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; Hoang, Nhu Tran Do; Tuyen, Ha Thanh; Lan, Nguyen Phu Huong; Thompson, Corinne N; +22 more...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 GORCID logo; Coia, John E; Brown, Derek J; Okoro, Chinyere; Parkhill, JulianORCID logo; Thomson, Nicholas RORCID logo; Chau, Nguyen Van Vinh; Thwaites, Guy E; Maskell, Duncan J; Dougan, Gordon; Kenney, Linda JORCID logo; and Baker, Stephen (2018) New Variant of Multidrug-Resistant Salmonella enterica Serovar Typhimurium Associated with Invasive Disease in Immunocompromised Patients in Vietnam. MBIO, 9 (5). ISSN 2150-7511 DOI: 10.1128/mBio.01056-18
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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.IMPORTANCESalmonella 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.


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