New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam

ABSTRACT Nontyphoidal Salmonella (NTS), particularly Salmonella enterica serovar Typhimurium, is among the leading etiologic agents of bacterial enterocolitis globally and a well-characterized cause of invasive disease (iNTS) in sub-Saharan Africa. In contrast, S. Typhimurium is poorly defined in So...

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Autores principales: Alison E. Mather, Tu Le Thi Phuong, Yunfeng Gao, Simon Clare, Subhankar Mukhopadhyay, David A. Goulding, Nhu Tran Do Hoang, Ha Thanh Tuyen, Nguyen Phu Huong Lan, Corinne N. Thompson, Nguyen Hoang Thu Trang, Juan Carrique-Mas, Ngo Tri Tue, James I. Campbell, Maia A. Rabaa, Duy Pham Thanh, Katherine Harcourt, Ngo Thi Hoa, Nguyen Vinh Trung, Constance Schultsz, Gabriel G. Perron, John E. Coia, Derek J. Brown, Chinyere Okoro, Julian Parkhill, Nicholas R. Thomson, Nguyen Van Vinh Chau, Guy E. Thwaites, Duncan J. Maskell, Gordon Dougan, Linda J. Kenney, Stephen Baker
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:3bbcd25618ea44648ab03b5e85d1b0442021-11-15T15:58:20ZNew Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam10.1128/mBio.01056-182150-7511https://doaj.org/article/3bbcd25618ea44648ab03b5e85d1b0442018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01056-18https://doaj.org/toc/2150-7511ABSTRACT Nontyphoidal Salmonella (NTS), particularly Salmonella enterica serovar Typhimurium, is among the leading etiologic agents of bacterial enterocolitis globally and a well-characterized cause of invasive disease (iNTS) in sub-Saharan Africa. In contrast, S. Typhimurium is poorly defined in Southeast Asia, a known hot spot for zoonotic disease with a recently described burden of iNTS disease. Here, we aimed to add insight into the epidemiology and potential impact of zoonotic transfer and antimicrobial resistance (AMR) in S. Typhimurium associated with iNTS and enterocolitis in Vietnam. We performed whole-genome sequencing and phylogenetic reconstruction on 85 human (enterocolitis, carriage, and iNTS) and 113 animal S. Typhimurium isolates isolated in Vietnam. We found limited evidence for the zoonotic transmission of S. Typhimurium. However, we describe a chain of events where a pandemic monophasic variant of S. Typhimurium (serovar I:4,[5],12:i:− sequence type 34 [ST34]) has been introduced into Vietnam, reacquired a phase 2 flagellum, and acquired an IncHI2 multidrug-resistant plasmid. Notably, these novel biphasic ST34 S. Typhimurium variants were significantly associated with iNTS in Vietnamese HIV-infected patients. Our study represents the first characterization of novel iNTS organisms isolated outside sub-Saharan Africa and outlines a new pathway for the emergence of alternative Salmonella variants into susceptible human populations. IMPORTANCE Salmonella Typhimurium is a major diarrheal pathogen and associated with invasive nontyphoid Salmonella (iNTS) disease in vulnerable populations. We present the first characterization of iNTS organisms in Southeast Asia and describe a different evolutionary trajectory from that of organisms causing iNTS in sub-Saharan Africa. In Vietnam, the globally distributed monophasic variant of Salmonella Typhimurium, the serovar I:4,[5],12:i:− ST34 clone, has reacquired a phase 2 flagellum and gained a multidrug-resistant plasmid to become associated with iNTS disease in HIV-infected patients. We document distinct communities of S. Typhimurium and I:4,[5],12:i:− in animals and humans in Vietnam, despite the greater mixing of these host populations here. These data highlight the importance of whole-genome sequencing surveillance in a One Health context in understanding the evolution and spread of resistant bacterial infections.Alison E. MatherTu Le Thi PhuongYunfeng GaoSimon ClareSubhankar MukhopadhyayDavid A. GouldingNhu Tran Do HoangHa Thanh TuyenNguyen Phu Huong LanCorinne N. ThompsonNguyen Hoang Thu TrangJuan Carrique-MasNgo Tri TueJames I. CampbellMaia A. RabaaDuy Pham ThanhKatherine HarcourtNgo Thi HoaNguyen Vinh TrungConstance SchultszGabriel G. PerronJohn E. CoiaDerek J. BrownChinyere OkoroJulian ParkhillNicholas R. ThomsonNguyen Van Vinh ChauGuy E. ThwaitesDuncan J. MaskellGordon DouganLinda J. KenneyStephen BakerAmerican Society for MicrobiologyarticleSalmonella Typhimuriumantimicrobial resistancegenomicsinvasive salmonellosisMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution DOAJ
collection DOAJ
language EN
topic Salmonella Typhimurium
antimicrobial resistance
genomics
invasive salmonellosis
Microbiology
QR1-502
spellingShingle Salmonella Typhimurium
antimicrobial resistance
genomics
invasive salmonellosis
Microbiology
QR1-502
Alison E. Mather
Tu Le Thi Phuong
Yunfeng Gao
Simon Clare
Subhankar Mukhopadhyay
David A. Goulding
Nhu Tran Do Hoang
Ha Thanh Tuyen
Nguyen Phu Huong Lan
Corinne N. Thompson
Nguyen Hoang Thu Trang
Juan Carrique-Mas
Ngo Tri Tue
James I. Campbell
Maia A. Rabaa
Duy Pham Thanh
Katherine Harcourt
Ngo Thi Hoa
Nguyen Vinh Trung
Constance Schultsz
Gabriel G. Perron
John E. Coia
Derek J. Brown
Chinyere Okoro
Julian Parkhill
Nicholas R. Thomson
Nguyen Van Vinh Chau
Guy E. Thwaites
Duncan J. Maskell
Gordon Dougan
Linda J. Kenney
Stephen Baker
New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam
description ABSTRACT Nontyphoidal Salmonella (NTS), particularly Salmonella enterica serovar Typhimurium, is among the leading etiologic agents of bacterial enterocolitis globally and a well-characterized cause of invasive disease (iNTS) in sub-Saharan Africa. In contrast, S. Typhimurium is poorly defined in Southeast Asia, a known hot spot for zoonotic disease with a recently described burden of iNTS disease. Here, we aimed to add insight into the epidemiology and potential impact of zoonotic transfer and antimicrobial resistance (AMR) in S. Typhimurium associated with iNTS and enterocolitis in Vietnam. We performed whole-genome sequencing and phylogenetic reconstruction on 85 human (enterocolitis, carriage, and iNTS) and 113 animal S. Typhimurium isolates isolated in Vietnam. We found limited evidence for the zoonotic transmission of S. Typhimurium. However, we describe a chain of events where a pandemic monophasic variant of S. Typhimurium (serovar I:4,[5],12:i:− sequence type 34 [ST34]) has been introduced into Vietnam, reacquired a phase 2 flagellum, and acquired an IncHI2 multidrug-resistant plasmid. Notably, these novel biphasic ST34 S. Typhimurium variants were significantly associated with iNTS in Vietnamese HIV-infected patients. Our study represents the first characterization of novel iNTS organisms isolated outside sub-Saharan Africa and outlines a new pathway for the emergence of alternative Salmonella variants into susceptible human populations. IMPORTANCE Salmonella Typhimurium is a major diarrheal pathogen and associated with invasive nontyphoid Salmonella (iNTS) disease in vulnerable populations. We present the first characterization of iNTS organisms in Southeast Asia and describe a different evolutionary trajectory from that of organisms causing iNTS in sub-Saharan Africa. In Vietnam, the globally distributed monophasic variant of Salmonella Typhimurium, the serovar I:4,[5],12:i:− ST34 clone, has reacquired a phase 2 flagellum and gained a multidrug-resistant plasmid to become associated with iNTS disease in HIV-infected patients. We document distinct communities of S. Typhimurium and I:4,[5],12:i:− in animals and humans in Vietnam, despite the greater mixing of these host populations here. These data highlight the importance of whole-genome sequencing surveillance in a One Health context in understanding the evolution and spread of resistant bacterial infections.
format article
author Alison E. Mather
Tu Le Thi Phuong
Yunfeng Gao
Simon Clare
Subhankar Mukhopadhyay
David A. Goulding
Nhu Tran Do Hoang
Ha Thanh Tuyen
Nguyen Phu Huong Lan
Corinne N. Thompson
Nguyen Hoang Thu Trang
Juan Carrique-Mas
Ngo Tri Tue
James I. Campbell
Maia A. Rabaa
Duy Pham Thanh
Katherine Harcourt
Ngo Thi Hoa
Nguyen Vinh Trung
Constance Schultsz
Gabriel G. Perron
John E. Coia
Derek J. Brown
Chinyere Okoro
Julian Parkhill
Nicholas R. Thomson
Nguyen Van Vinh Chau
Guy E. Thwaites
Duncan J. Maskell
Gordon Dougan
Linda J. Kenney
Stephen Baker
author_facet Alison E. Mather
Tu Le Thi Phuong
Yunfeng Gao
Simon Clare
Subhankar Mukhopadhyay
David A. Goulding
Nhu Tran Do Hoang
Ha Thanh Tuyen
Nguyen Phu Huong Lan
Corinne N. Thompson
Nguyen Hoang Thu Trang
Juan Carrique-Mas
Ngo Tri Tue
James I. Campbell
Maia A. Rabaa
Duy Pham Thanh
Katherine Harcourt
Ngo Thi Hoa
Nguyen Vinh Trung
Constance Schultsz
Gabriel G. Perron
John E. Coia
Derek J. Brown
Chinyere Okoro
Julian Parkhill
Nicholas R. Thomson
Nguyen Van Vinh Chau
Guy E. Thwaites
Duncan J. Maskell
Gordon Dougan
Linda J. Kenney
Stephen Baker
author_sort Alison E. Mather
title New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam
title_short New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam
title_full New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam
title_fullStr New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam
title_full_unstemmed New Variant of Multidrug-Resistant <italic toggle="yes">Salmonella enterica</italic> Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam
title_sort new variant of multidrug-resistant <italic toggle="yes">salmonella enterica</italic> serovar typhimurium associated with invasive disease in immunocompromised patients in vietnam
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/3bbcd25618ea44648ab03b5e85d1b044
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