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Taxonomy, Virulence Genes and Antimicrobial Resistance Of Zhou et al. BMC Infectious Diseases (2019) 19:158 https://doi.org/10.1186/s12879-019-3766-0 RESEARCH ARTICLE Open Access Taxonomy, virulence genes and antimicrobial resistance of Aeromonas isolated from extra-intestinal and intestinal infections Yanyan Zhou1 ,LiYu2, Zheng Nan1, Pingping Zhang1, Biao Kan3, Donghui Yan1* and Jianrong Su1* Abstract Background: Clinical characteristics (taxonomy, virulence genes and antimicrobial resistance ) of Aeromonas in isolated from extra-intestinal and intestinal infections were investigated to describe epidemiology, associated virulence factors and optimal therapy options. Methods: Clinical samples (n = 115) of Aeromonas were collected from a general hospital in Beijing between the period 2015 and 2017. Taxonomy was investigate by Multilocus phylogenetic analysis (MLPA), 10 putative virulence factors by use of polymerase chain reaction (PCR) and antimicrobial resistance to 15 antibiotics by use of the microbroth dilution method. Results: The most common species of Aeromonas detected in samples of intestinal tract included; A. caviae (43.9%), A. veronii (35.7%), and A. dhakensis (12.2%). Prevalent species of Aeromonas collected from extra-intestinal infections included; A. hydrophila (29.4%), A. caviae (29.4%), and A. dhakensis (23.5%). A. hydrophila were detected in 1% of stool samples and 29.4% (5/17) of extra-intestinal infections. A. hydrophila strains in extra-intestinal infections were related to malignancy. The most common medical conditions among patients with Aeromonas infections included malignancy and liver-transplant related cholecystitis. Multiple drug resistance (MDR) was prevalent in extra-intestinal isolates (82.3%, 14/17) and was greater than the prevalence in intestinal isolates (30.6%, 30/98) (P < 0.05). Resistant rates of extra-intestinal isolates were 70.6, 35.3, 23.5 and 5.9% for ceftriaxone, ciprofloxacin, gentamicin and imipenem, respectively, and were higher than found in previous studies. Despite differences in the number and type of virulence genes among samples of Aeromonas, no significant correlation was found between invasion and virulent genes in intestinal or extra-intestinal infections. Conclusions: Overall results of this study support a role for Aeromonas spp. as a potential causative infectious agent of gastroenteritis, and malignancy, liver cirrhosis, post liver transplantation in immunocompromised patients. A. hydrophila was more prevalent in samples of extra-intestinal infections when compared to samples of intestinal infections, and was especially prominent in samples of patients presenting with malignancy. Aeromonas isolates from extra-intestinal samples had high rates of drug resistance but 3rd generation cephalosporins, fluoroquinolones and aminoglycosides remain as options to treat severe diarrhea. However, increasing MDR of extra-intestinal infection samples warrants monitoring. Keywords: Aeromonas , Multilocus phylogenetic analysis (MLPA), Virulence genes , Multi-drug resistance * Correspondence: [email protected]; [email protected] 1Center of Clinical Laboratory, Beijing Friendship Hospital, Capital Medical University, Beijing 100050, China Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Zhou et al. BMC Infectious Diseases (2019) 19:158 Page 2 of 9 Background increasing resistance in bacterium to antimicrobial drugs. The genus Aeromonas is a common, gram-negative, faculta- Therefore it is prudent to monitor the development of anti- tive anaerobe, coccobacillary-to-bacillary bacteria that be- microbial resistance in species of Aeromonas to common longs to Aeromonadaceae [1].The genus Aeromonas is clinical treatment options. comprised of mesophiles and psychrophiles which can cause In the presented study, we investigated characteristics a number of diseases to warm and cold-blooded animals [2]. of strains of Aeromonas isolated from intestinal infec- Recently, mesophilic Aeromonas have received increased at- tions and extra-intestinal infection. Furthermore we tention as an emergent agent of foodborne illness [3]. In evaluated virulence associated genes and antimicrobial humans, Aeromonas can cause extra-intestinal diseases, es- resistance of species of Aeromonas. pecially in immunocompromised individuals, including septi- cemia, wound infections, urinary tract infections, Materials and methods hepatobiliary tract infections and necrotizing fasciitis [4]. Isolates of Aeromonas Aeromonas have a complex taxonomy and the genus is Overall, 1286 stool samples were collected from adults over comprised of over 30 species, however their identification 14 years old presenting with acute diarrhea at a general hos- has been limited by use of conventional biochemical identi- pital in Beijng, China, between June and July 2015, 2017. Epi- fication methods such as matrix-assisted laser desorption/ demiology related medical records were completed to assess ionization time of flight masss spectrometry (MALDI-TOF clinical history and physical fitness of patients (Additional file MS), and 16S ribosomal ribonucleic acid (rRNA) sequen- 1). Samples of Stool were enriched in alkaline peptone water cing [5–8]. To this end, the use of 5 or more housekeeping broth (Beijing landbrige, China) for 8 h at 37 °C, and a loop genes has been demonstrated as an effective approach for of the resulting mixture was subcultured on a blood agar multilocus phylogenetic analysis (MLPA) and species iden- plate (Oxoid, UK) supplemented with 20% ampicillin (Sigma, tification of Aeromonas spp. [5, 9]. In addition, MLPA has USA) for 16–24 h at 37 °C [28]. An oxidase test (BioMer- been recommended for the verification of taxonomic affili- ieuX, France) was performed to select the colonies which ation by genome sequencing before being submitted to the were different from Enterobacteriaceae. Microorganisms NCBI database [10]. Current literature indicates that A. were identified by use of an automatic bacteriologic analyzer hydrophila, A. veronii bv sobria,andA. caviae are respon- (VITEK2 Compact, BioMerieuX, France). Salmonella spp, sible for the majority of human infections and clinical isola- Shigella spp and Vibrio spp were also detected on a routine tions [11]. However, caution must be exercised as A. basis. simultaneously. dhakensis can be misidentified as A. hydrophila by use of Extra-intestinal infections due to Aeromonas were moni- some phenotypic methods [12] and MLPA is suggeted for tored and the strains were isolated between 2015 and 2017. molecular subtyping [13, 14]. Clinical samples of blood or bile were cultured in a BACTEC A. dhakensis was initially described as a A. hydrophila FX400 (BD Diagnostic Instrument Systems, USA). Samples subspecies in 2002, and A. aquariorum described later, positive for Aeromonas were simultaneously subcultured on and was recommended to be reclassified as a separate a blood agar plate and a Maconkey agar plate (BioMerieuX, species in 2012 [15]. France). Identification of the isolated microorganisms was The pathogenesis of Aeromonas spp. involves a series completed by use of an automatic bacteriologic analyzer of virulence factors [16]. Haemolytic toxins include: aero- (VITEK2 Compact, BioMerieuX, France). Concurrently, lysin-related cytotoxic enterotoxin (Act) [17], heat-labile medical records of the patients with extra-intestinal infec- cytotonic enterotoxin (Alt), heat-stable cytotonic toxins tions due to species of Aeromonas were reviewed and age, (Ast) [18], hemolysin (HlyA) and aerolysin (AerA) [19]. In gender, underlying conditions, microbiological findings and addition, the type III secretion system (TTSS) [20], polar outcome were assembled. flagellum (fla), lateral flagella (laf) [21, 22], elastase (Ela) Strains were stored in a Luria broth: glycerol mixture [23] and lipase (Lip) [24] contribute to the pathogenicity (80:20) at − 80 °C until identification was performed. of Aeromonas. Most cases of diarrheal due to Aeromonads are Molecular identification and subtyping of Aeromonas self-limiting and treatment with oral or intravenous fluids is isolates effective. However, patients with serious diarrhea or Molecular identification and subtyping of Aeromonas iso- extra-intestinal infection should receive an antimicrobial lates was completed by use of 16S rRNA sequencing and treatment [2]. Previously, Aeromonas has been observed as MLPA. Total chromosomal DNA from Aeromonas was resistant to ampicillin, while 3rd generation cephalosporin, prepared by use of the DNA purification kit (Tiangen Bio- fluoroquinolone and aminoglycosides demonstrated excel- tech, China) as specified by the manufacturer. PCR ampli- lent antimicrobial activity to Aeromonas species isolated fication was performed by use of 2 × Taq PCR MasterMix from clinical sources [14, 25–27]. However, extensive use of (Tiangen Biotech, China). Primers synthesis and sequen- antibiotics in aquaculture and human treatment has led to cing of PCR products were conducted
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