Global diversity and antimicrobial resistance of typhoid fever pathogens : insights from a meta-analysis of 13,000 Salmonella Typhi genomes

Carey, Megan E.; Dyson, Zoe A.; Ingle, Danielle J.; Amir, Afreenish; Aworh, Mabel K.; Chattaway, Marie Anne; Chew, Ka Lip; Crump, John A.; Feasey, Nicholas A.; Howden, Benjamin P.; Keddy, Karen H.; Maes, Mailis; Parry, Christopher M.; Van Puyvelde, Sandra; Webb, Hattie E.; Afolayan, Ayorinde Oluwatobiloba; Alexander, Anna P.; Anandan, Shalini; Andrews, Jason R.; Ashton, Philip M.; Basnyat, Buddha; Bavdekar, Ashish; Bogoch, Isaac I.; Clemens, John D.; Da Silva, Kesia Esther; De Ligt, Joep; Guevara, Paula Lucia Diaz; Dolecek, Christiane; Dutta, Shanta; Ehlers, Marthie Magdaleen; Watkins, Louise Francois; Garrett, Denise O.; Godbole, Gauri; Gordon, Melita A.; Greenhill, Andrew R.; Griffin, Chelsey; Gupta, Madhu; Hendriksen, Rene S.; Heyderman, Robert S.; Hooda, Yogesh; Hormazabal, Juan Carlos; Ikhimiukor, Odion O.; Iqbal, Junaid; Jacob, Jobin John; Jenkins, Claire; Jinka, Dasaratha Ramaiah; John, Jacob; Kang, Gagandeep; Kanteh, Abdoulie; Kapil, Arti; Karkey, Abhilasha; Kariuki, Samuel; Kingsley, Robert A.; Mary Koshy, Roshney; Lauer, A.C.; Levine, Myron M.; Lingegowda, Ravikumar Kadahalli; Luby, Stephen P.; Mackenzie, Grant Austin; Mashe, Tapfumanei; Msefula, Chisomo; Mutreja, Ankur; Nagaraj, Geetha; Nagaraj, Savitha; Nair, Satheesh; Naseri, Take K.; Nimarota-Brown, Susana; Njamkepo, Elisabeth; Okeke, Iruka N.; Perumal, Sulochana Putli Bai; Pollard, Andrew J.; Pragasam, Agila Kumari; Qadri, Firdausi; Qamar, Farah N.; Rahman, Sadia Isfat Ara; Rambocus, Savitra Devi; Rasko, David A.; Ray, Pallab; Robins-Browne, Roy; Rongsen-Chandola, Temsunaro; Rutanga, Jean Pierre; Saha, Samir K.; Saha, Senjuti; Saigal, Karnika; Sajib, Mohammad Saiful Islam; Seidman, Jessica C.; Shakya, Jivan; Shamanna, Varun; Shastri, Jayanthi; Shrestha, Rajeev; Sia, Sonia; Sikorski, Michael J.; Singh, Ashita; Smith, .Anthony M.; Tagg, Kaitlin A.; Tamrakar, Dipesh; Tanmoy, Arif Mohammed; Thomas, Maria; Thomas, Mathew S.; Thomsen, Robert; Thomson, Nicholas R.; Tupua, Siaosi; Vaidya, Krista; Valcanis, Mary; Veeraraghavan, Balaji; Weill, Francois-Xavier; Wright, Jackie; Dougan, Gordon; Argimon, Silvia; Keane, Jacqueline A.; Aanensen, David M.; Baker, Stephen; Holt, Kathryn E.; Global Typhoid Genomics Consortium Group Authorship

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Global diversity and antimicrobial resistance of typhoid fever pathogens : insights from a meta-analysis of 13,000 Salmonella Typhi genomes

Carey, Megan E.; Dyson, Zoe A.; Ingle, Danielle J.; Amir, Afreenish; Aworh, Mabel K.; Chattaway, Marie Anne; Chew, Ka Lip; Crump, John A.; Feasey, Nicholas A.; Howden, Benjamin P.; Keddy, Karen H.; Maes, Mailis; Parry, Christopher M.; Van Puyvelde, Sandra; Webb, Hattie E.; Afolayan, Ayorinde Oluwatobiloba; Alexander, Anna P.; Anandan, Shalini; Andrews, Jason R.; Ashton, Philip M.; Basnyat, Buddha; Bavdekar, Ashish; Bogoch, Isaac I.; Clemens, John D.; Da Silva, Kesia Esther; De Ligt, Joep; Guevara, Paula Lucia Diaz; Dolecek, Christiane; Dutta, Shanta; Ehlers, Marthie Magdaleen; Watkins, Louise Francois; Garrett, Denise O.; Godbole, Gauri; Gordon, Melita A.; Greenhill, Andrew R.; Griffin, Chelsey; Gupta, Madhu; Hendriksen, Rene S.; Heyderman, Robert S.; Hooda, Yogesh; Hormazabal, Juan Carlos; Ikhimiukor, Odion O.; Iqbal, Junaid; Jacob, Jobin John; Jenkins, Claire; Jinka, Dasaratha Ramaiah; John, Jacob; Kang, Gagandeep; Kanteh, Abdoulie; Kapil, Arti; Karkey, Abhilasha; Kariuki, Samuel; Kingsley, Robert A.; Mary Koshy, Roshney; Lauer, A.C.; Levine, Myron M.; Lingegowda, Ravikumar Kadahalli; Luby, Stephen P.; Mackenzie, Grant Austin; Mashe, Tapfumanei; Msefula, Chisomo; Mutreja, Ankur; Nagaraj, Geetha; Nagaraj, Savitha; Nair, Satheesh; Naseri, Take K.; Nimarota-Brown, Susana; Njamkepo, Elisabeth; Okeke, Iruka N.; Perumal, Sulochana Putli Bai; Pollard, Andrew J.; Pragasam, Agila Kumari; Qadri, Firdausi; Qamar, Farah N.; Rahman, Sadia Isfat Ara; Rambocus, Savitra Devi; Rasko, David A.; Ray, Pallab; Robins-Browne, Roy; Rongsen-Chandola, Temsunaro; Rutanga, Jean Pierre; Saha, Samir K.; Saha, Senjuti; Saigal, Karnika; Sajib, Mohammad Saiful Islam; Seidman, Jessica C.; Shakya, Jivan; Shamanna, Varun; Shastri, Jayanthi; Shrestha, Rajeev; Sia, Sonia; Sikorski, Michael J.; Singh, Ashita; Smith, .Anthony M.; Tagg, Kaitlin A.; Tamrakar, Dipesh; Tanmoy, Arif Mohammed; Thomas, Maria; Thomas, Mathew S.; Thomsen, Robert; Thomson, Nicholas R.; Tupua, Siaosi; Vaidya, Krista; Valcanis, Mary; Veeraraghavan, Balaji; Weill, Francois-Xavier; Wright, Jackie; Dougan, Gordon; Argimon, Silvia; Keane, Jacqueline A.; Aanensen, David M.; Baker, Stephen; Holt, Kathryn E.; Global Typhoid Genomics Consortium Group Authorship

URI: http://hdl.handle.net/2263/98652

Date: 2023-09-12

Abstract:

BACKGROUND : The Global Typhoid Genomics Consortium was established to bring together the typhoid research community to aggregate and analyse Salmonella enterica serovar Typhi (Typhi) genomic data to inform public health action. This analysis, which marks 22 years since the publication of the first Typhi genome, represents the largest Typhi genome sequence collection to date (n=13,000). METHODS : This is a meta-analysis of global genotype and antimicrobial resistance (AMR) determinants extracted from previously sequenced genome data and analysed using consistent methods implemented in open analysis platforms GenoTyphi and Pathogenwatch. RESULTS : Compared with previous global snapshots, the data highlight that genotype 4.3.1 (H58) has not spread beyond Asia and Eastern/Southern Africa; in other regions, distinct genotypes dominate and have independently evolved AMR. Data gaps remain in many parts of the world, and we show the potential of travel-associated sequences to provide informal ‘sentinel’ surveillance for such locations. The data indicate that ciprofloxacin non-susceptibility (>1 resistance determinant) is widespread across geographies and genotypes, with high-level ciprofloxacin resistance (≥3 determinants) reaching 20% prevalence in South Asia. Extensively drug-resistant (XDR) typhoid has become dominant in Pakistan (70% in 2020) but has not yet become established elsewhere. Ceftriaxone resistance has emerged in eight non-XDR genotypes, including a ciprofloxacin-resistant lineage (4.3.1.2.1) in India. Azithromycin resistance mutations were detected at low prevalence in South Asia, including in two common ciprofloxacin-resistant genotypes. CONCLUSIONS : The consortium’s aim is to encourage continued data sharing and collaboration to monitor the emergence and global spread of AMR Typhi, and to inform decision-making around the introduction of typhoid conjugate vaccines (TCVs) and other prevention and control strategies.

Description:

DATA AVAILABILITY : All data analysed during this study are publicly accessible. Raw Illumina sequence reads have been submitted to the European Nucleotide Archive (ENA), and individual sequence accession numbers are listed in Supplementary file 2. The full set of n=13,000 genome assemblies generated for this study are available for download from FigShare: https://doi.org/10.26180/21431883. All assemblies of suitable quality (n=12,849) are included as public data in the online platform Pathogenwatch (https://pathogen.watch). The data are organised into collections, which each comprise a neighbour-joining phylogeny annotated with metadata, genotype, AMR determinants, and a linked map. Each contributing study has its own collection, browsable at https://pathogen.watch/collections/all?organismId= 90370. In addition, we have provided three large collections, each representing roughly a third of the total dataset presented in this study: Typhi 4.3.1.1 (https://pathogen.watch/collection/ 2b7mp173dd57-clade-4311), Typhi lineage 4 (excluding 4.3.1.1) (https://pathogen.watch/collection/ wgn6bp1c8bh6-clade-4-excluding-4311), and Typhi lineages 0-3 (https://pathogen.watch/collection/ 9o4bpn0418n3-clades-0-1-2-and-3). In addition, users can browse the full set of Typhi genomes in Pathogenwatch and select subsets of interest (e.g. by country, genotype, and/or resistance) to generate a collection including neighbour-joining tree for interactive exploration.

SUPPLEMENTARY FILES : Available at https://elifesciences.org/articles/85867/figures#content. SUPPLEMENTARY FILE 1. Details of local ethical approvals provided for studies that were unpublished at the time of contributing data to this consortium project. Most data are now published, and the citations for the original studies are provided here. National surveillance programs in Chile (Maes et al., 2022), Colombia (Guevara et al., 2021), France, New Zealand, and Nigeria (Ikhimiukor et al., 2022b) were exempt from local ethical approvals as these countries allow sharing of non-identifiable pathogen sequence data for surveillance purposes. The US CDC Internal Review Board confirmed their approval was not required for use in this project (#NCEZID-ARLT- 10/ 20/21-fa687). SUPPLEMENTARY FILE 2. Line list of 13,000 genomes included in the study. SUPPLEMENTARY FILE 3. Source information recorded for genomes included in the study. ^Indicates cases included in the definition of ‘assumed acute illness’. SUPPLEMENTARY FILE 4. Summary of genomes by country. SUPPLEMENTARY FILE 5. Genotype frequencies per region (N, %, 95% confidence interval; annual and aggregated, 2010–2020). SUPPLEMENTARY FILE 6. Genotype frequencies per country (N, %, 95% confidence interval; annual and aggregated, 2010–2020). SUPPLEMENTARY FILE 7. Antimicrobial resistance (AMR) frequencies per region (N, %, 95% confidence interval; aggregated 2010–2020). SUPPLEMENTARY FILE 8. Antimicrobial resistance (AMR) frequencies per country (N, %, 95% confidence interval; annual and aggregated, 2010–2020). SUPPLEMENTARY FILE 9. Laboratory code master list. Three letter laboratory codes assigned by the consortium.

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