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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American Society for Microbiology
2018
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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) |
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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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