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Clostridium Innocuum Is a Significant Vancomycin-Resistant Pathogen For Clinical Microbiology and Infection 23 (2017) 560e566 Contents lists available at ScienceDirect Clinical Microbiology and Infection journal homepage: www.clinicalmicrobiologyandinfection.com Original article Clostridium innocuum is a significant vancomycin-resistant pathogen for extraintestinal clostridial infection y J.-H. Chia 1, 2, , 7,Y.Feng3, 4, 7, L.-H. Su 1, 2, 5, T.-L. Wu 1, 2, C.-L. Chen 5, Y.-H. Liang 5, * C.-H. Chiu 5, 6, 1) Department of Laboratory Medicine, Chang Gung Memorial Hospital, Taoyuan, Taiwan 2) Department of Medical Biotechnology and Laboratory Science, Chang Gung University, Taoyuan, Taiwan 3) Sir Run Run Shaw Hospital, Zhejiang University School of Medicine, Hangzhou, China 4) Institute of Translational Medicine, Zhejiang University School of Medicine, Hangzhou, China 5) Molecular Infectious Disease Research Centre, Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Taoyuan, Taiwan 6) Division of Paediatric Infectious Diseases, Department of Paediatrics, Chang Gung Children's Hospital, Chang Gung University College of Medicine, Taoyuan, Taiwan article info abstract Article history: Objectives: Extra-intestinal clostridial infection (EICI) is rare but can be fatal. Traditional phenotypic Received 16 October 2016 methods can only assign many of the Clostridium species to the genus level. Received in revised form Methods: A total of 376 non-repetitive Clostridium isolates from sterile sites were collected and subjected 15 February 2017 to matrix-assisted laser desorption/ionization time-of-flight (MALDI-TOF) Biotyper analysis and 16S Accepted 22 February 2017 rRNA sequencing. Antimicrobial susceptibility was determined, and clinical characteristics of the patients Available online 28 February 2017 were assessed. Clostridium innocuum isolates were characterized by genome sequencing and genotyping. Editor: P.T. Tassios We used molecular and cellular methods to explore the virulence and resistance mechanisms of C. innocuum. Keywords: Results: Clostridium innocuum was the second most common species to cause EICI, only next to Clos- Clostridium innocuum tridium perfringens. All Clostridium isolates showed susceptibility to clindamycin, metronidazole, peni- Extra-intestinal clostridial infection cillin, piperacillin and ampicillin-sulbatam, while C. innocuum isolates were invariably resistant to MALDI-TOF vancomycin. Among 24 patients with EICI caused by C. innocuum, two (8.3%) had diarrhoea, three (12.5%) 16S rRNA sequencing had soft-tissue infection, six (25%) had appendicitis and four (16.7%) each had shock and gastrointestinal Vancomycin resistance perforation. The 30-day mortality was 16.7%. The C. innocuum isolated from different sites could not be separated from one another by genotyping. No known toxin genes were identified in the genome of C. innocuum but the species expressed cytotoxicity to epithelial cells. D-Alanine-D-alanine ligase, alanine racemase and D-alanyl-D-alanine carboxypeptidase are three main genes responsible for vancomycin resistance in C. innocuum. Conclusions: Vancomycin-resistant C. innocuum is a previously unrecognized, yet prominent, cause for EICI. Genome analysis showed that the species could carry a lipopolysaccharide-like structure that is associated with cytotoxicity to cells in vitro. J.-H. Chia, Clin Microbiol Infect 2017;23:560 © 2017 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved. Introduction vulnerable to EICI is the elderly with underlying diseases such as gastrointestinal diseases, diabetes mellitus, liver cirrhosis, malig- Extra-intestinal clostridial infection (EICI) occurs infrequently nancy and chronic kidney diseases requiring haemodialysis [5,6]. but is associated with a high mortality [1e4]. A population Furthermore, most of the patients usually have a history of recent antimicrobial use [2,7]. Clostridium perfringens is the most frequent * Corresponding author. C.-H. Chiu, Division of Paediatric Infectious Diseases, species for EICI, followed by Clostridium septicum, Clostridium Department of Paediatrics, Chang Gung Children's Hospital, Chang Gung University difficile and Clostridium innocuum, according to previous reports College of Medicine, No. 5, Fu-Hsin Street, Kweishan 333, Taoyuan, Taiwan. [5,8,9]. Clostridium innocuum may attract special attention in that E-mail address: [email protected] (C.-H. Chiu). all of the C. innocuum isolates found so far are exclusively resistant 7 J-HC and YF contributed equally to this work. y Current address: Anti-infectious Group, Eurofins Panlabs Ltd., Taipei, Taiwan. to vancomycin [10,11], whereas the other Clostridium species are http://dx.doi.org/10.1016/j.cmi.2017.02.025 1198-743X/© 2017 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved. J.-H. Chia et al. / Clinical Microbiology and Infection 23 (2017) 560e566 561 susceptible [12e14]. Although the name ‘innocuum’ was chosen MALDI-TOF MS with FLEX CONTROL 3.0 software and the MALDI BIO- because of the organism's proposed lack of virulence, the very TYPER v3.1. limited literature based on few clinical cases indicated that the mortality rate caused by this organism was even higher than other Clinical data collection and definitions Clostridium species [15]. Due to factors such as Gram-stain variability, rare spores and This study was approved by the Institutional Review Board (101- atypical clostridial colonial morphology, traditional phenotypic 4682B) of Chang Gung Memorial Hospital, Taiwan. Clinical infor- methods can only assign many of the Clostridium species to the mation, including demographic data, underlying diseases, clinical genus level and yet exhibit a low level of selectivity for species diagnoses and outcome, of the patients with culture-confirmed identification [16], especially for Clostridium ramosum, C. innocuum C. innocuum infection were retrospectively collected. In addition and Clostridium clostridioforme, the so-called RIC group. Hence, 16S to the patients with EICI, clinical information of ten patients with rRNA sequencing has become the reference standard for species diarrhoeal disease with faecal samples growing C. innocuum in identification. Recently, the technology of matrix-assisted laser C. difficile selective agar and CDC-ANA blood agar (BD BBL, Sparks, desorptioneionization time-of-flight mass spectrometry (MALDI- MD, USA) were collected and used for comparison. The species TOF MS) was also used for bacterial species identification in the identification was accomplished by 16S rRNA sequencing. The clinical setting. To date, few studies have systematically charac- history of antimicrobial use for at least 5 days before the onset of terized EICI by genotypic method [9]. In this study we applied both the infections in these patients was also reviewed. phenotypic and genotypic methods to characterize 376 Clostridium isolates collected from a medical centre in Taiwan during Antimicrobial susceptibility testing 2007e2011. We found that C. innocuum was the second most common aetiological agent for EICI, and the clinical features of EICI Antimicrobial susceptibilities to clindamycin, metronidazole, caused by this organism were different from those described pre- penicillin, piperacillin and ampicillin-sulbatam were tested by the viously. We also sequenced the genome of a clinical C. innocuum break-point agar dilution method according to the CLSI criteria isolate and explored the putative mechanism of virulence and M11-A8 for anaerobic bacteria [17]. The interpretive criteria for vancomycin resistance in this species. susceptibility of the CLSI M100S were used for calls of susceptible or resistant: clindamycin, susceptible, 2 mg/L, resistant, 8 mg/L; Materials and methods metronidazole, susceptible, 8mg/L, resistant, 32 mg/L; peni- cillin, susceptible, 0.5 mg/L, resistant, 2 mg/L; piperacillin, Bacterial isolates 32 mg/L, resistant, 128 mg/L; ampicillin-sulbatam, susceptible, 8/4 mg/L, resistant, 32/16 mg/L; vancomycin, resistant, 8 mg/L From 2007 to 2011, a total of 3191 non-repetitive specimens [18]. from normally sterile sites were positive in anaerobic culture at Chang Gung Memorial Hospital, a 3700-bed medical centre in Genome sequencing and annotation northern Taiwan. The specimens included ascites, blood and pleural fluid. A total of 376 non-repetitive Clostridium isolates collected One C. innocuum isolate, designated AN88-98, was selected for from these sterile specimens, including 226 from ascites, 144 from whole genome sequencing. The genomic DNA was extracted using blood and six from pleural fluid, were studied from 2007 to 2011. QIAamp DNA Mini Kit (Qiagen, Valencia, CA, USA) and then Clostridium isolates were identified using rapid ID 32A system sequenced using an Illumina GAII instrument (Illumina Inc., San (BioMerieux, Durham, NC, USA), MALDI-TOF Biotyper (Bruker Diego, CA, USA) following a 2 Â 75-bp pair-end protocol. The raw Daltonik GmbH, Bremen, Germany), and 16S rRNA sequencing. All reads were assembled using CLC GENOMICS WORKBENCH software (CLC the isolates were cultured on CDC-ANA agar plates and incubated in bio, Aarhus, Denmark). The assembled draft genome has been anaerobic conditions at 37C for 2e5 days before examination. deposited into GenBank under the Accession Number JQIF0000- 0000. The genome annotation of the sequenced isolated AN88-98 Species identification by 16S rRNA sequencing was performed using NCBI Prokaryotic Genome Annotation Pipeline. A PCR assay targeting an
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