Publications by authors named "Stefan Schwarz"

531 Publications

Plasmid Fusion and Recombination Events That Occurred during Conjugation of -Carrying Plasmids in Enterococci.

Microbiol Spectr 2022 Jan 19:e0150521. Epub 2022 Jan 19.

College of Veterinary Medicine, Henan Agricultural Universitygrid.108266.b, Zhengzhou, People's Republic of China.

Linezolid plays a crucial role in the treatment of infections caused by multiresistant Gram-positive bacteria. The gene not only confers oxazolidinone and phenicol resistance but also decreases susceptibility to tetracycline. In this study, we investigated structural changes in mobilizable -carrying plasmids in enterococci which occurred during conjugation experiments using S1-PFGE (pulsed-field gel electrophoresis), Southern blot hybridization, and whole-genome sequencing (WGS) analysis. Two -carrying strains were identified in Enterococcus faecalis E006 and Enterococcus lactis E843, respectively. E. faecalis E006 contains the 121,520-bp conjugative plasmid pE006-121 and the 19,832-bp mobilizable -carrying plasmid pE006-19, while E843 contains the 171,930-bp conjugative plasmid pE843-171 and the 27,847-bp mobilizable -carrying plasmid pE843-27. Moreover, both -carrying plasmids were mobilized by their respective conjugative plasmid in enterococci by plasmid fusion; one was generated by homologous recombination in E. faecalis through an identical 864-bp homologous region in the plasmids of the parental strain, while another was generated by an IS-mediated plasmid integration in , involving a replicative transposition. Until now, all the genes described in enterococci, including E. faecalis, E. faecium, and E. hirae, are plasmid-borne, suggesting that plasmids play an important role in the dissemination of the gene among enterococci. This study showed that the mobilizable -carrying plasmid could transfer with the help of conjugative plasmid in enterococci via plasmid fusion, with one generated by homologous recombination in E. faecalis, and another by replicative transposition in . During both the fusion events, the -carrying plasmids changed from nonconjugative to conjugative, leading to the generation and enhanced dissemination of the larger phenicol-oxazolidinone-tetracycline resistance-encoding plasmids in enterococci.
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http://dx.doi.org/10.1128/spectrum.01505-21DOI Listing
January 2022

Characterization of the novel optrA-carrying pseudo-compound transposon Tn7363 and an Inc18 plasmid carrying cfr(D) in Vagococcus lutrae.

J Antimicrob Chemother 2022 Jan 17. Epub 2022 Jan 17.

State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin 150069, China.

Objectives: To investigate the genetic context and transferability of the oxazolidinone resistance genes cfr(D) and optrA in a porcine Vagococcus lutrae isolate.

Methods: V. lutrae isolate BN31 was screened for the presence of known oxazolidinone resistance genes via PCR assays. Conjugation experiments were carried out to assess horizontal transferability of resistance genes. WGS was performed using a combination of Nanopore MinION and Illumina HiSeq platforms. Detection of a translocatable unit (TU) was conducted by PCR.

Results: V. lutrae isolate BN31 harboured the oxazolidinone resistance genes cfr(D) and optrA. The optrA gene, together with the phenicol resistance gene fexA, was located on a novel pseudo-compound transposon, designated Tn7363. Tn7363 was bounded by two copies of the new insertion sequence ISVlu1, which represented a new member of the ISL3 family. A TU, comprising one copy of ISVlu1 and the segment between the two IS elements including the optrA gene, was detected. The cfr(D) gene and an erm(B) gene were identified on the broad-host-range Inc18 plasmid pBN31-cfrD, a pAMβ1-like plasmid. Similar to plasmid pAMβ1, plasmid pBN31-cfrD was conjugative.

Conclusions: To the best of our knowledge, we report the first identification of the cfr(D) and optrA in Vagococcus. Two novel oxazolidinone resistance gene-carrying mobile genetic elements, Tn7363 and pBN31-cfrD, were identified in V. lutrae BN31. Considering their transmission potential, attention should be paid to the risk of transfer of the optrA and cfr(D) genes from V. lutrae to clinically more important bacterial pathogens.
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http://dx.doi.org/10.1093/jac/dkab478DOI Listing
January 2022

(T)-Mediated Macrolide-Lincosamide Resistance in Streptococcus suis.

Microbiol Spectr 2022 Jan 12:e0165721. Epub 2022 Jan 12.

College of Veterinary Medicine, Henan Agricultural Universitygrid.108266.b, Zhengzhou, People's Republic of China.

To investigate the presence and location of (T) in clinical Streptococcus suis isolates and explore the transmission ability and fitness cost of (T)-carrying mobile genetic elements among S. suis isolates, MICs were determined by broth microdilution. The presence of (T) in S. suis was detected by PCR. The genetic environment of (T) in S. suis was explored by whole-genome sequencing (WGS) analysis. Intraspecies and interspecies transmission were examined by electrotransformation. The fitness cost associated with the carriage of an (T)-harboring plasmid or an integrative and conjugative element (ICE) was examined by competition experiments. Of 237 nonduplicate strains, (T) was detected in 2 S. suis strains (SC262-ST954 and SC117-ST1314), with its location on a 5,125-bp plasmid in S. suis SC262 and on a 64,013-bp ICESC117 in S. suis SC117, respectively. Both the (T)-carrying plasmid pSC262 and the ICESC117 were transmissible by transformation. Plasmid pSC262 can replicate and express macrolide-lincosamide resistance in heterologous hosts, including S. aureus and S. pneumoniae. Both the (T)-carrying plasmid and the ICE posed a fitness cost to the host S. suis isolate. To the best of our knowledge, this is the first report of the macrolide-lincosamide-streptogramin B resistance gene (T) in S. suis. Its location on a plasmid or an ICE will aid in its transmission. The low detection rate of (T) gene among the S. suis population might be due to the fitness cost of the (T)-carrying plasmid and ICE. Macrolide and lincosamide resistance due to the presence of (T) have posed a challenge for the treatment of Gram-positive pathogens. Although the low detection rate of (T) gene among the S. suis population due to the fitness cost of the (T)-carrying plasmid and ICE, the presence of (T) in S. suis and its potential transmission to other Gram-positive pathogens will be of important significance.
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http://dx.doi.org/10.1128/spectrum.01657-21DOI Listing
January 2022

Staphylococcus aureus isolates from Eurasian Beavers (Castor fiber) carry a novel phage-borne bicomponent leukocidin related to the Panton-Valentine leukocidin.

Sci Rep 2021 12 22;11(1):24394. Epub 2021 Dec 22.

Leibniz Institute of Photonic Technology (Leibniz-IPHT), Jena, Germany.

Staphylococcus aureus can be a harmless coloniser, but it can also cause severe infections in humans, livestock and wildlife. Regarding the latter, only few studies have been performed and knowledge on virulence factors is insufficient. The aim of the present study was to study S. aureus isolates from deceased wild beavers (Castor fiber). Seventeen isolates from eleven beavers, found in Germany and Austria, were investigated. Antimicrobial and biocide susceptibility tests were performed. Isolates were characterised using S. aureus-specific DNA microarrays, spa typing and whole-genome sequencing. From two isolates, prophages were induced by mitomycin C and studied by transmission electron microscopy. Four isolates belonged to clonal complex (CC) 8, CC12, and CC398. Twelve isolates belonged to CC1956 and one isolate was CC49. The CC49 and CC1956 isolates carried distinct lukF/S genes related to the Panton-Valentine leukocidin (PVL) from human isolates of S. aureus. These genes were located on related, but not identical, Siphovirus prophages. The beavers, from which those isolates originated, suffered from abscesses, purulent organ lesions and necrotising pneumonia, i.e., clinical manifestations resembling symptoms of severe PVL-associated disease in humans. It might thus be assumed that the "Beaver Leukocidin (BVL, lukF/S-BV)"-positive strains are beaver-specific pathogens, and further studies on their clinical role as well as on a possible transmissibility to other species, including humans, are warranted.
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http://dx.doi.org/10.1038/s41598-021-03823-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8695587PMC
December 2021

Novel Tet(L) Efflux Pump Variants Conferring Resistance to Tigecycline and Eravacycline in Staphylococcus Spp.

Microbiol Spectr 2021 12 8;9(3):e0131021. Epub 2021 Dec 8.

College of Veterinary Medicine, Henan Agricultural Universitygrid.108266.b, Zhengzhou, People's Republic of China.

Tigecycline is regarded as one of the few important last-resort antibiotics to treat complicated skin and intra-abdominal infections. Members of the genus Staphylococcus are zoonotic pathogens and pose a serious threat to public health. Tigecycline resistance in this species appears to be a rare phenomenon, and the mechanisms underlying tigecycline resistance have not been fully elucidated. Here, we report two novel variants of the (L) gene in Staphylococcus spp. from swine in China, designed as (L) and (L). The (L) was located within a 18,720 bp chromosomal multidrug resistance gene cluster flanked by two copies of IS in Staphylococcus cohnii 11-B-312, while the (L) was located on a 6,292 bp plasmid in 11-B-93, which could be transferred to S. aureus by electrotransformation. Cloning of each of the two (L) variants into S. aureus RN4220 showed 16- or 8-fold increases in the minimal inhibition concentrations (MICs), which can fully confer the resistance to tigecycline (MICs from 0.125 to 2 mg/liter) and eravacycline (MICs from 0.125 to 1 or 2 mg/liter), but no increase in the MICs of omadacycline, compared with the MICs of the recipient strain S. aureus RN4220. In the murine sepsis and in the murine pneumonia models, an increase in CFU of S. aureus 29213_pT93 carrying the (L) was seen despite tigecycline treatment. This observation suggests that the (L) and its associated gene product compromise the efficacy of tigecycline treatment and may lead to clinical treatment failure. Our finding, that novel Tet(L) efflux pump variants which confer tigecycline and eravacycline resistance have been identified in Staphylococcus spp., requires urgent attention. Tigecycline and eravacycline are both important last-resort broad spectrum antimicrobial agents. The presence of novel Tet(L) efflux pump variants conferring the resistance to tigecycline and eravacycline in Staphylococcus spp. and its potential transmission to S. aureus will compromise the efficacy of tigecycline and eravacycline treatment for S. aureus associated infection and may lead to clinical treatment failure.
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http://dx.doi.org/10.1128/Spectrum.01310-21DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8653819PMC
December 2021

Multiresistant Gram-Negative Pathogens—A Zoonotic Problem.

Dtsch Arztebl Int 2021 09;118(35-36):579-589

Institute for Hygiene, DRK Kliniken Berlin; Institute for Hygiene, University Hospital Münster; Bayerisches Landesamt für Gesundheit und Lebensmittelsicherheit, Munich; Global Environmental Health and Climate Change, Institute and Outpatient Clinic for Occupational, Social and Environmental Medicine, Clinical Centre of the Ludwig Maximilian University Munich; Institute for Biometry, Epidemiology and Information Processing, University of Veterinary Medicine Hannover; Institute of Microbiology and Epizootics, Department of Veterinary Medicine at the Freie Universtität Berlin; Department Biological Safety, German Federal Institute for risk assessment, Berlin; Advanced Light and Electron Microscopy, Robert Koch Institute, Berlin.

Background: Extended-spectrum-β-lactamase-producing, carbapenemase-producing, and colistin-resistant Enterobacterales (ESBL-E, CPE, and Col-E) are multiresistant pathogens that are increasingly being encountered in both human and veterinary medicine. In this review, we discuss the frequency, sources, and significance of the zoonotic transmission of these pathogens between animals and human beings.

Methods: This review is based on pertinent publications retrieved by a selective literature search. Findings for Germany are presented in the global context.

Results: ESBL-E are common in Germany in both animals and human beings, with a 6-10% colonization rate in the general human population. A major source of ESBL-E is human-to-human transmission, partly through travel. Some colonizations are of zoonotic origin (i.e., brought about by contact with animals or animal-derived food products); in the Netherlands, more than 20% of cases are thought to be of this type. CPE infections, on the other hand, are rare in Germany in both animals and human beings. Their main source in human beings is nosocomial transmission. Col-E, which bear mcr resistance genes, have been described in Germany mainly in food-producing animals and their meat. No representative data are available on Col-E in human beings in Germany; in Europe, the prevalence of colonization is less than 2%, with long-distance travel as a risk factor. The relevance of animals as a source of Col-E for human beings is not yet entirely clear.

Conclusion: Livestock farming and animal contact affect human colonization with the multiresistant Gram-negative pathogens CPE, ESBL-E and Col-E to differing extents. Improved prevention will require the joint efforts of human and veterinary medicine.
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http://dx.doi.org/10.3238/arztebl.m2021.0184DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8647294PMC
September 2021

Investigating Alkylated Prodigiosenes and Their Cu(II)-Dependent Biological Activity: Interactions with DNA, Antimicrobial and Photoinduced Anticancer Activity.

ChemMedChem 2021 Nov 14:e202100702. Epub 2021 Nov 14.

Institut für Chemie und Biochemie, Freie Universität Berlin, Fabeckstr. 34/36, 14195, Berlin, Germany.

Prodigiosenes are a family of red pigments with versatile biological activity. Their tripyrrolic core structure has been modified many times in order to manipulate the spectrum of activity. We have been looking systematically at prodigiosenes substituted at the C ring with alkyl chains of different lengths, in order to assess the relevance of this substituent in a context that has not been investigated before for these derivatives: Cu(II) complexation, DNA binding, self-activated DNA cleavage, photoinduced cytotoxicity and antimicrobial activity. Our results indicate that the hydrophobic substituent has a clear influence on the different aspects of their biological activity. The cytotoxicity study of the Cu(II) complexes of these prodigiosenes shows that they exhibit a strong cytotoxic effect towards the tested tumor cell lines. The Cu(II) complex of a prodigiosene lacking any alkyl chain excelled in its photoinduced anticancer activity, thus demonstrating the potential of prodigiosenes and their metal complexes for an application in photodynamic therapy (PDT). Two derivatives along with their Cu(II) complexes showed also antimicrobial activity against Staphylococcus aureus strains.
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http://dx.doi.org/10.1002/cmdc.202100702DOI Listing
November 2021

Outcomes with alemtuzumab induction therapy in lung transplantation: a comprehensive large-scale single-center analysis.

Transpl Int 2021 Dec 16;34(12):2633-2643. Epub 2021 Nov 16.

Department of Thoracic Surgery, Medical University of Vienna, Vienna, Austria.

Alemtuzumab is a monoclonal antibody targeting CD52, increasingly used as induction therapy after transplantation. The aim of this study was to analyze the outcomes of alemtuzumab induction therapy followed by a low-dose maintenance immunosuppression in a large single-center cohort of lung transplant recipients. All patients, who received alemtuzumab induction followed by a low-dose maintenance immunosuppression were included in the analysis. Short- and long-term outcomes were analyzed. 721 lung transplant recipients, transplanted between January 2008 and June 2019, were included in this retrospective study. Freedom from higher-grade ACR at 1, 5, and 10 years was 98%, 96%, and 96%, respectively. Thirty-nine patients (5%) developed clinical AMR. Twenty-one percent of patients developed high-grade CKD. A total of 1488 infections were recorded. Sixteen percent were diagnosed within the first 3 months. Sixty-two patients (9%) developed a malignancy during follow-up. Freedom from CLAD at 1, 5, and 10 years was 94%, 72%, and 53%, respectively. Overall survival rates at 1, 5, and 10 years were 85%, 71%, and 61%, respectively. Alemtuzumab induction combined with a low-dose tacrolimus protocol is safe and associated with low rates of acute and chronic rejection, as well as an excellent long-term survival.
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http://dx.doi.org/10.1111/tri.14153DOI Listing
December 2021

Outcomes with alemtuzumab induction therapy in lung transplantation: a comprehensive large-scale single-center analysis.

Transpl Int 2021 Dec 16;34(12):2633-2643. Epub 2021 Nov 16.

Department of Thoracic Surgery, Medical University of Vienna, Vienna, Austria.

Alemtuzumab is a monoclonal antibody targeting CD52, increasingly used as induction therapy after transplantation. The aim of this study was to analyze the outcomes of alemtuzumab induction therapy followed by a low-dose maintenance immunosuppression in a large single-center cohort of lung transplant recipients. All patients, who received alemtuzumab induction followed by a low-dose maintenance immunosuppression were included in the analysis. Short- and long-term outcomes were analyzed. 721 lung transplant recipients, transplanted between January 2008 and June 2019, were included in this retrospective study. Freedom from higher-grade ACR at 1, 5, and 10 years was 98%, 96%, and 96%, respectively. Thirty-nine patients (5%) developed clinical AMR. Twenty-one percent of patients developed high-grade CKD. A total of 1488 infections were recorded. Sixteen percent were diagnosed within the first 3 months. Sixty-two patients (9%) developed a malignancy during follow-up. Freedom from CLAD at 1, 5, and 10 years was 94%, 72%, and 53%, respectively. Overall survival rates at 1, 5, and 10 years were 85%, 71%, and 61%, respectively. Alemtuzumab induction combined with a low-dose tacrolimus protocol is safe and associated with low rates of acute and chronic rejection, as well as an excellent long-term survival.
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http://dx.doi.org/10.1111/tri.14153DOI Listing
December 2021

Emergence of bla carried by an IncX3 plasmid in Citrobacter freundii ST266 in China.

J Glob Antimicrob Resist 2021 12 27;27:250-252. Epub 2021 Oct 27.

State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin, 150069, China. Electronic address:

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http://dx.doi.org/10.1016/j.jgar.2021.10.016DOI Listing
December 2021

Dissection of Highly Prevalent -Carrying IncX Plasmid Types in Commensal from German Food and Livestock.

Antibiotics (Basel) 2021 Oct 12;10(10). Epub 2021 Oct 12.

Department Biological Safety, German Federal Institute for Risk Assessment (BfR), Max-Dohrn Str. 8-10, 10589 Berlin, Germany.

Plasmids are mobile genetic elements, contributing to the spread of resistance determinants by horizontal gene transfer. Plasmid-mediated quinolone resistances (PMQRs) are important determinants able to decrease the antimicrobial susceptibility of bacteria against fluoroquinolones and quinolones. The PMQR gene , especially, is broadly present in the livestock and food sector. Thus, it is of interest to understand the characteristics of plasmids able to carry and disseminate this determinant and therewith contribute to the resistance development against this class of high-priority, critically important antimicrobials. Therefore, we investigated all commensal (.) isolates, with reduced susceptibility to quinolones, recovered during the annual zoonosis monitoring 2017 in the pork and beef production chain in Germany (n = 2799). Through short-read whole-genome sequencing and bioinformatics analysis, the composition of the plasmids and factors involved in their occurrence were determined. We analysed the presence and structures of predominant plasmids carrying the PMQR . This gene was most frequently located on IncX plasmids. Although the harbouring these IncX plasmids were highly diverse in their sequence types as well as their phenotypic resistance profiles, the IncX plasmids-carrying the gene were rather conserved. Thus, we only detected three distinct IncX plasmids carrying in the investigated isolates. The IncX plasmids were assigned either to IncX1 or to IncX3. All -carrying IncX plasmids further harboured a β-lactamase gene (). In addition, all investigated IncX plasmids were transmissible. Overall, we found highly heterogenic harbouring conserved IncX plasmids as vehicles for the most prevalent gene . These IncX plasmids may play an important role in the dissemination of those two resistance determinants and their presence, transfer and co-selection properties require a deeper understanding for a thorough risk assessment.
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http://dx.doi.org/10.3390/antibiotics10101236DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8532951PMC
October 2021

Effect of topical antimicrobial therapy and household cleaning on meticillin-resistant Staphylococcus pseudintermedius carriage in dogs.

Vet Rec 2021 Sep 27:e937. Epub 2021 Sep 27.

Department of Clinical Services and Sciences, Royal Veterinary College, University of London, North Mymms, Hertfordshire, UK.

Background: Meticillin-resistant Staphylococcus pseudintermedius (MRSP) is a multidrug-resistant canine pathogen with a low zoonotic potential. This study investigated MRSP carriage and clearance through topical antimicrobial therapy and household cleaning in dogs recovered from MRSP infection.

Methods: Dogs were swabbed for MRSP carriage; household contamination was assessed using contact plates. Carrier dogs were allocated randomly to receive topical fusidic acid and chlorhexidine/miconazole treatment combined with owners implementing a household hygiene protocol (H&T) or implementation of hygiene alone (H) over three weeks. Carriage-negative dogs were monitored monthly. The relatedness of isolates over time was investigated by pulsed-field gel electrophoresis (PFGE).

Results: At inclusion, MRSP carriage was confirmed in 31/46 (67.4%) index dogs and 16/24 (66.7%) contact dogs, and contamination was found in 18/40 (45%) environments. In dogs completing all cycles, interventions cleared carriage in 5/9 (55.6%) dogs in group H&T and 2/6 (33.3%) in group H. Environmental contamination was infrequent but associated with carrier dogs (p = 0.047). Monthly monitoring of initially negative dogs showed intermittent carriage in 9/14 dogs. PFGE-concordance was found among all 34 MRSP isolated from eight index dogs over time.

Conclusion: MRSP carriage was common in dogs after recovery from infection. Topical antimicrobial therapy temporarily eliminated carriage but recurrence was frequent. Management efforts must include the prevention of recurrent infections and hygiene.
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http://dx.doi.org/10.1002/vetr.937DOI Listing
September 2021

Provisional Use of CLSI-Approved Quality Control Strains for Antimicrobial Susceptibility Testing of () .

Microorganisms 2021 Aug 28;9(9). Epub 2021 Aug 28.

Department of Veterinary Medicine, Institute of Microbiology and Epizootics, Freie Universität Berlin, 14163 Berlin, Germany.

Antimicrobial susceptibility testing (AST) should be conducted in a standardized manner prior to the start of an antimicrobial treatment. For fastidious bacteria, such as porcine () spp., specifically , neither guidelines or standards for the performance of AST, nor quality control strains for the validation of AST results are approved by organizations like the Clinical and Laboratory Standards Institute (CLSI) or the European Committee on Antimicrobial Susceptibility Testing (EUCAST). The CLSI- and EUCAST-approved quality control strains ATCC 29212 and ATCC 29213 were chosen to validate AST by broth microdilution using modified Friis broth, developed as growth medium for porcine () spp. The antimicrobial agents doxycycline, enrofloxacin, erythromycin, florfenicol, gentamicin, marbofloxacin, tetracycline, tiamulin, tilmicosin, tulathromycin, and tylosin were examined using customized Sensititre microtiter plates. Minimal inhibitory concentrations, determined after 24, 48, and 72 h, were mostly within the CLSI-approved quality control ranges for defined antimicrobial agents. We propose the use of the combination of ATCC 29212 and ATCC 29213 as surrogate quality control strains for the validation of future AST results obtained for by broth microdilution using modified Friis broth.
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http://dx.doi.org/10.3390/microorganisms9091829DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8466829PMC
August 2021

The First Report of -Carrying Originating from Animals in Serbia.

Antibiotics (Basel) 2021 Sep 3;10(9). Epub 2021 Sep 3.

Institute of Microbiology, University of Veterinary Medicine, 1010 Vienna, Austria.

The aim of this study was continuous monitoring of the presence of to genes in isolated from cattle, pigs, and domestic poultry at intensive breeding facilities in Northern Vojvodina, Serbia, from 1 January 1 to 1 October 2020. Out of 2167 examined samples, was observed in five isolates originating from healthy turkeys. Four isolates belonged to the phylogenetic group B1, and one isolate to the phylogenetic group A. Detected serogenotypes (somatic O and flagellar H antigens) were O8:H25 and O29:H25. Core-genome multi-locus sequence typing (cgMLST) revealed three ST58 isolates clustering together in Clonal Complex (CC) 155 and two singletons of ST641-CC86 and ST410-CC23, respectively. Clonotyping revealed CH4-32 ( = 3), CH6-53 ( = 1) and CH4-24 ( = 1). In all isolates, the gene was located on a large IncX4 replicon type plasmid. Eight virulence-associated genes (VAGs) typical of avian pathogenic (APEC) (, , , , , , ) were detected in four isolates. These isolates were investigated for susceptibility to four biocides and revealed MIC values of 0.125% for glutardialdehyde, of 0.00003-0.00006% for chlorohexidine, of 4-6% for isopropanol and of 0.001-0.002% for benzalkonium chloride. All obtained MIC values of the tested biocides were comparable to the reference strain, with no indication of possible resistance. This is the first report of -carrying from Serbia. Although only samples from turkeys were -positive in this study, continuous monitoring of livestock samples is advised to prevent a spill-over from animals to humans.
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http://dx.doi.org/10.3390/antibiotics10091063DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8467794PMC
September 2021

A New Tool to Assess Quality of Life in Patients with Idiopathic Pulmonary Fibrosis or Non-specific Interstitial Pneumonia.

Pneumologie 2021 Sep 14. Epub 2021 Sep 14.

Center for interstitial and rare lung diseases, Pneumology, Thoraxklinik, University of Heidelberg and German Center for Lung ResearchHeidelberg, Germany.

Background:  Quality of life (QoL) is significantly impaired in patients with pulmonary fibrosis, however reliable tools to assess QoL issues specific for this group of patients are still missing. We thus aimed to develop a new questionnaire called "Quality of life in patients with idiopathic pulmonary fibrosis" (QPF) to measure QoL in patients with fibrotic idiopathic interstitial pneumonias (IIP).

Methods:  An item pool was created on the basis of a German expert group with support of patients suffering from pulmonary fibrosis. In a 1st step, this version of the questionnaire was completed by 52 patients with idiopathic pulmonary fibrosis (IPF) or non-specific interstitial pneumonia (NSIP). Following this, an item- and an exploratory factor analysis was carried out and a 2nd version created. In a multicenter validation study in a one-group pre-post design, the questionnaire was filled in by 200 patients with IIP (IPF = 190, iNSIP = 10) at 2 time points with an interval of 6 months. Cross-validation was carried out with the St. Georges Respiratory Questionnaire (SGRQ).

Results:  The mean age of the patients was 71.0 years (50-90 years), 82.5 % were male. Item analysis revealed that most of Cronbach alpha and selectivity values of QPF-scales could be considered as sufficient (e. g. QPF-scale "condition" [alpha = 0.827], "impairment" [alpha = 0.882]). At scale level, there were significant differences in terms of a deterioration or improvement in the QPF-condition and QPF-breathlessness scales and also in the SGRQ-activity scale. Analysis of construct validation of QPF and SGRQ showed moderate correlations between both questionnaires. A deterioration in health status from the patient's and doctor's perspective was seen in the scales "impairment", "shortness of breath" and "health status" of the QPF. The QPF was able to detect a change in the patient's mood ("condition" scale) in the course of treatment.

Conclusion:  This newly developed questionnaire maps the special needs of the patients well. The QPF is suitable for screening of quality of life as well as for supplementing the medical history and for monitoring the course of disease in fibrotic IIPs.
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http://dx.doi.org/10.1055/a-1579-7618DOI Listing
September 2021

Emergence of a (M) Variant Conferring Resistance to Tigecycline in .

Front Vet Sci 2021 19;8:709327. Epub 2021 Aug 19.

College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China.

The aim of this study was to gain insight into the resistance determinants conferring resistance to tigecycline in (.) and to investigate the genetic elements involved in their horizontal transfer. A total of 31 tetracycline-resistant isolates were screened for tigecycline resistance by broth microdilution. isolate SC128 was subjected to whole genome sequencing with particular reference to resistance determinants involved in tigecycline resistance. Transferability of genomic island (GI) GISC128 was investigated by transformation. The roles of (L) or (M) in contributing to tigecycline resistance in were confirmed by transformation using different (L)- or (M)-carrying constructs. Only SC128 showed a tigecycline resistance phenotype. A (L)-(M) and co-carrying GISC128 was identified in this isolate. After transfer of the novel GI into a susceptible recipient, this recipient showed the same tigecycline resistance phenotype. Further transfer experiments with specific (L)- or (M)-carrying constructs confirmed that only (M), but not (L), contributes to resistance to tigecycline. Protein sequence analysis identified a Tet(M) variant, which is responsible for tigecycline resistance in SC128. It displayed 94.8% amino acid identity with the reference Tet(M) of DO plasmid 1. To the best of our knowledge, this is the first time that a (M) variant conferring resistance to tigecycline was identified in . Its location on a GI will accelerate its transmission among the population.
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http://dx.doi.org/10.3389/fvets.2021.709327DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8417041PMC
August 2021

Detection of a NDM-5-producing Klebsiella pneumoniae sequence type 340 (CG258) high-risk clone in swine.

Vet Microbiol 2021 Nov 30;262:109218. Epub 2021 Aug 30.

College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, 450046, PR China. Electronic address:

The emergence and rapid increase of carbapenem-resistant Enterobacteriaceae among food-producing animals poses a serious threat to public health. The aim of this study was to investigate the presence and dissemination of bla in porcine Klebsiella pneumoniae isolates. Of 19 meropenem-resistant K. pneumoniae isolates, 18 were bla-positive and one carried bla. Susceptibility testing indicated that all bla-carrying K. pneumoniae showed a multiple drug resistance (MDR) profile. The bla gene was located on a conjugative IncX3 plasmid of ∼46-kb in all 18 bla-carrying isolates. MLST analysis revealed that ST340 (n = 8), a member of the worldwide existing high-risk epidemic clonal group 258 (CG258), was predominant. Furthermore, whole genome sequence (WGS) analysis for one representative ST340 K. pneumoniae Kp19110124 showed a MDR profile for a wide range of antimicrobial agents, including meropenem, various cephalosporins, azteonam, gentamicin, ciprofloxacin, and florfenicol. Phylogenetic analysis exhibited that K. pneumoniae ST340 strains were clustered into one branch, which had spread across host species and across continents. Among them, K. pneumoniae Kp19110124 displayed a very close relationship with a clinical isolate collected from a patient in Canada. In conclusion, these results reveal the presence of a bla-carrying conjugative IncX3 type plasmid into K. pneumoniae ST340 clone, which then may accelerate the dissemination of the bla gene in porcine K. pneumoniae isolates. The detection of high-risk bla-carrying K. pneumoniae ST340 in food-producing animal poses a serious threat to public health.
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http://dx.doi.org/10.1016/j.vetmic.2021.109218DOI Listing
November 2021

The Pheno- and Genotypic Characterization of Porcine Isolates.

Microorganisms 2021 Aug 6;9(8). Epub 2021 Aug 6.

Institute of Microbiology, University of Veterinary Medicine, 1210 Vienna, Austria.

() is the main causative pathogen of neonatal and post-weaning diarrhea and edema disease in swine production. There is a significant health concern due to an increasing number of human infections associated with food and/or environmental-borne pathogenic and multidrug-resistant worldwide. Monitoring the presence of pathogenic and antimicrobial-resistant isolates is essential for sustainable disease management in livestock and human medicine. A total of 102 isolates of diseased pigs were characterized by antimicrobial and biocide susceptibility testing. Antimicrobial resistance genes, including mobile colistin resistance genes, were analyzed by PCR and DNA sequencing. The quinolone resistance-determining regions of and in ciprofloxacin-resistant isolates were analyzed. Clonal relatedness was investigated by two-locus sequence typing (CH clonotyping). Phylotyping was performed by the Clermont multiplex PCR method. Virulence determinants were analyzed by customized DNA-based microarray technology developed in this study for fast and economic molecular multiplex typing. Thirty-five isolates were selected for whole-genome sequence-based analysis. Most isolates were resistant to ampicillin and tetracycline. Twenty-one isolates displayed an ESBL phenotype and one isolate an AmpC β-lactamase-producing phenotype. Three isolates had elevated colistin minimal inhibitory concentrations and carried the gene. Thirty-seven isolates displayed a multi-drug resistance phenotype. The most predominant β-lactamase gene classes were (56%) and (13.71%). Mutations in QRDR were observed in 14 ciprofloxacin-resistant isolates. CH clonotyping divided all isolates into 51 CH clonotypes. The majority of isolates belonged to phylogroup A. Sixty-four isolates could be assigned to defined pathotypes wherefrom UPEC was predominant. WGS revealed that the most predominant sequence type was ST100, followed by ST10. ST131 was detected twice in our analysis. This study highlights the importance of monitoring antimicrobial resistance and virulence properties of porcine isolates. This can be achieved by applying reliable, fast, economic and easy to perform technologies such as DNA-based microarray typing. The presence of high-risk pathogenic multi-drug resistant zoonotic clones, as well as those that are resistant to critically important antibiotics for humans, can pose a risk to public health. Improved protocols may be developed in swine farms for preventing infections, as well as the maintenance and distribution of the causative isolates.
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http://dx.doi.org/10.3390/microorganisms9081676DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8400056PMC
August 2021

Identification of a Streptococcus parasuis isolate co-harbouring the oxazolidinone resistance genes cfr(D) and optrA.

J Antimicrob Chemother 2021 10;76(11):3059-3061

State Key Laboratory of Veterinary Biotechnology, Harbin Veterinary Research Institute, Chinese Academy of Agricultural Sciences, Harbin 150069, China.

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http://dx.doi.org/10.1093/jac/dkab297DOI Listing
October 2021

Animal and Human Brucellosis in Pakistan.

Front Public Health 2021 30;9:660508. Epub 2021 Jul 30.

Institute of Microbiology and Epizootics, Freie Universität Berlin, Berlin, Germany.

Brucellosis is a bacterial zoonotic disease that affects many animal species and can be transmitted to humans direct contact or contaminated food. Although brucellosis is a serious health hazard, its public health concern has been neglected in many countries. In some developing countries, such as Pakistan, where brucellosis is endemic, this disease continues to be of importance. A literature search for the past 11 years (2011-2021) provided a comprehensive insight into brucellosis in Pakistan. In this review, particular emphasis was placed on occurrence, diagnostic tests used, and prevention, treatment, and control in the context of the "One Health" approach.
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http://dx.doi.org/10.3389/fpubh.2021.660508DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8362930PMC
August 2021

Lung transplantation for acute respiratory distress syndrome: A multicenter experience.

Am J Transplant 2022 Jan 24;22(1):144-153. Epub 2021 Jul 24.

Department of Thoracic Surgery, Medical University of Vienna, Vienna, Austria.

Acute respiratory distress syndrome (ARDS) is a rapidly progressive lung disease with a high mortality rate. Although lung transplantation (LTx) is a well-established treatment for a variety of chronic pulmonary diseases, LTx for acute lung failure (due to ARDS) remains controversial. We reviewed posttransplant outcome of ARDS patients from three high-volume European transplant centers. Demographics and clinical data were collected and analyzed. Viral infection was the main reason for ARDS (n = 7/13, 53.8%). All patients were admitted to ICU and required mechanical ventilation, 11/13 were supported with ECMO at the time of listing. They were granted a median LAS of 76 (IQR 50-85) and waited for a median of 3 days (IQR 1.5-14). Postoperatively, median length of mechanical ventilation was 33 days (IQR 17-52.5), median length of ICU and hospital stay were 39 days (IQR 19.5-58.5) and 54 days (IQR 43.5-127). Prolongation of peripheral postoperative ECMO was required in 7/13 (53.8%) patients with a median duration of 2 days (IQR 2-7). 30-day mortality was 7.7%, 1 and 5-year survival rates were calculated as 71.6% and 54.2%, respectively. Given the lack of alternative treatment options, the herein presented results support the concept of offering live-saving LTx to carefully selected ARDS patients.
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http://dx.doi.org/10.1111/ajt.16759DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8441742PMC
January 2022

Multi-omics profiling predicts allograft function after lung transplantation.

Eur Respir J 2021 Jul 8. Epub 2021 Jul 8.

Research Laboratory of Infection Biology, Department of Medicine I, Medical University of Vienna, Vienna, Austria.

Rationale: Lung transplantation is the ultimate treatment option for patients with end-stage respiratory diseases but bears the highest mortality rate among all solid organ transplantations due to chronic lung allograft dysfunction (CLAD). The mechanisms leading to CLAD remain elusive due to insufficient understanding of the complex post-transplant adaptation processes.

Objectives: To better understand these lung adaptation processes after transplantation, and to investigate their association with future changes in allograft function.

Methods: We performed an exploratory cohort study in 78 patients on bronchoalveolar lavage samples from lung donors and recipients. We analysed the alveolar microbiome using 16S rRNA sequencing, the cellular composition using flow-cytometry, as well as metabolome and lipidome profiling.

Measurements And Main Results: We established distinct temporal dynamics for each of the analysed data sets. Comparing matched donor and recipient samples, we revealed that recipient-specific as well as environmental factors, rather than the donor microbiome, shape the long-term lung microbiome. We further discovered that the abundance of certain bacterial strains correlated with underlying lung diseases even after transplantation. A decline in forced expiratory volume during the first second (FEV1) is a major characteristic of lung allograft dysfunction in transplant recipients. By using a machine learning approach, we could accurately predict future changes in FEV1 from our multi-omics data, whereby microbial profiles showed a particularly high predictive power.

Conclusion: Bronchoalveolar microbiome, cellular composition, metabolome and lipidome show specific temporal dynamics after lung transplantation. The lung microbiome can predict future changes in lung function with high precision.
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http://dx.doi.org/10.1183/13993003.03292-2020DOI Listing
July 2021

Comparative analysis of genomic characteristics, fitness and virulence of MRSA ST398 and ST9 isolated from China and Germany.

Emerg Microbes Infect 2021 Dec;10(1):1481-1494

Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People's Republic of China.

Methicillin-resistant (MRSA) of sequence types ST398 and ST9 are dominant lineages among livestock in Europe and Asia, respectively. Although both STs were commonly found as colonizers of the skin and the mucosal membranes, MRSA ST398, rather than MRSA ST9, has been reported to cause infections in humans and animals. Herein, we comparatively analyzed the genomic characteristics, fitness and virulence of MRSA ST398 and ST9 isolated from pigs in both China (CHN) and Germany (GER) to explore the factors that lead to differences in their epidemics and pathogenicity. We observed that the CHN-MRSA ST9 and the GER-MRSA ST9 have evolved independently, whereas the CHN-MRSA ST398 and GER-MRSA ST398 had close evolutionary relationships. Resistance to antimicrobial agents commonly used in livestock, the enhanced ability of biofilm formation, and the resistance to desiccation contribute to the success of the dominant clones of CHN-MRSA ST9 and GER-MRSA ST398, and the gene on the genomic island might in part contribute to their colonization fitness in pigs. All MRSA ST398 strains revealed more diverse genome structures, higher tolerance to acids and high osmotic pressure, and greater competitive fitness in co-culture experiments. Notably, we identified and characterized a novel gene, which was located on the genomic island νSaβ of MRSA ST398 but was absent in MRSA ST9. The enhanced pathogenicity of the MRSA ST398 strains due to might in part explain why MRSA ST398 strains are more likely to cause infections.
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http://dx.doi.org/10.1080/22221751.2021.1951125DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8300935PMC
December 2021

Phenotypic and Genotypic Properties of Fluoroquinolone-Resistant, -Carrying Isolated from the German Food Chain in 2017.

Microorganisms 2021 Jun 16;9(6). Epub 2021 Jun 16.

German Federal Institute for Risk Assessment (BfR), Max-Dohrn Str. 8-10, 10589 Berlin, Germany.

Fluoroquinolones are the highest priority, critically important antimicrobial agents. Resistance development can occur via different mechanisms, with plasmid-mediated quinolone resistance (PMQR) being prevalent in the livestock and food area. Especially, genes, commonly located on mobile genetic elements, are major drivers for the spread of resistance determinants against fluoroquinolones. We investigated the prevalence and characteristics of -positive obtained from different monitoring programs in Germany in 2017. Furthermore, we aimed to evaluate commonalities of -carrying plasmids in . We found to be broadly spread over different livestock and food matrices, and to be present in various sequence types. The -positive isolates were predominantly detected within selectively isolated ESBL (extended spectrum beta-lactamase)-producing , leading to a frequent association with other resistance genes, especially cephalosporin determinants. Furthermore, we found that correlates with the presence of genes involved in resistance development against quaternary ammonium compounds (). The detection of additional point mutations in many isolates within the chromosomal QRDR region led to even higher MIC values against fluoroquinolones for the investigated . All of these attributes should be carefully taken into account in the risk assessment of -carrying from livestock and food.
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http://dx.doi.org/10.3390/microorganisms9061308DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8233838PMC
June 2021

Identification of Tn553, a novel Tn554-related transposon that carries a complete blaZ-blaR1-blaI β-lactamase operon in Staphylococcus aureus.

J Antimicrob Chemother 2021 09;76(10):2733-2735

Institute of Microbiology and Epizootics, Centre for Infection Medicine, Department of Veterinary Medicine, Freie Universität Berlin, Berlin, Germany.

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http://dx.doi.org/10.1093/jac/dkab210DOI Listing
September 2021

[Validity of the "Structured Inventory of Malingered Symptomatology" [SIMS] in the Assessment of Healthy Individuals and Patients with Psychiatric Disorders Outside the Forensic Context].

Fortschr Neurol Psychiatr 2021 Jun 11. Epub 2021 Jun 11.

Forensische Psychiatrie, Zentralinstitut für Seelische Gesundheit, Mannheim, Germany.

Objective: Assessment of the rate of false-positive results of the Structured Inventory of Malingered Symptomatology (SIMS) in healthy controls and authentic patients outside the forensic or rehabilitative context.

Methods: Beyond the SIMS scores, further variables (PANSS, Hamilton scale, MMSE) were obtained. SIMS scores of healthy individuals were compared with the SIMS scores of the different groups of patients. Additionally, correlations between the SIMS scores and other variables were investigated.

Results: Patients with psychotic disorders (n=30) or depressive episodes (n=32) more frequently achieved SIMS scores >16 as compared to healthy controls. In comparison, patients with amnestic disorders (n=15) had inconspicuous SIMS scores. Depressed patients with positive SIMS results were significantly more likely to be diagnosed with another psychiatric disorder and the scores of these patients on the Hamilton scale were correlated with positive results on 2 subscales of the SIMS (NI, AF).

Conclusion: If this instrument is to applied in clinical practice in the future, further validation of the SIMS is necessary. The specificity of the SIMS seems to be context-related.
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http://dx.doi.org/10.1055/a-1493-2782DOI Listing
June 2021

Oblique Carinal End-to-End-Anastomosis for Pig Bronchus in Organ Donor and Lung Transplant Recipient.

Ann Thorac Surg 2021 Jun 5. Epub 2021 Jun 5.

Department of Thoracic Surgery, Medical University of Vienna, Vienna, Austria. Electronic address:

Pig bronchi are rare anomalies, in which the right upper lobe bronchus originates above the carina. During surgery, this can lead to technical challenges associated with the bronchial anastomosis, especially during lung transplantation. We herein report the case of a combined liver-lung transplantation with a pig bronchus in both, the organ donor and the transplant recipient. In both cases the bronchi originated slightly above the level of the carina facilitating an oblique resection and a single tracheobronchial anastomosis with a running suture. Follow-up bronchoscopy showed a completely healed anastomosis with no evidence of malacia or stenosis.
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http://dx.doi.org/10.1016/j.athoracsur.2021.05.029DOI Listing
June 2021

Mobile Oxazolidinone Resistance Genes in Gram-Positive and Gram-Negative Bacteria.

Clin Microbiol Rev 2021 06 2;34(3):e0018820. Epub 2021 Jun 2.

Beijing Key Laboratory of Detection Technology for Animal-Derived Food Safety, College of Veterinary Medicine, China Agricultural University, Beijing, People's Republic of China.

Seven mobile oxazolidinone resistance genes, including , (B), (C), (D), (E), , and , have been identified to date. The genes code for 23S rRNA methylases, which confer a multiresistance phenotype that includes resistance to phenicols, lincosamides, oxazolidinones, pleuromutilins, and streptogramin A compounds. The and genes code for ABC-F proteins that protect the bacterial ribosomes from the inhibitory effects of oxazolidinones. The gene confers resistance to oxazolidinones and phenicols, while the gene confers elevated MICs or resistance to oxazolidinones, phenicols, and tetracycline. These oxazolidinone resistance genes are most frequently found on plasmids, but they are also located on transposons, integrative and conjugative elements (ICEs), genomic islands, and prophages. In these mobile genetic elements (MGEs), insertion sequences (IS) most often flanked the , , and genes and were able to generate translocatable units (TUs) that comprise the oxazolidinone resistance genes and occasionally also other genes. MGEs and TUs play an important role in the dissemination of oxazolidinone resistance genes across strain, species, and genus boundaries. Most frequently, these MGEs also harbor genes that mediate resistance not only to antimicrobial agents of other classes, but also to metals and biocides. Direct selection pressure by the use of antimicrobial agents to which the oxazolidinone resistance genes confer resistance, but also indirect selection pressure by the use of antimicrobial agents, metals, or biocides (the respective resistance genes against which are colocated on -, -, or -carrying MGEs) may play a role in the coselection and persistence of oxazolidinone resistance genes.
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http://dx.doi.org/10.1128/CMR.00188-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262807PMC
June 2021

Presence of β-Lactamase-producing Enterobacterales and Isolates in Marine Mammals.

Int J Mol Sci 2021 May 31;22(11). Epub 2021 May 31.

Institute of Microbiology, University of Veterinary Medicine, 1210 Vienna, Austria.

Marine mammals have been described as sentinels of the health of marine ecosystems. Therefore, the aim of this study was to investigate (i) the presence of extended-spectrum β-lactamase (ESBL)- and AmpC-producing Enterobacterales, which comprise several bacterial families important to the healthcare sector, as well as (ii) the presence of in these coastal animals. The antimicrobial resistance pheno- and genotypes, as well as biocide susceptibility of Enterobacterales isolated from stranded marine mammals, were determined prior to their rehabilitation. All isolates ( = 27) were screened for virulence genes via DNA-based microarray, and twelve selected isolates were analyzed by whole-genome sequencing. Seventy-one percent of the Enterobacterales isolates exhibited a multidrug-resistant (MDR) pheno- and genotype. The gene ( = 51) was the predominant β-lactamase gene. In addition, ( = 38), ( = 8), ( = 7), ( = 7), ( = 3), and ( = 2) were detected. The most prevalent non-β-lactamase genes were ( = 38), ( = 34), ( = 34), and (A) ( = 34). isolates belonging to the pandemic sequence types (STs) ST38, ST167, and ST648 were identified. Among isolates ( = 18), . Havana was the most prevalent serotype. The present study revealed a high prevalence of MDR bacteria and the presence of pandemic high-risk clones, both of which are indicators of anthropogenic antimicrobial pollution, in marine mammals.
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http://dx.doi.org/10.3390/ijms22115905DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8199236PMC
May 2021

Isolation Procedure for CP from Caeca Samples under Review towards an Increased Sensitivity.

Microorganisms 2021 May 20;9(5). Epub 2021 May 20.

German Federal Institute for Risk Assessment (Bundesinstitut für Risikobewertung), D-10589 Berlin, Germany.

Due to the increasing reports of carbapenemase-producing Enterobacteriaceae (CPE) from livestock in recent years, the European Reference Laboratory for Antimicrobial Resistances (EURL-AR) provided a protocol for their recovery from caecum and meat samples. This procedure exhibited limitations for the detection of CPE with low carbapenem MIC values. Therefore, it was modified by a second, selective enrichment in lysogeny broth with cefotaxime (CTX 1 mg/L) and with meropenem (MEM 0.125 mg/L) at 37 °C under microaerophilic conditions. By Real-time PCR, these enrichments are pre-screened for the most common carbapenemase genes. Another adaptation was the use of in-house prepared MacConkey agar with MEM and MEM+CTX instead of commercial selective agar. According to the EURL-method, we achieved 100% sensitivity and specificity using the in-house media instead of commercial agar, which decreased the sensitivity to ~75%. Comparing the method with and without the second enrichment, no substantial influence on sensitivity and specificity was detected. Nevertheless, this enrichment has simplified the CPE-isolation regarding the accompanying microbiota and the separation of putative colonies. In conclusion, the sensitivity of the method can be increased with slight modifications.
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http://dx.doi.org/10.3390/microorganisms9051105DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8161246PMC
May 2021
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