Genomic Content of Bordetella Pertussis Clinical Isolates Circulating in Areas of Intensive Children Vaccination

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2008 Jun 19

PMID 18560590

Citations 24

Authors

Valerie Bouchez

Valerie Caro

Erwan Levillain

Ghislaine Guigon

Nicole Guiso

Affiliations

Soon will be listed here.

Abstract

Background: The objective of the study was to analyse the evolution of Bordetella pertussis population and the influence of herd immunity in different areas of the world where newborns and infants are highly vaccinated.

Methodology: The analysis was performed using DNA microarray on 15 isolates, PCR on 111 isolates as well as GS-FLX sequencing technology on 3 isolates and the B. pertussis reference strain, Tohama I.

Principal Findings: Our analyses demonstrate that the current circulating isolates are continuing to lose genetic material as compared to isolates circulating during the pre-vaccine era whatever the area of the world considered. The lost genetic material does not seem to be important for virulence. Our study confirms that the use of whole cell vaccines has led to the control of isolates that were similar to vaccine strains. GS-FLX sequencing technology shows that current isolates did not acquire any additional material when compared with vaccine strains or with isolates of the pre-vaccine era and that the sequenced strain Tohama I is not representative of the isolates. Furthermore, this technology allowed us to observe that the number of Insertion Sequence elements contained in the genome of the isolates is temporally increasing or varying between isolates.

Conclusions: B. pertussis adaptation to humans is still in progress by losing genetic material via Insertion Sequence elements. Furthermore, recent isolates did not acquire any additional material when compared with vaccine strains or with isolates of the pre-vaccine era. Herd immunity, following intensive vaccination of infants and children with whole cell vaccines, has controlled isolates similar to the vaccine strains without modifying significantly the virulence of the isolates. With the replacement of whole cell vaccines by subunit vaccines, containing only few bacterial antigens targeting the virulence of the bacterium, one could hypothesize the circulation of isolates expressing less or modified vaccine antigens.

Citing Articles

Pathogenicity and virulence of and its adaptation to its strictly human host.

Belcher T, Dubois V, Rivera-Millot A, Locht C, Jacob-Dubuisson F Virulence. 2021; 12(1):2608-2632.

PMID: 34590541 PMC: 8489951. DOI: 10.1080/21505594.2021.1980987.

Comparative genomics of whole-cell pertussis vaccine strains from India.

Alai S, Ghattargi V, Gautam M, Patel K, Pawar S, Dhotre D BMC Genomics. 2020; 21(1):345.

PMID: 32381023 PMC: 7204287. DOI: 10.1186/s12864-020-6724-8.

Intercepting signalling mechanism to control environmental biofouling.

Pal S, Qureshi A, Purohit H 3 Biotech. 2018; 8(8):364.

PMID: 30105189 PMC: 6085211. DOI: 10.1007/s13205-018-1383-z.

Screening and Genomic Characterization of Filamentous Hemagglutinin-Deficient Bordetella pertussis.

Weigand M, Pawloski L, Peng Y, Ju H, Burroughs M, Cassiday P Infect Immun. 2018; 86(4).

PMID: 29358336 PMC: 5865017. DOI: 10.1128/IAI.00869-17.

A Functional Tricarboxylic Acid Cycle Operates during Growth of Bordetella pertussis on Amino Acid Mixtures as Sole Carbon Substrates.

Izac M, Garnier D, Speck D, Lindley N PLoS One. 2015; 10(12):e0145251.

PMID: 26684737 PMC: 4684311. DOI: 10.1371/journal.pone.0145251.

References

Ochman H, Moran N . Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science. 2001; 292(5519):1096-9. DOI: 10.1126/science.1058543. View

Maurelli A . Black holes, antivirulence genes, and gene inactivation in the evolution of bacterial pathogens. FEMS Microbiol Lett. 2007; 267(1):1-8. DOI: 10.1111/j.1574-6968.2006.00526.x. View

Caro V, Hot D, Guigon G, Hubans C, Arrive M, Soubigou G . Temporal analysis of French Bordetella pertussis isolates by comparative whole-genome hybridization. Microbes Infect. 2006; 8(8):2228-35. DOI: 10.1016/j.micinf.2006.04.014. View

Brinig M, Cummings C, Sanden G, Stefanelli P, Lawrence A, Relman D . Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J Bacteriol. 2006; 188(7):2375-82. PMC: 1428402. DOI: 10.1128/JB.188.7.2375-2382.2006. View

Gueirard P, Weber C, Le Coustumier A, Guiso N . Human Bordetella bronchiseptica infection related to contact with infected animals: persistence of bacteria in host. J Clin Microbiol. 1995; 33(8):2002-6. PMC: 228324. DOI: 10.1128/jcm.33.8.2002-2006.1995. View

Hallander H, Advani A, Riffelmann M, von Konig C, Caro V, Guiso N . Bordetella pertussis strains circulating in Europe in 1999 to 2004 as determined by pulsed-field gel electrophoresis. J Clin Microbiol. 2007; 45(10):3257-62. PMC: 2045341. DOI: 10.1128/JCM.00864-07. View

Wolfe D, Goebel E, Bjornstad O, Restif O, Harvill E . The O antigen enables Bordetella parapertussis to avoid Bordetella pertussis-induced immunity. Infect Immun. 2007; 75(10):4972-9. PMC: 2044517. DOI: 10.1128/IAI.00763-07. View

Diavatopoulos D, Cummings C, Schouls L, Brinig M, Relman D, Mooi F . Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog. 2006; 1(4):e45. PMC: 1323478. DOI: 10.1371/journal.ppat.0010045. View

Weber C, Boursaux-Eude C, Coralie G, Caro V, Guiso N . Polymorphism of Bordetella pertussis isolates circulating for the last 10 years in France, where a single effective whole-cell vaccine has been used for more than 30 years. J Clin Microbiol. 2001; 39(12):4396-403. PMC: 88555. DOI: 10.1128/JCM.39.12.4396-4403.2001. View

10.

Heikkinen E, Kallonen T, Saarinen L, Sara R, King A, Mooi F . Comparative genomics of Bordetella pertussis reveals progressive gene loss in Finnish strains. PLoS One. 2007; 2(9):e904. PMC: 1975675. DOI: 10.1371/journal.pone.0000904. View

11.

Khelef N, Danve B, Guiso N . Bordetella pertussis and Bordetella parapertussis: two immunologically distinct species. Infect Immun. 1993; 61(2):486-90. PMC: 302754. DOI: 10.1128/iai.61.2.486-490.1993. View

12.

Wendelboe A, Njamkepo E, Bourillon A, Floret D, Gaudelus J, Gerber M . Transmission of Bordetella pertussis to young infants. Pediatr Infect Dis J. 2007; 26(4):293-9. DOI: 10.1097/01.inf.0000258699.64164.6d. View

13.

Soubeyrand B, Plotkin S . Microbial evolution: antitoxin vaccines and pathogen virulence. Nature. 2002; 417(6889):609-10; discussion 610. DOI: 10.1038/417609b. View

14.

Caro V, Bouchez V, Guiso N, Gatti B, Agosti M, Ayala S . Pertussis in Argentina and France. Vaccine. 2007; 25(22):4335-9. DOI: 10.1016/j.vaccine.2006.08.024. View

15.

Kourova N, Caro V, Weber C, Thiberge S, Chuprinina R, Tseneva G . Comparison of the Bordetella pertussis and Bordetella parapertussis isolates circulating in Saint Petersburg between 1998 and 2000 with Russian vaccine strains. J Clin Microbiol. 2003; 41(8):3706-11. PMC: 179792. DOI: 10.1128/JCM.41.8.3706-3711.2003. View

16.

Caro V, Elomaa A, Brun D, Mertsola J, He Q, Guiso N . Bordetella pertussis, Finland and France. Emerg Infect Dis. 2006; 12(6):987-9. PMC: 3293437. DOI: 10.3201/eid1206.051283. View

17.

Pallen M, Wren B . Bacterial pathogenomics. Nature. 2007; 449(7164):835-42. DOI: 10.1038/nature06248. View

18.

Goodnow R . Biology of Bordetella bronchiseptica. Microbiol Rev. 1980; 44(4):722-38. PMC: 373201. DOI: 10.1128/mr.44.4.722-738.1980. View

19.

Gogol E, Cummings C, Burns R, Relman D . Phase variation and microevolution at homopolymeric tracts in Bordetella pertussis. BMC Genomics. 2007; 8:122. PMC: 1891110. DOI: 10.1186/1471-2164-8-122. View

20.

Lautrop H . Epidemics of parapertussis. 20 years' observations in Denmark. Lancet. 1971; 1(7711):1195-8. DOI: 10.1016/s0140-6736(71)91713-2. View