The deadliest infectious syndromes and pathogens varied by location and age. The age-standardised mortality rate associated with these bacterial pathogens was highest in the sub-Saharan Africa super-region, with 230 deaths (185–285) per 100 000 population, and lowest in the high-income super-region, with 52·2 deaths (37·4–71·5) per 100 000 population. S aureus was the leading bacterial cause of death in 135 countries and was also associated with the most deaths in individuals older than 15 years, globally. Among children younger than 5 years, S pneumoniae was the pathogen associated with the most deaths. In 2019, more than 6 million deaths occurred as a result of three bacterial infectious syndromes, with lower respiratory infections and bloodstream infections each causing more than 2 million deaths and peritoneal and intra-abdominal infections causing more than 1 million deaths. Interpretation The 33 bacterial pathogens that we investigated in this study are a substantial source of health loss globally, with considerable variation in their distribution across infectious syndromes and locations. Compared with GBD Level 3 underlying causes of death, deaths associated with these bacteria would rank as the second leading cause of death globally in 2019; hence, they should be considered an urgent priority for intervention within the global health community. Strategies to address the burden of bacterial infections include infection prevention, optimised use of antibiotics, improved capacity for microbiological analysis, vaccine development, and improved and more pervasive use of available vaccines. These estimates can be used to help set priorities for vaccine need, demand, and development. Funding Bill & Melinda Gates Foundation, Wellcome Trust, and Department of Health and Social Care, using UK aid funding managed by the Fleming Fund.
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            Updating benchtop sequencing performance comparison.

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              Staphylococcus aureus and its food poisoning toxins: characterization and outbreak investigation.

              Staphylococcal food poisoning (SFP) is one of the most common food-borne diseases and results from the ingestion of staphylococcal enterotoxins (SEs) preformed in food by enterotoxigenic strains of Staphylococcus aureus. To date, more than 20 SEs have been described: SEA to SElV. All of them have superantigenic activity whereas half of them have been proved to be emetic, representing a potential hazard for consumers. This review, divided into four parts, will focus on the following: (1) the worldwide story of SFP outbreaks, (2) the characteristics and behaviour of S. aureus in food environment, (3) the toxinogenic conditions and characteristics of SEs, and (4) SFP outbreaks including symptomatology, occurrence in the European Union and currently available methods used to characterize staphylococcal outbreaks. © European Union 2011 Published by Blackwell Publishing Ltd.
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                Author and article information

                Contributors
                URI : https://loop.frontiersin.org/people/985802/overviewRole: Role: Role: Role: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2608186/overviewRole: Role: Role: Role:
                URI : https://loop.frontiersin.org/people/2790630/overviewRole: Role: Role:
                URI : https://loop.frontiersin.org/people/2014017/overviewRole: Role: Role:
                Role: Role: Role: Role:
                Journal
                Front Vet Sci
                Front Vet Sci
                Front. Vet. Sci.
                Frontiers in Veterinary Science
                Frontiers Media S.A.
                2297-1769
                23 July 2024
                2024
                : 11
                : 1445413
                Affiliations
                [1] 1Department Biological Safety, German Federal Institute for Risk Assessment (BfR) , Berlin, Germany
                [2] 2Department Safety in the Food Chain, German Federal Institute for Risk Assessment (BfR) , Berlin, Germany
                [3] 3Department of Animal Sciences, University of Göttingen , Göttingen, Germany
                [4] 4TUM School of Life Sciences, Animal Nutrition and Metabolism,Technical University of Munich , Freising-Weihenstephan, Germany
                Author notes

                Edited by: Magdalena Baymakova, Military Medical Academy (Bulgaria), Bulgaria

                Reviewed by: Rumyana Markovska, Medical University Sofia, Bulgaria

                Francesca Pedonese, University of Pisa, Italy

                Yordan Hodzhev, National Center of Infectious and Parasitic Diseases (NCIPD), Bulgaria

                Tsvetelina Paunova-Krasteva, Bulgarian Academy of Sciences, Bulgaria

                Natalia Wiktorczyk-Kapischke, Nicolaus Copernicus University in Toruń, Poland

                *Correspondence: Tobias Lienen, tobias.lienen@ 123456bfr.bund.de

                ORCID: Tobias Lienen, https://orcid.org/0000-0003-2564-1472

                Rafael Hernán Mateus-Vargas, https://orcid.org/0000-0001-5489-2452

                Article
                10.3389/fvets.2024.1445413
                11300323
                47adb73b-1510-45d8-b0ea-bcb6ebd9f747
                Copyright © 2024 Lienen, Mateus-Vargas, Steinhoff-Wagner, Richter and Maurischat.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 07 June 2024
                : 11 July 2024
                Page count
                Figures: 1, Tables: 2, Equations: 0, References: 65, Pages: 8, Words: 7230
                Funding
                Funded by: BfR, doi 10.13039/501100008751;
                Award ID: 1322-769
                The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. This study was carried out in the framework of the BfR internal project No. 1322-769.
                Categories
                Veterinary Science
                Original Research
                Custom metadata
                Veterinary Epidemiology and Economics

                staphylococcus aureus,wild ungulates,virulence,antimicrobial resistance,phylogeny

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