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Acinetobacter Baumannii – a Neglected Pathogen in Veterinary and Environmental Health in Germany

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Acinetobacter Baumannii – a Neglected Pathogen in Veterinary and Environmental Health in Germany Veterinary Research Communications (2019) 43:1–6 https://doi.org/10.1007/s11259-018-9742-0 REVIEW ARTICLE Acinetobacter baumannii – a neglected pathogen in veterinary and environmental health in Germany Gamal Wareth1 & Heinrich Neubauer1 & Lisa D. Sprague1 Received: 25 October 2018 /Accepted: 6 December 2018 /Published online: 27 December 2018 # The Author(s) 2018 Abstract The emergence and global spread of drug resistant Acinetobacter (A.) baumannii is a cause of great concern. The current knowledge on antibiotic resistance in A. baumannii from animal origin is mostly based on few internationally published case reports, investigations of strain collections and several whole genome analyses. This lack of data results in a somewhat sketchy picture on how to assess the possible impact of drug resistant A. baumannii strains on veterinary and public health in Germany. Consequently, there is an urgent need to intensify the surveillance of A. baumannii in pet animals, the farm animal population and wildlife. Keywords Acinetobacter baumannii . Review . Antibiotic resistance . Germany Introduction limited number of widespread clones appear to be responsible for hospital outbreaks in many countries (Diancourt et al. Acinetobacter (A.) baumannii is a gram-negative opportunis- 2010). Eight international clonal lineages have been described tic nosocomial pathogen belonging to the genus Acinetobacter so far and comparative typing of outbreak strains obtained all and a member of the family Moraxellaceae. Acinetobacter over Europe revealed the dominance of three clones, original- spp. are non-motile, non-fastidious Gram-negative, non- ly named European clones I-III (Dijkshoorn et al. 1996; Karah fermenting, catalase positive, oxidase negative, strictly aero- et al. 2012). These clones were re-named Binternational clones bic coccobacilli with a DNA G + C content between 39 and (IC) 1-3^ after identifying them throughout the world. IC 1–3 47% (Peleg et al. 2008). Currently, there are 57 validly pub- correspond to the multi-locus sequence typing (MLST) clonal lished species names (including 4 synonymous species) (Parte complexes (ST1–3) (Diancourt et al. 2010; Antunes et al. 2018). Of these, the species A. baumannii, A. nosocomialis 2014). and A. pittii are of clinical importance, as they have been In humans, A. baumannii can cause a multitude of severe isolated from human infections and hospital outbreaks nosocomial infections of the skin and soft tissue, wound in- (Visca et al. 2011). According to Bergogne-Bérézin and fections, urinary tract infections and secondary meningitis. Towner (1996) the first reports on severe infections most like- The highest mortality rates however, are seen in ventilator- ly caused by A. baumannii date back to the 1970ies. However, associated pneumonia and bloodstream infections due to the numerous taxonomic changes the genus (Dijkshoorn et al. 2007). In comparison to human medicine, Acinetobacter has been subjected to, these earlier reports have the data obtained from veterinary medicine are relatively lim- to be regarded with caution as the species A. baumannii was ited (Müller et al. 2014; van der Kolk et al. 2018). In livestock formally just designated in 1986 by Bouvet and Grimont. (cattle, pig), A. baumannii has been observed as a cause of Strain typing by different techniques has revealed genotyp- mastitis, pneumonia, and sepsis. Horses have been reported to ic diversity within the species A. baumannii,however,onlya develop wound infections, septicaemia, and bronchopneumo- nia as well as neonatal encephalopathy and eye infections. In dogs and cats A. baumannii hasbeenisolatedfromwound, * Lisa D. Sprague bloodstream and urinary tract infections (Müller et al. 2014; [email protected] van der Kolk et al. 2018). The genus Acinetobacter has the tendency to develop anti- 1 Institut für bakterielle Infektionen und Zoonosen, Friedrich-Loeffler-Institut, Jena, Germany biotic resistance very rapidly, possibly due to its long-term 2 Vet Res Commun (2019) 43:1–6 evolutionary exposure to antibiotic-producing organisms in The aim of this short review is to summarise the current the soil environment (Bergogne-Bérézin and Towner 1996). knowledge and data on antimicrobial resistance determined in Moreover, a major feature of A. baumannii, enabling its A. baumannii strains isolated from animal and environmental prolonged survival and spread within the healthcare system, sources in Germany. is its ability to not only upregulate intrinsic but also to acquire foreign mechanisms of antimicrobial resistance (Pogue et al. 2013). The European Committee on Antimicrobial Antimicrobial resistance in A. baumannii Susceptibility Testing (EUCAST) expert rules V 3.1 state that originating from animal hosts A. baumannii is naturally (or intrinsically) resistant to the fol- lowing antimicrobials: ampicillin, amoxicillin-clavulanic ac- To date, only few reports exist on the prevalence of antibiotic id, cefazolin, cefalothin, cephalexin, cefadroxil, cefotaxime, resistance in A. baumannii isolated from animal origin in ceftriaxone, aztreonam, ertapenem, trimethoprim and Germany (Table 1). The earliest study on multidrug resistant fosfomycin. It is still a matter of debate as to whether the Acinetobacter spp. in Germany analysed 52 A. baumannii,3 augmented antimicrobial resistance found in clinical A. pittii strains and one non defined Acinetobacter isolate Acinetobacter baumannii isolates may also lead to reduced from hospitalised animals (dog, cat, horse, cow) collected be- susceptibility to disinfectants. While Ivancovic et al. (2017), tween 2000 and 2008. The isolates could be allocated to the Babaei et al. (2015) and Kawamura-Sato et al. (2010)were international clones 1, 2 and 3, respectively, and were resistant able to demonstrate reduced susceptibility to disinfectants, no to oxacillin, penicillin, cephaloitin, erythromycin, correlation was found by Martro et al. (2003). clindamycin, chloramphenicol, and, with the exception of A wide array of resistance mechanisms have been described two isolates, to colistin. Bar of one isolate, all strains were for A. baumannii such as ß-lactamases, outer membrane proteins sensitive to imipenem and amikacin, respectively. This study (OMPs), efflux influencing proteins, aminoglycoside modifying also revealed the possible endemic occurrence of enzymes, chromosomal mutations in the quinolone resistance Acinetobacter spp. within an animal clinic (Zordan et al. determining region (QRDR), enzymes targeting tetracycline- 2011). specific efflux, glycocyclines as well as ribosomal methylation The first description and genome sequence of a (Peleg et al. 2008; Evans et al. 2013). A particular challenge is carbapenem-resistant A. baumannii strain isolated in 2000 the resistance to carbapenems, which is predominantly mediated and originating from a cat was in 2016 by Ewers and co- by Ambler Class D ß-lactamases, such as the intrinsic workers. Phylogenetic analyses revealed that the isolate carbapenem-hydrolysing oxacillinase OXA-51, which confers belonged to the globally distributed international clone IC1 resistance to carbapenems when overexpressed or the acquisition and displayed a close resemblance to clonal lineages causing and production of the oxacillinases OXA-23-like, OXA-24/40- severe infections in humans. The strain harboured a plasmid like, OXA-58-like, OXA-143-like and OXA-235-like (da Silva encoding for blaoxa-23; other resistance coding genes detected et al. 2016). Their corresponding genes can be upregulated by in the genome were aminoglycoside resistance genes, blaoxa- insertion sequences (IS) located upstream of these genes, e.g. 51-like gene encoding OXA-69, a phenicol resitance gene ISAba-1. Metallo-ß-lactamases such as imipemenase (IMP), (catA1), a sulfonamide (sul1) and a tetracycline (tetA) resis- Verona integrin-encoded-metallo-ß-lactamase (VIM) and New tance coding gene, respectively. High MIC breakpoints were Delhi metallo-ß-lactamase (NDM) have been reported in determined for imipenem, piperacillin, cefpirome, Europe but currently appear to play a minor role (Evans et al. gentamycin, tetracycline and trimethoprim/sulfamethoxazole 2013). The production of K. pneumoniae carbapenemase (KPC) (Ewers et al. 2016). A later study by the same group screened and OXA-48 oxacillinase has been reported from the Middle 223 A. baumannii isolates collected between 2000 and 2013 East and South America, respectively (Elsherif et al. 2016; from companion animals (dog, cat, rabbit, ferret, snake, rat, Martinez et al. 2016). duck) for carbapenem-non-susceptibility testing (Ewers et al. The emergence of drug resistant Acinetobacter spp., espe- 2017). Fifty-eight isolates carried blaoxa-66 with the upstream cially A. baumannii in hospitals, but also in veterinary clinics insertion sequence element ISAba1; further three isolates (cat; and the environment has been observed throughout the world dogs) harboured blaoxa-23, belonged to the IC 1 and 8, respec- and has become a cause of concern (Dijkshoorn et al. 2007; tively, and were resistant to piperacillin, piperacillin/tazobac- Diancourt et al. 2010;Mülleretal.2014;vanderKolketal. tam, ampicillin/sulbactam, ceftazidime, cefuroxime, 2018). Severe nosocomial infections are recurrently associat- cefpodoxime, imipenem, meropenem and trimethoprim/ ed with epidemic spread, outbreak strains are frequently multi- sulphametazole. All three isolates carried the drug resistant (MDR) and the increasing occurrence of strains aminoglycoside-modifying enzyme gene aadA1,
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