Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study

<p><strong>Background</strong> Enteric fever, a systemic infection caused by <i>Salmonella enterica</i> serovars Typhi and Paratyphi A, remains a major cause of morbidity and mortality in low-income and middle-income countries. Enteric fever is preventable through the p...

Full description

Bibliographic Details
Main Authors: Browne, AJ, Chipeta, MG, Fell, FJ, Haines-Woodhouse, G, Kashef Hamadani, BH, Kumaran, EAP, Robles Aguilar, G, McManigal, B, Ashley, EA, Basnyat, B, Chansamouth, V, Dunachie, SJ, Henry, NJ, Karkey, A, Mayxay, M, Newton, PN, Phommasone, K, Pokharel, S, Pollard, AJ, Roberts, T, Shakya, M, Turner, C, Day, NPJ, Sartorius, B, Dolecek, C
Other Authors: GRAM Typhoid Collaborators
Format: Journal article
Language:English
Published: Elsevier 2024
_version_ 1826312691396902912
author Browne, AJ
Chipeta, MG
Fell, FJ
Haines-Woodhouse, G
Kashef Hamadani, BH
Kumaran, EAP
Robles Aguilar, G
McManigal, B
Ashley, EA
Basnyat, B
Chansamouth, V
Dunachie, SJ
Henry, NJ
Karkey, A
Mayxay, M
Newton, PN
Phommasone, K
Pokharel, S
Pollard, AJ
Roberts, T
Shakya, M
Turner, C
Day, NPJ
Sartorius, B
Dolecek, C
author2 GRAM Typhoid Collaborators
author_facet GRAM Typhoid Collaborators
Browne, AJ
Chipeta, MG
Fell, FJ
Haines-Woodhouse, G
Kashef Hamadani, BH
Kumaran, EAP
Robles Aguilar, G
McManigal, B
Ashley, EA
Basnyat, B
Chansamouth, V
Dunachie, SJ
Henry, NJ
Karkey, A
Mayxay, M
Newton, PN
Phommasone, K
Pokharel, S
Pollard, AJ
Roberts, T
Shakya, M
Turner, C
Day, NPJ
Sartorius, B
Dolecek, C
author_sort Browne, AJ
collection OXFORD
description <p><strong>Background</strong> Enteric fever, a systemic infection caused by <i>Salmonella enterica</i> serovars Typhi and Paratyphi A, remains a major cause of morbidity and mortality in low-income and middle-income countries. Enteric fever is preventable through the provision of clean water and adequate sanitation and can be successfully treated with antibiotics. However, high levels of antimicrobial resistance (AMR) compromise the effectiveness of treatment. We provide estimates of the prevalence of AMR <i>S</i> Typhi and <i>S</i> Paratyphi A in 75 endemic countries, including 30 locations without data.</p> <p><strong>Methods</strong> We used a Bayesian spatiotemporal modelling framework to estimate the percentage of multidrug resistance (MDR), fluoroquinolone non-susceptibility (FQNS), and third-generation cephalosporin resistance in <i>S</i> Typhi and <i>S</i> Paratyphi A infections for 1403 administrative level one districts in 75 endemic countries from 1990 to 2019. We incorporated data from a comprehensive systematic review, public health surveillance networks, and large multicountry studies on enteric fever. Estimates of the prevalence of AMR and the number of AMR infections (based on enteric fever incidence estimates by the Global Burden of Diseases study) were produced at the country, super-region, and total endemic area level for each year of the study.</p> <p><strong>Findings</strong> We collated data from 601 sources, comprising 184 225 isolates of <i>S</i> Typhi and <i>S</i> Paratyphi A, covering 45 countries over 30 years. We identified a decline of MDR <i>S</i> Typhi in south Asia and southeast Asia, whereas in sub-Saharan Africa, the overall prevalence increased from 6·0% (95% uncertainty interval 4·3–8·0) in 1990 to 72·7% (67·7–77·3) in 2019. Starting from low levels in 1990, the prevalence of FQNS <i>S</i> Typhi increased rapidly, reaching 95·2% (91·4–97·7) in south Asia in 2019. This corresponded to 2·5 million (1·5–3·8) MDR <i>S</i> Typhi infections and 7·4 million (4·7–11·3) FQNS <i>S</i> Typhi infections in endemic countries in 2019. The prevalence of third-generation cephalosporin-resistant <i>S</i> Typhi remained low across the whole endemic area over the study period, except for Pakistan where prevalence of third-generation cephalosporin resistance in <i>S</i> Typhi reached 61·0% (58·0–63·8) in 2019. For <i>S</i> Paratyphi A, we estimated low prevalence of MDR and third-generation cephalosporin resistance in all endemic countries, but a drastic increase of FQNS, which reached 95·0% (93·7–96·1; 3·5 million [2·2–5·6] infections) in 2019.</p> <p><strong>Interpretation</strong> This study provides a comprehensive and detailed analysis of the prevalence of MDR, FQNS, and third-generation cephalosporin resistance in <i>S</i> Typhi and <i>S</i> Paratyphi A infections in endemic countries, spanning the last 30 years. Our analysis highlights the increasing levels of AMR in this preventable infection and serves as a resource to guide urgently needed public health interventions, such as improvements in water, sanitation, and hygiene and typhoid fever vaccination campaigns.</p> <p><strong>Funding</strong> Fleming Fund, UK Department of Health and Social Care; Wellcome Trust; and Bill and Melinda Gates Foundation.</p>
first_indexed 2024-04-09T03:58:20Z
format Journal article
id oxford-uuid:b67dc431-4111-41d8-88c4-1f66ee7c8350
institution University of Oxford
language English
last_indexed 2024-04-09T03:58:20Z
publishDate 2024
publisher Elsevier
record_format dspace
spelling oxford-uuid:b67dc431-4111-41d8-88c4-1f66ee7c83502024-03-27T14:48:14ZEstimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling studyJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:b67dc431-4111-41d8-88c4-1f66ee7c8350EnglishSymplectic ElementsElsevier2024Browne, AJChipeta, MGFell, FJHaines-Woodhouse, GKashef Hamadani, BHKumaran, EAPRobles Aguilar, GMcManigal, BAshley, EABasnyat, BChansamouth, VDunachie, SJHenry, NJKarkey, AMayxay, MNewton, PNPhommasone, KPokharel, SPollard, AJRoberts, TShakya, MTurner, CDay, NPJSartorius, BDolecek, CGRAM Typhoid Collaborators<p><strong>Background</strong> Enteric fever, a systemic infection caused by <i>Salmonella enterica</i> serovars Typhi and Paratyphi A, remains a major cause of morbidity and mortality in low-income and middle-income countries. Enteric fever is preventable through the provision of clean water and adequate sanitation and can be successfully treated with antibiotics. However, high levels of antimicrobial resistance (AMR) compromise the effectiveness of treatment. We provide estimates of the prevalence of AMR <i>S</i> Typhi and <i>S</i> Paratyphi A in 75 endemic countries, including 30 locations without data.</p> <p><strong>Methods</strong> We used a Bayesian spatiotemporal modelling framework to estimate the percentage of multidrug resistance (MDR), fluoroquinolone non-susceptibility (FQNS), and third-generation cephalosporin resistance in <i>S</i> Typhi and <i>S</i> Paratyphi A infections for 1403 administrative level one districts in 75 endemic countries from 1990 to 2019. We incorporated data from a comprehensive systematic review, public health surveillance networks, and large multicountry studies on enteric fever. Estimates of the prevalence of AMR and the number of AMR infections (based on enteric fever incidence estimates by the Global Burden of Diseases study) were produced at the country, super-region, and total endemic area level for each year of the study.</p> <p><strong>Findings</strong> We collated data from 601 sources, comprising 184 225 isolates of <i>S</i> Typhi and <i>S</i> Paratyphi A, covering 45 countries over 30 years. We identified a decline of MDR <i>S</i> Typhi in south Asia and southeast Asia, whereas in sub-Saharan Africa, the overall prevalence increased from 6·0% (95% uncertainty interval 4·3–8·0) in 1990 to 72·7% (67·7–77·3) in 2019. Starting from low levels in 1990, the prevalence of FQNS <i>S</i> Typhi increased rapidly, reaching 95·2% (91·4–97·7) in south Asia in 2019. This corresponded to 2·5 million (1·5–3·8) MDR <i>S</i> Typhi infections and 7·4 million (4·7–11·3) FQNS <i>S</i> Typhi infections in endemic countries in 2019. The prevalence of third-generation cephalosporin-resistant <i>S</i> Typhi remained low across the whole endemic area over the study period, except for Pakistan where prevalence of third-generation cephalosporin resistance in <i>S</i> Typhi reached 61·0% (58·0–63·8) in 2019. For <i>S</i> Paratyphi A, we estimated low prevalence of MDR and third-generation cephalosporin resistance in all endemic countries, but a drastic increase of FQNS, which reached 95·0% (93·7–96·1; 3·5 million [2·2–5·6] infections) in 2019.</p> <p><strong>Interpretation</strong> This study provides a comprehensive and detailed analysis of the prevalence of MDR, FQNS, and third-generation cephalosporin resistance in <i>S</i> Typhi and <i>S</i> Paratyphi A infections in endemic countries, spanning the last 30 years. Our analysis highlights the increasing levels of AMR in this preventable infection and serves as a resource to guide urgently needed public health interventions, such as improvements in water, sanitation, and hygiene and typhoid fever vaccination campaigns.</p> <p><strong>Funding</strong> Fleming Fund, UK Department of Health and Social Care; Wellcome Trust; and Bill and Melinda Gates Foundation.</p>
spellingShingle Browne, AJ
Chipeta, MG
Fell, FJ
Haines-Woodhouse, G
Kashef Hamadani, BH
Kumaran, EAP
Robles Aguilar, G
McManigal, B
Ashley, EA
Basnyat, B
Chansamouth, V
Dunachie, SJ
Henry, NJ
Karkey, A
Mayxay, M
Newton, PN
Phommasone, K
Pokharel, S
Pollard, AJ
Roberts, T
Shakya, M
Turner, C
Day, NPJ
Sartorius, B
Dolecek, C
Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study
title Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study
title_full Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study
title_fullStr Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study
title_full_unstemmed Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study
title_short Estimating the subnational prevalence of antimicrobial resistant Salmonella enterica serovars Typhi and Paratyphi A infections in 75 endemic countries, 1990–2019: a modelling study
title_sort estimating the subnational prevalence of antimicrobial resistant salmonella enterica serovars typhi and paratyphi a infections in 75 endemic countries 1990 2019 a modelling study
work_keys_str_mv AT browneaj estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT chipetamg estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT fellfj estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT haineswoodhouseg estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT kashefhamadanibh estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT kumaraneap estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT roblesaguilarg estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT mcmanigalb estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT ashleyea estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT basnyatb estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT chansamouthv estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT dunachiesj estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT henrynj estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT karkeya estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT mayxaym estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT newtonpn estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT phommasonek estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT pokharels estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT pollardaj estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT robertst estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT shakyam estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT turnerc estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT daynpj estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT sartoriusb estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy
AT dolecekc estimatingthesubnationalprevalenceofantimicrobialresistantsalmonellaentericaserovarstyphiandparatyphiainfectionsin75endemiccountries19902019amodellingstudy