Persistence of Rare Salmonella Typhi Genotypes Susceptible to First-Line Antibiotics in the Remote Islands of Samoa
Michael J. Sikorski,
Tracy H. Hazen,
Sachin N. Desai,
Susana Nimarota-Brown,
Siaosi Tupua,
Michelle Sialeipata,
Savitra Rambocus,
Danielle J. Ingle,
Sebastian Duchene,
Susan A. Ballard,
Mary Valcanis,
Sara Zufan,
Jianguo Ma,
Jason W. Sahl,
Mailis Maes,
Gordon Dougan,
Robert E. Thomsen,
Roy M. Robins-Browne,
Benjamin P. Howden,
Take K. Naseri,
Myron M. Levine,
David A. Rasko
Affiliations
Michael J. Sikorski
Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
Tracy H. Hazen
Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
Sachin N. Desai
Center for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
Susana Nimarota-Brown
Ministry of Health, Government of Samoa, Apia, Samoa
Siaosi Tupua
Ministry of Health, Government of Samoa, Apia, Samoa
Michelle Sialeipata
Ministry of Health, Government of Samoa, Apia, Samoa
Savitra Rambocus
Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
Danielle J. Ingle
Department of Microbiology and Immunology at the Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Melbourne, Victoria, Australia
Sebastian Duchene
Department of Microbiology and Immunology at the Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Melbourne, Victoria, Australia
Susan A. Ballard
Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
Mary Valcanis
Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
Sara Zufan
Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
Jianguo Ma
Department of Geographical Sciences, University of Maryland, College Park, Maryland, USA
Jason W. Sahl
Pathogen & Microbiome Institute, Northern Arizona University, Flagstaff, Arizona, USA
Mailis Maes
Cambridge Institute of Therapeutic Immunology & Infectious Disease, Department of Medicine, University of Cambridge, Cambridge, United Kingdom
Gordon Dougan
Cambridge Institute of Therapeutic Immunology & Infectious Disease, Department of Medicine, University of Cambridge, Cambridge, United Kingdom
Robert E. Thomsen
Ministry of Health, Government of Samoa, Apia, Samoa
Roy M. Robins-Browne
Department of Microbiology and Immunology at the Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Melbourne, Victoria, Australia
Benjamin P. Howden
Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Victoria, Australia
Take K. Naseri
Ministry of Health, Government of Samoa, Apia, Samoa
Myron M. Levine
Center for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
David A. Rasko
Institute for Genome Sciences, University of Maryland School of Medicine, Baltimore, Maryland, USA
ABSTRACT For decades, the remote island nation of Samoa (population ~200,000) has faced endemic typhoid fever despite improvements in water quality, sanitation, and economic development. We recently described the epidemiology of typhoid fever in Samoa from 2008 to 2019 by person, place, and time; however, the local Salmonella enterica serovar Typhi (S. Typhi) population structure, evolutionary origins, and genomic features remained unknown. Herein, we report whole genome sequence analyses of 306 S. Typhi isolates from Samoa collected between 1983 and 2020. Phylogenetics revealed a dominant population of rare genotypes 3.5.4 and 3.5.3, together comprising 292/306 (95.4%) of Samoan versus 2/4934 (0.04%) global S. Typhi isolates. Three distinct 3.5.4 genomic sublineages were identified, and their defining polymorphisms were determined. These dominant Samoan genotypes, which likely emerged in the 1970s, share ancestry with other 3.5 clade isolates from South America, Southeast Asia, and Oceania. Additionally, a 106-kb pHCM2 phenotypically cryptic plasmid, detected in a 1992 Samoan S. Typhi isolate, was identified in 106/306 (34.6%) of Samoan isolates; this is more than double the observed proportion of pHCM2-containing isolates in the global collection. In stark contrast with global S. Typhi trends, resistance-conferring polymorphisms were detected in only 15/306 (4.9%) of Samoan S. Typhi, indicating overwhelming susceptibility to antibiotics that are no longer effective in most of South and Southeast Asia. This country-level genomic framework can help local health authorities in their ongoing typhoid surveillance and control efforts, as well as fill a critical knowledge gap in S. Typhi genomic data from Oceania. IMPORTANCE In this study, we used whole genome sequencing and comparative genomics analyses to characterize the population structure, evolutionary origins, and genomic features of S. Typhi associated with decades of endemic typhoid fever in Samoa. Our analyses of Samoan isolates from 1983 to 2020 identified a rare S. Typhi population in Samoa that likely emerged around the early 1970s and evolved into sublineages that are presently dominant. The dominance of these endemic genotypes in Samoa is not readily explained by genomic content or widespread acquisition of antimicrobial resistance. These data establish the necessary framework for future genomic surveillance of S. Typhi in Samoa for public health benefit.
