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Bacteriology

Genomic Serotyping, Clinical Manifestations, and Antimicrobial Resistance of Nontyphoidal Salmonella Gastroenteritis in Hospitalized Children in Ho Chi Minh City, Vietnam

Vu Thuy Duong, Hao Chung The, Tran Do Hoang Nhu, Ha Thanh Tuyen, James I. Campbell, Pham Van Minh, Hoang Le Phuc, Tran Thi Hong Chau, Nguyen Minh Ngoc, Lu Lan Vi, Alison E. Mather, Stephen Baker
Daniel J. Diekema, Editor
Vu Thuy Duong
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
bChildren’s Hospital No. 1, Ho Chi Minh City, Vietnam
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Hao Chung The
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
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Tran Do Hoang Nhu
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
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Ha Thanh Tuyen
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
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James I. Campbell
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
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Pham Van Minh
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
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Hoang Le Phuc
bChildren’s Hospital No. 1, Ho Chi Minh City, Vietnam
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Tran Thi Hong Chau
aThe Hospital for Tropical Diseases, Wellcome Trust Major Overseas Programme, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam
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Nguyen Minh Ngoc
cChildren’s Hospital No. 2, Ho Chi Minh City, Vietnam
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Lu Lan Vi
dThe Hospital for Tropical Diseases, Ho Chi Minh City, Vietnam
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Alison E. Mather
eQuadram Institute Bioscience, Norwich, United Kingdom
fUniversity of East Anglia, Norwich, United Kingdom
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Stephen Baker
gCambridge Institute of Therapeutic Immunology & Infectious Disease (CITIID), University of Cambridge, Cambridge, United Kingdom
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  • ORCID record for Stephen Baker
Daniel J. Diekema
University of Iowa College of Medicine
Roles: Editor
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DOI: 10.1128/JCM.01465-20
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  • FIG 1
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    FIG 1

    Monthly hospitalization incidence of nontyphoidal Salmonella. Only the eight most common sequence types are visualized. Sequence types that caused fewer than 10 incidences are grouped together as “Other.”

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    FIG 2

    Antimicrobial resistance in major nontyphoidal Salmonella sequence types. (A) Heat map of antimicrobial resistance phenotype of the eight most common sequence types. The left panel displays the proportion of nonsusceptibility to 7 classes of tested antimicrobial agents, including ampicillin/amoxicillin-clavulanate (AMP/AMC), ceftriaxone-ceftazidime (CRO/CAZ), imipenem (IMP), azithromycin (AZM), ciprofloxacin (CIP); trimethoprim-sulfamethoxazole (SXT), and chloramphenicol (CHL). The right panel displays the proportion of nonsusceptibility to the number of tested antimicrobial classes, including β-lactam (AMP, AMC, CRO, and CAZ), IMP, AZM, CIP, SXT, and CHL. Isolates were classified as nonsusceptible to an antimicrobial class if they were nonsusceptible to any agent of that class. The color intensity in a cell is proportional to the percentage of nonsusceptible NTS isolates to the tested antimicrobial class. The STs are arranged in decreasing order of prevalence (from top to bottom). (B) The prevalence of antimicrobial resistance determinants in the eight most common sequence types. These determinants are classified by antimicrobial classes, including 3rd-generation cephalosporin (blaCTX-M-14, blaCTX-M-15, and blaCTX-M-55), quinolone [qnrS1, qnrS2, qnrB6, qnrD1, oqxAB, patA, aac(6′)-Ib-cr, and QRDR mutations], azithromycin (ermB, ermF, ermT, mefB, and mphA), and cotrimoxazole (sul1, sul2, and sul3 plus + dfrA1, dfrA12, dfrA14, dfrA17, and dfrA5). Each bar graph denotes the proportion of isolates carrying any of these determinants, classified by antimicrobial class and sequence type.

  • FIG 3
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    FIG 3

    Resistance to first-line antimicrobials correlated with clinical severity. (A and B) Hospitalization duration (in days) of all 450 children infected with nontyphoidal Salmonella, classified by the number of first- and second-line antimicrobials (ciprofloxacin, ceftriaxone, azithromycin) to which the pathogen was phenotypically nonsusceptible (A), further classified by the eight most common sequence types (B). (C) Hospitalization duration of NTS infected children who received initial treatment of fluoroquinolone (CIP), 3rd-generation cephalosporin (CRO), or macrolide (AZM), stratified by the pathogen’s nonsusceptibility to the corresponding treating agent (ciprofloxacin, ceftriaxone, or azithromycin). The asterisk indicates statistical significance in the pairwise comparison (Wilcoxon signed-rank test, P < 0.05).

Tables

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  • TABLE 1

    Demographic and clinical manifestations of diarrheal pediatric patients infected with nontyphoidal Salmonella (n = 450)

    TABLE 1
    • ↵a Obese signifies weight-for-length Z score >3 SD in children aged <24 months; body mass index (BMI)-for-age Z score >3 SD in children aged ≥24 months. Overweight represents weight-for-length Z score >2 SD in children of age <24 months; BMI-for-age Z score >2 SD in children aged ≥24 months. Wasted signifies weight-for-length Z score less than −2 SD in children aged <24 months; BMI-for-age Z score less than −2 SD in children aged ≥24 months. Severely wasted signifies weight-for-length Z score less than −3 SD in children aged <24 months; BMI-for-age Z score less than −3 SD in children aged ≥24 months (30).

    • ↵b All of the dehydrated cases classified as some dehydration according to Integrated Management of Childhood Illness (31).

    • ↵c Hemoglobin level cutoff according to World Health Organization guidelines (18).

    • ↵d Defined as “recovered” if patient had <3 passages of loose stool in the 24 hours or “improved” if patient had less episodes of diarrhea and less mucus and/or bloody in comparison to the condition of the patient at enrollment.

  • TABLE 2

    Nontyphoidal Salmonella predicted serovars isolated from children with diarrheal diseases in three tertiary hospitals in Ho Chi Minh City (n = 450)a

    TABLE 2
    • ↵a Antigenic formulas are given in parentheses.

    • ↵b Monophasic.

  • TABLE 3

    The performance of whole-genome sequencing in determining the antimicrobial susceptibility of nontyphoidal Salmonella

    TABLE 3
    • ↵a Full resistance and intermediate resistance are included as nonsusceptible.

    • ↵b Quinolone resistance-determining region (QRDR) consists of gyrA-83 plus gyrA-87 plus parC-80.

    • ↵c Plasmid-mediated quinolone resistance genes (PMQR) include qnrB6, qnrD1, qnrS1, qnrS2, oqx_AB, patA, and aac(6′)-Ib-cr.

Additional Files

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      Tables S1 and S2 and Fig. S1

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Genomic Serotyping, Clinical Manifestations, and Antimicrobial Resistance of Nontyphoidal Salmonella Gastroenteritis in Hospitalized Children in Ho Chi Minh City, Vietnam
Vu Thuy Duong, Hao Chung The, Tran Do Hoang Nhu, Ha Thanh Tuyen, James I. Campbell, Pham Van Minh, Hoang Le Phuc, Tran Thi Hong Chau, Nguyen Minh Ngoc, Lu Lan Vi, Alison E. Mather, Stephen Baker
Journal of Clinical Microbiology Nov 2020, 58 (12) e01465-20; DOI: 10.1128/JCM.01465-20

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Genomic Serotyping, Clinical Manifestations, and Antimicrobial Resistance of Nontyphoidal Salmonella Gastroenteritis in Hospitalized Children in Ho Chi Minh City, Vietnam
Vu Thuy Duong, Hao Chung The, Tran Do Hoang Nhu, Ha Thanh Tuyen, James I. Campbell, Pham Van Minh, Hoang Le Phuc, Tran Thi Hong Chau, Nguyen Minh Ngoc, Lu Lan Vi, Alison E. Mather, Stephen Baker
Journal of Clinical Microbiology Nov 2020, 58 (12) e01465-20; DOI: 10.1128/JCM.01465-20
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    • ABSTRACT
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KEYWORDS

nontyphoidal Salmonella
Salmonella serovars
genomic serotyping
pediatric diarrhea
antimicrobial resistance
multidrug resistance

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