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Published in: European Journal of Clinical Microbiology & Infectious Diseases 4/2017

Open Access 01-04-2017 | Original Article

Genomic analysis reveals the presence of a class D beta-lactamase with broad substrate specificity in animal bite associated Capnocytophaga species

Authors: S. Zangenah, A. F. Andersson, V. Özenci, P. Bergman

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 4/2017

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Abstract

Capnocytophga canimorsus and Capnocytophga cynodegmi can be transmitted from cats and dogs to humans, and can cause a wide range of infections including wound infections, sepsis, or endocarditis. We and others recently discovered two new Capnocytophaga species, C. canis and C. stomatis, mainly associated with wound infections. The first-line treatment of animal bite related infections is penicillin, and in case of allergy, doxycycline and trimethoprim/sulfamethoxazole. However, there is a lack of antibiotic susceptibility patterns for animal bite associated Capnocytophaga species. Thus, we set out to study the antibiotic profiles against animal bite associated Capnocytophaga species isolated from wound and blood cultures after cat and dog bites and coupled the findings to whole genome sequencing data. A total of 24 strains were included in the study. Phenotypic analysis of antibiotic resistance was performed with E-tests. The web-based tool ‘Resfinder’ was used to identify resistance genes in the whole genome dataset. Two strains of C. cynodegmi and two strains of the recently discovered C. stomatis were resistant to penicillin (MIC > 24 mg/L) and cephalosporins (MIC > 24 mg/L), and three out of these strains also exhibited resistance to imipenem (MIC = 32 mg/L). Genomic analysis revealed that these strains carried a class D beta-lactamase gene, which has not previously been found in Capnocytophaga spp. A class D beta lactamase with broad substrate specificity was found in animal bite associated Capnocytophaga species, which could have important implications when treating wound infections after cat and dog bites. It also suggests that pet animal bacteria can harbour resistance genes with relevance for human infections.
Literature
1.
go back to reference Al-Bayssari C, Gupta SK, Dabboussi F, Hamze M, Rolain JM (2015) MUS-2, a novel variant of the chromosome-encoded beta-lactamase MUS-1, from Myroides odoratimimus. New Microbes New Infect 7:67–71CrossRefPubMedPubMedCentral Al-Bayssari C, Gupta SK, Dabboussi F, Hamze M, Rolain JM (2015) MUS-2, a novel variant of the chromosome-encoded beta-lactamase MUS-1, from Myroides odoratimimus. New Microbes New Infect 7:67–71CrossRefPubMedPubMedCentral
2.
go back to reference Beyrouthy R, Robin F, Cougnoux A, Dalmasso G, Darfeuille-Michaud A, Mallat H, Dabboussi F, Hamze M, Bonnet R (2013) Chromosome-mediated OXA-48 carbapenemase in highly virulent Escherichia coli. J Antimicrob Chemother 68:1558–1561CrossRefPubMed Beyrouthy R, Robin F, Cougnoux A, Dalmasso G, Darfeuille-Michaud A, Mallat H, Dabboussi F, Hamze M, Bonnet R (2013) Chromosome-mediated OXA-48 carbapenemase in highly virulent Escherichia coli. J Antimicrob Chemother 68:1558–1561CrossRefPubMed
3.
go back to reference Bremmelgaard A, Pers C, Kristiansen JE, Korner B, Heltberg O, Frederiksen W (1989) Susceptibility testing of Danish isolates of Capnocytophaga and CDC group DF-2 bacteria. APMIS 97:43–48CrossRefPubMed Bremmelgaard A, Pers C, Kristiansen JE, Korner B, Heltberg O, Frederiksen W (1989) Susceptibility testing of Danish isolates of Capnocytophaga and CDC group DF-2 bacteria. APMIS 97:43–48CrossRefPubMed
4.
go back to reference Butler T (2015) Capnocytophaga canimorsus: an emerging cause of sepsis, meningitis, and post-splenectomy infection after dog bites. Eur J Clin Microbiol Infect Dis 34:1271–1280CrossRefPubMed Butler T (2015) Capnocytophaga canimorsus: an emerging cause of sepsis, meningitis, and post-splenectomy infection after dog bites. Eur J Clin Microbiol Infect Dis 34:1271–1280CrossRefPubMed
5.
go back to reference Cimmino T, Olaitan AO, Rolain JM (2016) Whole genome sequence to decipher the resistome of Shewanella algae, a multidrug-resistant bacterium responsible for pneumonia, Marseille, France. Expert Rev Anti Infect Ther 14:269–275CrossRefPubMed Cimmino T, Olaitan AO, Rolain JM (2016) Whole genome sequence to decipher the resistome of Shewanella algae, a multidrug-resistant bacterium responsible for pneumonia, Marseille, France. Expert Rev Anti Infect Ther 14:269–275CrossRefPubMed
6.
go back to reference Dupin C, Tamanai-Shacoori Z, Ehrmann E, Dupont A, Barloy-Hubler F, Bousarghin L, Bonnaure-Mallet M, Jolivet-Gougeon A (2015) Oral Gram-negative anaerobic bacilli as a reservoir of beta-lactam resistance genes facilitating infections with multiresistant bacteria. Int J Antimicrob Agents 45:99–105CrossRefPubMed Dupin C, Tamanai-Shacoori Z, Ehrmann E, Dupont A, Barloy-Hubler F, Bousarghin L, Bonnaure-Mallet M, Jolivet-Gougeon A (2015) Oral Gram-negative anaerobic bacilli as a reservoir of beta-lactam resistance genes facilitating infections with multiresistant bacteria. Int J Antimicrob Agents 45:99–105CrossRefPubMed
7.
go back to reference Endicott-Yazdani TR, Dhiman N, Benavides R, Spak CW (2015) Myroides odoratimimus bacteremia in a diabetic patient. Proc (Bayl Univ Med Cent) 28:342–343 Endicott-Yazdani TR, Dhiman N, Benavides R, Spak CW (2015) Myroides odoratimimus bacteremia in a diabetic patient. Proc (Bayl Univ Med Cent) 28:342–343
9.
go back to reference Gerster JC, Dudler J (2004) Cellulitis caused by Capnocytophaga cynodegmi associated with etanercept treatment in a patient with rheumatoid arthritis. Clin Rheumatol 23:570–571CrossRefPubMed Gerster JC, Dudler J (2004) Cellulitis caused by Capnocytophaga cynodegmi associated with etanercept treatment in a patient with rheumatoid arthritis. Clin Rheumatol 23:570–571CrossRefPubMed
10.
go back to reference Guillon H, Eb F, Mammeri H (2010) Characterization of CSP-1, a novel extended-spectrum beta-lactamase produced by a clinical isolate of Capnocytophaga sputigena. Antimicrob Agents Chemother 54:2231–2234CrossRefPubMedPubMedCentral Guillon H, Eb F, Mammeri H (2010) Characterization of CSP-1, a novel extended-spectrum beta-lactamase produced by a clinical isolate of Capnocytophaga sputigena. Antimicrob Agents Chemother 54:2231–2234CrossRefPubMedPubMedCentral
11.
go back to reference Huang MB, Baker CN, Banerjee S, Tenover FC (1992) Accuracy of the E test for determining antimicrobial susceptibilities of staphylococci, enterococci, Campylobacter jejuni, and gram-negative bacteria resistant to antimicrobial agents. J Clin Microbiol 30:3243–3248PubMedPubMedCentral Huang MB, Baker CN, Banerjee S, Tenover FC (1992) Accuracy of the E test for determining antimicrobial susceptibilities of staphylococci, enterococci, Campylobacter jejuni, and gram-negative bacteria resistant to antimicrobial agents. J Clin Microbiol 30:3243–3248PubMedPubMedCentral
12.
go back to reference Jaindl M, Oberleitner G, Endler G, Thallinger C, Kovar FM (2016) Management of bite wounds in children and adults-an analysis of over 5000 cases at a level I trauma centre. Wien Klin Wochenschr 128:367–375CrossRefPubMed Jaindl M, Oberleitner G, Endler G, Thallinger C, Kovar FM (2016) Management of bite wounds in children and adults-an analysis of over 5000 cases at a level I trauma centre. Wien Klin Wochenschr 128:367–375CrossRefPubMed
13.
go back to reference Khawari AA, Myers JW, Ferguson DA Jr, Moorman JP (2005) Sepsis and meningitis due to Capnocytophaga cynodegmi after splenectomy. Clin Infect Dis 40:1709–1710CrossRefPubMed Khawari AA, Myers JW, Ferguson DA Jr, Moorman JP (2005) Sepsis and meningitis due to Capnocytophaga cynodegmi after splenectomy. Clin Infect Dis 40:1709–1710CrossRefPubMed
14.
go back to reference Krahn T, Wibberg D, Maus I, Winkler A, Bontron S, Sczyrba A, Nordmann P, Puhler A, Poirel L, Schluter A (2016) Intraspecies transfer of the chromosomal acinetobacter baumannii blaNDM-1 carbapenemase gene. Antimicrob Agents Chemother 60:3032–3040CrossRefPubMedPubMedCentral Krahn T, Wibberg D, Maus I, Winkler A, Bontron S, Sczyrba A, Nordmann P, Puhler A, Poirel L, Schluter A (2016) Intraspecies transfer of the chromosomal acinetobacter baumannii blaNDM-1 carbapenemase gene. Antimicrob Agents Chemother 60:3032–3040CrossRefPubMedPubMedCentral
15.
go back to reference Lewis KT, Stiles M (1995) Management of cat and dog bites. Am Fam Physician 52(2):479–485, 489–490PubMed Lewis KT, Stiles M (1995) Management of cat and dog bites. Am Fam Physician 52(2):479–485, 489–490PubMed
16.
go back to reference Li L, Olsen RH, Ye L, Yan H, Nie Q, Meng H, Shi L (2016) Antimicrobial resistance and resistance genes in aerobic bacteria isolated from pork at slaughter. J Food Prot 79:589–597CrossRefPubMed Li L, Olsen RH, Ye L, Yan H, Nie Q, Meng H, Shi L (2016) Antimicrobial resistance and resistance genes in aerobic bacteria isolated from pork at slaughter. J Food Prot 79:589–597CrossRefPubMed
17.
go back to reference Maury S, Leblanc T, Rousselot P, Legrand P, Arlet G, Cordonnier C (1999) Bacteremia due to Capnocytophaga species in patients with neutropenia: high frequency of beta-lactamase-producing strains. Clin Infect Dis 28:1172–1174CrossRefPubMed Maury S, Leblanc T, Rousselot P, Legrand P, Arlet G, Cordonnier C (1999) Bacteremia due to Capnocytophaga species in patients with neutropenia: high frequency of beta-lactamase-producing strains. Clin Infect Dis 28:1172–1174CrossRefPubMed
18.
go back to reference McFarland J (1907) The nephelometer: an instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. JAMA 14:1176–1178CrossRef McFarland J (1907) The nephelometer: an instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. JAMA 14:1176–1178CrossRef
19.
go back to reference Mouton JW, Brown DF, Apfalter P, Canton R, Giske CG, Ivanova M, MacGowan AP, Rodloff A, Soussy CJ, Steinbakk M et al (2012) The role of pharmacokinetics/pharmacodynamics in setting clinical MIC breakpoints: the EUCAST approach. Clin Microbiol Infect 18:E37–E45CrossRefPubMed Mouton JW, Brown DF, Apfalter P, Canton R, Giske CG, Ivanova M, MacGowan AP, Rodloff A, Soussy CJ, Steinbakk M et al (2012) The role of pharmacokinetics/pharmacodynamics in setting clinical MIC breakpoints: the EUCAST approach. Clin Microbiol Infect 18:E37–E45CrossRefPubMed
20.
go back to reference Oehler RL, Velez AP, Mizrachi M, Lamarche J, Gompf S (2009) Bite-related and septic syndromes caused by cats and dogs. Lancet Infect Dis 9:439–447CrossRefPubMed Oehler RL, Velez AP, Mizrachi M, Lamarche J, Gompf S (2009) Bite-related and septic syndromes caused by cats and dogs. Lancet Infect Dis 9:439–447CrossRefPubMed
21.
go back to reference Presutti RJ (2001) Prevention and treatment of dog bites. Am Fam Physician 63:1567–1572PubMed Presutti RJ (2001) Prevention and treatment of dog bites. Am Fam Physician 63:1567–1572PubMed
22.
go back to reference Renzi F, Dol M, Raymackers A, Manfredi P, Cornelis GR (2015) Only a subset of C canimorsus strains is dangerous for humans. Emerg Microbes Infect 4:e48CrossRefPubMedPubMedCentral Renzi F, Dol M, Raymackers A, Manfredi P, Cornelis GR (2015) Only a subset of C canimorsus strains is dangerous for humans. Emerg Microbes Infect 4:e48CrossRefPubMedPubMedCentral
23.
24.
go back to reference Srinivas J, Pillai M, Vinod V, Dinesh RK (2015) Skin and soft tissue infections due to Shewanella algae—an emerging pathogen. J Clin Diagn Res 9:DC16–DC20PubMedPubMedCentral Srinivas J, Pillai M, Vinod V, Dinesh RK (2015) Skin and soft tissue infections due to Shewanella algae—an emerging pathogen. J Clin Diagn Res 9:DC16–DC20PubMedPubMedCentral
25.
26.
go back to reference Zangenah S, Abbasi N, Andersson AF, Bergman P (2016) Whole genome sequencing identifies a novel species of the genus Capnocytophaga isolated from dog and cat bite wounds in humans. Sci Rep 6:22919CrossRefPubMedPubMedCentral Zangenah S, Abbasi N, Andersson AF, Bergman P (2016) Whole genome sequencing identifies a novel species of the genus Capnocytophaga isolated from dog and cat bite wounds in humans. Sci Rep 6:22919CrossRefPubMedPubMedCentral
27.
go back to reference Zangenah S, Guleryuz G, Borang S, Ullberg M, Bergman P, Ozenci V (2013) Identification of clinical Pasteurella isolates by MALDI-TOF—a comparison with VITEK 2 and conventional microbiological methods. Diagn Microbiol Infect Dis 77:96–98CrossRefPubMed Zangenah S, Guleryuz G, Borang S, Ullberg M, Bergman P, Ozenci V (2013) Identification of clinical Pasteurella isolates by MALDI-TOF—a comparison with VITEK 2 and conventional microbiological methods. Diagn Microbiol Infect Dis 77:96–98CrossRefPubMed
28.
go back to reference Zangenah S, Ozenci V, Borang S, Bergman P (2012) Identification of blood and wound isolates of C. canimorsus and C. cynodegmi using VITEK2 and MALDI-TOF. Eur J Clin Microbiol Infect Dis 31:2631–2637CrossRefPubMed Zangenah S, Ozenci V, Borang S, Bergman P (2012) Identification of blood and wound isolates of C. canimorsus and C. cynodegmi using VITEK2 and MALDI-TOF. Eur J Clin Microbiol Infect Dis 31:2631–2637CrossRefPubMed
29.
go back to reference Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644CrossRefPubMedPubMedCentral Zankari E, Hasman H, Cosentino S, Vestergaard M, Rasmussen S, Lund O, Aarestrup FM, Larsen MV (2012) Identification of acquired antimicrobial resistance genes. J Antimicrob Chemother 67:2640–2644CrossRefPubMedPubMedCentral
Metadata
Title
Genomic analysis reveals the presence of a class D beta-lactamase with broad substrate specificity in animal bite associated Capnocytophaga species
Authors
S. Zangenah
A. F. Andersson
V. Özenci
P. Bergman
Publication date
01-04-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 4/2017
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-016-2842-2

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