Global population structure and evolution of Bordetella pertussis and their relationship with vaccination

Marieke J. Bart, Simon R. Harris, Abdolreza Advani, Yoshichika Arakawa, Daniela Bottero, Valérie Bouchez, Pamela K. Cassiday, Chuen Sheue Chiang, Tine Dalby, Norman K. Fry, María Emilia Gaillard, Marjolein van Gent, Nicole Guiso, Hans O. Hallander, Eric T. Harvill, Qiushui He, Han G.J. van der Heide, Kees Heuvelman, Daniela F. Hozbor, Kazunari KamachiGennady I. Karataev, Ruiting Lan, Anna Lutyńska, Ram P. Maharjan, Jussi Mertsola, Tatsuo Miyamura, Sophie Octavia, Andrew Preston, Michael A. Quail, Vitali Sintchenko, Paola Stefanelli, M. Lucia Tondella, Raymond S.W. Tsang, Yinghua Xu, Shu Man Yao, Shumin Zhang, Julian Parkhill, Frits R. Mooi

Research output: Contribution to journalArticle

127 Citations (Scopus)

Abstract

Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from whole-cell vaccines (WCVs) to less effective acellular vaccines (ACVs), waning immunity, and pathogen adaptation. Pathogen adaptation is suggested by antigenic divergence between vaccine strains and circulating strains and by the emergence of strains with increased pertussis toxin production. We applied comparative genomics to a worldwide collection of 343 B. pertussis strains isolated between 1920 and 2010. The global phylogeny showed two deep branches; the largest of these contained 98% of all strains, and its expansion correlated temporally with the first descriptions of pertussis outbreaks in Europe in the 16th century. We found little evidence of recent geographical clustering of the strains within this lineage, suggesting rapid strain flow between countries. We observed that changes in genes encoding proteins implicated in protective immunity that are included in ACVs occurred after the introduction of WCVs but before the switch to ACVs. Furthermore, our analyses consistently suggested that virulence-associated genes and genes coding for surface-exposed proteins were involved in adaptation. However, many of the putative adaptive loci identified have a physiological role, and further studies of these loci may reveal less obvious ways in which B. pertussis and the host interact. This work provides insight into ways in which pathogens may adapt to vaccination and suggests ways to improve pertussis vaccines.

Original languageEnglish (US)
Article numbere01074-14
JournalmBio
Volume5
Issue number2
DOIs
StatePublished - Apr 22 2014

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Acellular Vaccines
Bordetella pertussis
Vaccination
Vaccines
Whooping Cough
Immunity
Population
Pertussis Vaccine
Pertussis Toxin
Infant Mortality
Phylogeny
Genomics
Genes
Disease Outbreaks
Cluster Analysis
Virulence
Membrane Proteins
Proteins

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Virology

Cite this

Bart, M. J., Harris, S. R., Advani, A., Arakawa, Y., Bottero, D., Bouchez, V., ... Mooi, F. R. (2014). Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. mBio, 5(2), [e01074-14]. https://doi.org/10.1128/mBio.01074-14
Bart, Marieke J. ; Harris, Simon R. ; Advani, Abdolreza ; Arakawa, Yoshichika ; Bottero, Daniela ; Bouchez, Valérie ; Cassiday, Pamela K. ; Chiang, Chuen Sheue ; Dalby, Tine ; Fry, Norman K. ; Gaillard, María Emilia ; van Gent, Marjolein ; Guiso, Nicole ; Hallander, Hans O. ; Harvill, Eric T. ; He, Qiushui ; van der Heide, Han G.J. ; Heuvelman, Kees ; Hozbor, Daniela F. ; Kamachi, Kazunari ; Karataev, Gennady I. ; Lan, Ruiting ; Lutyńska, Anna ; Maharjan, Ram P. ; Mertsola, Jussi ; Miyamura, Tatsuo ; Octavia, Sophie ; Preston, Andrew ; Quail, Michael A. ; Sintchenko, Vitali ; Stefanelli, Paola ; Tondella, M. Lucia ; Tsang, Raymond S.W. ; Xu, Yinghua ; Yao, Shu Man ; Zhang, Shumin ; Parkhill, Julian ; Mooi, Frits R. / Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. In: mBio. 2014 ; Vol. 5, No. 2.
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abstract = "Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from whole-cell vaccines (WCVs) to less effective acellular vaccines (ACVs), waning immunity, and pathogen adaptation. Pathogen adaptation is suggested by antigenic divergence between vaccine strains and circulating strains and by the emergence of strains with increased pertussis toxin production. We applied comparative genomics to a worldwide collection of 343 B. pertussis strains isolated between 1920 and 2010. The global phylogeny showed two deep branches; the largest of these contained 98{\%} of all strains, and its expansion correlated temporally with the first descriptions of pertussis outbreaks in Europe in the 16th century. We found little evidence of recent geographical clustering of the strains within this lineage, suggesting rapid strain flow between countries. We observed that changes in genes encoding proteins implicated in protective immunity that are included in ACVs occurred after the introduction of WCVs but before the switch to ACVs. Furthermore, our analyses consistently suggested that virulence-associated genes and genes coding for surface-exposed proteins were involved in adaptation. However, many of the putative adaptive loci identified have a physiological role, and further studies of these loci may reveal less obvious ways in which B. pertussis and the host interact. This work provides insight into ways in which pathogens may adapt to vaccination and suggests ways to improve pertussis vaccines.",
author = "Bart, {Marieke J.} and Harris, {Simon R.} and Abdolreza Advani and Yoshichika Arakawa and Daniela Bottero and Val{\'e}rie Bouchez and Cassiday, {Pamela K.} and Chiang, {Chuen Sheue} and Tine Dalby and Fry, {Norman K.} and Gaillard, {Mar{\'i}a Emilia} and {van Gent}, Marjolein and Nicole Guiso and Hallander, {Hans O.} and Harvill, {Eric T.} and Qiushui He and {van der Heide}, {Han G.J.} and Kees Heuvelman and Hozbor, {Daniela F.} and Kazunari Kamachi and Karataev, {Gennady I.} and Ruiting Lan and Anna Lutyńska and Maharjan, {Ram P.} and Jussi Mertsola and Tatsuo Miyamura and Sophie Octavia and Andrew Preston and Quail, {Michael A.} and Vitali Sintchenko and Paola Stefanelli and Tondella, {M. Lucia} and Tsang, {Raymond S.W.} and Yinghua Xu and Yao, {Shu Man} and Shumin Zhang and Julian Parkhill and Mooi, {Frits R.}",
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Bart, MJ, Harris, SR, Advani, A, Arakawa, Y, Bottero, D, Bouchez, V, Cassiday, PK, Chiang, CS, Dalby, T, Fry, NK, Gaillard, ME, van Gent, M, Guiso, N, Hallander, HO, Harvill, ET, He, Q, van der Heide, HGJ, Heuvelman, K, Hozbor, DF, Kamachi, K, Karataev, GI, Lan, R, Lutyńska, A, Maharjan, RP, Mertsola, J, Miyamura, T, Octavia, S, Preston, A, Quail, MA, Sintchenko, V, Stefanelli, P, Tondella, ML, Tsang, RSW, Xu, Y, Yao, SM, Zhang, S, Parkhill, J & Mooi, FR 2014, 'Global population structure and evolution of Bordetella pertussis and their relationship with vaccination', mBio, vol. 5, no. 2, e01074-14. https://doi.org/10.1128/mBio.01074-14

Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. / Bart, Marieke J.; Harris, Simon R.; Advani, Abdolreza; Arakawa, Yoshichika; Bottero, Daniela; Bouchez, Valérie; Cassiday, Pamela K.; Chiang, Chuen Sheue; Dalby, Tine; Fry, Norman K.; Gaillard, María Emilia; van Gent, Marjolein; Guiso, Nicole; Hallander, Hans O.; Harvill, Eric T.; He, Qiushui; van der Heide, Han G.J.; Heuvelman, Kees; Hozbor, Daniela F.; Kamachi, Kazunari; Karataev, Gennady I.; Lan, Ruiting; Lutyńska, Anna; Maharjan, Ram P.; Mertsola, Jussi; Miyamura, Tatsuo; Octavia, Sophie; Preston, Andrew; Quail, Michael A.; Sintchenko, Vitali; Stefanelli, Paola; Tondella, M. Lucia; Tsang, Raymond S.W.; Xu, Yinghua; Yao, Shu Man; Zhang, Shumin; Parkhill, Julian; Mooi, Frits R.

In: mBio, Vol. 5, No. 2, e01074-14, 22.04.2014.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Global population structure and evolution of Bordetella pertussis and their relationship with vaccination

AU - Bart, Marieke J.

AU - Harris, Simon R.

AU - Advani, Abdolreza

AU - Arakawa, Yoshichika

AU - Bottero, Daniela

AU - Bouchez, Valérie

AU - Cassiday, Pamela K.

AU - Chiang, Chuen Sheue

AU - Dalby, Tine

AU - Fry, Norman K.

AU - Gaillard, María Emilia

AU - van Gent, Marjolein

AU - Guiso, Nicole

AU - Hallander, Hans O.

AU - Harvill, Eric T.

AU - He, Qiushui

AU - van der Heide, Han G.J.

AU - Heuvelman, Kees

AU - Hozbor, Daniela F.

AU - Kamachi, Kazunari

AU - Karataev, Gennady I.

AU - Lan, Ruiting

AU - Lutyńska, Anna

AU - Maharjan, Ram P.

AU - Mertsola, Jussi

AU - Miyamura, Tatsuo

AU - Octavia, Sophie

AU - Preston, Andrew

AU - Quail, Michael A.

AU - Sintchenko, Vitali

AU - Stefanelli, Paola

AU - Tondella, M. Lucia

AU - Tsang, Raymond S.W.

AU - Xu, Yinghua

AU - Yao, Shu Man

AU - Zhang, Shumin

AU - Parkhill, Julian

AU - Mooi, Frits R.

PY - 2014/4/22

Y1 - 2014/4/22

N2 - Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from whole-cell vaccines (WCVs) to less effective acellular vaccines (ACVs), waning immunity, and pathogen adaptation. Pathogen adaptation is suggested by antigenic divergence between vaccine strains and circulating strains and by the emergence of strains with increased pertussis toxin production. We applied comparative genomics to a worldwide collection of 343 B. pertussis strains isolated between 1920 and 2010. The global phylogeny showed two deep branches; the largest of these contained 98% of all strains, and its expansion correlated temporally with the first descriptions of pertussis outbreaks in Europe in the 16th century. We found little evidence of recent geographical clustering of the strains within this lineage, suggesting rapid strain flow between countries. We observed that changes in genes encoding proteins implicated in protective immunity that are included in ACVs occurred after the introduction of WCVs but before the switch to ACVs. Furthermore, our analyses consistently suggested that virulence-associated genes and genes coding for surface-exposed proteins were involved in adaptation. However, many of the putative adaptive loci identified have a physiological role, and further studies of these loci may reveal less obvious ways in which B. pertussis and the host interact. This work provides insight into ways in which pathogens may adapt to vaccination and suggests ways to improve pertussis vaccines.

AB - Bordetella pertussis causes pertussis, a respiratory disease that is most severe for infants. Vaccination was introduced in the 1950s, and in recent years, a resurgence of disease was observed worldwide, with significant mortality in infants. Possible causes for this include the switch from whole-cell vaccines (WCVs) to less effective acellular vaccines (ACVs), waning immunity, and pathogen adaptation. Pathogen adaptation is suggested by antigenic divergence between vaccine strains and circulating strains and by the emergence of strains with increased pertussis toxin production. We applied comparative genomics to a worldwide collection of 343 B. pertussis strains isolated between 1920 and 2010. The global phylogeny showed two deep branches; the largest of these contained 98% of all strains, and its expansion correlated temporally with the first descriptions of pertussis outbreaks in Europe in the 16th century. We found little evidence of recent geographical clustering of the strains within this lineage, suggesting rapid strain flow between countries. We observed that changes in genes encoding proteins implicated in protective immunity that are included in ACVs occurred after the introduction of WCVs but before the switch to ACVs. Furthermore, our analyses consistently suggested that virulence-associated genes and genes coding for surface-exposed proteins were involved in adaptation. However, many of the putative adaptive loci identified have a physiological role, and further studies of these loci may reveal less obvious ways in which B. pertussis and the host interact. This work provides insight into ways in which pathogens may adapt to vaccination and suggests ways to improve pertussis vaccines.

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Bart MJ, Harris SR, Advani A, Arakawa Y, Bottero D, Bouchez V et al. Global population structure and evolution of Bordetella pertussis and their relationship with vaccination. mBio. 2014 Apr 22;5(2). e01074-14. https://doi.org/10.1128/mBio.01074-14