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

Author:

Carey Megan E123ORCID,Dyson Zoe A245ORCID,Ingle Danielle J6,Amir Afreenish7,Aworh Mabel K89,Chattaway Marie Anne10,Chew Ka Lip11,Crump John A12ORCID,Feasey Nicholas A1314,Howden Benjamin P1516ORCID,Keddy Karen H17,Maes Mailis1,Parry Christopher M13ORCID,Van Puyvelde Sandra118ORCID,Webb Hattie E19ORCID,Afolayan Ayorinde Oluwatobiloba20ORCID,Alexander Anna P21,Anandan Shalini22,Andrews Jason R23ORCID,Ashton Philip M2425,Basnyat Buddha26,Bavdekar Ashish27,Bogoch Isaac I28,Clemens John D29303132,da Silva Kesia Esther23,De Anuradha33ORCID,de Ligt Joep34,Diaz Guevara Paula Lucia35ORCID,Dolecek Christiane3637,Dutta Shanta38,Ehlers Marthie M3940,Francois Watkins Louise19ORCID,Garrett Denise O41,Godbole Gauri10,Gordon Melita A25,Greenhill Andrew R4243,Griffin Chelsey19,Gupta Madhu44,Hendriksen Rene S45,Heyderman Robert S46,Hooda Yogesh47,Hormazabal Juan Carlos48,Ikhimiukor Odion O20ORCID,Iqbal Junaid49ORCID,Jacob Jobin John22,Jenkins Claire10,Jinka Dasaratha Ramaiah50ORCID,John Jacob51,Kang Gagandeep51ORCID,Kanteh Abdoulie52,Kapil Arti53,Karkey Abhilasha26,Kariuki Samuel54ORCID,Kingsley Robert A55,Koshy Roshine Mary56,Lauer AC19,Levine Myron M57,Lingegowda Ravikumar Kadahalli58,Luby Stephen P23,Mackenzie Grant Austin52,Mashe Tapfumanei5960,Msefula Chisomo61ORCID,Mutreja Ankur1,Nagaraj Geetha58,Nagaraj Savitha62,Nair Satheesh10ORCID,Naseri Take K63,Nimarota-Brown Susana63,Njamkepo Elisabeth64,Okeke Iruka N20ORCID,Perumal Sulochana Putli Bai65,Pollard Andrew J6667,Pragasam Agila Kumari22,Qadri Firdausi30,Qamar Farah N49,Rahman Sadia Isfat Ara30,Rambocus Savitra Devi16,Rasko David A6869,Ray Pallab44,Robins-Browne Roy670,Rongsen-Chandola Temsunaro71,Rutanga Jean Pierre72,Saha Samir K47ORCID,Saha Senjuti47ORCID,Saigal Karnika73,Sajib Mohammad Saiful Islam4774,Seidman Jessica C41,Shakya Jivan7576,Shamanna Varun58,Shastri Jayanthi3377,Shrestha Rajeev78,Sia Sonia79,Sikorski Michael J576869,Singh Ashita80,Smith Anthony M81,Tagg Kaitlin A19,Tamrakar Dipesh78,Tanmoy Arif Mohammed47,Thomas Maria82,Thomas Mathew S83,Thomsen Robert63,Thomson Nicholas R5,Tupua Siaosi63,Vaidya Krista84,Valcanis Mary16,Veeraraghavan Balaji22,Weill François-Xavier64,Wright Jackie34,Dougan Gordon1,Argimón Silvia85,Keane Jacqueline A1,Aanensen David M85ORCID,Baker Stephen13,Holt Kathryn E24ORCID,

Affiliation:

1. Cambridge Institute of Therapeutic Immunology and Infectious Disease (CITIID), University of Cambridge School of Clinical Medicine, Cambridge Biomedical Campus

2. Department of Infection Biology, Faculty of Infectious and Tropical Diseases, London School of Hygiene & Tropical Medicine

3. IAVI, Chelsea & Westminster Hospital

4. Department of Infectious Diseases, Central Clinical School, Monash University

5. Wellcome Sanger Institute, Wellcome Genome Campus

6. Department of Microbiology and Immunology at the Peter Doherty Institute for Infection and Immunity, The University of Melbourne

7. National Institute of Health

8. Nigeria Field Epidemiology and Laboratory Training Programme

9. College of Veterinary Medicine, North Carolina State University

10. United Kingdom Health Security Agency

11. National University Hospital

12. Centre for International Health, University of Otago

13. Department of Clinical Sciences, Liverpool School of Tropical Medicine

14. Malawi-Liverpool Wellcome Programme, Kamuzu University of Health Sciences

15. Centre for Pathogen Genomics, Department of Microbiology and Immunology, University of Melbourne at Doherty Institute for Infection and Immunity

16. Microbiological Diagnostic Unit Public Health Laboratory, The University of Melbourne at the Peter Doherty Institute for Infection and Immunity

17. Independent consultant

18. University of Antwerp

19. Centers for Disease Control and Prevention

20. Global Health Research Unit (GHRU) for the Genomic Surveillance of Antimicrobial Resistance, Faculty of Pharmacy, University of Ibadan

21. Lady Willingdon Hospital

22. Department of Clinical Microbiology, Christian Medical College

23. Division of Infectious Diseases and Geographic Medicine, Stanford University

24. Malawi-Liverpool Wellcome Programme

25. Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool

26. Oxford University Clinical Research Unit Nepal

27. KEM Hospital Research Centre

28. Department of Medicine, Division of Infectious Diseases, University of Toronto

29. International Vaccine Institute

30. International Centre for Diarrhoeal Disease Research

31. UCLA Fielding School of Public Health

32. Korea University

33. Topiwala National Medical College

34. ESR, Institute of Environmental Science and Research Ltd., Porirua

35. Grupo de Microbiologia, Instituto Nacional de Salud

36. Centre for Tropical Medicine and Global Health, Nuffield Department of Medicine, University of Oxford

37. Mahidol Oxford Tropical Medicine Research Unit, Mahidol University

38. ICMR - National Institute of Cholera & Enteric Diseases

39. Department of Medical Microbiology, Faculty of Health Sciences, University of Pretoria

40. Department of Medical Microbiology, Tshwane Academic Division, National Health Laboratory Service

41. Sabin Vaccine Institute

42. Federation University Australia

43. Papua New Guinea Institute of Medical Research

44. Post Graduate Institute of Medical Education and Research

45. Technical University of Denmark

46. Research Department of Infection, Division of Infection and Immunity, University College London

47. Child Health Research Foundation

48. Bacteriologia, Subdepartamento de Enfermedades Infecciosas, Departamento de Laboratorio Biomedico, Instituto de Salud Publica de Chile (ISP)

49. Department of Pediatrics and Child Health, Aga Khan University

50. Rural Development Trust Hospital

51. Department of Community Health, Christian Medical College

52. Medical Research Council Unit The Gambia at London School Hygiene & Tropical Medicine

53. All India Institute of Medical Sciences

54. Centre for Microbiology Research, Kenya Medical Research Institute

55. Quadram Institute Bioscience

56. Makunda Christian Hospital

57. Center for Vaccine Development and Global Health (CVD), University of Maryland School of Medicine, Baltimore, Maryland, USA

58. Central Research Laboratory, Kempegowda Institute of Medical Sciences

59. National Microbiology Reference Laboratory

60. World Health Organization

61. Kamuzu University of Health Sciences

62. Saint Johns Medical College and Hospital

63. Ministry of Health, Government of Samoa

64. Institut Pasteur, Université Paris Cité

65. Kanchi Kamakoti CHILDS Trust Hospital

66. Oxford Vaccine Group, Department of Paediatrics, University of Oxford

67. The NIHR Oxford Biomedical Research Centre

68. Department of Microbiology and Immunology, University of Maryland School of Medicine

69. Institute for Genome Sciences, University of Maryland School of Medicine

70. Murdoch Children’s Research Institute, Royal Children’s Hospital

71. Centre for Health Research and Development, Society for Applied Studies

72. University of Rwanda, College of Science and Technology

73. Chacha Nehru Bal Chikitsalaya

74. Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow

75. Dhulikhel Hospital

76. Institute for Research in Science and Technology

77. Kasturba Hospital for Infectious Diseases

78. Center for Infectious Disease Research & Surveillance, Dhulikhel Hospital, Kathmandu University Hospital

79. Research Institute for Tropical Medicine, Department of Health

80. Chinchpada Christian Hospital

81. Centre for Enteric Diseases, National Institute for Communicable Diseases

82. Christian Medical College, Ludhiana

83. Duncan Hospital

84. University of California Davis

85. Centre for Genomic Pathogen Surveillance, Big Data Institute, University of Oxford

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.Funding:No specific funding was awarded for this meta-analysis. Coordinators were supported by fellowships from the European Union (ZAD received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No 845681), the Wellcome Trust (SB, Wellcome Trust Senior Fellowship), and the National Health and Medical Research Council (DJI is supported by an NHMRC Investigator Grant [GNT1195210]).

Funder

HORIZON EUROPE Marie Sklodowska-Curie Actions

Bill and Melinda Gates Foundation

Biotechnology and Biological Sciences Research Council

Wellcome Trust

National Institutes of Health

National Institute for Health Research

Canadian Institutes of Health Research

Department of Health and Social Care

UK Medical Research Council

Institut Pasteur and Santé Publique France

Medical Research Council

United States Department of Health and Human Services

Indian Council of Medical Research

World Health Organization and Gavi, the Vaccine Alliance

National Institute for Health and Care Research

Department for Health and Social Care, the Department for International Development/Global Challenges Research Fund, the UK Medical Research Council, and the Wellcome Trust

Bill & Melinda Gates Foundation

Wellcome

Publisher

eLife Sciences Publications, Ltd

Subject

General Immunology and Microbiology,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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