New variant of multidrug-resistant Salmonella enterica serovar typhimurium associated with invasive disease in immunocompromised patients in Vietnam

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 SchultszGabriel 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 Kenney, Stephen Baker

Research output: Contribution to journalArticle

4 Citations (Scopus)

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 de-scribe 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.

Original languageEnglish (US)
Article numbere01056-18
JournalmBio
Volume9
Issue number5
DOIs
StatePublished - Sep 1 2018
Externally publishedYes

Fingerprint

Salmonella enterica
Vietnam
Immunocompromised Host
Salmonella
Enterocolitis
Africa South of the Sahara
Zoonoses
Salmonella typhimurium
Southeastern Asia
Flagella
Serogroup
Plasmids
HIV
Genome
Pandemics
Vulnerable Populations
Bacterial Infections
Population
Epidemiology
Clone Cells

Keywords

  • Antimicrobial resistance
  • Genomics
  • Invasive salmonellosis
  • Salmonella typhimurium

ASJC Scopus subject areas

  • Microbiology
  • Virology

Cite this

Mather, A. E., Phuong, T. L. T., Gao, Y., Clare, S., Mukhopadhyay, S., Goulding, D. A., ... Baker, S. (2018). New variant of multidrug-resistant Salmonella enterica serovar typhimurium associated with invasive disease in immunocompromised patients in Vietnam. mBio, 9(5), [e01056-18]. https://doi.org/10.1128/mBio.01056-18

New variant of multidrug-resistant Salmonella enterica serovar typhimurium associated with invasive disease in immunocompromised patients in Vietnam. / Mather, Alison E.; Phuong, Tu Le Thi; Gao, Yunfeng; Clare, Simon; Mukhopadhyay, Subhankar; Goulding, David A.; Do Hoang, Nhu Tran; Tuyen, Ha Thanh; Lan, Nguyen Phu Huong; Thompson, Corinne N.; Trang, Nguyen Hoang Thu; Carrique-Mas, Juan; Tue, Ngo Tri; Campbell, James I.; Rabaa, Maia A.; Thanh, Duy Pham; Harcourt, Katherine; Hoa, Ngo Thi; Trung, Nguyen Vinh; Schultsz, Constance; Perron, Gabriel G.; Coia, John E.; Brown, Derek J.; Okoro, Chinyere; Parkhill, Julian; Thomson, Nicholas R.; Chau, Nguyen Van Vinh; Thwaites, Guy E.; Maskell, Duncan J.; Dougan, Gordon; Kenney, Linda; Baker, Stephen.

In: mBio, Vol. 9, No. 5, e01056-18, 01.09.2018.

Research output: Contribution to journalArticle

Mather, AE, Phuong, TLT, Gao, Y, Clare, S, Mukhopadhyay, S, Goulding, DA, Do Hoang, NT, Tuyen, HT, Lan, NPH, Thompson, CN, Trang, NHT, Carrique-Mas, J, Tue, NT, Campbell, JI, Rabaa, MA, Thanh, DP, Harcourt, K, Hoa, NT, Trung, NV, Schultsz, C, Perron, GG, Coia, JE, Brown, DJ, Okoro, C, Parkhill, J, Thomson, NR, Chau, NVV, Thwaites, GE, Maskell, DJ, Dougan, G, Kenney, L & Baker, S 2018, 'New variant of multidrug-resistant Salmonella enterica serovar typhimurium associated with invasive disease in immunocompromised patients in Vietnam', mBio, vol. 9, no. 5, e01056-18. https://doi.org/10.1128/mBio.01056-18
Mather, Alison E. ; Phuong, Tu Le Thi ; Gao, Yunfeng ; Clare, Simon ; Mukhopadhyay, Subhankar ; Goulding, David A. ; Do Hoang, Nhu Tran ; Tuyen, Ha Thanh ; Lan, Nguyen Phu Huong ; Thompson, Corinne N. ; Trang, Nguyen Hoang Thu ; Carrique-Mas, Juan ; Tue, Ngo Tri ; Campbell, James I. ; Rabaa, Maia A. ; Thanh, Duy Pham ; Harcourt, Katherine ; Hoa, Ngo Thi ; Trung, Nguyen Vinh ; Schultsz, Constance ; Perron, Gabriel G. ; Coia, John E. ; Brown, Derek J. ; Okoro, Chinyere ; Parkhill, Julian ; Thomson, Nicholas R. ; Chau, Nguyen Van Vinh ; Thwaites, Guy E. ; Maskell, Duncan J. ; Dougan, Gordon ; Kenney, Linda ; Baker, Stephen. / New variant of multidrug-resistant Salmonella enterica serovar typhimurium associated with invasive disease in immunocompromised patients in Vietnam. In: mBio. 2018 ; Vol. 9, No. 5.
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AU - Mather, Alison E.

AU - Phuong, Tu Le Thi

AU - Gao, Yunfeng

AU - Clare, Simon

AU - Mukhopadhyay, Subhankar

AU - Goulding, David A.

AU - Do Hoang, Nhu Tran

AU - Tuyen, Ha Thanh

AU - Lan, Nguyen Phu Huong

AU - Thompson, Corinne N.

AU - Trang, Nguyen Hoang Thu

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AU - Harcourt, Katherine

AU - Hoa, Ngo Thi

AU - Trung, Nguyen Vinh

AU - Schultsz, Constance

AU - Perron, Gabriel G.

AU - Coia, John E.

AU - Brown, Derek J.

AU - Okoro, Chinyere

AU - Parkhill, Julian

AU - Thomson, Nicholas R.

AU - Chau, Nguyen Van Vinh

AU - Thwaites, Guy E.

AU - Maskell, Duncan J.

AU - Dougan, Gordon

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