Global spatial dynamics and vaccine-induced fitness changes of Bordetella pertussis

Author:

Lefrancq Noémie12ORCID,Bouchez Valérie34ORCID,Fernandes Nadia3ORCID,Barkoff Alex-Mikael5,Bosch Thijs6,Dalby Tine7ORCID,Åkerlund Thomas8ORCID,Darenberg Jessica8ORCID,Fabianova Katerina9ORCID,Vestrheim Didrik F.10,Fry Norman K.1112ORCID,González-López Juan José1314ORCID,Gullsby Karolina15ORCID,Habington Adele16ORCID,He Qiushui517,Litt David11ORCID,Martini Helena18ORCID,Piérard Denis18ORCID,Stefanelli Paola19ORCID,Stegger Marc7ORCID,Zavadilova Jana20,Armatys Nathalie34ORCID,Landier Annie34ORCID,Guillot Sophie34,Hong Samuel L.21ORCID,Lemey Philippe21ORCID,Parkhill Julian22ORCID,Toubiana Julie3423,Cauchemez Simon1ORCID,Salje Henrik12ORCID,Brisse Sylvain34ORCID

Affiliation:

1. Insitut Pasteur, Université Paris Cité, Mathematical Modelling of Infectious Diseases Unit, UMR2000, CNRS, 75015 Paris, France.

2. Department of Genetics, University of Cambridge, Cambridge CB2 3EH, UK.

3. Institut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, 75724 Paris, France.

4. National Reference Center for Whooping Cough and Other Bordetella Infections, 75724 Paris, France.

5. University of Turku UTU, Institute of Biomedicine, Research Center for Infections and Immunity, FI-20520 Turku, Finland.

6. Centre for Infectious Disease Control, National Institute for Public Health and the Environment (RIVM), 3720 BA Bilthoven, Netherlands.

7. Statens Serum Institut, Bacteria, Parasites and Fungi/Infectious Disease Preparedness, 2300 Copenhagen, Denmark.

8. The Public Health Agency of Sweden, Unit for Laboratory Surveillance of Bacterial Pathogens, SE-171 82 Solna, Sweden.

9. National Institute of Public Health, Department of Infectious Diseases Epidemiology, CZ-10000 Prague, Czech Republic.

10. Norwegian Institute of Public Health, Department of Infectious Disease Control and Vaccine, N-0213 Oslo, Norway.

11. Respiratory and Vaccine Preventable Bacteria Reference Unit, Public Health England–National Infection Service, London NW9 5EQ, UK.

12. Immunisation and Countermeasures Division, Public Health England–National Infection Service, London NW9 5EQ, UK.

13. University Hospital Vall d’Hebron, Microbiology Department, 08035 Barcelona, Spain.

14. Universitat Autònoma de Barcelona, Department of Genetics and Microbiology, 08193 Barcelona, Spain.

15. Centre for Research and Development, Uppsala University/Region Gävleborg, 80187 Gävle, Sweden.

16. Molecular Microbiology Laboratory, Children’s Health Ireland, Crumlin, D12 N512 Dublin, Ireland.

17. InFLAMES Research Flagship Center, University of Turku, FI-20520 Turku, Finland.

18. Department of Microbiology, National Reference Centre for Bordetella pertussis, Universitair Ziekenhuis Brussel, Vrije Universiteit Brussel (VUB), B-1090 Brussels, Belgium.

19. Department of Infectious Diseases, Istituto Superiore di Sanità, IT-00161 Rome, Italy.

20. National Institute of Public Health, National Reference Laboratory for Pertussis and Diphtheria, 100 00 Prague, Czech Republic.

21. Department of Microbiology, Immunology and Transplantation, Rega Institute, KU Leuven, 3000 Leuven, Belgium.

22. Department of Veterinary Medicine, University of Cambridge, Cambridge CB3 0ES, UK.

23. Université Paris Cité, Department of General Paediatrics and Paediatric Infectious Diseases, Necker–Enfants Malades Hospital, APHP, 75015 Paris, France.

Abstract

As with other pathogens, competitive interactions between Bordetella pertussis strains drive infection risk. Vaccines are thought to perturb strain diversity through shifts in immune pressures; however, this has rarely been measured because of inadequate data and analytical tools. We used 3344 sequences from 23 countries to show that, on average, there are 28.1 transmission chains circulating within a subnational region, with the number of chains strongly associated with host population size. It took 5 to 10 years for B. pertussis to be homogeneously distributed throughout Europe, with the same time frame required for the United States. Increased fitness of pertactin-deficient strains after implementation of acellular vaccines, but reduced fitness otherwise, can explain long-term genotype dynamics. These findings highlight the role of vaccine policy in shifting local diversity of a pathogen that is responsible for 160,000 deaths annually.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

General Medicine

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