Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia

ABSTRACT An increasing number of isolations of Corynebacterium diphtheriae has been observed in recent years in the archipelago of New Caledonia. We aimed to analyze the clinical and microbiological features of samples with C. diphtheriae. All C. diphtheriae isolates identified in New Caledonia from...

Full description

Bibliographic Details
Main Authors: Eve Tessier, Melanie Hennart, Edgar Badell, Virginie Passet, Julie Toubiana, Antoine Biron, Ann-Claire Gourinat, Audrey Merlet, Julien Colot, Sylvain Brisse
Format: Article
Language:English
Published: American Society for Microbiology 2023-06-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.04616-22
_version_ 1827925104230662144
author Eve Tessier
Melanie Hennart
Edgar Badell
Virginie Passet
Julie Toubiana
Antoine Biron
Ann-Claire Gourinat
Audrey Merlet
Julien Colot
Sylvain Brisse
author_facet Eve Tessier
Melanie Hennart
Edgar Badell
Virginie Passet
Julie Toubiana
Antoine Biron
Ann-Claire Gourinat
Audrey Merlet
Julien Colot
Sylvain Brisse
author_sort Eve Tessier
collection DOAJ
description ABSTRACT An increasing number of isolations of Corynebacterium diphtheriae has been observed in recent years in the archipelago of New Caledonia. We aimed to analyze the clinical and microbiological features of samples with C. diphtheriae. All C. diphtheriae isolates identified in New Caledonia from May 2015 to May 2019 were included. For each case, a retrospective consultation of the patient files was conducted. Antimicrobial susceptibility phenotypes, tox gene and diphtheria toxin expression, biovar, and the genomic sequence were determined. Core genome multilocus sequence typing (cgMLST), 7-gene MLST, and search of genes of interest were performed from genomic assemblies. Fifty-eight isolates were included, with a median age of patients of 28 years (range: 9 days to 78 years). Cutaneous origin accounted for 51 of 58 (87.9%) isolates, and C. diphtheriae was associated with Staphylococcus aureus and/or Streptococcus pyogenes in three-quarters of cases. Half of cases came either from the main city Noumea (24%, 14/58) or from the sparsely populated island of Lifou (26%, 15/58). Six tox-positive isolates were identified, associated with recent travel to Vanuatu; 5 of these cases were linked and cgMLST confirmed recent transmission. Two cases of endocarditis in young female patients with a history of rheumatic fever involved tox-negative isolates. The 58 isolates were mostly susceptible to commonly used antibiotics. In particular, no isolate was resistant to the first-line molecules amoxicillin or erythromycin. Resistance to tetracycline was found in a genomic cluster of 17 (29%) isolates, 16 of which carried the tetO gene. There were 13 cgMLST sublineages, most of which were also observed in the neighboring country Australia. Cutaneous infections may harbor nontoxigenic C. diphtheriae isolates, which circulate largely silently in nonspecific wounds. The possible introduction of tox-positive strains from a neighboring island illustrates that diphtheria surveillance should be maintained in New Caledonia, and that immunization in neighboring islands must be improved. Genomic sequencing uncovers how genotypes circulate locally and across neighboring countries. IMPORTANCE The analysis of C. diphtheriae from the tropical archipelago of New Caledonia revealed a high genetic diversity with sublineages that may be linked to Polynesia, Australia, or metropolitan France. Genomic typing allowed confirming or excluding suspected transmission events among cases and contacts. A highly prevalent tetracycline-resistant sublineage harboring the tetO gene was uncovered. Toxigenic isolates were observed from patients returning from Vanuatu, showing the importance of improving vaccination coverage in settings where it is insufficient. This study also illustrates the importance for diphtheria surveillance of the inclusion of isolates from cutaneous sources in addition to respiratory cases, in order to provide a more complete epidemiological picture of the diversity and transmission of C. diphtheriae.
first_indexed 2024-03-13T05:20:23Z
format Article
id doaj.art-ae39ebe0647d4dfe871eafa4889ff49d
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-03-13T05:20:23Z
publishDate 2023-06-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-ae39ebe0647d4dfe871eafa4889ff49d2023-06-15T13:18:32ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-06-0111310.1128/spectrum.04616-22Genomic Epidemiology of Corynebacterium diphtheriae in New CaledoniaEve Tessier0Melanie Hennart1Edgar Badell2Virginie Passet3Julie Toubiana4Antoine Biron5Ann-Claire Gourinat6Audrey Merlet7Julien Colot8Sylvain Brisse9CHU Nantes, Service de Bactériologie et des Contrôles Microbiologiques, Nantes, FranceInstitut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Paris, FranceInstitut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Paris, FranceInstitut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Paris, FranceInstitut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Paris, FranceMicrobiology Laboratory, Centre Hospitalier Territorial Gaston Bourret, Nouméa, New CaledoniaMicrobiology Laboratory, Centre Hospitalier Territorial Gaston Bourret, Nouméa, New CaledoniaInfectious diseases unit, Centre Hospitalier Territorial Gaston Bourret, Nouméa, New CaledoniaMicrobiology Laboratory, Centre Hospitalier Territorial Gaston Bourret, Nouméa, New CaledoniaInstitut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Paris, FranceABSTRACT An increasing number of isolations of Corynebacterium diphtheriae has been observed in recent years in the archipelago of New Caledonia. We aimed to analyze the clinical and microbiological features of samples with C. diphtheriae. All C. diphtheriae isolates identified in New Caledonia from May 2015 to May 2019 were included. For each case, a retrospective consultation of the patient files was conducted. Antimicrobial susceptibility phenotypes, tox gene and diphtheria toxin expression, biovar, and the genomic sequence were determined. Core genome multilocus sequence typing (cgMLST), 7-gene MLST, and search of genes of interest were performed from genomic assemblies. Fifty-eight isolates were included, with a median age of patients of 28 years (range: 9 days to 78 years). Cutaneous origin accounted for 51 of 58 (87.9%) isolates, and C. diphtheriae was associated with Staphylococcus aureus and/or Streptococcus pyogenes in three-quarters of cases. Half of cases came either from the main city Noumea (24%, 14/58) or from the sparsely populated island of Lifou (26%, 15/58). Six tox-positive isolates were identified, associated with recent travel to Vanuatu; 5 of these cases were linked and cgMLST confirmed recent transmission. Two cases of endocarditis in young female patients with a history of rheumatic fever involved tox-negative isolates. The 58 isolates were mostly susceptible to commonly used antibiotics. In particular, no isolate was resistant to the first-line molecules amoxicillin or erythromycin. Resistance to tetracycline was found in a genomic cluster of 17 (29%) isolates, 16 of which carried the tetO gene. There were 13 cgMLST sublineages, most of which were also observed in the neighboring country Australia. Cutaneous infections may harbor nontoxigenic C. diphtheriae isolates, which circulate largely silently in nonspecific wounds. The possible introduction of tox-positive strains from a neighboring island illustrates that diphtheria surveillance should be maintained in New Caledonia, and that immunization in neighboring islands must be improved. Genomic sequencing uncovers how genotypes circulate locally and across neighboring countries. IMPORTANCE The analysis of C. diphtheriae from the tropical archipelago of New Caledonia revealed a high genetic diversity with sublineages that may be linked to Polynesia, Australia, or metropolitan France. Genomic typing allowed confirming or excluding suspected transmission events among cases and contacts. A highly prevalent tetracycline-resistant sublineage harboring the tetO gene was uncovered. Toxigenic isolates were observed from patients returning from Vanuatu, showing the importance of improving vaccination coverage in settings where it is insufficient. This study also illustrates the importance for diphtheria surveillance of the inclusion of isolates from cutaneous sources in addition to respiratory cases, in order to provide a more complete epidemiological picture of the diversity and transmission of C. diphtheriae.https://journals.asm.org/doi/10.1128/spectrum.04616-22Corynebacterium diphtheriaediphtheriaNew Caledoniaclinical presentationgenomic epidemiologytropical island
spellingShingle Eve Tessier
Melanie Hennart
Edgar Badell
Virginie Passet
Julie Toubiana
Antoine Biron
Ann-Claire Gourinat
Audrey Merlet
Julien Colot
Sylvain Brisse
Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia
Microbiology Spectrum
Corynebacterium diphtheriae
diphtheria
New Caledonia
clinical presentation
genomic epidemiology
tropical island
title Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia
title_full Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia
title_fullStr Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia
title_full_unstemmed Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia
title_short Genomic Epidemiology of Corynebacterium diphtheriae in New Caledonia
title_sort genomic epidemiology of corynebacterium diphtheriae in new caledonia
topic Corynebacterium diphtheriae
diphtheria
New Caledonia
clinical presentation
genomic epidemiology
tropical island
url https://journals.asm.org/doi/10.1128/spectrum.04616-22
work_keys_str_mv AT evetessier genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT melaniehennart genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT edgarbadell genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT virginiepasset genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT julietoubiana genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT antoinebiron genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT annclairegourinat genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT audreymerlet genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT juliencolot genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia
AT sylvainbrisse genomicepidemiologyofcorynebacteriumdiphtheriaeinnewcaledonia