NDM-1-producing Vibrio parahaemolyticus isolated from imported seafood

NDM-1-producing Vibrio parahaemolyticus isolated from imported seafood Sir, Vibrio parahaemolyticus is a marine microorganism, frequently isolated from seafood, at water temperatures above 15°C.1 It is also a foodborne pathogen, often linked to consumption of raw or uncooked seafood, mostly encountered in patients in Asia or the USA.1 Ingestion of V. parahaemolyticus-contaminated seafood can lead to gastroenteritis. Symptoms are abdominal cramps, nausea, diarrhoea, fever, headache and chills.1 In most cases, V. parahaemolyticus infections are self-limiting but, in patients with underlying diseases, V. parahaemolyticus can cause septicaemia.1 To treat severe or prolonged infections, antibiotics such as fluoroquinolones, azithromycin or rifaximin can be prescribed.2 WT V. parahaemolyticus are characterized as being susceptible to all antibiotic classes, except penicillins.3 V. parahaemolyticus strain 16-B3PA-006 was isolated in January 2016, from a shelled shrimp tail imported from Vietnam to France. Antimicrobial susceptibility was tested by the disc diffusion method (Bio-Rad, Marne-La-Coquette, France), following CLSI recommendations.4 Genomic characterization of the isolate was performed by WGS on a NextSeq (Illumina, San Diego, CA, USA). The raw reads were trimmed (minimum length, 35 bp; quality score, 0.03) and assembled in CLC Genomics Workbench 7.5.1, firstly by mapping chromosome 1 and 2 from the V. parahaemolyticus reference genome (V. parahaemolyticus RIMD 2210633) and then de novo assembly of the remaining paired-end reads. A total of 190 contigs were obtained including 60 contigs that did not map the reference genome, indicating the presence of acquired genetic material. The Center for Genomic Epidemiology server (https://cge.cbs.dtu.dk/services/) was used to identify acquired antimicrobial resistance genes (Resfinder), plasmid presence (PlasmidFinder) and ST (MLST). Strain 16-B3PA-006 was assigned to V. parahaemolyticus ST-864. PlasmidFinder identified a unique IncA/C2 plasmid. V. parahaemolyticus strain 16-B3PA-006 was phenotypically resistant to amoxicillin/clavulanate, cefoxitin, cefotaxime, ceftazidime, cefuroxime, cefepime and trimethoprim/sulfamethoxazole, but remained susceptible to imipenem, tetracycline, ciprofloxacin and gentamicin. Resfinder identified with 100% identity the resistance genes blaNDM-1, sul1, sul2, dfrA16, strA, strB and aadA2. Moreover, floR and tet(A) were detected with 98.19% and 99.83% identity, respectively. No resistance gene was neighbouring blaNDM-1, only sul1 was on the opposite side of the contig, at a distance of 14 kb. A Blastn analysis of this contig with the National Center for Biotechnology Information nucleotide database identified a part of transposon Tn125: ΔISAba125, blaNDM-1, ble, trpF, tat, dct, groS, groL and IS91. Despite the apparent susceptibility to imipenem, the carbapenem inactivation method result was positive, confirming carbapenemase production by this strain.5 Even if the chromosomal or plasmidic location of blaNDM-1 had not been assessed so far, the carbapenemase phenotype had been successfully transferred to Escherichia coli UB5201 strain by conjugation assay. V. parahaemolyticus 16-B3PA-006 was confirmed to be MDR, by both genotype and phenotype, being resistant to more than three antibiotic classes: β-lactams, folate pathway inhibitors, phenicols, aminoglycosides and tetracyclines. The Tn125 transposon, carried by strain 16-B3PA-006, has been partially described in a clinical case of Vibrio fluvialis, but the transposon was not complete.6 Since its first description in 2009 in a patient returning from India, NDM-1 has been described in almost all parts of the world and is considered as one of the most clinically significant carbapenemases.7 In many of the first cases reported, patients were reporting recent inter-country travel history, not only to the Indian subcontinent, but also to the Balkan states, the Arabian Peninsula and North Africa; some of them having been repatriated for medical purposes.7 NDM-1-producing Vibrio spp. have been reported to a lesser extent in V. fluvialis and Vibrio cholerae clinical or environmental samples.6,8–10 To our knowledge, this report is the first description of a V. parahaemolyticus strain producing NDM-1 isolated from a food item. Other carbapenemase-producing bacteria isolated from foodstuffs have already been reported: NDM-1-producing Salmonella and Enterobacter cloacae from chicken and clam; and VIM-1-producing Salmonella and E. coli from pork and Venus clam.11–14 Nicol et al.12 and Roschanski et al.14 highlighted that the sampled food products in their studies were also imported. Interestingly, strain 16-B3PA-006 was proved to both carry the blaNDM-1 gene and display in vitro carbapenemase activity; nonetheless, the antibiogram categorized it as clinically susceptible to imipenem according to CLSI criteria. In vitro susceptibility to any carbapenem had not been described previously in NDM-1-producing Vibrio spp.6,8–10 Clinical microbiologists should be aware that NDM-1 carbapenemase activity in V. parahaemolyticus might be challenging to evidence through routine susceptibility tests. It is generally assumed that travellers, colonized by carbapenemase-producing bacteria, import it from endemic to non-endemic parts of the world.15 However, imported food should also be taken into consideration as a potential vector of dissemination of clinically significant carbapenemases such as NDM-1. The role of the global food trade should certainly not be underestimated anymore as an alternative route for carbapenemase dissemination. Nucleotide sequence accession number Strain 16-B3PA-006 sequence is available under GenBank accession number PETB00000000. Acknowledgements We would like to thank Stéphanie Copin, Virginie Raguenet, Guylaine Leleu and Régine Quenu for their assistance. We are especially grateful to Didier Mazel for his assistance with the conjugation assay and for providing the recipient strain. We would like to thank the iGenSeq core facility (Brain & Spine Institute, Hôpital Pitié Salpêtrière, Paris, France) for excellent sequencing services. Funding This work was supported by a doctoral fellowship from Région Hauts-de-France and by the French national effort to reduce antimicrobial resistance in veterinary medicine called ‘EcoAntibio2017’ from the Ministry of Agriculture. Transparency declarations None to declare. References 1 Su Y-C , Liu C. Vibrio parahaemolyticus: a concern of seafood safety . Food Microbiol 2007 ; 24 : 549 – 58 . Google Scholar CrossRef Search ADS PubMed 2 Diemert DJ. Prevention and self-treatment of traveler’s diarrhea . Clin Microbiol Rev 2006 ; 19 : 583 – 94 . Google Scholar CrossRef Search ADS PubMed 3 Chiou J , Li R , Chen S. CARB-17 family of β-lactamases mediates intrinsic resistance to penicillins in Vibrio parahaemolyticus . Antimicrob Agents Chemother 2015 ; 59 : 3593 – 5 . Google Scholar CrossRef Search ADS PubMed 4 Clinical and Laboratory Standards Institute . Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria—Third Edition: M45 . CLSI , Wayne, PA, USA , 2015 . 5 van der Zwaluw K , de Haan A , Pluister GN et al. The carbapenem inactivation method (CIM), a simple and low-cost alternative for the Carba NP test to assess phenotypic carbapenemase activity in Gram-negative rods . PLoS One 2015 ; 10 : e0123690. Google Scholar CrossRef Search ADS PubMed 6 Chowdhury G , Pazhani GP , Sarkar A et al. Carbapenem resistance in clonally distinct clinical strains of Vibrio fluvialis isolated from diarrheal samples . Emerg Infect Dis 2016 ; 22 : 1754 – 61 . Google Scholar CrossRef Search ADS PubMed 7 Nordmann P , Poirel L. The difficult-to-control spread of carbapenemase producers among Enterobacteriaceae worldwide . Clin Microbiol Infect 2014 ; 20 : 821 – 30 . Google Scholar CrossRef Search ADS PubMed 8 Darley E , Weeks J , Jones L et al. NDM-1 polymicrobial infections including Vibrio cholerae . Lancet 2012 ; 380 : 1358 . Google Scholar CrossRef Search ADS PubMed 9 Diep TT , Nguyen NT , Nguyen TN et al. Isolation of New Delhi metallo-β-lactamase 1-producing Vibrio cholerae non-O1, non-O139 strain carrying ctxA, st and hly genes in southern Vietnam . Microbiol Immunol 2015 ; 59 : 262 – 7 . Google Scholar CrossRef Search ADS PubMed 10 Walsh TR , Weeks J , Livermore DM et al. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study . Lancet Infect Dis 2011 ; 11 : 355 – 62 . Google Scholar CrossRef Search ADS PubMed 11 Borowiak M , Szabo I , Baumann B et al. VIM-1-producing Salmonella Infantis isolated from swine and minced pork meat in Germany . J Antimicrob Chemother 2017 ; 72 : 2131 – 3 . Google Scholar CrossRef Search ADS PubMed 12 Nicol J , Sarah-Lynn M , Brent PA et al. Carbapenem-resistant Enterobacter spp. in retail seafood imported from Southeast Asia to Canada . Emerg Infect Dis 2016 ; 22 : 1675 – 7 . Google Scholar CrossRef Search ADS PubMed 13 Wang W , Baloch Z , Peng Z et al. Genomic characterization of a large plasmid containing a blaNDM-1 gene carried on Salmonella enterica serovar Indiana C629 isolate from China . BMC Infect Dis 2017 ; 17 : 479 . Google Scholar CrossRef Search ADS PubMed 14 Roschanski N , Guenther S , Vu TTT et al. VIM-1 carbapenemase-producing Escherichia coli isolated from retail seafood, Germany 2016 . Euro Surveill 2017 ; 22 : pii=17-00032. 15 van der Bij AK , Pitout JDD. The role of international travel in the worldwide spread of multiresistant Enterobacteriaceae . J Antimicrob Chemother 2012 ; 67 : 2090 – 100 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Journal of Antimicrobial Chemotherapy Oxford University Press

NDM-1-producing Vibrio parahaemolyticus isolated from imported seafood

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com.
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0305-7453
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1460-2091
D.O.I.
10.1093/jac/dky200
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Abstract

Sir, Vibrio parahaemolyticus is a marine microorganism, frequently isolated from seafood, at water temperatures above 15°C.1 It is also a foodborne pathogen, often linked to consumption of raw or uncooked seafood, mostly encountered in patients in Asia or the USA.1 Ingestion of V. parahaemolyticus-contaminated seafood can lead to gastroenteritis. Symptoms are abdominal cramps, nausea, diarrhoea, fever, headache and chills.1 In most cases, V. parahaemolyticus infections are self-limiting but, in patients with underlying diseases, V. parahaemolyticus can cause septicaemia.1 To treat severe or prolonged infections, antibiotics such as fluoroquinolones, azithromycin or rifaximin can be prescribed.2 WT V. parahaemolyticus are characterized as being susceptible to all antibiotic classes, except penicillins.3 V. parahaemolyticus strain 16-B3PA-006 was isolated in January 2016, from a shelled shrimp tail imported from Vietnam to France. Antimicrobial susceptibility was tested by the disc diffusion method (Bio-Rad, Marne-La-Coquette, France), following CLSI recommendations.4 Genomic characterization of the isolate was performed by WGS on a NextSeq (Illumina, San Diego, CA, USA). The raw reads were trimmed (minimum length, 35 bp; quality score, 0.03) and assembled in CLC Genomics Workbench 7.5.1, firstly by mapping chromosome 1 and 2 from the V. parahaemolyticus reference genome (V. parahaemolyticus RIMD 2210633) and then de novo assembly of the remaining paired-end reads. A total of 190 contigs were obtained including 60 contigs that did not map the reference genome, indicating the presence of acquired genetic material. The Center for Genomic Epidemiology server (https://cge.cbs.dtu.dk/services/) was used to identify acquired antimicrobial resistance genes (Resfinder), plasmid presence (PlasmidFinder) and ST (MLST). Strain 16-B3PA-006 was assigned to V. parahaemolyticus ST-864. PlasmidFinder identified a unique IncA/C2 plasmid. V. parahaemolyticus strain 16-B3PA-006 was phenotypically resistant to amoxicillin/clavulanate, cefoxitin, cefotaxime, ceftazidime, cefuroxime, cefepime and trimethoprim/sulfamethoxazole, but remained susceptible to imipenem, tetracycline, ciprofloxacin and gentamicin. Resfinder identified with 100% identity the resistance genes blaNDM-1, sul1, sul2, dfrA16, strA, strB and aadA2. Moreover, floR and tet(A) were detected with 98.19% and 99.83% identity, respectively. No resistance gene was neighbouring blaNDM-1, only sul1 was on the opposite side of the contig, at a distance of 14 kb. A Blastn analysis of this contig with the National Center for Biotechnology Information nucleotide database identified a part of transposon Tn125: ΔISAba125, blaNDM-1, ble, trpF, tat, dct, groS, groL and IS91. Despite the apparent susceptibility to imipenem, the carbapenem inactivation method result was positive, confirming carbapenemase production by this strain.5 Even if the chromosomal or plasmidic location of blaNDM-1 had not been assessed so far, the carbapenemase phenotype had been successfully transferred to Escherichia coli UB5201 strain by conjugation assay. V. parahaemolyticus 16-B3PA-006 was confirmed to be MDR, by both genotype and phenotype, being resistant to more than three antibiotic classes: β-lactams, folate pathway inhibitors, phenicols, aminoglycosides and tetracyclines. The Tn125 transposon, carried by strain 16-B3PA-006, has been partially described in a clinical case of Vibrio fluvialis, but the transposon was not complete.6 Since its first description in 2009 in a patient returning from India, NDM-1 has been described in almost all parts of the world and is considered as one of the most clinically significant carbapenemases.7 In many of the first cases reported, patients were reporting recent inter-country travel history, not only to the Indian subcontinent, but also to the Balkan states, the Arabian Peninsula and North Africa; some of them having been repatriated for medical purposes.7 NDM-1-producing Vibrio spp. have been reported to a lesser extent in V. fluvialis and Vibrio cholerae clinical or environmental samples.6,8–10 To our knowledge, this report is the first description of a V. parahaemolyticus strain producing NDM-1 isolated from a food item. Other carbapenemase-producing bacteria isolated from foodstuffs have already been reported: NDM-1-producing Salmonella and Enterobacter cloacae from chicken and clam; and VIM-1-producing Salmonella and E. coli from pork and Venus clam.11–14 Nicol et al.12 and Roschanski et al.14 highlighted that the sampled food products in their studies were also imported. Interestingly, strain 16-B3PA-006 was proved to both carry the blaNDM-1 gene and display in vitro carbapenemase activity; nonetheless, the antibiogram categorized it as clinically susceptible to imipenem according to CLSI criteria. In vitro susceptibility to any carbapenem had not been described previously in NDM-1-producing Vibrio spp.6,8–10 Clinical microbiologists should be aware that NDM-1 carbapenemase activity in V. parahaemolyticus might be challenging to evidence through routine susceptibility tests. It is generally assumed that travellers, colonized by carbapenemase-producing bacteria, import it from endemic to non-endemic parts of the world.15 However, imported food should also be taken into consideration as a potential vector of dissemination of clinically significant carbapenemases such as NDM-1. The role of the global food trade should certainly not be underestimated anymore as an alternative route for carbapenemase dissemination. Nucleotide sequence accession number Strain 16-B3PA-006 sequence is available under GenBank accession number PETB00000000. Acknowledgements We would like to thank Stéphanie Copin, Virginie Raguenet, Guylaine Leleu and Régine Quenu for their assistance. We are especially grateful to Didier Mazel for his assistance with the conjugation assay and for providing the recipient strain. We would like to thank the iGenSeq core facility (Brain & Spine Institute, Hôpital Pitié Salpêtrière, Paris, France) for excellent sequencing services. Funding This work was supported by a doctoral fellowship from Région Hauts-de-France and by the French national effort to reduce antimicrobial resistance in veterinary medicine called ‘EcoAntibio2017’ from the Ministry of Agriculture. Transparency declarations None to declare. References 1 Su Y-C , Liu C. Vibrio parahaemolyticus: a concern of seafood safety . Food Microbiol 2007 ; 24 : 549 – 58 . Google Scholar CrossRef Search ADS PubMed 2 Diemert DJ. Prevention and self-treatment of traveler’s diarrhea . Clin Microbiol Rev 2006 ; 19 : 583 – 94 . Google Scholar CrossRef Search ADS PubMed 3 Chiou J , Li R , Chen S. CARB-17 family of β-lactamases mediates intrinsic resistance to penicillins in Vibrio parahaemolyticus . Antimicrob Agents Chemother 2015 ; 59 : 3593 – 5 . Google Scholar CrossRef Search ADS PubMed 4 Clinical and Laboratory Standards Institute . Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria—Third Edition: M45 . CLSI , Wayne, PA, USA , 2015 . 5 van der Zwaluw K , de Haan A , Pluister GN et al. The carbapenem inactivation method (CIM), a simple and low-cost alternative for the Carba NP test to assess phenotypic carbapenemase activity in Gram-negative rods . PLoS One 2015 ; 10 : e0123690. Google Scholar CrossRef Search ADS PubMed 6 Chowdhury G , Pazhani GP , Sarkar A et al. Carbapenem resistance in clonally distinct clinical strains of Vibrio fluvialis isolated from diarrheal samples . Emerg Infect Dis 2016 ; 22 : 1754 – 61 . Google Scholar CrossRef Search ADS PubMed 7 Nordmann P , Poirel L. The difficult-to-control spread of carbapenemase producers among Enterobacteriaceae worldwide . Clin Microbiol Infect 2014 ; 20 : 821 – 30 . Google Scholar CrossRef Search ADS PubMed 8 Darley E , Weeks J , Jones L et al. NDM-1 polymicrobial infections including Vibrio cholerae . Lancet 2012 ; 380 : 1358 . Google Scholar CrossRef Search ADS PubMed 9 Diep TT , Nguyen NT , Nguyen TN et al. Isolation of New Delhi metallo-β-lactamase 1-producing Vibrio cholerae non-O1, non-O139 strain carrying ctxA, st and hly genes in southern Vietnam . Microbiol Immunol 2015 ; 59 : 262 – 7 . Google Scholar CrossRef Search ADS PubMed 10 Walsh TR , Weeks J , Livermore DM et al. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study . Lancet Infect Dis 2011 ; 11 : 355 – 62 . Google Scholar CrossRef Search ADS PubMed 11 Borowiak M , Szabo I , Baumann B et al. VIM-1-producing Salmonella Infantis isolated from swine and minced pork meat in Germany . J Antimicrob Chemother 2017 ; 72 : 2131 – 3 . Google Scholar CrossRef Search ADS PubMed 12 Nicol J , Sarah-Lynn M , Brent PA et al. Carbapenem-resistant Enterobacter spp. in retail seafood imported from Southeast Asia to Canada . Emerg Infect Dis 2016 ; 22 : 1675 – 7 . Google Scholar CrossRef Search ADS PubMed 13 Wang W , Baloch Z , Peng Z et al. Genomic characterization of a large plasmid containing a blaNDM-1 gene carried on Salmonella enterica serovar Indiana C629 isolate from China . BMC Infect Dis 2017 ; 17 : 479 . Google Scholar CrossRef Search ADS PubMed 14 Roschanski N , Guenther S , Vu TTT et al. VIM-1 carbapenemase-producing Escherichia coli isolated from retail seafood, Germany 2016 . Euro Surveill 2017 ; 22 : pii=17-00032. 15 van der Bij AK , Pitout JDD. The role of international travel in the worldwide spread of multiresistant Enterobacteriaceae . J Antimicrob Chemother 2012 ; 67 : 2090 – 100 . Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For permissions, please email: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

Journal

Journal of Antimicrobial ChemotherapyOxford University Press

Published: May 22, 2018

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