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. 2021 Sep;26(37):2001213.
doi: 10.2807/1560-7917.ES.2021.26.37.2001213.

Evolution of Bordetella pertussis over a 23-year period in France, 1996 to 2018

Valérie Bouchez  1   2 , Sophie Guillot  1   2 , Annie Landier  1   2 , Nathalie Armatys  1   2 , Soraya Matczak  1   3 ; French pertussis microbiology study group  4 ; Julie Toubiana  1   2   5 , Sylvain Brisse  1   2
Collaborators, Affiliations

Evolution of Bordetella pertussis over a 23-year period in France, 1996 to 2018

Valérie Bouchez et al. Euro Surveill. 2021 Sep.

Abstract

BackgroundBordetella pertussis is the main agent of whooping cough. Vaccination with acellular pertussis vaccines has been largely implemented in high-income countries. These vaccines contain 1 to 5 antigens: pertussis toxin (PT), filamentous haemagglutinin (FHA), pertactin (PRN) and/or fimbrial proteins (FIM2 and FIM3). Monitoring the emergence of B. pertussis isolates that might partially escape vaccine-induced immunity is an essential component of public health strategies to control whooping cough.AimWe aimed to investigate temporal trends of fimbriae serotypes and vaccine antigen-expression in B. pertussis over a 23-year period in France (1996-2018).MethodsIsolates (n = 2,280) were collected through hospital surveillance, capturing one third of hospitalised paediatric pertussis cases. We assayed PT, FHA and PRN production by Western blot (n = 1,428) and fimbriae production by serotyping (n = 1,058). Molecular events underlying antigen deficiency were investigated by genomic sequencing.ResultsThe proportion of PRN-deficient B. pertussis isolates has increased steadily from 0% (0/38) in 2003 to 48.4% (31/64) in 2018 (chi-squared test for trend, p < 0.0001), whereas only 5 PT-, 5 FHA- and 9 FIM-deficient isolates were found. Impairment of PRN production was predominantly due to IS481 insertion within the prn gene or a 22 kb genomic inversion involving the prn promoter sequence, indicative of convergent evolution. FIM2-expressing isolates have emerged since 2011 at the expense of FIM3.ConclusionsB. pertussis is evolving through the rapid increase of PRN-deficient isolates and a recent shift from FIM3 to FIM2 expression. Excluding PRN, the loss of vaccine antigen expression by circulating B. pertussis isolates is epidemiologically insignificant.

Keywords: Bordetella pertussis; fimbriae serotype; pertactin; population evolution; vaccine antigen deficiency.

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Conflict of interest statement

Conflict of interest: None of the authors had any conflict of interest or an interest that could be perceived as such in relation to this work.

Figures

Figure 1
Figure 1
Number of Bordetella pertussis isolates and pertussis vaccine antigen-negative isolates collected per year, France, 1996–2018 (n = 2,280)
Figure 2
Figure 2
Identification of filamentous haemagglutinin- and pertussis toxin-negative Bordetella pertussis isolates by Western blot, France, 1996 to 2018 (n = 1,428)
Figure 3
Figure 3
Genomic events leading to loss of pertactin expression in Bordetella pertussis isolates per year, France, 2004–2018 (n = 188)
Figure 4
Figure 4
Evolution of fimbrial protein production by Bordetella pertussis isolates per year, France, 2006–2018 (n = 1,058)
See this image and copyright information in PMC

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